Gene Therapy & Molecular Biology Volume 12 Issue B - PART 1

GENE THERAPY & MOLECULAR BIOLOGY

Volume 12 Number 2 December 2008 Published by Gene Therapy Press ISSN 1529-9120

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GENE THERAPY & MOLECULAR BIOLOGY Addresses of Members of the Editorial Board OPEN ACCESS www.gtmb.org Editor

Editor Assistants Boulikas, Teni, Ph.D. Chairman of the Board, Regulon, Inc. Mt View CA 94043 and Regulon AE, Athens, Greece

Koutoudi, Maria M.A. Vougiouka, Maria, B.Sc. Kruit, Adrian, Ph.D. Bellimezi, M., Ph.D Katsoupi J, Mph, Tsogas I., Ph.D, Magkos, A., Ph.D, Christofis Petros., Ph.D, Leto Tziveleka., Ph.D

Associate Editors Missailidis, Sotiris, DPhil (York) Lecturer in Chemistry and Analytical Sciences, The Open University, UK

Roberts, Michael, Ph.D., Regulon A.E., Athens Greece

Berezney, Ronald, Ph.D., State University of New York at Buffalo, USA

Rossi, John, Ph.D., Beckman Research Institute of the City of Hope, USA

Crooke, Stanley, M.D., Ph.D., ISIS Pharmaceuticals, Inc, USA

Shen, James, Ph.D., Institute of Molecular Biology, Academia Sinica, Taipei, Taiwan, Republic of China & University of California at Davis, USA.

Gronemeyer, Hinrich, Ph.D. I.N.S.E.R.M., IGBMC, France

Webb, David, Ph.D., Celgene Corporation, USA

Aguilar-Cordova, Estuardo, Ph.D., AdvantaGene, Inc., USA

Editorial Board Members Akporiaye, Emmanuel, Ph.D., Arizona Cancer Center, USA

Baldwin, H. Scott, M.D Vanderbilt University Medical Center, USA

Anson, Donald S., Ph.D., Women's and Children's Hospital, Australia

Barranger, John, MD, Ph.D., University of Pittsburgh, USA

Ariga, Hiroyoshi, Ph.D., Hokkaido University, Japan

Black, Keith L. M.D., Maxine Dunitz Neurosurgical Institute, Cedars-Sinai Medical Center, USA

Blum, Kenneth, Ph.D., Wake Forest University School of Medicine, USA

Eckstein, Jens W., Ph.D., Akikoa Pharmaceuticals Inc, USA

Bode, Jürgen, Gesellschaft für Biotechnologische Forschung m.b.H., Germany

Fisher, Paul A. Ph.D., State University of New York, USA

Bohn, Martha C., Ph.D., The Feinberg School of Medicine, Northwestern University, USA

Georgiev, Georgii, Ph.D., Russian Academy of Sciences, USA

Bresnick, Emery, Ph.D., University of Wisconsin Medical School, USA

Getzenberg, Robert, Ph.D., Institute Shadyside Medical Center, USA

Caiafa, Paola, Ph.D., Università di Roma “La Sapienza”, Italy

Ghosh, Sankar Ph.D., Yale University School of Medicine, USA

Cheng, Seng H. Ph.D., Genzyme Corporation, USA

Gojobori, Takashi, Ph.D., Center for Information Biology, National Institute of Genetics, Japan

Cole, David J. M.D., Medical University of South Carolina, USA

Harris David T., Ph.D., Cord Blood Bank, University of Arizona, USA

Crooke, Stanley, M.D., Ph.D. ISIS Pharmaceuticals, Inc. USA

Heldin, Paraskevi Ph.D., Uppsala Universitet, Sweden

Davie, James R, Ph.D., Manitoba Institute of Cell Biology, USA

Hesdorffer, Charles S., M.D., Columbia University, USA

DePamphilis, Melvin L, Ph.D., National Institute of Child Health and Human, National Institutes of Health, USA

Hoekstra, Merl F, Ph.D., Epoch Biosciences, Inc., USA

Hung, Mien-Chie, Ph.D., The University of Texas, USA

Kuroki, Masahide, M.D., Ph.D., Fukuoka University School of Medicine, Japan

Johnston, Brian, Ph.D., Somagenics, Inc, USA

Lai, Mei T. Ph.D., Lilly Research Laboratories USA

Jolly, Douglas J, Ph.D., Advantagene, Inc.,USA

Latchman, David S., PhD, Dsc, MRCPath

Joshi, Sadhna, Ph.D., D.Sc., University of Toronto Canada

Lavin, Martin F, Ph.D., The Queensland Cancer Fund Research Unit, The Queensland Institute of Medical Research, Australia

Kiyama, Ryoiti, Ph.D., National Institute of Bioscience and HumanTechnology, Japan

Lebkowski, Jane S., Ph.D., GERON Corporation, USA

Kotoku Kurachi, Ph.D., University of Michigan Medical School, USA

Li, Liangping Ph.D., MaxDelbr端ck-Center for Molecular Medicine, Germany

Kottaridis, Stavros D., Ph.D. Regulon Inc. USA

Lu, Yi, Ph.D., University of Tennessee Health Science Center, USA

University of London, UK

Krawetz, Stephen A., Ph.D., Wayne State University School of Medicine. USA

Lundstrom Kenneth, Ph.D., Bioxtal/Regulon, Inc. Switzerland

Kruse, Carol A., Ph.D., Sidney Kimmel Cancer Center. USA

MacDougald, Ormond A, Ph.D., University of Michigan Medical School, USA

Kuo, Tien, Ph.D., The University of Texas M. D. Anderson Cancer USA

Malone, Robert W., M.D., Aeras Global TB Vaccine Foundation, USA

Mirkin, Sergei, M. Ph.D., University of Illinois at Chicago, USA

Royer, Hans-Dieter, M.D., (CAESAR), Germany

Noteborn, Mathieu, Ph.D., Leiden University, The Netherlands

Rubin, Joseph, M.D., Mayo Medical School Mayo Clinic, USA

Paleos, Constantinos M., Ph.D. Institute of Physical Chemistry Demokritos.

Greece

Saenko Evgueni L., Ph.D., University of Maryland School of Medicine Center for Vascular and Inflammatory Diseases, USA

Pomerantz, Roger, J., M.D., Tibotec, Inc., USA

Santoro, M. Gabriella, Ph.D., University of Rome Tor Vergata, Italy

Raizada, Mohan K., Ph.D., University of Florida, USA

Salmons, Brian, Ph.D., (FSGBiotechnologie GmbH), Austria

Razin, Sergey, Ph.D., Institute of Gene Biology Russian Academy of Sciences, USA

Sharrocks, Andrew, D., Ph.D., University of Manchester, UK

Robbins, Paul, D, Ph.D., University of Pittsburgh, USA

Smythe Roy W., M.D., Texas A&M University Health Sciences Center, USA

Rosenblatt, Joseph, D., M.D, University of Miami School of Medicine, USA

Srivastava, Arun Ph.D., University of Florida College of Medicine, USA

Rosner, Marsha, R., Ph.D., Ben May Institute for Cancer Research, University of Chicago, USA

Steiner, Mitchell, M.D., University of Tennessee, USA

Tainsky, Michael A., Ph.D., Karmanos Cancer Institute, Wayne State University, USA

White, Robert, J., University of Glasgow, UK

Taira, Kazunari, Ph.D., The University of Tokyo, Japan

White-Scharf, Mary, Ph.D., Biotransplant, Inc., USA

Thierry, Alain, Ph.D., National Cancer Institute, National Institutes of Health, France

Wiginton, Dan, A., Ph.D., Children's Hospital Research Foundation, CHRF , USA

Trifonov, Edward, N. Ph.D., University of Haifa, Israel

Yung, Alfred, M.D., University of Texas, USA

Van Dyke, Michael, W., Ph.D., The University of Texas M. D. Anderson Cancer Center, USA

Zannis-Hadjopoulos, Maria Ph.D., McGill Cancer Centre, Canada

Vournakis, John N., Ph.D. Medical University of South Carolina, USA

Zorbas, Haralabos, Ph.D., BioM AG Team, Germany

Chi-Un Pae, MD, PhD, Associate Professor, Department of Psychiatry The Catholic Universoty of Korea College of Medicine

Associate Board Members Falasca, Marco, M.D., University College London, UK

Hiroki, Maruyama, M.D., Ph.D., Niigata University Graduate School of Medical and Dental Sciences, Japan

Gao, Shou-Jiang, Ph.D., The University of Texas Health Science Center at San Antonio, USA

Kazunori, Aoki, M.D., Ph.D., National Cancer Center Research Institute, Japan

Gibson, Spencer Bruce, Ph.D., University of Manitoba, USA

Rigoutsos, Isidore, Ph.D., Thomas J. Watson Research Center, USA

Gu, Baohua, Ph.D., The Jefferson Center, USA

Priya, Aggarwal Ph.D., University of Pennsylvania

Morris, Kevin Vance, Assistant Professor, The Scripps Research Institute, La Jolla, CA

W. Todd Penberthy, PH.D.,

Romano, Gaetano Ph.D. Research Associate Professor; Temple University, Philadelphia, U.S.A.

Yuefei Yu Ph.D. Texas Tech University Health Science Center. Research Scientist. Head of the research group.

Hongying Hao M.D./Ph.D., Instructor, Department of Surgery School of Medicine University of Louisville U.S.A.

Assistant Professor, Department of Molecular Genetics,Biochemistry, and Microbiology,

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Editorial Office Teni Boulikas, Ph.D./ Maria Koutoudi, B.A. , M.A. Gregoriou Afxentiou 7 Alimos, Athens 17455 Greece Tel: +30-210-985-8454 Fax: +30-210-985-8453 and electronically to maria.koutoudi@cancer-therapy.org The free electronic access to articles published in "GTMB" to a big general audience, the attractive journal title, the speed of the reviewing process, the no-charges for page numbers or color figure reproduction, the 25 complimentary reprints, the rapid electronic publication, the embracing of many fields in cancer, the anticipated high quality in depth reviews and first rate research articles and most important, the eminent members of the Editorial Board being assembled are prognostic factors of a big success for the newly established journal.

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Table of contents

Gene Therapy and Molecular Biology Vol 12 Number 2, December 2008

Pages

Type of Article

Article title

Authors (corresponding author is in boldface)

141-146

Review Article

Vaccinomics

Virendra S Gomase, Somnath Tagore

147-166

Research Article

Prediction of antigenic binders from cterminal domain Human papillomavirus oncoprotein e7

Virendra S Gomase, Somnath Tagore, Krishnan Shyamkumar

167-174

Research Article

Retrovirally-mediated genetic correction of mesenchymal stem cells from patients affected by mucopolysaccharidosis type II (Hunter Syndrome)

Carla Corradi-Perini, Thomas D. Southgate, Guy T Besley, Alan Cooper, John A Deakin, J Ed Wraith, Leslie J. Fairbairn, Robert F. Wynn, Ilaria Bellantuono

175-180

Research Article

A characterization of genetic haplotypes Josefa Salgado, Carmen Gil, Maitane Robles, Cristina Gutierrez, Carmen in BRCA1 identifies linkage Reyna, JesĂşs GarcĂ­a-Foncillas disequilibrium with a novel polymorphism in intron 7

181-188

Review Article

Molecular targets in medullary thyroid carcinoma

Sam W Moore

189-206

Research Article

Let-7, miR-125, miR-205, and miR-296 are prospective therapeutic agents in breast cancer molecular medicine

Debmalya Barh, Sanjeeb Parida, Bibhu Prasad Parida1, Geetha Viswanathan

207-218

Research Article

Suppression of Primary and Disseminated Murine Tumor Growth with eIF5A1 Gene Therapy

Songmu Jin, Catherine A. Taylor, Zhongda Liu, Zhong Sun, Bin Ye, John E.Thompson

219-238

Review Article

Hexavalent chromium exposure, genomic instability and lung cancer

Ana M. Urbano, Carlos F.D. Rodrigues, Maria Carmen Alpoim

239-246

Research Article

Fraz Arshad Malik, Mahmood Akhter Kayani1, Hina Iqbal, Wen G Jiang, Rafshan Sadiq

247-252

Research Article

Screening of coding region of metastasis suppressor genes KISS1 and KAI-1 for germ line mutations in breast cancer patients A new potential radiosensitizer- multiwalled carbon nanotubes modified by ammonium persulfate

253-258

Research Article

Jian-She Yang, Xigang Jing, Wen-Jian Li, Xiang-Kai Hu, Wei Wei, Zhuan-Zi Wang

Decreased risk of bladder cancer in men Frances M. Martin, Andrew M. Harris, Randall G. Rowland, William Conner1, treated with quinazoline-based !1Matthew Lane, Erik Durbin, Andre T. adrenoceptor antagonists Baron, Natasha Kyprianou

259-266

Review Article

Hematopoietic growth factors in the elderly

Wassim Mchayleh, Rajesh Sehgal, James Natale, Gurkamal Chatta

267-276

Research Article

HSP70 variations in the acute treatment with mood stabilizers in patients with bipolar disorder: results of a preliminary work

Chi-Un Pae, Antonio Drago, Jung-Jin Kim, Laura Mandelli, Ashwin A. Patkar, Diana De Ronchi, Alessandro Serretti

277-292

Review Article

Recombinant adeno-associated virus as vaccine delivery vehicles

Komal Vig, Roland Herzog, Douglas Martin, Eddie G. Moore, Vida A. Dennis, Shreekumar Pillai, Shree R. Singh

293-300

Research Article

Inhibition of focal adhesion kinase with her-2 targeted antibody pertuzumab (Omnitarg®, 2C4) in breast cancer cells

Emel Canbay, Bala Gur-Dedeoglu, Betul Bozkurt, Melih Karabeyoglu, Bulent Unal, Osman Yıldırım, Omer Cengiz3, Isik G Yulug

301-311

Research Article

Enhanced splenic protection and reduction of parasitaemia following transplantation of splenocytes overexpressing Bcl-2 in a murine malaria model

313-357

Review Article

Microtubule-targeted antitumor drugs: chemistry, mechanisms and nanoparticle formulations

Francisco Martínez-Flores, José Luis Ventura-Gallegos, Eréndira G. EstradaVillaseñor, Hilda Villegas-Castrejón, Epifanio Cruz-Zaragoza, Luis Covarrubias-Robles, Alejandro ZentellaDehesa, Martha Legorreta-Herrera Teni Boulikas, Ioannis Tsogas

359-370

Research Article

371-382

Research Article

Gene expression signature-based chemical genomics and activity pattern in a panel of tumour cell lines propose linalyl acetate as a protein kinase/NF"B inhibitor A short term pilot open label study to evaluate efficacy and safety of LG839, a customized DNA directed nutraceutical in obesity: Exploring Nutrigenomics

383-386

Case Report

387-394

Research Article

395-404

Review Article

405-414

Research Article

Severe phenotype of Morquio A disease in a child with S287L Nacetylgalactosamine-6-sulfate sulfatase mutation Attenuation of experimental liver fibrosis by hepatocyte growth factor gene delivery mediated by adenovirus Regulation of hormonal therapy resistance by cell cycle machinery Reversal of MDR1/P-glycoprotein associated drug resistance in human Hepatoblastoma

Saadia Bashir Hassan, Elin Lindhagen, Hanna Göransson, Mårten Fryknäs, Anders Isaksson, Hala Gali-Muhtasib, Rolf Larsson Kenneth Blum, Thomas JH Chen, Lonna Williams, Amanda LC Chen, William B. Downs, Roger L. Waite, T. Huntington, Simon Sims, Thomas Prihoda, Patrick Rhoads, Jeffrey Reinking, Dasha Braverman, Mallory Kerner, Seth H. Blum, Brien Quirk, Eric R Braverman Zoran S Gucev, Hassan Bouzidi, Velibor Tasic, Nada Popjordanova1, Ilija Kirovski, Zoran Trajkovski, Aleksandra Jancevska, Sami. Bajrami Yin Xu, Fei-qun Zheng, Jia Fang, Qunwei Zhang, Yi-de Qin, Yang Liu2, Renjie Yang3, Bin Wu Binoj Chandrasekharan Nair, Ratna K. Vadlamudi Steven W. Warmann, Joerg Fuchs

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Gene Therapy and Molecular Biology Vol 12, page 301 Gene Ther Mol Biol Vol 12, 301-311, 2008

Enhanced splenic protection and reduction of parasitaemia following transplantation of splenocytes overexpressing Bcl-2 in a murine malaria model Research Article

Francisco Martínez-Flores1,§, José Luis Ventura-Gallegos2,§, Eréndira G. EstradaVillaseñor1, Hilda Villegas-Castrejón1, Epifanio Cruz-Zaragoza3, Luis Covarrubias-Robles4, Alejandro Zentella-Dehesa2,5,*, Martha LegorretaHerrera6,* 1

Departamento de Morfología Celular y Molecular, Instituto Nacional de Rehabilitación.

Departamento de Medicina Genómica y Toxicología Ambiental, Instituto de Investigaciones Biomédicas, UNAM, México, D.F. 3 Instituto de Ciencias Nucleares, UNAM 4 Instituto de Biotecnología, UNAM 5 Departamento de Bioquímica, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán 6 Laboratorio de Inmunología Molecular, FES Zaragoza, UNAM 2

__________________________________________________________________________________ *Correspondence: Martha Legorreta-Herrera PhD, Laboratorio de Inmunología Molecular, Facultad de Estudios Superiores Zaragoza, Universidad Nacional Autonóma de México, Batalla 5 de mayo s/n Iztaplapa, CP 09230, México, DF México; Tel/Fax: 52(55)56230736; e-mail: marthal@servidor.unam.mx Alejandro Zentella-Dehesa PhD. Departamento de Bioquímica, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán.

Vasco de Quiroga 15, Sector XVI, Tlalpan, CP 14000, DF México; Tel 52(55)54870900 ext 2126; Fax: 52(55)56550011; e-mail: azentel@biomedicas.unam.mx Key words: Apoptosis, retroviral vectors, promoter PolII, oxidative stress Abbreviations: green fluorescent protein, (GFP); intravenously, (iv); Moloney Leukaemia Virus, (MLV) Received: 17 November 2008; Revised: 9 December 2008 Accepted: 9 December 2008; electronically published: December 2008

Summary Malaria is one of the most important infectious diseases worldwide. During acute infection, the activation of the immune response and parasite clearance by the spleen are key host defence mechanisms. Apoptosis of lymphocytes is believed to compromise the immune response in malaria cases. As limited progress has been made using gene therapy against parasitic infections, we explored the potential beneficial effect of reconstituting Plasmodium chabaudi infected mice with transduced splenocytes overexpressing Bcl-2. An ecotropic retrovirus encoding GFP and Bcl-2 was packaged in 293T cells. A second retrovirus expressing only GFP was used as control. Initially, CBA/Ca mice were transplanted with 2 x 107 total splenocytes from syngenic donor mice transduced with retroviral particles. Two hours later recipient mice were infected with 5 x 104 P. chabaudi parasitised erythrocytes.

Parasitaemia was evaluated every 24 h. Seven days post-infection, we evaluated splenic histology and Bcl-2 expression via RT-PCR and western blot. The protection against H2O2- induced apoptosis was tested on isolated total splenocytes. The efficiency of retroviral infection, expression of Bcl-2 and reporter gene was confirmed by Fluorescence microscopy, RT-PCR and western blotting of splenocytes from transplanted with cells transduced with GFP- or Bcl-2-expressing retroviruses. Parasitaemia in mice transplanted with GFP-transduced splenocytes transiently decreased 10-fold at day five after Plasmodium infection and was further decreased when mice were transplanted with Bcl-2-transduced splenocytes. The splenic architecture of mice that received transduced cells was preserved compared to control mice. Cytoprotection in vitro was enhanced with the Bcl-2 construct. The protective effect correlated with increased the cellularity in the spleen and overexpression Bcl-2. We tested the use of standard gene therapy strategies based on the reconstitution of irradiated mice with genetically modified heterologous cells in 301

MartĂ­nez-Flores et al: Enhanced splenic protection and reduction in a murine malaria model an experimental murine model of malaria. We observed transient reduction of parasitaemia, preservation of splenic architecture and increased cell survival in vitro against oxidative stress. Although the experimental design aimed to test the effect of Bcl-2 overexpression, transplantation of cells transduced with the empty retroviral vector resulted in a significant protective effect accompanied by the increased expression of endogenous Bcl-2.

introduced by genetic vectors (plasmids and viral vectors) encoding the corresponding cDNAs. Although this principle can be applied to a variety of diseases its applications to the treatment of infectious diseases remains to be developed. Reconstitution of infected individuals with genetically modified immune cells provides a simple application of the principles of the genetic therapy in these kinds of diseases.

If apoptosis is important for the progression of malaria, overexpression of anti-apoptotic proteins such as Bcl-2 should have a protective effect. Consequently, we explored the evolution and course of parasitaemia in P. chabaudi-infected mice previously transplanted with splenocytes over-expressing Bcl-2, as well as the resistance against hydrogen peroxide-induced apoptosis in splenocytes. We also documented the cytoarchitecture and histology of the spleen during P. chabaudi infection.

I. Introduction Malaria is the leading infectious cause of death worldwide, and estimated of two billion people (more than 40% of the world population) live in areas with a high risk of infection. The global annual incidence ranges between three to five hundred million clinical cases, with a total mortality between 2 to 3 millions a year (Wykes and Good, 2007).

Attempts to curtail the devastating effects of malaria have encountered many obstacles including the rapid development and spread of vector resistance to residual insecticides, a decreasing parasite response to clinically used drugs and the lack of effective and affordable alternative anti-malarial therapies. Despite all these difficulties the use of the gene therapy against infectious diseases, particularly malaria, has been poorly explored.

The cellular immune response to Plasmodium infection has been widely studied (Good and Currier, 1992; Taylor-Robinson and Phillips, 1993; Von Der Weid et al, 1994). In general, acute infection with Plasmodium is associated with the activation of peripheral T cells, alterations in the level of cytokine production (Cross and Langhorne, 1998) and lymphopaenia (Wipasa et al, 2001).

These changes can compromise the immune response and have been explained by apoptosis of lymphocytes, relocation of peripheral lymphocytes or both. In fact, it has been shown that schistosome, toxoplasma, and trypanosome infections induce apoptosis in host mononuclear cells (Lopes et al, 1995; Khan et al, 1996; Estaquier et al, 1997). Moreover, apoptosis of lymphocytes may contribute to parasite survival, through down regulation of anti-parasite inflammatory responses and immunosuppression.

Bcl-2 was the first characterised member of a family of genes that regulate apoptosis by preventing or inducing cell death (Korsmeyer et al, 1995; Kluck et al, 1997; Yang et al, 1997). The biochemical basis of their actions has not been completely elucidated and remains unclear.

However, over-expression of Bcl-2 can block many forms of apoptosis in transfected cell lines, transgenic mice or transduced organs in several in vivo models (Bilbao et al, 1999; Molto et al, 2003; Mitsiades et al, 2007).

Apoptosis is a major mechanism y which the development, maturation and activation of lymphocytes is regulated. During Plasmodium infection, apoptosis has been implicated as a mechanism whereby parasites escape from the immune system. Helmby et al have described the increased frequency of apoptosis in macrophages, B and T cells in the spleen of P chabaudi-infected mice (Helmby et al, 2000). These alterations correlate with increased expression of Fas and Fas-ligand, suggesting that apoptosis is, in part, Fas-mediated.

Gene therapy aims to correct defects in gene expression through the expression of exogenous proteins

II. Materials and Methods A. Animal model design CBA/Ca mice (kindly donated by Dr. W. Jarra, National Institute for Medical Research, London, UK) were used in all experiments; animals were maintained and cared for according to the Mexican Animal Regulations in a specific pathogen free environment. Splenocytes were isolated from healthy male mice, cultured in RPMI-1640 media supplemented with 10% foetal bovine serum, penicillin-streptomycin and amphotericin B (100 U/ml, 100 !g/ml and 0.25 !g/ml respectively) and stimulated with recombinant IL-2 (100 U/ml Sigma, USA). Cells were transduced with retroviral vectors encoding either GFP alone or GFP and Bcl-2. After twenty-four hours post transduction the cells were transplanted intravenously (iv) into sub-lethally irradiated mice in tree groups: 1) Control: non-transduced cells; 2) GFP: cells expressing only GFP; 3) Bcl-2: cells expressing both GFP and Bcl-2. The sub-lethal irradiation allowed the transplanted cells to repopulate the spleen of the recipient mice.

After four hours post transplant, all mice were infected with P. chabaudi parasitised erythrocytes. Mice were bred and maintained at the FES-Zaragoza-UNAM animal care facility in microisolator cages and were provided with a parasite promoting diet (TD.993 Harlan USA) and acidified water ad libitum; animals were sacrificed at the indicated days post-infection for the different studies.

B. Plasmid constructs All retroviral plasmids were based on the echotropic system using the Moloney Leukaemia Virus (MLV) Long Terminal Repeats (IMGENEX Corp.). The pCNRX-GFP plasmid expresses of the green fluorescent protein (GFP) under the transcriptional control of the minimal CMV promoter, flanked by the LTR´s of MLV. The Bcl-2 cDNA was cloned downstream of the DNA Polymerase II promoter into an EcoRI site of the pCLNRX-GFP plasmid. The resulting construct was named pCLNRX-GFP-Bcl-2. Endotoxin-free, high scale plasmid preparations (Qiagen Inc, USA) were used for plasmid sequencing, transfection assays, functional expression and viral packaging in HEK-293T cells.

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Gene Therapy and Molecular Biology Vol 12, page 303 µL of the cDNA (RT reaction mixture). #-actin and Bcl-2 were simultaneously amplified in the same tube. After 28 cycles, the PCR products were separated on 5 % acrylamide gels and stained with ethidium bromide. Band intensity was measured via densitometry (GelDoc, BioRad, Hercules, USA). Results are shown as the ratio between the density (arbitrary units) of Bcl-2 and the density of #-actin.

C. Packaging of retroviral particles The night before transfection, 3 x 105 HEK-293T cells/well were seeded in 6-well plates with DMEM media (Gibco/Invitrogen, USA) supplemented with 10% heat inactivated foetal bovine serum, (Gibco/Invitrogen) and incubated at 37°C with 5% CO2.

The media was replaced 3 h before co-transfecting the cells with 5 µg of both pCLNRX-GFP and pCL-Eco or pCLNRXGFP-Bcl-2 and pCL-Eco using a calcium phosphate precipitation protocol (Gibco/Invitrogen). In all transfection experiments, endotoxin-free plasmids were used to transfect the cells. The media was replaced 24 h post-transfection and the supernatants were collected 48 h after transfection. polybrene (Sigma, USA) was added to a final concentration of 8 µg/mL before infecting the target splenocytes.

H. Microscopy analysis GFP expression in infected cells was detected using an epifluorescent microscope (Bio-Rad Inc). Histological analysis was performed on frozen spleen slice sections embedded in Tissuetek (Dako). Several slices were fixed for routine haematoxylin and eosin staining protocol. Morphometric analysis and histopathological description was performed in the Department of Pathology of the Instituto Nacional de Rehabilitación (Mexico City).

D. Retroviral infection Splenocytes were isolated from healthy male mice and 3 x 108 cells were maintained in supplemented RPMI-1640 and 100 U/ml of recombinant IL-2 (Sigma-Aldrich, USA). The infection procedure was performed by adding the retrovirus-containing supernatants at a1:1 ratio to the splenocytes. After 24 h of incubation under standard conditions, transduced cells were used for transplants.

I. Cell phenotype characterization Suspensions of 1 x 106 splenocytes were washed in PBS and stained with pre-calibrated dilutions of PE-conjugated anti mouse CD3, CD4, CD8 or B220 monoclonal antibodies (BD Pharmingen, San Diego, CA, USA). Cells were incubated for 30 min at 4 °C, washed twice with FACS-buffer (0.1% bovine serum albumin, 0.1% sodium azide in PBS) and suspended in 500 µl of the same buffer. Fluorescence was analysed using a FACSCalibur flow cytometer and Cell Quest software (BD, San Jose, CA, USA). For each sample, 40,000 events were acquired and analysed. Dead cells were excluded by gating on PI negative cells.

E. Irradiation and spleen cell-transplant Recipient mice were exposed to "-irradiation equivalent to a total dose of 4.5 Gy at a rate of 450 cGy /min using the Siemens Biomed Inc. irradiator with a Cobalt-68 source (Instituto de Ciencias Nucleares, UNAM). Two hours postirradiation, the mice were transplanted with 2 x 107 transduced splenocytes resuspended in 100 µl of PBS (Gibco/ Invitrogen) by iv injection.

J. Statistical analysis Student’s significance.

t-test

was

used

to

determine

statistical

F. Infection and parasitaemias

III. Results

Groups of 6-8 week-old male CBA/Ca mice were inoculated iv with 5 X 104 P. chabaudi-parasitised erythrocytes as previously described (Legorreta-Herrera et al, 1993). Parasites were kindly donated by Dr. K N Brown (National Institute for Medical Research, London, UK). Parasitaemia was evaluated with Giemsa-stained blood smears starting at day 4 through day 7 post-infection. The course of infection in each group is shown as the percentage of parasitaemia.

A. Expression vectors and splenocyte infection Hematopoietic and lymphoid cells that have been transduced with retroviral vectors have been reported to reconstitute approximately 20 % of the total population of splenocytes (Mcmillin et al, 2005; Ide et al, 2008). In order to introduce a recombinant form of Bcl-2 into total splenocytes of mice which will be infected with P. chabaudi, to retroviral expression vectors, pCLNRX-GFP and pCLNRX-GFP-Bcl-2, were developed (Figure 1A).

In both constructs, the GFP cDNA was placed under the transcriptional control of the CMV enhancer promoter. In the case of pCLNRX-GFP-Bcl-2, the cDNA of rat Bcl-2 was placed under the control of the DNA polymerase II promoter. Therefore, Bcl-2 will only be expressed in proliferating cells, while GFP should be constitutively expressed even in quiescent cells.

Freshly prepared retroviral particles were used to transduced total murine splenocytes as described in Materials and Methods. Using fluorescence microscopy to detect the expression of GFP, we verified that the transduction protocol had no effect on the viability of the splenocytes (Figure 1B). The optimal multiplicity of infection was determined by serial dilution.

Approximately 1 x 106 viral particles/ml were used in all experiments and mixed with 1 x 106 total splenocytes in a final volume of 1 ml. Normally, splenocytes were

G. Bcl-2 mRNA expression On day 7 post-infection, mice were sacrificed and splenic mRNA was extracted using Trizol (Invitrogen). DNA was digested with DNAse I (Invitrogen) according to the manufacturer’s instructions and total RNA was quantified spectrophotometrically. Total RNA (1.5 µg) was reverse transcribed using 0.5 mM dNTP’s (Pharmacia, Uppsala, Sweden), 40 U of RNAse inhibitor (Invitrogen) and 200 U of MMLV-RT (Invitrogen) and incubated at 37°C for 30 min. A 1 µl sample of the resulting cDNA was used to amplify Bcl-2 and !-actin in duplicate. Both the number of cycles and the cDNA concentrations were optimised such that the reactions were in the logarithmic phase of amplification.

The following primers were used for Bcl-2 amplification: forward TCATGAAGACAGGGGCCTTTT, reverse TGGAGCTGCAGAGGATGATTG; and for !-actin: forward GTGGGCCGCTCTAGGCACCAA, reverse CTCTTTGATGTCACGCACGATTTC. PCR reactions were performed in a total volume of 20 µl. Amplification was carried out in 50 mM KCl, 10 mM Tris-HCl, 0.1 mg/mL Gelatin (SigmaAldrich), dNTP’s 200 mM each (Pharmacia, Uppsala, Sweeden), 2 mM MgCl2, 100 n moles each primers, 0.5 U Ampli Taq polymerase (Applied Biosystems, Branchburg, NY, USA) and 1

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MartĂ­nez-Flores et al: Enhanced splenic protection and reduction in a murine malaria model transplanted into irradiated mice 18 h after in vitro viral infection. In order to evaluate the efficiency of transduction, control cultures were monitored for GFP expression for 24, 48 and 72 h (data not shown). Figure 1B shows representative images of transduced splenocytes. The GFP signal was always bright in cells transduced with the construct encoding only GFP (Figure 1B, +/-). The GFP signal in cells transduced with the construct encoding Bcl-2 (+/+) was always of a lower intensity compared to the construct expressing only GFP. Despite the fact that the splenocyte came from different donors the transduction was consistent and reproducible.

The transduction efficiency was quantified by flow cytometry on the transduced cells 25-35 % of the total population of transduced splenocytes was GFP positive (Figure 1C central and right histograms).

B. In situ localization revealed homing of transplanted cells to the spleens of recipient mice To verify the homing of the transplanted cells to the spleens of recipient mice, we used GFP expression as a marker. Seven days post-transplantation and infection with P. chabaudi, longitudinal spleen slices were analysed for GFP expression. Large clusters of fluorescent cells were detected in the spleens of mice transplanted with Bcl-2 transduced cells (Figure 2, Bcl-2) compared to untransduced controls (-/-) or to GFP-transduced cells (+/). Additionally, more fluorescent cells were found along the periphery of the spleens of mice transplanted with cells transduced with the Bcl-2-expressing construct (+/+).

Interestingly, the spleens of mice transplanted with control cells were more fragile than the spleens from animals transplanted with transduced cells. These observations

Figure 1. Plasmid constructs used for retroviral gene delivery and expression in murine splenocytes. (A) Schematic representation of plasmid constructs for packaging of retroviral particles in 293-T cells (as described in Materials and Methods). (B) Fluorescence microscopy of uninfected murine splenocytes (-/-), infected with GFP vector (+/-) and infected with GFP-Bcl-2 (+/+). (C) Flow cytometry histograms examining the efficiency of transduction in total splenocytes before transplant. Control (CTR), cells transduced with GFP (GFP) or with GFP-Bcl-2 (Bcl-2).

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Figure 2. GFP signal in the spleens of recipient mice after transduction and seven days post-transplant. After irradiation mice received a transplant with the different transduced splenocytes were iv infected withP. chabaudi, spleens were removed and the fluorescent signal was evaluated in fresh tissue slices. Each field is presented in light transmission (Halogen light), UV/blue illumination (UV/blue) and green fluorescence (excitation 488 nm emission 530 nm). The first line correspondsto control animals transplanted with not-transduced splenocytes (-/-). The second (+/-) and third (+/+) lines correspond to the spleens of animals transplanted with GFP- or Bcl-2-transduced cells respectively.

demonstrate that the homing of splenocytes transduced with the different retroviral constructs took place in recipient mice transplanted with similar efficiencies.

transplanted cells, but it is also possible that the presence of the transplanted population leads to the expression of endogenous Bcl-2 in their surrounding cells.

C. Bcl-2 mRNA and protein expression in the spleens of transplanted mice

D. Decreased susceptibility to oxidative stress in cells expressing Bcl-2 both in vitro and in vivo

In order to identify and verify Bcl-2 transgene expression, RT-PCR and western blot analysis were performed on the spleens of transplanted mice.

Interestingly, the spleens of mice transplanted with GFPtransduced cells exhibited significantly enhanced Bcl-2 mRNA and protein expression (Figures 3A and B, GFP).

Figure 3A (Bcl-2) shows the amplified Bcl-2 fragment from the spleens of mice receiving Bcl-2-transduced cells.

Western blot analysis revealed Bcl-2 protein in the spleens of mice receiving splenocytes transduced with either construct (Figure 3B, GFP and Bcl-2). A 15-fold increase in the expression of Bcl-2, when compared to mice receiving untransduced cells, was seen in mice receiving GFP-transduced splenocytes (GFP). However, Bcl-2 expression was greater (50-fold increase) in the spleens of mice transplanted with Bcl-2 transduced cells (Figures 3A and B, Bcl-2). These results confirm the overexpression of Bcl-2 when cells are transduced with retroviruses encoding Bcl-2. Nevertheless, transduction alone appears to be enough to promote the expression of endogenous Bcl-2. This expression could occur in the transduced

As Bcl-2 overexpression confers protection against a variety of stressful conditions, including high concentrations of H2O2 and inducers of apoptosis (Korsmeyer et al, 1995; Yang et al, 1997; Mitsiades et al, 2007), we tested the potential protective effects of Bcl-2 overexpression on the viability of total splenocytes exposed to increasing concentration of H2O2 (Figure 4).

Initially, the efficiency of the protective effect of Bcl-2 overexpression was evaluated 48 hrs after in vitro culture following transduction (Figure 4A). Cell viability was assessed 2 h after the addition of increasing concentrations of H2O2 and is expressed relative to normal splenocytes not exposed to H2O2 (100%). In untransduced cells, the viability decreased with increasing H2O2 concentrations, while GFP-transduced cells were refractory to H2O2induced cell death, and viability remained relatively unchanged at approximately 50%. Statistical significance was only observed when the viability of normal cells and Bcl-2-transduced cells treated with 2 mM of H2O2 was compared (p<0.05). Having shown that the transduction 305

MartĂ­nez-Flores et al: Enhanced splenic protection and reduction in a murine malaria model with the retrovirus expressing Bcl-2 confers protection against H2O2 in vitro we evaluated if the protective phenotype was retained in vivo when mice were transplanted with transduced cells and infected with P. chabaudi. Given the difficulties in evaluating the potential protective effect of the expression of Bcl-2 in vivo, we evaluated cell viability in vitro in the total splenocyte population 72 h after transplantation (Figure 4B).

Interestingly, the general trend was similar to that observed in total splenocytes prior to transplantation (Figure 4A). Statistically significant differences (p<0.05) in the viability of splenocytes from mice receiving untransduced control cells or Bcl-2-transduced cells were only observed when cells were treated with the lowest dose of H2O2 (1 mM; Figure 4B).

Figure 3. Bcl-2 expression in the spleens of transplanted mice infected with P. chabaudi. Mice were transplanted with 2 x 107 splenocytes from donor mice, these cells were previously transduced with the Bcl-2expressing retrovirus (Bcl-2), the GFP-expressing retrovirus (GFP) or subjected to mock transduction (CTR). All mice were infected iv with 5 x 104 parasitised erythrocytes the same day. Seven days after parasite infection, animals were sacrificed and Bcl-2 expression in the spleen was analysed. (A) RT-PCR of Bcl-2 (lower panel) and densitometric analysis (histogram) compared to !-actin expression. (B) Western blot of Bcl-2 on total spleen cell protein extracts. L929e1: Total protein extracts from the L929 murine fibroblast cell line constitutively overexpressing Bcl2 used as a positive control. !actin was used as a loading control. Numbers below the western indicate the fold increase in the !-actin-normalised Bcl-2 signal compared to the control.

Figure 4. Hydrogen peroxide resistance of splenocytes before and after transplant into irradiated receptor mice infected with P. chabaudi. The viability of splenocytes after 2 h of challenge with different concentrations of H2O2 was determined. (A) Viability was measured after culture for 48 h in vitro. (B) Viability was evaluated 72 h after mice were irradiated and reconstituted with 3 x 107 splenocytes. As in previous experiments donor cells were either GFP- or BCL-2-transduced. Control cells were subjected to mock transduction (CTR). * p< 0.05 compared to control (CTR).

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Gene Therapy and Molecular Biology Vol 12, page 307 Taken together, these results demonstrate an increased cell viability in transduced cells, regardless of the presence or absence of the Bcl-2 cDNA, and this protective effect remained 72 h post-transplantation into irradiated mice.

While splenocytes transduced with the retrovirus expressing GFP alone demonstrated an increased viability compared to untransduced cells, the viability was always higher in cells expressing Bcl-2.

revealed a marked reduction in cellularity (Figure 5C, CTR), close to 40% with respect to the spleens from normal, non-transplanted animals. More than 90% of these cells were immunoblasts in the lymphoid compartment.

Additionally, the white:red pulp ratio was 1:3 in the spleens of mice transplanted with non-transduced cells compared to 1:5 in normal untransplanted spleens (Figure 5A, NORMAL and CTR). Haemosiderin deposits and detritus were also observed in the spleens of mice transplanted with untransduced splenocytes.

In the GFP group, the total cell population in the lymphoid compartment was 53% of the normal, untransplanted spleen (Figure 5C). Immunoblasts were the most abundant cell type (90% of the cells) with a small amount of macrophages. Apoptotic bodies and mitotic figures were distributed randomly. Additionally, the red pulp was enlarged and contained a high number of parasitised cells as well as macrophages with haemosiderin (data not shown). The white:red pulp ratio was 2:1.

E. Histologic and morphometric analysis of the spleen Both a macroscopic and microscopic analysis of the spleens of recipient mice was carried out. All the spleens had increased friability but it was more evident in the control and GFP groups (data not shown). The histology of the spleens from mice transplanted with normal splenocytes (Figure 5A, NORMAL) was different when compared to the spleens of normal, non-transplanted mice (Figure 5A, CTR). Spleens from mice transplanted with non-transduced cells and infected with P. chabaudi

Figure 5. Histologic and morphometric analysis of the fresh spleen slices stained with haematoxilin and eosin. A ( ) Comparative analysis of tissues from mice spleens of different experimental groups. Histology of an animal that was not transplanted and nor infected with P. chabaudi (NORMAL). Histologies of animals infected with P. chabaudi and transplanted with: normal cells (CTR), GFP transduced cells (GFP) or Bcl-2-transduced cells (Bcl-2). Red Pulp (RP); White Pulp (WP). (B) Magnification of the micrograph labelled Bcl-2.

Immunoblasts (I); small cell (S); detritus (D); haemosiderin (H). (C ) Histogram of the morphometric analysis from the four groups.

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MartĂ­nez-Flores et al: Enhanced splenic protection and reduction in a murine malaria model The spleens of mice transplanted with Bcl-2transduced cells and infected with P. chabaudi (Figure 5A, Bcl-2) had 77% of the cellularity seen in normal, untransplanted spleen (Figure 5C, Bcl-2). In this group a new cell population was observed that was characterised by a small size with a clear, defined central round nucleus.

This new population comprised 30% of the total splenocytes, while immunoblasts and macrophages comprised 66% and 4%, respectively. As seen in Figure 5C, the number of immunoblasts and macrophages was very similar in the three groups infected with P. chabaudi (CTR, GFP and Bcl-2). Combined other cell types in the lymphoid compartment represented less than 1% of the total population. The white to red pulp ratio was similar to that observed in the GFP group (2:1).

We conclude that the spleens from mice transplanted with cells transformed with the Bcl-2-transduced cells infected with P. chabaudi retained the cytoarchitecture with diminished cellularity when compared to the spleens from normal, non-transplanted mice. In addition, a higher white:red pulp ratio was observed in the spleens of mice transplanted with transduced cells, regardless of the presence or absence of Bcl-2.

evaluated daily after day 4 and until day 7 post-parasite infection. Parasitaemia increased gradually and no difference was observed at day 4. Interestingly, on day 5 post-infection mice transplanted with splenocytes transduced with either retrovirus showed a transient 10fold decrease in parasitaemia (solid squares and triangles, p<0.01). Additionally, mice transplanted with the Bcl-2transduced cells (solid triangles, p<0.05) showed a significantly lower level of parasitaemia compared to mice transplanted with GFP-transduced cells (solid squares).

However, by day 6, the protective effect of Bcl-2 was lost.

We conclude that the retroviral transduction alone conferred a transient protection that was strengthened with the additional expression of Bcl-2.

IV. Discussion The use of viral vectors for gene therapy has focused on genetic disorders, such as metabolic diseases or cancer (Grompe et al, 1995; Bilbao et al, 1999; Gomez-Navarro and Curiel, 2000; Bartsch et al, 2007; Muul and Candotti, 2007), while little work has been done utilizing the vector to treat infectious diseases. Using conventional methods, we have introduced an exogenous form of Bcl-2 cDNA into murine splenocytes with the aim of interfering with the apoptosis present in an experimental model of malaria.

In spite of the relatively small percentage of cells transduced with the retroviral vector that repopulated the spleens of irradiated mice, their presence appeared to be enough to induce biological effects against Plasmodium, even in the absence of the Bcl-2 cDNA. Taken together, these findings suggest that the transduction procedure with the retroviral vector is sufficient to induce beneficial responses against Plasmodium, possibly by recruiting normal splenocytes. Similar to other studies (Del Vecchio et al, 2001; Mcmillin et al, 2005; Kinyanjui et al, 2006) that have used viral vectors, we encountered the problem of generating a high enough viral titre to elicit a robust biological response (Figure 1B, C).

F. Transfer of transduced cells into animals infected with P. chabaudi reduces parasitaemia During P. chabaudi infection, a variety of immunological mechanisms have been implicated in the destruction of infected erythrocytes, including the effector function of splenic macrophages. Immunosupression linked to the activation of lymphocyte apoptosis has been described in malaria, leishmania and schistosoma parasitosis (Estaquier et al, 1997; Das et al, 1999; Mukherjee et al, 2006). Consequently, we tested the effect of Bcl-2 overexpression sub-lethally irradiated mice transplanted with transduced splenocytes and infected with P. chabaudi (Figure 6) on parasitaemia. Parasitaemia was

Figure 6. Course of parasitaemia with Plasmodium chabaudi in mice transplanted with genetically modified cells. Parasitaemia was measured as described in Materials and Methods in mice sublethally irradiated and transplanted with: normal splenocytes (CTR); GFPtransduced splenocytes (GFP) or Bcl-2-transduced splenocytes (Bcl-2). Bars represent standard deviation of the mean.

Comparison CTR against GFP or Bcl-2 is represented by *, with a p< 0.01. Comparison between GFP and Bcl-2 is represented by **, with a p<0.05.

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Gene Therapy and Molecular Biology Vol 12, page 309 We attempted to increase the efficiency of transduction in different ways: i) identification of the optimal time to harvest the viral particles; ii) concentration of the retroviral particles with different reagents such as hexadimethrine bromide (polybrene) or chondroitin 6sulphate (Cepko, 2001; Del Vecchio et al, 2001; Mcmillin et al, 2005); iii) the use of a variety of re-infection protocols; iv) expansion of the transduced cell population with growth factors such as IL-2. However, the optimal combination of all these variables did not lead to transduction efficiencies above 30 % (Figure 1C).

The reconstitution protocol most frequently used in experimental models of transplantation uses the total splenocyte population, as it is believed that the interactions between the various populations of cells are required for the generation of an adequate immune response (Legorreta-Herrera et al, 1993). As such, we transplanted total splenocytes following in vitro transduction.

Preliminary attempts to characterize the transduced cells suggest that they include B220+ cells, a minority CD3+ cells and other cells negative for these markers (data not shown). While it is possible that splenic repopulation with untransduced cells may contribute to the protective effects observed, we discounted this possibility based on the fact that the control group corresponds to irradiated animals transplanted with mock-transduced cells.

In spite of the low number of transduced cells used in the transplant, we were able to observe GFP positive cells in the spleen of transplanted mice 48 h (Figure 2) and even 7 days after transplantation (data not shown).

Interestingly, despite the fact that our study was designed to observed the effects of over-expression of Bcl2, the transduction of splenocytes with the empty construct (pCLNRX-GFP) led to the increased expression of endogenous Bcl-2 in vivo 7 days post-transplant (Figures 3A, B). Taking into account that only a small number of GFP positive cells were present at day 7 after transplantation, both Bcl-2 mRNA and protein are likely generated in non-transduced cells. We postulate that transduced cells influence the splenic microenvironment such that endogenous Bcl-2 expression is stimulated. It is possible that the transduction with retroviruses expressing Bcl-2 confers an increased survival of these cells further improving their influence on the rest of the spleenocytes.

We also postulate that the transduced cells influence the splenic microenvironment through the secretion of paracrine factors. Alternatively, the presence of transduced cells could activate a defence response in the remaining population of splenocytes. At this point we cannot distinguish between these two possibilities. In any event, the fact that expression of transgenic Bcl-2 has only a minor contribution to the in vitro protection against H2O2 as well as the decreased parasitaemia observed in vivo could be due to the low transduction efficiency (Figures 4, B).

In contrast, the gross morphology and cytoarchitecture of the spleen were well-preserved only in mice transplanted with Bcl-2-transduced cells and infected with P. chabaudi. This effect could be appreciated macroscopically with less organ fragility and the preservation of the proportion of red pulp compared to

normal spleens. One measure of the organ damage during Plasmodium infection is the marked reduction in cellularity observed in the control group reconstituted with untransduced splenocytes compared to the other three groups. Additionally, a new cell population represented mainly by cells with morphology similar to mature lymphocytes was observed. Further analysis with surface markers could better define this population (Figure 5A, Bcl-2, magnified in Figure 5B).

Increasing splenic fragility is commonly observed during the progression of malaria. This event is the consequence of clearance of the parasitised erythrocytes by the spleen. However, the radiation procedure used to promote cellular homing in this animal model could have a synergistic effect on the splenic integrity. These factors could explain the increased spleen friability in all animals.

However, the marked reduction of fragility observed only in the Bcl-2-transduced mice correlates with the overexpression of exogenous protein. Recently, Hanson et al, reported that increased intracellular levels of Bcl-2 confer an anti-apoptotic effect that depends on the kind of promoter employed to express Bck-2 (Hanson et al, 2008).

In this study, exogenous Bcl-2 expression is directed by the Pol-II promoter suggesting that Bcl-2 expression is limited only to replicating cells. It is noteworthy that in the GFP-transduced group endogenous Bcl-2 is already increased. Consequently, in the Bcl-2-transduced group, an additive effect of endogenous and exogenous Bcl-2 can be postulated. In summary, the biological effect of a small number of cells expressing recombinant Bcl-2 on splenic morphology and cytoarchitecture could be interpreted to favour survival and maturation of the surronding cells. A similar effect has been reported previously in a model of endothelial cells (Enis et al, 2008).

As opposed to the white:red pulp ratio in the control group, the white:red pulp ratio in the spleens of mice transplanted with either population of transduced cells was similar to ratio seen in normal spleens. This could be interpreted as an active cellular phase of the immune response.

Interestingly, the positive effects in the splenic cytoarchitecture and in the white:red pulp ratio correlate with the homing of a small number of the transplanted transduced splenocytes expressing Bcl-2 and the appearance of a distinct cell population characterized by its small size and clear, defined central nucleus. The morphology of this latter cell population is suggestive of mature splenocytes (Figure 5).

The most dramatic biological effect observed was the 10-fold decrease in parasitaemia that implies an efficient host response against the parasite despite the small number of transplanted cells transduced with the retroviral vector.

The fact that this protective effect was elicited with a small number of cells expressing only GFP suggests that the positive modulation of immune cells from the recipient mouse lead to ore efficient parasite elimination. This effect correlates with the15-fold increased expression of endogenous Bcl-2 (Figures 3A,B). Exogenous expression of Bcl-2 provided an additional 2-3-fold increase in protection (Figure 6) that correlated with a similar increased expression of Bcl-2 due to the expression

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construct. In addition, all correlate with the histological findings that suggest an improved splenic microenviroment that could effectively induce a cellular immune response against the parasite. However, it remains unclear why protection is transient.

While gene therapy is based on the premise of introducing a specific cDNA to compensate for endogenous deficiencies, we found that in the case of experimental murine malaria, the presence of splenocytes transduced with the empty retroviral vector have a significant protective effect both in vitro and in vivo. Our observations indicate that a small number of genetically manipulated splenocytes had a significant biological effect likely due to the recruitment of normal cells. In this regard, malaria offers an interesting model in which the spleen plays a central role in the destruction of parasitised erythrocytes. This observation suggests that in parasitic infections that require efficient splenic function, empty viral vectors used in gene therapy may be able to activate host defence responses by themselves.

Author’s contributions FMF, JVG and MLH. Performed all experiments and wrote the manuscript AZD wrote the manuscript and contributed to the analyses of the data. EGE and HVC and FMF performed and interpreted the histopathology. LCR provide the constructs and viral vectors. ECZ was responsible for the animal irradiation.

Acknowledgements We thank to units of electronic microscopy and molecular biology (Instituto de Fisiología Celular, UNAM) for assistance. This work was supported by the following grants: PAPIIT, UNAM: IN22929607, IN214007; CONACyT: 45519-M and 52782.

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Gene Therapy and Molecular Biology Vol 12, page 313 Gene Ther Mol Biol Vol 12, 313-357, 2008

Microtubule-targeted antitumor drugs: chemistry, mechanisms and nanoparticle formulations Review Article

Teni Boulikas1,2*, Ioannis Tsogas3 1

Regulon, Inc. 715 North Shoreline Blvd, Mountain View, California 94043, USA Regulon AE, Afxentiou 7, Alimos, Athens 17455, Greece 3 Dendrigen AE, Afxentiou 3, Alimos, Athens 17455, Greece 2

__________________________________________________________________________________ *Correspondence: Teni Boulikas, Ph.D., Regulon AE, Afxentiou 7, Alimos, Athens 17455, Greece; Tel: +30-210-9858454; Fax: +30210-9858453; e-mail: teni@regulon.org Keywords: Microtubules, tubulin, vinca alkaloids, vinblastine, vinorelbine, vincristine, vindesine, vinflunine, taxanes, paclitaxel, docetaxel, epothilones A, B, D, ixabepilone, sagopilone, discodermolide, P-glycoprotein, dictyostatin, abraxane, colchicine, aplidine, nocodazole, dictyostatin, peloruside A, cyclostreptin, vinflunine, griseofulvin, nanoparticle Abbreviations: 2!,3!-cyclic nucleotide-3!-phosphodiesterase, (CNP); Breast Cancer Gene 1, (BRCA1); disease control rate, (DCR); Epidermal Growth Factor Receptor, (EGFR); Guanosine 5'-Triphosphate, (GTP); half maximal inhibitory concentration, (IC50); highdensity lipoprotein, (HDL); metastatic breast cancer, (MBC); Microtubules, (MTs); overall response rate, (ORR); renal cell carcinoma, (RCC); Retinoblastoma, (RB); response rate, (RR); vascular endothelial growth factor, (VEGF) Received: 30 September 2008; revised: 10 December 2008; Accepted: 19 December 2008 Electronically published: 19 December 2008

Summary The ingenious application of vinca alkaloids (vinblastine, vinorelbine, vincristine, vindesine, vinflunine) destabilizing microtubules and of taxanes (paclitaxel, docetaxel) stabilizing microtubules has been a milestone achievement in oncology. Recent investigations into their molecular mechanism revealed that all compounds possess additional pleiotropic effects that converge on induction of apoptosis in cancer cells via activation of signaling pathways. Their success has prompted vigorous investigations into microtubule-targeting activity from natural products as well as synthetic molecules arising from molecular modeling that led to the identification of Epothilones A, B, D, Ixabepilone, Sagopilone, Discodermolides, Dictyostatin, Peloruside A, and ABT-751; an additional purpose for epothilone drug discovery has been to bypass paclitaxel resistance mainly arising from the efflux function of Pglycoprotein. Nanoparticles provide a new mode of cancer drug delivery functioning as a carrier for entry through fenestrations in tumor vasculature. The 130-nm nanoparticle formulation albumin-bound paclitaxel (Nabpaclitaxel, Abraxane™) utilizes the natural properties of albumin to reversibly bind paclitaxel, transport it across the endothelial cell and concentrate in tumors; Abraxane™ received regulatory approval in the USA from a higher response rate and longer time to progression than Taxol in patients with metastatic breast cancer. The success of Abraxane™ led to an explosion in research on polymer nanoparticle formulations for taxanes using micellar PEGylated hyperbranched polyesters, polyglycerol-polyethylene glycol copolymers, cyclodextrin nanoparticles, polylactide-co-glycolide PEG and many others. Several such formulations are expected to enter the market. Other tubulin polymerization inhibitors reviewed here include tubulysin A, a highly cytotoxic peptide from myxobacteria, CC-5079, bisbenzylisoquinoline alkaloids, aplidine, nocodazole, GMC-5-193, cyclostreptin, colchicine, TLK-286 and vinflunine, a novel third generation vinca alkaloid. Structural similarities have been used to further modify the successful microtubule-targeted drugs in order to seek molecules of improved efficacy, of lower toxicity or able to overcome tumor resistance. We review the molecular mechanism of these drugs, whenever feasible, we suggest correlations between their chemical structure and mechanism and point to the importance of drug delivery for success.

estimated 6.72 million people worldwide were newly diagnosed with any the most 10 prevalent forms of solid cancers; of these, 4.15 million died within the same year.

Based on projections, the death toll will rise to 9 million cancer deaths in 2015.

I. Introduction Cancer is one of the leading causes of death worldwide; it claimed 7.6 million deaths (13.1%) in 2005 out of 58 million deaths from all causes. In 2002, an

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Boulikas and Tsogas: Microtubule-targeting anticancer drugs page Chemotherapy, surgery and radiotherapy continue to be the mainstay treatments of cancer. Over 700 FDAapproved drugs have entered into clinical practice during the last 30 years; these are classified into six major groups that include (1) the platinum coordination complex, (2) antimicrotubule agents (vinca alkaloids, taxanes), (3) antimetabolites (methotrexate, fluoropyrimidines, cytocine arabinose, gemcitabine), (4) antitumor antibiotics (actinomycin D, mitomycin C, bleomycin, anthracyclines, podofylotoxines, camptothecines), (5) alkylating agents, and (6) others including a number of biological drugs or monoclonal antibodies that target specific pathways such as EGFR or angiogenesis.

Tubulin has been an attractive anticancer target since the dawn of medical oncology because of its role in chromatid separation in mitosis and the possibility of intervention at this step of the cell cycle with agents that stabilize tubulin polymers (microtubules). Microtubules (MTs) can be viewed as dynamically unstable tubulin polymers in equilibrium with monomers that interconvert stochastically between growing and shrinking states, a property central to their cellular functions. Each time a tubulin monomer is incorporated into the polymer, one GTP molecule is hydrolyzed. The GTPase activity of tubulin is enhanced by stathmin-like domains and colchicine and is inhibited by vinblastine and by the Nterminal part of stathmin-like domains. The residues involved in GTPase activity comprise the !-tubulin GTP binding site and !-tubulin residues that participate in intermolecular interactions in protofilaments (Wang et al, 2007).

We have previously reviewed platinum drugs that have been synthesized for cancer and entered into clinical trials, including successful nanoparticle formulations (Boulikas et al, 2007). We review here the class of antimicrotubule agents.

II. Microtubules (MTs) as dynamic structures involved in spindle formation A. Microtubules and the centrosome The mitotic spindle is a specialized structure required for exact chromosome segregation in mitosis. Spindle formation is dependent on the reorganization of interphase microtubule network, regulated by cell cycle-regulatory mechanisms. The centrosome (known as the microtubule organizing center) is involved in the formation of spindle poles during mitosis, which ensures the distribution of the correct number of chromosomes to daughter cells.

Aberrant centrosome duplication could cause centrosome amplification and chromosomal instability.

In many animal cells, minus ends of microtubules are capped by the centrosome whereas plus ends are free and display dynamic instability. The role of the centrosome in microtubule dynamics was explored by studying microtubule behavior in cytoplasts from which the centrosome was removed. Fibroblast (CHO-K1) and epithelial (BSC-1) cells were investigated. Removal of the nucleus through centrifugation after cytochalasin/nocodazole treatment gave cytoplasts that either contained the centrosome and displayed a dense radial microtubule array (Figure 1, Middle pictures) or lacked the centrosome and displayed a loose and sparse network of randomly arranged microtubules (Figure 1, Right). The pattern of MT dynamics were evaluated by injecting intact cells with Cy3-tubulin, preparing cytoplasts, and acquiring digital-fluorescence time-lapse sequences of images. Living fibroblast cytoplasts containing or lacking centrosomes were readily distinguishable by the high density and radial arrangement of MTs invariably associated with the centrosome.

Figure 1.

Distribution of microtubules in intact cells and cytoplasts. Intact cells (Left) and cytoplasts containing (Center) or lacking (Right) the centrosome were fixed and triple-stained with !-tubulin antibody for microtubules (red), "-tubulin antibody for the centrosome (green, but superposition makes the spot appear yellow) and 4!,6diamidino-2-phenylindole (DAPI) for the nucleus (blue). (Upper) Fibroblast CHO cells; (Lower) epithelial BSC-1 cells. In contrast to fibroblast cells, minus ends of MTs in epithelial cells did not depend on the centrosome for their stability. (Bar = 10 #m.) From "Rodionov V, Nadezhdina E, Borisy G (1999) Proc. Natl. Acad.

Sci. USA. 96: 115-120. Copyright 1999 National Academy of Sciences, U.S.A."

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Gene Therapy and Molecular Biology Vol 12, page 315 These studies suggested that a minus-end depolymerization mechanism functioned to eliminate errors in microtubule organization and that dynamic instability of plus ends was a result of capping of minus ends by the centrosome (Rodionov et al, 1999).

Fluorescence imaging of microtubules in living cytoplasts with or without a centrosome is shown in Figure 2. In CHO cytoplasts containing the centrosome, most MTs (68%) displayed dynamic instability behavior with alternating phases of growth and shortening at their distal (plus) ends. In contrast, in cytoplasts lacking the centrosome, dynamic instability was never observed. In contrast to fibroblast cells, minus ends of MTs in epithelial cells did not depend on the centrosome for their stability.

membrane as 2!,3!-cyclic nucleotide-3!-phosphodiesterase (CNP). The CNP is both prenylated and palmitoylated, providing hydrophobic domains for membrane intercalation. The association of CNP and tubulin in membrane and cytoskeletal compartments was shown with immunofluorescence. Fluorescent labeling of microtubules (green) and CNP (red) of FRTL-5 cells revealed patches of colocalization (yellow) of the two proteins at the membrane and subplasmalemmal region. The patches are interrupted by zones, containing only CNP. Microtubules extending toward the membrane show no association with CNP, but the perinuclear region again shows abundant overlap of the two proteins. Thus, CNP acts as a microtubule-associated protein and this activity resides in the C terminus of the enzyme. Submembranous colocalization of the proteins and CNP-dependent microtubule organization (Figure 3) suggest that CNP is a membrane-bound microtubule-associated protein that can link tubulin to membranes and may regulate cytoplasmic microtubule distribution (Bifulco et al, 2002).

B. Association of tubulin with plasma membrane The bulk of cellular tubulin is cytoplasmic, but a significant fraction is embedded in, or firmly associated with, the plasma membrane and other membranes. A possible linker protein for microtubules to the plasma

Figure 2. Fluorescence imaging of microtubules in living cytoplasts. In centrosome containing cytoplasts (Top), microtubules (MTs) showed dynamic instability at their plus ends whereas free MTs rapidly shortened from their minus ends. In centrosome-free cytoplasts (Middle), MTs persistently grew at one end and shortened at the other end. Injection of tubulin at low concentration resulted in nonuniform incorporation of subunits along MTs and produced â&#x20AC;&#x153;specklesâ&#x20AC;? along their length. Speckles remained stationary, indicating that the mechanism of translocation was treadmilling (Bottom). Black arrowheads point to shortening and white arrowheads to growing ends. White arrows point to speckles. Numbers indicate time in seconds. (Bars = 1 #m). From "Rodionov V, Nadezhdina E, Borisy G (1999) Proc. Natl. Acad. Sci. USA. 96: 115-120. Copyright 1999 National Academy of Sciences, U.S.A."

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Figure 3. Colocalization of tubulin and CNP in FRTL-5 rat thyroid cells. Cells were grown on coverslips, fixed, and stained with a monoclonal anti-!-tubulin antibody [fluorescein (a)] or an antibody to CNP1 [rhodamine (b)]. (c) Double immunofluorescence (superimposition of a and b staining). (d) Enlarged membrane region from c. (e) Overlap of CNP and tubulin in a cytoskeleton prepared from a COS cell. Cells were fixed and incubated with monoclonal anti-!-tubulin antibody (Amersham Pharmacia) for 1 h, followed by tetramethylrhodamine isothiocyanate (TRITC)-labeled goat anti-mouse IgG (Sigma) for 1 h. Secondary antibodies for tubulin were either fluorescein- or rhodamine-labeled. From "Bifulco M, Laezza C, Stingo S, Wolff J (2002) Proc. Natl. Acad. Sci. U S A. 99: 18071812, Copyright 2002 National Academy of Sciences, U.S.A."

C. Tumor suppressor proteins are localized in centrosomes

transition, and a complex with Rad51 is associated with chromosomes during S phase and participates in DNA repair. BRCA1 is a component of RNA polymerase II and a coactivator of p53-mediated transcription, and may thus regulate the expression of other genes required for cell cycle progression.

BRCA1 was associated with the centrosome during mitosis. This was shown by coimmunostaining of COS-7 cells with mouse monoclonal "-tubulin antibody and rabbit polyclonal BRCA1 antibody (Figure 4). Two BRCA1specific antibodies were used: MS110, a mouse mAb raised against a BRCA1-GST fusion protein containing amino acids 1-304 of human BRCA1 protein, and C-20, a rabbit polyclonal antibody raised against a peptide corresponding to amino acids 1843-1862 of human BRCA1. A series of double-staining experiments have confirmed the localization of BRCA1 protein at mitotic centrosomes using C-20 and MS110 for BRCA1 staining, "-tubulin and pericentrin antibodies for centrosome staining, and "-tubulin antibody for microtubule staining.

In addition, DAPI staining of DNA was used to locate the nucleus. Double-staining of COS-7 cells with "-tubulin antibody and BRCA1 C-20 antibody provided direct evidence for the presence of BRCA1 protein at mitotic centrosomes. Two-color (BRCA1+"-tubulin) or threecolor (BRCA1+"-tubulin+DAPI) composite images showed colocalization of the BRCA1 and "-tubulin signals at mitotic centrosomes (Figure 4). The concentration of BRCA1 signal at mitotic centrosomes was apparent from prometaphase to metaphase (Figure 4A) and early anaphase (Figure 4B). BRCA1 staining diminished at the centrosome as cells proceeded to late anaphase (Figure 4C). Results were similar when COS-7 cells were

The centrosome controls assembly of microtubules, a process that plays a central role in organizing cell structure, determining cell polarity, directing cell movement during interphase, and orchestrating formation of the bipolar spindle during mitosis. Furthermore, centrosomes play an important role in maintaining the fidelity of chromosome distribution during cell division.

Loss of these functions might cause chromosomal instability and aneuploidy. Centrosome amplification drives chromosomal instability in tumor development.

Tumor suppressor proteins such as p53 and retinoblastoma (RB) have been localized to the centrosome in a cell cycle-dependent manner. A number of proteins involved in the G2/M checkpoint were also found to be associated with centrosomes during cell cycling, e.g., cyclin B, p34cdc2, and 14-3-3. Poly(ADPribose) polymerase 1 involved in opening up chromatin for DNA repair and transcription and able to bind to DNA strand breaks was also found to be localized to the centrosomes during mitosis and was suggested to be involved in maintenance of chromosomal stability (Kanai et al, 2007).

BRCA1, a suppressor of tumorigenesis in breast and ovary, is a protein of 1,863 amino acids with an Nterminal zinc-ring domain, a C-terminal transactivation domain and two putative nuclear localization signals.

BRCA1 is involved in progression of the cell cycle. Its expression and phosphorylation are cell cycle dependent and its overexpression induces growth arrest or apoptosis.

BRCA1 plays a continuous role throughout the cell cycle: expression and phosphorylation is induced at G1/S 316

Gene Therapy and Molecular Biology Vol 12, page 317 costained with the MS110 BRCA1-specific antibody (Figure 5) (Hsu and White, 1998).

A hypophosphorylated form of BRCA1, a suppressor of tumorigenesis in breast and ovary, localized with the centrosome during mitosis and coimmunoprecipitated with "-tubulin, a centrosomal component essential for nucleation of microtubules (Figure 5).

Immunofluorescence staining of a population of replicating COS-7 cells revealed the usual dot pattern in the nucleus. However, a unique staining pattern reminiscent of centrosomes was observed in mitotic cells.

These data suggested that BRCA1 also plays a functional role with mitotic centrosomes (Hsu and White, 1998).

The cellular targets for estramustine, an antitumor drug used in the treatment of hormone-refractory prostate cancer, are believed to be the spindle microtubules responsible for chromosome separation at mitosis. Video microscopy showed that estramustine strongly stabilized growing and shortening dynamics at plus ends of bovine brain microtubules devoid of microtubule-associated proteins. The combined suppressive effects of vinblastine and estramustine on the rate and extent of shortening and dynamicity were additive. Thus, like the antimitotic mechanisms of action of the antitumor drugs vinblastine and taxol, the antimitotic mechanism of action of estramustine may be due to kinetic stabilization of spindle microtubule dynamics (Panda et al, 1997).

D. Microtubule-associated proteins A number of microtubule-associated proteins have been reported; CLIPs are proteins known to associate specifically with the ends of growing microtubules, and CLASPs colocalize with CLIPs at the microtubule plus distal ends. CLASP1 localizes near the plus ends of growing spindle microtubules and is required for attachment of microtubules to kinetochore. hOrbit1 plays a role in polymerization of tubulin and interaction between microtubules (Figure 6) (Aonuma et al, 2005). Time-lapse fluorescence microscopy demonstrated that noncentrosomal MTs in cultured epithelial cells arise primarily by constitutive nucleation at, and release from, the centrosome. After release, MTs moved away from the centrosome and tended to depolymerizes (Keating et al, 1997). Aurora B is a protein kinase and a chromosomal passenger protein that undergoes dynamic redistribution during mitosis. Aurora B was found at centromeres at prophase but redistributed to the spindle midzone and became concentrated at the equator along midzone microtubules. Depolymerization of microtubules inhibited the dissociation of aurora B from centromeres at early anaphase and caused the dispersion of aurora B from the spindle midzone at late anaphase (Murata-Hori et al, 2002).

Figure 4. Coimmunostaining of COS-7 cells with mouse monoclonal "-tubulin antibody and rabbit polyclonal BRCA1 antibody C-20.

(A) a prometaphase to metaphase cell; (B) an early anaphase cell, and (C) a late anaphase cell. The colocalized signals of BRCA1 and "tubulin are yellow. DAPI counterstained DNA. Arrows indicate the positions of centrosomes. From "Hsu LC, White RL (1998) Proc.

Natl. Acad. Sci. U S A. 95: 12983-12988, Copyright 1998 National Academy of Sciences, U.S.A."

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Figure 5. COS-7 and E6/BE46 cells were costained with mouse monoclonal BRCA1 antibody MS110 (a) and rabbit polyclonal pericentrin antibody 4B (b); with MS110 (d) and rabbit polyclonal BRCA1 antibody C-20 (e); with mouse monoclonal "-tubulin antibody (g) and C-20 (h); or with mouse monoclonal !-tubulin antibody (j) and C-20 (k). c, f, i, and l include DAPI counterstain of DNA. a-f highlight mitotic COS-7 cells; g-i are interphase COS-7 cells; j-l illustrate a mitotic E6/BE46 cell. Arrows indicate the positions of centrosomes. From "Hsu LC, White RL (1998) Proc. Natl. Acad. Sci. U S A. 95: 12983-12988, Copyright 1998 National Academy of Sciences, U.S.A."

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Figure 6. Localization of GFP-hOrbit1 NF (GFP-hOrbit1 N-terminal fragment) and microtubules. (A-D) Immunofluorescent images of GFP-hOrbit1 NF expression cell. Cells were cultured for 16 h after transfection. Microtubules immunostained with anti-!-tubulin antibody, and DNA stained with DAPI. GFP-hOrbit1 NF image (A), microtubule image (B) and DNA image (C) were merged (D). In the merged image, the yellow color indicates colocalization of GFP-hOrbit1 NF and microtubules. (E) Immunofluorescent images of control cells. The cells without GFP-hOrbit1 NF transfection were immunostained with anti-!-tubulin antibody, and DNA was stained with DAPI. Microtubule image (red) and DNA image (blue) were overlaid. Bar represents 10 #m. From: Aonuma M, Miyamoto M, Inoue YH, Tamai K, Sakai H, Kamasawa N, Matsukage A (2005) Cell Struct Funct. 30: 7-13, with kind permission from the Japanese Society for Cell Biology

The orbit encodes Orbit/Mast, a 165-kDa microtubuleassociated protein (MAP) with GTP-binding motifs; hypomorphic mutations in the Drosophila orbit gene cause abnormal chromosome segregation (Aonuma et al, 2005).

Two human homologues of the Orbit/Mast, CLASP1 (hOrbit1) and CLASP2 (hOrbit2) have been identified.

Using an antibody, the 150 kDa CLASP1/hOrbit1 polypeptide was found to be associated with microtubules.

Figure 6 shows the subcellular localization of GFPhOrbit1 after trasfection of cells with a plasmid expressing a fusion protein of the putative microtubule-binding domain (1-662 out of 1289 residues) of hOrbit1 with GFP. Confocal laser scanning microscopic observation revealed that the GFP-fluorescence associated with short and thin filaments in the perinuclear region during the short period after plasmid transfection, and colocalized with only part of the microtubules. GFP fluorescence was later detected on the abnormally longer and thick bundles of microtubule filaments. Finally the bundles formed networks in the perinuclear region. The results suggest that the GFPhOrbit1 N-terminal fragment (GFP-hOrbit1 NF) binds to the newly formed microtubules rather than the pre-formed ones (Aonuma et al, 2005).

III. Taxanes When taxanes (paclitaxel, docetaxel) were introduced as anticancer agents some 20 years ago, their broad spectrum of activity was striking. Taxanes were shown to be microtubule-targeting agents, able to stabilize tubulin polymers but also to disrupt additional cellular processes and to induce apoptosis (reviewed by Rowinsky and Calvo, 2006). A plethora of clinical trials was set to optimize the different ways drugs can be administered; for example, the addition of cisplatin or carboplatin to paclitaxel resulted in higher response rates than for each of the drugs as single agents (reviewed by Ranson and Thatcher, 1999).

Antimicrotubule agents appear to act also by induction of apoptosis by convergence of several signaling pathways ending with caspase activation and chromatin fragmentation. A functional p53 protein and expression of the apoptosis-promoting protein, bax are the most studied pathways for drug-induced apoptosis. Necrosis can be assessed by Annexin binding and propidium iodide permeability in aqueous medium (Serafin and Bohm, 2005).

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Boulikas and Tsogas: Microtubule-targeting anticancer drugs page undergo apoptosis, suggesting that phosphorylation of Bcl2 may inhibit Bcl2 function. In addition, Bcl2 phosphorylation appears to inhibit its binding to Bax, since less Bax was observed in an immunocomplex with Bcl2 in taxol-treated cancer cells. Overexpression of Bcl2 counteracts the apoptotic effects of low doses of paclitaxel but has no effect against high doses. Furthermore, microtubule-damaging drugs such as paclitaxel induced apoptosis, caused growth arrest in G2/M phase of the cell cycle, induced caspase 3 activation as well as poly(ADPribose) polymerase (PARP) degradation, but did not induce p53 (Srivastana et al, 1998).

A model showing the binding of Taxol with tubulin is shown in Figure 8.

Incubation of cells with high Taxol concentrations leads to the formation of stable bundles of microtubules that disrupt the normal polymerization/depolymerization cycle of microtubules and results in the arrest of cells in the G2/M phase of the cell cycle. In addition to massive bundle formation, increased microtubule polymer mass is observed after treatment with high concentrations of Taxol. However, low concentrations of Taxol (10 nM) inhibit mitosis in HeLa cells by suppressing microtubule dynamics rather than by altering the microtubule polymer mass or inducing bundle formation. The mitotic block induced by 10 nM Taxol is sufficient to induce apoptosis.

These observations in HeLa cells indicate that Taxolinduced cell death may result from different mechanisms depending on drug concentration. Taxol alters specific intracellular signal transduction events. It has been reported that Taxol induces the production of cytokines, interleukin-1, and tumor necrosis factor ! (TNF-!) and increases tyrosine phosphorylation of proteins, including mitogen-activated protein kinase. Prolonged exposure of cells to Taxol induces DNA fragmentation, characteristic of apoptotic cell death, and it has been suggested that Raf1 is a mediator of Taxol-induced apoptosis.

A. Paclitaxel Paclitaxel (Taxol, Onxol) is a naturally occurring taxane molecule that inhibits depolymerization of tubulin in the spindle apparatus thus inducing apoptosis in dividing cells. It is FDA approved for salvage therapy in ovarian cancer and in both metastatic and adjuvant setting in breast cancer. It is also used in lung, head and neck and bladder cancers. Figure 7 shows its chemical structure and with its differentiating features from docetaxel marked in red.

B. Docetaxel Docetaxel (Taxotere, Sanofi) is a semisynthetic taxane, from a class of compounds that inhibit the mitotic spindle apparatus by stabilizing tubulin polymers, leading to death of mitotic cells. FDA has approved it for metastatic breast cancer and first and second line treatment for non-small cell lung cancer. However, clinical experience is increasing in ovarian cancer, prostate cancer, stomach cancer and other epithelial neoplasms and it is likely to get approvals for additional indications.

C. Molecular mechanism of taxanes The mechanism of action of taxanes against tumor cells is by alteration of microtubule dynamics, which causes cell-cycle arrest during mitosis. Docetaxel binds to the microtubules with a higher affinity than paclitaxel, and over a broader range of cell-cycle activities. It has also been shown to promote apoptosis via Bcl2 phosphorylation.

Recently, it has been shown that Bcl2 may protect cancer cells from apoptosis induced by a variety of anticancer agents. The precise mechanism of the Bcl2induced multi-drug resistance is unknown. Microtubulestabilizing agents such as paclitaxel and docetaxel have antimitotic and apoptosis-inducing activity. Human leukemic, breast cancer, and prostate cancer cells exposed to paclitaxel express a phosphorylated form of Bcl2 and

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Figure 7. Structure of Paclitaxel and Docetaxel; their differentiating features are marked in red.

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Figure 8. Taxol binding site on mammalian $-tubulin. The location of residues Lys-19, Val-23, Asp-26, His-227, and Phe-270 are indicated and are shown in dark gray. Labels on Taxol (gray) denote the following: I, C3! phenyl ring; II, C3! benzamido phenyl ring; and III, C2 benzoyl phenyl ring. Specific regions of $-tubulin that form the binding pocket are labeled, including !-helices H1, H7, H9, and H10, the $-strands B7-B10, and the B7-H9 M-loop. From "Gupta, Jr. LM, Bode CJ, Georg, GI, Himes RH (2003) Proc. Natl. Acad.

Sci. USA 100: 6394â&#x20AC;&#x201C;6397, Copyright 2003 National Academy of Sciences, U.S.A."

Raf-1 is known as an important intermediate in the transmission of proliferative and developmental signals, connecting upstream tyrosine kinases with downstream serine/threonine kinases. It is not clear whether Raf-1 activation is a consequence of disruption of the normal microtubule cytoskeleton and/or of activating the spindle mitotic checkpoint (Torres and Horwitz, 1998).

Paclitaxel is known to induce a proinflammatory response in macrophages; combination therapy with trastuzumab and paclitaxel for inflammatory local recurrence after breast conserving surgery has been suggested as a treatment of choice (Nomura et al, 2005).

Paclitaxel might have a role in inhibiting angiogenesis and vascularization (Shnyder et al, 2005).

In hormone-refractory prostate cancer, docetaxel has been studied as both a single agent and in combination with estramustine, and in different treatment schedules, with demonstrated efficacy. Two phase III trials have confirmed a survival benefit, making docetaxel the first chemotherapy agent with proven efficacy against prostate cancer (Mackler and Pienta, 2005).

In urothelial cancer, docetaxel has demonstrated activity and has been investigated as a single agent and in combination regimens. A phase III trial comparing docetaxel and cisplatin to methotrexate, vinblastine, doxorubicin, and cisplatin was inferior when evaluating response rates and overall survival. More recent phase II trials combining docetaxel with two additional agents have shown promise, but confirmatory trials are needed (Mackler and Pienta, 2005).

D. Indications of taxanes Paclitaxel is indicated as first-line treatment for advanced ovarian carcinoma in combination with cisplatin; as first-line treatment of Non Small Cell Lung Cancer (NSCLC, stages IIIb and IV) in combination with cisplatin; for the adjuvant treatment of node-positive breast cancer administered sequentially to standard doxorubicin-containing combination; for the treatment of breast cancer after failure of combination chemotherapy for metastatic disease or relapse within 6 months of adjuvant chemotherapy; and for the second-line treatment of AIDS-related Kaposi's sarcoma.

E. Side effects of taxanes The dose limiting effect of paclitaxel is myelosuppression (mostly neutropenia) that can be reduced with shorter infusions of the same dose. Other common side effects are mucositis (especially after longer infusions), peripheral neuropathy (that increases with cumulative dose), acute neuromyopathy (that occurs for several days after infusion and could require opiate analgesics in order to control pain), cardiovascular side effects, including hypertension, hypotension, premature contractions, bradyarrhythmias and hypersensitivity

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Boulikas and Tsogas: Microtubule-targeting anticancer drugs page reactions to the drug including chest pain, dyspnea, urticaria, wheezing, hypotension (that can be reduced by premedication with corticosteroids and H1, H2 histamine receptor blockers). Alopecia is one of the expected side effects, whereas nausea, vomiting, diarrhea, liver toxicity and interstitial pneumonitis are uncommon (Saville et al, 1995; Blum et al, 2006; Langer et al, 2007).

The severe side effects of docetaxel include myelotoxicity, allergic reactions during infusion, diarrhea that can be severe in some patients, nausea and/or vomiting, hair loss occurring in most patients (including the hair on head, underarm hair, pubic hair, eyebrows, and eyelashes), fatigue in about 10% of patients, and muscle pain that is rarely severe in about 20% of the infusions.

Rash occurs commonly but is severe in about 5% of patients. About half of patients feel numbness, tingling, or burning sensations in their hands and feet.

Myelosuppression and alopecia are universal side effects of docetaxel with myelosuppression being the dose limiting effect. Edema and fluid accumulation, including pleural effusions and ascites are common and can be dose limiting. Fluid accumulation can be partially prevented with corticosteroid treatment before and after each cycle of docetaxel. Mild sensory or sensorimotor neuropathy is common. Mucositis and diarrhea are common and usually mild. Hypersensitivity reactions are uncommon and can be prevented through premedication with corticosteroids and antihistamines. Rash and elevated liver function tests are uncommon (Baker et al, 2004; Georgoulias et al, 2005).

Taxanes require pre-medication and may cause important side effects such as febrile neutropenia and neuropathy. Neuropathy is a major adverse effect of microtubule-stabilizing agent-based chemotherapy, with severe peripheral neuropathy (grade 3 or 4) occurring in as many as 30% of patients treated. Neuropathy usually presents as sensory neuropathy and is more common with paclitaxel than docetaxel; it depends on the drug dose per treatment cycle, the schedule of treatment, and the duration of the infusion (reviewed by Lee and Swain, 2006).

(Figure 9). However, mutations in !-tubulin are also linked to resistance to taxanes but not epothilones in vitro (Pusztai, 2007). Resistance against paclitaxel also correlates with an increase in the relative abundance of tubulin isoform !III; the mode of recognition and the mechanism of stabilization of paclitaxel with the type I and III isoforms of !-tubulin are different; no preference for any of the two isoforms can be detected for epothilone A known to bypass paclitaxel resistance (Magnani et al, 2006).

F. Taxane drug resistance The majority of initially responsive breast cancer patients treated with taxanes eventually develop resistance to taxanes (acquired resistance) and a non-negligible percentage of patients are primarily resistant to these agents (de novo resistance). Taxane drug resistance is caused by the drug efflux pump protein, P-glycoprotein. Pglycoprotein, produced by the multidrug resistance-1 gene (mdr-1), is a main mechanism developed by cancer cells to guard against anticancer drugs. Alterations of DNA methylation of the mdr-1 gene promoter are known to be linked to mdr-1 gene expression and are probably related to intracellular S-adenosyl-methionine.

Overexpression of P-glycoprotein is associated with resistance to taxanes, but not ixabepilone, in vitro.

Obviously, different functional groups on the paclitaxel (or docetaxel) molecules are involved in tubulin binding and in interaction with P-glycoprotein; the similarity in molecular structures between taxanes on one hand and epothilones in the other is shown by molecular modeling

Figure 9. Structural similarities between paclitaxel and epothilone B. Paclitaxel structure is shown in grey and epothilone B is superimposed in yellow (A), while in (B) Paclitaxel is the yellow structure and epothilone B is the grey.

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Gene Therapy and Molecular Biology Vol 12, page 323 Preclinical xenograft studies comparing ABI-007 and Taxol showed that both caused tumor regression and prolonged survival in various tumors; the order of sensitivity was lung > breast congruent with ovary > prostate > colon. The LD50 and Maximum Tolerated Dose (MTD) for ABI-007 were 47 and 30 mg/kg/d and for Taxol were 30 and 13.4 mg/kg/d, respectively. At equitoxic dose, the ABI-007-treated groups showed more regressions and prolonged survival supposedly from a higher intratumoral accumulation of ABI-007; finally ABI-007 exhibited enhanced endothelial cell binding and transcytosis compared to Taxol (Desai et al, 2006).

G. Mechanisms of taxane drug resistance One mechanism of resistance to taxanes involves mutations, especially L and V substitutions at proline 220 of !-tubulin. Indeed, expression of tubulin containing the P220L and P220V mutations from expression vectors reduced microtubule assembly, conferred resistance to paclitaxel and epothilone A (microtubule-stabilizing drugs), but increased sensitivity to colcemid and vinblastine (microtubule-destabilizing drugs).

An important aspect of these studies is that different substitutions at the same amino acid residue in !1-tubulin can confer cellular resistance to either microtubulestabilizing or microtubule-destabilizing drugs (Yin et al, 2007). Additional mutations involved in resistance to paclitaxel are the L215, L217, and L228 in the H6/H7 loop region of !1-tubulin as shown in Chinese hamster ovary cells selected in the presence of paclitaxel.

A. Dose-limiting toxicity (DLT) of Abraxane Clinical studies have shown that nab-paclitaxel has almost double the response than paclitaxel formulated as Cremophor EL (Taxol) with an increased time to disease progression and increased survival in second-line patients.

Nab-paclitaxel showed a lower rate of severe neutropenia compared to Taxol. Also the combination of ABI-007 and carboplatin may have significant activity in a variety of tumor types including non-small and small cell lung cancer, ovarian cancer, and breast cancer. However, lifethreatening toxicities with metastatic breast cancer and hepatic insufficiency have been observed (Lee Villano et al, 2006).

In a Phase I study ABI-007 was administered in three different schedules in combination with carboplatin at AUC of 6 on day 1. Myelosuppression was the primary dose limiting toxicity. Responses were seen in melanoma, lung, bladder, esophageal, pancreatic, breast cancer, and cancer of unknown primary among 41 patients. The MTD of ABI-007 was 300 mg/m2 administered on day 1 every 21 days; 100 mg/m2 administered on days 1, 8, and 15 every 28 days; and 125 mg/m2 administered on days 1 and 8 every 21 days (Stinchcombe et al, 2007). In a different Phase I dose-escalating study the dose-limiting toxicity (DLT), which occurred in 3 of 6 patients treated at level 3 (375 mg/m2), consisted of sensory neuropathy (3 patients), stomatitis (2 patients), and superficial keratopathy (2 patients). The MTD was thus determined to be 300 mg/m2 (level 2). Identified features of clinical interest of ABI007, included rapid infusion rate, absence of requirement for steroid premedication, and a high paclitaxel MTD (Ibrahim et al, 2002).

IV. Nab-paclitaxel (ABI-007, Abraxane) Taxane delivery systems through tumor cell surface receptor-targeted delivery mechanisms such as smallmolecule peptides and monoclonal antibodies, as well as those on non-targeted procedures such as liposomes, nanostructures, and natural and synthetic polymers hold promise for improving the toxicity profiles and biodistribution of the drug.

Albumin is emerging as a versatile protein carrier for drug targeting and for improving the pharmacokinetic profile of peptide or protein-based drugs. Nab-paclitaxel (ABI-007, Abraxane) is a novel albumin-bound (nab) paclitaxel formulated into 130-nm particles. This differs from the more conventional formulation of Taxol, which uses cremophor (castor oil) to increase the solubility of paclitaxel and is responsible for side effects, especially neutropenia and peripheral neuropathy. Abraxane utilizes the natural properties of albumin to reversibly bind paclitaxel, transport it across the endothelial cell and concentrate it in tumors. The proposed mechanism involves an endothelial cell-surface albumin receptor (gp60) and an albumin-binding protein expressed by tumor cells and secreted into the tumor interstitium (secreted protein, acidic and rich in cysteine, SPARC). Thus, glycoprotein 60-mediated endothelial cell transcytosis of the albumin nanoparticles and tumor accumulation by binding to SPARC enhances the therapeutic efficacy of ABI-007 compared to the free drug. The albumin receptormediated paclitaxel-transport mechanism is analogous to the opening of a 'trapdoor' on the endothelial cell wall within blood vessels. This facilitates the passage of ABI 007 from the bloodstream via the blood vessels to the underlying tumor tissue (reviewed by Moreno-Aspitia and Perez, 2005; Gradishar, 2006).

Studies in rats have shown that ABI-007 differs from paclitaxel formulated as Taxol, with a higher plasma clearance and a larger volume of distribution. The same study also showed that fecal excretion was the main elimination pathway with both formulations (Sparreboom et al, 2005).

B. Maximum tolerated dose (MTD) of Abraxane In a Phase I study the MTDs for heavily and lightly pretreated patients were 100 and 150 mg/m2, respectively; and the dose-limiting toxicities were grade 4 neutropenia and grade 3 peripheral neuropathy, respectively (Nyman et al, 2005).

An interim analysis from a more recent randomized Phase II trial suggested that weekly nab-paclitaxel was more effective and safer than either 3-weekly nabpaclitaxel or 3-weekly docetaxel. The superior efficacy of nab-paclitaxel was presumably due to the improved safety profile, which allows for the administration of higher doses, a greater proportion of which actually reaches the tumor (reviewed by Henderson and Bhatia, 2007).

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Boulikas and Tsogas: Microtubule-targeting anticancer drugs page Additional studies include a phase II trial of ABI 007 in metastatic breast cancer patients who have failed taxane therapy evaluating a weekly rather than 3-weekly regimen and a multicentre phase II trial in patients with metastatic melanoma to evaluate both chemotherapy-naive patients (at a dose of 150 mg/m2 administered weekly) and to pretreated patients (at a dose of 100 mg/m2 administered weekly). ABI 007 is also being evaluated for the treatment of NSCLC, ovarian and cervical cancers.

American Pharmaceutical Partners (APP) secured exclusive North American marketing and manufacturing rights to ABI 007 in November 2001 and formed Abraxis Oncology for marketing purposes; APP is the owner of the US patent No. 6,506,405, which has 89 claims covering compositions of matter and unit dosage forms and patent No. 5,780,653 which covers three next-generation taxane anticancer compounds. In addition, the patent covers methods of use without the requirement for pretreatment with steroid therapy or growth factor support. The US FDA granted fast-track status to ABI 007 for metastatic breast cancer in January 2003. In September 2003, APP and American BioScience jointly announced positive interim results from the trial, which shows that the primary efficacy objective had been exceeded. Enrollment was completed in December 2002 with 460 first- and secondline metastatic breast cancer patients enrolled. A Data Monitoring Committee concluded in October 2002 that a sample-size adjustment of the phase III trial was not required and that the study could be continued to completion.

C. Clinical development of Abraxane A multicenter phase II study was designed to evaluate the efficacy and safety of Abraxane 260 mg/m2 without premedication every 3 weeks in NSCLC patients; ORR was 16%; the disease control rate (ORR plus stable disease) was 49% and the 1-year survival was 45%. Side effects included neuropathy, fatigue but no severe hypersensitivity reactions and no grade 4 treatment-related toxicity (Green et al, 2006).

Paclitaxel albumin-bound particles improved outcomes when compared against single agent cremophorbased paclitaxel; addition of bevacizumab (10 mg/kg), gemcitabine (1000 mg/m2) or both agents to abraxane (100mg/m2) also improved outcomes in clinical trials with manageable peripheral neuropathy and thrombocytopenia (Lobo et al, 2007).

A multicenter phase II study in MBC on 63 women at the M.D. Anderson Cancer Center, Houston was the prelude of the pivotal Phase III trial. ABI-007 at 300 mg/m2 was given to previously-treated or chemonaive patients. The overall response rates was 48% but for the group of patients who received ABI-007 as first-line treatment, the response rate was 64% and for the group of patients who received ABI-007 as second- or third-line treatment the response rate was 21%. Toxicities observed were typical of paclitaxel and included grade 4 neutropenia (24%), grade 3 sensory neuropathy (11%), and grade 4 febrile neutropenia (5%). Median time to disease progression was 26.6 weeks, and median survival was 63.6 weeks (Ibrahim et al, 2005).

In a randomized trial that formed the basis of its regulatory approval in the USA, 3-weekly nab-paclitaxel induced a higher response rate and longer time to progression than Taxol in patients with metastatic breast cancer. Except for grade 3 sensory neuropathy, nabpaclitaxel was also safer. The pivotal phase III study was performed to confirm preclinical studies demonstrating superior efficacy and reduced toxicity of ABI-007 compared with standard paclitaxel. ABI-007 at 260 mg/m2 was given intravenously without corticosteroid premedication compared to 175 mg/m2 Taxol with premedication both in 3-week cycles and demonstrated significantly higher response rates compared with standard paclitaxel (33% versus 19%, respectively) and significantly longer time to tumor progression (23.0 v 16.9 weeks, respectively). The incidence of grade 4 neutropenia was significantly lower for ABI-007 compared with Taxol (9% v 22%, respectively). Grade 3 sensory neuropathy was more common in the ABI-007 arm than in the standard paclitaxel arm (10% v 2%, respectively) (Gradishar et al, 2005).

D. Targeting to tumors in animals Tumor-homing peptides were used to target abraxane to tumors in mice. The targeting was accomplished with two peptides, CREKA and LyP-1 (CGNKRTRGC). The CREKA pentapeptide binds to clotted plasma proteins and homes to tumors because interstitial tissue of tumors and the vessel walls contain clotted plasma proteins, whereas the vessels in normal tissues do not. Fluorescein (FAM)labeled CREKA-abraxane, injected intravenously into mice bearing human cancer xenografts, accumulated in tumor blood vessels, forming aggregates that contained red blood cells and fibrin. FAM-LyP-1-abraxane colocalized with extravascular islands expressing its receptor, p32. Untargeted FAM-abraxane was detected in the form of a faint meshwork in tumor interstitium. LyP-1abraxane produced a statistically highly significant inhibition of tumor growth compared with untargeted abraxane in the xenografts (Karmali et al, 2008).

V. Epothilones Epothilones are 16-membered ring macrolides with antimicrotubule activity that have a mechanism of action similar enough to the taxanes to retain their broad spectrum of activity, but different enough to escape the multidrug resistance caused by P-glycoprotein. These properties are especially promising for patients with metastatic breast cancer who have run out of therapeutic options as a result of multidrug resistance. Due to improved water solubility, cremophors (solubilizing agents used in paclitaxel which can affect cardiac function and cause severe hypersensitivity) are no longer needed in the formulation of epothilones.

Two major compounds, epothilone A and epothilone B, were originally identified as secondary metabolites produced by the soil-dwelling myxobacterium Sorangium cellulosum endowed with selective antifungal activity and strong cytotoxic activity against cancer cell lines (reviewed by Reichenbach and Hรถfle, 2008). Optimization of the production of extracellular epothilone B using 3% 324

Gene Therapy and Molecular Biology Vol 12, page 325 calcium alginate carrier for immobilization of Sorangium cellulosum has been described able to produce 5.03 mg/l/day (Park et al, 2007). Additional anticancer substances appear to be present in Sorangium cellulosum strains isolated in China (Guo et al, 2007). Epothilones are potential anticancer drugs that stabilize microtubules by binding to tubulin in a manner similar to paclitaxel.

Cytochrome P450epoK (P450epoK), a heme containing monooxygenase involved in epothilone biosynthesis in the myxobacterium Sorangium cellulosum, catalyzes the epoxidation of epothilones C and D into epothilones A and B, respectively.

Hodgkin's lymphoma in phase II studies. Response rates in taxane-refractory metastatic breast cancer are relatively modest; however, ixabepilone and patupilone have shown promising efficacy in hormone-refractory metastatic prostate cancer and in taxane-refractory ovarian cancer (reviewed by Larkin and Kaye, 2006).

C. Mechanism of action of epothilones Like taxol, epothilone B binds to the !$-tubulin heterodimer subunit. Once bound, the rate of !$-tubulin dissociation decreases, thus stabilizing the microtubules.

Furthermore, epothilone B has also been shown to induce tubulin polymerization into microtubules without the presence of GTP. This is caused by formation of microtubule bundles throughout the cytoplasm. Finally, epothilone B also causes cell cycle arrest at the G2/M transition phase, thus leading to cytotoxicity and eventually cell apoptosis (Balog et al, 1996).

Epothilone B and D enhanced the constitutional activation of nuclear factor-#B (NF-#B) via I#B degradation through I#B kinase (IKK! and IKK!) activation, and this resulted in p50 and p65 translocation to the nucleus in SW620 colon cancer cells. Moreover, epothilone B and D increased the expressions Bax, p53, caspase-3, but reduced Bcl-2 expression. Cells treated with sodium salicylate, an IKK inhibitor, did not show epothilone-induced cell growth inhibition or p50 translocation. These studies have unraveled additional mechanisms of epothilone-induced apoptosis in a tubulin polymerization-independent manner (Lee et al, 2007).

A. Epothilone drug discovery Epothilones are anticancer agents with a taxane-like mechanism of action that have demonstrated activity in taxane-resistant tumors. Marine invertebrate animals such as sponges, gorgonians, tunicates and bryozoans are under intense investigation as sources of medicinal natural products.

Non-taxane microtubule-stabilizers of diverse chemical structures, including the epothilones and discodermolide have been advanced in chemical synthesis and been promoted to clinical trials (reviewed by Cardoso et al, 2008). Non-taxane microtubule-stabilizers of diverse chemical structures show promising preclinical activities and several are progressing through clinical trials (Mooberry, 2007).

The structural diversity of the epothilone group of clinical compounds is rather limited, as their structures show little divergence from the original natural product leads. A series of epothilone-derived macrolactones were elaborated to discover improved versions some of which had potent antiproliferative activities, promoted tubulin polymerization and induced mitotic arrest; changes were at the natural epoxide geometry from cis to trans, the incorporation of a conformationally constrained side chain, the removal of the C3-hydroxyl group, and the replacement of C12 with nitrogen. Interesting from many points of view appeared to be the 12-aza-epothilone ("azathilone" 40) especially because it lies outside of the general scope of Nature's biosynthetic machinery for polyketide synthesis but nevertheless retains most of the overall structural characteristics of a true natural product (Feyen et al, 2008).

D. Epothilone B (patupilone; EPO960) Patupilone (Figure 10) is a novel tubulinpolymerizing agent with activity against paclitaxelresistant cell lines. Patients with refractory solid tumors received fixed doses of gemcitabine (1,000 or 750 mg/m2) along with escalating doses of patupilone (1.5-3 mg/m2) on days 1 and 8 of a 21-day cycle. The recommended phase II dose was gemcitabine 750 mg/m2 and patupilone 1.5 mg/m2 on days 1 and 8 of a 21-day cycle. DLTs were grade 3 asthenia and grade 3 dehydration but also asthenia and persistent nausea were observed (Schelman et al, 2008).

The principal mechanism of the epothilone class is inhibition of microtubule function (Goodin et al, 2004).

Microtubules are essential to cell division, and epothilones therefore stop cells from properly dividing. Epothilone B possesses the same biological effects as taxol both in vitro and in cultured cells. This is due to the fact that they share the same binding site, as well as binding affinity to the microtubule. Epothilone B binds to the !$-tubulin heterodimer subunit. Once bound, the rate of !$-tubulin dissociation decreases, thus stabilizing the microtubules.

Furthermore, epothilone B has also been shown to induce tubulin polymerization into microtubules without the presence of GTP. This is caused by formation of microtubule bundles throughout the cytoplasm. Finally, epothilone B also causes cell cycle arrest at the G2/M transition phase, thus leading to cytotoxicity and eventually cell apoptosis (Balog et al, 1996). Epothilone B has similar biological properties to Epothilone A.

B. Epothilones under clinical evaluation At least six epothilones are in clinical trials for cancer treatment. Molecules under phase I or II clinical evaluation include epothilone B (patupilone; EPO960), epothilone D (KOS-862) and their second-generation (ixabepilone, BMS-310705, KOS-1584) and thirdgeneration (ZK-EPO, ABJ-879) derivatives. Although similar in chemical structure, the epothilones demonstrated a striking difference in toxicity profile in phase I studies.

Diarrhea was the dose-limiting toxicity (DLT) associated with patupilone, whereas neurotoxicity and neutropenia are the DLTs most commonly encountered with other epothilones (reviewed by Fumoleau et al, 2007).

Epothilones have demonstrated activity in lung, ovarian, breast, prostate, and renal carcinomas and in non325

Boulikas and Tsogas: Microtubule-targeting anticancer drugs page H3C

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Figure 10. Structures of Epothilone B, Ixabepilone, Sagopilone, Epothilone D and KOS-1584. Structural differences are marked red.

However, Epothilone B is 10-fold more potent than Epothilone A against P-glycoprotein-expressing multidrug resistant (MDR) cells. (-)-Epothilone B is similar to paclitaxel in binding displacement, and a substitution for paclitaxel in dependent cell growth. Epothilone B causes cell cycle arrest (IC50=3.5 nM).

Epothilone B shares the same or an overlapping binding site with paclitaxel and has been reported to have the same effects as paclitaxel on purified microtubules in vitro and on mitotic spindle structure and function in cultured cells. Epothilone B and paclitaxel alter the same microtubule dynamic parameters and to a similar extent.

At the IC50 for mitotic arrest, dynamicity was reduced by 54% by paclitaxel compared with 62% for epothilone B. In addition, no anaphase or telephone figures were observed at the IC50 for both drugs, and in 65% of the cells treated with paclitaxel, the microtubules were completely stabilized compared with 80% for epothilone B. Thus, the effects of epothilone B on microtubule dynamics are remarkably similar to those of paclitaxel, suggesting that both drugs work by the same mechanism to induce mitotic block. Epothilone B overcomes P-glycoprotein-mediated paclitaxel resistance and is more water-soluble than paclitaxel (Klamath and Jordan, 2003).

Epothilone B is a 16-membered polyketide macrolactone with a methylthiazole group connected to the macrocycle by an olefinic bond (Molnรกr et al, 2000).

Cytochrome P450epoK (P450epoK), a heme containing monooxygenase involved in epothilone biosynthesis in the myxobacterium Sorangium cellulosum, catalyzes the epoxidation of epothilones C and D into epothilones A and B, respectively. The epothilones are positioned with the macrolide ring roughly perpendicular to the heme plane and I helix, and the thiazole moiety provides key interactions that very likely are critical in determining substrate specificity. Interestingly, there are strong

parallels between the epothilone/P450epoK paclitaxel/tubulin interactions (Nagano et al, 2003).

and

E. Ixabepilone (BMS-247550) Ixabepilone (BMS-247550, azaepothilone B) is a semi-synthetic, microtubule stabilizing epothilone B analogue developed by Bristol-Myers Squibb (Stachel et al, 2000), which is more potent than taxanes and has displayed activity in taxane-resistant patients. Like all epothilones, Ixabepilone binds to tubulin and promotes tubulin polymerization and microtubule stabilization, thereby arresting cells in the G2/M phase of the cell cycle and inducing tumor cell apoptosis.

Ixabepilone demonstrated antineoplastic activity against taxane-resistant cell lines. FDA approved ixabepilone in 2007 (IXEMPRA, Bristol) for the treatment of aggressive metastatic or locally advanced breast cancer based on two multicenter trials on 878 patients using IXEMPRA either as a monotherapy or in combination with capecitabine. A single-arm monotherapy Phase II enrolled 126 patients with metastatic or locally advanced breast cancer resistant to three prior therapies (an anthracycline, a taxane and capecitabine). The primary endpoint was objective response rate and gave a partial response of 12.4% in 113 response-evaluable patients.

Treatment-related non-hematological adverse events (greater than or equal to 20%) included: peripheral sensory neuropathy 62% (Grade 3/4: 14%), fatigue/asthenia 56% (Grade 3/4: 13%), myalgia/arthralgia 49% (Grade 3/4: 8%), alopecia 48% (Grade 3/4: 0%), nausea 42% (Grade 3/4: 2%), stomatitis/mucositis 29% (Grade 3/4: 6%), vomiting 29% (Grade 3/4: 1%), diarrhea 22% (Grade 3/4: 1%), and musculoskeletal pain 20% (Grade 3/4: 3%).

Treatment-related hematological adverse events (greater than or equal to 20%) included: neutropenia (Grade 3/4: 54%) and leukopenia (Grade 3/4: 49%).

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Gene Therapy and Molecular Biology Vol 12, page 327 A randomized Phase III trial evaluated the efficacy and safety of IXEMPRA in combination with capecitabine in comparison with capecitabine as monotherapy. This trial included 752 patients who were previously treated with anthracyclines and taxanes, and whose tumors had demonstrated prior resistance to these therapies.

Evaluation of the primary endpoint demonstrated that IXEMPRA in combination with capecitabine resulted in a statistically significant improvement in progression-free survival compared to capecitabine monotherapy - median 5.7 vs. 4.1 months. Adverse events included neutropenia (Grade 3/4: 68%), leukopenia (Grade 3/4: 57%), peripheral neuropathy 65% (Grade 3/4: 21%), palmarplantar erythrodysesthesia (hand-foot) syndrome 64% (Grade 3/4: 18%), fatigue/asthenia 60% (Grade 3/4: 16%), and others.

A randomized phase II trial in 92 chemotherapynaive patients with progressive castrate metastatic prostate cancer treated with ixabepilone either as a single agent or in combination with estramustine phosphate reported a PSA RR of 48% in the ixabepilone arm and 69% in the combination arm, with an acceptable safety profile (Galsky et al, 2005). The predominant toxicities in the patients treated with ixabepilone alone or in combination with estramustine phosphate included grade 3/4 neutropenia (22% vs. 29%, respectively), grade 3 neuropathy (13% vs. 7%), and grade 3 fatigue (9% vs.

9%). A study of single-agent ixabepilone (SWOG S0111) reported a PSA RR of 33% in 42 evaluable patients with HRPC (Hussain et al, 2005). Although there were no confirmed objective responses in the 20 patients with measurable disease, 1 patient (5%) achieved an unconfirmed complete response, and 2 patients (10%) achieved an unconfirmed PR. Estimated median PFS was 6 months (95% CI, 4-8 months), and median survival was 18 months (95% CI, 13-24 months). A phase II trial conducted by the Eastern Cooperative Oncology Group (E3803) is evaluating the efficacy of ixabepilone in patients with no prior chemotherapy as well as in patients who have received % 2 prior regimens, and initial findings from a noncomparative phase II trial evaluating ixabepilone and mitoxantrone/prednisone in patients with taxane-refractory pretreated Hormone Refractory Prostate Cancer (HRPC) were reported recently (Small et al, 2006).

Eligible patients were randomized to second-line treatment with ixabepilone or mitoxantrone/prednisone, and, upon progression, patients were allowed to cross over to the alternate regimen for third-line treatment. Clinical outcomes of patients with taxane-resistant HRPC who were treated with subsequent chemotherapy were also reported recently. A total of 82 evaluable patients were treated with ixabepilone or mitoxantrone/prednisone.

Median OS from protocol entry was 12.5 months for the patients in the ixabepilone arm and 13.0 months for those in the mitoxantrone/prednisone arm. Seventeen percent of the patients in the ixabepilone group and 20% of those in the mitoxantrone/prednisone group achieved a second-line PSA decline (& 50%). One of the 23 evaluable patients receiving second-line ixabepilone and 1 of the 20 evaluable patients receiving second-line mitoxantrone/prednisone achieved a PR. Neutropenia was

the most frequent grade 3/4 adverse event associated with second line therapy (41% in the ixabepilone arm, 56% in the mitoxantrone/prednisone arm). Third-line crossover therapy occurred in 39% of the patients treated with ixabepilone and 68% of those treated with mitoxantrone/prednisone. Third-line therapy yielded a PSA decline (& 50%) in 3 of the 25 patients (12%) treated with ixabepilone and 4 of the 13 patients (31%) treated with mitoxantrone/prednisone.

Vascular smooth muscle cells (VSMCs) form the lining of arterial walls and their abnormal proliferation is linked with atherosclerosis and restenosis after angioplasty. Epothilone B has been used in preventing postangioplasty restenosis. Epothilone B treatment of VSMCs caused a significant decrease in the level of cyclin-dependent protein kinase (CDK) 2 and downregulated the phosphorylation of retinoblastoma, which plays a critical role in cell cycle regulation. Furthermore, levels of p27, an inhibitor of cyclin E/CDK2 complex, were significantly increased in VSMCs treated with epothilone B, indicating that this might be a major molecular mechanism for the inhibitory effects of epothilone B on the proliferation and cell cycle of VSMCs (Lim et al, 2007).

The excretory pathways of ixabepilone were studied in Eight patients with advanced cancer who received 70 mg, 80 nCi of [14C]ixabepilone over 3 h; fecal excretion was 52.2% and urinary excretion was 25.1% (Beumer et al, 2007). Neuropathy has led to the uneven and slower than expected clinical development of ixabepilone. Singleagent ixabepilone also demonstrated robust antitumor activity in women with metastatic breast cancer that was resistant to taxanes, anthracyclines and capecitabine in phase II trials (reviewed by Pronzato, 2008).

A phase II study of ixabepilone monotherapy in metastatic renal-cell carcinoma (RCC) administered at a dose of 40 mg/m2 every 21 days did not give objective responses in the first 12 evaluable patients, but six patients showed stable disease for more than 18 weeks on therapy ensuring advancement in Phase III against RCC. Grade 3 adverse events included lymphopenia, neutropenia, leukopenia, diarrhea, and infection. Common grade 2 toxicities included alopecia, fatigue and anemia (Posadas et al, 2007).

F. Epothilone D (KOS-862) Epothilone D (KOS-862; 12,13-desoxyepothilone B) was also isolated from the myxobacterium Sorangium cellulosum. The drug was shown to reduce neointimal hyperplasia after in vivo rat carotid artery injury; from the significantly decrease in the level of CDK2 protein and inhibition of the phosphorylation of Rb, it was concluded that the major molecular mechanism of Epothilone D may involve regulation of the cell cycle G1-checkpoint proteins (Kim et al, 2007).

Epothilone D is capable of causing mitotic arrest by stabilizing tubulin polymerization. Epothilone D has demonstrated in vitro cytotoxic activity in a panel of human cell lines, equipotent to that of paclitaxel.

Epothilone D is more potent than paclitaxel in pglycoprotein overexpressing cell lines that demonstrate

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Boulikas and Tsogas: Microtubule-targeting anticancer drugs page multiple drug resistant activities. Epothilone D has also been shown to be active in the androgen-independent PC-3 human prostate cancer cells with IC50 of 0.0128 #M. In vivo, Epothilone D has shown significant antitumor activity in a range of xenograft models, including those that are resistant to paclitaxel. The dose limiting toxicity for epothilone D in phase I studies has been neurologic including both central and peripheral neurologic toxicity.

Approximately 75% of patients enrolled in phase I studies experienced at least one neurologic toxicity (Beer et al, 2007). Epothilone D is being tested in combination with trastuzumab (Herceptin) in patients with HER-2 metastatic breast cancer. Adverse events were mostly Grade 1 or 2, with three Grade 3 incidents of sensory neurological toxicities

described using a convergent synthetic approach; the aim of this synthesis was the restriction of the mobility of the aromatic side chain. The C1-C8 sector remained unchanged, in view of its seemingly crucial role in biological activity. A single methylene bridge was introduced between C14 and C17 (Figure 11). The resulting cyclopentene moiety, which incorporated the C16-C17 double bond, was designed to rigidify the side chain while still permitting sufficient mobility of the pyridine ring to allow for the preferred N-atom orientation for a hydrogen bonding interaction with the receptor.

These epothilone analogues showed strong and selective growth inhibitory activity against leukemia cell lines (Alhamadsheh et al, 2008).

I. Sagopilone G. KOS-1584

The process of sagopilone development at Bayer Schering Pharma is an interesting story. One day, an external researcher offered the company a substance he had discovered, which he considered as a possible anticancer medication but the offer was rejected. By the time interest developed a rival company had already secured the rights to the substance. Bayer Schering Pharma now owns sagopilone, an epothilone analogue, with a structure somewhat different to the naturally occurring one; chemical ingenuity was used to modify the structure deriving at 450 compounds and broadening the therapeutic window of natural epothilones. Approximately half of the compounds synthesized, differed only slightly from the prototype epothilone, were promising with respect to toxicity, therapeutic efficacy and development of resistance after treatment of cells in culture and ease of chemical synthesis. A total of 39 chemical steps were used to produce three initial subunits of Sagopilone, which were then used to construct the finished molecule. How could such a complex process ever be implemented costeffectively on a large scale? Converting one step in the chemical process from the laboratory to production-scale (up scaling), normally takes a month and for the 39 steps of sagopilone synthesis mere up scaling would take more than three years. Acceleration of this process resulted in the production of 36 grams of the substance in six months, sufficient for the treatment of approximately 200 patients whereas further improvements and up scaling took place.

Bayer is now the only company with a fully synthetic epothilone, sagopilone, in advanced clinical development.

KOS-1584 (9,10-didehydroepothilone D) along with KOS-862 (Epothilone D) are the most advanced epothilone drug candidates of Kosan Biosciences. KOS1584 is a second-generation compound with increased potency, favorable tissue distribution, and ease of formulation. Kosan is developing its epothilone compounds in collaboration with Roche.

KOS-1584 has demonstrated in vitro cytotoxicity, more potent or equipotent to that of paclitaxel in a panel of human cell lines. KOS-1584 has shown significant antitumor activity in a range of xenograft models, including non-small cell lung cancer models resistant to paclitaxel and those expressing multidrug resistance. A long elimination half-life was seen in Phase I trials. KOS1584 has demonstrated antitumor activity and favorable tolerability in Phase 1 trials in patients with solid tumors, including substantial tumor shrinkage measured by objective responses in non-small cell lung, ovarian and pancreatic cancers, as well as durable stable disease in many additional tumors.

In April 2008, Kosan initiated a Phase 2 trial of epothilone KOS-1584 in patients with non-small cell lung cancer who have previously received only one prior chemotherapy regimen. The primary endpoint of the Phase 2 trial is objective response rate. KOS-1584 will be administered via a 3-hour intravenous infusion weekly for two weeks out of every three weeks at a dose of 25 mg/m2.

H. Conformationally restrained epothilones Stereoselective total syntheses of two novel conformationally restrained epothilone analogues has been

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Figure 11. Structures of conformationally restrained epothilone analogues.

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Gene Therapy and Molecular Biology Vol 12, page 329 The effectiveness of sagopilone, the first fully synthetic third generation epothilone in clinical development, against paclitaxel in a breast cancer bone metastasis model was evaluated in a recent study. The therapeutic effect of sagopilone and paclitaxel on tumorinduced osteolysis and tumor burden in athymic nude mice inoculated intracardially with MDA-MB-231(SA)/luc human breast cancer cells was investigated. On day 12 after tumor cell inoculation, animals were randomized into treatment groups according to the lesion size as measured by radiography. A single dose of sagopilone was administered on day 13 (10 mg/ kg, i.v.). Paclitaxel was given once daily on days 13-17 (9 mg/ kg, i.p.). At sacrifice (day 23), bone lesions were measured using radiography and micro-CT. Tumor cell dissemination was detected by bioluminescence imaging and histomorphometry. The effect of compounds on bone resorption was determined by measuring Tartrate-resistant acid phosphatase 5b (TRACP5b) in serum and by counting the number of osteoclasts on tumor-bone interface by histomorphometry. Radiographic analysis revealed that further tumor-induced bone destruction was merely reduced by paclitaxel, whereas sagopilone completely

prevented it. Sagopilone-treated animals had also higher bone volume compared to other groups as measured by micro-CT. A marked effect of sagopilone on tumor growth in bone was observed as reduced bioluminescence signal intensity in vivo.

This was confirmed by histomorphometry in H&E-stained bone sections.

Paclitaxel had no significant effect on tumor growth in bone. Sagopilone had significantly better effect on reducing bone destruction and tumor burden when compared to paclitaxel in a mouse model of established breast cancer bone metastasis (Strube et al, 2008).

J. Discodermolide and analogues Discodermolide (Figure 12) stabilizes microtubules and blocks cells at the G2/M phase of the cell cycle in a manner similar to that of Taxol. Non-taxane microtubulestabilizers including the epothilones and discodermolide, are progressing through clinical trials. An advanced synthesis for discodermolide was based on the readily available fermentation product oleandomycin (Parker and Wang, 2007).

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Figure 12. Structures of discodermolide, C19-[4-(4-3H-benzoyl-phenyl)-carbamate]-discodermolide discodermolide analogue. Structural differences are marked in red.

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coumarin-derived

Boulikas and Tsogas: Microtubule-targeting anticancer drugs page Discodermolide has been shown to inhibit the proliferation of human cells by arresting the cell cycle in G2/M phase.

Discodermolide hyperstabilized microtubules, an event especially prevalent during cell division (Day et al, 1996). Hyperstabilization of the mitotic spindle causes cell cycle arrest and cell death by apoptosis. Over a variety of cell lines, activity has been measured at IC50 = 3-80 nM. Discodermolide competed with paclitaxel for microtubule binding, but with higher affinity and was also effective in paclitaxel- and epothilone-resistant cancer cells (Jordan, 2002). It has been reported that Discodermolide-treated breast carcinoma cells displayed spectacular rearrangement of the microtubule cytoskeleton, including extensive microtubule bundling. Microtubule rearrangement that occurred with 10 nM discodermolide required 1 #M Taxol. Discodermolide had equally impressive effects on tubulin assembly in vitro. Near-total polymerization occurred at 0 째C with tubulin plus microtubule-associated proteins (MAPs) under conditions in which Taxol at an identical concentration was inactive. Without MAPs and/or without GTP, tubulin assembly was also more vigorous with discodermolide than with Taxol under every reaction condition examined. Discodermolide-induced polymer differed from Taxol- induced polymer in that it was completely stable at 0 째C in the presence of high concentrations of Ca2+. In a quantitative assay designed to select for agents more effective than Taxol in inducing assembly, discodermolide had an EC50 value of 3.2 #M versus 23 #M for Taxol (Day et al, 1996; Amos et al, 2003). In a recent comparative study A549 human lung carcinoma cells were treated with discodermolide at concentrations higher than 8nM, accelerated cell aging was observed by a functional $-galactosidase activity at pH=6. When the cells were treated with IC50 concentrations of doxorubicin, Taxol and discodermolide, only the latter two resulted in aberrant mitosis. However only discodermolide produced an aging associated $galactosidase activity (Horwitz et al, 2005).

Coumarin-derived discodermolide analogues (Figure 12) possessing equivalent antiproliferative activity to the natural product have been described; the complete C-1 to C-7 fragment was replaced with a coumarin moiety in these compounds (Shaw et al, 2007). Photoaffinity-labeled discodermolide analogues have been used to investigate their binding site in tubulin; all promoted microtubule polymerization in the absence of GTP. The analogue, C19[4-(4-3H-benzoyl-phenyl)-carbamate] -discodermolide (Figure 12) had the highest extent of photoincorporation, it was more cytotoxic than discodermolide, could displace [3H]Taxol from microtubules, and bound amino acid residues 355-359, in !-tubulin, which is in close proximity to the Taxol binding site (Xia et al, 2006).

intravenously (IV). After injection, they are eventually metabolized by the liver and excreted. They work in a cellcycle specific manner, halting mitosis of affected cells and causing cell death. The mechanism of action involves binding to the tubulin monomers and keeping the microtubules (spindle fibers) from forming. These alkaloids also seem to interfere with cells' ability to synthesize DNA and RNA. Although the plant has medical uses, it can produce many serious side effects if smoked or ingested.

There are four major vinca alkaloids in clinical use: Vinblastine, vinorelbine, vincristine and vindesine.

A. Vinblastine Vinblastine (Velban, Velsar), a vinca alkaloid acts as an inhibitor of tubulin polymerization and mitosis. This contrasts the stabilization of tubulin polymers by taxanes.

It also seems to exert its anticancer properties by interfering with glutamic acid metabolism (specifically, the pathways leading from glutamic acid to the Krebs cycle and to urea formation). Vinblastine treatment suppresses angiogenesis (Albertsson et al, 2008).

Vinblastine (Figure 13), is approved by FDA for multiple hematologic and solid tumors. It is most often used in Hodgkin's disease, non-Hodgkin's lymphoma, breast cancer, and germ cell tumors. Because it is a vesicant, extravasation precautions are required during administration.

The major adverse effect of vinblastine is hematologic toxicity which occurs much more frequently than with vincristine therapy.

Leukopenia (granulocytopenia) occurs most commonly and is usually the dose-limiting factor in vinblastine therapy. Other side effects include nausea, vomiting and constipation, dyspnea, chest or tumor pain, wheezing and fever during administration. Some rare cases of syndrome of inappropriate antidiuretic hormone secretion as well as angina pectoris have been reported (Gobbi et al, 2005; Connors, 2005).

Vinblastine induced an accumulation of the G2/M cells with the appearance of aneugenic micronuclei during monocyte-macrophage differentiation induced in a monocytic cell line by phorbol 12-myristate 13-acetate (PMA). Actinomycin D on the contrary, induced under similar conditions a drastic reduction of the G2/M cells (Spano et. al, 2007). Apoptosis is not a major mechanism of cell death induced by etoposide, vinblastine and estramustine in prostate cell lines and appeared to be independent of p53 status and bax/bcl-2 expression (Serafin and Bohm, 2005).

1. Mechanisms of vinblastine Vinblastine is a microtubule-depolymerizing drug.

The X-ray structure of vinblastine bound to tubulin in a complex with the RB3 protein stathmin-like domain (RB3SLD) showed that vinblastine introduces a wedge at the interface of two tubulin molecules and thus interferes with tubulin assembly; furthermore, EM studies showed that vinblastine induced tubulin self-association into spiral aggregates at the expense of microtubule growth in a

VI. Vinca alkaloids The Vinca alkaloids are a subset of drugs that are derived from the periwinkle plant, Catharanthus roseus (also Vinca rosea, Lochnera rosea, and Ammocallis rosea).

While it has been historically used to treat numerous diseases, it has most recently been employed for its anticancer properties. All vinca alkaloids are administered 330

Gene Therapy and Molecular Biology Vol 12, page 331 reaction that appears to be regulated by the C-terminus of $-tubulin and is enhanced by GDP and GTP. Vinblastine also arrests the cell cycle in G2/M-phase by blocking mitotic spindle formation. Triggers Raf-1 activation, phosphorylation of bcl-2-family proteins, induction of p53 expression, and apoptosis in several tumor cell lines (Rai and Wolff, 1998). Vinblastine and the amino-terminal part of RB3-SLD binding sites share a hydrophobic groove on the alpha-tubulin surface that is located at an intermolecular contact in microtubules. Drugs designed to perturb microtubule dynamics by interfacial interference at this site of !-tubulin, can be an attractive anticancer target (Gigant et al, 2005).

Efflux of the P-glycoprotein substrate vinblastine sulfate through Caco-2 cell monolayers was reduced by polyoxyethylene 40 stearate (PS40) thus enhancing the antitumor activity of vinblastine (Luo et al, 2007).

2. Regimens containing vinblastine Advanced urothelial cancer is treated with conventional frontline chemotherapy with gemcitabine and cisplatin; however, traditional or dose-dense methotrexate, vinblastine, doxorubicin and cisplatin regimens are also in current use (Sonpavde et al, 2008).

3. Preclinical regimens containing vinblastine A significant synergistic effect of vinblastine and HSV-Tk/GCV "suicide" gene therapy mediated by human serum albumin (HSA)-associated lipoplexes has been found in cell cultures (Faneca et al, 2008).

A novel way of diminishing cellular resistance to vinblastine has been suggested: Alterations in DNA methylation of the mdr-1 gene promoter are known to be linked to mdr-1 gene expression and related to intracellular S-adenosyl-methionine; cobalamin, a cofactor of methionine-synthase, downregulates mdr-1 gene expression, as well as P-glycoprotein expression and function, and significantly increases cytotoxicity of vinblastine (Marguerite et al, 2007).

Tubulin, the major protein of microtubules, is posttranslationally modified by palmitoylation; this modification is inhibited in vitro by stoichiometric levels of vinblastine; a low, clinically relevant dose of vinblastine, inhibited palmitoylation of tubulin in human leukemic lymphocytes, microtubules were disassembled and cells became apoptotic (Caron and Herwood, 2007).

4. Reactive oxygen species (ROS), vinblastine and apoptosis Reactive oxygen species (ROS), such as superoxide anion radicals (O2-) and hydrogen peroxide (H2O2) are potentially harmful by-products of normal cellular metabolism; ROS is generated by all aerobic organisms and it seems to be indispensable for signal transduction pathways. Overproduction of reactive oxygen species initiate lethal chain reactions involving oxidation and damage to cellular structures, that are crucial for integrity and survival.

OH N

C2H5

N

C2H5 N N H H3COOC

N N H H3COOC

H C2H5 N

H3CO

H

CH3

OH

OCOCH3 COOCH3

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Vinblastine

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Vincristine

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N CH3

H OH

OCOCH3 COOCH3

Vinorelbine

H

N H

C2H5

COOCH3 H3CO

N CH3

H OH

Vindesine

Figure 13. Structures of vinblastine, vinorelbine, vincristine and vindesine.Structural differences are marked in red.

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OH CONH2

Boulikas and Tsogas: Microtubule-targeting anticancer drugs page Vinblastine, cisplatin, mitomycin C, doxorubicin, camptothecin, inostamycin, neocarzinostatin and other anticancer drugs exhibit antitumor activity via ROSdependent activation of apoptotic cell death. The "oxidation therapy of cancer" has been attempted either by inducing the generation of ROS in solid tumors by delivery for example, H2O2, or by inhibiting the antioxidative enzyme (defense) system of tumor cells.

However no successful and practical results were obtained probably because of the lack of tumor selective ROS delivery and in induction of severe side effects. Delivering PEGylated enzymes generating reactive oxygen species, such as xanthine oxidase and D-amino acid oxidase (DAO) is an interesting approach. In addition, a PEGylated zinc protoporphyrin (PEG-ZnPP) and a highly water soluble micellar formulation of ZnPP based on amphiphilic styrene maleic acid copolymer were prepared, which were potent inhibitors of heme oxygenase-1 for oxidation therapy of cancer (Fang et al, 2007).

Whereas antioxidative enzymes such as catalase and SOD are down-regulated in most solid tumors in vivo, heme oxygenase-1 is highly upregulated exerting antiapoptosis in tumors and therefore, its targeting by zinc protoporphyrin might find application as an anticancer drug (Fang et al, 2007).

interdigitation, since cholesterol interrupts the upraise of enthalpy change (Koukoulitsa et al, 2006).

Vinorelbine has a number of side-effects that can limit its use: Lowered resistance to infection, bruising or bleeding, anemia, constipation, diarrhea, nausea, numbness or tingling in hands or feet (peripheral neuropathy), tiredness and a general feeling of weakness (asthenia), inflammation of the vein into which it was injected (phlebitis). Less common effects are hair loss and allergic reaction.

C. Vincristine Vincristine (Oncovin, Vincasar), (Figure 13), is another vinca alkaloid compound that inhibits tubulin polymerization. As it is a vesicant it should be administered with extravasation precautions. It is FDA approved to treat acute leukemia, rhabdomyosarcoma, neuroblastoma, Wilmâ&#x20AC;&#x2122;s tumor, Hodgkin's disease and other lymphomas.

Vincristine is administrated intravenously.

Peripheral neuropathy is the dose limiting side effect, because of this, people with neuromuscular disorders should steer clear of this drug if possible. Likewise, people with some forms of Charcot-Marie-Tooth syndrome should avoid vincristine. Other side effects include mild myelosuppression, constipation -rather commonly-, autonomic neuropathy, CNS toxicity, nausea and vomiting. There have been reported a few cases of acute cardiopulmonary or pain symptoms during administration as well as transient elevation of liver function tests (Pappo et al, 2007; Chow et al, 2006).

As the microtubule is a dynamic protein, constantly polymerizing and depolymerizing, vinca alkaloid poisoned dimers could easily be incorporated into the microtubule polymer, preventing further growth. The incorporation of vincristine onto the heterodimer is rapidly reversible, and appears to occur at two sites per tubulin dimer. At higher concentrations of drug, microtubular crystals are formed, consisting of two intertwined helices of tubulin. Arrests cell cycle in G2/M-phase by blocking mitotic spindle formation. Triggers Raf-1 activation, phosphorylation of bcl-2-family proteins, induction of p53 expression, and apoptosis in several tumor cell lines. Inhibits VEGF production in leukemia cell lines. MRP1 transports vincristine in an ATP- and GSH-dependent manner induces the destabilization of polymerized tubulin, by binding to a site recently localized on !-tubulin, and has a high affinity for the protein.

Accidental injection of vinca alkaloids into the spinal canal (intrathecal administration) is highly dangerous, with a mortality rate approaching 100%. The medical literature documents cases of ascending paralysis due to massive encephalopathy and spinal nerve demyelination, accompanied by intractable pain, almost uniformly leading to death; a handful of survivors were left with devastating neurological damage with no hope of recovery. Rescue treatments consist of washout of the cerebrospinal fluid and administration of protective medications. A significant series of inadvertent intrathecal vincristine administration occurred in China in 2007 when batches of cytarabine and methotrexate (both often used intrathecally) manufactured

B. Vinorelbine Vinorelbine (Navelbine, Figure 13) is a semisynthetic vinca alkaloid that acts the same way as Vinblastine.

Vinorelbine and mitoxantrone (a topoisomerase II inhibitor) have both been demonstrated to have significant antitumor activity in patients with breast cancer. Vinorelbine is approved from the FDA for the treatment of relapsed metastatic breast cancer and for NSCLC either as a single agent or combined with a platinating agent. It is a mild vesicant, requiring extravasation precautions. Myelosuppression -mostly leucopenia- is the dose limiting effect. Not significant nausea and vomiting are reported as well neuropathy -but milder than it is observed with vinblastine- and tumor pain during administration. Acute reaction, such as dyspnea, chest pain and wheezing has been reported during administration but can be prevented in some cases by premedication with corticosteroids (Zelek et al, 2001; Gridelli et al, 2003; Georgoulias et al, 2005).

1. Vinorelbine mechanisms In addition to exerting its antitumor activity by interfering with the polymerization of tubulin, vinorelbine showed antiproliferative effects in human osteosarcoma cells inducing apoptosis without affecting phosphorylation of Bcl-2 but rather by down-regulation of cyclin D1 and up-regulation of p53 expression in wild-type cells; in p53 negative osteosarcoma cells, however, vinorelbine showed no alteration in cyclin D1 (Roncuzzi et al, 2006).

The total enthalpy change in dipalmytoylphosphatidylcholine (DPPC) bilayers was increased by vinorelbine indicating a partial interdigitation of the lipid alkyl chains. The presence of cholesterol in Vinorelbine-DPPC bilayers induced an obstruction of the

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Gene Therapy and Molecular Biology Vol 12, page 333 by the company Shanghai Hualian were found to be contaminated with vincristine.

On the basis of encouraging preclinical activity vinflunine has been selected for clinical development in patients with a wide spectrum of solid tumors. Clinically significant activity has been seen in phase II studies, mainly in the treatment of transitional cell carcinoma of the urothelial tract, non-small cell lung cancer, and carcinoma of the breast. Vinflunine is currently in phase III trial assessment in patients with (second line) transitional cell carcinoma of the urothelium and first-line advanced breast cancer. The efficacy of vinflunine in patients with advanced non-small cell lung cancer previously treated with a platinum-containing regimen was confirmed by a large phase III trial (Nguyen et al, 2008).

In a phase II study the efficacy of vinflunine against malignant pleural mesothelioma (MPM) was assessed.

Patients with a histologically confirmed diagnosis of MPM were eligible for enrollment onto this multicenter phase II trial if they had not received prior chemotherapy or radiotherapy and had measurable lesions by Response Evaluation Criteria in Solid Tumors (RECIST). Vinflunine 320 mg/m2 by 10-minute intravenous infusion was administered on day 1 of 21-day cycles. A response rate of 13.8% was found. The median survival was 10.8 months.

The most common adverse events were anemia, neutropenia, fatigue, constipation, and nausea. Of grade 3 and 4 toxicities, neutropenia and constipation were the most common (45% and 9% of patients, respectively) (Talbot et al, 2007).

D. Vindesine Vindesine (Eldisine and Fildesin) has a serum halflife of about 24 hours and is administered at a dose of 3 milligrams per square meter of body surface. Its toxicity and side effects are similar to those of vinblastine.

Vindesine (Figure 13) is used mainly to treat melanoma and lung cancers (carcinomas) and, with other drugs, to treat uterine cancers.

A study published in 2006 reported the effects of vindesine and gemcitabine on patients with advanced nonsmall cell lung cancer (NSCLC). 44 patients (36 males and 8 females with a median age of 70 years and a median Karnofsky performance score of 60) were recruited between January 1998 and June 2001. 9 patients (20.5%) were stage IIIB patients and 35 (79.5%) were stage IV patients. 20 patients (45.5%) had squamous carcinoma and 24 (54.5%) non-squamous carcinoma. The patients received gemcitabine 1000 mg/m2 and vindesine 3mg/m2 (max 5mg) on days 1 and 8 every 3 weeks, and were all evaluable for response and toxicity: 17 (38.6%) were partial responders, 17 (38.6%) experienced stable disease, and 10 (22.3%) progressive disease. Grade 3-4 anemia, neutropenia and thrombocytopenia were observed in, respectively, 6.8, 9.1 and 2.3% of the patients, and grade 2-3 fatigue, paresthesias and skin toxicity in, respectively, 11.4, 20.4 and 2.3%. After a median follow-up of 54 months, 43/44 patients died; median survival was 12 months, and a clinical benefit was observed in 54.5% of cases. Gemcitabine plus vindesine proved to be an active and well-tolerated schedule (Cetto et al, 2006).

VII. Other tubulin polymerization inhibitors A. Tubulysin A Tubulysin A (Figure 15A) is a highly cytotoxic peptide from myxobacteria with antimitotic activity.

Tubulysin A inhibited tubulin polymerization more efficiently than vinblastine, induced depolymerization of isolated microtubule preparations and triggered the apoptotic process (Figure 15B); electron microscopy studies showed that tubulysin A induced the formation of rings, double rings, and pinwheel structures. The mode of action of tubulysin A resembled that of peptide antimitotics dolastatin 10, phomopsin A, and hemiasterlin (Khalil et al, 2006).

E. Vinflunine Vinflunine is a novel third generation vinca alkaloid with superior antitumor activity in preclinical models, a more favorable toxicity profile compared to the other vinca alkaloids and with radiosensitizing potential (Simoens et al, 2006, 2008). Vinflunine (Javlor) is the first fluorinated microtubule inhibitor and is obtained by semisynthesis using superacidic chemistry to selectively introduce two fluorine atoms at the 20' position of the catharanthine moiety (Figure 14).

Its mechanism of action differs from other members of the vinca alkaloid class in terms of tubulin-binding affinity, microtubule dynamics, spiral formation, and intracellular accumulation. Vinflunine altered adhesion site targeting by microtubules and suppressed the microtubule (+) end pause that occurs at adhesion sites during endothelial cell migration; it has, therefore, an antiangiogenesis potential (HonorĂŠ et al, 2008). The high antitumor activity of vinflunine is not well understood since it binds to tubulin with an overall affinity severalfold lower than that of vinblastine or vincristine; vinflunine suppressed calmodulin interaction with the microtubule-associated protein STOP (stable tubule only polypeptide); this finding and the different binding modes of vinflunine and vinblastine to calmodulin could explain the remarkable antitumor activity of vinflunine (Makarov et al, 2007).

H N

F

F N N H H3COOC

H3CO

H C2H5 N CH3

H OH

OCOCH3 COOCH3

Vinflunine Figure 14. Structure of Vinflunine with the differences marked red.

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Boulikas and Tsogas: Microtubule-targeting anticancer drugs page

OH O

O O NH

O

O

N

N S

H N

N O

O O

OH

Figure 15. (Top) Structure of Tubulisin A. (A, B) Tubulysin induces a depletion of microtubules. PtK2 potoroo kidney cells were cultured in the absence and presence of tubulysin A (59 nm) for 4 h. (A) The control sample shows the normal microtubular network (green) in interphase cells and two mitotic bipolar spindles. Chromosomes and nuclei are stained blue. B ( ) In tubulysin treated cells the microtubule network is less dense and the centrosomes become visible. The mitotic cell in the middle shows metaphase chromosomes and few longer microtubules that do not form a mitotic spindle. From Khalil MW, Sasse F, L端nsdorf H, Elnakady YA, Reichenbach H Mechanism of action of tubulysin, an antimitotic peptide from myxobacteria. Chembiochem. 2006, 7, 678-683. Copyright Wiley-VCH Verlag GmbH & Co.KGaA. Reproduced with permission.

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Gene Therapy and Molecular Biology Vol 12, page 335 Tubulysins are cytotoxic peptides, which include 9 members (A-I). Tubulysin A has potential application as an anticancer agent. It arrests cells in the G2/M phase.

Tubulysin A inhibits polymerization more efficiently than vinblastine and induces depolymerization of isolated microtubules. Tubulysin A has potent cytostatic effects on various tumor cell lines with IC50 in the picomolar range.

Tubulysin A is a highly cytotoxic peptide with antimitotic activity that induces depletion of cell microtubules and triggers the apoptotic process. Treated cells accumulated in the G2/M phase. Tubulysin A inhibited tubulin polymerization more efficiently than vinblastine and induced depolymerization of isolated microtubule preparations. In competition experiments, tubulysin A strongly interfered with the binding of vinblastine to tubulin in a noncompetitive way (Reichenbach et al, 2006).

secretion from lipopolysaccharide-stimulated human peripheral blood mononuclear cells (Zhang et al, 2006).

C. Bisbenzylisoquinoline alkaloids Bisbenzylisoquinoline alkaloids (Figure 17) and their derivatives are possible candidates as modifiers of MDR in cancer chemotherapy by enhancing the cytotoxic effect of vinblastine; partially synthesized compounds from fangchinoline and tetrandrine at 0.1 microM were as potent as 10 #M verapamil in enhancing the cyctotoxic effect of vinblastine in the resistant cell line P388/ADR; a compound with a 5,14-dibromotetrandrine group showed the strongest potentiation effect as an inhibitor of P-gp without affecting the expression of P-gp (Wang et al, 2005).

N

B. CC-5079 The synthetic compound CC-5079 (Celgene, Summit, NJ) potently inhibits cancer cell growth associated with cell cycle arrest in G2/M phase. CC-5079 (Figure 16) prevents polymerization of purified tubulin, competes with colchicines (but not with paclitaxel or vinblastine) for binding to tubulin, and depolymerizes microtubules in cultured cancer cells. Furthermore, CC5079 remains active against multidrug-resistant cancer cells, inhibits the enzymatic activity of phosphodiesterase type 4 and thus, inhibits tumor necrosis factor-! (TNF-!)

O

O O

O

Figure 16. Structure of CC-5079.

OCH3 H3CO H3CN

NCH3

R1

H

H

O

OH

H3CO

OCH3 H3CO H3CN

NR3 R1

H

H

O O R2 OH OCH3 H3CO

H3CN H

NCH3

OCH3 O

H

O HO

Figure 17. Structure of different bisbenzylisoquinoline alkaloids.

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Boulikas and Tsogas: Microtubule-targeting anticancer drugs page however, has led to speculation that it is in reality a microbial, rather than sponge metabolite, as sponges are known to support a wide range of microbes. If this is the case, fermentation technologies could provide a useful supply of the drug.

E7389 (Figure 18), which is in phase I and II clinical trials, is a synthetic macrocyclic ketone analogue of the marine sponge natural product halichondrin B; its main target seems to be tubulin and the microtubules by an endpoisoning mechanism that results predominantly in inhibition of microtubule growth, but not shortening and by induction of tubulin aggregates. E7389 may suppress mitosis by directly binding to microtubule ends as unliganded E7389 (Jordan et al, 2005).

D. Halichondrin B and E7389 First isolated from Halichondria okadai and later from the unrelated sponges Axinella carteri and Phankella carteri, halichondrin B (Figure 18) is a complex polyether macrolide, which has recently been synthesized and arrests cell growth at subnanomolar concentrations. In cell line screenings, halichondrin B showed a similar pattern of activity to other antitubulin drugs, suggesting its possible mode of action as an antimitotic agent, and this prediction was later confirmed experimentally. Halichondrin B is noncompetitive inhibitor of the binding of both vincristine and vinblastine to tubulin, suggesting that the drug binds to the vinca binding site, or a site nearby. The isolation of halichondrin B from two unrelated genera of sponge, CH 3 H H HO H

O

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CH3

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H2N

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H

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Halichondrin B

E7389

Figure 18. Structure of Halichondrin B (left) and E7389 (right).

allowed improving aplidine-induced neuromuscular toxicity. In summary, aplidine is a novel marine anticancer agent with a very particular delayed neuromuscular toxicity that requires careful follow-up with promising antitumor activity (Faivre et al, 2007). Aplidine generally lacks cross-resistance with other known cytotoxic drugs.

Aplidine induces an early oxidative stress response, which results in a rapid and sustained activation of EGFR, of the nonreceptor protein tyrosine kinase Src, of the c-Jun NH2terminal kinase, of the p38 mitogen-activated protein kinase; furthermore, Aplidine induces the cyclindependent kinase inhibitor p27kip1 (p27) through an

E. Aplidine Aplidine (plitidepsin, Figure 19) is a novel anticancer drug isolated from the marine tunicate Aplidium albicans, currently in phase II clinical trials in a variety of solid tumors and hematologic malignancies. It displays a broad spectrum of antitumor activities, inducing apoptosis by triggering mitochondrial cytochrome c release, initiating the Fas/DC95, JNK pathway and activating caspase 3 activation. This agent also inhibits elongation factor 1-a, thereby interfering with protein synthesis, and induces G1 arrest and G2 blockade, thereby inhibiting tumor cell growth. Aplidine's mechanism of action involves several pathways, including cell cycle arrest, inhibition of protein synthesis and antiangiogenic activity. Phase I studies have been reported for a number of several schedules including 1-hour, 3-hour and 24-hour infusion. Evidences of antitumor activity and clinical benefit of aplidine in several tumor types were noted across phase I trials, particularly in advanced medullar thyroid carcinoma. Phase II studies are underway. Within the entire phase I program, dose-limiting toxicities of aplidine were neuromuscular toxicity, asthenia, skin toxicity, and diarrhea. Interestingly, no hematological toxicity was observed. Aplidine displayed a very peculiar delayed neuromuscular toxicity that was found to be closely related to the symptoms described in the adult form of carnitine palmitoyl transferase deficiency type 2, which is a genetic disease treated with L-carnitine.

Consistently, concomitant administration of L-carnitine

OH

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O

NH

O

O

HN

N N

O N H

O

O N

O O

N

OCH3

Figure 19. Structure of Aplidine.

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Gene Therapy and Molecular Biology Vol 12, page 337 oxidation-dependent mechanism. Because sensitivity to Aplidine correlates inversely with the levels of expression of p27, analysis of p27 levels are used to establish response to Aplidine in currently ongoing clinical trials (Moneo et al, 2007).

H. Dictyostatin and 10,11Dihydrodictyostatin The total synthesis of 10,11-Dihydrodictyostatin (Figure 21) was achieved; the compound was found to retain potent antimitotic activity, with a comparable profile to discodermolide and Taxol, functioning by microtubule stabilization and G2/M arrest (Paterson et al, 2008).

A recent study demonstrated that dictyostatin-1 (Figure 21) induced a strong G2/M block and accumulation of A549 cells in the S phase at concentrations as low as 10 nM. A large increase of sub-G1 population was also observed, indicative of cells undergoing active apoptosis.

Paclitaxel induced similar changes at 10 nM, but these were not as extensive as those produced by dictyostatin-1.

The microtubule morphology was also investigated, where it became evident that dictyostatin-1 promoted the rearrangement of microtubules into bundle formations similar to those induced by paclitaxel, although dictyostatin-1 had much more prominent effects at lower concentrations. The percentage of the microtubule matrix condensed into bundles increased with higher concentrations of dictyostatin-1, although there appeared to be little additional bundling at concentrations greater than 100 nM. Dictyostatin-1 also proved to be highly potent in two paclitaxel-resistant human cancer cell lines expressing active P-glycoprotein. Together, these results indicate that dictyostatin-1 is a potent inducer of tubulin polymerization and retains activity in cells expressing the P-glycoprotein efflux pump (Wright et al, 2003).

F. Nocodazole Nocodazole (Figure 20) is an antimitotic agent that disrupts microtubules by binding to $ tubulin and preventing formation of one of the two interchain disulfide linkages, thus inhibiting microtubule dynamics, disruption of mitotic spindle function, and fragmentation of the Golgi complex. Arrests the cell cycle at G2/M phase. Prevents phosphorylation of the T cell antigen receptor and inhibits its activity. Stimulates the intrinsic GTPase activity of tubulin. Activates the JNK/SAPK signaling pathway and induces apoptosis in several normal and tumor cell lines (Ley et al, 1998).

G. GMC-5-193 GMC-5-193 (GMC) is a novel anticancer smallmolecule quinazolinone analogue with properties that possesses antimicrotubule activity. In a recent study a liposomal formulation for tumor-targeting delivery of GMC was prepared and systemically administered to enhance the anticancer effect of this compound and evaluate its bioefficacy. GMC was encapsulated within a cationic liposome, which was decorated on the surface with an anti-transferrin receptor single-chain antibody fragment (TfRscFv) as the tumor-targeting moiety.

Confocal imaging of fluorescent GMC uptake in a human melanoma cell line, MDA-MB-435, showed higher cellular uptake of GMC when delivered via the liposomal formulation compared with free GMC. Delivery of GMC by the tumor-targeting liposomal formulation also resulted in a 3- to 4-fold decrease in IC50 values in human cancer cells DU145 (prostate) and MDA-MB-435, compared with the effects of GMC administered as free GMC. In addition, the GMC liposomal formulation increased the sensitivity of cancer cells to doxorubicin, docetaxel, or mitoxantrone by 3- to 30-fold. In the MDA435/LCC6 athymic nude mice xenograft lung metastases model, GMC was specifically delivered to tumors by the liposomal formulation (Chang et al, 2008).

O H N NH S N O

Figure 20. Structure of Nocodazole.

OH

OH

HO

HO

O

O

O 11 10

OH

O

OH

OH

Figure 21. Structure of Dictyostatin (left) and 10,11-Dihydrodictyostatin (right).

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OH

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Boulikas and Tsogas: Microtubule-targeting anticancer drugs page design. Thus, the function of a biologically active lead structure can be recapitulated, tuned, or greatly enhanced with simpler scaffolds. Analogs of bryostatin, a natural product that restores apoptosis in cancer cells, reverses MDR, and bolsters the immune system, synthesized according to the FOS principle were superior to bryostatin (Wender et al, 2008).

I. Peloruside A Peloruside A (Figure 22) is a naturally occurring compound isolated from a New Zealand marine sponge.

Peloruside A binds to a unique site on the tubulin !!heterodimer, the laulimalide site, which is distinct from the taxoid site and thus differentiates it from paclitaxel, docetaxel, epothilone A, and discodermolide (Hamel et al, 2006). Peloruside A exhibited synergy with paclitaxel and epothilone A in cell proliferation assays (Wilmes et al, 2007). Peloruside, unlike paclitaxel, does not induce murine macrophages to produce the proinflammatory mediators interleukin-12p40 (IL-12p40), tumor necrosis factor-! (TNF-!), and nitric oxide; thus, peloruside may prove to be an effective anti-inflammatory agent (Crume et al, 2007).

Like paclitaxel and other microtubule stabilizing agents, Peloruside A binds to and stabilizes the polymerized form of tubulin, thereby blocking cells in G2/M of the cell cycle. Peloruside A is a good candidate for development as an anticancer drug. It has a similar mechanism of action to paclitaxel and docetaxel (Taxotere), but has a number of distinct advantages compared to the taxanes. For example, it is less lipophilic and therefore easier to solubilize and deliver as a drug (although a disadvantage for liposomal formulation at the lipid bilayer and delivery as a nanoparticle). Peloruside A is also more likely to be effective against cells that express the multidrug resistance (MDR) phenotype. Most microtubule stabilizing drugs like paclitaxel, docetaxel, Epothilones and discodermolide bind to a well-defined site (taxoid site) on $-tubulin. However, Peloruside A has a unique binding site on tubulin that differs from the taxoid site; therefore, $-tubulin mutant cell lines with amino acid substitutions in the taxoid binding site are more susceptible to Peloruside A than to paclitaxel or Epothilones. In a recent study, it was established that Peloruside A bind to a distinct site on the !-tubulin monomer, and not to the $-tubulin monomer like the taxoid drugs (Miller et al, 2007).

K. Cyclostreptin Studies with cyclostreptin (Figure 23) that irreversibly stabilizes microtubules, inhibits paclitaxel binding to microtubules but weakly induces tubulin assembly, have given important clues on the mechanism by which taxoid-site compounds reach the kinetically unfavorable lumenal site. Cyclostreptin was able to form covalent crosslinks to !-tubulin in cellular microtubules distributed between Thr220 (at the outer surface of a pore in the microtubule wall) and Asn228 (at the lumenal paclitaxel site); unpolymerized tubulin was only labeled at Thr220 (Buey et al, 2007).

Although cyclostreptin weakly stimulates tubulin assembly, it avidly binds to microtubules, thereby strongly inhibiting the binding of other microtubule-stabilizing agents to polymer. In addition, cyclostreptin-stabilized microtubules disassemble at 0 oC more slowly than paclitaxel- stabilized microtubules. Cyclostreptin interacts covalently both in vitro and in cells with polymerized tubulin, blocking the binding of even the most potent taxoid-site ligands. Moreover, cyclostreptin is fully active in multidrug-resistant (MDR) ovarian carcinoma (A2780/AD) cells overexpressing P-glycoprotein, which indicates that covalent binding might be a way to overcome MDR.

L. ABT-751, Colchicine, TLK-286.

ABT-751 (Figure 24) is an agent that targets the colchicine site of tubulin. Another approach is to enhance the activity of currently available agents by targeting detoxification and resistance pathways. TLK-286 is a novel agent that may enhance the activity of previously available agents by inhibiting GST-pi, a detoxifying mechanism that may be of particular relevance to platinum agents (reviewed by Edelman, 2006).

ABT-751 is a novel oral antimitotic agent that binds to the colchicine site on tubulin and inhibits polymerization of microtubules. Disruption of new microtubules leads to arrest in the cell division cycle and

J. Function-oriented synthesis (FOS) of therapeutic drugs Many biologically active natural products are scarce or difficult to obtain, highly complex and not optimally suitable for therapeutic use. FOS can provide access to newly designed structures with novel activities while at the same time allowing for synthetic innovation by target

O

O

OH

OMe O

HO

O OH HO

OH HO

O O

MeO

OMe OH

Figure 23. Structure of Cyclostreptin.

Figure 22. Structure of Peloruside A.

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Gene Therapy and Molecular Biology Vol 12, page 339 induction of apoptosis. There are currently no colchicinesite agents approved for cancer chemotherapy. ABT-751 has demonstrated anti-tumor activity against a variety of syngeneic and human xenograft tumor models including colon, lung, stomach, breast, and nasopharyngeal cancer models, and is also active in vivo against vincristine-, cisplatin- and 5-fluorouracil-resistant cells. ABT-751 is not a multiple drug resistance (MDR) substrate. A phase I trial of orally administered ABT-751 given daily x 7 every 3 weeks was instituted to determine the dose limiting toxicity (DLT), maximum tolerated dose (MTD) and pharmacokinetics. A total of 15 patients have been studied to date. Doses of 200 and 250 mg pc qd x 7 were found to be tolerable. DLT was seen in 2/6 patients (neuropathy and ileus) at the qd dose of 300 mg/d. One of 3 patients studied to date at the 125 mg pc bid x 7d dose developed a supraventricular arrhythmia. This occurred 17 days after ABT dosing and is thought unlikely to be drug related (Rothenberg et al, 2002).

Grade 2 toxicities noted to date include constipation, fatigue, nausea, vomiting, myalgias, and anemia.

Myelosuppression has not been noted. Pharmacokinetic studies were performed on day 7 of therapy.

Colchicine (Figure 24) inhibits microtubule polymerization by binding to tubulin (Banerjee, 1997) one of the main constituents of microtubules. Availability of tubulin is essential to mitosis, and therefore colchicine effectively functions as a "mitotic poison" or spindle poison. Since one of the defining characteristics of cancer cells is a significantly increased rate of mitosis, this means that cancer cells are significantly more vulnerable to colchicine poisoning than are normal cells. However, the therapeutic value of colchicine against cancer is (as is typical with chemotherapy agents) limited by its toxicity against normal cells. Side effects include gastro-intestinal upset and neutropenia. High doses can also damage bone marrow and lead to anemia. Note that all of these side effects can result from hyper-inhibition of mitosis. The toxicity of colchicine poisoning has been compared to arsenic poisoning: symptoms start 2 to 5 hours after the toxic dose has been ingested and include burning in the mouth and throat, fever, vomiting, diarrhea, abdominal pain and kidney failure. Death from respiratory failure can

follow. There is no specific antidote for colchicine, although various treatments do exist.

TLK-286 (Figure 24) is a novel prodrug that is preferentially activated by glutathione S-transferase P1-1 (GSTP1-1) and is currently developed by Telik, Inc. (Palo Alto, CA, USA). TLK-286 is the lead clinical candidate from a group of rationally designed glutathione analogues designed to exploit high GSTP1-1 levels in solid tumors and drug-resistant cell populations. This concept was based on extensive literature showing that the overexpression of GSTP1-1 in human tumours is associated with malignancy, poor prognosis and the development of drug resistance. Thus, the selective targeting of susceptible tumour phenotypes is a strategy that should result in the release of more active drug in malignant cells compared with normal tissue, thereby achieving an improved therapeutic index. In a series of Phase II clinical trials, TLK-286 was initially shown to have clinical activity and a favorable toxicity profile as a single agent in the salvage setting in ovarian, non-small cell lung, breast and colorectal cancers. Recently, Phase II trials have been reported that demonstrated TLK-286 is active and did not increase the toxicity in combination treatment regimens with standard chemotherapeutic agents, including platinums, taxanes and anthracyclines in previously treated patients with ovarian and non-small cell lung cancers, and in the first-line treatment setting in nonsmall cell lung cancer patients. TLK-286 is also presently under active testing in Phase III settings for non-small cell lung and ovarian cancers (Kenneth, 2005).

M. Colchicine-like microtubule binding agents Known antitumor substances isolated from microorganism metabolites (including anthracyclines and mitomycins) exhibit antitumor activity by binding to DNA. Diketopiperazine-type metabolites (Figure 25) isolated from various fungi as mycotoxins (Ali et al, 1989) or as secondary metabolites (Smedsgaard, Frisvad et al, 1996) also possess antitumor activity.

The closely related (-)-Phenylahistine and (-)Aurantiamine (dehyro-(2,5)-diketopiperazines, Figure 25) have been isolated from Aspergillus ustus NSC-F038 Cl

O

OCH3

O S HN H N

O

OCH3

H3CO

H

O

B

O

HO

HN

S O

H2N O

O

O

ABT-751

Colchicine

Figure 24. Structures of ABT-751, colchicine and TLK-286.

339

Cl O OH

N HO

Cl

O

A

C

Cl

N O O P N

H3CO

TLK-286

Boulikas and Tsogas: Microtubule-targeting anticancer drugs page (Katada et al, 1997) and Penicillium aurantiogriseum (Larsen et al, 1992), respectively. These diketopiperazine derivatives consist of an L-phenylalanine or L-valine residues, respectively, and a unique isoprenylated dehydro-histidine residue with a quaternary carbon at the 5-position of the imidazole ring.

The former is a member of a new class of colchicinelike microtubule binding agents that exhibit cytotoxic activities against a wide variety of tumor cell lines. This activity was found to be similar to the Vinca alkaloids.

Vincristine and vinblastine are cross-resistant to multidrug resistant cancer cells, which overexpress the Pglycoprotein drug efflux pump; on the contrary, (-)phenylahistine showed no such cross resistance (Fenical et al, 2003). Similar to the Vinca alkaloids, it is collaterally sensitive to a paclitaxel resistant cell line with altered !tubulin. (-)-Phenylahistine exhibited antitumor activity against 8 tumor cell lines with IC50 values ranging from 1.8 x 10-7 to 3.7 x 10-7 M, while (+)-phenylahistine exhibited less potent activity than (-)-phenylahistine. Also, it showed antitumor activity against P388 leukemia and Lewis lung carcinoma in vivo (Kanoh et al, 1999).

(-)-Aurantiamine (Figure 25) was isolated as a blue fluorescence compound for chemotaxonomic indication of growth in some toxigenic varieties of P. aurantiogriseum and lately it showed antibacterial activity (Khaddor et al, 2007). In spite the structural similarities these molecules, exhibit different biological activities. The solution phase (Hayashi et al, 2000) and solid phase total synthesis of these two natural products gave a novel approach to their synthesis (Couladouros and Magos, 2005a). An essential component of their synthesis was the construction of a dehydro-(2,5)-diketopiperazine library with a rapid parallel synthesis of a large number of diversified structures, molecules with potential anticancer activity (Couladouros and Magos, 2005b).

O Ph

The antifungal drug griseofulvin (Figure 26, Left) inhibits mitosis strongly in fungal cells and weakly in mammalian cells by affecting mitotic spindle microtubule function. Griseofulvin also blocked cell-cycle progression at G2/M and induced apoptosis in human tumor cell lines.

Very high concentrations of griseofulvin (>100 microM) were required to inhibit microtubule polymerization in vitro but lower drug concentrations (1-20 microM) strongly suppressed the dynamic instability behavior of the microtubules (Figure 26, Right). It was suggested that griseofulvin could be an interesting anticancer agent inhibiting mitosis by suppressing spindle microtubule dynamics in a manner qualitatively similar to that of vinca alkaloids and taxanes (Panda et al, 2005).

VIII. Nanoparticle formulations of taxanes A number of tubulin stabilizing agents are under clinical evaluation and more, currently at preclinical stage, are expected to be clinically tested (Table 1).

A. Polymeric micelle formulations of paclitaxel Following the success of Abraxane, there has been an explosion in the area of research on nanoparticle formulations of taxanes and other microtubule-targeting agents. Poly-(DL)-lactide co-glycolide 50:50 microspheres of 50 Âľm in diameter impregnated with paclitaxel were used for intra-articular injection to suppress proliferative synovitis in animal models (Bragdon et al, 2001). A new polymer-conjugated derivative of paclitaxel, PNU166945, was investigated in a dose-finding phase I study in patients with refractory solid tumors. PNU16645 was administered

O NH

Ph

N NH

HN

O NH

NH

HN

O

NH

N

O

(-)-Phenylahistine

(+)-Phenylahistine

R

NH

HN O

O L-Aminoacid core

N

NH Heterocycle

HN O

Glycine Backbone

Dehydro-(2,5)-Diketopiperazine library Figure 25. Dehydro-(2,5)-diketopiperazines: (Âą)-phenylahistine and (-)-aurantiamine.

340

(-)-Aurantiamine

Gene Therapy and Molecular Biology Vol 12, page 341

O

O

Cl

O O

O

O

Figure 26 (Left) Structure of the antifungal drug griseofulvin. (Right) Effects of 20, 40, and 120 #M griseofulvin on interphase microtubules in HeLa cells. HeLa cells were incubated with the indicated concentrations of griseofulvin for 40 h. At 40#M griseofulvin, 85-90% of the interphase cells were multinuclear and significantly larger than control cells. At 120 #M griseofulvin, which completely inhibited proliferation, ~50% of the cells remained in interphase and had substantial numbers of microtubules, although the density of the microtubules was decreased, compared with the density in control cells.Cells were fixed and incubated with mouse monoclonal anti!-tubulin antibody (Sigma) at 1:300 dilution for 2 h at 37°C then with anti-mouse IgG antibody labeled with Alexa Fluor 568 (Molecular Probes) at 1:100 dilution for 1 h at 37°C then then rinsed with PBS and incubated with DAPI (1 #g/ml) for 20 s for DNA staining. From "Panda D, Rathinasamy K, Santra MK, Wilson L (2005) Proc. Natl. Acad. Sci. USA 102: 9878–9883, Copyright 2005 National Academy of Sciences, U.S.A."

Table 1. Microtubule stabilizing agents Name or formulation

Active compound and properties

CT-2103 (Poliglumex, PGTXL)

Conjugated poly(L-glutamic acid)- Paclitaxel

BMS-188797 BMS-184476 BMS-275183

RPR 109881A (Figure 27)

PNU166945

NK105 (Figure 29) BMS-185660 Polymeric micellar Paclitaxel thermosensitive micellar

Semi-synthetic derivative of Paclitaxel Ether derivative of Paclitaxel

Development stage Phase III NSCLC Phase II ovarian Phase II in breast cancer was terminated because of toxicity

Reference Nemunaitis et al, 2005; Lin et al, 2007; O'Brien et al, 2008; Paz-Ares et al, 2008

Phase I/II

Advani et al, 2003; Fishman et al, 2006 Sun et al, 2003

orally administered C-4 methyl carbonate paclitaxel analogue

Phase I/II

Bröker et al, 2006, 2007

semisynthetic taxoid with a similar mechanism to docetaxel

Phase I

Kurata et al, 2000; Sessa et al, 2002

Polymer- conjugated Paclitaxel

Phase I was discontinued prematurely due to severe neurotoxicity

Meerum Terwogt et al, 2001

Phase I

Hamaguchi et al, 2005, 2007; Negishi et al, 2006

Preclinical

Rose et al, 2000

Preclinical

Zhang et al, 1997

Preclinical

Liu et al, 2008

polymeric micelle carrier system for paclitaxel Semi-synthetic derivative of Paclitaxel Poly(DL-lactide)-b-mPEG micellar Paclitaxel poly(N-isopropylacrylamide-coacrylamide)-b-poly(DL-lactide) 341

Phase I/II

Boulikas and Tsogas: Microtubule-targeting anticancer drugs page delivery system for docetaxel and paclitaxel PTX-DLPC

Aerosol-liposomal Paclitaxel

Preclinical

Koshkina et al, 2001

FR182877 (WS9885B)

Natural product

Early preclinical

Vanderwal et al, 1999

micellar PEGylated hyperbranched polyester

drug delivery system for paclitaxel

Early preclinical

Kontoyianni et; al, 2008

Hyaluronic acid (HA)paclitaxel conjugate micelles (Figure 28)

Nanocomplexes of Paclitaxel chemically conjugated to HA via an ester linkage

Early preclinical

Lee et al, 2008

PEG and poly(2-(4vinylbenzyloxy)-N,Ndiethylnicotinamide) amphiphilic copolymers

micellar paclitaxel

Early preclinical

Lee et al, 2007

hyperbranched polyglycerolpolyethylene glycol copolymers

paclitaxel with sustained drug release characteristics

Early preclinical

Kainthan et al, 2008

Early preclinical

Sznitowska et al, 2008

Early preclinical

Huh et al, 2008

Paclitaxel in micellar lecithin hydrotropic polymer micelles

Paclitaxel in 5% egg lecithin / water dispersion paclitaxel-loaded polymeric micelles

amphiphilic copolymers of poly(ethyl ethylene phosphate) and poly($-caprolactone)

paclitaxel-loaded polymeric micelles

Early preclinical

Wang YC et al, 2008

poly(N-isopropylacrylamideco-acrylamide)-b-poly(DLlactide) copolymers

docetaxel or paclitaxel polymeric thermosensitive micelles

Early preclinical

Liu et al, 2008

mPEG-b-oligo('-caprolactone) micelles (Figure 29)

docetaxel or paclitaxel in 10-nm micelles

Early preclinical

Carstens et al, 2008

P105 or L101 Pluronic block copolymers with folate as a targeting ligand

paclitaxel micelles to overcome MDR and target ovarian cancer

Early preclinical

Wang Y et al, 2007

P123 Pluronic polymeric micellar formulation of paclitaxel

paclitaxel micelles

Early preclinical

Han et al, 2006

Early preclinical

Quaglia et al, 2009

Early preclinical

Xu et al, 2009

SC16OH cyclodextrin nanoparticles hepatoma-targeted solid lipid nanoparticle (tSLN)

Docetaxel-loaded SC16OH nanoparticles docetaxel-loaded galactosylated dioleoylphosphatidyl ethanolamine

A mixture of poly(lactide-bethylene glycol-b-lactide) and prostate specific membrane antigen-inhibitor bound !amino-%-hydroxy terminated poly (ethylene glycol-b-'caprolactone)

nanoparticles loaded with docetaxel

Early preclinical

Chandran et al, 2008

polylactide-co-glycolidepolyethylene glycol-folate (PLGA-PEG-FOL) conjugate

folate-receptor-targeted nanoparticles loaded with docetaxel

Early preclinical

Esmaeili et al, 2008

DTX-HGC nanoparticles (hydrophobically modified glycol chitosan)

docetaxel-loaded

Early preclinical

Hwang et al, 2008

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Gene Therapy and Molecular Biology Vol 12, page 343 O

.

O

O

H3C

O

H3C O

NH

CH3

O

CH3

x 2H2O

O

HO

O

OH

O

O

CH3 O

O

Figure 27. Structure of RPR 109881A

O H3C H3C O

NH

O

O

OH

CH3

O

CH3 O

HO

O

O O

O O O

O

CH 3

O NH

HN

OH O

O HO

O

O

HO

OH

OH

n Figure 28. Structure of micellar Poly(hyaluronic acid)-Paclitaxel conjugates.

as a 1-h infusion every 3 weeks at a starting dose of 80 mg/m2, as paclitaxel equivalents, up to 196 mg/m2 as the highest dose level. A partial response was observed in one patient with advanced breast cancer. However, this study was discontinued prematurely due to severe neurotoxicity observed in additional rat studies (Meerum Terwogt et al, 2001). Paclitaxel was also encapsulated into dilauroylphosphatidylcholine liposomal formulations (PTX-DLPC) and was administered by aerosol in the lungs for evaluation of inhibition of pulmonary metastases in a murine renal carcinoma model. PTX-DLPC aerosols were generated with the Aero-Mist jet nebulizer (cisUSA). The most effective schedule of treatment was when mice inhaled the drug for 30 min 3 days per week. and led to prolonged survival in mice inoculated with Renca cells (Koshkina et al, 2001).

The size of the micelles can be controlled within the diameter range of 20 to 100 nm, to ensure that the micelles do not pass through normal vessel walls; therefore, a reduced incidence of the side effects of the drugs may be expected due to the decreased volume of distribution.

Polymeric micelles are expected to increase the accumulation of drugs in tumor tissues utilizing the EPR effect and to incorporate various kinds of drugs into the inner core by chemical conjugation or physical entrapment with relatively high stability.

Chemical conjugates of paclitaxel and hyaluronic acid (HA) (Figure 28) were synthesized by utilizing a novel HA solubilization method in a single organic phase.

Hydrophilic HA was completely dissolved in anhydrous DMSO with addition of poly(ethylene glycol) (PEG) by forming nanocomplexes. Paclitaxel was then chemically 343

Boulikas and Tsogas: Microtubule-targeting anticancer drugs page conjugated to HA in the DMSO phase via an ester linkage without modifying extremely hydrophilic HA (Lee et al, 2008).

A copolymer of poly(ethyl ethylene phosphate) and poly(e-caprolactone) was further surface conjugated with galactosamine to target asialoglycoprotein receptor (ASGP-R) of HepG2 cells. The 70-nm particles were negatively charged in aqueous solution. Paclitaxel-loaded micelles with galactose ligands were developed for drug transportation and intracellular drug release (Wang et al, 2008). Oral administration of anticancer agents using block-graft copolymers of the poly(ethylene oxide) (PEO) and poly(propylene oxide) (PPO) Pluronic速 polyethers and poly(acrylic acid) (PAA) bound by carbon-carbon bonds has been proposed. The Pluronic-PAA copolymers

are surface-active and self-assemble, at physiological pH, into intra- and intermolecular micelles with hydrophobic cores of dehydrated PPO and multilayered coronas of hydrophilic PEO and partially ionized PAA segments.

These micelles efficiently solubilize hydrophobic drugs such as paclitaxel. Weakly basic and water-soluble drugs such as doxorubicin, mitomycin C, mitoxantrone, fluorouracil, and cyclophosphamide are formulated through electrostatic interactions with the micellar corona (Bromberg, 2008). Micelles and mixed micelles prepared from Pluronic block copolymer P105 or L101 were used for paclitaxel delivery to overcome MDR; both micelle systems were further covalently modified with folate as a targeting ligand for tumors overexpressing the folate receptor (Wang Y et al, 2007).

O O

O H

x

H

y

O

H N

O

H N

H O

y

z

O

O

OH

O

y

Poly(ethylene glycol-b-lactic acid)

O

x

H

O x

Poly(ethylene glycol-b-!- caprolactone)

O

O

O

H

O

O y

x

O

NK105

O N

O N

PEG-b-(2-(4-vinylbenzyloxy)-N,N-diethylnicotinamide) O H

O

x H2N HN

O

H

yO

O

z

O

Poly[(NIPAAm-co-IPAAm)-b-(DL-lactide)]

O O H

O O

O P

OH

O

x

y

Poly(ethyl ethylene phosphate-b-!-caprolactone)

Figure 29. Structure of micellar amphiphilic block copolymers that solubilize paclitaxel in their hydrophobic core.

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Gene Therapy and Molecular Biology Vol 12, page 345 Amphiphilic block copolymers consisted of a micellar shell-forming poly(ethylene glycol) (PEG) block and a core-forming poly(2-(4-vinylbenzyloxy)-N,Ndiethylnicotinamide) (Figure 29) were used to load paclitaxel up to 37.4 wt %; the presence of N,NDiethylnicotinamide (DENA) in the micellar inner core resulted in effective paclitaxel solubilization and stabilization. The maximum loading capacity of poly(ethylene glycol)-b-P(D,L-lactide) (PEG-b-PLA) micelles (Figure 29) for comparison was 27.6 wt %. The hydrotropic polymer micelles were more effective than PEG-PLA micelle formulations in inhibiting the proliferation of human cancer cells (Lee et al, 2007).

The polymeric micellar formulation of paclitaxel with Pluronic P123 can effectively solubilize, prolong blood circulation time, and modify the biodistribution of paclitaxel (Han et al, 2006).

Hydrophobically modified hyperbranched polyglycerol-polyethylene glycol copolymers assume unimolecular micellar structures in aqueous solution were used for paclitaxel; although these polymers aggregate weakly in solution, the aggregates are broken down by low shear forces or by encapsulating a hydrophobic ligand within the polymer (Kainthan et al, 2008). A biocompatible, lecithin-based carrier for paclitaxel suitable for intravenous infusion has been proposed; among aqueous dispersions of egg or soya lecithin, mixed micellar solutions of egg lecithin and sodium deoxycholate, and formulations containing lecithin plus the co-surfactants and co-solvents poloxamer, polysorbate, Span, benzalkonium chloride, and macrogol the best formulation was a 5% egg lecithin / water dispersion containing 1 mg/ml paclitaxel (Sznitowska et al, 2008).

The poorly water soluble paclitaxel was formulated into hydrotropic polymer micelles without using organic solvents required for solubilization; poly(ethylene glycol) was used as a hydrophilic block and poly[4-(2vinylbenzyloxy-N-picolylnicotinamide)] as hydrotropic

block. The hydrotropic block copolymers synthesized were able to form paclitaxel-loaded polymeric micelles in aqueous solution and were proposed as novel carriers for hydrophobic drugs (Huh et al, 2008). Biodegradable triblock copolymers composed of a hydrophobic core of poly('-caprolactone) (PCL) and a hydrophilic shell of poly(ethyl ethylene phosphate) (PEEP) formed spherical micelles in aqueous solution; paclitaxel was successfully loaded into the micelles and were proposed as novel carriers for hydrophobic drug delivery (Wang YC et al, 2008). A polymeric thermosensitive micellar delivery system for docetaxel or paclitaxel based on [poly(Nisopropylacrylamide-co-acrylamide)-b-poly(DL-lactide) was proposed (Figure 29); hyperthermia greatly enhanced the antitumor effect of micellar taxanes in mouse xenografts (Liu et al, 2008). Oligomeric micelles composed of mPEG750-b-oligo(e-caprolactone)5 (mPEG750b-OCL5) with a hydroxyl (OH), benzoyl (Bz) or naphthoyl (Np) end group were studied; the presence of an aromatic end group (Bz or Np) resulted in the formation of 10-nm, almost monodisperse, micelles with stable encapsulation of 10% (w/w) docetaxel or paclitaxel dissolved in the core (Carstens et al, 2008). Hydrophobic prodrugs of paclitaxel were synthesized via DCC/DMAP or anhydride chemistry to overcome the poor loading (<1% w/w) of paclitaxel in amphiphilic block co-polymer micelles of poly(ethylene glycol)-b-poly('-caprolactone) (PEG-b-PCL) (Forrest et al, 2008). The diblock copolymer poly(ethylene oxide)-bpoly ('-caprolactone) (Figure 29) was used for coreloading of paclitaxel. This polymer formed two types micelles: worm-like micelles of nanometer in crosssection that spontaneously formed stable lengths of microns with improved solubilization efficiency for paclitaxel, and spherical micelles that exhibited lower drug loads (Cai et al, 2007). A schematic represenation of micellar amphiphilic block copolymers incorporating paclitaxel is shown in Figure 30.

Figure 30: Schematic represenation of micelles formed by amphiphilic block copolymers having a hydrophobic core and a hydrophilic corona.

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B. Docetaxel nanoparticles

C. NK105

Nanoparticles composed of the amphiphilic cyclodextrin heptakis (2-O-oligo(ethyleneoxide)-6hexadecylthio-)-!-CD (SC16OH) were prepared by the emulsion-solvent evaporation technique and were used to entrap docetaxel with an efficiency close to 100%. These were determined to be spherical vesicular nanoparticles displaying a hydrodynamic radius of about 95 nm having a negative zeta potential. Docetaxel-loaded SC16OH nanoparticles were not hemolytic toward red blood cells as compared to a commercial docetaxel and also had superior cell killing and cell damage to HEp-2 cells (Quaglia et al, 2009). A solid lipid 120nm nanoparticle (tSLN) was designed and prepared with galactosylated dioleoylphosphatidyl ethanolamine for docetaxel targeted to hepatoma cells (Xu et al, 2009). An encapsulation efficiency >90% was achieved. Cytotoxicity of tSLNs against a hepatocellular carcinoma cell line was superior to Taxotereâ&#x201E;˘ and a non-targeted SLNs (Xu et al, 2009).

The relative efficacy of polysorbate-based docetaxel was significantly lower compared with nab-paclitaxel in HER2-negative tumors in preclinical studies (Desai et al, 2008). A combined approach was used to decorate the surface of a nanoparticle with a urea-based small-molecule peptidomimetic inhibitor of prostate specific membrane antigen (PSMA). PSMA is overexpressed in normal and malignant prostate epithelial cells and by the neovasculature of almost all solid tumors. Nanoparticles loaded with docetaxel were formulated using a mixture of poly(lactide-b-ethylene glycol-b-lactide) and PSMAinhibitor bound &-amino-%-hydroxy terminated poly (ethylene glycol-b-$-caprolactone) (Chandran et al, 2008).

Hydrophobically modified glycol chitosan (HGC) nanoparticles were prepared by introducing a hydrophobic molecule, cholanic acid, to water-soluble glycol chitosan.

The HGC nanoparticles were easily loaded with the anticancer drug docetaxel using a dialysis method, and the resulting nanoparticles formed spontaneously selfassembled aggregates with a mean diameter of 350 nm; these docetaxel nanoparticles showed higher reduction in tumor volume and increased survival rate in A549 lung cancer cells-bearing mice with reduced toxicity compared to docetaxel (Hwang et al, 2008).

NK105 (Figure 29) is a new polymeric micelle carrier system for paclitaxel under Phase I clinical evaluation. Paclitaxel was incorporated into the inner core of the micelle system by physical entrapment through hydrophobic interactions between the drug and the welldesigned block copolymers (Hamaguchi et al, 2005).

Neutropenia was the most common haematological toxicity whereas neuropathy and other grade 3 or 4 nonhaematological toxicities were not observed; the drug formulation was administered without antiallergic premedication and the plasma AUC of NK105 at 150 mg/m2 was 15-fold higher than that of paclitaxel (Hamaguchi et al, 2007). Lewis lung carcinoma-bearing mice were administered a single intravenous injection of paclitaxel or NK105 followed by radiation to the tumour site 24 h after drug administration; tumors were excised and specimens were prepared for flow-cytometric analysis; this approach showed that NK105-treated tumor cells had a severe arrest at the G2/M phase compared to paclitaxel-treated tumor cells. Thus, NK105 was found to possess a superior radiosensitising activity attributable to its potent cell cycle arrest at the G2/M phase (Negishi et al, 2006).

D. BMS-188797 BMS-188797 has a single C-4 modification, a 4desacetyl-4-methylcarbonate, compared with paclitaxel (Figure 31). A phase I monotherapy study on 51 patients established febrile neutropenia as the dose-limiting toxicity at 200 mg/m2 and with moderate to severe sensory neuropathy in 24% of the patients (Garrett et al, 2005). A phase I and pharmacokinetic study of BMS-188797 and 75 mg/m2 cisplatin every 21 days in 16 patients resulted in three complete remissions in ovarian and cervical cancer patients and one partial response; leucopenia/neutropenia, neuropathy, nausea, diarrhoea and stomatits were the main side effects (du Bois et al, 2006). In a different phase I study, a fixed dose of carboplatin was combined with a dose escalation schedule of BMS-188797, both administered once every 3 weeks two radiographic partial responses were observed (Fishman et al, 2006).

O O O

O O

OH

H3C O

NH

H O OH OH

O

H O

O

O O

O

Figure 31. Structure of BMS-188797.

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E. BMS-184476

G. Paclitaxel poliglumex

BMS-184476 is a 7-methylthiomethyl ether derivative of paclitaxel (Figure 32) that inhibits the growth of paclitaxel-resistant human tumor cell lines with multidrug resistance mediated by either P-glycoprotein or mutated tubulin. Given the known synergy between taxanes and cisplatin in vitro and their clinical activity in combination, a Phase I trial was performed with BMS184476 and cisplatin on 27 patients (Sun et al, 2003).

Targeted drug delivery aims to increase the therapeutic index by making more drug molecules available at the diseased sites while reducing systemic drug exposure. Paclitaxel poliglumex (PPX, XYOTAX or CT-2103; Figure 34) is a macromolecular drug conjugate that links paclitaxel with a biodegradable polymer, poly-Lglutamic acid, giving a water-soluble conjugate with a prolonged half-life and limited volume of distribution (Boddy et al, 2005; Chipman et al, 2006). It is currently under Phase III evaluation (O'Brien et al, 2008). In a Phase I study CT-2103 administered at 225 mg/m2 every 21 days in combination with carboplatin administered at AUC 6 had a manageable safety profile in patients with solid tumors (Nemunaitis et al, 2005). However, another Phase I study showed that neuropathy was more severe than expected (Veronese et al, 2005). PPX enhances tumor exposure by taking advantage of the hyperpermeable vasculature and suppressed lymphatic clearance characteristic of tumor tissue. Single-agent PPX, dosed at 175 mg/m2, was active and well tolerated in patients with advanced NSCLC. Patients on PPX required fewer red blood cell transfusions, hematopoietic growth factors, opioid analgesics, and clinic visits than patients receiving gemcitabine or vinorelbine (O'Brien et al, 2008). It is also being evaluated with carboplatin as first-line therapy in ovarian, peritoneal and fallopian tube cancer (Morgan et al, 2008). Neurotoxicity and hypersensitivity reactions led to early termination of a Phase II trial in with HER2negative metastatic breast cancer (Lin et al, 2007). Of the 20 patients with stage IV NSCLC, 2 exhibited a PR, and 13 exhibited SD at a dose of 175 mg/m2 as first-line monotherapy (Richards et al, 2005).

F. BMS-275183 BMS-275183 (Figure 33) is an orally administered C-4 methyl carbonate paclitaxel analogue able to induce growth suppression, cell-cycle arrest, and apoptosis. BMS275183 altered the expression of cell-cycle regulators, such as cyclin A and cyclin B1 whereas the expression of E2F and p27 was decreased and increased, respectively, in all HNSCC cell lines examined; the mechanism involved molecular pathways similar to other taxanes (Yoo et al, 2007). It showed promising activity in a phase I trial investigating a weekly treatment regimen, but was associated with a relatively high incidence of neuropathic side effects. Based on these results, a phase II trial in NSCLC has been initiated using the twice weekly schedule (Brรถker et al, 2006, 2007).

O O O

O O

O

H3C O

NH

S

H. Microtubule destabilizing agents

H

As of 2008 there were 17 microtubule destabilizing agents under clinical assessment, most in Phase I (Carlson, 2008). Table 2 gives a glimpse of new molecules under development destabilizing microtubules. It is worth mentioning that Stathmin 1 (STMN1), also known as metablastin, oncoprotein 18, LAP 18 and Op18, a 19 kDa cytosolic protein, is the first discovered member of a family of microtubule-destabilizing phosphoproteins critically involved in the construction and function of the mitotic spindle; its therapeutic manipulation has an anticancer potential (Rana et al, 2008).

O OH OH

O

H O

O

CH3 O

O

Figure 32. Structure of BMS-184476 O O O

O O

NH

IX. Prospects

OH

H3C O

Docetaxel and paclitaxel are highly active agents in metastatic breast cancer and may represent a safer alternative to anthracycline-based regimens when combined with the human epidermal growth factor receptor (HER)-2-targeted agent trastuzumab (Herceptin).

Results from two large, phase III trials that examined the addition of carboplatin to a taxane-trastuzumab doublet did not demonstrate a difference in survival with carboplatin. In one study, the addition of carboplatin to paclitaxel-trastuzumab therapy resulted in a higher response rate and longer progression-free survival time; in

H O OH OH

O

H O

O

O O

O

Figure 33. Structure of BMS-275183

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Boulikas and Tsogas: Microtubule-targeting anticancer drugs page O

O

O

HO H

H3C O

O

O NH

H

OH O

O

O

CH3

O O

O

O

O

O

O

H N

H N

a

b O

x HO

O

HO

O

Figure 34. Structure of Paclitaxel Polyglumex.

Table 2. Microtubule destabilizing agents Name

Active compound

Development stage

Onco-TCS

Liposomal Vincristine

Phase II/III

Cryptophycin 52

Derivative of Cryptophycin

LY355703

synthetic product structurally related to cryptophycin

Dolastatin-10

Dolastatin-10

Phase I phase II in in patients with platinum-resistant ovarian cancer and NSCLC Phase I/II in Metastatic Soft Tissue Sarcomas, pancreaticobiliary cancers and advanced breast cancer

Tasidotin (ILX651)

a peptide analogue of the antimitotic depsipeptide dolastatin 15

TZT-1027

synthetic dolastatin 10 derivative

ENMD-1198 combretastatin-A4phosphate (CA4P)

Reference Sarris et al, 2000; Gelmon et al, 1999 Teicher et al, 2000 Edelman et al, 2003; D'Agostino et al, 2006 von Mehren et al, 2004; Kindler et al, 2005; Perez et al, 2005

Phase II

Bai et al, 2008

novel tubulin-binding agent

Phase I & II in metastatic soft-tissue sarcomas and NSCLC Preclinical

Patel et al, 2006; Riely et al, 2007; Tamura et al, 2007; Horti et al, 2008 Moser et al, 2008

microtubule-targeting agent

Preclinical

Petit et al, 2008

a second study, the docetaxel-trastuzumab and docetaxeltrastuzumab-carboplatin combinations were equally effective (Bullock and Blackwell, 2008). Future studies may show better synergies in the various regimens for MBC as well as other cancers using other microtubuletargeted agents reviewed here.

Preclinical studies have shown that frequent administration in vivo of low doses of chemotherapeutic

drugs ("metronomic" dosing) can affect tumor endothelium and inhibit tumor angiogenesis with concomitant reduction in side effects even after chronic treatment. The continuous low-dose therapy with paclitaxel, 4-hydroperoxycyclophosphamide, the oral taxane BMS-275183, doxorubicin, epothilone B (EpoB) and its analogue 5-methylpyridine EpoB may have a

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Gene Therapy and Molecular Biology Vol 12, page 349 highly selective effect against cycling vascular endothelial cells (Bocci et al, 2002).

Most of the anticancer molecules described in this review have side effects. The side effects of paclitaxel include myelosuppression, mucositis, peripheral neuropathy, and cardiovascular toxicity. The side effects of docetaxel include myelotoxicity, allergic reactions during infusion, diarrhea, nausea / vomiting, and hair loss.

The side effects of vinblastine, vinorelbine, vincristine and vindesine include myelosuppression, constipation, diarrhea, nausea, peripheral neuropathy, and asthenia.

Encapsulation into liposome nanoparticles or entrapment into dendrimers and polymers is expected to lower side effects and improve tumor targeting in a way similar to that successfully attempted for cisplatin (Boulikas, 2007).

Albumin-bound paclitaxel 100 mg/m2 given weekly demonstrated the same antitumor activity as albuminbound paclitaxel 125 mg/m2 weekly and a more favorable safety profile in patients with metastatic breast cancer (MBC) that had progressed with previous taxane therapy; the carrier-mediated paclitaxel has already shown significant efficacy in taxane resistant cancers, an approach highly relevant in prostate cancer, where taxanes are the treatment of choice (Blum et al, 2007). Secondgeneration enhanced-delivery taxanes, including Tocosol Paclitaxel (Sonus Pharmaceuticals, Inc., Bothell, Washington) and paclitaxel poliglumex, use biocompatible drug delivery vehicles to eliminate the need for toxic conventional solvents and exploit tumor pathophysiological phenomena such as enhanced permeability and retention (Perez, 2007). Certainly drug delivery plays a major role especially nanoparticle formulations that are able to preferentially concentrate at tumor sites using imperfections in the endothelium of tumor vasculature. Our group has demonstrated targeting of liposomal cisplatin nanoparticles (Lipoplatin) in patients (Boulikas et al, 2005). A similar liposomal formulation of paclitaxel is at preclinical testing.

Nanotechnology promises to wrap up drugs and optimize in vivo delivery (Boulikas, 2007). Nanoparticles provide a new mode of cancer drug delivery functioning as a carrier for entry through fenestrations in tumor vasculature allowing direct cell access. Taxane delivery systems through tumor cell surface receptor-targeted delivery mechanisms such as small-molecule peptides and monoclonal antibodies, as well as those on non-targeted procedures such as liposomes, nanostructures, and natural and synthetic polymers hold promise for improving the toxicity profiles and biodistribution of the drug (Safavy, 2008; Haley and Frenkel, 2008). Other modifications including transferrin receptor and folate receptor targeted drug delivery molecules are emerging.

PEG2000-stearic acid was used to prepare PEGylated solid lipid nanoparticles loading vinorelbine bitartrate of a particle size of 180-250nm; octadecylamine-fluorescein isothiocynate was used as a fluorescence marker to incorporate into nanoparticles and study their cellular uptake (Wan et al, 2008). Poly(D,L-lactide-co-glycolide) (PLGA) was used to load the vinca alkaloid vinpocetine forming microparticles suited for intramuscular injection (Li et al, 2008). An ultrasonic-solvent emulsification

technique was adopted to prepare vinpocetine loaded Glyceryl monostearate (GMS) nanodispersions with narrow size distribution (Luo et al, 2006). PLGA nanoparticles of a size of 140 nm simultaneously loaded with vincristine sulfate and quercetin were prepared via oil/water emulsion solvent evaporation (Song et al, 2008).

Vinorelbine bitartrate (VB) was loaded into solid lipid nanoparticles (SLNs) of 150 to 350 nm by a cold homogenization technique; enhancement of lecithin content in lipid matrix resulted in smaller particle of SLNs (You et al, 2007). Nanoparticles allow exquisite modification for binding to cancer cell membranes, the microenvironment, or to cytoplasmic or nuclear receptor sites.

Intact plasma lipoproteins are complex macromolecules that transport highly water-insoluble compounds (cholesteryl esters and triacylglycerols) from the intestine to the liver through blood; this property renders them ideal carriers of hydrophobic drugs. Both low and high density lipoprotein-based formulations have been used as drug carriers (Lacko et al, 2007). One important factor to be taken into consideration in anticancer drug delivery using HDL is the promotion of angiogenesis by DHL, a property that may counteract the beneficial effect of the drug in the induction of tumor apoptosis (Chen et al, 2007). Spherical nanoparticles of reconstituted (synthetic) high-density lipoproteins (HDL) carrying paclitaxel have been reported with high drug to lipoprotein ratio with exceptional stability for up to 6 months. The nanoparticles had superior cytotoxicity against MCF7, DU145, OV1063 and OVCAR-3 cancer cell lines and their IC50 was 5-20 times lower than that of the free drug (McConathy et al, 2008).

Docetaxel arose from the natural compound paclitaxel by substitution of the benzyl- group by a tertbutoxy-group (Figure 7). Fluorination of the ethyl group in the vinblastine molecule at the 20' position of the catharanthine moiety led to the introduction of vinflunine (Figures 13 and 14). Other type of modifications could have given molecules of superior activity with lower side effects in human trials; however, because of the huge cost involved in testing so many substances into humans, the industry is limited in the number of molecules to be promoted and the decision on the molecules to be tested in clinical trials is based on preclinical studies that may not reflect the human experience.

Structural similarities can be used to further modify a successful anticancer drug in order to seek molecules of improved efficacy with lower toxicity or able to overcome tumor resistance of the prototype molecule; because of the complexity of the biological systems and the number of parameters that define a successful drug (its interaction with serum components, biodistribution, circulation time and urine or other route of excretion, interaction with cell surface molecules, entry across the cell membrane, resistance mechanisms, type of subcellular components it damages, induction of signaling pathways resulting to apoptosis and others) it is very difficult to predict effectiveness and side effects from mere chemistry. Trial and error on cell lines, animals and ultimately human patients remains the only way to test new molecules.

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Acknowledgements Supported by the European grants RIGHT: LSH-CT2005-005276, NanoBiopharmaceutics: NMP4-CT-2006026723 and MYASTAID: LSHM-CT-2006-037833, to Regulon AE as well as two grants from the Hellenic government (General Secretariat of Research and Development) for the clinical development of Lipoplatin, Lipoxal and LipoVIL12. We are grateful to Alexandros Magos, Petros Christofis, Alexandros Pantos and Evagelos Bellis for stimulating discussions.

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From left to right: Teni Boulikas and Ioannis Tsogas

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Gene Therapy and Molecular Biology Vol 12, page 359 Gene Ther Mol Biol Vol 12, 359-370, 2008

Gene expression signature-based chemical genomics and activity pattern in a panel of tumour cell lines propose linalyl acetate as a protein kinase/NF-!B inhibitor Research Article

Saadia Bashir Hassan1,*, Elin Lindhagen1, Hanna Göransson1, Mårten Fryknäs1, Anders Isaksson1, Hala Gali-Muhtasib2, Rolf Larsson1 1 2

Division of Clinical Pharmacology, Department of Medical Sciences, University Hospital, SE-751 85 Uppsala, Sweden Department of Biology, American University of Beirut, Lebanon

__________________________________________________________________________________ *Correspondence: Saadia Bashir Hassan, Division of Clinical Pharmacology, Department of Medical Sciences, University Hospital, 751 85 Uppsala, Sweden; Tel: +46 18 611 93 81; Fax: +46 18 51 92 37; e-mail: sadia.hassan@medsci.uu.se Key words: Linalyl acetate, NF-!B, Connectivity Map Abbreviations: American Type Culture Collection, (ATCC); chronic lymphocytic leukaemia, (CLL); fluorescein diacetate, (FDA); Fluorometric Microculture Cytotoxicity Assay, (FMCA); glutathione, (GSH); heat-inactivated fetal calf serum, (FCS); inhibitory concentration 50%, (IC50); multi-drug resistance, (MDR); multidrug-resistance protein, (MRP); normal mononuclear cells, (PBMCs); Nuclear factor-"B, (NF-!B); P-glycoprotein 170, (Pgp); phosphate-buffered saline, (PBS); robust multi-array average, (RMA); survival index, (SI); topoisomerase II, (TopoII); Tumour Necrosis Factor-#, (TNF#) Received: 18 September 2008; Revised: 28 October 2008 Accepted: 7 November 2008; electronically published: December 2008

Summary The essential oil of Lebanese sage, Salvia libanotica, was reported to have anti-tumour activity; however, the mechanism of action has not been identified yet. In this study, 14- cancer cell lines including drug-sensitive and resistant lung, leukaemia, and colon, as well as primary human tumours of chronic lymphocytic leukaemia (CLL) and primary normal mononuclear cells (PBMCs) were used to characterize the anti-tumour activity and mechanism of action of linalyl acetate, a component of the Lebanese sage essential oil. Drug activity and gene expression data sets were utilized to identify drugs with similar activity patterns and genes involved in drug sensitivity/resistance. In addition, the Connectivity Map, a gene expression signature-based screening approach, assisted in predicting further the molecular action of linalyl acetate. Small cell lung carcinoma and colorectal cancer cell lines were the most sensitive to the drug and greater tumour selectivity was observed against chronic lymphocytic leukaemia cells compared to normal mononuclear cells. Only limited effect of some of the classical mechanisms of multi-drug resistance on the activity of Linalyl acetate was noted which makes it potentially interesting for drug-resistant patients. There was high similarity between the activity-pattern/gene expression profile of linalyl acetate and that of protein kinase/NF-!B inhibitors. Validating this, linalyl acetate was found to strongly inhibit Janus kinase, JAK3, and p38" kinases in a cell-free assay as well as the NF-!B translocation in a dose-dependent manner. Taken together, our results show that the NF-kB inhibitor, linalyl acetate, may represent a new therapeutic compound in the management of inflammation and cancer.

anti-tumour activities (Liu et al, 2000; Fiore et al, 2006).

Water extracts of Salvia libanotica (also known as Salvia triloba or three-lobed sage), a plant endemic to the Eastern Mediterranean, have been used by local populations to cure many health problems such as abdominal pain, indigestion, headaches and respiratory problems (GaliMuhtasib et al, 2000). The oil extract of this plant has

I. Introduction Herbs have been considered natural and valuable sources for anti-cancer drug discovery. Nowadays, many of the drugs that have been used for treatment of malignant diseases are derived from natural products. The genus Salvia, a herbal plant comprised of numerous species, has shown diverse biological activities including 359

Hassan et al: Linalyl acetate as a protein kinase/NF-!B inhibitor resistant ACHN (renal adenocarcinoma). All cells were grown in culture medium RPMI-1640. Four colorectal cell lines, HCT-8, SW620, HCT-116 and HT-29 were obtained from American Type Culture Collection (ATCC, Manassas, VA) and were cultured in RPMI-1640, Leibovitz’s L-15, McCoy’s and Dulbecco’s Modified Eagle’s media, respectively. The breast cancer epithelial cell line, MCF7 and the human cervix (Hela) cell lines obtained from ATCC, were cultured in DMEM deprived of phenol red and Eagle’s Minimal Essential medium with 1 mM sodium pyruvate, respectively. All cell lines were supplemented with 10% heat-inactivated fetal calf serum (FCS), 2 mM glutamine, 100 µg/ml streptomycin and 100 IE/ml penicillin (all from Sigma Aldrich Co, St Louis, MO, USA) and incubated at 37°C in humidified air containing 5% CO2. The resistant cell lines were tested regularly for maintained resistance to the selected drugs. Growth and morphology of all cell lines were monitored on a weekly basis.

strong anti-microbial properties (Hilan, 1997) and was found to suppress the formation of skin papillomas in a mouse model as well as exert anti-inflammatory effects on the skin of treated mice (Gali-Muhtasib and Affara, 2000).

Twelve components were identified in the essential oil of Salvia libanotica (Farhat et al, 2001), three of which were found to exert potent anti-proliferative effects on a panel of cancer and normal cell lines (Hala Gali-Muhtasib unpublished data). Linalyl acetate, one of those three components, belongs to the terpenoid family of compounds. This compound is the acetate ester of the unsaturated acyclic monoterpene alcohol, the linalool (Figure 1). Linalyl acetate is the principal component of many essential oils from herbal plants such as lavender, cardamom and common thyme. Linalyl acetate has been shown to be cytotoxic to human skin cells, endothelial cells and fibroblasts (Prashar et al, 2004) and has shown, in combination with two sage components, to have antitumour activity against colon cancer cell lines (Itani et al, 2008). In addition, linalyl acetate has been ascribed antiinflammatory (Peana et al, 2002), anti-bacterial (Trombetta et al, 2005), and anti-fungal activities (Barra et al, 2007) and it is used in aromatherapy and in the flavouring and fragrance industries.

In an effort to characterize the anti-tumour activity of new substances and to elucidate their mechanism of action several approaches have been proposed. Drug-response analysis in a panel of cell lines has proven to be an important tool in anti-cancer drug discovery and early evaluation. The patterns of drug activity across cell lines can provide information on mechanisms of drug action (Paull et al, 1989; Boyd, 1995; Dhar et al, 1996). The development of molecular technologies, such as expression micro-arrays, has made it easier to identify genes involved in chemo-sensitivity, while integration of gene expression and drug activity data sets can identify genes involved in drug sensitivity or resistance to specific drugs (Scherf et al, 2000; Rickardson et al, 2005).

Recently, the gene expression signature-based screening approach, the Connectivity Map, has been developed as a new tool that relies on genes to connect diseases with potential therapeutic drugs and to predict how new drugs function in cells. The map has the ability to accurately predict the molecular actions of novel therapeutic compounds and has also shown that genomic signatures can be used to recognize drugs with common mechanisms of action as well as to discover unknown mechanisms of action of existing drugs (Hieronymus et al, 2006; Lamb et al, 2006; Wei et al, 2006).

In this study, we characterized the anti-tumour activity of linalyl acetate and investigated its mechanisms of action.

B. Primary human tumour and normal mononuclear cells Tumour cell samples were obtained from two patients with chronic lymphocytic leukaemia (CLL). The patient samples were obtained from peripheral blood sampling and leukaemia cells were isolated from the blood by density gradient centrifugation on 1.077 g/ml Ficoll-Paque (Pharmacia Biotech, Uppsala, Sweden) gradient. CLL patients were previously treated with standard cytotoxic drugs. Cell viability was determined by trypan blue exclusion test and the proportion of tumour cells in the preparation was judged by inspection of May-Grunwald-Giemsastained cytospin preparations by a haematologist. Cell culture medium RPMI 1640 (supplemented as described above) was used throughout. Normal mononuclear cells (PBMCs) from two healthy donors were collected and prepared in the same way as leukaemia samples.

C. Linalyl acetate concentration and drugplate preparation Linalyl acetate (Acros, Belgium) was tested in duplicate at 8 concentrations from a maximum of 50 mM using 2-fold serial dilutions in phosphate-buffered saline (PBS; pH 7.4 Hyclone).

384-well microtitre plates (Nunc, Roskilde, Denmark) were prepared with 5 µl drug solutions at 10 times the final drug concentration using the pipetting robot BioMek 2000 (Beckman Coulter, Fullerton, CA).

D. Viability assays Tumour cells from the cell line panel (5000 cells per well), and from CLL and PBMCs (50000 cells per well), were seeded separately in the drug-prepared 384-well plates using the pipetting robot Precision 2000 (Bio-Tek Instruments Inc., Winooski, VT, USA). Three columns without drugs served as controls and one column with medium only served as blank.

II. Material and Methods A. Cell line cultures The panel of ten human cancer cell lines has been described previously (Dhar et al, 1996). The panel consists of the parental cell lines RPMI 8226 (myeloma), CCRF-CEM (leukaemia), U937-GTB (lymphoma) and NCI-H69 (small-cell lung cancer); the drug-resistant sub-lines 8226/Dox40, 8226/LR5, CEMVM-1, U937-vcr, H69AR and the primary

Figure 1. Linalyl acetate structural formula.

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Gene Therapy and Molecular Biology Vol 12, page 361 The plates were incubated at 37°C for 72 h and were then analyzed using the fluorometric microculture cytotoxicity assay (FMCA). Three repeated experiments were performed where cell preparation, drug preparation as well as FMCA analysis were performed independently.

Technologies, Wilmington, DE) and RNA quality was evaluated using the Agilent 2100 Bioanalyzer system (Agilent Technologies Inc, Palo Alto, CA). Total RNA (2 µg) from each sample were used to prepare biotinylated fragmented cRNA according to the GeneChip® Expression Analysis Technical Manual (Rev. 5, Affymetrix Inc., Santa Clara, CA). Affymetrix GeneChip® expression arrays (Human Genome U133 Plus 2.0 Array) were hybridized for 16 h in a 45°C incubator, rotated at 60 rpm. According to the GeneChip® Expression Analysis Technical Manual (Rev. 5, Affymetrix Inc., Santa Clara, CA), the arrays were then washed and stained using the Fluidics Station 450 and scanned using the GeneChip® Scanner 3000 7G.

E. The fluorometric microculture cytotoxicity assay (FMCA) and quantification of results The fluorometric microculture cytotoxicity assay (FMCA), described in detail previously (Larsson et al, 1992; Rickardson et al, 2005), was performed to measure cell survival. The method is based on measurement of fluorescence generated from hydrolysis of fluorescein diacetate (FDA) to fluorescein by cells with intact plasma membranes. After 72 h incubation at 37°C, medium and drugs were aspirated, the cells were washed twice with PBS, 50 $l of physiological buffer and 1 $l of 0.5 mg/ml FDA were added and after 50-70 min of incubation, the fluorescence, which is proportional to the number of living cells, was measured at 485/520 nm in the FLUOstar Optima. Cell survival was presented as survival index (SI) defined as fluorescence in test wells as a percentage of that in control wells, with blank values subtracted. Quality criteria for a successful assay included a mean coefficient of variation of less than 30% in the control and a fluorescence signal in control wells of more than five times the signal in the blank wells.

I. Connectivity Map data analysis The raw data was normalized using the robust multi-array average (RMA) method (Irizarry et al, 2003). Genes were then ranked according to the expression differences compared to the vehicle-treated control, and the 100 genes that increased or decreased most compared to the vehicle-treated control were used as “signatures” in the next step of analysis. To investigate the target activity of our compound, we used an approach to connect the activity of linalyl acetate to drugs with known biological activities at the gene expression level (Lamb et al, 2006). The current version of the Connectivity Map data set contains genome-wide expression data for 6100 treatment and vehicle control pairs, representing 1309 distinct small molecule bioactive compounds (perturbagens), www.broad.mit.edu/cmap.

Enrichment of both the up- and down-regulated genes from a given signature in the profiles of each treatment instance were estimated as described (Lamb et al, 2006) and combined to produce a “connectivity score.” Instances were then ranked in descending order of connectivity score. A 6 h treatment time was chosen to capture the primary and potentially mechanistic effects of the compounds.

F. FMCA data evaluation Data from all three experiments were processed using GraphPad Prism (GraphPad Software, Inc. San Diego, CA) with non-linear regression to a standard sigmoidal dose-response model. Maximum effect and baseline were set at 0% and 100% cell survival, respectively, and IC50 (inhibitory concentration 50%) was estimated. When the exposure to the test substance resulted in less than 50% reduction in cell survival in all of the concentration ranges tested, the IC50 was set to the lowest concentration used.

K. Kinase profiling Linalyl acetate kinase profiling was performed, in a cellfree system, against the SelectScreenTM kinase panel of 50 key kinase targets from Invitrogen (SelectScreen Kinome Sampler Panel) at a single concentration of 6.25 mM. The kinases were selected to broadly cover the kinome and to provide a good approximation of compound potency. The assays were performed according to the Screening Protocol and Assay Conditions of Invitrogen www.invitrogen.com. Briefly, the Z’-LYTE TM biochemical assay employs a fluorescence-based, coupledenzyme format and is based on the differential sensitivity of phosphorylated and non-phosphorylated peptides to proteolytic cleavage.

10-points titration curves in a cell free system, obtained from a maximum of 18.75 mM by 3-fold serial dilution, to identify the IC50 of the linalyl acetate inhibitory effect on JAK3, AKT1 and IKK& activity, were performed. ATP was used at a concentration of 10 µM in all kinase assays except for Kit, MAP2K1, MAPK14, MAPK8 and NTRK1 where the concentration was 100 µM.

G. Drug and gene expression database A total of 400 standard drugs with known mechanism of action representing different mechanistic groups and investigational substances were tested in the panel of 10 tumour cell lines using the 72 h FMCA, and their IC50s were estimated and included in the database.

The cell lines from the 10 cell lines panel were analyzed for gene expression using cDNA microarrays as described in detail previously (Rickardson et al, 2005). The arrays, which contained 7409 cDNA clones included in the Human Sequence Verified Set, were obtained from Research Genetics (Huntsville, AL, USA). A complete list of genes printed on the arrays is available at http://www.medsci.uu.se/klinfarm/arrayplatform/cDNAgenelist.h tm. The drug and gene expression databases were integrated (Rickardson et al, 2005) and a correlation analysis was performed. Pearson's correlation coefficients for all the drugdrug (log10 IC50) and drug-gene correlations (log10, log2) were calculated. A correlation coefficient %0.7 was used to identify the drugs that correlated with linalyl acetate activity and % ±0.7 was chosen to extract the genes associated with its resistance and sensitivity. Resistance factors were defined as IC50 values in the resistant subline divided by IC50 values in the parental cell line.

L. Nuclear factor-!B translocation Hela cells (1500 cells/90 µl/well) were seeded in standard black 96-well clear bottom microplates (Packard ViewPlate®, Packard USA) and left to adhere overnight before the addition of 10 µl of test compounds. In a preliminary experiment, Hela cells were exposed either to 6.25 mM linalyl acetate or 2.5 µM celastrol, which was obtained from commercial sources. The plate was incubated for 2 h at 37°C. In the second experiment, linalyl acetate was tested at 5 concentrations from a maximum of 6.25 mM using 2-fold serial dilutions. Rottlerin, MG-132 and 15' prostaglandin J2 were obtained from commercial sources and

H. Microarray expression analysis MCF7 cells were treated with PBS, 25 mM linalyl acetate or with vehicle for 6 h in RPMI-1640 with 10% FCS. RNA was isolated using Qiagen columns (Qiagen GmbH, Hilden, Germany). RNA concentration for the two samples was measured using an ND-1000 spectrophotometer (NanoDrop

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Hassan et al: Linalyl acetate as a protein kinase/NF-!B inhibitor tested at 100, 20 and 10 µM, respectively. The plate was incubated for 4 h at 37°C. All concentrations were tested in triplicate. At the end of the incubation times, treated cells and positive control cells were stimulated with 50 ng/ml of Tumour Necrosis Factor-# (TNF#) for 30 min. Negative control cells were used as a reference to quantify the extent of baseline NF-!B translocation in the cell line studied.

NF-!B translocation into the nucleus was evaluated using the NF-!B Activation HCS HitKit™ (High Content Screening, obtained from Cellomics, Inc. USA.) utilizing the ArrayScan® HCS reader (Cellomics, Inc. USA) as described earlier (Ding et al, 1998). The ArrayScan® reader automatically quantifies the mean nucleus-cytoplasm intensity difference of the amount of p65 immunofluorescence staining in a predefined number of cells (500 cells/well). The mean nucleus-cytoplasm intensity difference was presented as NF-!B translocation %, defined as the mean nucleus-cytoplasm intensity difference in the experimental wells as a percentage of that in control wells.

To determine the cytotoxicity of linalyl acetate in parallel to NF-!B translocation analysis, 96 -well microtiter plates (Nunc, Roskilde, Denmark) were prepared with 20 µl per well of drug solution at ten times the desired concentration. Linalyl acetate was tested at 5 concentrations from a maximum of 12.5 mM using 2-fold serial dilutions. Each concentration was prepared in triplicate. Hela cells were seeded at 20 000 cells /180 µl and the plates were incubated at 37°C for 72 h and at the end of the incubation period, the cell survival was determined with the FMCA as described above.

(CLL) than in normal mononuclear cells from healthy donors (PBMCs) (Figure 2b). The tumour selectivity ratio, the ratio between the mean IC50 in PBMC and CLL for linalyl acetate, was found to be around 6.

The cytotoxicity of some of the standard agents confirmed the known resistance pattern of the drug resistant sublines (Lindhagen et al, 2007) (Table 1).

Overall, the resistance factors for linalyl acetate were low.

The greatest difference in sensitivity between a parental line and its subline was observed for H69 and its subline H69AR with a ratio exceeding 4. Resistance factors around 3 were observed for resistance associated with Pgp and GSH. With respect to log IC50 patterns, the closest matches to linalyl acetate activity found in the drug activity database were the cardiac glycoside, lanatoside C, the tyrosine kinase inhibitor, PKC412 and the phenothiazine derivative, calmodulin inhibitor, thioridazine. The cardiac glycosides and the calmodulin inhibitors are reported to inhibit NF-!B while PKC412 is a known multi-target kinase inhibitor. In addition, linalyl acetate showed correlations to compounds whose mechanism of action is not clearly defined (Table 2). The clinically used agents vincristine, melphalan, cytarabine, topotecan and doxorubicin generally showed lower negative correlations compared to the activity pattern of linalyl acetate.

Using the drug activity-gene expression correlations, 83 genes were identified for linalyl acetate that correlated to resistance (r>0.7) and 160 correlated to sensitivity (r<0.7). For the genes identified, the distribution of Gene Ontology (GO) terms was investigated using a hypergeometric test (one-sided p value<0.05) (Ameur et al, 2006). In terms of associated biological processes, both groups of genes correlating to resistance and sensitivity showed an over-representation of several processes.

Considering the genes associated with these overrepresented biological processes there were 68 genes for linalyl acetate sensitivity (supplement 1). These biological processes involved cell cycle, mitotic cell cycle, DNA repair and negative regulation of cell proliferation.

III. Results Among the 14 cell lines tested, the small cell lung carcinoma cell line, NCI-H69, and the colorectal cancer cell lines, HCT-116 and HCT-8, were the most sensitive to linalyl acetate (IC50 was set to 0.2 mM, see Materials and Methods). The small cell lung carcinoma subline, H69AR, and the myeloma RPMI 8226/S cell lines were also sensitive (IC50: 0.8 and 2.4 mM, respectively) (Figure 2a).

The IC50 in mM of the remaining cell lines were as follows: CCRF-CEM (4.3), CEMVM-1 (4.5), U937-GTB (4.8), SW620 (4.9), U937-vcr, (5.7), ACHN (7.1), 8226/Dox40 (7.9), 8226/LR5 (8.8) and HT-29 (16.4).

Linalyl acetate showed higher activity in tumour cells from chronic lymphocytic leukaemia patient samples

Figure 2. Effect of linalyl acetate, as individual dose response curves assayed by the FMCA, on: (a) the small-cell lung, the colon and the myeloma human cancer cell lines (b) chronic lymphocytic leukaemia, CLL, (n=2) and normal mononuclear cells, PBMCs, (n=2).

Data are represented as mean survival index ± SEM.

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Gene Therapy and Molecular Biology Vol 12, page 363 Table 1 Influence of resistance mechanisms on cytotoxic potency of linalyl acetate, and five standard cytotoxic agents in the cell line panel.

Parental cell line Resistant subline Resistance factor linalyl acetate doxorubicin* vincristine* melphalan* cytarabine* cisplatin*

TopoII-associated MDR

MRP-associated MDR

Pgp-associated MDR

GSH-associated MDR

Tubulinassociated MDR

CCRF-CEM

NCI-H69

RPMI 8226

RPMI 8226

U937-GTB

CEM/VM-1

H69AR

8226/Dox40

8226/LR-5

U937/Vcr

1.0 5.6 1.0 1.1 1.0 0.71

>4 33 27 0.55 1.0 0.89

3.3 43 398 3.2 1.0 4.7

3.6 0.61 1.1 3.5 0.03 1.1

1.2 2.0 61 1.6 0.89 1.4

The resistance factor was defined as the IC50 value in the resistant subline divided by that in its parental cell line. TopoII; topoisomerase II, MDR; multi-drug resistance, MRP; multidrug-resistance protein, Pgp; P-glycoprotein 170, GSH; glutathione. * Resistance factor values were from (Lindhagen et al, 2007).

Table 2 Correlation between the activity pattern of linalyl acetate and drugs from the drug database with Pearsonâ&#x20AC;&#x2122;s correlation coefficient > 0.7 and 5 of the standard cytotoxic drugs and their proposed mechanism of action. drug

Classification

Pearsonâ&#x20AC;&#x2122;s correlation coefficient

lanatoside C

cardiac glycoside, NF- !B inhibitor, antiinflammatory protein kinase inhibitor herbicide antifungal antipsychotic, calmodulin inhibitor, antiinflammatory, cyclooxygenase 2/lipoxygenase inhibitor. platinum compound alkylating agent antimetabolite topoisomerase I inhibitor topoisomerase II inhibitor

0.91

PKC412 acetochlor cetrimonium thioridazine

vincristine melphalan cytarabine topotecan doxorubicin

0.85 0.76 0.74 0.71

-0.5 -0.17 -0.29 -0.44 -0.16

Pearsonâ&#x20AC;&#x2122;s correlation coefficient between the log IC50s of the ten cell lines is shown.

To further classify the mechanism of action of linalyl acetate, its gene expression profile (signature) was defined in order to use the Connectivity Map database. The Connectivity Map database was used to identify drugs with high similar gene expression profiles to that of linalyl acetate (linalyl acetate query signature is provided as supplement 2). The up- and down-regulated genes obtained from affymetrix expression analysis of linalyl acetate effect on the breast cancer cell line, MCF7, showed association to several biological processes involving apoptosis and cell cycle. To use the Connectivity Map, we loaded the linalyl acetate query signature to the database and executed the query of substances that induce the biological state represented by the linalyl acetate

signature. To develop hypotheses on the mechanism of action of linalyl acetate we scanned the first 100 instances, out of the 6100 instances of the Connectivity Map resources, at the top of the list. High connectivity scores were found for multiple instances of a several perturbagens in which protein kinase/ NF-!B and calmodulin inhibition contributes to their anti-tumour activity. Next we examined the rank of the identified perturbages according to the permutation P value (an estimate of the likelihood that the enrichment of a set of instances in the list of all instances in a given result would be observed by chance). Most of the identified perturbagens with high connectivity scores were ranked below 50 out of all 1309 bioactive compounds of the 363

Hassan et al: Linalyl acetate as a protein kinase/NF-!B inhibitor Connectivity Map resources (permutation P value ranged between 0.00000-0.001). Given these results we considered the 50 highest ranking perturbagens to be likely relevance in the hypothesis generation process.

Analysis of the 50 highest ranking perturbagens resulted in identification of many other agents that protein kinase/ NF-!B inhibition contributes to their anti-tumour activity.

Generally, JAK, p38 MAPK, AKT1 and IKK kinases were shown to be inhibited by these perturbagens (Table 3).

To test the hypothesis that linalyl acetate is acting on the protein kinase and/or NF-!B pathways, in vitro protein kinase profiling and an NF-!B assay were performed.

The single concentration percent inhibition determinations of each kinase are presented in Table 4.

Linalyl acetate was found to strongly inhibit JAK3, MAPK14 (p38#), NEK1 and showed a tendency to inhibit other kinases including AKT1, IKK& and MAPKAPK2 kinases. The concentration- inhibition effect curves of the linalyl acetate on JAK3, AKT1 and IKK& activity in a cell-free system are displayed in Figure 3a. The percent inhibition in the activities of these kinases with linalyl acetate concentrations had the tendency to have the

classical sigmoid shape which was more evident with JAK3 activity although the titrations were not carried out to saturation under the concentration range tested. The IC50 value of the inhibitory effect of linalyl acetate on JAK3 kinase was 0.8 mM. The NF-!B assay showed that exposure of Hela cells to linalyl acetate inhibited TNF#-induced NF-!B translocation into the nucleus (Figure 3b). The 2 h exposure to celastrol (2.5 µM) and the 4 h exposure to rottelrin (100 µM), MG 132 (20 µM) and 15-' prostaglandin J2 (10 µM) resulted in 10%, 22%, 27% and 55% of the TNF#-induced NF-!B translocation, respectively. The survival of Hela cells was inhibited by 72 h exposure to linalyl acetate. A concentrationdependent decrease in NF-!B translocation and SI % followed by a tendecy to blateau was observed. The decrease in NF-!B translocation seems to be time dependent as well. The potency of linalyl acetate in the NF-!B translocation and cell survival assays were in the same range (Figure 3b).

Table 3 The top perturbagens, among the 50 highest ranking perturbagens, identified through the Connectivity Map in which protein kinase/ NF-!B and calmodulin inhibition contributes to their anti-tumour activity.

Connectivity Map name (n)1

maximum connectivity score2

Rank3

description

rottlerin (3)

1.000

17

phenoxybenzamine (4) thioridazine (20) pyrvinium (6) calmidazolium (2) clioquinol (5) MG-262 (3) prochlorperazine (16) Gossypol (6) 15-' prostaglandin J2 (15) resveratrol (9) trifluperazine (16) fluphenazine (18) tanespimycin (62) geldanamycin (15) withaferin A (4) valinomycin (4) trichostatin A (182) alvespimycin (12) vorinostat (12) lanatoside C (4) LY-294002 (61) helveticoside (4) sirolimus (44) digoxin (4)

0.985 0.979 0.916 0.858 0.851 0.821 0.807 0.799 0.789 0.774 0.759 0.748 0.728 0.706 0.700 0.696 0.573 0.554 0.543 0.534 0.529 0.520 0.498 0.490

1 6 2 30 23 43 7 33 28 46 9 24 10 8 21 19 11 36 25 15 12 16 39 40

NF-!B, p38 MAPK, IKK, MAPKAPK2, and Ca/calmodulin-dependent kinase II inhibitor calmodulin inhibitor calmodulin inhibitor, anti-inflammatory Akt kinase inhibitor calmodulin inhibitor NF-!B, proteasome inhibitor NF-!B, proteasome inhibitor calmodulin inhibitor, anti-inflammatory Akt kinase inhibitor JAK, I!B kinase, NF-!B inhibitor JAK, I!B kinase, NF-!B inhibitor calmodulin inhibitor, anti-inflammatory calmodulin inhibitor, anti-inflammatory Hsp90 inhibitor Hsp90 inhibitor, NF-!B inhibitor NF-!B inhibitor Akt, p38 MAPK kinase inhibitor HDAC, Akt, NF-!B inhibitor Hsp90 inhibitor HDAC, NF-!B inhibitor cardiac glycoside, NF- !B inhibitor Akt, PI3, NF-!B inhibitor cardiac glycoside, NF- !B inhibitor Akt, NF-!B, mTOR inhibitor cardiac glycoside, NF- !B inhibitor

1

the number of all treatment instances of the perturbagen (n) Maximum connectivity score among all treatment instances 3 Rank according to permutation P value 2

364

Gene Therapy and Molecular Biology Vol 12, page 365 Table 4 Inhibition of protein kinases activity by 6.25 mM linalyl acetate. Results are presented as % inhibition of kinase (average of duplicate determination). ATP was 10 µM in all assays except for Kit, MAP2K1, MAPK14, MAPK8 and NTRK1 where it was 100 µM. kinase tested

% inhibition

kinase tested

% inhibition

ABL1 ACVR1B (ALK4) AKT1 (PKB #) AMPK A1/B1/G1 AURKA (Aurora A) BTK CDK1/cyclin B CHEK1 (CHK1) CSNK1G2 (CK1 ( 2) CSNK2A1 (CK2 # 1) DYRK3 EGFR (ErbB1) FGFR1 FLT3 FRAP1 (mTOR) GSK3B (GSK3 &) IGF1R IKBKB (IKK &) INSR IRAK4 JAK3 KDR (VEGFR2) KIT LCK MAP2K1 (MEK1)

3 6 23 26 20 34 9 15 4 2 4 4 9 7 1 11 4 18 0 -2 78 2 -8 0 15

MAP4K4 (HGK) MAPK1 (ERK2) MAPK14 (p38 ") MAPK8 (JNK1) MAPKAPK2 MARK2 NEK1 NTRK1 (TRKA) PAK4 PDGFRB (PDGFR &) PHKG2 PIM1 PLK1 PRKACA (PKA) PRKCA (PKC #) PRKCB1 (PKC & I) PRKCG (PKC () PRKCD (PKC ') RET ROCK1 RPS6KA3 (RSK2) RPS6KB1 (p70S6K) SRC SYK TEK (Tie2)

20 2 61 18 32 1 65 -4 3 -4 2 7 15 -4 10 1 13 -1 -3 14 6 13 -11 13 15

Negative values indicate that linalyl acetate was inactive.

Figure 3. Effect of different concentrations of linalyl acetate on (a) JAK3, AKT1 and IKK& kinases activity in a cell-free system presented as inhibition % (b) on the TNF# induced NF-!B translocation and cell survival of the human cervix (Hela) cell line. Data for cell survival are represented as mean ± SEM.

tumour cell lines than to the other tumour cell lines and is more active against CLL cells compared to PBMC cells, indicating possible tumour selectivity. The potential tumour selectivity of the sage component is interesting, and major toxicity in circulating normal lymphocytes might not be expected if linalyl acetate is tested clinically.

IV. Discussion The approaches we used in the work presented here identified protein kinases and/or NF-!B inhibition as a possible mechanism for linalyl acetate cytotoxicity. Here we show that linalyl acetate is more cytotoxic, at low concentrations, to the colon and small-cell lung human 365

Hassan et al: Linalyl acetate as a protein kinase/NF-!B inhibitor The relatively limited effect of the classical mechanisms of resistance represented in the panel on the cytotoxic efficacy of linalyl acetate makes the compound potentially interesting for patients with drug resistant tumours.

Previous studies on the panel of the 10 cell lines have shown that drug activity patterns can be used to classify anti-cancer drugs according to mechanism of action and this classification matched identifiable patterns of gene expression (Dhar et al, 1996; Rickardson et al, 2005).

When comparing the activity pattern of linalyl acetate with the activity of the drugs in the database, the low correlations seen between linalyl acetate and the standard cytotoxic agents from pharmacologically distinct groups suggest that the libanese sage essential oil compound may act by mechanism(s) different from those of clinically established agents. Lanatoside C, PKC412 and thioridazine are agents with response patterns in the cell line panel closely resembling that of linalyl acetate. It has been proposed that NF-!B inhibition is one of the mechanisms through which cardiac glycosides and calmodulin inhibitors exert their cytotoxicity. Structurally related cardiac glycosides such as digitoxin and UNBS1450 have been previously reported to inhibit NF!B activity in tumour cells (Yang et al, 2005; Mijatovic et al, 2006). There have been no published reports on the mechanism of action of lanatoside C in cancer cells, but interestingly, the activity pattern of lanatoside C in the ten cell lines panel has been shown to correlate with the activity pattern of other structurally related cardiac glycosides such as digoxin and digitoxin (Johansson et al, 2001). Thioridazine, a phenothiazine derivative, is a potent calmodulin inhibitor (Mylari et al, 1990) and phenothiazine derivatives have been reported to have antiinflammatory activity (Mylari et al, 1990). Inhibitors of calmodulin have been reported to prevent NF-!B activation (Hughes et al, 1998; Shumway et al, 2002). The third agent, PKC412, a staurosporine derivative, is known as a multi-target protein kinase inhibitor that has among its targets AKT kinase (Bahlis et al, 2005). This result thus suggests a potential similarity in mechanism of action between linalyl acetate and these agents.

The gene expression signature-based screening approach, the Connectivity Map developed by Lamb and others, has been shown to accurately predict the molecular actions of novel therapeutic compounds and to suggest ways in which existing drugs can be newly applied to treat diseases such as cancer (Hieronymus et al, 2006; Lamb et al, 2006; Wei et al, 2006). The approach is based on the similarity of a compound-induced signature to signatures of existing drugs with known mechanism. Using this approach, we were able to better predict the mechanism of action of linalyl acetate. The Connectivity Map revealed a strong connection between linalyl acetate and protein kinase/NF-!B inhibitors such as rottelrin, pyrvinium, clioquinol, MG-262, gossypol, 15-' prostaglandin J2, resveratrol, geldanamycin, trichostatin A, LY-29400 2, valinomycin withaferin A, vorinostat, and sirolimus an observation far beyond that expected by chance (permutation p-value 0.00000-0.001). These inhibitors have been reported to inhibit JAK (Park et al, 2003; Sallman et al, 2007), p38 MAPK (Han and Im, 2008; Ravi

et al, 2008) and AKT (Esumi et al, 2004; Chen et al, 2005; Denlinger et al, 2005; Dan et al, 2008; Han and Im, 2008; Moon et al, 2008) kinases as well as the NF-!B (Rossi et al, 2000; Ding et al, 2005; Zavrski et al, 2005; Imre et al, 2006; Yao et al, 2006; Kaileh et al, 2007; Yu et al, 2007; Torricelli et al, 2008; Crevecoeur et al, 2008). In addition, the results demonstrated a strong connection to other substances known as calmodulin inhibitors such as phenoxybenzamine, calmidazolium and the phenothiazine derivatives, thioridazine, prochlorperazine, trifluoperazine and fluphenazine. Three cardiac glycosides, lanatoside C, helveticoside and digoxin were also identified to be best connected to linalyl acetate signature. As discussed earlier in this article, calmodulin inhibitors and cardiac glycosides have been shown to prevent NF-!B activation (Hughes et al, 1998; Shumway et al, 2002; Yang et al, 2005; Mijatovic et al, 2006).

Our data thus suggested that linalyl acetate has protein kinase and NF-!B inhibiting properties, which warranted further evaluation. This hypothesis was confirmed in the subsequent preliminary mechanistic studies performed in this work.

Kinases regulate many different processes such as cell proliferation, differentiation and cell signaling. Our data shows that linalyl acetate had induced strong inhibition of JAK3, NEK and MAPK14 (p38#) kinases in a dose-dependent manner in cell-free system. In addition, linalyl acetate had moderate inhibitory activity to AKT1 (45%) and IKK& (36%) kinases. Janus kinase (JAK) is an intracellular kinase that regulates signalling pathways activated by a variety of cytokines and its activation results in the activation of the transcription factors STAT (signal transducers and activators of transcription). Several neoplastic diseases including colon cancer have been reported to involve JAK3 activation and targeting JAK3 may be useful for the treatment of colon cancer (Lin et al, 2005; Uckun et al, 2007). MAPK14 (p38#) is another kinase that was inhibited by linalyl acetate. MAPK14 (p38#) is one of the essential kinases for the fate of colorectal cancer cells and its blockade causes growth arrest and cell death (Comes et al, 2007). Interestingly, the colorectal cancer cell lines were the most sensitive tumour cells to linalyl acetate. The concentrations of linalyl acetate that inhibited the protein kinases were in the same range as those that induced cytotoxicity in the different tumour types tested, however in the current study, the protein kinase assays were performed in a cell-free system and it is presently unknown whether the inhibition of the protein kinases is connected to the decreased cell viability.

Further experimental data on living cells is needed to have conclusive evidence on protein kinase inhibition by linalyl acetate, and whether linalyl acetate binds specifically to the kinase active-site will be addressed in the future mechanistic studies that are underway in our laboratory.

The NF-!B signalling pathway is a central common regulator for the process of inflammation, and compounds that inhibit different components in the pathway are widely sought as potential therapeutics for inflammatory disorders and cancer (Garg and Aggarwal, 2002). NF-!B is a key antiapoptotic factor in mammalian cells and has a critical role in protecting cells from apoptosis induced by

366

Gene Therapy and Molecular Biology Vol 12, page 367 various anticancer drugs (Baldwin, 2001). NF-!B inhibition may be achieved at various points in the signalling pathway of NF-!B including the downstream kinases (IKK# and IKK&), the proteosome-mediated degradation of NF-!B inhibitory protein and nuclear NF!B binding to DNA (Karin et al, 2004). Previously, linalyl acetate has been reported to have anti-inflammatory effects (Peana et al, 2002). Our results indicated an inhibition of NF-!B translocation in response to incubation with linalyl acetate, which seems to be concentration- and time- dependent. Linalyl acetate showed moderate inhibitory activity (36%) against IKK& kinase in the in vitro, cell-free kinase assay performed in this study. Our study domenstrated that the inhibition of NF-!B translocation was linked to the anti-tumour effect of linalyl acetate in the cell line tested, yet this needs to be explored further and this is the topic of our future paper on linalyl acetate and other sage component modulation of NF-!B pathway.

Disruption of the membrane structure has been used to explain the antimicrobial and the cytotoxic action of linalyl acetate on bacteria and human skin cells (Prashar et al, 2003; Trombetta et al, 2005). A resent study (Itani et al, 2008) has shown that, disruption of mitochondrial membrane potential and subsequent release of cytochrome c are the reasons for apoptosis induction by the combination of linalyl acetate with two other Lebanese sage components in colon cancer cell lines. The same study has shown that treatment with linalyl acetate alone induced PARP cleavage, a feature that known to mediate apoptotic features (Ghobrial et al, 2005). Interestingly, the apoptosis-inducing activity of many of the protein kinase and NF-!B inhibitors that were strongly connected to linalyl acetate activity in the current study, have been shown to be associated with the loss of mitochondrial membrane potential and release of cytochrome c such as rottlerin (Liao et al, 2005), gossypol (Lei et al, 2006), 15-' prostaglandin J2 (Cho et al, 2006), resveratrol (Aziz et al, 2006), geldanamycin (Nomura et al, 2004), withaferin A (Malik et al, 2007).

The genes from the drug-activity/gene expression correlation approach and the genes from the gene expression signature-based screening approach had diverse functions but a considerable number were found to be related to apoptosis, cell cycle, DNA repair and to the negative regulation of cell proliferation. Interestingly, some of the genes associated with linalyl acetate sensitivity such as the poly (ADP-ribose) polymerase family members PARP2 (Sharkey et al, 2007), nucleophosmin/B23 NPM1 (Lu et al, 1996), the cyclindependent kinase inhibitor 1C (p57, Kip2) CDKN1C (Samuelsson et al, 2002) and the genes upregulated by linalyl acetate such as metallothionein MT1 (Chen et al, 2001) and heme oxygenase (decycling) 1 HMOX1 (Das et al, 2006; Lim et al, 2007) have been shown to be linked to the activity of some of the protein kinases/NF-!B inhibitors discussed in this study, or are upregulated by them (supplement 1 and 2).

In conclusion, the approaches used here - correlation analysis in a drug and gene-expression database, gene expression signature-based screening (the Connectivity

Map), protein kinase profiling and the NF-!B translocation assay - proposed that protein kinases and/or the NF-!B pathway are targets for linalyl acetate cytotoxicity. This, in addition to all published reports on linaly acetate and sage components cytotoxicity, makes linalyl acetate an interesting compound for cancer therapy especially colon cancer which warrant conducting clinical trials.

Acknowledgment This work was supported by The Swedish International Development Co-operation Agency (Sida).

Grant number 348-2005-6053.

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Gene Therapy and Molecular Biology Vol 12, page 371 Gene Ther Mol Biol Vol 12, 371-382, 2008

A short term pilot open label study to evaluate efficacy and safety of LG839, a customized DNA directed nutraceutical in obesity: Exploring Nutrigenomics Research Article

Kenneth Blum1,3,8,9,*,#, Thomas JH Chen2, Lonna Williams3, Amanda LC Chen2,*, William B. Downs3, Roger L. Waite3, T. Huntington3, Simon Sims4, Thomas Prihoda5, Patrick Rhoads6, Jeffrey Reinking7, Dasha Braverman8, Mallory Kerner8, Seth H. Blum9, Brien Quirk10, Eric R Braverman11 1

Department of Physiology & Pharmacology, Wake Forest University School of Medicine, Winston-Salem, North Carolina, USA 2 Chang Jung Christian University, Tainan, Taiwan Republic of China 3 Department of Nutrigenomics, LifeGen®, Inc. La Jolla, California, USA 4 DNA Services of America, Lafayette, Louisiana, USA 5 Department of Pathology, University of Texas Health Science Center, San Antonio, Texas, USA 6 Central Valley Comprehensive Obesity Clinic, Modesto, California, USA 7 Department of Medicine, University of California School of Medicine at Davis, Davis California, USA 8 Department of Clinical Neurology, Path Medical and Research Foundation, New York, New York, USA 9 Department of Psychoneurogenetics, Synaptamine, Inc., San Antonio, Texas, USA 10 Draco Natural Products, Inc. Eugene, Oregon, USA 11 Department of Neurosurgery, Weill Cornell College of Medicine, New York, New York, USA

__________________________________________________________________________________ *Correspondence: Kenneth Blum, Ph.D., Department of Physiology & Pharmacology, Wake Forest University School of Medicine, Medical Center Boulevard, Winston-Salem, North Carolina, 27157, USA; Tel: 210-823-1504; e-mail drd2gene@al.com Amanda LC Chen, Chang Jung Christian University, Tainan, Taiwan Republic of China: e-mail Tjhchen@yahoo.com.tw # All reprint request to Kenneth Blum e-mail: drd2gene@aol.com Key words: LG839; Synaptamine™, Reward Deficiency Syndrome (RDS), Obesity, Diabetes, nutrigenomics, polymorphisms, genes Abbreviations: Allelic Discrimination, (AD); body mass index, (BMI); cardiovascular disease, (CVD); CCAAT/enhancer-binding protein alpha, (C/EBP!); cocaine- and amphetamine-regulated transcript, (CART); deoxynucleotide 5’-triphosphates, (dNTPs); dopamine D2 receptor, (DRD2); adrenergic receptors, (ADBRs); interleukin-6, (IL-6); leptin receptor, (LEPR); leptin, (LEP); lipid metabolism including hepatic lipase, (LIPC); lipoprotein lipase, (LPL); logarithm of odds, (LOD); methylenetetrahydrofolate reductase, (MTHFR); perilipin, (PLIN); peroxisome proliferator activator receptor delta, (PPAR"); Peroxisome Proliferator-Activated Receptor gamma, (PPAR-#); polymerase chain reaction, (PCR); quantitative trait loci, (QTL); restriction fragment length polymorphism, (RFLP); serotonin receptor, (5-HT2a); sterol regulatory element-binding transcription factor 1, (SREBP-1); uncoupling proteins, (UCPs)

Conflict of Interest: Kenneth Blum, Roger L. Waite, Lonna Williams, B William Downs, own stock in LifeGen® Inc. Synaptamine ™ and LG839 and all patent variants have been exclusively licensed to LifeGen® Inc. Received: 7 October 2008; Revised: 3 December 2008 Accepted: 5 December 2008; electronically published: January 2009

Summary We hypothesized that genotyping certain known candidate genes would provide DNA-individualized customized nutraceuticals that may have significant influence on body re-composition by countering various genetic traits. It is well known that obesity and related symptoms significantly aggravates type 2 diabetes. Both obesity and diabetes are influenced by the interaction of both genes and environmental factors. Exploration of the current literature has identified a number of candidate genes to be associated with both of these two disorders and include amongst others the dopamine D2 receptor (DRD2), methylenetetrahydrofolate reductase (MTHFR), serotonin receptor (5-HT2a),

371

Blum et al: Exploring Nutrigenomics Peroxisome Proliferator-Activated Receptor gamma (PPAR-!), and Leptin (OB) genes. In the present study, we systematically evaluated the impact of polymorphisms of these five candidate genes as important targets for the development of a DNA-customized nutraceutical LG839 [dl-phenylalanine, chromium, l-tyrosine other select amino-acids and adaptogens]) to combat obesity with special emphasis on body recomposition as measured by Body Mass Index (BMI). A total of 21 individuals were evaluated in a preliminary investigational study of LG839. Based on the results of buccal swab genotyping of each subject, an individualized customized nutraceutical formula was provided as a function of measured gene polymorphisms of the five gene candidates assessed. At the inception of the study and every two weeks subsequently, each subject completed a modified Blum-Downs OPAQuE Scaleâ&#x201E;˘ [Overweight Patient Assessment Questionnaire]. The alleles included the DRD2 A1; MTHFR C 677T; 5HT2a 1438G/A; PPAR-!Pro12A1a and Leptin Ob1875<208bp. Pre- and post ad hoc analysis revealed a significant difference between the starting BMI and the BMI following an average of 41 days (28-70d) of LG839 intake in the 21 individuals. The pre- BMI was 31.2 (weight/Ht2) compared to the post BMI of 30.4 (weight/Ht2) with a significance value of P < 0.034 (one tailed). Similarly the pre -weight in pounds (lb) was 183.52 compared to the post weight of 179 lb with a significance value of P<(0.047). We also found trends for reduction of late night snacking, carbohydrate craving reduction, reduction of stress, reduction of waist circumference. Moreover, in the 41 day period we found a trend in weight loss whereby 71.4% of subjects lost weight. Thus 15 out of 21 subjects lost weight with a z score of 2.4 and significance value of P <(0.02). In this group 53% lost on average over 2.5% of their starting weight. Further confirmation of these preliminary results (ongoing) warrants investigation and should ultimately provide novel DNA directed â&#x20AC;&#x153;omicâ&#x20AC;? therapeutic targets of novel anti-obesity agents especially in diabetes and other related diseases.

such as insulin, leptin, ghrelin, cholecystokinin, and corresponding receptors. Polymorphic central regulators of energy intake include hypothalamic neuropeptide Y, agouti-related protein, melanocortin pathway factors, CART (cocaine- and amphetamine-regulated transcript), some other neuropeptides, and receptors for these molecules. Potentially important polymorphisms in the genes encoding energy expenditure modulators (alphaand beta- adrenoceptors, uncoupling proteins, and regulators of adipocyte growth and differentiation and the dopamine D2 receptor genes ) related gene polymorphisms comprising those involved in the pathogenesis of obesity, blood pressure regulation, hemostasis control, and homocysteine metabolism are known and these multiple polymorphisms affect lipid transport and metabolism and their interactions with diet. There is an apparent progress in the field with hundreds of new gene polymorphisms discovered and characterized, however firm evidence consistently linking them with pathogenesis of complex chronic diseases is still limited. It appears that several new directions emerge as targets of research on the role of genetic variation in relation to diet and complex chronic diseases. Regulation of energy homeostasis is a fundamental problem insufficiently investigated in this context so far (Martinez et al, 2008). Impacts of genetic variation on systems controlling angiogenesis, inflammatory reactions, and cell growth and differentiation (comprising regulation of the cell cycle, DNA repair, and DNA methylation) are also largely unknown and need thorough analysis. However, these goals can be achieved by complex simultaneous analysis of multiple polymorphic genes controlling carefully defined and selected elements of relevant metabolic and regulatory pathways in meticulously designed large-scale studies (Loktionov, 2003).

Indeed, a number of genes involved in the regulation of energy expenditure, appetite, lipid metabolism and adipogenesis have been reported to affect the risk of treatment failure in some obese subjects. Some candidate

I. Introduction Our generating hypothesis was that genotyping certain known candidate genes would provide DNAindividualized customized genetic targets by manipulation of specific ingredient components of a nutraceutical that may have significant influence on body re-composition by countering various genetic traits involved in obesityrelated deficient pathways. This paper will present preliminary evidence to support both safety and efficacy potential of LG839 and provide a brief review of the literature of gene-environmental influence on obesity risk.

A. Genes and obesity One example of how genes may affect behavior related to obesity involves the genetic aspects of the dorsal striatum of the brain. The dorsal striatum plays a role in consummatory food reward, and striatal dopamine receptors are reduced in obese individuals, compared to non-obese subjects. This suggests that the striatum and dopaminergic transmission in this brain region contribute to the development of obesity. Stice and colleagues in 2008 using functional MRI found that subjects may overeat to compensate for a blunted or hypofunctioning dorsal striatum, especially in subjects carrying the dopamine D2 A1 variant (DRD2A1 allele). Certainly we are cognizant that multiple gene polymorphisms play a role in obesity and related behaviors.

Rapid progress in human genome decoding has accelerated the search for the role of gene polymorphisms in the pathogenesis of complex multifactorial diseases. It is evident that several major chronic diseases are closely related (often through obesity) to deregulation of energy homeostasis. Multiple polymorphic genes encoding central and peripheral determinants of energy intake and expenditure have been revealed over the past decade (Martinez et al, 2008). Food intake control may be affected by polymorphisms in the genes encoding taste receptors and a number of peripheral signaling peptides

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Gene Therapy and Molecular Biology Vol 12, page 373 genes for the prognosis of weight loss response related to energy expenditure are those codifying for the adrenergic receptors (ADBRs) and uncoupling proteins (UCPs), while genes related to appetite potentially affected by energy restriction are leptin (LEP), leptin receptor (LEPR), melanocortin pathways genes (MC3R, POMC), dopamine D2 receptor (DRD2) and the serotonin receptor.

Furthermore, adipogenesis related genes such as peroxisome proliferator-activated receptor gamma (PPAR#2) (Rosmond et al, 2003) and genes related to cytokines such as interleukin-6 (IL-6) and lipid metabolism including hepatic lipase (LIPC), perilipin (PLIN) and lipoprotein lipase (LPL) have also been associated with the weight lowering outcome induced by hypocaloric diets. Therefore, preliminary evidence from human studies supports the existence of a genetic component in the fat reduction process associated to a negative energy balance (Table 1).

been also observed in several genes, and some genes were found to influence the effect of dietary intake and physical activity on obesity-related phenotypes. Integration of genetic epidemiology with functional genomics and proteomics studies will be required to fully understand the role of genetic variants in the etiology and prevention of obesity (Barnard et al, 2008).

Moreover, the concept of gene-environment interaction is receiving support from emerging evidence coming primarily from studies involving diet and cardiovascular disease (CVD), diabetes and various risk factors. The accumulating evidence shows that common variants at candidate genes for lipid metabolism, inflammation, and obesity are associated with altered plasma levels of classic and new biomarkers of metabolic syndrome. Major contributors to this knowledge have been a series of large population studies containing phenotyperich databases and dietary information to which genetic data have been added (Ordovas and Shen, 2008).

Current population studies are starting to incorporate experimental and analytical approaches that could provide more solid and comprehensive results. However, other limitations, such as the size of the populations required to examine higher-level interactions, are still major obstacles to translating this knowledge into practical public health applications. Nevertheless, data from numerous molecular and genetic epidemiological studies provide tantalizing evidence suggesting that gene-environment interactions, i.e., the modulation by a genetic polymorphism of a dietary component effect on a specific phenotype (e.g., cholesterol levels and obesity), can interact in ways that increase the risk for developing chronic disease, including susceptibility to developing the metabolic syndrome.

B. Polygenetic approaches Obesity has become a global epidemic and contributes to the increasing burden of type 2 diabetes, cardiovascular disease, stroke, some types of cancer, and premature death worldwide. Obesity is highly heritable and arises from the interactions of multiple genes, environmental factors, and behavior. Heritabilities for obesity-related phenotypes varies from 6% to 85% among various populations. As of October 2005, 253 quantitative trait loci for obesity-related phenotypes have been localized in 61 genome-wide linkage scans, and genetic variants in 127 biologic candidate genes have been reported to be associated with obesity-related phenotypes from 426 positive findings. Gene-gene interactions have

Table 1. Number of Scientific Studies Validating Specific Genes Analyzed in Proposed Panel for Nutrigenomic Application. As of July 31, 2008 Gene Leptin OB Serotonergic 2A receptor Gene Phenylethanolamine-NMethyltransferase Dopamine D2 receptor Tumor necrosis factors (or the TNFfamily Steroid sulfatase (STS) gene peroxisome proliferator-activated receptor ! (PPAR!) Carbohydrate responsive elementbinding protein (ChREBP) gene FTO Gene Monoamine Oxidase ADAM 8-ADAM metallopeptidase domain 8, also known as ADAM8 Corticotrophin-Releasing Factor (CRF) Vitamin D gene

General 3618 289

Reward & appetite regulation 57 13

Stress

Metabolism & energy

Neuroendocrine

Immune system

104 8

981 2

3 6

108 4

247

3

38

1

6

5

1999

334

31

8

73

23

593

-0-

37

443

-0-

160

156

-0-

-0-

2

-0-

15

2878

-0-

100

87

1

303

27

-0-

-0-

24

27

-0-

*

-018

-015

107 882

-047

-061

10 7

13

-0-

-0-

1

1

-0-

612

-0-

243

16

202

221

5443

-0-

64

82

28

223

373

Blum et al: Exploring Nutrigenomics Once further experience is gained from patients and/or individuals at high risk, more personalized genetic-based approaches may be applied toward the primary prevention and treatment of obesity.

While there is enough data from human studies it is important to support these studies with animal experimentation, albeit possibility of non-relevance between murine genes and human obesity, utilizing a well established approach referred to as QTL. Cross-breeding experiments with different mouse strains have successfully been used by many groups to identify genetic loci that predispose for obesity. In order to provide a statistical assessment of these quantitative trait loci (QTL) as a basis for a systematic investigation of candidate genes, Wuschke and colleagues have performed in 2007 a metaanalysis of genome-wide linkage scans for body weight and body fat. From a total of 34 published mouse crossbreeding experiments, they compiled a list of 162 nonredundant QTL for body weight and 117 QTL for fat weight and body fat percentage. Collectively, these studies include data from 42 different parental mouse strains and >14,500 individual mice. The analysis revealed significant evidence (logarithm of odds (LOD) score >4.3) for linkage of body weight and adiposity to 49 different segments of the mouse genome. The most prominent regions with linkage for body weight and body fat (LOD scores 14.821.8) on chromosomes 1, 2, 7, 11, 15, and 17. At least 34 candidate genes and genetic loci, which have been implicated in regulation of body weight and body composition in rodents and/or humans, are found in these regions, including CCAAT/enhancer-binding protein alpha (C/EBP!), sterol regulatory element-binding transcription factor 1 (SREBP-1), peroxisome proliferator activator receptor delta (PPAR"), and hydroxysteroid 11-beta dehydrogenase 1 (HSD11B1). The risks for any individual to become obese may involve the impairment of many physiological processesâ&#x20AC;&#x2122; and a number of major pathways.

The next section will provide specific information related to these defined pathways.

to G allele carriers (105+/-11 cm vs 112+/-17 cm; P=0.011). In conclusion, although the -1438G>A polymorphism is not a relevant marker for obesity risk, this variant may play a role in determining BMI in obese subjects (SorlĂ­ et al, 2008). Moreover a similar result was obtained for polymorphisms of the DRD2gene. In Pima Indians with diabetes individuals with a 'CG' genotype at the Ser311Cys SNP of the Dopamine D2 receptor gene had a higher BMI than those with a 'CC' genotype (36.7 vs 35.5 kg/m2, P= 0.04).

Furthermore, in neuroimaging studies (Volkow et al, 2008), the associations between striatal D2 receptors and prefrontal metabolism in obese subjects suggest that decreases in striatal D2 receptors could contribute to overeating via their modulation of striatal prefrontal pathways, which participate in inhibitory control and salience attribution. The association between striatal D2 receptors and metabolism in somatosensory cortices (regions that process palatability) could underlie one of the mechanisms through which dopamine regulates the reinforcing properties of food and may ultimately contribute to BMI. No obesity disease-causing genes, however, have been conclusively identified, most likely because this is a multigenic disease for which effects of many causative genes may be small and combined with environmental effects. However, while there are more sophisticated approaches such as Prioritisation of candidate disease genes (Tiffin et al, 2008), less sophisticated clinical approaches are still informative.

E. Other supporting nutrigenomic studies In exploring the literature to determine results of other laboratories that may also utilize a nutrigenomic approach to counter genetic traits related to obesity treatment PUBMED analysis only resulted in a citation of our original research in this emerging field.

In an earlier study in this journal we have discussed the role of Nutrigenomics in obesity (Chen et al, 2008). It is our contention that unraveling the multitude of nutrigenomic (nutritional genomics), transriptomic (gene expression), epigenomic (organization of the chromatin) proteomics (posttranslational modifications) and metabolomic (metabolic profiles) patterns that arise from nutrient-induced bioactive cellular mechanisms are likely to provide insights into a tailored approach to adhere to a diet and induce health and lead to anti-obesity novel personalized medicine and nutrition (Trujillo et al, 2006).

In this regard our laboratory has embarked on a nutrigenomic approach and recently published a number of studies suggesting the validity of this approach (Meshkin et al, 2008). Additionally, in a recent published study (Blum et al, 2008b), whereby five candidate genes and associated polymorphism were assessed: methylenetetrahydrofolate reductase-k, MTHFR (folate metabolism); Peroxisome Proliferator-Activated ReceptorPPRA-#2 (lipid regulator); serotonin receptor -5-HT2a (sweet taste); Leptin-Leptin Ob (obesity); and dopamine D2 receptor -DRD2 gene (CART). Outcome results of this earlier pilot revealed significant benefits of DNA customization of LG839 (80 days of treatment) as follows:

C. Genes and specific pathways The following Table 1 provides the number of scientific studies of various known obesity related genes that our laboratory has proposed for the development of a nutrigenomic panel to counter certain genetic traits. This table is presented to inform the reader as to the extent of the literature.

D. Genes and BMI It is well known that a number of genes are associated with body mass index (BMI) and we will briefly discuss only the serotonin and dopamine receptor genes as two examples.

In terms of serotonin (5HT2a receptor polymorphisms) it was reported that in an obese population case control study, when only the obese group was analyzed, it was observed that AA subjects presented a lower body mass index (BMI) than G allele carriers (35.2+/-5.3 kg/m2 vs 37.5+/-7.8 kg/m2; P=0.039).

Moreover, significant differences were also obtained in waist perimeter that was lower in AA subjects compared 374

Gene Therapy and Molecular Biology Vol 12, page 375 weight loss (p <0.008); sugar craving reduction (p<0.008); appetite suppression (p<0.004); snack reduction (p< 0.005); reduction of late night binging (p<0.007); increased perception of over-eating (p<0.02)]; increased energy (p<0.004); enhanced quality of sleep (p<0.02) and increased happiness (p<0.02).

Other work from our laboratory showed a significant association of the DRD2 gene Taq 1A allele and percent body fat (Chen et al, 2007a). Additionally our laboratory showed an association of the PPAR -#Pro 12 allele with a self identified obese Dutch population compared to unscreened control Dutch population (Chen et al, 20007b).

In follow-up studies carriers of the DRD2 gene Taq 1A allele significantly complied with days on treatment with LG839 compared to DRD2A2 carriers by a factor of 2 fold (Blum et al, 2008a). Over the last two decades earlier work from our laboratory clinically evaluated a patented complex Synaptamine™ as an anti- glucose craving agent in a number of studies with positive outcomes: a 90 day out-patient barometric clinic (Blum et al, 1990); a 2-year out-patient barometric clinic compared to vitamin placebo (Blum et al, 1997); and a one year open trial in a consumer based cross sectional study providing a PATH analysis (Blum et al, 2006).

In consideration of all of above we decided to further evaluate LG839 customized for each patient following genotyping of MTHFR, PPRA-#2, -5-HT2a, Leptin Ob and the DRD2 genes in a short term (41 days) open label study whereby each subject served as their own control.

C. Study outcomes The primary objective was to evaluate the safety and efficacy of LG839 in obese and overweight subjects, and specifically to look at differences in weight, mood, sleep, digestion, wellness and other health issues before and after taking LG839. All participants provided written consent, and the study protocol was approved by the institutional review board of the non-profit research organization, PATH Medical & Research Foundation, located in New York, NY USA. Data were collected on line independently by LooseFoot Computing Ltd. of Regina, Saskatchewan, Canada and manually by two of us (LW and TH).

Genotyping of the five candidate genes for polymorphic alleles resulted in a number of significant associations of this population. These alleles included the DRD2 A1; MTHFR C 677T; 5HT2a 1438G/A; PPAR -#Pro12A1a and Leptin Ob1875<208bp.

D. Laboratory measurements and genotyping The laboratory testing was performed in a highcomplexity, CLIA-certified laboratory under contract with the company based in Los Angeles, California, USA. Genotyping was carried out as a research project. All subjects were genotyped based on a neutral identification number and read without knowledge of the individual being typed. Total genomic DNA was extracted from each coded blood sample, and aliquots were used for polymerase chain reaction (PCR) analysis.

E. DRD2 The DRA1 and DRA2 genotyping was performed using PCR (The oligonucleotide primers 5’CCGTCGACCCTTCCTGAGTGTCATCA-3’ (Blum et al 1990; Comings et al, 1996) and 5’CCGTCGACGGCTGGCCAAGTTGTCTA-3’were used to amplify a 310-base pair (bp) fragment spanning the polymorphic Taq1A1 site of the DRD2 gene. PCR was performed in 30mL reaction mixtures containing 1.5mM MgCl2,

II. Materials and Methods A. Subjects A total of 21 individuals (1 males and 20 females; mean age 37.5 ±1.7 yr, range 22-51yr) clients of DNA Services of America, a DNA service company located in Lafayette, Louisiana, were evaluated in a preliminary investigational study of LG839. The IRB of the Path Research & Medical Foundation approved the project (NIH Registration # IRB00002334 ) and all participants signed an approved consent form prior to the study.

The subjects received educational material about the experimental concept, however were only told to eat appropriately. No attempt was made to control diet as well as to exercise (i.e. no attempt to develop a standardized exercise program).

Table 2. Blum-Downs OPAQuE Scale™ [Overweight Patient Assessment Questionnaire Assessment area and question* Anxiety Appetite Drug craving Tobacco craving Depression Ease of Sleep Energy Exercise Get along with others Happiness Interrupted sleep Late night eating Perception of Over-eating Quality of sleep Regularity of digestion Snacking Sugar craving Waist (cm) Weight (kg)

B. Blum-Downs OPAQuE Scale™ This cross-sectional, observational study included a genetic analysis involving a panel of genes, and an evaluation questionnaire providing two key self-reported retrospective data sets on the subjects’ health before taking LG839 and then after taking LG839. Self-reported evaluations were collected through an online questionnaire disseminated over email to study participants. These subjects with a starting BMI of 31.2 were evaluated by survey analysis over 41(28-70 d) days of administration of LG839. Based on the results of buccal swab genotyping of each subject, a customized nutraceutical formula was provided as a function of measured gene polymorphisms of the five gene candidates assessed. At the inception of the study and every two weeks subsequently, each subject completed a modified Blum-Downs OPAQuE Scale™ [Overweight Patient Assessment Questionnaire-see questions Table 2]. The BMI was subsequently calculated by our staff using this self-guiding survey.

*

Responses during LG839 administration minus baseline responses. BMI was calculated on each study participant by LW, TH and TP.

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Blum et al: Exploring Nutrigenomics 2mM 2’- deoxynucleotide 5’-triphosphates (dNTPs), 0.5 uM primers, 1 $g of template DNA 1, 5U of Taq polymerase (Boehringer Mannheim Corp., Indianapolis, IN), and PCR buffer (20 mM Tris-HCL [pH 8.4] and 50mM KCl). After an initial denaturation at 94ºC for 4 minutes, the DNA was amplified with 35 cycles of 30 seconds at 94ºC, 30 seconds at 58ºC, and 30 seconds at 72ºC, followed by a final extension step of 5 minutes at 72ºC. The PCR product was digested with 5 U of Taq 1 for 22 hours at 65ºC for the Taq1A polymorphism. Digestion products were then resolved on a 3% agarose gel (5V/cm) containing 0.65 ug/ml ethidium bromide. There were three DRD2 Taq1A genotypes: 1) the predominant homozygote A2/A2, which exhibits two restriction fragments of 180 and 130 bp; 2) the heterozygote A1/A2, which exhibits three restriction fragments of 310, 180, and 130bp; and 3) the rare homozygote A1/A1, which produces only the uncleaved 310-bp fragment

MGB probes and TaqMan Universal PCR Master Mix (Applied Biosystems) were added. These were sealed with optical seals (Applied Biosystems) and incubated at 95°C for 10 min followed by 40 cycles of 95°C for 15 s and 60°C for 1 min before analysis on a 7900HT plate reader (Applied Biosystems). Individual genotypes were determined using SDSv2.1 software (Applied Biosystems) (Rosmond et al, 2003).

I. Leptin (OB) We used the following dinucleotide repeats (D7S1873, D7S1875, D7S514 and D7S680) present on the YAC contig containing the human OB gene as described by Liu and colleagues in 2007.The primers used for PCR were the same as in their report. Of these, D7S1875 was closest to the OB gene.

We refer to this as OB1875. The frequency of the different alleles of the OB 1875 polymorphism has been reported previously (Comings et al 1996). The alleles ranged in size from 199 to 225 bp in length. Our a priori approach to the examination of dinucleotide repeats in behavioral disorders is based on other research (Rance et al, 2007). Comingsand colleagues in 1996 was to first divide the alleles into approximately equal groups, since there was a natural tendency for a bimodal distribution, which was the case for the OB1875 polymorphism and the cut was made at 208 bp. The resulting genotypes were <208 bp/<208 bp, <208 bp/%208 bp, and %208 bp/%208bp. In this experiment we used Coming’s cut off point in our analysis providing for only positive and negative allelic associations.

F. MTHFR Genotyping for the MTHFR C677T polymorphism was performed using PCR and restriction fragment length polymorphism (RFLP) analysis. We designed PCR primers 5’CCCAGCCACTCACTGTTTTAG-3’ and 5’TGGGAAGAACTCAGCGAACT-3’ with DNASIS Pro Ver.2.0 (Hitachi Software Engineering Co. Ltd., Tokyo, Japan). Since the C to T transition at nucleotide 677 produces a Hinf I digestion site, the amplified 469-bp product derived from the mutant gene was cleaved into 393-bp and 76-bp fragments by Hinf I (TaKaRa Bio Inc., Shiga, Japan), which leaves the wildtype gene unaffected. After electrophoresis through 6% polyacrylamide gel, the digestion products were visualized by staining with ethidium bromide.

J. Nutraceutical customization Based upon the genetic profiles derived, certain ingredients in LG839 were customized according to subjects’ genotype (Table 3).

G. 5-HT2a Genotyping of the -1438G/A polymorphism of the 5-HT2A gene was carried out by PCR and restriction digestion as described previously (Nonogaki et al, 2006). Genomic leukocyte DNA (100ng in a final volume of 10$L) was amplified by PCR using the following primers: 5’AAGCTGCAAGGTAGCAACAGC-3’ and 5’AACCAACTTATTTCCTACCAC-3’. The primers amplified a product of 468 bp. The PCR conditions were as follows: an initial denaturation step at 94 °C for 3 minutes, followed by 35 cycles of denaturation at 94 °C for 15 seconds, annealing at 55 °C for 15 seconds, and extension at 72 °C for 30 seconds, with a final extension of 10 minutes at 72 °C. The PCR reaction product was digested at 37 °C overnight with 5 U of the restriction enzyme MspI (New England Biolabs, Beverly, MA). The -1438G allele was cut into 244-bp and 224-bp fragments, whereas the 1438A allele remained undigested. The fragments were separated on a 2% agarose gel and visualized by staining with ethidium bromide.

K. Measurements of Efficacy and Safety Separate from the laboratory measurements, all measurements of efficacy and safety were self-reported by the study subjects using a one-time retrospective online questionnaire. The primary endpoint was weight loss in kilograms and BMI (the subject of this report). Secondary endpoints included changes in appetite, sugar cravings, waist circumference, mood, sleep, and digestion (the subject of ongoing catchment data for subsequent analysis with increasing numbers of study subjects). The changes in these factors were measured generally using a scale of 1 to 5 where 5 was the least healthy rating and 1 was the most healthy rating to provide consistency across the multiple measures. Tertiary endpoints included changes in incidences of depression and cravings for alcohol/tobacco/recreational drugs. To monitor persistency, we asked study subjects to self-report on their frequency of compliance to the product’s serving instructions.

H. PPAR-!2

L. Statistics

Two hundred base pairs of sequence surrounding PPAR-#2 Pro12Ala was provided to Applied Biosystems (Foster City, CA) to develop Taqman Allelic Discrimination (AD) assays using their assay by design platform. Genotyping of the Pro12Ala AD was performed using the following primers (0.9 molL each); Forward 5'-TTATGGGTGAAACTCTGGGAGATT-3' and reverse 5'-TGCAGACAGTGTATCAGTGAAGGA-3' and the Taqman MGB probes Fam- TTCTGGGTCAATAGG and VicCTTTCTGCGTCAATAG (0.1moli/L each; Applied Biosystems). Four $l of a 10 ng/L stock of DNA was dispensed into 384-well PCR plates using a Biomek FX robot (Beckman Coulter), to which 6uL of a mix containing primers, TaqMan

The means and standard deviations were calculated before and during LG839 -DNA based customized treatment for each item in the questionnaire. To test for a change in weight, the paired t-test (one - tailed) was used on the change score, with change calculated as response during treatment minus the response before treatment for each item. The BMI at start was compared with the last measurement ranging from 28-70 days with an average of 41 days. The Statistical Analysis System (SAS Institute, version 9.1 for the PC, Cary, North Carolina, 2006) was used for these calculations. Due to the small sample size we used a one-tail test instead of a 2 tailed test.

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Gene Therapy and Molecular Biology Vol 12, page 377 Table 3. Customization of the nutraceutical LG839 according to genotype in 21 subjects Genotype Ingredient MTHFR C677T Vitamin B9 (folic acid) Homozygous or Normal/Wild Type (CC)1-12 MTHFR C677T Heterozygous Mutant (CT) or Vitamin B9 (folic acid) Homozygous Mutant (TT)8 SuperCitrimax (-) Hydroxycitric Acid (extract 5-HT2A -1438A Heterozygous or Normal 13 of Garcinia Cambogia) 5-HT2a â&#x20AC;&#x201C; 1438A Heterozygous or Homozygous SuperCitrimax (-) Hydroxycitric Acid (extract Mutant or Leptin OB 1875 14 of Garcinia Cambogia) Synaptamine Complex (DL-phenylalanine, Chromium, L-glutamine, L-tyrosine, L-5-HTP, 14-16 Dopamine D2 Receptor Wild type A2/A2 Vitamin B6 [pyridoxal-5-phosphate]),Rhodiola rosea, passion flower Synaptamine Complex (DL-phenylalanine, Dopamine D2 Receptor Heterzygous A1/A2 or Chromium, L-glutamine, L-tyrosine, L-5-HTP, Homozygous A1/A1 Vitamin B6 [pyridoxal-5-phosphate]), Rhodiola rosea, passion flower

Serving 800 Âľg 5 mg 2,500 mg 4,667 mg

1,725 mg

2,750 mg

Reproduced from Blum et al, 2008 with kind permission from Advance Therapeutics.

Note: In terms of weight loss formulations the PPAR gene variation is linked to a novel substance Irvingia gobonensis seed extract shown to up-regulate the adiponectin gene (Oben JE, Ngondi JL, Blum K (2008) Inhibition of Irvingia gabonensis seed extract (OB131) on adipogenesis as mediated via down regulation of the PPARgamma and Leptin genes and up-regulation of the adiponectin gene.

Lipids Health Dis 7, 44.

References 1. Federation of American Societies for Experimental Biology, Life Sciences Research Office (1995) Prepared for the Interagency Board for Nutrition Monitoring and Related Research. Third Report on Nutrition Monitoring in the United States: Volumes 1 and 2. U.S. Government Printing Office, Washington, DC. 2. Grosse SD, Waitzman NJ, Romano PS Mulinare J (2008) Reevaluating the benefits of folic Acid fortification in the United States: economic analysis, regulation, and public health. Am J Public Health 95, 1917-1922.

3. Huhta JC, Hernandez-Robles JA (2005) Homocysteine, folate, and congenital heart defects. Fetal Pediatr Pathol 24(2):71-9.

4. Homocysteine Lowering Trialists' Collaboration. (2005) Dose-dependent effects of folic acid on blood concentrations of homocysteine: a meta-analysis of the randomized trials. Am J Clin Nutr 82, 806-12.

5. Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith Jr SC, Spertus JA, Costa F (2005) Diagnosis and management of the metabolic syndrome. An American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Executive summary. Cardiol Rev 13, 322-7.

6. Russo GT, Di Benedetto A, Alessi E, Giandalia A, Gaudio A, Ientile R, Horvath KV, Asztalos B, Raimondo G, Cucinotta D (2006) Mild hyperhomocysteinemia and the common C677T polymorphism of methylene tetrahydrofolate reductase gene are not associated with the metabolic syndrome in Type 2 diabetes. J Endocrinol Invest 29, 201-7.

7. Thawnashom K, Tungtrongchitr R, Petmitr S, Pongpaew P, Phonrat B, Tungtrongchitr A, Schelp FP (2005) Methylenetetrahydrofolate reductase (MTHFR) polymorphism (C677T) in relation to homocysteine concentration in overweight and obese Thais. Southeast Asian J Trop Med Public Health 36, 459-66.

8. Sheu WH, Chin HM, Lee WJ, Wan CJ, Su HY, Lang HF (2005) Prospective evaluation of folic acid supplementation on plasma homocysteine concentrations during weight reduction: a randomized, double-blinded, placebo-controlled study in obese women. Life Sci 76, 2137-2145.

9. Henning BF, Tepel M, Riezler R, Gillessen A, Doberauer C (1998) Vitamin supplementation during weight reduction--favourable effect on homocysteine metabolism. Res Exp Med (Berl) 198, 37-42.

10. Volek JS, Gomez AL, Love DM, Weyers AM, Hesslink R Jr, Wise JA, Kraemer WJ (2002) Effects of an 8-week weight-loss program on cardiovascular disease risk factors and regional body composition. Eur J Clin Nutr 56, 585-92.

11. Dixon JB, Dixon ME, O'Brien PE (2001) Elevated homocysteine levels with weight loss after Lap-Band surgery: higher folate and vitamin B12 levels required to maintain homocysteine level. Int J Obes Relat Metab Disord 25, 219-27.

12. Gallistl S, Sudi K, Mangge H, Erwa W, Borkenstein M (2000) Insulin is an independent correlate of plasma homocysteine levels in obese children and adolescents. Diabetes Care 23, 1348-52.

13. Thom E (1996) Hydroxycitrate (HCA) in the Treatment of Obesity. Int J Obes Relat Metab Disord 20(suppl 4), 75.

14. Preuss HG, Bagchi D, Bagchi M, Ohia SE, Bramble JD, Garis R, Rao CV (2004) Efficacy of a Novel, Natural Extract of (-)Hydroxycitric Acid (HCA-SX) and a Combination of HCA-SX, Niacin Bound Chromium and Gymnema sylvestre Extract in Weight Management in Human Volunteers: A Pilot Study. Nutrition Research 24, 45-58 15. Chen TJ, Blum K, Payte JT, Schoolfield J, Hopper D, Stanford M, Braverman ER (2004) Narcotic antagonists in drug dependence: pilot study showing enhancement of compliance with SYN-10, amino-acid precursors and enkephalinase inhibition therapy. Med Hypotheses 63, 538-48.

16. Milner JD, Irie K, Wurtman RJ (1986) Effect of phenylalanine on the release of endogenous dopamine from rat striatal slices. J Neurochem 47, 1444-1448.

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Blum et al: Exploring Nutrigenomics administered formula. We found that the following percentage genotypes (Drd2A1; MTHFRC 677T; 5Ht2a 1438g?A; PPAR-Gamma Pro12A1a and Leptin OB1875<280bp):

III. Results In the present study, the genotype data is the subject of another report elsewhere and in the present study it was used solely to define the customization requirements of the Gene combinations** MTHFR SEROTONIN SEROTONIN ÷ MTHFR SEROTONIN ÷ MTHFR ÷LEP SEROTONIN ÷ PPAR ÷ MTHFR DOPAMINE ÷ MTHFR DOPAMINE ÷ SEROTONIN DOPAMINE ÷ SEROTONIN ÷ MTHFR ** These are the combinations found for the five candidate genes

Percentage Presence of Polymorphism* 11.81 7.84 13.42 5.77 5.58 5.29 4.54 10.40

±.24 (weight/Ht2) compared to the post BMI of 30.4 SEM±.16 (weight/Ht2) with a significance value of P < 0.034 (one tailed) (Figure 1). Similarly the pre -weight in pounds (lb) was 183.52 SEM ±.49 compared to the post weight of 179 lb SE ±1.3 with a significance value of P< (0.047) (Figure 2). We also found trends for reduction of late night snaking, carbohydrate craving reduction, reduction of stress, reduction of waist circumference.

Moreover, in the 41 day period we found a trend in weight loss whereby 71.4% of subjects lost weight. Thus 15 out of 21 subjects lost weight with a z score of 2.4 and significance value of P <(0.02). In this group 53% lost on average over 2.5% of their starting weight. Over the cause of the study we noticed that a few females complained about breakthrough bleeding and minor mood alteration.

A total of 21 individuals were evaluated in a preliminary investigational study of LG839. These subjects with a starting BMI of 31.2 were evaluated by survey analysis over 41(28-70 d) days of administration of LG839. Based on the results of buccal swab genotyping of each subject, a customized nutraceutical formula was provided as a function of measured gene polymorphisms of the five gene candidates assessed.

Genotyping of the five candidate genes for polymorphic alleles resulted in a number of significant associations of this population. These alleles included the DRD2 A1; MTHFR C 677T; 5HT2a 1438G/A; PPAR #Pro12A1a and Leptin Ob1875<208bp. Pre- and post ad hoc analysis revealed a significant difference between the starting BMI and the BMI following 41 days of LG839 intake in the 21 individuals. The pre- BMI was 31.2 SEM

Figure 1. Pre- and post ad hoc analysis revealed a significant difference between the starting BMI and the BMI following 41 days of LG839 intake in the 21 individuals. The pre- BMI was 31.2 SEM ±.24 (weight/Ht2) compared to the post BMI of 30.4 SEM± .16 (weight/Ht2) with a significance value of P < 0.034 (one tailed). N=21.

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Gene Therapy and Molecular Biology Vol 12, page 379 Figure 2. The one tailed pre weight in pounds (lb) was 183.52 SEM ±.49 compared to the post weight of 179 lb SEM ± 1.3 with a significance value of P< (0.047) N=21.

Other more recent work investigated reward sensitivity with regard to binge eating behavior. The sensitivity of dopamine reward pathways has been implicated in the risk for various psychiatric disorders including compulsive overeating. The evidence is divided, however, about the direction of causal association. One argument is that a Reward Deficiency Syndrome (RDS) is the risk factor, while others contend that hyper-sensitivity to reward enhances the motivation for pleasurable activities like eating. Davis and colleagues found in 2008 genotype x group ANOVAs revealed significant main effects and an interaction on the personality measures for Taq1A. Binge Eating Disorder (BED) and obese subjects reported greater reward sensitivity than normal-weight controls, but only among those carrying the A1 allele.

They also found that normal-weight controls with at least one copy of the T allele of the C957T marker had significantly lower reward sensitivity scores than any of the other groups who did not differ from each other. Given evidence linking the A1 allele with reduced receptor density, an inverse relationship was expected between psychological measures of reward sensitivity and presence of the A1 allele. One explanation for their findings could be that the BED and obese participants possess another genetic variant that interacts with the A1 allele to produce higher dopamine activity. However, in RDS it is possible that low dopaminergic activity may translate to aberrant reward hypersensitivity because of the anxious need to obtain a dopamine “fix” (Blum et al, 2006; Davis et al, 2008).

While the present study represents a small sample of individuals who purchased the DNA customized LG839 at DNA-Services of America clinics across the nation, the significant reduction of BMI as well as s significant

IV. Discussion It is well known that obesity and related symptoms significantly aggravates type 2 diabetes. Both obesity and diabetes are influenced by the interaction of both genes and environmental factors. These findings take on an even greater importance relative to the well known neurointeraction of dopamine and glucose (Blum et al, 2006).

Confirmation of reduced glucose craving behavior by LG839 may reduce the risk of a number of genes which affect aberrant behavior for type 2 diabetics. Barnard and colleagues found in 2008 that DRD2 A1 allele was highly prevalent, occurring in 47% of white participants (n = 49), which was significantly higher than the 29% prevalence previously reported in non-diabetic whites (P = 0.01). The A1 allele was found in 55% of black participants (n = 44).

Black participants with A1(+) genotypes had significantly greater mean body weight (11.2 kg heavier, P = 0.05) and greater intake of fat (P = 0.002), saturated fat (P = 0.01), and cholesterol (P = 0.02) compared with A2A2 (A1(-)) individuals while dietary changes during the study did not favor one genotype group.

It is noteworthy that one mechanism may involve the role of chromium salts (an ingredient in LG839), a known anti-diabetic compound affecting glucose utilization/body composition as a function of the DRD2 gene polymorphisms (Chen et al, 2007a), whereby carriers of the DRD2 A1 allele did not respond to chromium picolinate compared to DRD2 A2 carriers. Thus previous work suggests the need to prior genotype individuals to assist in obtaining information concerning proper dosing.

The findings of this report coupled with our most recent publications (Blum et al 2008a,b) further support a nutrigenomic approach to weight management.

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Blum et al: Exploring Nutrigenomics decrease in weight suggests the need for additional studies involving a tailored personalized DNA based approach.

We are somewhat surprised in that LG839 -DNA based was able to cause significant changes in both BMI and weight in subjects self-Identified as desirous of utilizing this anti-obesity regimen in only 41 days (an average days on treatment).We further caution any interpretation of these results because we utilized a less conservative onetailed statistic to analyze the data.

These results are consistent with earlier reports involving LG839 variants (Blum et al, 1990, 1997, 2006).

Furthermore, a loss of 2.5 kg in only 41 days is quite robust especially when considering guidelines from the United Sates FDA regarding meaningful weight loss of approved medical use of any anti-obesity pharmaceutical.

The NI H 1998 Practical Guide: Identification, Evaluation, and Treatment of Overweight and Obesity in Adults defines normal weight as a body mass index (BMI) of 18.5 - 24.9 kg/m2, overweight as a BMI of 25 - 29.9 kg/m2, and obese as a BMI %30 kg/m2. The Practical Guide recommends weight loss through a combination of diet modification, increased physical activity, and behavior therapy for obese patients, and for patients who are overweight or have a high-risk waist circumference, when accompanied by two or more risk factors. In the event that lifestyle changes do not promote weight loss after 6 months, the Practical Guide recommends that drugs should be considered as adjunctive therapy for select patients who have gender based BMI %30 kg/m2, or a BMI %27 kg/m2 if concomitant obesity-related risk factors or disease exist.

The FDA’s approach to the approval of prescription weight-loss drugs mirrors the recommendations provided in the NIH’s Practical Guide. For example, the prescription of orlistat was studied and approved for longterm weight loss in patients moderately-to-severely overweight (BMI 27-9.9 kg/m2) with comorbid conditions such as hypertension, type 2 diabetes, or dyslipidemia and in obese subjects (BMI %30 kg/m2) regardless of the presence of comorbidities. Limiting approval of prescription weight-loss drugs to moderately-to-severely overweight individuals with comorbidities and to obese patients maximizes the therapeutic risk-benefit profile by targeting drug therapy to individuals whose risk for weight-related disease is high and likely to outweigh the risks associated with any given pharmacological agent. In clinical studies, orlistat demonstrated weight loss of 5% or more at 6 and 12 months (Food And Drug Administration Center For Drug Evaluation and Research (CDER), 2006).

In light of the current results which suggest a potential weight loss of 2.5% in 41 days (in this group 53% lost on average over 2.5% of their starting weight), or less than 3 months, the LG839 product warrants further investigation to evaluate whether these pilot study results are replicable in a randomized, placebo-controlled study of a longer duration.

Limitations of this present study involving sample size and lack of placebo controls caution any definitive interpretation of these results albeit significant findings, and must await further confirmation. In this present pilot study which was an extension of previously reported

outcomes with LG839 (Blum et al, 2008b), each patient served as it’s own control. In future studies albeit difficult and costly, we intend to develop studies which will provide a placebo group matched to each individualized DNA solution. We believe that the breakthrough bleeding one of the ingredients in the formulation (which will be altered in future studies) and the mood alteration may be due to enhanced serotonin levels. In an open label study because a control is not employed interpretation of the result is suspect.

Since our formula includes both dl-phenylalanine and chromium we find it of considerable interest that a novel chromium -d-phenylalanine complex in other studies possesses better cardio-protective and insulinsensitizing properties against obesity in ob/ob mice than chromium picolinate alone (Dong et al, 2007). A major benefit of this novel compound is the potential of eliminating the proposed cytoclastic toxicity of chromium picolinate alone. This novel complex which is imbedded in Synaptamine™ will be the subject of future investigation.

Of great interest is the finding of slowed intracellular Ca2+ decay observed in myocytes from ob/ob mice following a 3 month treatment with Cr(D-Phe)3.This takes on real importance when we consider the important role of intracellular calcium in neurotransmitter release of neuronal dopamine. A substance linked to glucose craving (Blum et al, 2007).

V. Conclusion Based on this preliminary investigation and others (Blum et al 2008 a,b) we suggest that DNA-directed targeting of certain regulator genes along with customized nutraceutical intervention may provide a unique framework and strategic modality to combat obesity, weight problems, and their associated co-morbidities. In light of many dietary supplement ingredients and other tactics used empirically for weight loss without preliminary analysis to deem their merit, this study maintains previous foundational research involving the LG839 technology that a scientific and rationale approach of laboratory testing and laboratory-directed nutritional supplementation may present beneficial health outcomes in the treatment of obesity, along with healthy eating and exercise. This pioneering research will pave the way for additional gene-environmental studies utilizing nutigenomics as a principle modality in the combat of obesity related diseases including larger samples and longer term therapy. One major outcome if this pilot study suggests that LG839 is well tolerated in subjects in the short term and other work from our lab supports this notion as well (Chen et al, 2008b).

Thus confirmation of these preliminary results (ongoing) will support our hypothesis and warrants investigation. These and other large independent controlled reports should ultimately provide novel DNA directed “omic” therapeutic targets of novel anti-obesity agents especially in diabetes and other obesity related diseases.

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Gene Therapy and Molecular Biology Vol 12, page 381 induces changes in body composition as a function of the Taq 1 dopmine D2 receptor polymorphisms in a randomized double-blind placebo controlled study. Gene Ther Mol Biol 11, 161-170.

Chen TJH, Blum K, Kaats G, Braverman ER, PullinM D, Downd BW, Martinez-Pons M. Blum SH, Mengucci J, Bagchi D, Bagchi M, Robarge A, Meshkin B, Arcuri V, Varshavisky M, Notaro A, Comings DE, White L (2007b) Reviewing the role of putative candidate genes in “Neurobesigenics” aclinical subtype of Reward Deficiency Syndrome (RDS).

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Dong F, Yang X, Sreejayan N, Ren J (2007) Chromium (DPhenylalanine)3 Improves Obesity-Induced Cardiac Contractile Defect in ob/ob Mice. Obesity (Silver Spring) 15, 2699-2711.

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Meshkin B, Chen TJH, Chen ALC, Prihoda TJH, Morrisette H, Braverman ER, Blum SH, Cassel K, Williams L, Waite RL, Downs BW, Tung H, Rhoades P, Blum K (2008) Health economics of nutrigenomics in weight management. Gene Ther Mol Biol 12, 25-30.

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Acknowledgements The authors appreciate the funding support of the PATH Medical & Research Foundation, New York, New York, LifeGen, Inc. La Jolla, California and Electronic Waveform Lab, Huntington , Beach California. They especially appreciate the donations of Don Reuben, Eduardo Cruz, Rein Norma, and Elizabeth Daiber.

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Blum K, Chen ALC, Chen TJH, Rhoades P, Prihoda TJ, Downs BW, Bagchi, Bagchi M, Blum SH, Williams L, Braverman ER, Kerner M, Waite RL, Quirk B, White L (2008a) Dopamine D2 Receptor Taq A1 allele predicts treatment compliance of LG839 in a subset analysis of a pilot study in the Netherlands. Gene Ther Mol Biol 12, 129-140.

Blum K, Chen ALC, Chen TJH, Rhoades, Prihoda TJ, Downs BW, Waite RL, Williams L, Braverman Er, Braverman D, Arcuri V, Kerner M, Blum SH, Reinking J, Palomo T (2008b) LG839 (an experimental DNA-Customized nutraceutical): Anti-obesity effects and polymorphic gene correlates of Reward Deficiency Syndrome (RDS). Adv Ther (in press) Blum K, Chen TJ, Meshkin B ,Downs BW, Gordon CA, Blum SH, Mengucci JF, Braverman ER, Martinez-Pons M (2006) Reward deficiency syndrome in obesity: a preliminary crosssectional trial with a Genotrim variant. Adv Ther 23, 10401051.

Blum K, Chen TJ, Meshkin B, Downs BW, Gordon CA, Blum S, Mangucci JF, Braverman ER, Arcuri V, Deutsch R, Pons MM (2007) Genotrim, a DNA-customized nutrigenomic product, targets genetic factors of obesity: hypothesizing a dopamine-glucose correlation demonstrating reward deficiency syndrome (RDS). Med Hypotheses 68, 844-852.

Blum K, Chen TJH, Meshkin B, Blum SH, Mengucci JF, Notaro A, Arcuri V, Waite RL, Braverman ER (2007) The PPARGamam Pro 12Ala allele polymorphism of the Peroxisome Proliferator -Activated Receptor gene (PPARG2) is a risk factor with a self-identified obese Dutch population. Gene Ther Mol Biol 11, 37-42.

Blum K, Cull JG, Chen TJH, Swan SG, Holder JM, Wood R, Braverman ER, Bucci LR, Trachtenberg MG (1997) Clinical evidence for effectiveness of Phencal™ in maintaining weight loss in an open-label, controlled, 2-year study. Curr Ther Res 58, 745-763.

Blum K, Noble EP, Sheridan PJ, Montgomery A, Ritchie T, Jagadeeswaran P, Nogami H, Briggs AH, Cohn JB (1990) Allelic association of human dopamine D 2 receptor gene in alcoholism. JAMA 263, 2055-2060.

Blum K, Trachtenberg MC, Cook DW (1990) Neuronutrient effects on weight loss in carbohydrate bingers: an open clinical trial. Curr Ther Res 48, 217-233.

Chen ALC, Blum K, Chen TJH, Rhinking J, Waite RL, Downs BW, Braverman ER, Arcuri V, Kerner M, Notaro A, Cassel K, Blum SH, Bagchi D, Bagchi M, Robarge A, Kaats G, Comings E. (2008) The impact of biomics technology and DNA directed anti-obesity targeting of the brain reward circuitry. Gene Therapy and Mol Biol 12, 45-68.

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Tiffin N, Okpechi I, Perez-Iratxeta C, Andrade-Navarro MA, Ramesar R (2008) Prioritisation of candidate disease genes for metabolic syndrome by computational analysis of its defining phenotypes. Physiol Genomics, in press.

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Severe phenotype of Morquio A disease in a child with S287L N-acetylgalactosamine-6-sulfate sulfatase mutation Case Report

Zoran S Gucev1,*, Hassan Bouzidi2, Velibor Tasic1, Nada Popjordanova1, Ilija Kirovski1, Zoran Trajkovski2, Aleksandra Jancevska1, Sami. Bajrami1 1

University Hospital for Sick Children, Medical School, Skopje, FYROM Laboratory of Biochemestry, Tahar Sfar Hospital, 5100, Mahdia, Tunisia 3 Institute of Radiology, Medical School, Skopje, FYROM 2

__________________________________________________________________________________ *Correspondence: Zoran S Gucev, University Hospital for Sick Children, Medical School, 17 Vodnjanska, 1000 Skopje, FYROM; Tel/Fax: 00389-2-3111-366; e-mail: gucevz@gmail.com Key words: Morquio A disease; N-acetyl galactosamine-6-sulphate sulfatase; S287L mutation; severe phenotype Abbreviations: denaturing high performance liquid chromatography, (DHPLC); glycosaminoglycans, (GAG); Mucopolysaccharidosis IVA, (MPS IVA); N-acetyl-galactosamine-6-sulfate sulfatase, (GALNS) Received: 4 December 2008; Revised: 22 December 2008 Accepted: 23 December 2008; electronically published: January 2009

Summary Mucopolysaccharidosis IVA is caused by a deficiency of lysosomal N-acetyl-galactosamine-6-sulfate sulfatase (GALNS; E.C.3.1.6.4). One hundred fourty-eight GALNS mutations were described in patients with different phenotype severity. Our patient was a 6.5 year old boy with severe kyphoscoliosis and growth delay. He developed coarsening of the facial features and megalencephaly. Both corneas were cloudy. His gait was difficult with limited and painful movements in the hips, the spine and the knees. X-ray studies showed platispondily with ovoid vertebrae, bulging sternum and flaring of the rib cage. The long bones were short with irregular trabeculation.

Metaphyses were widened, femoral head was flattened. The metacarpals had conical bases. Total excretion of glycosaminoglycans (GAG) in urine was increased. Thin layer chromatography of urinary GAG showed massive excretion of keratan sulphate. N-acetyl Galactosamine-6-sulphate sulfatase activity in leukocytes was low (0.7 nmol/MU17h/mg protein). DNA sequencing detected a S287L mutation (c.860C>Tc.860 C>T). This is the first GALNS mutation described in our population. The same mutation conferred a severe MPS IVA phenotype in a American, Austrian and Polish patients.

About 70% of known lesions stem from missense mutations. It has been well documented that the patientsâ&#x20AC;&#x2122; clinical severity correlates with the genotype, its effect on the tertiary structure, the level of conservation of altered amino acids, and the residual enzyme activity (Sukegawa et al, 2000). Some mutations are common in specific ethnic groups (Tomatsu et al, 2005).

In this article, we describe a boy with a severe MPS IVA phenotype caused by a S287L mutation (c.860C>Tc.860 C>T), the first described mutation in our population.

I. Introduction Mucopolysaccharidosis IVA (MPS IVA; Morquio A disease; MIM#253000) is an autosomal recessive lysosomal storage disorder caused by a deficiency of lysosomal N-acetyl-galactosamine-6-sulfate sulfatase (GALNS; E.C.3.1.6.4) (Matalon et al, 1974). The enzyme deficiency results in the progressive accumulation of the undegraded substrates leading to a characteristic bone dysplasia. One hundred fourty-eight GALNS mutations and sixteen polymorphisms were documented (Tomatsu et al, 2005). We distinguish three forms of Morquio disease: severe, intermediate and mild forms. The phenotypes have a large diversity: from short trunk dwarfism, severe bone dysplasia, and a life span of 20-30 years, to mild bone dysplasia and visceral involvement (Tomatsu et al, 2005).

II. Case report A 6.5 year old boy with short stature (-4.5 SD) progressively developed coarsening of the face (Figure 1A).

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Gucev et al: Severe phenotype of Morquio A disease Macrocephaly, broad mouth, short and anteverted nose, widely spaced teeth, brittle and greyish enamel were evident. Intraocular pressure and hearing were normal, corneas were cloudy. The neck was short, kyphoscoliosis was pronounced (Figure 1B). He had progressive pains in the hips and the spine, the gait was difficult and he has recently begun to walk. Movements were limited and painful in the hips, the spine and the knees. In contrast, there was joint laxity in the wrists and the small joints.

Platispondily with ovoid vertebrae in anterior projection was seen on X-rays (Figure 2A). The sternum was bulging and the rib cage was flaring. The long bones were short, curved and with irregular trabeculation. Metaphyses were widened, the femoral head was flattened, the femoral neck was abnormal (Figure 2B). He had coxa valga and a knock-knee with medial spur of tibial metaphyses. The metacarpals had conical bases; hands were short and stubby (Figure 2C). MRI of the cervical spine showed no evidence for C1-C2 or C2-C3 subluxation. In addition, bone densitometry revealed reduced bone density.

Mental development was normal. No cardiac anomalies or hepatomegaly were found.

Total excretion of glycosaminoglycans (GAGs) in urine (dimethylmethylene blue assay) was increased for the age group (16.2 mg/mmol creatinine; reference 7.6-9.2 mg/mmol creatinine) (de Jong et al, 1989). Thin layer chromatography of urinary GAG showed massive excretion of keratan sulphate (Humbel and Collart, 1975). N-acetyl galactosamine-6-sulphate sulphatase activity in leukocytes was low (0.7 nmol/MU17h/mg protein) compared to the controls (20-70 nmol/MU17h/mg protein) (Van et al, 1990). Analysis of GAGs in urine for the siblings and the parents was unavailable.

PCR amplification of the entire GALNS coding sequence and their flanking intronic regions was carried out on genomic DNA. PCR products were then subjected to denaturing high

performance liquid chromatography (DHPLC) performed by a WAVE DNA fragment analysis system (Transgenomic, Omaha, Ne). Briefly, PCR products were denatured at 95 oC for 5 min followed by gradual annealing to 50 oC. Samples were automatically loaded on a DNAsep column (Transgenomic) and eluted with a linear acetonitrile gradient at the temperature for heteroduplex detection. The eluted DNA fragments were detected by an UV-C detector (Transgenomic). A S287L mutation (c.860C>Tc.860 C>T) was identified.

III. Discussion The GALNS gene is located on chromosome arm16q24.3 (Masue et al, 1991; Tomatsu et al, 1992) and encodes 522 aminoacids, including a signal peptide of 26 residues. A total of 148 mutations included 103 missense mutations, eight nonsense mutations, 10 splice-site mutations, 20 small deletions, two large deletions and five insertions have been identified. In addition, sixteen polymorphisms producing amino acid changes have been identified (Tomatsu et al, 2005). A S287L mutation (c.860C>Tc.860 C>T) was previously described in American, Austrian and Polish populations to cause a severe clinical phenotype (Bunge et al, 1997; Tomatsu et al, 2004). The S287L mutation affects the amino acids (p.G96V), and is placed on exon 8. Interestingly, more than 5% of all mutations were 3 missense mutations, and the 10 most frequent mutations (in over seven mutant alleles) were represented by single nucleotide changes (except for c.334delG). Those ten mutations account for 35.3% of all described mutations (Tomatsu et al, 2005).

Figure 1. Photo of the patient. (A) Short neck, macrocephaly, coarse face with broad mouth, short and anteverted nose and widely spaced teeth. Genu vara. (B) Kyphosis, prominent sternum.

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Figure 2. Bone X-ray. (B) Vertebra (lateral view): Platyspondyly with ovoid vertebrae and anterior projection and end-plates have irregular and rough surfaces. (B) Hip joints: Coxa valga, dysplastic and wave-like acetabula. (C) Hand: Hypoplastic scafoid and lunate bones. Madelung deformity of the radiocarpal articulation; and heads and bases of metacarpal bones spiky and mildly hypoplastic.

Our patient had normal intelligence, a severe form of bone dysplasia with marked platispondily, short neck and trunk plus severe kyphoscoliosis. In addition, joint restriction, especially in the hips was prominent and megalencephaly was also noted.

GALNS enzyme protein has been purified from human placenta as an oligomer with a molecular mass of 120 kDa, consisting of 40 and 15 kDa polypeptides linked by a disulfide bond (Masue et al, 1991). The model structure of GALNS has a monomeric from with two domains; the larger, N-terminal and the smaller, C terminal (Sukegawa et al, 2000). This model offerded the opportunity to analyze potential structural consequences of missense mutations in GALNS protein. Sukegawa K et al proposed three different reasons for the severe phenotype: destruction of the hydrophobic core or modification of the packing; removal of of a salt bridge to destabilize the entire conformation; modification of the active site

(Sukegawa et al, 2000). S287L, which is a semiconservative aminoacid change, affect the hydrophobic core and this substitution appears to break the packing and leading to a severe form of MPS IVA (Sukegawa et al, 2000).

MPS IVA is a rare disorder, and precise epidemiologic data are scare. The incidence of MPS IVA in Macedonia is unknown. However, this incidence was reported to be one per 76,000 live births in Northern Ireland (Nelson, 1997), one in 201 000 in Australia (Meikle et al, 1999), one in 450,000 live births in Portugal (Pinto et al, 2004). In Japan, the incidence was one in 500 000 live births (Tomatsu et al, 2005). For Tunisian MPS IVA patients, the incidence rate was approximately 2.8 in 100,000 live births (Laradi et al, 2006; Khedhiri, 2008).

Dental changes might be a prominent feature of MPS IVA. Our patients had brittle and thin dental enamel,

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Gucev et al: Severe phenotype of Morquio A disease Humbel R, Collart M (1975) Oligosaccharides in urine of patients with glycoprotein storage diseases. I. Rapid detection by thin-layer chromatography. Clin Chim Acta 60, 143-5. van Diggelen OP, Zhao H, Kleijer WJ, Janse HC, Poorthuis BJ, van Pelt J, Kamerling JP, Galjaard H (1990) A fluorimetric enzyme assay for the diagnosis of Morquio disease type A (MPS IV A). Clin Chim Acta 187, 131-9.

Masue M, Sukegawa K, Orii T, Hashimoto T (1991) Nacetylgalactosamine-6-sulfate sulfatase in human placenta, Purification and characterization J Biochem 110, 965-970.

Tomatsu S, Fakuda S, Masue M, Sukegawa K, Masuno M, Orii T (1992) Mucopolysaccharidosis type IVA, characterization and chromosomal localization of N-acetylgalactosamine-6sulfate sulfatase gene and genetic heterogeinity. Am J Hum genet 51(supplA), 178.

Bunge S, Kleijer WJ, Tylki-Szymanska A, Steglich C, Beck M, Tomatsu S, Fukuda S, Poorthuis BJ, Czartoryska B, Orii T, Gal A (1997) Identification of 31 novel mutations in the Nacetylgalactosamine-6-sulfatase gene reveals excessive allelic heterogeneity among patients with Morquio A syndrome. Hum Mutation 223-232.

Tomatsu S, Nishioka T, Montaño AM, Gutierrez MA, Pena OS, Orii KO, Sly WS, Yamaguchi S, Orii T, Paschke E, Kircher SG, Noguchi A (2004) Mucopolysaccharidosis IVA, identification of mutations and methylation study in GALNS gene. J Med Genet 41, e98 Nelson J (1997) Incidence of the mucopolysaccharidoses in Nothern Ireland. Hum Genet 101, 355-8.

Meikle PJ, Hopwood JJ, Clague AE, Carey WF (1999) Prevalence of lysosomal storage disorders. JAMA 281, 24954.

Pinto R, Caseiro C, Lemos M, Lopes L, Fontes A, Ribeiro H, Pinto E, Silva E, Rocha S, Marcão A, Ribeiro I, Lacerda L, Ribeiro G, Amaral O, Sá Miranda MC (2004) Prevalence of lysosomal storage diseases in Portugal. Eur J Hum Genet 12, 87-92.

Laradi S, Tukel T, Khediri S, Shabbeer J, Erazo M, Chkioua L, Chaabouni M, Ferchichi S, Miled A, Desnick RJ (2006) Mucopolysaccharidosis type IV, N-acetylgalactosamine-6sulphatase mutations in Tunisian patients. Mol Genet Metab 87, 213-218.

Khedhiri S (2008) Mucopolysaccharodoses type I and IVA, Clinical features and consanguinity in Tunisia, Pathologie Biologie, doi, 10.1016/j.patbio.

Beck M, Glossl J, Grubisic A, Spranger J (1986) Heterogeneity of Morquio disease. Clin Genet 29, 325-331.

Levin LS, Jorgenson RJ, Salinas CF (1975) Oral findings in the Morquio syndrome (mucopolysaccharidosis IV) Oral Surg Oral Med Oral Path 39, 390-395.

Nelson J, Kinirons M (1988) Clinical findings in 12 patients with MPS IV A (Morquio's disease), further evidence for heterogeneity. Part II, dental findings. Clin Genet 33, 121125.

changes previously described by other authors (Levin et al, 1975; Beck et al, 1986; Nelson and Kinirons, 1988).

Although our patient was young he had corneal clouding further indicating the severity of the phenotype.

However, no aortic regurgitation was present which might indicate that the severity of the symptoms is not always linked to all the systems involved. Born at term with unknown birth length, his growth velocity deteriorated since the age of 3. It also seems that the more severe form of the disease the earlier the start of the growth delay. So far, in spite of the severity of the phenotype the patient did not develop cord compression as the result of the severity of the defects of vertebrae. His history included frequent upper resiratory infections. The earliest signs of the disease were the thoracic changes: flaring of the ribs and prominent sternum.

In summary, it is obvious that the described S287L mutation (c.860C>Tc.860 C>T) in this boy resulted in an early and severe clinical phenotype.The identification of this mutation provide the opportunity to this family to have a prenatal diagnosis to ovoid another child suffering for this syndrome.

Acknowledgments We wish to express our thankfulness to Shunji Tomatsu and his team from the Department of Pediatrics, Saint Louis University, Pediatric Research Institute St. Louis, Missouri, USA, for the sequencing of the GALNS gene.

References Matalon R, Arbogast B, Justice P, Brandt IK, Dorfman A (1974) Morquio’s syndrome, deficiency of a chondroitin sulfate Nacetylhexosamine sulfate sulfatase. Biochem Biophys Res 61, 709-715.

Tomatsu S, Montaño AM, Nishioka T, Gutierrez MA, Peña OM, Tranda Firescu GG, Lopez P, Yamaguchi S, Noguchi A, Orii T (2005) Mutation and polymorphism spectrum of the GALNS gene in mucopolysaccharidosis IVA (Morquio A) Hum Mutat 26, 500-512.

Sukegawa K, Nakamura H, Kato Z, Tomatsu S, Montaño AM, Fukao T, Toietta G, Tortora P, Orii T, Kondo N (2000) Biochemical and structural analysis of missense mutations in N-acetylgalactosamine-6-sulfate sulfatase causing mucopolysaccharidosis IVA phenotypes. Hum Mol Genet 9, 1283-1290. de Jong JG, Wevers RA, Laarakkers C, Poorthuis BJ (1989) Dimethylmethylene blue-based spectrophotometry of glycosaminoglycans in untreated urine, a rapid screening procedure for mucopolysaccharidoses. Clin Chem 35, 14721477.

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Attenuation of experimental liver fibrosis by hepatocyte growth factor gene delivery mediated by adenovirus Research Article

Yin Xu1,2, Fei-qun Zheng2,3, Jia Fang1,2, Qun-wei Zhang2, Yi-de Qin1, Yang Liu2, Ren-jie Yang3, Bin Wu2 1

Basic Medical Science School, Anhui Medical University, Hefei 230032, Anhui Province, China Department of Experimental Hematology, Beijing Institute of Radiation Medicine, Beijing 100850, China 3 Key laboratory of Carcinogenesis and Translational Research (Ministry of Education), Department of Interventional Therapy, Peking University School of Oncology, Beijing Cancer Hospital & Institute, Beijing 100036, China 2

__________________________________________________________________________________ *Correspondence: Dr. Bin Wu, Department of Experimental Hematology, Beijing Institute of Radiation Medicine, 27 Taiping Road, Beijing 100850, China; Tel: +86-10-66932202; Fax: +86-10-68158312; e-mail: wubin63@yahoo.com.cn Dr. Ren-jie Yang, Department of Interventional Therapy, Peking University School of Oncology, Beijing Cancer Hospital & Institute, Beijing 100036, China; Tel: +86-10-88196324; Fax: +86-10-88131600; e-mail: renjieyang2007@163.com Key words: Liver fibrosis; Hepatocyte growth factor; Transforming growth factor; Gene therapy; Adenovirus Abbreviations: adenovirus, (Ad); albumin, (ALB); carbon tetrachloride, (CCl4); extracelluar material, (ECM); glutamate pyruvvate transminase, (GPT); glutamic oxaloacetic transminase, (GOT); hepatocyte growth factor, (HGF); hydroxyproline, (Hyp); plaque-forming units, (PFU); total billirubin, (Tbil); total protein, (TP); transforming growth factor-!1, (TGF-!1)

Yin Xu and Fei-qun Zheng contributed equally to this work.

Received: 7 November 2008; Revised: 5 January 2009 Accepted: 8 January 2009; electronically published: January 2009

Summary The hepatocyte growth factor (HGF), originally identified and cloned as a potent mitogen for hepatocytes, has an essential part in the development and regeneration of the liver. In this study, HGF expression in vitro and in vivo was determined using ELISA. Rats were injected subcutaneously with CCl4 for eight weeks to induce liver fibrosis, and then divided randomly into groups for administration of various doses of adenovirus HGF (Ad-HGF) or vehicle. All rats were sacrificed 8 weeks after obtaining samples of serum and hepatic tissue. The results showed that glutamic oxaloacetic transaminase (GOT), glutamate pyruvate transaminase (GPT), total protein (TP), albumin (ALB), and total bilirubin (TBil) in serum were significantly recovered after gene therapy (P<0.05). AdHGF also attenuated the expression of TGF-!1 and the deposition of collagen. We conclude that intravenous administration of Ad-HGF may be useful for the treatment of fibrotic liver by promoting liver function recovery and collagenolytic capacities.

an increase in the production of extracellular matrix components, such as laminin and collagen, which results in liver fibrosis (Hayashi et al, 2008). There is no effective treatment for this disease, other than liver transplantation (Pinzani and Rombouts, 2004).

The pathogenesis of liver fibrosis is characterized by the excess production and deposition of collagen, which could frustrate the normal hepatic parenchyma (Xia et al, 2006). There are several reports that many growth factors participate in the progression of liver fibrosis, for instance, hepatocyte growth factor (HGF), transforming growth factor-!1 (TGF-!1) and platelet-derived growth factor

I. Introduction Liver fibrosis is a common result of chronic hepatic diseases caused by various types of injurious trauma and inflammatory agents, such as hepatitis virus, chemical toxicity, alcohol and autoallergy. Liver consists of parenchymal (hepatocytes) and non-parenchymal cells (Kupffer, stellate, and endothelial cells), and activation of Kupffer cells by membrane components from impaired hepatocytes and infiltrating inflammatory cells leads to the secretion of pro-fibrotic factors, such as reactive oxygen species. These pro-fibrotic factors activate hepatic stellate cells, leading to a change of myofibroblast phenotype and 387

Xu et al: HGF gene therapy on liver fibrosis (PDGF), which regulate various cellular functions and act antagonistically against each other (Borkham-Kamphorst et al, 2007; Doh et al, 2008; Ogura et al, 2001). Matsuda et al reported that expression of HGF mRNA in the liver decreases gradually following initial fibrosis induced by treatment with dimethylnitrosamine (DMN), whereas TGF-!1 mRNA is over-expressed persistently during the entire period. Consistent with this, the level of plasma HGF decreased during the onset of hepatic fibrosis following the initial elevation due to treatment with DMN, which is a consequence of apoptotic and fibrotic stress (Matsuda et al, 1995). Both chronic and acute liver injury can induce transient elevation of the level of HGF (Cui et al, 2008). Tsubouchi et al developed an enzyme-linked immunosorbent assay (ELISA) with high levels of specificity and sensitivity for HGF in human serum. They found that levels of HGF in the serum of patients with acute hepatitis, chronic hepatitis and cirrhosis were higher than those in normal subjects (Tsubouchi et al, 1991).

These results suggest strongly that HGF may be a key factor in the pathogenesis of liver fibrosis.

HGF is a multifunctional polypeptide that elicits mitogenic, motogenic and morphogenic activities, and is known to be the most potent mitogen for parenchymal hepatocytes but not for non-epithelial liver stromal cells (Matsuda et al, 1995). HGF stimulates proliferation of epithelial and endothelial cells (Nakamura et al, 1986; Bussolino et al, 1992), and triggers the 'scatter' effect by inducing cell dissociation and migration (Stoker et al, 1987). HGF increases the formation of branching tubules by epithelial cells grown in a collagen gel matrix (Montesano et al, 1991; Brinkmann et al, 1995; Medico et al, 1996), and prevents cell death induced by inhibition of adhesion (Frisch and Francis, 1994). The receptor for HGF is the heterodimeric tyrosine kinase encoded by the c-met proto-oncogene (Giordano et al, 1989; Bottaro et al, 1991; Naldini et al, 1995). HGF receptor signaling is mediated by phosphorylation of a multifunctional docking site located in the C-terminal region that interacts with multiple SH2-containing signal transducers (Ponzetto et al, 1994). The biological response is elicited by the concomitant activation of multiple intracellular effectors, including phosphatidylinositol 3-kinase and the Ras pathway (Graziani et al, 1993; Ponzetto et al, 1993).

In vivo, HGF produced resolution of fibrosis in the cirrhotic liver, inhibited hepatocyte apoptosis and stimulated hepatocyte mitosis, resulting in the survival of rats with an otherwise lethal illness (Ueki T et al, 1999).

Reduction of TGF-!1 expression and collagen deposition is the most important pathway for the attenuation of liver fibrosis via HGF (Jiang et al, 2008). The curative effect of HGF has been elucidated by many studies. The half-life of exogenous HGF in blood circulation is only 3–5 min; therefore, the application of HGF is limited (Kawaida et al, 1994). Gene therapy is a potential strategy to overcome this problem, which could allow cells to secrete HGF persistently and maintain it in the serum (Xue et al, 2003).

Carbon tetrachloride (CCl4) is widely used to induce toxic liver injury and fibrosis in laboratory animals, and it was used to induce liver fibrosis in this study. It has been suggested that CCl4-induced hepatotoxicity involves the

metabolism of CCl4 by cytochrome P450 to the trichloromethyl radical (CCl3·), leading to lipid peroxidation (Lee et al, 2007). This process is followed by the activation of Kupffer cells, which is accompanied by the production of proinflammatory mediators and profibrotic factors (Planagumà et al, 2005).

HGF has an important role in liver regeneration and amelioration of fibrosis, and we supposed that systemic administration of Ad-HGF might have therapeutic potential in the treatment of CCl4-induced liver fibrosis.

To test this possibility, the anti-fibrotic role and therapeutic effect of Ad-HGF were determined in a rat model.

II. Materials and Methods A. HGF expression in vitro and in vivo Hepatocytes were isolated from adult male Wistar rats by collagenase perfusion as described (Cui et al, 2008). The isolated hepatocytes, showing more than 90% viability by trypan blue exclusion, were suspended in complete culture medium (Williams’ medium E supplemented with 10% fetal calf serum, 5 mM Hepes, 100 U/ml penicillin, 0.1 mg/ml streptomycin, 10 nM dexamethasone, and 10 nM insulin), diluted to 1 " 106 cells/ml, and seeded onto 12-well plates (Costar, USA). The cells were transfected with vehicle vector or Ad-HGF at a multipicity of infection (MOI) of 100. After incubation for 2 h, viruses were removed by rinsing twice with PBS, and then cultured for 48 h in serum-free medium. The conditioned medium was collected and analyzed by ELISA (Bio-source, USA).

Rats were given 1 " 109 plaque-forming units (PFU) of vehicle vector or Ad-HGF by intravenous injection, and plasma was collected 5, 7, 11 and 14 days later and analyzed by ELISA.

B. Animal Model Adult male Wistar rats (30; body weight 200–280g) were obtained from the Academy of Military Medical Sciences (Beijing, China) and housed under conventional clean conditions.

All animals received humane care and the experimental protocol was approved by the Committee of Laboratory Animals according to the guidelines of the Institute of Radiation Medicine (Beijing, China).

Six rats were used as the control group (group A). On the first day of the study, the other 24 rats were each given a single subcutaneous injection of CCl4 (a 2:3 (v/v) mixture of CCl4 (400 mL/L) and olive oil) at a CCl4 dose of 5mL/kg body weight, and a single subcutaneous injection of the CCl4/oil mixture at a CCl4 dose of 3mL/kg body weight twice a week for eight weeks. The 24 CCl4-treated rats were divided at random into four groups of 6 (groups B – E). Group B was the 5 " 109 PFU vehicle-infused group. Group C was the 1 " 109 PFU Ad-HGF-infused group.

Group D was the 2.5 " 109 PFU Ad-HGF-infused group. Group E was the 5 " 109 PFU Ad-HGF-infused group. After injection of CCl4/oil for four weeks, adenoviruses were infused through the tail vein each two days, five times totally. The model schedule and treatment are shown in Figure 1.

C. Biochemical Assays Blood samples were taken at the time of sacrifice. Serum biochemical parameters glutamic oxaloacetic transaminase (GOT), glutamate pyruvate transaminase (GPT), total protein (TP), albumin (ALB), and total bilirubin (TBil) were determined by an automated analyzer in the Clinical Laboratory in Beijing Cancer Hospital.

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Figure 1 Schedule of CCl4 adminstration and injection of vehicle or Ad-HGF. Rats were given CCl4 by intraperitoneal injection for 8 weeks to produce liver fibrosis. Vehicle vectors or various doses of Ad-HGF were injected 5 times from the 4th week after the first injection of CCl4. The 30 adult male rats were divided into five groups: A, untreated control; B, 5 " 109 PFU of vehicle; C, 1 " 109 PFU of Ad-HGF; D, 2.5 " 109 PFU of Ad-HGF; E, 5 " 109 PFU of Ad-HGF. Group A was infused with 100#l of PBS each time.

Group B was infused with 1 " 109 PFU of vehicle vectors in 100#l of PBS each time.

Group C was infused with 1 " 109 PFU of Ad-HGF in 100#l of PBS the first time, and with 1 " 109 PFU of vehicle vector in 100#l of PBS the second to fifth time.

Group D was infused with 1 " 109 PFU of Ad-HGF in 100#l of PBS the first and second time, with 5 " 108 PFU of Ad-HGF in 100#l of PBS the third time, and with 1 " 109 PFU of vehicle vectors in 100#l of PBS the fourth and fifth time.

Group E was infused with 1 " 109 PFU of Ad-HGF in 100#l of PBS each time.

increased about 44-fold and reached a concentration of 8.8 ng/ml in the culture supernatant of Ad-HGF infected cells.

To elucidate HGF expression in vivo, normal rats were injected intravenously with 1 " 109 PFU of vehicle or Ad-HGF. A substantial amount of HGF in the plasma of rats after two weeks was detected by ELISA (Figure 2).

The concentration of plasma HGF increased about 5-fold and exceeded 50 ng/mL for at least 10 days in the AdHGF-injected rats.

D. Hydroxyproline Content The hydroxyproline content of liver samples was measured with a hydroxyproline assay kit (Nanjing Jiancheng Bioengineering Institute, China). Briefly, liver samples (30–40 mg) were homogenized in distilled water. The homogenate was hydrolyzed by incubation in 10 mol/L HCl at 110ºC for 18 h. The hydrolysates were dried by speed vacuum centrifugation for 3–5 h and then dissolved in 0.2 mol/L citric acid, 0.2 mol/L glacial acetic acid, 0.4 mol/L sodium acetate, 0.85 mol/L sodium hydroxide, pH 6.0. Hydroxyproline in the hydrolysates was measured as described (Ren et al, 2007).

B. Ad-HGF alleviate hepatosis caused by CCl4 Injection

E. Histological and Immunohistochemical Staining

Repeated administration of CCl4 has been shown to cause hepatocyte destruction and liver dysfunction, resulting in the manifestation of chronic liver injury (Nagano et al, 2007). Figure 3 shows the morphological changes of the livers of virus-injected rats. The surface of the liver was coarse and pale in the model group, while it was glossy and ruddy in the normal and the 5 " 109 PFU Ad-HGF infused group. As shown in Table 1, the injection of CCl4 resulted in a significant increase in GOT/GPT from 175.9/56.4 U/L in the normal control group to 469.7/110.3 U/L in the model group, and was reduced significantly, to 336.1/80.4 U/L, in the 5 " 109 PFU Ad-HGF infused group compared with the model group (*P <0.05). The TP, ALB and Tbil levels in serum were determined to evaluate liver function. The levels of TP and ALB in rat serum decreased to 49.6 g/L and 22.9 g/L, respectively, in the model group from 60.3 g/L and 29.3 g/L in the normal group. The TP and ALB levels in the liver injury rats recovered to 55.3 g/L and 27.7 g/L after administration of 5 " 109 PFU Ad-HGF (*P <0.05).

The level of Tbil also recovered from 28.1 #mol/L in the model group to 15.2 #mol/L in the 5 " 109 PFU Ad-HGF treated group (*P <0.05). The histological sections showed significant necrosis and inflammation in the model group, while 5 " 109 PFU Ad-HGF was effectively able to relieve the histopathological changes of hepatic cells injured by administration of CCl4 (Figure 4).

Liver tissue sections were stained with hematoxylin and eosin (H&E) for histopathological examination or with Sirius red for collagen determination (Duan et al, 2003). The expression of TGF-!1 was detected by immunohistochemical staining. The paraffin sections of left median hepatic lobes were incubated with 30 ml/L H 2O2 in methanol at 37ºC for 10 min to quench endogenous peroxidase activity. The sections were blocked at room temperature for 20 min, then incubated with antibodies against TGF-!1 (Santa Cruz, CA) overnight at 4ºC. The sections were washed with PBS then treated with DAB to stain.

F. Statistical Analysis All data are expressed as mean ± SD. Differences between mean values of groups were tested for statistical significance (P !0.05) by the Kruskal-Wallis test using the SAS system.

III. Results A. HGF expression in vitro and in vivo Currently, the clinical use of adenovirus is limited to local application; systemic administration leads to redundant transgene expression in the liver (Yao et al, 2007). However, this characteristic may be used to treat liver disease. Using an MOI of 100, primary cultured rat hepatocytes were transfected with vehicle vector or AdHGF. The expression of the HGF transgene was determined by ELISA (Figure 2). HGF secretion was

389

Xu et al: HGF gene therapy on liver fibrosis Figure 2. Expression of HGF in vitro and in vivo. (A) Primary rat hepatocytes were infected at MOI of 100, and HGF expression was measured by ELISA in the culture supernatant 48 h post infection.

(B) The rats were given 1 " 109

PFU of vehicle vector or AdHGF intravenously, and the plasma HGF was determined by ELISA. Values are expressed as mean Âą SD.

Figure 3. Morphology of livers in virus injected rats. The livers were excised and photographed. Note the morphological changes and the smaller volume of livers treated with Ad-HGF versus livers treated with vehicle alone.

390

Gene Therapy and Molecular Biology Vol 12, page 391 Table 1. Effects of Ad-HGF on liver function. Glutamic oxaloacetic transaminase (GOT) glutamate pyruvate transaminase (GPT), and total billirubin (TBil) were markedly reduced, whereas total protein (TP) and albumin (ALB) were increased significantly in the Ad-HGF-injected group. Values are expressed as mean ± SD (n = 6). *P <0.05, **P <0.01 versus with CCl4 + 5 " 109 PFU in the vehicle group.

Group Normal

n 6

GOT (U/L) 175.9±11.9**

GPT (U/L) 56.4±6.0**

TP (g/L) 60.3±5.1**

ALB (g/L) 29.3±1.0**

Tbil ("mol/L) 8.3±1.0**

CCl4 + 5"109PFU vehicle

6

469.7±83.5

110.3.±16.8

49.6±3.0

22.9±2.6

28.1±1.5

9

6

404.4±73.5

102.2±16.4

52.7±6.9

23.4±1.7

19.9±3.0**

6

394.8±59.3

96.0±12.6

53.3±6.6

25.4±1.8**

18.1±2.9**

6

336.1±61.0*

80.4±5.8**

55.3±4.7*

27.7±1.9**

15.2±3.2**

CCl4 + 1"10 PFU Ad-HGF 9

CCl4 + 2.5"10 PFU Ad-HGF 9

CCl4 + 5"10 PFU Ad-HGF

Figure 4. Attenuation of liver fibrosis by HGF gene therapy. Extensive interstitial collagen stain was noticeable in liver sections of the rat injected with vehicle and pseudolobule formations were found in this group. The collagen content and TGF-!1 expression were decreased significantly with increasing dose of Ad-HGF. (A) Histological sections stained with H&E (original magnification, " 100).

(B) Collagen content determined by staining with Sirius red (original magnification, " 100). (C) TGF-!1 expression, determined by staining with antibody to TGF-!1 (original magnification, " 400).

391

Xu et al: HGF gene therapy on liver fibrosis hepatic expression of TGF-!1, while the level of TGF-!1 was extremely low in normal liver. Treatment with AdHGF largely suppressed its induction by CCl4.

C. Ad-HGF attenuate the fibrosis induced by chronic liver injury Hepatic fibrosis is the result of the wound-healing response of the liver to chronic injury. In acute liver injury, parenchymal cells regenerate and replace the necrotic and apoptotic cells. This process is associated with an inflammatory response and a limited deposition of extracelluar material (ECM). If the injury is chronic and persistent, however, liver regeneration eventually fails, and hepatocytes are substituted with abundant ECM. HGF is a potent activator of latent hepatic collagenases that promote the degradation of ECM. In order to evaluate the effect of Ad-HGF on hepatic fibrosis, rats were injected with various doses of Ad-HGF. Figure 4 shows representative micrographs of liver tissue sections stained with Sirius red. In rats treated with vehicle alone, extensive deposition of collagen was observed (Figure 3 B); however, it was markedly reduced after administration of Ad-HGF. In addition, biochemical methods were used to determine the hydroxyproline content of the hydrolysates extracted from liver tissue. This assay is based on the observation that essentially all of the hydroxyproline in animal tissues is found in collagen. As shown in Figure 5, the quantitative assay of liver hydroxyproline content revealed an increase in the liver extracts at 8 weeks after the injection of CCl4, suggesting increasd hepatic fibrosis; while that in the 2.5 " 109 PFU and 5 " 109 PFU Ad-HGF injected groups was lower than that in vehicle injected group (*P <0.05). The results indicated the high dose of Ad-HGF was more effective for fibrosis reduction than low dose.

IV. Discussion Liver fibrosis is a process of liver cirrhosis, which is associated with most chronic liver diseases and thought to be reversible; nevertheless, there is no reliable treatment in current clinical practice to reverse this pathological process. There is growing evidence that several growth factors participate in this procession. Hepatic injury can induce a transient high concentration of HGF in the liver, which is the stress reaction to trauma and has a crucial role in liver regeneration. There are two variants of HGF, an active single-chain protein (scHGF), which is cleaved proteolytically at the Arg-Val-Val site to form an active two-chain HGF (tcHGF). The two variants have the ability to bind the HGF receptor c-Met, but only tcHGF can activate the c-Met tyrosine kinase domain (Shima et al, 1994). It has been hypothesized that scHGF activation is blocked in cirrhotic liver, which induced the retarded regeneration (Xue et al, 2003). Chang-Goo Huh reported that loss of c-Met appeared not to be detrimental to hepatocyte function under physiological conditions, but enhanced Fas-induced apoptosis (Huh et al, 2004). c-Met tyrosine kinase can upregulate many downstream signal pathways, such as extracellular signal-regulated kinasemitogen-activated protein kinase (ERK1/2-MAPK), phosphatidylinositol 3-kinase (PI3K), sphingosine kinasesphingosine 1 phosphate-endothelial differentiation gene (SPK-S1P-DEG), which mediate the multifunction of HGF (Duan et al, 2004). Two different mechanisms have been proposed to explain the antifibrotic effects of HGF. One is proposed to promote the activity of hepatic collagenase and accelerate the degradation of the ECM. The other is proposed to be a reduction of protein levels of procollagens and TGF-!1 (Xue et al, 2003). TGF-!1 is a crucial factor in the liver cirrhosis process and a potent growth inhibitor of hepatocytes, which could serve as a chemoattractant for fibroblasts and monocytes/macrophages, and induce these cells to secrete pro-inflammatory and fibrogenic cytokines; for example, TNF-$, IL-1!, and TGF-!1 itself. Ueki and colleagues reported that HGF could antagonize TGF-!1 directly, thus improving liver regeneration (Chen et al, 2005).

D. Measurement of TGF-!1 Expression TGF-! is the most intensively studied regulator of the ECM and has an important role in the development of liver fibrosis (Clouthier et al, 1997). There are three isotypes of TGF-! in mammals, TGF-!1, TGF-!2, and TGF-!3, which all have similar biological activity; however, liver fibrosis is attributed primarily to the TGF!1 isoform (Gorelik and Flavell, 2002). As TGF-!1 is critical to elicit liver fibrosis, we asked whether HGF would alter the expression of TGF-!1 in the liver under fibrosis conditions. We examined the expression of protein TGF-!1 in the liver by immunohistochemical staining. As shown in Figure 4 C, CCl4 induced a dramatic increase in

Figure 5. Total tissue hydroxyproline content. The hydroxyproline content was determined by biochemical assay. Data were expressed as micrograms of hydroxyproline per milligram of tissue and presented as mean Âą SD (n=6). *P<0.05 versus with CCl4 + 5"109PFU vehicle group.

392

Gene Therapy and Molecular Biology Vol 12, page 393 In addition, injuries associated with hypoxia and neovascularization are related to the progression of liver fibrosis (Chaparro et al, 2007). Neovascularization includes angiogenesis and vasculogenesis, representing formation of blood vessels by distinction of endothelial progenitor cells. HGF has been recognized as one of the most efficient angiogenetic factors and endothelial chemoattractants, which also mobilizes endothelial progenitor cells and bone marrow stem cells to participate in injury repair and in vasculogenesis (Purdie et al, 2002; Van Belle et al, 1998). Therefore, HGF should be one of the most efficient growth factors, with the ability to promote liver regeneration and rivalry fibrosis.

Unfortunately, the half-life of the HGF protein is very short in the blood circulation. Accordingly, gene therapy is needed urgently to apply in liver disease. Adenovirus, which is in general use in gene therapy, is utilized to treat many diseases. In earlier work, Ad-HGF was proven to cure myocardial ischemia efficiently, which has been applied in clinical research in China PR. Yao et al showed the level of gene expression in liver induced by intravenous injection of adenovirus is significantly higher than that in other organs (Yao et al, 2007), which indicates the strong probability of systemic administration of adenovirus for liver disease gene therapy. In this study, we proved systemic administration of 1 " 109 PFU of Ad-HGF could upregulate the plasma HGF level significantly and maintain it for at least 10 days. That means Ad-HGF therapy effect may be through both hepatocytesâ&#x20AC;&#x2122; autocrine HGF and paracrine HGF from circulation. However this dose of Ad-HGF cannot attenuate the extent of CCl4-induced liver fibrosis. The 5 " 109 PFU of Ad-HGF injected intravenously recovered the serum levels of GOT, GPT, TP, ALB, and TBil significantly, which indicated the chronic injury induced

by CCl4 was repaired. The Hyp content may represent hepatic collagens, which are major extracellular matrix proteins in hepatic fibrosis. In this study, the Hyp content was decreased, which coincided with the reduction of collagen deposition observed by staining with H&E and with Sirius red. Immunohistochemical staining showed the expression of TGF-!1 was attenuated in the gene therapy group. In histological sections, we observed the pesudolobule formation in the control group, which was reduced significantly in the Ad-HGF-injected group. There was no significant change of liver function or collagen deposition (data not shown), indicating that Ad-HGF therapy may be ineffective against severe liver cirrhosis.

The starting effective dose in rat models is 5 " 109 PFU, so the counterpart in humans should exceed 1 " 1012 PFU. This high dose may carry clinical risk to some extent. It is therefore important to consider means to reduce the dose of adenovirus administeed as well as ways to alter the tropism of adenovirus; for instance, utilizing albumin as a promoter and enhancer to control the specificity of gene expression.

In conclusion, adenovirus gene therapy is a convenient and efficient way to express high levels of exogenous HGF in vivo. Here, we evaluated intravenous injection of Ad-HGF as a method to transfect the HGF gene and maintain the serum level of HGF that would be

suitable for treating chronic liver injury. It will be important to examine the feasibility of systemic therapy with 5 " 109 PFU of Ad-HGF, which could decrease the amount of collagen deposited and accelerate normalization of liver function. Thus, Ad-HGF systemic therapy is a potential therapeutic method for liver fibrosis in a clinical setting.

Acknowlegements This project was supported by Chinese National High-Tech R&D Program, No. 2003AA216081.

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Gene Therapy and Molecular Biology Vol 12, page 395 Gene Ther Mol Biol Vol 12, 395-404, 2008

Regulation of hormonal therapy resistance by cell cycle machinery Review Article

Binoj Chandrasekharan Nair, Ratna K. Vadlamudi* Department of Obstetrics and Gynecology, The University of Texas Health Science Center at San Antonio, San Antonio, Texas 78229

__________________________________________________________________________________ *Correspondence: Ratna K. Vadlamudi, Department of Obstetrics and Gynecology, University of Texas Health Science Center, Floyd curl drive, San Antonio, TX, 78229-3900, USA; Tel: 210-567-4930; Fax: 210-567-4958; e-mail: vadlamudi@uthscsa.edu Key words: Cell Cycle, CDKs, Estrogen, Estrogen Receptor, Co-regulators, Breast cancer, Therapy resistance, Antiestrogens Abbreviations: cyclin-dependent kinase, (CDK); epidermal growth factor, (EGF); estrogen receptor, (ER); mitogen-activated protein kinase, (MAPK); modulator of nongenomic actions of the ER, (MNAR); nuclear receptor, (NR); phosphatidylinositol-3 kinase, (PI3K); proline-, glutamic acid-, and leucine-rich protein, (PELP); protein kinase A, (PKA); retinoblastoma protein, (pRb)

Received: 11 December 2008; Revised: 30 December 2008 Accepted: 31 December 2008; electronically published: January 2009

Summary Estrogen Receptor (ER) plays a central role in the development and progression of breast cancer. Hormonal therapy substantially improves disease-free survival of ER+ve breast tumors, however acquired resistance to endocrine therapies frequently occur. Emerging data implicate growth factor signaling pathways and their cross talk with ER as major cause of resistance. Both these pathways have been recently shown to use cell cycle machinery as downstream effectors in mediating therapy resistance. Several studies have demonstrated deregulation of cell cycle regulators and their cross talk with ER in therapy resistant tumors. The objective of this article is to review the underlying mechanisms by which tumor cells use cell cycle machinery to override hormonal therapy and to explore cell cycle machinery components as novel therapy targets for overcoming hormonal therapy resistance.

factor signaling pathways and its cross talk with ER as a major cause of resistance (Shou et al, 2004). Both these pathways have been recently shown to use cell cycle machinery as downstream effectors in mediating therapy resistance (Shou et al, 2004; Perez-Tenorio et al, 2006; Ru et al, 2006). The prime focus of this review is to recapitulate the literature elucidating the role of cell cycle machinery as downstream effectors of various pathways leading to hormone therapy resistance.

I. Introduction Steroidal hormone estradiol (E2) and Estrogen Receptor (ER) plays a central role in the development and progression of breast cancer and 70-80% of breast tumors are ER positive at the time of presentation (McGuire and Clark, 1992). ER positive tumors respond well with therapeutic agents targeting ER functions (Ariazi et al, 2006). Endocrine therapy using Tamoxifen, a selective estrogen receptor modulator (SERM), has been shown to improve relapse-free and overall survival (Lewis-Wambi and Jordan, 2005). More recently, aromatase inhibitors, which deplete peripheral estrogen (E2) synthesis, are shown to substantially improve disease-free survival in postmenopausal women (Leary and Dowsett, 2006).

Despite the success of antiestrogens, de novo and/or acquired resistance to endocrine therapies frequently occur. Approximately 30% of these patients acquire resistance to endocrine therapy in later stages and is a significant problem in the treatment regime (Riggins et al, 2007). Although mechanisms for hormonal therapy resistance remain elusive, emerging data implicate growth

II. Estrogen coregulators

receptors

and

The human estrogen receptor (ER) is a key transcriptional regulator in breast cancer biology (Green and Carroll, 2007; Heldring et al, 2007). The biological effects of estrogen is mediated by its binding to the structurally and functionally distinct ERs (ER! and ER") (Warner et al, 1999). ER ! is the major ER in the mammary epithelium and this has been further shown by ER (Esr1) knockout mice, which display grossly impaired ductal epithelial cell proliferation and branching 395

Nair and Vadlamudi: Cell cycle machinery in therapy resistance (Lubahn et al, 1993; Bocchinfuso and Korach, 1997). ERs comprises an N-terminal activation function 1 (AF1) domain, a DNA-binding domain, and a C-terminal ligand binding region that contains an activation function 2 (AF2) domain (Kumar et al, 1987). The AF-2 of the ER is located in the ligand binding domain, while the N-terminal AF-1 functions in a ligand-independent manner. AF-1 and AF-2 exhibit cell type and promoter context specificity (Berry et al, 1990). Upon binding of E2 to ER, the ligandactivated ER translocates to the nucleus, binds to the responsive element in the target gene promoters, and stimulates gene transcription (genomic/nuclear signaling) (McKenna et al, 1999; McDonnell and Norris, 2002). In addition to its well-studied nuclear functions, ER also participates in non-genomic signaling events in the cytoplasm and membrane. Such signaling has been linked to rapid responses to E2 which generally involves the stimulation of the Src kinase, MAPK, and AKT (Pedram et al, 2002).

Transcriptional activity of ERs is regulated not only by hormones but also by several coregulatory proteins called coactivators and corepressors (McKenna et al, 1999). The transcription functions of ER are shown to be influenced by several coactivators, including SRC1, GRIP1, AIB1, PELP1 and corepressors including nuclear receptor corepressor (NCoR), silencing mediator for retinoic and thyroid receptor (SMRT) and MTA1 (Tsai and O'Malley, 1994; Barnes et al, 2004). Coactivators preferentially associate with ligand bound ER while corepressors have been shown to preferentially associate with antagonist occupied ERs (Jepsen and Rosenfeld, 2002). Evidence suggests that multi-protein complexes containing coactivators, ERs, and transcriptional regulators assemble in response to hormone binding and activate transcription (McKenna et al, 1999).

Accumulating evidence suggests that ER-coregulators play an essential role in hormonal responsiveness and cancer progression (Bocchinfuso and Korach, 1997; McKenna et al, 1999).

III. Estrogen progression

and

cell

controls transition through M-phase. The kinases are traditionally known to phosphorylate many key downstream substrates, most notably retinoblastoma and exhibit strict and elegant control of cell cycle progression.

In addition, Cyclin D1 was identified as a target of E2 action, and estrogen treatment was shown to up-regulate Cyclin D1 levels (Altucci et al, 1996). Up-regulation of Cyclin D1 by ER signaling is accompanied by an increased proliferative response in breast cancer cells. E2 is shown to induce Cdc25A, a tyrosine phosphatase that controls G1-S transition in cell cycle by regulating the dephosphorylation of Cyclin-dependent kinase complexes (Ru et al, 2006). Collectively, these findings suggest that Estrogen induces proliferation of ER-positive breast epithelial cells by stimulating G1/S transition, which is associated with increased cyclin D1 expression and activation of CDKs (Foster et al, 2001). Since CDK4 and CDK2 are key players for G1-S transition in the cell cycle and for tumorigenesis, ER crosstalk with CDKs will have implications in therapy resistance.

IV. ER coregulators and cell cycle progression Evolving evidence suggests that many of the ER coregulators play a vital role in cell cycle progression.

Emerging evidence suggest that oncogenic ERcoregulatory proteins such as AIB1, PELP1 modulate Cyclin D1 expression and function, thus may enhance tumorigenesis and therapy resistance. We have summarized below some of the ER coregulators that are shown to play a role in E2-ER mediated cell cycle progression.

A. AIB1 ER coregulator SRC3/AIB1 is shown to regulate cell cycle machinery in numerous ways. AIB1 is shown to enhance E2-dependent induction of Cyclin D1, suggesting a role for ER coregulators in modulating Cyclin D1 expression (Planas-Silva et al, 2001). AIB1 is also shown to interact with E2F directly and modulate its transactivation function and is required for E2F1-mediated gene expression (Louie et al, 2004). Recent evidence also suggests that AIB1 has oncogenic potential and the transformation ability of AIB1 has been ascribed to its ability to control the expression of genes important for initiating DNA replication like cdc6, MCM7, Cyclin E, and CDK2 (Louie et al, 2006). E2F regulates AIB1 expression by cooperating with the transcription factor specificity protein 1 (Sp1) without direct interaction with E2F consensus sites, suggesting a positive feedback regulatory loop comprising of E2F and AIB1 (Mussi et al, 2006)

cycle

It is well accepted that estrogen induces mitogenesis by recruiting non-cycling cells into the cell cycle and by increasing the rate of progression from G1 to S phase.

However, the molecular mechanism by which E2-ER signaling controls cell proliferation is not completely understood. Induction of the early-response genes (such as c-myc and c-fos) is proposed as one mechanism of this process (Prall et al, 1998a; Lamb et al, 2000), whereas regulation of Cyclin Dependent Kinase (CDK2 and CDK4) activities was proposed as another (Neuman et al, 1997; Prall et al, 1997; Foster et al, 2001). Each phases of cell cycle (G1, S, G2 and M) is strictly under the control of different Cyclins and CDKs. CDK4 and CDK2 enhance G1-S transition in the cell cycle and for tumorigenesis, indicating that phosphorylation of downstream effector proteins by CDKs is vital for cell proliferation. Previous studies have shown that Cyclin D1-CDK4 and Cyclin ECDK2 are major regulators of G1/S transition, while Cyclin A-CDK2 controls S-phase and Cyclin B1-CDK1

B. Ciz1 Ciz1, a p21(Cip1/Waf1)-interacting zinc finger protein is shown to function as an ER co-regulator and Ciz1 over-expression confers estrogen hypersensitivity and promotes the growth rate, anchorage independency, and tumorigenic properties of breast cancer cells. These effects on cell cycle progression is shown to be ER

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Gene Therapy and Molecular Biology Vol 12, page 397 dependent through upregulation of Cyclin D1 expression (Den et al, 2006). However, a direct role of Ciz1 in DNA replication process in S phase has also been suggested.

Ciz1 co-localizes with PCNA during S phase while depletion of Ciz1 restrains cell proliferation by inhibiting entry to S phase (Coverley et al, 2005).

and septum (Khan et al, 2005). Collectively, these emerging findings suggest that PELP1 plays a key role in relaying mitogenic signals, both in cytoplasm and nucleus and therefore is an attractive therapeutic target. The fact that siRNA mediated knockdown of PELP1 reduces cell proliferation in MCF-7 breast cancer cells strongly suggest that blocking PELP1 functions will undeniably benefit cancer therapeutic regime (Chandrasekharan Nair et al, 2008).

C. CARM1/PRMT4 CARM1 is a methyltransferase that associate with ER coregulators and regulate transcription by histone H3 methylation and is essential for estrogen induced cell cycle progression (Chen et al, 1999). SiRNA mediated depletion of CARM1 in ER positive MCF7 and T47D cells reduced E2 mediated cell cycle progression (Frietze et al, 2008).

Recent evidence also suggest that CARM1 regulate not only E2 mediated E2F expression but also expression of E2F target genes. The recruitment of CARM1 to E2F target genes and associated increase in H3R17 dimethylation during transcriptional activation has been shown to be dependent on another ER coactivator AIB1(Frietze et al, 2008). In a recent study, expression of Cyclin E gene has been shown to correlate with recruitment of CARM1 on its promoter and associated increase in H3-R26 and H3-R17 methylation at its promoter (El et al, 2006). Consistent with the role of CARM1 in regulating cell cycle genes, CARM1 knockout mice show small embryos and perinatal lethality (Yadav et al, 2003).

V. Modulation of cell progression by anti-estrogens

cycle

Estrogens and anti-estrogens both are shown to exert their functions in G1 phase, where they regulate Cyclin D1 and Cyclin E expression and hence modulate the kinase function of CDK4 and CDK2, respectively. Inhibition of CDK kinase function leads to accumulation of hypophosphorylated retinoblastoma and resulting in cell cycle arrest. In short, the consensus is that estrogen accelerates the G1 phase passage while antiestrogens inhibit cell cycle progression by affecting these key cell cycle proteins. On the contrary, a recent transcriptional profiling presented a rather intriguing result regarding functioning of tamoxifen at the molecular level. Tamoxifen and estrogen both positively regulated a large set of cell cycle genes like cmyc, myb, fos, cdc25a, Cyclin E, Cyclin A2, and stk15 while the differential effect was on only few cell cycle genes, most notably on Cyclin D1 (Hodges et al, 2003).

Interestingly, only Tamoxifen but not Roloxifene induced these key cell cycle regulators (Hodges et al, 2003).

Emerging evidence suggest that CDK inhibitors are also regulated by antiestrogens in mediating growth arrest.

Tamoxifen treated breast cancer cell lines show a reduction in Cyclin D, increase p27 and simultaneous increase in Cyclin E-CDK2 bound p27 (Chu et al, 2005).

In the same study, combination treatment of Tamoxifen along with a dual HER1/HER2 inhibitor, lapatinib (GW572016) showed more profound effect on these cell cycle regulators and rapid cell cycle arrest in all the three cell lines tested. Transduction of Tamoxifen treated cells with p-27 peptides (TAT-p27) helped in maintaining quiescence and made the cells resistant to mitogen stimulation (Carroll et al, 2003). These studies evoke the potential of using anti-p27 molecules in future to reverse Tamoxifen resistance. The recent findings that miRNAs also regulate Tamoxifen response in cancer cells is an exciting advance in understanding therapy resistance.

Upregulation of miR-221 and/or miR-222 has been directly shown to promote therapy resistance through downregulation of ER ! (Zhao et al, 2008).

Recent studies also implicated role of p53 in Tamoxifen mediated cell cycle arrest. Ichikawa et al. reported a concomitant increase in p53 expression and p21, a known CDK2 inhibitor in Tamoxifen treated MCF7 in time and dose dependent manner, suggesting possible role of p53 in mediating the G1 arrest caused by Tamoxifen (Ichikawa et al, 2008).

Future studies, however, are required to understand whether antiestrogens affect the expression of Cyclins at transcriptional level or whether unidentified intermediary players govern this pathway in a similar fashion as p53.

D. PELP1/MNAR PELP1 is another ER coregulator that is shown to play a role in E2-mediated G1/S-phase progression (Balasenthil and Vadlamudi, 2003). PELP1 is a pRbinteracting protein and PELP1 deregulation promotes cyclin D1 expression. Breast cancer model cells, which overexpressed PELP1 showed persistent hyperphosphorylation of the pRb protein in an E2 dependent manner accompanied with increase in proliferation rate (Balasenthil and Vadlamudi, 2003).

Recent studies suggested that PELP1 is a phospho-protein and its phosphorylation changes during cell cycle progression. PELP1 interacts with G1/S phase CDKs (both CDK4 and CDK2), and is a novel substrate to both of these enzymes (Chandrasekharan Nair et al, 2008a).

Furthermore, increased PELP1 expression in a mammary gland during pregnancy, when the rate of cell proliferation is high, supports a physiological role for PELP1 in E2mediated cell cycle progression in mammary glands (Vadlamudi et al, 2001). PELP1 is also known to interact with key proteins like Src, PI3K, four and a half LIM only protein2 to mediate E2 dependent non-genomic functions of ER. Mitogenic stimulus promotes PELP1 interaction with growth factor signaling component, epidermal growth factor (EGFR), HER2, STAT3, and hepatocyte growth factor regulated tyrosine kinase substrate (HRS) (Vadlamudi and Kumar, 2007). PELP1 has highest tissue expression in brain, testes, ovary and uterus (Khan et al, 2005; Vadlamudi and Kumar, 2007) and studies from rodent biology suggest that PELP1 is developmentally regulated and expressed at classical steroid target sites in brain like hippocampus, cortex, hypothalamus, amygdale 397

Nair and Vadlamudi: Cell cycle machinery in therapy resistance Identifying key G1-S transition regulatory genes that are relieved of pRb mediated repression due to treatment with antiestrogens will be a priority to unravel more downstream players in antiestrogen mediated cell cycle arrest and such studies will further enhance understanding of antiestrogen resistance.

VI. Cell cycle regulators hormonal therapy resistance

We have summarized below the evidence that showed potential role of the regulators of cell cycle machinery in promoting therapy resistance (Figure 1).

A. Cyclin D1 Cyclin D1 was originally cloned as an oncogene (Motokura et al, 1991) and over-expression of Cyclin D1 has been noted in over 50% of human breast tumors of all histological types (Gillett et al, 1994; Kenny et al, 1999).

There is surmounting evidence to suggest that altered Cyclin D1 expression promotes antiestrogen resistance (Wilcken et al, 1997; Pacilio et al, 1998; Hui et al, 2002).

Cyclin D1 binds ER and increases its transcriptional activity (Neuman et al, 1997). This ability of Cyclin D1 to

and

There has been phenomenal advance in our understanding the role of cell cycle regulators in hormonal therapy resistance. Since tamoxifen mediate the cell cycle arrest by deregulating cell cycle regulators, it is perhaps not surprising that aberrant change in cell cycle machinery often contribute to induction of antiestrogen resistance.

Figure 1. Schematic representation of the current understanding of regulation of hormonal therapy resistance by cell cycle machinery.

Convergence of growth factors and estrogen receptor signaling pathways in therapy resistant cells suggest that deregulation cell cycle regulators are likely to contribute to the development of therapy resistance in breast cancer cells.

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Gene Therapy and Molecular Biology Vol 12, page 399 transactivate ER functions was independent of estrogen stimulation and interestingly, on its CDK4 association as well (Neuman et al, 1997). Over-expression of Cyclin D1 indeed was able to overcome the growth arrest mediated by antiestrogens but Cyclin D1 mutant that is unable to activate CDK4 but having intact ER transactivating potential was not able to promote cell proliferation in the presence of antiestrogens (Bindels et al, 2002). Cyclin D1 is shown to be over-expressed among different Tamoxifen resistant breast cancer cells (Kilker et al, 2004) and Cyclin D1 specific siRNAs restored the sensitivity of these cells to Tamoxifen suggesting therapies targeting Cyclin D1 may have therapeutic effect in hormonal therapy resistant cells (Kilker and Planas-Silva, 2006).

Furthermore, an alternative splice variant of Cyclin D1 named Cyclin D1b is reported to be over expressed in a variety of breast cancers (Betticher et al, 1995; Hosokawa et al, 1997; Wang et al, 2008) and appears to function as a nuclear oncogene (Lu et al, 2003). Cyclin D1b is also known to associate with CDK4 with a weaker kinase activity and over-expression of this alternative transcript Cyclin D1b is shown to overcome the antiestrogen mediated cell cycle arrest (Wang et al, 2008).

Unlike Cyclin D1, this effect was independent of ER transactivation as Cyclin D1b lacks nuclear receptor interaction LXXLL motif but retains binding site for CDK4 (Wang et al, 2008).

In addition to activating CDK4, Cyclin D1 is also shown to promote hormonal therapy resistance through other pathways (Ishii et al, 2008). Cyclin D1 is known to mediate STAT3 repression but cells treated with Tamoxifen can potentially reverse this STAT3 repression by the redistribution of Cyclin D1 from STAT3 to ERcomplex. This was confirmed by in vivo nude mice assays, where it was shown that growth of Cyclin D1â&#x20AC;&#x201C; overexpressing tumors was stimulated by Tamoxifen treatment with concurrent elevation and activation of STAT3 (Ishii et al, 2008). PI3K/AKT or MAPK/ERK1 signaling is also reported to contribute to Cyclin D1 expression and promote to therapy resistance to Tamoxifen underscoring the importance of cross talk between various mitogenic pathways with cell cycle machinery in ultimately achieving antiestrogen resistance (Kilker et al, 2004).

Cyclin D1 negative tumor patients show better relapse free survival upon Tamoxifen-based therapy while Cyclin D1 expression correlated well with poor outcome upon antiestrogen treatment (Rudas et al, 2008). Clinical study with randomized post-menopausal breast cancer patients also show that Cyclin D1 over-expression correlates with poor outcome with Tamoxifen treatment (Stendahl et al, 2004). Similar results were obtained with premenopausal breast cancer patients with Cyclin D1 gene amplification (Jirstrom et al, 2005). Collectively these emerging finding suggest importance of Cyclin D1 as a useful predictive marker in the selection of Tamoxifenbased therapy regime.

Tamoxifen and this effect in part was attributed to the aberrant activation of E2F-Rb pathway (Dhillon and Mudryj, 2002). Subsequent studies showed that Cyclin E level showed good correlation with poor relapse-freesurvival in patients treated with antiestrogens (Span et al, 2003). Interestingly, Cyclin E was not observed to be good prognostic marker for breast cancer as a whole, however, Cyclin E is a good predictor of antiestrogen resistance (Span et al, 2003; Desmedt et al, 2006). Another important feature of Cyclin E is its tumor specific proteolytic cleavage, yielding low molecular weight (LMW) forms of Cyclin E (Porter et al, 2001). Recent reports suggest that these LMW Cyclin E, lacking varying amount of amino terminal region of whole length Cyclin E, plays a vital role in promoting hormone therapy resistance (Akli et al, 2004). The LMW forms of Cyclin E could complex with CDK2 and accounts for increased CDK2 activity as compared to full length Cyclin E (Akli et al, 2004). LMWCyclin E overexpressing MCF-7 cells showed greater resistance toward ICI- 182,780 mediated growth arrest as compared to full length Cyclin E and this resistance was attributed to decreased inhibitory effects of p21 and p27 on these LMW-Cyclin E forms (Akli et al, 2004).

C. Cyclin A Emerging evidences suggest that Cyclin A also play important role in hormone therapy resistance. Detection of Cyclin A over expression by immuno-histochemical methods correlated well with early breast cancer relapse and can be considered a good marker of Tamoxifen resistance (Michalides et al, 2002). Cyclin A is also known to associate with CDK2 and phosphorylates ER and thereby increase its transactivation potential (Trowbridge et al, 1997). Cyclin A/CDK2 complex phosphorylates Ser104 and Ser-106 located in the AF-1 domain of ER and increase its transcriptional activity (Rogatsky et al, 1999).

The ER transactivation through CDK2-Cyclin A phosphorylation is evident in presence and the absence of estrogen stimulation and also with Tamoxifen treatment (Rogatsky et al, 1999). Large scale randomized trials are however required to understand the potential of CDK2Cyclin A mediated phosphorylation of ER as a prognostic marker for assessing the efficacy of antiestrogen therapy regime.

D. Cyclin dependent kinases Most downstream events in antiestrogen resistance signaling pathways, like upregulation of various Cyclins ultimately converge upon modulation of Cyclin Dependent Kinases; the most conspicuous of which is the activation of Cyclin Dependent Kinase 2 (CDK2) (Dhillon and Mudryj, 2002; Akli et al, 2004). Apart from CDK2, CDK10 has been recently implicated in hormone resistance. CDK10 is a newly reported player in mediating antiestrogen therapy resistance, identified by functional genomics approach (siRNA screen) (Iorns et al, 2008; Swanton and Downward, 2008). An unbiased loss of function SiRNA screen performed by Iorns et al, identified modulators of Tamoxifen sensitivity and found that RNAi mediated downregulation of CDK10 increases ETS2driven transcription of c-RAF, resulting in MAPK

B. Cyclin E Deregulation of Cyclin E in breast cancer model cells has been shown to resist cell cycle arrest mediated by 399

Nair and Vadlamudi: Cell cycle machinery in therapy resistance pathway activation and independence from ER pathway.

Loss of CDK10 in ER positive breast cancer was shown to be associated with relapse of cancer after anti-hormone therapy. CDK10 is cdc2 related kinase found to play important role in G2-M progression. While no Cyclins have been identified to associate with CDK10, it is known that ETS2 is interacting partner of CDK10 (Kasten and Giordano, 2001). This low amount of CDK10 in antiestrogen resistant cells were attributed to the methylation of CDK10 promoter in vivo, underscoring the importance of epigenetic changes accompanying the hormone resistance phenotype (Iorns et al, 2008).

F. Retinoblastoma and E2Fs Rb-E2F pathway plays a fundamental role in cell proliferation and deregulation is frequently observed in breast cancer. siRNA mediated Rb ablation is able to overcome the growth arrest by antiestrogen treatment and using in vivo xenograft model, Rb deficient tumors were shown to retain the ability to grow in spite of Tamoxifen treatment (Bosco et al, 2007). Furthermore, the same study included analysis of 60 human breast cancer patients treated with Tamoxifen to generate a Rb gene expression signature (Bosco et al, 2007). Another study found that expression of viral T-antigens in breast cancer cells (MCF7) that promote inactivation of endogenous Rb, elicited antiestrogen resistance (Varma and Conrad, 2000).

P53 binding ability of T-antigen was however shown not required for this phenotype. In continuation of this work, Conrad and colleagues elucidate the molecular mechanism behind Rbâ&#x20AC;&#x2122;s role in promoting antiestrogen resistance (Varma et al, 2007). Inducible pyLT cell lines were utilized to demonstrate that functional inactivation of pRb can lead to CDK2/Cyclin A activation and reversal of antiestrogen mediated cell cycle arrest. The new hypothesis put forward was that ER+ Rb- tumors showing increased CDK2 activity and resulting hormone therapy resistance can be targeted by agents blocking CDK2.

Currently many such CDK2 targeting drugs (although not very specific ones) are available in clinical trials and need to be evaluated in the context.

E. CDK inhibitors Down regulation of p21 has been implicated with Tamoxifen resistant phenotype. Somatic deletion of p21 gene in human breast cancer cells demonstrated that these cells were resistant to Tamoxifen mediated growth arrest (Abukhdeir et al, 2008). The mechanism behind this effect was attributed to increased ER phosphorylation at serine 118 by CDK complex upon p21 decrease. Role of ER phosphorylation as an effector of Tamoxifen resistance was elucidated by transfecting p21 null-MCF10A cells with ER cDNA constructs with Serine118 mutated to alanine. These transfected cells became responsive to Tamoxifen, proving that ER activation is the downstream element in p21 mediated Tamoxifen growth resistant phenotype (Abukhdeir et al, 2008). Antiestrogen resistance could be abolished by treating cells with antisense p21 or p27 oligonucleotides, leading to activation of Cyclin Dependent Kinase 2 (Cariou et al, 2000).

Among various molecular pathways implicated in down regulating CDK inhibitors, MAPK/MEK activation is notable (Donovan et al, 2001). MEK inhibitor, U0126 was used to inhibit MEK pathway and re-sensitized to growth arrest by antiestrogen in LY-2 model cells of antiestrogen resistance. Different phospho-isoforms of p27 were detected in these antiestrogen resistant model cells that may contribute toward generating resistance phenotype (Donovan et al, 2001). Detailed studies are however warranted to delineate and correlate specific sites of phosphorylation on p27 with clinical outcome with antiestrogen therapy.

Localization of CDK inhibitors has also been implicated in the development of antiestrogen resistance.

Studies have shown that heregulin "1 over-expression that activates PI3K and MAPK pathway, also promotes p21 localization into cytoplasm (Perez-Tenorio et al, 2006).

Tumors with increased cytoplasmic localization of p21 respond poorly with Tamoxifen treatment (Perez-Tenorio et al, 2006). In premenopausal women with early breast cancer, an increase in p27/KIP1 expression was able to predict better relapse free survival upon Tamoxifen combination treatment (Pohl et al, 2003). This trial included 512 randomized patients wherein multivariate analysis revealed decreased p27 expression to be correlated with poor outcome upon combination endocrine therapy. A recent study indicated that p27kip1 is another important target of miR-221 that promotes mediate resistance to hormonal therapy (Miller et al, 2008).

G. c-Myc c-Myc is a well known cell cycle regulator and oncogene frequently up regulated in breast cancer. It is also one of the earliest estrogen responsive gene, showing a noticeable increase in protein level within 15 min of estrogen treatment (Dubik et al, 1987). C-myc expression when induced in MCF-7 using Tet-on expression system could potentially abrogate antiestrogen mediated growth arrest (Venditti et al, 2002). Similar results were obtained in a different study, wherein over expression of c-myc down regulated p21 expression and mediated antiestrogen resistance(Mukherjee and Conrad, 2005). C-myc expression can rescue the G1 arrest mediated by Tamoxifen by activating CDK2/Cyclin E complex and further phosphorylation of p130 (Prall et al, 1998a).

Involvement of c-myc in regulating p21 expression levels and contributing to emergence of antiestrogen resistance is also reported (Mukherjee and Conrad, 2005). p21 levels in antiestrogen resistant cells increased when treated with cmyc siRNAs, suggesting important role of c-myc in downregulating p21 levels and promoting hormonal therapy resistance (Mukherjee and Conrad, 2005).

From the above mentioned studies, we present an interesting case that cell cycle regulators play a vital role in the emergence of hormone therapy resistance. However, the studies performed so far do not provide clear distinction of using cell cycle regulators as prognostic markers of therapy resistance or therapeutic targets against resistant cells. The key challenge in this area is to unequivocally show that targeting cell cycle regulators can potentially reverse the hormone therapy resistance but the side effects may limit their use as evidenced by recent 400

Gene Therapy and Molecular Biology Vol 12, page 401 studies. Targeting kinase functions of CDK2 is a feasible option and currently there are some ongoing clinical studies employing pan CDK inhibitors against non-small cell lung cancer like r-roscovitine (Seliciclib or CYC202).

Our lab has recently tested the efficacy of combinatorial usage of r-roscovitine with Tamoxifen against various hormone resistant cell lines like MCF-tam (resistant to Tamoxifen), MCF-7-Her2 (overexpressing Her2), and MCF7-PELP1 (overexpressing PELP1) and found encouraging results in sensitizing these cells to Tamoxifen treatment (Chandrasekharan Nair et al, 2008b). Another possibility to overcome toxic side effects would be to explore nanotechnology methods that allow cancer cell specific delivery of the cell cycle inhibitors reducing toxic side effects. Such combinatorial use of cell cycle inhibitors along with classical hormone therapy represents a novel therapeutic modality to circumvent the problem of toxicity and to enhance therapeutic success.

Acknowledgements Work in the authorâ&#x20AC;&#x2122;s laboratories is supported by NIH grant CA095681 (RKV) and DOD grant W81XWH08-1-0604 (RKV) and DOD Pre-doctoral Fellowship W81XWH-09-1-0010 (CBN).

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VII. Conclusions and Future Direction The estrogen receptor (ER) plays a central role in the progression of breast cancer and endocrine therapy is widely used to target ER+ve breast cancer. Despite the positive effects, de novo and/or acquired resistance to endocrine therapies frequently occur. Most downstream events in the resistance signaling pathways appear to converge upon modulation of cell cycle regulatory proteins. Evolving evidence suggests that cell cycle machinery cross talk with estrogen receptors, ERcoregulators and growth factor receptors and such interaction play a role in the development of therapy resistance. It is therefore of great interest to understand how cell cycle machinery promotes therapy resistance.

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Gene Therapy and Molecular Biology Vol 12, page 405 Gene Ther Mol Biol Vol 12, 405-414, 2008

Reversal of MDR1/P-glycoprotein associated drug resistance in human Hepatoblastoma Research Article

Steven W. Warmann*, Joerg Fuchs Department of Pediatric Surgery, University Childrenâ&#x20AC;&#x2122;s Hospital, Hoppe-Seyler-Str.3, 72076 Tuebingen, Germany

__________________________________________________________________________________ *Correspondence: Steven W. Warmann, MD, Department of Pediatric Surgery, University Childrenâ&#x20AC;&#x2122;s Hospital, Hoppe-Seyler-Str. 3, 72076 Tuebingen, Germany; Tel: + 49 7071 29 86621; Fax. + 49 7071 29 4046; e-mail: Steven.Warmann@med.uni-tuebingen.de Key words: MDR1/P-glycoprotein, Hepatoblastoma, Standard Therapy (IPA), CARBO/VP-16, High dose CARBO/VP-16 Abbreviations: !-fetoprotein (AFP); ATP-binding cassette (ABC); breast cancer resistance protein (BCRP)Cisplatin (CDDP); hepatoblastoma (HB); multi drug resistance (MDR); Multidrug Resistance Gene 1 (MDR1); P-glycoprotein (P-gp); RNA interference technology (RNAi) Received: 5 February 2007; Accepted: 16 March 2007; electronically published: January 2009

Summary Despite impressive improvements of treatment results in children suffering from hepatoblastoma (HB), advanced tumor stages still provide unsolved problems for treating physicians. A major factor for this phenomenon is the phenotype of drug resistance. The mechanism related to the Multidrug Resistance Gene 1 (MDR1) and its product P-glycoprotein (P-gp) has been identified in experimental studies as major factor contributing to drug resistance in HB. P-gp is an ATP dependant membrane channel, which pumps cytotoxic agents out of the tumor cells.

Modulation of P-gp using atoxic chemosensitizers improved treatment results in several tumor types. There is a correlation between MDR1 gene expression levels and the amount of applied chemotherapy courses in resected HB. Relapses and metastases show the highest expression followed by primary tumors after neoadjuvant chemotherapy.

Lowest expression levels are found in tumors that were not pre-treated before surgery. We also observed significant treatment improvements of chemosensitizers compared to respective mono-therapies both, in cell lines and in xenotransplanted HB. In cell cultures, cell viabilities decreased significantly without an increase of MDR1 gene expression levels. In xenotransplanted HB, tumor growth and serum alpha-fetoprotein levels were decreased significantly. Again, there were no effects of chemosensitizers on MDR1/P-gp expression levels. Our data underline the hypothesis that chemosensitizers may represent a promising tool for the treatment of advanced types of HB.

resistant after a certain number of chemotherapy courses (Lockwood et al, 1993; von Schweinitz et al, 1995, 1997).

P-glycoprotein, the product of the human MDR1 gene, belongs to the ATP-binding cassette (ABC) family of proteins and is physiologically localized in epithelial cells of the gastrointestinal tract, liver, kidney, and capillaries of the brain, testes, and ovaries. P-gp acts as a barrier to the uptake of xenobiotics, and promotes their excretion in the bile and urine. Some tumor cells show enhanced MDR1/P-gp expression after chemotherapy. Pgp actively pumps cytotoxic agents out of tumor cells thus increasing their resistance against cytotoxic agents. P-gp has been proposed as a major factor for the development of drug resistance in experimental models of HB (Bader et al, 1998; Minemura et al, 1999).

The P-gp related resistance has been antagonized using chemosensitizers in various malignancies under experimental and clinical conditions (Mistry et al, 2001;

I. Introduction Hepatoblastoma (HB) is the most common primary malignant pediatric liver tumor in children of the western hemisphere (Ishak and Glunz, 1967; Ishak, 1976; Ross and Gurney, 1998). Treatment results of children with HB have been improved remarkably during the last twenty years through treatment strategies developed by several national and international trials in which surgery is combined with perioperative chemotherapy (Ortega et al, 2000; Fuchs et al, 2002; Haberle et al, 2003; Perilongo et al, 2004). Complete surgical resection of the tumors is the main goal of the treatment and is essential for survival of the patients. It also represents a major prognostic factor.

Most HB show a good response to chemotherapy.

Nevertheless, chemotherapy alone can not eradicate primary tumors (Fuchs et al, 2002; Perilongo et al, 2004).

Some tumors remain unresectable after chemotherapy.

Also, advanced and metastasized HB may become drug

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Warmann and Fuchs: Reversal of MDR1/P-glycoprotein associated drug resistance in human Hepatoblastoma For gene expression analyses we used 12 well plates with 300.000 cells per well. All used cells were Mycoplasma negative.

Cell viabilities were assessed using the MTT (3-(4,5dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromid) -assay (Mosmann, 1983). The IC50 of Cisplatin (CDDP) or Doxorubicin (DOXO) was used for chemotherapy. As chemosensitizers we used ascending concentrations (Table 1) of verapamil, PSC 833, a non immunosupressine derivate of cyclosporin, and GG 918, an acridine-carboxamide (Tai, 2000; Thomas and Coley, 2003; Ward and Azzarano, 2004). Incubation with the different agents was carried out for 72 hours.

Lee et al, 2003; Limtrakul et al, 2005; Kankesan et al, 2006). We present the analyses of MDR1/P-gp expression in resected HB specimen in order to reveal a correlation between chemotherapy administration and MDR1/P-gp related drug resistance. Also we investigated the effects of P-gp modulation on the treatment of HB in vitro and in vivo.

II. Patients and Methods A. Patients Clinical data were registered according to the questionnaires of the prospective multi center trials HB 89 and HB 94 of the German Society for Pediatric Oncology and Hematology (Fuchs et al, 2002a,b). In this study cytotoxic agents were administered following the listed schemes:

C. Animal studies For in vivo analyses we used a cell line which was established by our group (nude mouse hepatoblastoma No. 1, NMHB#1) (Warmann et al, 2002) as well as the HepT1 cell line (NMHB#2). Nude mice NMRI (nu/nu) were xenotransplanted according to the model of Fuchs and colleagues, 1996. Animals bearing subcutaneous HB xenografts were treated with CDDP or DOXO +/- verapamil or PSC 833. All agents were administered intraperitoneally. CDDP (9mg/m! days 1-3 and 15-17) and DOXO (15mg/m! days 1-4 and 15-18) were given in cumulative doses equitoxic to the regimens in the HB99 Study. The concentrations for verapamil (5mg/kg) and PSC 833 (5mg/kg) were taken from previously described studies (Todd and Abernethy, 1987; Colombo et al, 1996; Fuchs et al, 1998). The chemosensitizers were administered 10 minutes before the cytotoxic agents.

Tumors were measured every five days (length (a), height (b) and width (c)) and tumor volumes were calculated according to the formula: a b c 4 VTumor = " " " 2 2 2 3#

i. Standard Therapy (IPA) 1. Ifosfamid: 1g/m!/24h for 96h (total dose 3g/m!) together with Uromitexan in equal dosage (day 1-3).

2. Cisplatin: 1x/d 20mg/m! over 1 hour (total dose 100mg/m!, day 4-8).

3. Doxorubicin: 60mg/m! over 48h (day 9 and 10). ii. CARBO/VP-16 1. Carboplatin: 800 mg/m! as continuous infusion (day 1-4) 2. Etoposid: 400mg/m! as continuous infusion (day 1-4) iii. High dose CARBO/VP-16 1. Carboplatin: 500mg/m!/day over 96h 2. Etoposid: 500mg/m!/day over 96h Histological analyses were performed by the local pathologist as well as by the Study reference pathology (Prof.

Harms, PD Dr. med. Leuschner, Kiel, Germany). Additionally, all tumor specimens were processed and analysed for expression of P-gp against negative controls using antibodies C219 and MM 4.17. A qualitative evaluation was performed using light microscopy. P-gp expression on representative sections was considered negative (no positive signal), low (<10% positive), moderate (10-25% positive), strong (25-50% positive), or very ! strong (>50% positive).

All tumor specimens were also assessed for MDR1 gene expression using rt-PCR as described earlier (Mosmann, 1983; Warmann et al, 2003). GAPDH served as internal standard, and samples from regular liver tissue was analysed simultaneously to determine relative gene expression levels. The relative expression levels of the MDR1 gene were calculated according to the formula:

For statistical analysis we used relative volumes:

!V Vrelativ = dx V , where Vdx: volume on day x; V d0: initial d0 volume Before and after treatment we determined serum !fetoprotein (AFP) levels in the mice using a radioimmunoassay (CIS biointernational, Behring Institute, Germany). Samples from xenografts after treatment were assessed for MDR1 gene expression using rT-PCR. All animal studies were approved by the Regional Government’s Ethic Committees for animal studies in Hannover and Tuebingen, Germany.

III. Results

("MDRT-" MDRL) / " MDRT

A. Patients

with "MDR T representing the MDR1 gene expression of the tumors against GAPDH and MDRL representing the MDR1 gene expression of the liver against GAPDH. All studies were approved by the Regional Government’s Ethical Committtee in Hannover, Germany.

i. Patients’ data From the studies HB 89, HB 94, and HB 99 we analysed 28 resected tumor specimens. However, only 13 of them were of sufficient quality to be used for immunohistochemistry and PCR against P-gp/MDR1. One

B. Cell lines

Table 1. Chemosensitizer concentrations.

For invitro analyses we used the cell lines HepT1, HUH6, and HepT3 which have been described previously (Doi, 1976; Pietsch et al, 1996; Warmann et al, 2003). HepT1 was derived from a HB of embryonal subtype, HUH6 originated from a mixed HB, and HepT3 from an embryonal/fetal HB. The cell lines were cultured in DMEM + 10%FCS at 37°C in a humidified atmosphere containing 5% CO2. Viability analyses were performed using 96 well plates with 20.000 cells per well.

GG 918 Verapamil PSC 833

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1 0.01µM 1µM 0.1µM

2 0.05µM 3µM 0.3µM

4 0.5µM 30µM 3µM

3 0,1µM 10µM 1µM

Gene Therapy and Molecular Biology Vol 12, page 407 child had a relapse and one had metastases. Therefore, 15 tumor specimens were evaluated. The mean age at operation was 39.2 months (1.5-144). Patients’ specific data are shown in Table 2.

the internal control) and the amount of administered chemotherapy (Figure 1). Lowest levels were seen in tumor specimens without chemotherapy. Higher levels were found in resected tumors after neoadjuvant chemotherapy and highest levels were present in tumor relapses and metastases (Figure 1).

ii. Histology and clinical course 14/15 Tumor specimen were of epithelial origin (2 embryonal, 4 fetal and 8 embryonal/fetal HB). One was a teratoid HB. From the 4 patients who died, 2 had an embryonal tumor, one a teratoid and one an embryonal/fetal. Three of these 4 children had a stage IV tumor and one a stage II tumor. Data of histological analyses after chemotherapy and immunohistochemistry are shown in Table 3.

B. Cell lines i. Chemosensitizer effects on DOXO treated cells.

Addition of chemosensitizers lead to a relevant growth reduction in all cell lines compared to the respective monotherapy. When added to DOXO in the highest concentration (Figure 2), strongest effects were seen for PSC 833 (growth reduction 66.3-75.7%) followed by verapamil (53.2-66%) and GG 918 (10.2-41.3%).

iii. MDR1 gene expression In operated patients we found a close correlation between MDR1 gene expression levels (as compared to

Table 2: Patient specific data; (x) †=died after (x) months. Two patients had relapses/metastases Pat.-No. 1 2 3 4 5 6 7 8 9 10 11 12a 12b 13a 13b

Age at surgery (months) 20,5 12 20 30,5 17 35 49 16,5 98,5 1,5 32 33 144

Tumor-Stage I IV I I I IV IV IV I I IV II IV I I

Preoperative Chemotherapy 2 x IPA 5 x IPA,3 x Carbo/VP 16 3 x IPA 2x IPA 3xIPA 3x IPA 3 x IPA, 2 x Carbo/VP 16 3 x IPA 2 x IPA none 4 x IPA, 3 x Carbo/VP 16 3 x IPA 3x Carbo/VP 16-HD 2 x IPA 2-VP 16/Carbo

Follow up (months) 87 127 43 42,5 32 28 (36) † (5) † 32 22 (98) † (36) † 53

Table 3. Clinical data of outcomes, tumor staging, histology, and P-gp expression levels. Antibody MM 4.17 was used for P-gp detection in immunohistochemistry.

Pat.-No. 1 2 3 4 5 6 7 8 9 10 11 12a 12b 13a 13b

Tumor Staging I IV I I I IV IV IV I I IV II IV I I

Histology e/f, vital e/f, vital e/f, regressive e/f f, necrotic e/f, necrotic teratoid, vital e/f, necrotic e/f, regressive f e, vital e, vital e/f, vital f f

Outcome alive alive alive alive alive alive died died alive alive died died alive

P-gp-Expression (MM4.17) strong very strong strong strong strong negative strong strong moderate moderate strong strong very strong strong strong

Preop Chemotherapy 2 x IPA 5 x IPA,3 x Carbo/VP 16 3 x IPA 2 x IPA 3 x IPA 3 x IPA 3x IPA, 2 x Carbo/VP 16 3 x IPA 2 x IPA none 4x IPA, 3 x Carbo/VP 16 3 x IPA 3 x Carbo/VP 16-HD 2 x IPA 2 x VP 16/Carbo

Histology: e = embryonal, f = fetal, n.m. = not measurable. For explanation of chemotherapy regimens see text.

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There were no differences between untreated control cells and cells incubated with chemosensitizers only (p 0.076-0.38). Mono therapy with DOXO resulted in enhanced MDR1 gene expression against control (p=0.018). Addition of chemosensitisers did not further increase gene expression compared to cells after mono therapy (p 0.07-0.29). In all other cells and treatment regimens there were no differences regarding the MDR1 gene expression (all p>0.05).

ii. Chemosensitizer effects on CDDP treated cells.

When added to CDDP in the highest concentration (Figure 3), strongest effects were seen for PSC 833 (growth reduction 14.367.5%) followed by GG 918 (31.3-43.8%) and verapamil (8.241.5%).

iii. MDR1 gene expression Enhanced MDR1 gene expression levels were only detected in HepT1 cells after treatment with DOXO.

Figure 1. MDR1 Expression levels in tumor specimen after resection [%].Circle: tumors without preoperative chemotherapy; square: primary tumors after standard chemotherapy (IPA); triangle: Relapses and metastases (mean, sd).

Figure 2. Additional effects of chemosensitisers on tumor cells treated with DOXO. The related DOXO mono therapy was set as 0%.

Triangles: HepT3; squares: HUH6; circles: HepT1.

Figure 3. Additional effects of chemosensitisers on tumor cells treated with CDDP. The related CDDP mono therapy was set as 0%.

Triangles: HepT3; squares: HUH6, circles: HepT1.

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Gene Therapy and Molecular Biology Vol 12, page 409 Chemosensitizers alone had no influence on the tumor vitality (Figure 6).

In NMHB#2 serum AFP was significantly decreased after treatment with CDDP (p=0.013) and DOXO (p=0.011). Addition of chemosensitizers further decreased AFP levels in the animalsâ&#x20AC;&#x2122; sera, however, differences were not significant (p 0.1-0.31). Chemosensitizers alone had no influence on the tumor vitality (Figure 7).

C. Animal studies i. Tumor volumes In NMHB#1 there were no differences between tumor volumes in control animals and animals that received chemosensitizers only. Treatment with DOXO and CDDP led to significantly decreased tumor volumes (p<0.001 for both). Addition of chemosensitizers further improved treatment results; PSC 833 was more effective than verapamil (p 0.0004-0.011, Figure 4).

In NMHB#2 results were comparable; however, chemosensitizers were less effective than in NMHB#1.

Improvements were observed in all regimens but reached significance only in one case (DOXO+PSC 833, p=0.007, Figure 5).

iii. MDR1 gene expression MDR1 gene expression levels in untreated NMHB#1 was 22.8 (+/- 8.6). Gene expression was enhanced after treatment with DOXO (38.4 +/- 10.3, p=0.01) and CDDP (47.9 +/- 11.3, p=0.003). Chemosensitizers had no influence on the MDR1 gene expression in control cells as well as in combination with cytotoxic agents (all p>0.05).

In NMHB#2 results were identical: untreated tumors: 36.6 +/- 12.5, increased expression levels after chemotherapy with DOXO (47.9 +/- 11.3, p=0.024) and CDDP (52.1 +/14.4, p=0.0013), and no significant differences through addition of chemosensitizers (all p>0.05).

ii. Serum AFP levels In NMHB#1 serum AFP was significantly decreased after treatment with CDDP (p=0.002) and DOXO (p=0.01). Addition of chemosensitizers further decreased AFP levels in the animalsâ&#x20AC;&#x2122; sera (p 0.0001-0.0023).

Figure 4. Relative tumor volumes NMHB#1 after treatment (log, n=10, expected and observed).

Figure 5. Relative tumor volumes NMHB#2 after treatment (log, n=10, expected and observed).

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Warmann and Fuchs: Reversal of MDR1/P-glycoprotein associated drug resistance in human Hepatoblastoma

Figure 6. Serum AFP levels NMHB#1 after treatment (log, n=10, expected and observed).

Figure 7. Serum AFP levels NMHB#2 after treatment (log, n=10, expected and observed).

al, 1988; Cordon Cardo et al, 1989; Sasongko et al, 2005).

Relating observations could be verified using nock-out models (Schinkel et al, 1994; Van Asperen et al, 1996). Pgp shows enhanced expression levels in cell line presenting the MDR phenotype. The P-gp concentration hereby correlates with the grade of MDR. This predominantly affects anthracyclines, epipodophyllotoxines, vinca-alcaloids and taxanes (Juliano and Ling, 1976; Kartner et al, 1983, 1985; Ueda et al, 1986; Di Nicolantonio et al, 2005). The relevance of MDR1/P-gp as major factor for MDR has also been demonstrated for HB (Bader et al, 1998; Minemura et al, 1999).

IV. Discussion P-gp is a membrane-bound glycoprotein (170 kDA, 1280 amino acids), which transports substances out of cells in an active process. It belongs to a number of proteins that are encoded by the MDR-gene family. In humans there exist two genes (MDR1 and MDR 2/3), however, only the MDR1 gene contributes to the phenotype of multi drug resistance (MDR) (Gros et al, 1986; Ueda et al, 1987; Devault and Gros, 1990). P-gp is physiologically localized in excretory tissues such as the liver and kidneys. Itâ&#x20AC;&#x2122;s existence in capillaries of the CNS, testicles and placenta indicates the relevance of P-gp in the functioning of the blood-brain barrier, the conservation of the germline and of the intrauterine embryo (Sugawara et 410

Gene Therapy and Molecular Biology Vol 12, page 411 Analysing the the resected tumor specimen, we found a correlation between MDR1 gene expression levels and the amount of administered chemotherapy: Highest levels were found in tumor relapses and metastases compared to tumors after neoadjuvant standard treatment. Lowest levels were found in tumors that were not treated before operation. This observation is in concordance with clinical findings, where most tumors develop multi drug resistance after a certain number of chemotherapy courses (von Schweinitz et al, 1997). It also affirms the experimental data and emphasizes the transfer to the clinical conditions.

In HB cell lines we observed significant improvements of chemotherapy through MDR1 modulation. PSC 833 proved to be the strongest in vitro Pgp inhibitor. Highest effects were observed in combination with DOXO. This fact underlines the observation that DOXO acts as substrate of P-gp. However, we also observed positive effects of chemosensitizers in combination with CDDP. In other studies the same observation has been made (Baekelandt et al, 2001). Since CDDP is not considered to belong to the P-gp substrates, the exact mechanisms of this interaction remain unclear.

Nevertheless, we found significant evidence for a positive effect both, in vitro and in vivo. Expression levels of the MDR1 gene were not altered in vitro with one exception.

But in this case also, there were no effects of chemosensitizers on the MDR1 gene expression. For a more reliable conclusion, we would, however, prefer the data drawn from patients’ or in vivo studies.

In xenotransplanted HB there were significant improvements of chemotherapy through combination with chemosensitizers. According to the in vitro findings, the treatment with CDDP could be improved in vivo also. The histologically more favorable HB cell line responded better to the P-gp directed approach. There was a significant increase of MDR1 gene expression levels after chemotherapy in all xenotransplants. These findings were discordant to the in vitro studies but seem in our view more appropriate because of the solid formation of the tumors. Also the higher amount of RNA for assessment studies seems to play a role here. Finally, these results resemble the clinical observations as described above. In every case, P-gp inhibitors did not further enhance MDR1 gene expression, which seems to indicate that there is no increased drug resistance through co-administration of chemosensitizers. The importance of the described observations makes MDR1/P-gp a promising target for the future treatment of HB (Schnater et al, 2003).

The development of P-gp inhibitors underwent several Steps in recent years. First generation chemosensitizers were not specifically developed to inhibit MDR. They had low affinities to MDR transporters (Perez-Tomas, 2006). Second generation agents, to which PSC 833 belongs, were more promising in preclinical studies and have been investigated in clinical studies already. Unfortunately, most of them did not display promising results (Nobili et al, 2006; Perez-Tomas, 2006).

Third generation inhibitors were developed to specifically block efflux capacities of ABC transporters. Clinical studies analysing the potential of these agents (e.g. VX 710, LY 35979, XR 9576) are ongoing and some of them

seem more favourable than the preceding substances.

Besides the specifity one major reason for their superiority seems to be caused by simultaneous effects against several transporters such as P-gp, the breast cancer resistance protein (BCRP), and the multi drug resistance protein (MRP-1) (Minderman et al, 2004; Mahadevan and Shirahatti, 2005; Jekerle et al, 2006; Nobili et al, 2006).

Another important observation has been recently reported in which P-gp enhances TRAIL-triggered apoptosis in MDR cancer cells via the death receptor DR5 (Park et al, 2006).

Lately, the RNA interference technology (RNAi) has been introduced as experimental strategy to reverse MDR. RNAi is a physiological double stranded RNA-triggered mechanism resulting in gene-silencing in a sequencespecific manner. Different RNAi strategies have been successfully applied to silence the MDR1 gene in vitro and in vivo (Stege et al, 2004; Chen et al, 2006; Lage, 2006; Shi et al, 2006). We could recently demonstrate that the technique of RNAi can be successfully applied to HB in vitro (Warmann et al, 2006).

Due to it’s important value, MDR1/P-gp remains an important and promising target for the improvement of chemotherapy results in HB. Our data demonstrate that overcoming P-gp related MDR might improve treatment results, especially in advanced tumors. Last generation chemosensitizers as well as the RNAi technique seem to be the most promising developments in this regard.

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GENE THERAPY & MOLECULAR BIOLOGY

Volume 12 Number 2 December 2008 Published by Gene Therapy Press

!

GENE THERAPY & MOLECULAR BIOLOGY Addresses of Members of the Editorial Board OPEN ACCESS www.gtmb.org Editor

Editor Assistants Boulikas, Teni, Ph.D. Chairman of the Board, Regulon, Inc. Mt View CA 94043 and Regulon AE, Athens, Greece

Koutoudi, Maria M.A. Vougiouka, Maria, B.Sc. Kruit, Adrian, Ph.D. Bellimezi, M., Ph.D Katsoupi J, Mph, Tsogas I., Ph.D, Magkos, A., Ph.D, Christofis Petros., Ph.D, Leto Tziveleka., Ph.D

Associate Editors Missailidis, Sotiris, DPhil (York) Lecturer in Chemistry and Analytical Sciences, The Open University, UK

Roberts, Michael, Ph.D., Regulon A.E., Athens Greece

Berezney, Ronald, Ph.D., State University of New York at Buffalo, USA

Rossi, John, Ph.D., Beckman Research Institute of the City of Hope, USA

Crooke, Stanley, M.D., Ph.D., ISIS Pharmaceuticals, Inc, USA

Shen, James, Ph.D., Institute of Molecular Biology, Academia Sinica, Taipei, Taiwan, Republic of China & University of California at Davis, USA.

Gronemeyer, Hinrich, Ph.D. I.N.S.E.R.M., IGBMC, France

Webb, David, Ph.D., Celgene Corporation, USA

Aguilar-Cordova, Estuardo, Ph.D., AdvantaGene, Inc., USA

Editorial Board Members Akporiaye, Emmanuel, Ph.D., Arizona Cancer Center, USA

Baldwin, H. Scott, M.D Vanderbilt University Medical Center, USA

Anson, Donald S., Ph.D., Women's and Children's Hospital, Australia

Barranger, John, MD, Ph.D., University of Pittsburgh, USA

Ariga, Hiroyoshi, Ph.D., Hokkaido University, Japan

Black, Keith L. M.D., Maxine Dunitz Neurosurgical Institute, Cedars-Sinai Medical Center, USA

Blum, Kenneth, Ph.D., Wake Forest University School of Medicine, USA

Eckstein, Jens W., Ph.D., Akikoa Pharmaceuticals Inc, USA

Bode, Jürgen, Gesellschaft für Biotechnologische Forschung m.b.H., Germany

Fisher, Paul A. Ph.D., State University of New York, USA

Bohn, Martha C., Ph.D., The Feinberg School of Medicine, Northwestern University, USA

Georgiev, Georgii, Ph.D., Russian Academy of Sciences, USA

Bresnick, Emery, Ph.D., University of Wisconsin Medical School, USA

Getzenberg, Robert, Ph.D., Institute Shadyside Medical Center, USA

Caiafa, Paola, Ph.D., Università di Roma “La Sapienza”, Italy

Ghosh, Sankar Ph.D., Yale University School of Medicine, USA

Cheng, Seng H. Ph.D., Genzyme Corporation, USA

Gojobori, Takashi, Ph.D., Center for Information Biology, National Institute of Genetics, Japan

Cole, David J. M.D., Medical University of South Carolina, USA

Harris David T., Ph.D., Cord Blood Bank, University of Arizona, USA

Crooke, Stanley, M.D., Ph.D. ISIS Pharmaceuticals, Inc. USA

Heldin, Paraskevi Ph.D., Uppsala Universitet, Sweden

Davie, James R, Ph.D., Manitoba Institute of Cell Biology, USA

Hesdorffer, Charles S., M.D., Columbia University, USA

DePamphilis, Melvin L, Ph.D., National Institute of Child Health and Human, National Institutes of Health, USA

Hoekstra, Merl F, Ph.D., Epoch Biosciences, Inc., USA

Hung, Mien-Chie, Ph.D., The University of Texas, USA

Kuroki, Masahide, M.D., Ph.D., Fukuoka University School of Medicine, Japan

Johnston, Brian, Ph.D., Somagenics, Inc, USA

Lai, Mei T. Ph.D., Lilly Research Laboratories USA

Jolly, Douglas J, Ph.D., Advantagene, Inc.,USA

Latchman, David S., PhD, Dsc, MRCPath

Joshi, Sadhna, Ph.D., D.Sc., University of Toronto Canada

Lavin, Martin F, Ph.D., The Queensland Cancer Fund Research Unit, The Queensland Institute of Medical Research, Australia

Kiyama, Ryoiti, Ph.D., National Institute of Bioscience and HumanTechnology, Japan

Lebkowski, Jane S., Ph.D., GERON Corporation, USA

Kotoku Kurachi, Ph.D., University of Michigan Medical School, USA

Li, Liangping Ph.D., MaxDelbr端ck-Center for Molecular Medicine, Germany

Kottaridis, Stavros D., Ph.D. Regulon Inc. USA

Lu, Yi, Ph.D., University of Tennessee Health Science Center, USA

University of London, UK

Krawetz, Stephen A., Ph.D., Wayne State University School of Medicine. USA

Lundstrom Kenneth, Ph.D., Bioxtal/Regulon, Inc. Switzerland

Kruse, Carol A., Ph.D., Sidney Kimmel Cancer Center. USA

MacDougald, Ormond A, Ph.D., University of Michigan Medical School, USA

Kuo, Tien, Ph.D., The University of Texas M. D. Anderson Cancer USA

Malone, Robert W., M.D., Aeras Global TB Vaccine Foundation, USA

Mirkin, Sergei, M. Ph.D., University of Illinois at Chicago, USA

Royer, Hans-Dieter, M.D., (CAESAR), Germany

Noteborn, Mathieu, Ph.D., Leiden University, The Netherlands

Rubin, Joseph, M.D., Mayo Medical School Mayo Clinic, USA

Paleos, Constantinos M., Ph.D. Institute of Physical Chemistry Demokritos.

Greece

Saenko Evgueni L., Ph.D., University of Maryland School of Medicine Center for Vascular and Inflammatory Diseases, USA

Pomerantz, Roger, J., M.D., Tibotec, Inc., USA

Santoro, M. Gabriella, Ph.D., University of Rome Tor Vergata, Italy

Raizada, Mohan K., Ph.D., University of Florida, USA

Salmons, Brian, Ph.D., (FSGBiotechnologie GmbH), Austria

Razin, Sergey, Ph.D., Institute of Gene Biology Russian Academy of Sciences, USA

Sharrocks, Andrew, D., Ph.D., University of Manchester, UK

Robbins, Paul, D, Ph.D., University of Pittsburgh, USA

Smythe Roy W., M.D., Texas A&M University Health Sciences Center, USA

Rosenblatt, Joseph, D., M.D, University of Miami School of Medicine, USA

Srivastava, Arun Ph.D., University of Florida College of Medicine, USA

Rosner, Marsha, R., Ph.D., Ben May Institute for Cancer Research, University of Chicago, USA

Steiner, Mitchell, M.D., University of Tennessee, USA

Tainsky, Michael A., Ph.D., Karmanos Cancer Institute, Wayne State University, USA

White, Robert, J., University of Glasgow, UK

Taira, Kazunari, Ph.D., The University of Tokyo, Japan

White-Scharf, Mary, Ph.D., Biotransplant, Inc., USA

Thierry, Alain, Ph.D., National Cancer Institute, National Institutes of Health, France

Wiginton, Dan, A., Ph.D., Children's Hospital Research Foundation, CHRF , USA

Trifonov, Edward, N. Ph.D., University of Haifa, Israel

Yung, Alfred, M.D., University of Texas, USA

Van Dyke, Michael, W., Ph.D., The University of Texas M. D. Anderson Cancer Center, USA

Zannis-Hadjopoulos, Maria Ph.D., McGill Cancer Centre, Canada

Vournakis, John N., Ph.D. Medical University of South Carolina, USA

Zorbas, Haralabos, Ph.D., BioM AG Team, Germany

Chi-Un Pae, MD, PhD, Associate Professor, Department of Psychiatry The Catholic Universoty of Korea College of Medicine

Associate Board Members Falasca, Marco, M.D., University College London, UK

Hiroki, Maruyama, M.D., Ph.D., Niigata University Graduate School of Medical and Dental Sciences, Japan

Gao, Shou-Jiang, Ph.D., The University of Texas Health Science Center at San Antonio, USA

Kazunori, Aoki, M.D., Ph.D., National Cancer Center Research Institute, Japan

Gibson, Spencer Bruce, Ph.D., University of Manitoba, USA

Rigoutsos, Isidore, Ph.D., Thomas J. Watson Research Center, USA

Gu, Baohua, Ph.D., The Jefferson Center, USA

Priya, Aggarwal Ph.D., University of Pennsylvania

Morris, Kevin Vance, Assistant Professor, The Scripps Research Institute, La Jolla, CA

W. Todd Penberthy, PH.D.,

Romano, Gaetano Ph.D. Research Associate Professor; Temple University, Philadelphia, U.S.A.

Yuefei Yu Ph.D. Texas Tech University Health Science Center. Research Scientist. Head of the research group.

Hongying Hao M.D./Ph.D., Instructor, Department of Surgery School of Medicine University of Louisville U.S.A.

Assistant Professor, Department of Molecular Genetics,Biochemistry, and Microbiology,

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Table of contents

Gene Therapy and Molecular Biology Vol 12 Number 2, December 2008

Pages

Type of Article

Article title

Authors (corresponding author is in boldface)

141-146

Review Article

Vaccinomics

Virendra S Gomase, Somnath Tagore

147-166

Research Article

Prediction of antigenic binders from cterminal domain Human papillomavirus oncoprotein e7

Virendra S Gomase, Somnath Tagore, Krishnan Shyamkumar

167-174

Research Article

Retrovirally-mediated genetic correction of mesenchymal stem cells from patients affected by mucopolysaccharidosis type II (Hunter Syndrome)

Carla Corradi-Perini, Thomas D. Southgate, Guy T Besley, Alan Cooper, John A Deakin, J Ed Wraith, Leslie J. Fairbairn, Robert F. Wynn, Ilaria Bellantuono

175-180

Research Article

A characterization of genetic haplotypes Josefa Salgado, Carmen Gil, Maitane Robles, Cristina Gutierrez, Carmen in BRCA1 identifies linkage Reyna, JesĂşs GarcĂ­a-Foncillas disequilibrium with a novel polymorphism in intron 7

181-188

Review Article

Molecular targets in medullary thyroid carcinoma

Sam W Moore

189-206

Research Article

Let-7, miR-125, miR-205, and miR-296 are prospective therapeutic agents in breast cancer molecular medicine

Debmalya Barh, Sanjeeb Parida, Bibhu Prasad Parida1, Geetha Viswanathan

207-218

Research Article

Suppression of Primary and Disseminated Murine Tumor Growth with eIF5A1 Gene Therapy

Songmu Jin, Catherine A. Taylor, Zhongda Liu, Zhong Sun, Bin Ye, John E.Thompson

219-238

Review Article

Hexavalent chromium exposure, genomic instability and lung cancer

Ana M. Urbano, Carlos F.D. Rodrigues, Maria Carmen Alpoim

239-246

Research Article

Fraz Arshad Malik, Mahmood Akhter Kayani1, Hina Iqbal, Wen G Jiang, Rafshan Sadiq

247-252

Research Article

Screening of coding region of metastasis suppressor genes KISS1 and KAI-1 for germ line mutations in breast cancer patients A new potential radiosensitizer- multiwalled carbon nanotubes modified by ammonium persulfate

253-258

Research Article

Jian-She Yang, Xigang Jing, Wen-Jian Li, Xiang-Kai Hu, Wei Wei, Zhuan-Zi Wang

Decreased risk of bladder cancer in men Frances M. Martin, Andrew M. Harris, Randall G. Rowland, William Conner1, treated with quinazoline-based !1Matthew Lane, Erik Durbin, Andre T. adrenoceptor antagonists Baron, Natasha Kyprianou

259-266

Review Article

Hematopoietic growth factors in the elderly

Wassim Mchayleh, Rajesh Sehgal, James Natale, Gurkamal Chatta

267-276

Research Article

HSP70 variations in the acute treatment with mood stabilizers in patients with bipolar disorder: results of a preliminary work

Chi-Un Pae, Antonio Drago, Jung-Jin Kim, Laura Mandelli, Ashwin A. Patkar, Diana De Ronchi, Alessandro Serretti

277-292

Review Article

Recombinant adeno-associated virus as vaccine delivery vehicles

Komal Vig, Roland Herzog, Douglas Martin, Eddie G. Moore, Vida A. Dennis, Shreekumar Pillai, Shree R. Singh

293-300

Research Article

Inhibition of focal adhesion kinase with her-2 targeted antibody pertuzumab (Omnitarg®, 2C4) in breast cancer cells

Emel Canbay, Bala Gur-Dedeoglu, Betul Bozkurt, Melih Karabeyoglu, Bulent Unal, Osman Yıldırım, Omer Cengiz3, Isik G Yulug

301-311

Research Article

Enhanced splenic protection and reduction of parasitaemia following transplantation of splenocytes overexpressing Bcl-2 in a murine malaria model

313-357

Review Article

Microtubule-targeted antitumor drugs: chemistry, mechanisms and nanoparticle formulations

Francisco Martínez-Flores, José Luis Ventura-Gallegos, Eréndira G. EstradaVillaseñor, Hilda Villegas-Castrejón, Epifanio Cruz-Zaragoza, Luis Covarrubias-Robles, Alejandro ZentellaDehesa, Martha Legorreta-Herrera Teni Boulikas, Ioannis Tsogas

359-370

Research Article

371-382

Research Article

Gene expression signature-based chemical genomics and activity pattern in a panel of tumour cell lines propose linalyl acetate as a protein kinase/NF"B inhibitor A short term pilot open label study to evaluate efficacy and safety of LG839, a customized DNA directed nutraceutical in obesity: Exploring Nutrigenomics

383-386

Case Report

387-394

Research Article

395-404

Review Article

405-414

Research Article

Severe phenotype of Morquio A disease in a child with S287L Nacetylgalactosamine-6-sulfate sulfatase mutation Attenuation of experimental liver fibrosis by hepatocyte growth factor gene delivery mediated by adenovirus Regulation of hormonal therapy resistance by cell cycle machinery Reversal of MDR1/P-glycoprotein associated drug resistance in human Hepatoblastoma

Saadia Bashir Hassan, Elin Lindhagen, Hanna Göransson, Mårten Fryknäs, Anders Isaksson, Hala Gali-Muhtasib, Rolf Larsson Kenneth Blum, Thomas JH Chen, Lonna Williams, Amanda LC Chen, William B. Downs, Roger L. Waite, T. Huntington, Simon Sims, Thomas Prihoda, Patrick Rhoads, Jeffrey Reinking, Dasha Braverman, Mallory Kerner, Seth H. Blum, Brien Quirk, Eric R Braverman Zoran S Gucev, Hassan Bouzidi, Velibor Tasic, Nada Popjordanova1, Ilija Kirovski, Zoran Trajkovski, Aleksandra Jancevska, Sami. Bajrami Yin Xu, Fei-qun Zheng, Jia Fang, Qunwei Zhang, Yi-de Qin, Yang Liu2, Renjie Yang3, Bin Wu Binoj Chandrasekharan Nair, Ratna K. Vadlamudi Steven W. Warmann, Joerg Fuchs

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Gene Therapy and Molecular Biology Vol 12, page 301 Gene Ther Mol Biol Vol 12, 301-311, 2008

Enhanced splenic protection and reduction of parasitaemia following transplantation of splenocytes overexpressing Bcl-2 in a murine malaria model Research Article

Francisco Martínez-Flores1,§, José Luis Ventura-Gallegos2,§, Eréndira G. EstradaVillaseñor1, Hilda Villegas-Castrejón1, Epifanio Cruz-Zaragoza3, Luis Covarrubias-Robles4, Alejandro Zentella-Dehesa2,5,*, Martha LegorretaHerrera6,* 1

Departamento de Morfología Celular y Molecular, Instituto Nacional de Rehabilitación.

Departamento de Medicina Genómica y Toxicología Ambiental, Instituto de Investigaciones Biomédicas, UNAM, México, D.F. 3 Instituto de Ciencias Nucleares, UNAM 4 Instituto de Biotecnología, UNAM 5 Departamento de Bioquímica, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán 6 Laboratorio de Inmunología Molecular, FES Zaragoza, UNAM 2

__________________________________________________________________________________ *Correspondence: Martha Legorreta-Herrera PhD, Laboratorio de Inmunología Molecular, Facultad de Estudios Superiores Zaragoza, Universidad Nacional Autonóma de México, Batalla 5 de mayo s/n Iztaplapa, CP 09230, México, DF México; Tel/Fax: 52(55)56230736; e-mail: marthal@servidor.unam.mx Alejandro Zentella-Dehesa PhD. Departamento de Bioquímica, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán.

Vasco de Quiroga 15, Sector XVI, Tlalpan, CP 14000, DF México; Tel 52(55)54870900 ext 2126; Fax: 52(55)56550011; e-mail: azentel@biomedicas.unam.mx Key words: Apoptosis, retroviral vectors, promoter PolII, oxidative stress Abbreviations: green fluorescent protein, (GFP); intravenously, (iv); Moloney Leukaemia Virus, (MLV) Received: 17 November 2008; Revised: 9 December 2008 Accepted: 9 December 2008; electronically published: December 2008

Summary Malaria is one of the most important infectious diseases worldwide. During acute infection, the activation of the immune response and parasite clearance by the spleen are key host defence mechanisms. Apoptosis of lymphocytes is believed to compromise the immune response in malaria cases. As limited progress has been made using gene therapy against parasitic infections, we explored the potential beneficial effect of reconstituting Plasmodium chabaudi infected mice with transduced splenocytes overexpressing Bcl-2. An ecotropic retrovirus encoding GFP and Bcl-2 was packaged in 293T cells. A second retrovirus expressing only GFP was used as control. Initially, CBA/Ca mice were transplanted with 2 x 107 total splenocytes from syngenic donor mice transduced with retroviral particles. Two hours later recipient mice were infected with 5 x 104 P. chabaudi parasitised erythrocytes.

Parasitaemia was evaluated every 24 h. Seven days post-infection, we evaluated splenic histology and Bcl-2 expression via RT-PCR and western blot. The protection against H2O2- induced apoptosis was tested on isolated total splenocytes. The efficiency of retroviral infection, expression of Bcl-2 and reporter gene was confirmed by Fluorescence microscopy, RT-PCR and western blotting of splenocytes from transplanted with cells transduced with GFP- or Bcl-2-expressing retroviruses. Parasitaemia in mice transplanted with GFP-transduced splenocytes transiently decreased 10-fold at day five after Plasmodium infection and was further decreased when mice were transplanted with Bcl-2-transduced splenocytes. The splenic architecture of mice that received transduced cells was preserved compared to control mice. Cytoprotection in vitro was enhanced with the Bcl-2 construct. The protective effect correlated with increased the cellularity in the spleen and overexpression Bcl-2. We tested the use of standard gene therapy strategies based on the reconstitution of irradiated mice with genetically modified heterologous cells in 301

MartĂ­nez-Flores et al: Enhanced splenic protection and reduction in a murine malaria model an experimental murine model of malaria. We observed transient reduction of parasitaemia, preservation of splenic architecture and increased cell survival in vitro against oxidative stress. Although the experimental design aimed to test the effect of Bcl-2 overexpression, transplantation of cells transduced with the empty retroviral vector resulted in a significant protective effect accompanied by the increased expression of endogenous Bcl-2.

introduced by genetic vectors (plasmids and viral vectors) encoding the corresponding cDNAs. Although this principle can be applied to a variety of diseases its applications to the treatment of infectious diseases remains to be developed. Reconstitution of infected individuals with genetically modified immune cells provides a simple application of the principles of the genetic therapy in these kinds of diseases.

If apoptosis is important for the progression of malaria, overexpression of anti-apoptotic proteins such as Bcl-2 should have a protective effect. Consequently, we explored the evolution and course of parasitaemia in P. chabaudi-infected mice previously transplanted with splenocytes over-expressing Bcl-2, as well as the resistance against hydrogen peroxide-induced apoptosis in splenocytes. We also documented the cytoarchitecture and histology of the spleen during P. chabaudi infection.

I. Introduction Malaria is the leading infectious cause of death worldwide, and estimated of two billion people (more than 40% of the world population) live in areas with a high risk of infection. The global annual incidence ranges between three to five hundred million clinical cases, with a total mortality between 2 to 3 millions a year (Wykes and Good, 2007).

Attempts to curtail the devastating effects of malaria have encountered many obstacles including the rapid development and spread of vector resistance to residual insecticides, a decreasing parasite response to clinically used drugs and the lack of effective and affordable alternative anti-malarial therapies. Despite all these difficulties the use of the gene therapy against infectious diseases, particularly malaria, has been poorly explored.

The cellular immune response to Plasmodium infection has been widely studied (Good and Currier, 1992; Taylor-Robinson and Phillips, 1993; Von Der Weid et al, 1994). In general, acute infection with Plasmodium is associated with the activation of peripheral T cells, alterations in the level of cytokine production (Cross and Langhorne, 1998) and lymphopaenia (Wipasa et al, 2001).

These changes can compromise the immune response and have been explained by apoptosis of lymphocytes, relocation of peripheral lymphocytes or both. In fact, it has been shown that schistosome, toxoplasma, and trypanosome infections induce apoptosis in host mononuclear cells (Lopes et al, 1995; Khan et al, 1996; Estaquier et al, 1997). Moreover, apoptosis of lymphocytes may contribute to parasite survival, through down regulation of anti-parasite inflammatory responses and immunosuppression.

Bcl-2 was the first characterised member of a family of genes that regulate apoptosis by preventing or inducing cell death (Korsmeyer et al, 1995; Kluck et al, 1997; Yang et al, 1997). The biochemical basis of their actions has not been completely elucidated and remains unclear.

However, over-expression of Bcl-2 can block many forms of apoptosis in transfected cell lines, transgenic mice or transduced organs in several in vivo models (Bilbao et al, 1999; Molto et al, 2003; Mitsiades et al, 2007).

Apoptosis is a major mechanism y which the development, maturation and activation of lymphocytes is regulated. During Plasmodium infection, apoptosis has been implicated as a mechanism whereby parasites escape from the immune system. Helmby et al have described the increased frequency of apoptosis in macrophages, B and T cells in the spleen of P chabaudi-infected mice (Helmby et al, 2000). These alterations correlate with increased expression of Fas and Fas-ligand, suggesting that apoptosis is, in part, Fas-mediated.

Gene therapy aims to correct defects in gene expression through the expression of exogenous proteins

II. Materials and Methods A. Animal model design CBA/Ca mice (kindly donated by Dr. W. Jarra, National Institute for Medical Research, London, UK) were used in all experiments; animals were maintained and cared for according to the Mexican Animal Regulations in a specific pathogen free environment. Splenocytes were isolated from healthy male mice, cultured in RPMI-1640 media supplemented with 10% foetal bovine serum, penicillin-streptomycin and amphotericin B (100 U/ml, 100 !g/ml and 0.25 !g/ml respectively) and stimulated with recombinant IL-2 (100 U/ml Sigma, USA). Cells were transduced with retroviral vectors encoding either GFP alone or GFP and Bcl-2. After twenty-four hours post transduction the cells were transplanted intravenously (iv) into sub-lethally irradiated mice in tree groups: 1) Control: non-transduced cells; 2) GFP: cells expressing only GFP; 3) Bcl-2: cells expressing both GFP and Bcl-2. The sub-lethal irradiation allowed the transplanted cells to repopulate the spleen of the recipient mice.

After four hours post transplant, all mice were infected with P. chabaudi parasitised erythrocytes. Mice were bred and maintained at the FES-Zaragoza-UNAM animal care facility in microisolator cages and were provided with a parasite promoting diet (TD.993 Harlan USA) and acidified water ad libitum; animals were sacrificed at the indicated days post-infection for the different studies.

B. Plasmid constructs All retroviral plasmids were based on the echotropic system using the Moloney Leukaemia Virus (MLV) Long Terminal Repeats (IMGENEX Corp.). The pCNRX-GFP plasmid expresses of the green fluorescent protein (GFP) under the transcriptional control of the minimal CMV promoter, flanked by the LTR´s of MLV. The Bcl-2 cDNA was cloned downstream of the DNA Polymerase II promoter into an EcoRI site of the pCLNRX-GFP plasmid. The resulting construct was named pCLNRX-GFP-Bcl-2. Endotoxin-free, high scale plasmid preparations (Qiagen Inc, USA) were used for plasmid sequencing, transfection assays, functional expression and viral packaging in HEK-293T cells.

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Gene Therapy and Molecular Biology Vol 12, page 303 µL of the cDNA (RT reaction mixture). #-actin and Bcl-2 were simultaneously amplified in the same tube. After 28 cycles, the PCR products were separated on 5 % acrylamide gels and stained with ethidium bromide. Band intensity was measured via densitometry (GelDoc, BioRad, Hercules, USA). Results are shown as the ratio between the density (arbitrary units) of Bcl-2 and the density of #-actin.

C. Packaging of retroviral particles The night before transfection, 3 x 105 HEK-293T cells/well were seeded in 6-well plates with DMEM media (Gibco/Invitrogen, USA) supplemented with 10% heat inactivated foetal bovine serum, (Gibco/Invitrogen) and incubated at 37°C with 5% CO2.

The media was replaced 3 h before co-transfecting the cells with 5 µg of both pCLNRX-GFP and pCL-Eco or pCLNRXGFP-Bcl-2 and pCL-Eco using a calcium phosphate precipitation protocol (Gibco/Invitrogen). In all transfection experiments, endotoxin-free plasmids were used to transfect the cells. The media was replaced 24 h post-transfection and the supernatants were collected 48 h after transfection. polybrene (Sigma, USA) was added to a final concentration of 8 µg/mL before infecting the target splenocytes.

H. Microscopy analysis GFP expression in infected cells was detected using an epifluorescent microscope (Bio-Rad Inc). Histological analysis was performed on frozen spleen slice sections embedded in Tissuetek (Dako). Several slices were fixed for routine haematoxylin and eosin staining protocol. Morphometric analysis and histopathological description was performed in the Department of Pathology of the Instituto Nacional de Rehabilitación (Mexico City).

D. Retroviral infection Splenocytes were isolated from healthy male mice and 3 x 108 cells were maintained in supplemented RPMI-1640 and 100 U/ml of recombinant IL-2 (Sigma-Aldrich, USA). The infection procedure was performed by adding the retrovirus-containing supernatants at a1:1 ratio to the splenocytes. After 24 h of incubation under standard conditions, transduced cells were used for transplants.

I. Cell phenotype characterization Suspensions of 1 x 106 splenocytes were washed in PBS and stained with pre-calibrated dilutions of PE-conjugated anti mouse CD3, CD4, CD8 or B220 monoclonal antibodies (BD Pharmingen, San Diego, CA, USA). Cells were incubated for 30 min at 4 °C, washed twice with FACS-buffer (0.1% bovine serum albumin, 0.1% sodium azide in PBS) and suspended in 500 µl of the same buffer. Fluorescence was analysed using a FACSCalibur flow cytometer and Cell Quest software (BD, San Jose, CA, USA). For each sample, 40,000 events were acquired and analysed. Dead cells were excluded by gating on PI negative cells.

E. Irradiation and spleen cell-transplant Recipient mice were exposed to "-irradiation equivalent to a total dose of 4.5 Gy at a rate of 450 cGy /min using the Siemens Biomed Inc. irradiator with a Cobalt-68 source (Instituto de Ciencias Nucleares, UNAM). Two hours postirradiation, the mice were transplanted with 2 x 107 transduced splenocytes resuspended in 100 µl of PBS (Gibco/ Invitrogen) by iv injection.

J. Statistical analysis Student’s significance.

t-test

was

used

to

determine

statistical

F. Infection and parasitaemias

III. Results

Groups of 6-8 week-old male CBA/Ca mice were inoculated iv with 5 X 104 P. chabaudi-parasitised erythrocytes as previously described (Legorreta-Herrera et al, 1993). Parasites were kindly donated by Dr. K N Brown (National Institute for Medical Research, London, UK). Parasitaemia was evaluated with Giemsa-stained blood smears starting at day 4 through day 7 post-infection. The course of infection in each group is shown as the percentage of parasitaemia.

A. Expression vectors and splenocyte infection Hematopoietic and lymphoid cells that have been transduced with retroviral vectors have been reported to reconstitute approximately 20 % of the total population of splenocytes (Mcmillin et al, 2005; Ide et al, 2008). In order to introduce a recombinant form of Bcl-2 into total splenocytes of mice which will be infected with P. chabaudi, to retroviral expression vectors, pCLNRX-GFP and pCLNRX-GFP-Bcl-2, were developed (Figure 1A).

In both constructs, the GFP cDNA was placed under the transcriptional control of the CMV enhancer promoter. In the case of pCLNRX-GFP-Bcl-2, the cDNA of rat Bcl-2 was placed under the control of the DNA polymerase II promoter. Therefore, Bcl-2 will only be expressed in proliferating cells, while GFP should be constitutively expressed even in quiescent cells.

Freshly prepared retroviral particles were used to transduced total murine splenocytes as described in Materials and Methods. Using fluorescence microscopy to detect the expression of GFP, we verified that the transduction protocol had no effect on the viability of the splenocytes (Figure 1B). The optimal multiplicity of infection was determined by serial dilution.

Approximately 1 x 106 viral particles/ml were used in all experiments and mixed with 1 x 106 total splenocytes in a final volume of 1 ml. Normally, splenocytes were

G. Bcl-2 mRNA expression On day 7 post-infection, mice were sacrificed and splenic mRNA was extracted using Trizol (Invitrogen). DNA was digested with DNAse I (Invitrogen) according to the manufacturer’s instructions and total RNA was quantified spectrophotometrically. Total RNA (1.5 µg) was reverse transcribed using 0.5 mM dNTP’s (Pharmacia, Uppsala, Sweden), 40 U of RNAse inhibitor (Invitrogen) and 200 U of MMLV-RT (Invitrogen) and incubated at 37°C for 30 min. A 1 µl sample of the resulting cDNA was used to amplify Bcl-2 and !-actin in duplicate. Both the number of cycles and the cDNA concentrations were optimised such that the reactions were in the logarithmic phase of amplification.

The following primers were used for Bcl-2 amplification: forward TCATGAAGACAGGGGCCTTTT, reverse TGGAGCTGCAGAGGATGATTG; and for !-actin: forward GTGGGCCGCTCTAGGCACCAA, reverse CTCTTTGATGTCACGCACGATTTC. PCR reactions were performed in a total volume of 20 µl. Amplification was carried out in 50 mM KCl, 10 mM Tris-HCl, 0.1 mg/mL Gelatin (SigmaAldrich), dNTP’s 200 mM each (Pharmacia, Uppsala, Sweeden), 2 mM MgCl2, 100 n moles each primers, 0.5 U Ampli Taq polymerase (Applied Biosystems, Branchburg, NY, USA) and 1

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MartĂ­nez-Flores et al: Enhanced splenic protection and reduction in a murine malaria model transplanted into irradiated mice 18 h after in vitro viral infection. In order to evaluate the efficiency of transduction, control cultures were monitored for GFP expression for 24, 48 and 72 h (data not shown). Figure 1B shows representative images of transduced splenocytes. The GFP signal was always bright in cells transduced with the construct encoding only GFP (Figure 1B, +/-). The GFP signal in cells transduced with the construct encoding Bcl-2 (+/+) was always of a lower intensity compared to the construct expressing only GFP. Despite the fact that the splenocyte came from different donors the transduction was consistent and reproducible.

The transduction efficiency was quantified by flow cytometry on the transduced cells 25-35 % of the total population of transduced splenocytes was GFP positive (Figure 1C central and right histograms).

B. In situ localization revealed homing of transplanted cells to the spleens of recipient mice To verify the homing of the transplanted cells to the spleens of recipient mice, we used GFP expression as a marker. Seven days post-transplantation and infection with P. chabaudi, longitudinal spleen slices were analysed for GFP expression. Large clusters of fluorescent cells were detected in the spleens of mice transplanted with Bcl-2 transduced cells (Figure 2, Bcl-2) compared to untransduced controls (-/-) or to GFP-transduced cells (+/). Additionally, more fluorescent cells were found along the periphery of the spleens of mice transplanted with cells transduced with the Bcl-2-expressing construct (+/+).

Interestingly, the spleens of mice transplanted with control cells were more fragile than the spleens from animals transplanted with transduced cells. These observations

Figure 1. Plasmid constructs used for retroviral gene delivery and expression in murine splenocytes. (A) Schematic representation of plasmid constructs for packaging of retroviral particles in 293-T cells (as described in Materials and Methods). (B) Fluorescence microscopy of uninfected murine splenocytes (-/-), infected with GFP vector (+/-) and infected with GFP-Bcl-2 (+/+). (C) Flow cytometry histograms examining the efficiency of transduction in total splenocytes before transplant. Control (CTR), cells transduced with GFP (GFP) or with GFP-Bcl-2 (Bcl-2).

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Figure 2. GFP signal in the spleens of recipient mice after transduction and seven days post-transplant. After irradiation mice received a transplant with the different transduced splenocytes were iv infected withP. chabaudi, spleens were removed and the fluorescent signal was evaluated in fresh tissue slices. Each field is presented in light transmission (Halogen light), UV/blue illumination (UV/blue) and green fluorescence (excitation 488 nm emission 530 nm). The first line correspondsto control animals transplanted with not-transduced splenocytes (-/-). The second (+/-) and third (+/+) lines correspond to the spleens of animals transplanted with GFP- or Bcl-2-transduced cells respectively.

demonstrate that the homing of splenocytes transduced with the different retroviral constructs took place in recipient mice transplanted with similar efficiencies.

transplanted cells, but it is also possible that the presence of the transplanted population leads to the expression of endogenous Bcl-2 in their surrounding cells.

C. Bcl-2 mRNA and protein expression in the spleens of transplanted mice

D. Decreased susceptibility to oxidative stress in cells expressing Bcl-2 both in vitro and in vivo

In order to identify and verify Bcl-2 transgene expression, RT-PCR and western blot analysis were performed on the spleens of transplanted mice.

Interestingly, the spleens of mice transplanted with GFPtransduced cells exhibited significantly enhanced Bcl-2 mRNA and protein expression (Figures 3A and B, GFP).

Figure 3A (Bcl-2) shows the amplified Bcl-2 fragment from the spleens of mice receiving Bcl-2-transduced cells.

Western blot analysis revealed Bcl-2 protein in the spleens of mice receiving splenocytes transduced with either construct (Figure 3B, GFP and Bcl-2). A 15-fold increase in the expression of Bcl-2, when compared to mice receiving untransduced cells, was seen in mice receiving GFP-transduced splenocytes (GFP). However, Bcl-2 expression was greater (50-fold increase) in the spleens of mice transplanted with Bcl-2 transduced cells (Figures 3A and B, Bcl-2). These results confirm the overexpression of Bcl-2 when cells are transduced with retroviruses encoding Bcl-2. Nevertheless, transduction alone appears to be enough to promote the expression of endogenous Bcl-2. This expression could occur in the transduced

As Bcl-2 overexpression confers protection against a variety of stressful conditions, including high concentrations of H2O2 and inducers of apoptosis (Korsmeyer et al, 1995; Yang et al, 1997; Mitsiades et al, 2007), we tested the potential protective effects of Bcl-2 overexpression on the viability of total splenocytes exposed to increasing concentration of H2O2 (Figure 4).

Initially, the efficiency of the protective effect of Bcl-2 overexpression was evaluated 48 hrs after in vitro culture following transduction (Figure 4A). Cell viability was assessed 2 h after the addition of increasing concentrations of H2O2 and is expressed relative to normal splenocytes not exposed to H2O2 (100%). In untransduced cells, the viability decreased with increasing H2O2 concentrations, while GFP-transduced cells were refractory to H2O2induced cell death, and viability remained relatively unchanged at approximately 50%. Statistical significance was only observed when the viability of normal cells and Bcl-2-transduced cells treated with 2 mM of H2O2 was compared (p<0.05). Having shown that the transduction 305

MartĂ­nez-Flores et al: Enhanced splenic protection and reduction in a murine malaria model with the retrovirus expressing Bcl-2 confers protection against H2O2 in vitro we evaluated if the protective phenotype was retained in vivo when mice were transplanted with transduced cells and infected with P. chabaudi. Given the difficulties in evaluating the potential protective effect of the expression of Bcl-2 in vivo, we evaluated cell viability in vitro in the total splenocyte population 72 h after transplantation (Figure 4B).

Interestingly, the general trend was similar to that observed in total splenocytes prior to transplantation (Figure 4A). Statistically significant differences (p<0.05) in the viability of splenocytes from mice receiving untransduced control cells or Bcl-2-transduced cells were only observed when cells were treated with the lowest dose of H2O2 (1 mM; Figure 4B).

Figure 3. Bcl-2 expression in the spleens of transplanted mice infected with P. chabaudi. Mice were transplanted with 2 x 107 splenocytes from donor mice, these cells were previously transduced with the Bcl-2expressing retrovirus (Bcl-2), the GFP-expressing retrovirus (GFP) or subjected to mock transduction (CTR). All mice were infected iv with 5 x 104 parasitised erythrocytes the same day. Seven days after parasite infection, animals were sacrificed and Bcl-2 expression in the spleen was analysed. (A) RT-PCR of Bcl-2 (lower panel) and densitometric analysis (histogram) compared to !-actin expression. (B) Western blot of Bcl-2 on total spleen cell protein extracts. L929e1: Total protein extracts from the L929 murine fibroblast cell line constitutively overexpressing Bcl2 used as a positive control. !actin was used as a loading control. Numbers below the western indicate the fold increase in the !-actin-normalised Bcl-2 signal compared to the control.

Figure 4. Hydrogen peroxide resistance of splenocytes before and after transplant into irradiated receptor mice infected with P. chabaudi. The viability of splenocytes after 2 h of challenge with different concentrations of H2O2 was determined. (A) Viability was measured after culture for 48 h in vitro. (B) Viability was evaluated 72 h after mice were irradiated and reconstituted with 3 x 107 splenocytes. As in previous experiments donor cells were either GFP- or BCL-2-transduced. Control cells were subjected to mock transduction (CTR). * p< 0.05 compared to control (CTR).

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Gene Therapy and Molecular Biology Vol 12, page 307 Taken together, these results demonstrate an increased cell viability in transduced cells, regardless of the presence or absence of the Bcl-2 cDNA, and this protective effect remained 72 h post-transplantation into irradiated mice.

While splenocytes transduced with the retrovirus expressing GFP alone demonstrated an increased viability compared to untransduced cells, the viability was always higher in cells expressing Bcl-2.

revealed a marked reduction in cellularity (Figure 5C, CTR), close to 40% with respect to the spleens from normal, non-transplanted animals. More than 90% of these cells were immunoblasts in the lymphoid compartment.

Additionally, the white:red pulp ratio was 1:3 in the spleens of mice transplanted with non-transduced cells compared to 1:5 in normal untransplanted spleens (Figure 5A, NORMAL and CTR). Haemosiderin deposits and detritus were also observed in the spleens of mice transplanted with untransduced splenocytes.

In the GFP group, the total cell population in the lymphoid compartment was 53% of the normal, untransplanted spleen (Figure 5C). Immunoblasts were the most abundant cell type (90% of the cells) with a small amount of macrophages. Apoptotic bodies and mitotic figures were distributed randomly. Additionally, the red pulp was enlarged and contained a high number of parasitised cells as well as macrophages with haemosiderin (data not shown). The white:red pulp ratio was 2:1.

E. Histologic and morphometric analysis of the spleen Both a macroscopic and microscopic analysis of the spleens of recipient mice was carried out. All the spleens had increased friability but it was more evident in the control and GFP groups (data not shown). The histology of the spleens from mice transplanted with normal splenocytes (Figure 5A, NORMAL) was different when compared to the spleens of normal, non-transplanted mice (Figure 5A, CTR). Spleens from mice transplanted with non-transduced cells and infected with P. chabaudi

Figure 5. Histologic and morphometric analysis of the fresh spleen slices stained with haematoxilin and eosin. A ( ) Comparative analysis of tissues from mice spleens of different experimental groups. Histology of an animal that was not transplanted and nor infected with P. chabaudi (NORMAL). Histologies of animals infected with P. chabaudi and transplanted with: normal cells (CTR), GFP transduced cells (GFP) or Bcl-2-transduced cells (Bcl-2). Red Pulp (RP); White Pulp (WP). (B) Magnification of the micrograph labelled Bcl-2.

Immunoblasts (I); small cell (S); detritus (D); haemosiderin (H). (C ) Histogram of the morphometric analysis from the four groups.

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MartĂ­nez-Flores et al: Enhanced splenic protection and reduction in a murine malaria model The spleens of mice transplanted with Bcl-2transduced cells and infected with P. chabaudi (Figure 5A, Bcl-2) had 77% of the cellularity seen in normal, untransplanted spleen (Figure 5C, Bcl-2). In this group a new cell population was observed that was characterised by a small size with a clear, defined central round nucleus.

This new population comprised 30% of the total splenocytes, while immunoblasts and macrophages comprised 66% and 4%, respectively. As seen in Figure 5C, the number of immunoblasts and macrophages was very similar in the three groups infected with P. chabaudi (CTR, GFP and Bcl-2). Combined other cell types in the lymphoid compartment represented less than 1% of the total population. The white to red pulp ratio was similar to that observed in the GFP group (2:1).

We conclude that the spleens from mice transplanted with cells transformed with the Bcl-2-transduced cells infected with P. chabaudi retained the cytoarchitecture with diminished cellularity when compared to the spleens from normal, non-transplanted mice. In addition, a higher white:red pulp ratio was observed in the spleens of mice transplanted with transduced cells, regardless of the presence or absence of Bcl-2.

evaluated daily after day 4 and until day 7 post-parasite infection. Parasitaemia increased gradually and no difference was observed at day 4. Interestingly, on day 5 post-infection mice transplanted with splenocytes transduced with either retrovirus showed a transient 10fold decrease in parasitaemia (solid squares and triangles, p<0.01). Additionally, mice transplanted with the Bcl-2transduced cells (solid triangles, p<0.05) showed a significantly lower level of parasitaemia compared to mice transplanted with GFP-transduced cells (solid squares).

However, by day 6, the protective effect of Bcl-2 was lost.

We conclude that the retroviral transduction alone conferred a transient protection that was strengthened with the additional expression of Bcl-2.

IV. Discussion The use of viral vectors for gene therapy has focused on genetic disorders, such as metabolic diseases or cancer (Grompe et al, 1995; Bilbao et al, 1999; Gomez-Navarro and Curiel, 2000; Bartsch et al, 2007; Muul and Candotti, 2007), while little work has been done utilizing the vector to treat infectious diseases. Using conventional methods, we have introduced an exogenous form of Bcl-2 cDNA into murine splenocytes with the aim of interfering with the apoptosis present in an experimental model of malaria.

In spite of the relatively small percentage of cells transduced with the retroviral vector that repopulated the spleens of irradiated mice, their presence appeared to be enough to induce biological effects against Plasmodium, even in the absence of the Bcl-2 cDNA. Taken together, these findings suggest that the transduction procedure with the retroviral vector is sufficient to induce beneficial responses against Plasmodium, possibly by recruiting normal splenocytes. Similar to other studies (Del Vecchio et al, 2001; Mcmillin et al, 2005; Kinyanjui et al, 2006) that have used viral vectors, we encountered the problem of generating a high enough viral titre to elicit a robust biological response (Figure 1B, C).

F. Transfer of transduced cells into animals infected with P. chabaudi reduces parasitaemia During P. chabaudi infection, a variety of immunological mechanisms have been implicated in the destruction of infected erythrocytes, including the effector function of splenic macrophages. Immunosupression linked to the activation of lymphocyte apoptosis has been described in malaria, leishmania and schistosoma parasitosis (Estaquier et al, 1997; Das et al, 1999; Mukherjee et al, 2006). Consequently, we tested the effect of Bcl-2 overexpression sub-lethally irradiated mice transplanted with transduced splenocytes and infected with P. chabaudi (Figure 6) on parasitaemia. Parasitaemia was

Figure 6. Course of parasitaemia with Plasmodium chabaudi in mice transplanted with genetically modified cells. Parasitaemia was measured as described in Materials and Methods in mice sublethally irradiated and transplanted with: normal splenocytes (CTR); GFPtransduced splenocytes (GFP) or Bcl-2-transduced splenocytes (Bcl-2). Bars represent standard deviation of the mean.

Comparison CTR against GFP or Bcl-2 is represented by *, with a p< 0.01. Comparison between GFP and Bcl-2 is represented by **, with a p<0.05.

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Gene Therapy and Molecular Biology Vol 12, page 309 We attempted to increase the efficiency of transduction in different ways: i) identification of the optimal time to harvest the viral particles; ii) concentration of the retroviral particles with different reagents such as hexadimethrine bromide (polybrene) or chondroitin 6sulphate (Cepko, 2001; Del Vecchio et al, 2001; Mcmillin et al, 2005); iii) the use of a variety of re-infection protocols; iv) expansion of the transduced cell population with growth factors such as IL-2. However, the optimal combination of all these variables did not lead to transduction efficiencies above 30 % (Figure 1C).

The reconstitution protocol most frequently used in experimental models of transplantation uses the total splenocyte population, as it is believed that the interactions between the various populations of cells are required for the generation of an adequate immune response (Legorreta-Herrera et al, 1993). As such, we transplanted total splenocytes following in vitro transduction.

Preliminary attempts to characterize the transduced cells suggest that they include B220+ cells, a minority CD3+ cells and other cells negative for these markers (data not shown). While it is possible that splenic repopulation with untransduced cells may contribute to the protective effects observed, we discounted this possibility based on the fact that the control group corresponds to irradiated animals transplanted with mock-transduced cells.

In spite of the low number of transduced cells used in the transplant, we were able to observe GFP positive cells in the spleen of transplanted mice 48 h (Figure 2) and even 7 days after transplantation (data not shown).

Interestingly, despite the fact that our study was designed to observed the effects of over-expression of Bcl2, the transduction of splenocytes with the empty construct (pCLNRX-GFP) led to the increased expression of endogenous Bcl-2 in vivo 7 days post-transplant (Figures 3A, B). Taking into account that only a small number of GFP positive cells were present at day 7 after transplantation, both Bcl-2 mRNA and protein are likely generated in non-transduced cells. We postulate that transduced cells influence the splenic microenvironment such that endogenous Bcl-2 expression is stimulated. It is possible that the transduction with retroviruses expressing Bcl-2 confers an increased survival of these cells further improving their influence on the rest of the spleenocytes.

We also postulate that the transduced cells influence the splenic microenvironment through the secretion of paracrine factors. Alternatively, the presence of transduced cells could activate a defence response in the remaining population of splenocytes. At this point we cannot distinguish between these two possibilities. In any event, the fact that expression of transgenic Bcl-2 has only a minor contribution to the in vitro protection against H2O2 as well as the decreased parasitaemia observed in vivo could be due to the low transduction efficiency (Figures 4, B).

In contrast, the gross morphology and cytoarchitecture of the spleen were well-preserved only in mice transplanted with Bcl-2-transduced cells and infected with P. chabaudi. This effect could be appreciated macroscopically with less organ fragility and the preservation of the proportion of red pulp compared to

normal spleens. One measure of the organ damage during Plasmodium infection is the marked reduction in cellularity observed in the control group reconstituted with untransduced splenocytes compared to the other three groups. Additionally, a new cell population represented mainly by cells with morphology similar to mature lymphocytes was observed. Further analysis with surface markers could better define this population (Figure 5A, Bcl-2, magnified in Figure 5B).

Increasing splenic fragility is commonly observed during the progression of malaria. This event is the consequence of clearance of the parasitised erythrocytes by the spleen. However, the radiation procedure used to promote cellular homing in this animal model could have a synergistic effect on the splenic integrity. These factors could explain the increased spleen friability in all animals.

However, the marked reduction of fragility observed only in the Bcl-2-transduced mice correlates with the overexpression of exogenous protein. Recently, Hanson et al, reported that increased intracellular levels of Bcl-2 confer an anti-apoptotic effect that depends on the kind of promoter employed to express Bck-2 (Hanson et al, 2008).

In this study, exogenous Bcl-2 expression is directed by the Pol-II promoter suggesting that Bcl-2 expression is limited only to replicating cells. It is noteworthy that in the GFP-transduced group endogenous Bcl-2 is already increased. Consequently, in the Bcl-2-transduced group, an additive effect of endogenous and exogenous Bcl-2 can be postulated. In summary, the biological effect of a small number of cells expressing recombinant Bcl-2 on splenic morphology and cytoarchitecture could be interpreted to favour survival and maturation of the surronding cells. A similar effect has been reported previously in a model of endothelial cells (Enis et al, 2008).

As opposed to the white:red pulp ratio in the control group, the white:red pulp ratio in the spleens of mice transplanted with either population of transduced cells was similar to ratio seen in normal spleens. This could be interpreted as an active cellular phase of the immune response.

Interestingly, the positive effects in the splenic cytoarchitecture and in the white:red pulp ratio correlate with the homing of a small number of the transplanted transduced splenocytes expressing Bcl-2 and the appearance of a distinct cell population characterized by its small size and clear, defined central nucleus. The morphology of this latter cell population is suggestive of mature splenocytes (Figure 5).

The most dramatic biological effect observed was the 10-fold decrease in parasitaemia that implies an efficient host response against the parasite despite the small number of transplanted cells transduced with the retroviral vector.

The fact that this protective effect was elicited with a small number of cells expressing only GFP suggests that the positive modulation of immune cells from the recipient mouse lead to ore efficient parasite elimination. This effect correlates with the15-fold increased expression of endogenous Bcl-2 (Figures 3A,B). Exogenous expression of Bcl-2 provided an additional 2-3-fold increase in protection (Figure 6) that correlated with a similar increased expression of Bcl-2 due to the expression

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construct. In addition, all correlate with the histological findings that suggest an improved splenic microenviroment that could effectively induce a cellular immune response against the parasite. However, it remains unclear why protection is transient.

While gene therapy is based on the premise of introducing a specific cDNA to compensate for endogenous deficiencies, we found that in the case of experimental murine malaria, the presence of splenocytes transduced with the empty retroviral vector have a significant protective effect both in vitro and in vivo. Our observations indicate that a small number of genetically manipulated splenocytes had a significant biological effect likely due to the recruitment of normal cells. In this regard, malaria offers an interesting model in which the spleen plays a central role in the destruction of parasitised erythrocytes. This observation suggests that in parasitic infections that require efficient splenic function, empty viral vectors used in gene therapy may be able to activate host defence responses by themselves.

Author’s contributions FMF, JVG and MLH. Performed all experiments and wrote the manuscript AZD wrote the manuscript and contributed to the analyses of the data. EGE and HVC and FMF performed and interpreted the histopathology. LCR provide the constructs and viral vectors. ECZ was responsible for the animal irradiation.

Acknowledgements We thank to units of electronic microscopy and molecular biology (Instituto de Fisiología Celular, UNAM) for assistance. This work was supported by the following grants: PAPIIT, UNAM: IN22929607, IN214007; CONACyT: 45519-M and 52782.

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Gene Therapy and Molecular Biology Vol 12, page 313 Gene Ther Mol Biol Vol 12, 313-357, 2008

Microtubule-targeted antitumor drugs: chemistry, mechanisms and nanoparticle formulations Review Article

Teni Boulikas1,2*, Ioannis Tsogas3 1

Regulon, Inc. 715 North Shoreline Blvd, Mountain View, California 94043, USA Regulon AE, Afxentiou 7, Alimos, Athens 17455, Greece 3 Dendrigen AE, Afxentiou 3, Alimos, Athens 17455, Greece 2

__________________________________________________________________________________ *Correspondence: Teni Boulikas, Ph.D., Regulon AE, Afxentiou 7, Alimos, Athens 17455, Greece; Tel: +30-210-9858454; Fax: +30210-9858453; e-mail: teni@regulon.org Keywords: Microtubules, tubulin, vinca alkaloids, vinblastine, vinorelbine, vincristine, vindesine, vinflunine, taxanes, paclitaxel, docetaxel, epothilones A, B, D, ixabepilone, sagopilone, discodermolide, P-glycoprotein, dictyostatin, abraxane, colchicine, aplidine, nocodazole, dictyostatin, peloruside A, cyclostreptin, vinflunine, griseofulvin, nanoparticle Abbreviations: 2!,3!-cyclic nucleotide-3!-phosphodiesterase, (CNP); Breast Cancer Gene 1, (BRCA1); disease control rate, (DCR); Epidermal Growth Factor Receptor, (EGFR); Guanosine 5'-Triphosphate, (GTP); half maximal inhibitory concentration, (IC50); highdensity lipoprotein, (HDL); metastatic breast cancer, (MBC); Microtubules, (MTs); overall response rate, (ORR); renal cell carcinoma, (RCC); Retinoblastoma, (RB); response rate, (RR); vascular endothelial growth factor, (VEGF) Received: 30 September 2008; revised: 10 December 2008; Accepted: 19 December 2008 Electronically published: 19 December 2008

Summary The ingenious application of vinca alkaloids (vinblastine, vinorelbine, vincristine, vindesine, vinflunine) destabilizing microtubules and of taxanes (paclitaxel, docetaxel) stabilizing microtubules has been a milestone achievement in oncology. Recent investigations into their molecular mechanism revealed that all compounds possess additional pleiotropic effects that converge on induction of apoptosis in cancer cells via activation of signaling pathways. Their success has prompted vigorous investigations into microtubule-targeting activity from natural products as well as synthetic molecules arising from molecular modeling that led to the identification of Epothilones A, B, D, Ixabepilone, Sagopilone, Discodermolides, Dictyostatin, Peloruside A, and ABT-751; an additional purpose for epothilone drug discovery has been to bypass paclitaxel resistance mainly arising from the efflux function of Pglycoprotein. Nanoparticles provide a new mode of cancer drug delivery functioning as a carrier for entry through fenestrations in tumor vasculature. The 130-nm nanoparticle formulation albumin-bound paclitaxel (Nabpaclitaxel, Abraxane™) utilizes the natural properties of albumin to reversibly bind paclitaxel, transport it across the endothelial cell and concentrate in tumors; Abraxane™ received regulatory approval in the USA from a higher response rate and longer time to progression than Taxol in patients with metastatic breast cancer. The success of Abraxane™ led to an explosion in research on polymer nanoparticle formulations for taxanes using micellar PEGylated hyperbranched polyesters, polyglycerol-polyethylene glycol copolymers, cyclodextrin nanoparticles, polylactide-co-glycolide PEG and many others. Several such formulations are expected to enter the market. Other tubulin polymerization inhibitors reviewed here include tubulysin A, a highly cytotoxic peptide from myxobacteria, CC-5079, bisbenzylisoquinoline alkaloids, aplidine, nocodazole, GMC-5-193, cyclostreptin, colchicine, TLK-286 and vinflunine, a novel third generation vinca alkaloid. Structural similarities have been used to further modify the successful microtubule-targeted drugs in order to seek molecules of improved efficacy, of lower toxicity or able to overcome tumor resistance. We review the molecular mechanism of these drugs, whenever feasible, we suggest correlations between their chemical structure and mechanism and point to the importance of drug delivery for success.

estimated 6.72 million people worldwide were newly diagnosed with any the most 10 prevalent forms of solid cancers; of these, 4.15 million died within the same year.

Based on projections, the death toll will rise to 9 million cancer deaths in 2015.

I. Introduction Cancer is one of the leading causes of death worldwide; it claimed 7.6 million deaths (13.1%) in 2005 out of 58 million deaths from all causes. In 2002, an

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Boulikas and Tsogas: Microtubule-targeting anticancer drugs page Chemotherapy, surgery and radiotherapy continue to be the mainstay treatments of cancer. Over 700 FDAapproved drugs have entered into clinical practice during the last 30 years; these are classified into six major groups that include (1) the platinum coordination complex, (2) antimicrotubule agents (vinca alkaloids, taxanes), (3) antimetabolites (methotrexate, fluoropyrimidines, cytocine arabinose, gemcitabine), (4) antitumor antibiotics (actinomycin D, mitomycin C, bleomycin, anthracyclines, podofylotoxines, camptothecines), (5) alkylating agents, and (6) others including a number of biological drugs or monoclonal antibodies that target specific pathways such as EGFR or angiogenesis.

Tubulin has been an attractive anticancer target since the dawn of medical oncology because of its role in chromatid separation in mitosis and the possibility of intervention at this step of the cell cycle with agents that stabilize tubulin polymers (microtubules). Microtubules (MTs) can be viewed as dynamically unstable tubulin polymers in equilibrium with monomers that interconvert stochastically between growing and shrinking states, a property central to their cellular functions. Each time a tubulin monomer is incorporated into the polymer, one GTP molecule is hydrolyzed. The GTPase activity of tubulin is enhanced by stathmin-like domains and colchicine and is inhibited by vinblastine and by the Nterminal part of stathmin-like domains. The residues involved in GTPase activity comprise the !-tubulin GTP binding site and !-tubulin residues that participate in intermolecular interactions in protofilaments (Wang et al, 2007).

We have previously reviewed platinum drugs that have been synthesized for cancer and entered into clinical trials, including successful nanoparticle formulations (Boulikas et al, 2007). We review here the class of antimicrotubule agents.

II. Microtubules (MTs) as dynamic structures involved in spindle formation A. Microtubules and the centrosome The mitotic spindle is a specialized structure required for exact chromosome segregation in mitosis. Spindle formation is dependent on the reorganization of interphase microtubule network, regulated by cell cycle-regulatory mechanisms. The centrosome (known as the microtubule organizing center) is involved in the formation of spindle poles during mitosis, which ensures the distribution of the correct number of chromosomes to daughter cells.

Aberrant centrosome duplication could cause centrosome amplification and chromosomal instability.

In many animal cells, minus ends of microtubules are capped by the centrosome whereas plus ends are free and display dynamic instability. The role of the centrosome in microtubule dynamics was explored by studying microtubule behavior in cytoplasts from which the centrosome was removed. Fibroblast (CHO-K1) and epithelial (BSC-1) cells were investigated. Removal of the nucleus through centrifugation after cytochalasin/nocodazole treatment gave cytoplasts that either contained the centrosome and displayed a dense radial microtubule array (Figure 1, Middle pictures) or lacked the centrosome and displayed a loose and sparse network of randomly arranged microtubules (Figure 1, Right). The pattern of MT dynamics were evaluated by injecting intact cells with Cy3-tubulin, preparing cytoplasts, and acquiring digital-fluorescence time-lapse sequences of images. Living fibroblast cytoplasts containing or lacking centrosomes were readily distinguishable by the high density and radial arrangement of MTs invariably associated with the centrosome.

Figure 1.

Distribution of microtubules in intact cells and cytoplasts. Intact cells (Left) and cytoplasts containing (Center) or lacking (Right) the centrosome were fixed and triple-stained with !-tubulin antibody for microtubules (red), "-tubulin antibody for the centrosome (green, but superposition makes the spot appear yellow) and 4!,6diamidino-2-phenylindole (DAPI) for the nucleus (blue). (Upper) Fibroblast CHO cells; (Lower) epithelial BSC-1 cells. In contrast to fibroblast cells, minus ends of MTs in epithelial cells did not depend on the centrosome for their stability. (Bar = 10 #m.) From "Rodionov V, Nadezhdina E, Borisy G (1999) Proc. Natl. Acad.

Sci. USA. 96: 115-120. Copyright 1999 National Academy of Sciences, U.S.A."

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Gene Therapy and Molecular Biology Vol 12, page 315 These studies suggested that a minus-end depolymerization mechanism functioned to eliminate errors in microtubule organization and that dynamic instability of plus ends was a result of capping of minus ends by the centrosome (Rodionov et al, 1999).

Fluorescence imaging of microtubules in living cytoplasts with or without a centrosome is shown in Figure 2. In CHO cytoplasts containing the centrosome, most MTs (68%) displayed dynamic instability behavior with alternating phases of growth and shortening at their distal (plus) ends. In contrast, in cytoplasts lacking the centrosome, dynamic instability was never observed. In contrast to fibroblast cells, minus ends of MTs in epithelial cells did not depend on the centrosome for their stability.

membrane as 2!,3!-cyclic nucleotide-3!-phosphodiesterase (CNP). The CNP is both prenylated and palmitoylated, providing hydrophobic domains for membrane intercalation. The association of CNP and tubulin in membrane and cytoskeletal compartments was shown with immunofluorescence. Fluorescent labeling of microtubules (green) and CNP (red) of FRTL-5 cells revealed patches of colocalization (yellow) of the two proteins at the membrane and subplasmalemmal region. The patches are interrupted by zones, containing only CNP. Microtubules extending toward the membrane show no association with CNP, but the perinuclear region again shows abundant overlap of the two proteins. Thus, CNP acts as a microtubule-associated protein and this activity resides in the C terminus of the enzyme. Submembranous colocalization of the proteins and CNP-dependent microtubule organization (Figure 3) suggest that CNP is a membrane-bound microtubule-associated protein that can link tubulin to membranes and may regulate cytoplasmic microtubule distribution (Bifulco et al, 2002).

B. Association of tubulin with plasma membrane The bulk of cellular tubulin is cytoplasmic, but a significant fraction is embedded in, or firmly associated with, the plasma membrane and other membranes. A possible linker protein for microtubules to the plasma

Figure 2. Fluorescence imaging of microtubules in living cytoplasts. In centrosome containing cytoplasts (Top), microtubules (MTs) showed dynamic instability at their plus ends whereas free MTs rapidly shortened from their minus ends. In centrosome-free cytoplasts (Middle), MTs persistently grew at one end and shortened at the other end. Injection of tubulin at low concentration resulted in nonuniform incorporation of subunits along MTs and produced â&#x20AC;&#x153;specklesâ&#x20AC;? along their length. Speckles remained stationary, indicating that the mechanism of translocation was treadmilling (Bottom). Black arrowheads point to shortening and white arrowheads to growing ends. White arrows point to speckles. Numbers indicate time in seconds. (Bars = 1 #m). From "Rodionov V, Nadezhdina E, Borisy G (1999) Proc. Natl. Acad. Sci. USA. 96: 115-120. Copyright 1999 National Academy of Sciences, U.S.A."

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Figure 3. Colocalization of tubulin and CNP in FRTL-5 rat thyroid cells. Cells were grown on coverslips, fixed, and stained with a monoclonal anti-!-tubulin antibody [fluorescein (a)] or an antibody to CNP1 [rhodamine (b)]. (c) Double immunofluorescence (superimposition of a and b staining). (d) Enlarged membrane region from c. (e) Overlap of CNP and tubulin in a cytoskeleton prepared from a COS cell. Cells were fixed and incubated with monoclonal anti-!-tubulin antibody (Amersham Pharmacia) for 1 h, followed by tetramethylrhodamine isothiocyanate (TRITC)-labeled goat anti-mouse IgG (Sigma) for 1 h. Secondary antibodies for tubulin were either fluorescein- or rhodamine-labeled. From "Bifulco M, Laezza C, Stingo S, Wolff J (2002) Proc. Natl. Acad. Sci. U S A. 99: 18071812, Copyright 2002 National Academy of Sciences, U.S.A."

C. Tumor suppressor proteins are localized in centrosomes

transition, and a complex with Rad51 is associated with chromosomes during S phase and participates in DNA repair. BRCA1 is a component of RNA polymerase II and a coactivator of p53-mediated transcription, and may thus regulate the expression of other genes required for cell cycle progression.

BRCA1 was associated with the centrosome during mitosis. This was shown by coimmunostaining of COS-7 cells with mouse monoclonal "-tubulin antibody and rabbit polyclonal BRCA1 antibody (Figure 4). Two BRCA1specific antibodies were used: MS110, a mouse mAb raised against a BRCA1-GST fusion protein containing amino acids 1-304 of human BRCA1 protein, and C-20, a rabbit polyclonal antibody raised against a peptide corresponding to amino acids 1843-1862 of human BRCA1. A series of double-staining experiments have confirmed the localization of BRCA1 protein at mitotic centrosomes using C-20 and MS110 for BRCA1 staining, "-tubulin and pericentrin antibodies for centrosome staining, and "-tubulin antibody for microtubule staining.

In addition, DAPI staining of DNA was used to locate the nucleus. Double-staining of COS-7 cells with "-tubulin antibody and BRCA1 C-20 antibody provided direct evidence for the presence of BRCA1 protein at mitotic centrosomes. Two-color (BRCA1+"-tubulin) or threecolor (BRCA1+"-tubulin+DAPI) composite images showed colocalization of the BRCA1 and "-tubulin signals at mitotic centrosomes (Figure 4). The concentration of BRCA1 signal at mitotic centrosomes was apparent from prometaphase to metaphase (Figure 4A) and early anaphase (Figure 4B). BRCA1 staining diminished at the centrosome as cells proceeded to late anaphase (Figure 4C). Results were similar when COS-7 cells were

The centrosome controls assembly of microtubules, a process that plays a central role in organizing cell structure, determining cell polarity, directing cell movement during interphase, and orchestrating formation of the bipolar spindle during mitosis. Furthermore, centrosomes play an important role in maintaining the fidelity of chromosome distribution during cell division.

Loss of these functions might cause chromosomal instability and aneuploidy. Centrosome amplification drives chromosomal instability in tumor development.

Tumor suppressor proteins such as p53 and retinoblastoma (RB) have been localized to the centrosome in a cell cycle-dependent manner. A number of proteins involved in the G2/M checkpoint were also found to be associated with centrosomes during cell cycling, e.g., cyclin B, p34cdc2, and 14-3-3. Poly(ADPribose) polymerase 1 involved in opening up chromatin for DNA repair and transcription and able to bind to DNA strand breaks was also found to be localized to the centrosomes during mitosis and was suggested to be involved in maintenance of chromosomal stability (Kanai et al, 2007).

BRCA1, a suppressor of tumorigenesis in breast and ovary, is a protein of 1,863 amino acids with an Nterminal zinc-ring domain, a C-terminal transactivation domain and two putative nuclear localization signals.

BRCA1 is involved in progression of the cell cycle. Its expression and phosphorylation are cell cycle dependent and its overexpression induces growth arrest or apoptosis.

BRCA1 plays a continuous role throughout the cell cycle: expression and phosphorylation is induced at G1/S 316

Gene Therapy and Molecular Biology Vol 12, page 317 costained with the MS110 BRCA1-specific antibody (Figure 5) (Hsu and White, 1998).

A hypophosphorylated form of BRCA1, a suppressor of tumorigenesis in breast and ovary, localized with the centrosome during mitosis and coimmunoprecipitated with "-tubulin, a centrosomal component essential for nucleation of microtubules (Figure 5).

Immunofluorescence staining of a population of replicating COS-7 cells revealed the usual dot pattern in the nucleus. However, a unique staining pattern reminiscent of centrosomes was observed in mitotic cells.

These data suggested that BRCA1 also plays a functional role with mitotic centrosomes (Hsu and White, 1998).

The cellular targets for estramustine, an antitumor drug used in the treatment of hormone-refractory prostate cancer, are believed to be the spindle microtubules responsible for chromosome separation at mitosis. Video microscopy showed that estramustine strongly stabilized growing and shortening dynamics at plus ends of bovine brain microtubules devoid of microtubule-associated proteins. The combined suppressive effects of vinblastine and estramustine on the rate and extent of shortening and dynamicity were additive. Thus, like the antimitotic mechanisms of action of the antitumor drugs vinblastine and taxol, the antimitotic mechanism of action of estramustine may be due to kinetic stabilization of spindle microtubule dynamics (Panda et al, 1997).

D. Microtubule-associated proteins A number of microtubule-associated proteins have been reported; CLIPs are proteins known to associate specifically with the ends of growing microtubules, and CLASPs colocalize with CLIPs at the microtubule plus distal ends. CLASP1 localizes near the plus ends of growing spindle microtubules and is required for attachment of microtubules to kinetochore. hOrbit1 plays a role in polymerization of tubulin and interaction between microtubules (Figure 6) (Aonuma et al, 2005). Time-lapse fluorescence microscopy demonstrated that noncentrosomal MTs in cultured epithelial cells arise primarily by constitutive nucleation at, and release from, the centrosome. After release, MTs moved away from the centrosome and tended to depolymerizes (Keating et al, 1997). Aurora B is a protein kinase and a chromosomal passenger protein that undergoes dynamic redistribution during mitosis. Aurora B was found at centromeres at prophase but redistributed to the spindle midzone and became concentrated at the equator along midzone microtubules. Depolymerization of microtubules inhibited the dissociation of aurora B from centromeres at early anaphase and caused the dispersion of aurora B from the spindle midzone at late anaphase (Murata-Hori et al, 2002).

Figure 4. Coimmunostaining of COS-7 cells with mouse monoclonal "-tubulin antibody and rabbit polyclonal BRCA1 antibody C-20.

(A) a prometaphase to metaphase cell; (B) an early anaphase cell, and (C) a late anaphase cell. The colocalized signals of BRCA1 and "tubulin are yellow. DAPI counterstained DNA. Arrows indicate the positions of centrosomes. From "Hsu LC, White RL (1998) Proc.

Natl. Acad. Sci. U S A. 95: 12983-12988, Copyright 1998 National Academy of Sciences, U.S.A."

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Figure 5. COS-7 and E6/BE46 cells were costained with mouse monoclonal BRCA1 antibody MS110 (a) and rabbit polyclonal pericentrin antibody 4B (b); with MS110 (d) and rabbit polyclonal BRCA1 antibody C-20 (e); with mouse monoclonal "-tubulin antibody (g) and C-20 (h); or with mouse monoclonal !-tubulin antibody (j) and C-20 (k). c, f, i, and l include DAPI counterstain of DNA. a-f highlight mitotic COS-7 cells; g-i are interphase COS-7 cells; j-l illustrate a mitotic E6/BE46 cell. Arrows indicate the positions of centrosomes. From "Hsu LC, White RL (1998) Proc. Natl. Acad. Sci. U S A. 95: 12983-12988, Copyright 1998 National Academy of Sciences, U.S.A."

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Figure 6. Localization of GFP-hOrbit1 NF (GFP-hOrbit1 N-terminal fragment) and microtubules. (A-D) Immunofluorescent images of GFP-hOrbit1 NF expression cell. Cells were cultured for 16 h after transfection. Microtubules immunostained with anti-!-tubulin antibody, and DNA stained with DAPI. GFP-hOrbit1 NF image (A), microtubule image (B) and DNA image (C) were merged (D). In the merged image, the yellow color indicates colocalization of GFP-hOrbit1 NF and microtubules. (E) Immunofluorescent images of control cells. The cells without GFP-hOrbit1 NF transfection were immunostained with anti-!-tubulin antibody, and DNA was stained with DAPI. Microtubule image (red) and DNA image (blue) were overlaid. Bar represents 10 #m. From: Aonuma M, Miyamoto M, Inoue YH, Tamai K, Sakai H, Kamasawa N, Matsukage A (2005) Cell Struct Funct. 30: 7-13, with kind permission from the Japanese Society for Cell Biology

The orbit encodes Orbit/Mast, a 165-kDa microtubuleassociated protein (MAP) with GTP-binding motifs; hypomorphic mutations in the Drosophila orbit gene cause abnormal chromosome segregation (Aonuma et al, 2005).

Two human homologues of the Orbit/Mast, CLASP1 (hOrbit1) and CLASP2 (hOrbit2) have been identified.

Using an antibody, the 150 kDa CLASP1/hOrbit1 polypeptide was found to be associated with microtubules.

Figure 6 shows the subcellular localization of GFPhOrbit1 after trasfection of cells with a plasmid expressing a fusion protein of the putative microtubule-binding domain (1-662 out of 1289 residues) of hOrbit1 with GFP. Confocal laser scanning microscopic observation revealed that the GFP-fluorescence associated with short and thin filaments in the perinuclear region during the short period after plasmid transfection, and colocalized with only part of the microtubules. GFP fluorescence was later detected on the abnormally longer and thick bundles of microtubule filaments. Finally the bundles formed networks in the perinuclear region. The results suggest that the GFPhOrbit1 N-terminal fragment (GFP-hOrbit1 NF) binds to the newly formed microtubules rather than the pre-formed ones (Aonuma et al, 2005).

III. Taxanes When taxanes (paclitaxel, docetaxel) were introduced as anticancer agents some 20 years ago, their broad spectrum of activity was striking. Taxanes were shown to be microtubule-targeting agents, able to stabilize tubulin polymers but also to disrupt additional cellular processes and to induce apoptosis (reviewed by Rowinsky and Calvo, 2006). A plethora of clinical trials was set to optimize the different ways drugs can be administered; for example, the addition of cisplatin or carboplatin to paclitaxel resulted in higher response rates than for each of the drugs as single agents (reviewed by Ranson and Thatcher, 1999).

Antimicrotubule agents appear to act also by induction of apoptosis by convergence of several signaling pathways ending with caspase activation and chromatin fragmentation. A functional p53 protein and expression of the apoptosis-promoting protein, bax are the most studied pathways for drug-induced apoptosis. Necrosis can be assessed by Annexin binding and propidium iodide permeability in aqueous medium (Serafin and Bohm, 2005).

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Boulikas and Tsogas: Microtubule-targeting anticancer drugs page undergo apoptosis, suggesting that phosphorylation of Bcl2 may inhibit Bcl2 function. In addition, Bcl2 phosphorylation appears to inhibit its binding to Bax, since less Bax was observed in an immunocomplex with Bcl2 in taxol-treated cancer cells. Overexpression of Bcl2 counteracts the apoptotic effects of low doses of paclitaxel but has no effect against high doses. Furthermore, microtubule-damaging drugs such as paclitaxel induced apoptosis, caused growth arrest in G2/M phase of the cell cycle, induced caspase 3 activation as well as poly(ADPribose) polymerase (PARP) degradation, but did not induce p53 (Srivastana et al, 1998).

A model showing the binding of Taxol with tubulin is shown in Figure 8.

Incubation of cells with high Taxol concentrations leads to the formation of stable bundles of microtubules that disrupt the normal polymerization/depolymerization cycle of microtubules and results in the arrest of cells in the G2/M phase of the cell cycle. In addition to massive bundle formation, increased microtubule polymer mass is observed after treatment with high concentrations of Taxol. However, low concentrations of Taxol (10 nM) inhibit mitosis in HeLa cells by suppressing microtubule dynamics rather than by altering the microtubule polymer mass or inducing bundle formation. The mitotic block induced by 10 nM Taxol is sufficient to induce apoptosis.

These observations in HeLa cells indicate that Taxolinduced cell death may result from different mechanisms depending on drug concentration. Taxol alters specific intracellular signal transduction events. It has been reported that Taxol induces the production of cytokines, interleukin-1, and tumor necrosis factor ! (TNF-!) and increases tyrosine phosphorylation of proteins, including mitogen-activated protein kinase. Prolonged exposure of cells to Taxol induces DNA fragmentation, characteristic of apoptotic cell death, and it has been suggested that Raf1 is a mediator of Taxol-induced apoptosis.

A. Paclitaxel Paclitaxel (Taxol, Onxol) is a naturally occurring taxane molecule that inhibits depolymerization of tubulin in the spindle apparatus thus inducing apoptosis in dividing cells. It is FDA approved for salvage therapy in ovarian cancer and in both metastatic and adjuvant setting in breast cancer. It is also used in lung, head and neck and bladder cancers. Figure 7 shows its chemical structure and with its differentiating features from docetaxel marked in red.

B. Docetaxel Docetaxel (Taxotere, Sanofi) is a semisynthetic taxane, from a class of compounds that inhibit the mitotic spindle apparatus by stabilizing tubulin polymers, leading to death of mitotic cells. FDA has approved it for metastatic breast cancer and first and second line treatment for non-small cell lung cancer. However, clinical experience is increasing in ovarian cancer, prostate cancer, stomach cancer and other epithelial neoplasms and it is likely to get approvals for additional indications.

C. Molecular mechanism of taxanes The mechanism of action of taxanes against tumor cells is by alteration of microtubule dynamics, which causes cell-cycle arrest during mitosis. Docetaxel binds to the microtubules with a higher affinity than paclitaxel, and over a broader range of cell-cycle activities. It has also been shown to promote apoptosis via Bcl2 phosphorylation.

Recently, it has been shown that Bcl2 may protect cancer cells from apoptosis induced by a variety of anticancer agents. The precise mechanism of the Bcl2induced multi-drug resistance is unknown. Microtubulestabilizing agents such as paclitaxel and docetaxel have antimitotic and apoptosis-inducing activity. Human leukemic, breast cancer, and prostate cancer cells exposed to paclitaxel express a phosphorylated form of Bcl2 and

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Figure 7. Structure of Paclitaxel and Docetaxel; their differentiating features are marked in red.

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Figure 8. Taxol binding site on mammalian $-tubulin. The location of residues Lys-19, Val-23, Asp-26, His-227, and Phe-270 are indicated and are shown in dark gray. Labels on Taxol (gray) denote the following: I, C3! phenyl ring; II, C3! benzamido phenyl ring; and III, C2 benzoyl phenyl ring. Specific regions of $-tubulin that form the binding pocket are labeled, including !-helices H1, H7, H9, and H10, the $-strands B7-B10, and the B7-H9 M-loop. From "Gupta, Jr. LM, Bode CJ, Georg, GI, Himes RH (2003) Proc. Natl. Acad.

Sci. USA 100: 6394â&#x20AC;&#x201C;6397, Copyright 2003 National Academy of Sciences, U.S.A."

Raf-1 is known as an important intermediate in the transmission of proliferative and developmental signals, connecting upstream tyrosine kinases with downstream serine/threonine kinases. It is not clear whether Raf-1 activation is a consequence of disruption of the normal microtubule cytoskeleton and/or of activating the spindle mitotic checkpoint (Torres and Horwitz, 1998).

Paclitaxel is known to induce a proinflammatory response in macrophages; combination therapy with trastuzumab and paclitaxel for inflammatory local recurrence after breast conserving surgery has been suggested as a treatment of choice (Nomura et al, 2005).

Paclitaxel might have a role in inhibiting angiogenesis and vascularization (Shnyder et al, 2005).

In hormone-refractory prostate cancer, docetaxel has been studied as both a single agent and in combination with estramustine, and in different treatment schedules, with demonstrated efficacy. Two phase III trials have confirmed a survival benefit, making docetaxel the first chemotherapy agent with proven efficacy against prostate cancer (Mackler and Pienta, 2005).

In urothelial cancer, docetaxel has demonstrated activity and has been investigated as a single agent and in combination regimens. A phase III trial comparing docetaxel and cisplatin to methotrexate, vinblastine, doxorubicin, and cisplatin was inferior when evaluating response rates and overall survival. More recent phase II trials combining docetaxel with two additional agents have shown promise, but confirmatory trials are needed (Mackler and Pienta, 2005).

D. Indications of taxanes Paclitaxel is indicated as first-line treatment for advanced ovarian carcinoma in combination with cisplatin; as first-line treatment of Non Small Cell Lung Cancer (NSCLC, stages IIIb and IV) in combination with cisplatin; for the adjuvant treatment of node-positive breast cancer administered sequentially to standard doxorubicin-containing combination; for the treatment of breast cancer after failure of combination chemotherapy for metastatic disease or relapse within 6 months of adjuvant chemotherapy; and for the second-line treatment of AIDS-related Kaposi's sarcoma.

E. Side effects of taxanes The dose limiting effect of paclitaxel is myelosuppression (mostly neutropenia) that can be reduced with shorter infusions of the same dose. Other common side effects are mucositis (especially after longer infusions), peripheral neuropathy (that increases with cumulative dose), acute neuromyopathy (that occurs for several days after infusion and could require opiate analgesics in order to control pain), cardiovascular side effects, including hypertension, hypotension, premature contractions, bradyarrhythmias and hypersensitivity

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Boulikas and Tsogas: Microtubule-targeting anticancer drugs page reactions to the drug including chest pain, dyspnea, urticaria, wheezing, hypotension (that can be reduced by premedication with corticosteroids and H1, H2 histamine receptor blockers). Alopecia is one of the expected side effects, whereas nausea, vomiting, diarrhea, liver toxicity and interstitial pneumonitis are uncommon (Saville et al, 1995; Blum et al, 2006; Langer et al, 2007).

The severe side effects of docetaxel include myelotoxicity, allergic reactions during infusion, diarrhea that can be severe in some patients, nausea and/or vomiting, hair loss occurring in most patients (including the hair on head, underarm hair, pubic hair, eyebrows, and eyelashes), fatigue in about 10% of patients, and muscle pain that is rarely severe in about 20% of the infusions.

Rash occurs commonly but is severe in about 5% of patients. About half of patients feel numbness, tingling, or burning sensations in their hands and feet.

Myelosuppression and alopecia are universal side effects of docetaxel with myelosuppression being the dose limiting effect. Edema and fluid accumulation, including pleural effusions and ascites are common and can be dose limiting. Fluid accumulation can be partially prevented with corticosteroid treatment before and after each cycle of docetaxel. Mild sensory or sensorimotor neuropathy is common. Mucositis and diarrhea are common and usually mild. Hypersensitivity reactions are uncommon and can be prevented through premedication with corticosteroids and antihistamines. Rash and elevated liver function tests are uncommon (Baker et al, 2004; Georgoulias et al, 2005).

Taxanes require pre-medication and may cause important side effects such as febrile neutropenia and neuropathy. Neuropathy is a major adverse effect of microtubule-stabilizing agent-based chemotherapy, with severe peripheral neuropathy (grade 3 or 4) occurring in as many as 30% of patients treated. Neuropathy usually presents as sensory neuropathy and is more common with paclitaxel than docetaxel; it depends on the drug dose per treatment cycle, the schedule of treatment, and the duration of the infusion (reviewed by Lee and Swain, 2006).

(Figure 9). However, mutations in !-tubulin are also linked to resistance to taxanes but not epothilones in vitro (Pusztai, 2007). Resistance against paclitaxel also correlates with an increase in the relative abundance of tubulin isoform !III; the mode of recognition and the mechanism of stabilization of paclitaxel with the type I and III isoforms of !-tubulin are different; no preference for any of the two isoforms can be detected for epothilone A known to bypass paclitaxel resistance (Magnani et al, 2006).

F. Taxane drug resistance The majority of initially responsive breast cancer patients treated with taxanes eventually develop resistance to taxanes (acquired resistance) and a non-negligible percentage of patients are primarily resistant to these agents (de novo resistance). Taxane drug resistance is caused by the drug efflux pump protein, P-glycoprotein. Pglycoprotein, produced by the multidrug resistance-1 gene (mdr-1), is a main mechanism developed by cancer cells to guard against anticancer drugs. Alterations of DNA methylation of the mdr-1 gene promoter are known to be linked to mdr-1 gene expression and are probably related to intracellular S-adenosyl-methionine.

Overexpression of P-glycoprotein is associated with resistance to taxanes, but not ixabepilone, in vitro.

Obviously, different functional groups on the paclitaxel (or docetaxel) molecules are involved in tubulin binding and in interaction with P-glycoprotein; the similarity in molecular structures between taxanes on one hand and epothilones in the other is shown by molecular modeling

Figure 9. Structural similarities between paclitaxel and epothilone B. Paclitaxel structure is shown in grey and epothilone B is superimposed in yellow (A), while in (B) Paclitaxel is the yellow structure and epothilone B is the grey.

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Gene Therapy and Molecular Biology Vol 12, page 323 Preclinical xenograft studies comparing ABI-007 and Taxol showed that both caused tumor regression and prolonged survival in various tumors; the order of sensitivity was lung > breast congruent with ovary > prostate > colon. The LD50 and Maximum Tolerated Dose (MTD) for ABI-007 were 47 and 30 mg/kg/d and for Taxol were 30 and 13.4 mg/kg/d, respectively. At equitoxic dose, the ABI-007-treated groups showed more regressions and prolonged survival supposedly from a higher intratumoral accumulation of ABI-007; finally ABI-007 exhibited enhanced endothelial cell binding and transcytosis compared to Taxol (Desai et al, 2006).

G. Mechanisms of taxane drug resistance One mechanism of resistance to taxanes involves mutations, especially L and V substitutions at proline 220 of !-tubulin. Indeed, expression of tubulin containing the P220L and P220V mutations from expression vectors reduced microtubule assembly, conferred resistance to paclitaxel and epothilone A (microtubule-stabilizing drugs), but increased sensitivity to colcemid and vinblastine (microtubule-destabilizing drugs).

An important aspect of these studies is that different substitutions at the same amino acid residue in !1-tubulin can confer cellular resistance to either microtubulestabilizing or microtubule-destabilizing drugs (Yin et al, 2007). Additional mutations involved in resistance to paclitaxel are the L215, L217, and L228 in the H6/H7 loop region of !1-tubulin as shown in Chinese hamster ovary cells selected in the presence of paclitaxel.

A. Dose-limiting toxicity (DLT) of Abraxane Clinical studies have shown that nab-paclitaxel has almost double the response than paclitaxel formulated as Cremophor EL (Taxol) with an increased time to disease progression and increased survival in second-line patients.

Nab-paclitaxel showed a lower rate of severe neutropenia compared to Taxol. Also the combination of ABI-007 and carboplatin may have significant activity in a variety of tumor types including non-small and small cell lung cancer, ovarian cancer, and breast cancer. However, lifethreatening toxicities with metastatic breast cancer and hepatic insufficiency have been observed (Lee Villano et al, 2006).

In a Phase I study ABI-007 was administered in three different schedules in combination with carboplatin at AUC of 6 on day 1. Myelosuppression was the primary dose limiting toxicity. Responses were seen in melanoma, lung, bladder, esophageal, pancreatic, breast cancer, and cancer of unknown primary among 41 patients. The MTD of ABI-007 was 300 mg/m2 administered on day 1 every 21 days; 100 mg/m2 administered on days 1, 8, and 15 every 28 days; and 125 mg/m2 administered on days 1 and 8 every 21 days (Stinchcombe et al, 2007). In a different Phase I dose-escalating study the dose-limiting toxicity (DLT), which occurred in 3 of 6 patients treated at level 3 (375 mg/m2), consisted of sensory neuropathy (3 patients), stomatitis (2 patients), and superficial keratopathy (2 patients). The MTD was thus determined to be 300 mg/m2 (level 2). Identified features of clinical interest of ABI007, included rapid infusion rate, absence of requirement for steroid premedication, and a high paclitaxel MTD (Ibrahim et al, 2002).

IV. Nab-paclitaxel (ABI-007, Abraxane) Taxane delivery systems through tumor cell surface receptor-targeted delivery mechanisms such as smallmolecule peptides and monoclonal antibodies, as well as those on non-targeted procedures such as liposomes, nanostructures, and natural and synthetic polymers hold promise for improving the toxicity profiles and biodistribution of the drug.

Albumin is emerging as a versatile protein carrier for drug targeting and for improving the pharmacokinetic profile of peptide or protein-based drugs. Nab-paclitaxel (ABI-007, Abraxane) is a novel albumin-bound (nab) paclitaxel formulated into 130-nm particles. This differs from the more conventional formulation of Taxol, which uses cremophor (castor oil) to increase the solubility of paclitaxel and is responsible for side effects, especially neutropenia and peripheral neuropathy. Abraxane utilizes the natural properties of albumin to reversibly bind paclitaxel, transport it across the endothelial cell and concentrate it in tumors. The proposed mechanism involves an endothelial cell-surface albumin receptor (gp60) and an albumin-binding protein expressed by tumor cells and secreted into the tumor interstitium (secreted protein, acidic and rich in cysteine, SPARC). Thus, glycoprotein 60-mediated endothelial cell transcytosis of the albumin nanoparticles and tumor accumulation by binding to SPARC enhances the therapeutic efficacy of ABI-007 compared to the free drug. The albumin receptormediated paclitaxel-transport mechanism is analogous to the opening of a 'trapdoor' on the endothelial cell wall within blood vessels. This facilitates the passage of ABI 007 from the bloodstream via the blood vessels to the underlying tumor tissue (reviewed by Moreno-Aspitia and Perez, 2005; Gradishar, 2006).

Studies in rats have shown that ABI-007 differs from paclitaxel formulated as Taxol, with a higher plasma clearance and a larger volume of distribution. The same study also showed that fecal excretion was the main elimination pathway with both formulations (Sparreboom et al, 2005).

B. Maximum tolerated dose (MTD) of Abraxane In a Phase I study the MTDs for heavily and lightly pretreated patients were 100 and 150 mg/m2, respectively; and the dose-limiting toxicities were grade 4 neutropenia and grade 3 peripheral neuropathy, respectively (Nyman et al, 2005).

An interim analysis from a more recent randomized Phase II trial suggested that weekly nab-paclitaxel was more effective and safer than either 3-weekly nabpaclitaxel or 3-weekly docetaxel. The superior efficacy of nab-paclitaxel was presumably due to the improved safety profile, which allows for the administration of higher doses, a greater proportion of which actually reaches the tumor (reviewed by Henderson and Bhatia, 2007).

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Boulikas and Tsogas: Microtubule-targeting anticancer drugs page Additional studies include a phase II trial of ABI 007 in metastatic breast cancer patients who have failed taxane therapy evaluating a weekly rather than 3-weekly regimen and a multicentre phase II trial in patients with metastatic melanoma to evaluate both chemotherapy-naive patients (at a dose of 150 mg/m2 administered weekly) and to pretreated patients (at a dose of 100 mg/m2 administered weekly). ABI 007 is also being evaluated for the treatment of NSCLC, ovarian and cervical cancers.

American Pharmaceutical Partners (APP) secured exclusive North American marketing and manufacturing rights to ABI 007 in November 2001 and formed Abraxis Oncology for marketing purposes; APP is the owner of the US patent No. 6,506,405, which has 89 claims covering compositions of matter and unit dosage forms and patent No. 5,780,653 which covers three next-generation taxane anticancer compounds. In addition, the patent covers methods of use without the requirement for pretreatment with steroid therapy or growth factor support. The US FDA granted fast-track status to ABI 007 for metastatic breast cancer in January 2003. In September 2003, APP and American BioScience jointly announced positive interim results from the trial, which shows that the primary efficacy objective had been exceeded. Enrollment was completed in December 2002 with 460 first- and secondline metastatic breast cancer patients enrolled. A Data Monitoring Committee concluded in October 2002 that a sample-size adjustment of the phase III trial was not required and that the study could be continued to completion.

C. Clinical development of Abraxane A multicenter phase II study was designed to evaluate the efficacy and safety of Abraxane 260 mg/m2 without premedication every 3 weeks in NSCLC patients; ORR was 16%; the disease control rate (ORR plus stable disease) was 49% and the 1-year survival was 45%. Side effects included neuropathy, fatigue but no severe hypersensitivity reactions and no grade 4 treatment-related toxicity (Green et al, 2006).

Paclitaxel albumin-bound particles improved outcomes when compared against single agent cremophorbased paclitaxel; addition of bevacizumab (10 mg/kg), gemcitabine (1000 mg/m2) or both agents to abraxane (100mg/m2) also improved outcomes in clinical trials with manageable peripheral neuropathy and thrombocytopenia (Lobo et al, 2007).

A multicenter phase II study in MBC on 63 women at the M.D. Anderson Cancer Center, Houston was the prelude of the pivotal Phase III trial. ABI-007 at 300 mg/m2 was given to previously-treated or chemonaive patients. The overall response rates was 48% but for the group of patients who received ABI-007 as first-line treatment, the response rate was 64% and for the group of patients who received ABI-007 as second- or third-line treatment the response rate was 21%. Toxicities observed were typical of paclitaxel and included grade 4 neutropenia (24%), grade 3 sensory neuropathy (11%), and grade 4 febrile neutropenia (5%). Median time to disease progression was 26.6 weeks, and median survival was 63.6 weeks (Ibrahim et al, 2005).

In a randomized trial that formed the basis of its regulatory approval in the USA, 3-weekly nab-paclitaxel induced a higher response rate and longer time to progression than Taxol in patients with metastatic breast cancer. Except for grade 3 sensory neuropathy, nabpaclitaxel was also safer. The pivotal phase III study was performed to confirm preclinical studies demonstrating superior efficacy and reduced toxicity of ABI-007 compared with standard paclitaxel. ABI-007 at 260 mg/m2 was given intravenously without corticosteroid premedication compared to 175 mg/m2 Taxol with premedication both in 3-week cycles and demonstrated significantly higher response rates compared with standard paclitaxel (33% versus 19%, respectively) and significantly longer time to tumor progression (23.0 v 16.9 weeks, respectively). The incidence of grade 4 neutropenia was significantly lower for ABI-007 compared with Taxol (9% v 22%, respectively). Grade 3 sensory neuropathy was more common in the ABI-007 arm than in the standard paclitaxel arm (10% v 2%, respectively) (Gradishar et al, 2005).

D. Targeting to tumors in animals Tumor-homing peptides were used to target abraxane to tumors in mice. The targeting was accomplished with two peptides, CREKA and LyP-1 (CGNKRTRGC). The CREKA pentapeptide binds to clotted plasma proteins and homes to tumors because interstitial tissue of tumors and the vessel walls contain clotted plasma proteins, whereas the vessels in normal tissues do not. Fluorescein (FAM)labeled CREKA-abraxane, injected intravenously into mice bearing human cancer xenografts, accumulated in tumor blood vessels, forming aggregates that contained red blood cells and fibrin. FAM-LyP-1-abraxane colocalized with extravascular islands expressing its receptor, p32. Untargeted FAM-abraxane was detected in the form of a faint meshwork in tumor interstitium. LyP-1abraxane produced a statistically highly significant inhibition of tumor growth compared with untargeted abraxane in the xenografts (Karmali et al, 2008).

V. Epothilones Epothilones are 16-membered ring macrolides with antimicrotubule activity that have a mechanism of action similar enough to the taxanes to retain their broad spectrum of activity, but different enough to escape the multidrug resistance caused by P-glycoprotein. These properties are especially promising for patients with metastatic breast cancer who have run out of therapeutic options as a result of multidrug resistance. Due to improved water solubility, cremophors (solubilizing agents used in paclitaxel which can affect cardiac function and cause severe hypersensitivity) are no longer needed in the formulation of epothilones.

Two major compounds, epothilone A and epothilone B, were originally identified as secondary metabolites produced by the soil-dwelling myxobacterium Sorangium cellulosum endowed with selective antifungal activity and strong cytotoxic activity against cancer cell lines (reviewed by Reichenbach and Hรถfle, 2008). Optimization of the production of extracellular epothilone B using 3% 324

Gene Therapy and Molecular Biology Vol 12, page 325 calcium alginate carrier for immobilization of Sorangium cellulosum has been described able to produce 5.03 mg/l/day (Park et al, 2007). Additional anticancer substances appear to be present in Sorangium cellulosum strains isolated in China (Guo et al, 2007). Epothilones are potential anticancer drugs that stabilize microtubules by binding to tubulin in a manner similar to paclitaxel.

Cytochrome P450epoK (P450epoK), a heme containing monooxygenase involved in epothilone biosynthesis in the myxobacterium Sorangium cellulosum, catalyzes the epoxidation of epothilones C and D into epothilones A and B, respectively.

Hodgkin's lymphoma in phase II studies. Response rates in taxane-refractory metastatic breast cancer are relatively modest; however, ixabepilone and patupilone have shown promising efficacy in hormone-refractory metastatic prostate cancer and in taxane-refractory ovarian cancer (reviewed by Larkin and Kaye, 2006).

C. Mechanism of action of epothilones Like taxol, epothilone B binds to the !$-tubulin heterodimer subunit. Once bound, the rate of !$-tubulin dissociation decreases, thus stabilizing the microtubules.

Furthermore, epothilone B has also been shown to induce tubulin polymerization into microtubules without the presence of GTP. This is caused by formation of microtubule bundles throughout the cytoplasm. Finally, epothilone B also causes cell cycle arrest at the G2/M transition phase, thus leading to cytotoxicity and eventually cell apoptosis (Balog et al, 1996).

Epothilone B and D enhanced the constitutional activation of nuclear factor-#B (NF-#B) via I#B degradation through I#B kinase (IKK! and IKK!) activation, and this resulted in p50 and p65 translocation to the nucleus in SW620 colon cancer cells. Moreover, epothilone B and D increased the expressions Bax, p53, caspase-3, but reduced Bcl-2 expression. Cells treated with sodium salicylate, an IKK inhibitor, did not show epothilone-induced cell growth inhibition or p50 translocation. These studies have unraveled additional mechanisms of epothilone-induced apoptosis in a tubulin polymerization-independent manner (Lee et al, 2007).

A. Epothilone drug discovery Epothilones are anticancer agents with a taxane-like mechanism of action that have demonstrated activity in taxane-resistant tumors. Marine invertebrate animals such as sponges, gorgonians, tunicates and bryozoans are under intense investigation as sources of medicinal natural products.

Non-taxane microtubule-stabilizers of diverse chemical structures, including the epothilones and discodermolide have been advanced in chemical synthesis and been promoted to clinical trials (reviewed by Cardoso et al, 2008). Non-taxane microtubule-stabilizers of diverse chemical structures show promising preclinical activities and several are progressing through clinical trials (Mooberry, 2007).

The structural diversity of the epothilone group of clinical compounds is rather limited, as their structures show little divergence from the original natural product leads. A series of epothilone-derived macrolactones were elaborated to discover improved versions some of which had potent antiproliferative activities, promoted tubulin polymerization and induced mitotic arrest; changes were at the natural epoxide geometry from cis to trans, the incorporation of a conformationally constrained side chain, the removal of the C3-hydroxyl group, and the replacement of C12 with nitrogen. Interesting from many points of view appeared to be the 12-aza-epothilone ("azathilone" 40) especially because it lies outside of the general scope of Nature's biosynthetic machinery for polyketide synthesis but nevertheless retains most of the overall structural characteristics of a true natural product (Feyen et al, 2008).

D. Epothilone B (patupilone; EPO960) Patupilone (Figure 10) is a novel tubulinpolymerizing agent with activity against paclitaxelresistant cell lines. Patients with refractory solid tumors received fixed doses of gemcitabine (1,000 or 750 mg/m2) along with escalating doses of patupilone (1.5-3 mg/m2) on days 1 and 8 of a 21-day cycle. The recommended phase II dose was gemcitabine 750 mg/m2 and patupilone 1.5 mg/m2 on days 1 and 8 of a 21-day cycle. DLTs were grade 3 asthenia and grade 3 dehydration but also asthenia and persistent nausea were observed (Schelman et al, 2008).

The principal mechanism of the epothilone class is inhibition of microtubule function (Goodin et al, 2004).

Microtubules are essential to cell division, and epothilones therefore stop cells from properly dividing. Epothilone B possesses the same biological effects as taxol both in vitro and in cultured cells. This is due to the fact that they share the same binding site, as well as binding affinity to the microtubule. Epothilone B binds to the !$-tubulin heterodimer subunit. Once bound, the rate of !$-tubulin dissociation decreases, thus stabilizing the microtubules.

Furthermore, epothilone B has also been shown to induce tubulin polymerization into microtubules without the presence of GTP. This is caused by formation of microtubule bundles throughout the cytoplasm. Finally, epothilone B also causes cell cycle arrest at the G2/M transition phase, thus leading to cytotoxicity and eventually cell apoptosis (Balog et al, 1996). Epothilone B has similar biological properties to Epothilone A.

B. Epothilones under clinical evaluation At least six epothilones are in clinical trials for cancer treatment. Molecules under phase I or II clinical evaluation include epothilone B (patupilone; EPO960), epothilone D (KOS-862) and their second-generation (ixabepilone, BMS-310705, KOS-1584) and thirdgeneration (ZK-EPO, ABJ-879) derivatives. Although similar in chemical structure, the epothilones demonstrated a striking difference in toxicity profile in phase I studies.

Diarrhea was the dose-limiting toxicity (DLT) associated with patupilone, whereas neurotoxicity and neutropenia are the DLTs most commonly encountered with other epothilones (reviewed by Fumoleau et al, 2007).

Epothilones have demonstrated activity in lung, ovarian, breast, prostate, and renal carcinomas and in non325

Boulikas and Tsogas: Microtubule-targeting anticancer drugs page H3C

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Figure 10. Structures of Epothilone B, Ixabepilone, Sagopilone, Epothilone D and KOS-1584. Structural differences are marked red.

However, Epothilone B is 10-fold more potent than Epothilone A against P-glycoprotein-expressing multidrug resistant (MDR) cells. (-)-Epothilone B is similar to paclitaxel in binding displacement, and a substitution for paclitaxel in dependent cell growth. Epothilone B causes cell cycle arrest (IC50=3.5 nM).

Epothilone B shares the same or an overlapping binding site with paclitaxel and has been reported to have the same effects as paclitaxel on purified microtubules in vitro and on mitotic spindle structure and function in cultured cells. Epothilone B and paclitaxel alter the same microtubule dynamic parameters and to a similar extent.

At the IC50 for mitotic arrest, dynamicity was reduced by 54% by paclitaxel compared with 62% for epothilone B. In addition, no anaphase or telephone figures were observed at the IC50 for both drugs, and in 65% of the cells treated with paclitaxel, the microtubules were completely stabilized compared with 80% for epothilone B. Thus, the effects of epothilone B on microtubule dynamics are remarkably similar to those of paclitaxel, suggesting that both drugs work by the same mechanism to induce mitotic block. Epothilone B overcomes P-glycoprotein-mediated paclitaxel resistance and is more water-soluble than paclitaxel (Klamath and Jordan, 2003).

Epothilone B is a 16-membered polyketide macrolactone with a methylthiazole group connected to the macrocycle by an olefinic bond (Molnรกr et al, 2000).

Cytochrome P450epoK (P450epoK), a heme containing monooxygenase involved in epothilone biosynthesis in the myxobacterium Sorangium cellulosum, catalyzes the epoxidation of epothilones C and D into epothilones A and B, respectively. The epothilones are positioned with the macrolide ring roughly perpendicular to the heme plane and I helix, and the thiazole moiety provides key interactions that very likely are critical in determining substrate specificity. Interestingly, there are strong

parallels between the epothilone/P450epoK paclitaxel/tubulin interactions (Nagano et al, 2003).

and

E. Ixabepilone (BMS-247550) Ixabepilone (BMS-247550, azaepothilone B) is a semi-synthetic, microtubule stabilizing epothilone B analogue developed by Bristol-Myers Squibb (Stachel et al, 2000), which is more potent than taxanes and has displayed activity in taxane-resistant patients. Like all epothilones, Ixabepilone binds to tubulin and promotes tubulin polymerization and microtubule stabilization, thereby arresting cells in the G2/M phase of the cell cycle and inducing tumor cell apoptosis.

Ixabepilone demonstrated antineoplastic activity against taxane-resistant cell lines. FDA approved ixabepilone in 2007 (IXEMPRA, Bristol) for the treatment of aggressive metastatic or locally advanced breast cancer based on two multicenter trials on 878 patients using IXEMPRA either as a monotherapy or in combination with capecitabine. A single-arm monotherapy Phase II enrolled 126 patients with metastatic or locally advanced breast cancer resistant to three prior therapies (an anthracycline, a taxane and capecitabine). The primary endpoint was objective response rate and gave a partial response of 12.4% in 113 response-evaluable patients.

Treatment-related non-hematological adverse events (greater than or equal to 20%) included: peripheral sensory neuropathy 62% (Grade 3/4: 14%), fatigue/asthenia 56% (Grade 3/4: 13%), myalgia/arthralgia 49% (Grade 3/4: 8%), alopecia 48% (Grade 3/4: 0%), nausea 42% (Grade 3/4: 2%), stomatitis/mucositis 29% (Grade 3/4: 6%), vomiting 29% (Grade 3/4: 1%), diarrhea 22% (Grade 3/4: 1%), and musculoskeletal pain 20% (Grade 3/4: 3%).

Treatment-related hematological adverse events (greater than or equal to 20%) included: neutropenia (Grade 3/4: 54%) and leukopenia (Grade 3/4: 49%).

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Gene Therapy and Molecular Biology Vol 12, page 327 A randomized Phase III trial evaluated the efficacy and safety of IXEMPRA in combination with capecitabine in comparison with capecitabine as monotherapy. This trial included 752 patients who were previously treated with anthracyclines and taxanes, and whose tumors had demonstrated prior resistance to these therapies.

Evaluation of the primary endpoint demonstrated that IXEMPRA in combination with capecitabine resulted in a statistically significant improvement in progression-free survival compared to capecitabine monotherapy - median 5.7 vs. 4.1 months. Adverse events included neutropenia (Grade 3/4: 68%), leukopenia (Grade 3/4: 57%), peripheral neuropathy 65% (Grade 3/4: 21%), palmarplantar erythrodysesthesia (hand-foot) syndrome 64% (Grade 3/4: 18%), fatigue/asthenia 60% (Grade 3/4: 16%), and others.

A randomized phase II trial in 92 chemotherapynaive patients with progressive castrate metastatic prostate cancer treated with ixabepilone either as a single agent or in combination with estramustine phosphate reported a PSA RR of 48% in the ixabepilone arm and 69% in the combination arm, with an acceptable safety profile (Galsky et al, 2005). The predominant toxicities in the patients treated with ixabepilone alone or in combination with estramustine phosphate included grade 3/4 neutropenia (22% vs. 29%, respectively), grade 3 neuropathy (13% vs. 7%), and grade 3 fatigue (9% vs.

9%). A study of single-agent ixabepilone (SWOG S0111) reported a PSA RR of 33% in 42 evaluable patients with HRPC (Hussain et al, 2005). Although there were no confirmed objective responses in the 20 patients with measurable disease, 1 patient (5%) achieved an unconfirmed complete response, and 2 patients (10%) achieved an unconfirmed PR. Estimated median PFS was 6 months (95% CI, 4-8 months), and median survival was 18 months (95% CI, 13-24 months). A phase II trial conducted by the Eastern Cooperative Oncology Group (E3803) is evaluating the efficacy of ixabepilone in patients with no prior chemotherapy as well as in patients who have received % 2 prior regimens, and initial findings from a noncomparative phase II trial evaluating ixabepilone and mitoxantrone/prednisone in patients with taxane-refractory pretreated Hormone Refractory Prostate Cancer (HRPC) were reported recently (Small et al, 2006).

Eligible patients were randomized to second-line treatment with ixabepilone or mitoxantrone/prednisone, and, upon progression, patients were allowed to cross over to the alternate regimen for third-line treatment. Clinical outcomes of patients with taxane-resistant HRPC who were treated with subsequent chemotherapy were also reported recently. A total of 82 evaluable patients were treated with ixabepilone or mitoxantrone/prednisone.

Median OS from protocol entry was 12.5 months for the patients in the ixabepilone arm and 13.0 months for those in the mitoxantrone/prednisone arm. Seventeen percent of the patients in the ixabepilone group and 20% of those in the mitoxantrone/prednisone group achieved a second-line PSA decline (& 50%). One of the 23 evaluable patients receiving second-line ixabepilone and 1 of the 20 evaluable patients receiving second-line mitoxantrone/prednisone achieved a PR. Neutropenia was

the most frequent grade 3/4 adverse event associated with second line therapy (41% in the ixabepilone arm, 56% in the mitoxantrone/prednisone arm). Third-line crossover therapy occurred in 39% of the patients treated with ixabepilone and 68% of those treated with mitoxantrone/prednisone. Third-line therapy yielded a PSA decline (& 50%) in 3 of the 25 patients (12%) treated with ixabepilone and 4 of the 13 patients (31%) treated with mitoxantrone/prednisone.

Vascular smooth muscle cells (VSMCs) form the lining of arterial walls and their abnormal proliferation is linked with atherosclerosis and restenosis after angioplasty. Epothilone B has been used in preventing postangioplasty restenosis. Epothilone B treatment of VSMCs caused a significant decrease in the level of cyclin-dependent protein kinase (CDK) 2 and downregulated the phosphorylation of retinoblastoma, which plays a critical role in cell cycle regulation. Furthermore, levels of p27, an inhibitor of cyclin E/CDK2 complex, were significantly increased in VSMCs treated with epothilone B, indicating that this might be a major molecular mechanism for the inhibitory effects of epothilone B on the proliferation and cell cycle of VSMCs (Lim et al, 2007).

The excretory pathways of ixabepilone were studied in Eight patients with advanced cancer who received 70 mg, 80 nCi of [14C]ixabepilone over 3 h; fecal excretion was 52.2% and urinary excretion was 25.1% (Beumer et al, 2007). Neuropathy has led to the uneven and slower than expected clinical development of ixabepilone. Singleagent ixabepilone also demonstrated robust antitumor activity in women with metastatic breast cancer that was resistant to taxanes, anthracyclines and capecitabine in phase II trials (reviewed by Pronzato, 2008).

A phase II study of ixabepilone monotherapy in metastatic renal-cell carcinoma (RCC) administered at a dose of 40 mg/m2 every 21 days did not give objective responses in the first 12 evaluable patients, but six patients showed stable disease for more than 18 weeks on therapy ensuring advancement in Phase III against RCC. Grade 3 adverse events included lymphopenia, neutropenia, leukopenia, diarrhea, and infection. Common grade 2 toxicities included alopecia, fatigue and anemia (Posadas et al, 2007).

F. Epothilone D (KOS-862) Epothilone D (KOS-862; 12,13-desoxyepothilone B) was also isolated from the myxobacterium Sorangium cellulosum. The drug was shown to reduce neointimal hyperplasia after in vivo rat carotid artery injury; from the significantly decrease in the level of CDK2 protein and inhibition of the phosphorylation of Rb, it was concluded that the major molecular mechanism of Epothilone D may involve regulation of the cell cycle G1-checkpoint proteins (Kim et al, 2007).

Epothilone D is capable of causing mitotic arrest by stabilizing tubulin polymerization. Epothilone D has demonstrated in vitro cytotoxic activity in a panel of human cell lines, equipotent to that of paclitaxel.

Epothilone D is more potent than paclitaxel in pglycoprotein overexpressing cell lines that demonstrate

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Boulikas and Tsogas: Microtubule-targeting anticancer drugs page multiple drug resistant activities. Epothilone D has also been shown to be active in the androgen-independent PC-3 human prostate cancer cells with IC50 of 0.0128 #M. In vivo, Epothilone D has shown significant antitumor activity in a range of xenograft models, including those that are resistant to paclitaxel. The dose limiting toxicity for epothilone D in phase I studies has been neurologic including both central and peripheral neurologic toxicity.

Approximately 75% of patients enrolled in phase I studies experienced at least one neurologic toxicity (Beer et al, 2007). Epothilone D is being tested in combination with trastuzumab (Herceptin) in patients with HER-2 metastatic breast cancer. Adverse events were mostly Grade 1 or 2, with three Grade 3 incidents of sensory neurological toxicities

described using a convergent synthetic approach; the aim of this synthesis was the restriction of the mobility of the aromatic side chain. The C1-C8 sector remained unchanged, in view of its seemingly crucial role in biological activity. A single methylene bridge was introduced between C14 and C17 (Figure 11). The resulting cyclopentene moiety, which incorporated the C16-C17 double bond, was designed to rigidify the side chain while still permitting sufficient mobility of the pyridine ring to allow for the preferred N-atom orientation for a hydrogen bonding interaction with the receptor.

These epothilone analogues showed strong and selective growth inhibitory activity against leukemia cell lines (Alhamadsheh et al, 2008).

I. Sagopilone G. KOS-1584

The process of sagopilone development at Bayer Schering Pharma is an interesting story. One day, an external researcher offered the company a substance he had discovered, which he considered as a possible anticancer medication but the offer was rejected. By the time interest developed a rival company had already secured the rights to the substance. Bayer Schering Pharma now owns sagopilone, an epothilone analogue, with a structure somewhat different to the naturally occurring one; chemical ingenuity was used to modify the structure deriving at 450 compounds and broadening the therapeutic window of natural epothilones. Approximately half of the compounds synthesized, differed only slightly from the prototype epothilone, were promising with respect to toxicity, therapeutic efficacy and development of resistance after treatment of cells in culture and ease of chemical synthesis. A total of 39 chemical steps were used to produce three initial subunits of Sagopilone, which were then used to construct the finished molecule. How could such a complex process ever be implemented costeffectively on a large scale? Converting one step in the chemical process from the laboratory to production-scale (up scaling), normally takes a month and for the 39 steps of sagopilone synthesis mere up scaling would take more than three years. Acceleration of this process resulted in the production of 36 grams of the substance in six months, sufficient for the treatment of approximately 200 patients whereas further improvements and up scaling took place.

Bayer is now the only company with a fully synthetic epothilone, sagopilone, in advanced clinical development.

KOS-1584 (9,10-didehydroepothilone D) along with KOS-862 (Epothilone D) are the most advanced epothilone drug candidates of Kosan Biosciences. KOS1584 is a second-generation compound with increased potency, favorable tissue distribution, and ease of formulation. Kosan is developing its epothilone compounds in collaboration with Roche.

KOS-1584 has demonstrated in vitro cytotoxicity, more potent or equipotent to that of paclitaxel in a panel of human cell lines. KOS-1584 has shown significant antitumor activity in a range of xenograft models, including non-small cell lung cancer models resistant to paclitaxel and those expressing multidrug resistance. A long elimination half-life was seen in Phase I trials. KOS1584 has demonstrated antitumor activity and favorable tolerability in Phase 1 trials in patients with solid tumors, including substantial tumor shrinkage measured by objective responses in non-small cell lung, ovarian and pancreatic cancers, as well as durable stable disease in many additional tumors.

In April 2008, Kosan initiated a Phase 2 trial of epothilone KOS-1584 in patients with non-small cell lung cancer who have previously received only one prior chemotherapy regimen. The primary endpoint of the Phase 2 trial is objective response rate. KOS-1584 will be administered via a 3-hour intravenous infusion weekly for two weeks out of every three weeks at a dose of 25 mg/m2.

H. Conformationally restrained epothilones Stereoselective total syntheses of two novel conformationally restrained epothilone analogues has been

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Figure 11. Structures of conformationally restrained epothilone analogues.

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Gene Therapy and Molecular Biology Vol 12, page 329 The effectiveness of sagopilone, the first fully synthetic third generation epothilone in clinical development, against paclitaxel in a breast cancer bone metastasis model was evaluated in a recent study. The therapeutic effect of sagopilone and paclitaxel on tumorinduced osteolysis and tumor burden in athymic nude mice inoculated intracardially with MDA-MB-231(SA)/luc human breast cancer cells was investigated. On day 12 after tumor cell inoculation, animals were randomized into treatment groups according to the lesion size as measured by radiography. A single dose of sagopilone was administered on day 13 (10 mg/ kg, i.v.). Paclitaxel was given once daily on days 13-17 (9 mg/ kg, i.p.). At sacrifice (day 23), bone lesions were measured using radiography and micro-CT. Tumor cell dissemination was detected by bioluminescence imaging and histomorphometry. The effect of compounds on bone resorption was determined by measuring Tartrate-resistant acid phosphatase 5b (TRACP5b) in serum and by counting the number of osteoclasts on tumor-bone interface by histomorphometry. Radiographic analysis revealed that further tumor-induced bone destruction was merely reduced by paclitaxel, whereas sagopilone completely

prevented it. Sagopilone-treated animals had also higher bone volume compared to other groups as measured by micro-CT. A marked effect of sagopilone on tumor growth in bone was observed as reduced bioluminescence signal intensity in vivo.

This was confirmed by histomorphometry in H&E-stained bone sections.

Paclitaxel had no significant effect on tumor growth in bone. Sagopilone had significantly better effect on reducing bone destruction and tumor burden when compared to paclitaxel in a mouse model of established breast cancer bone metastasis (Strube et al, 2008).

J. Discodermolide and analogues Discodermolide (Figure 12) stabilizes microtubules and blocks cells at the G2/M phase of the cell cycle in a manner similar to that of Taxol. Non-taxane microtubulestabilizers including the epothilones and discodermolide, are progressing through clinical trials. An advanced synthesis for discodermolide was based on the readily available fermentation product oleandomycin (Parker and Wang, 2007).

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Figure 12. Structures of discodermolide, C19-[4-(4-3H-benzoyl-phenyl)-carbamate]-discodermolide discodermolide analogue. Structural differences are marked in red.

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coumarin-derived

Boulikas and Tsogas: Microtubule-targeting anticancer drugs page Discodermolide has been shown to inhibit the proliferation of human cells by arresting the cell cycle in G2/M phase.

Discodermolide hyperstabilized microtubules, an event especially prevalent during cell division (Day et al, 1996). Hyperstabilization of the mitotic spindle causes cell cycle arrest and cell death by apoptosis. Over a variety of cell lines, activity has been measured at IC50 = 3-80 nM. Discodermolide competed with paclitaxel for microtubule binding, but with higher affinity and was also effective in paclitaxel- and epothilone-resistant cancer cells (Jordan, 2002). It has been reported that Discodermolide-treated breast carcinoma cells displayed spectacular rearrangement of the microtubule cytoskeleton, including extensive microtubule bundling. Microtubule rearrangement that occurred with 10 nM discodermolide required 1 #M Taxol. Discodermolide had equally impressive effects on tubulin assembly in vitro. Near-total polymerization occurred at 0 째C with tubulin plus microtubule-associated proteins (MAPs) under conditions in which Taxol at an identical concentration was inactive. Without MAPs and/or without GTP, tubulin assembly was also more vigorous with discodermolide than with Taxol under every reaction condition examined. Discodermolide-induced polymer differed from Taxol- induced polymer in that it was completely stable at 0 째C in the presence of high concentrations of Ca2+. In a quantitative assay designed to select for agents more effective than Taxol in inducing assembly, discodermolide had an EC50 value of 3.2 #M versus 23 #M for Taxol (Day et al, 1996; Amos et al, 2003). In a recent comparative study A549 human lung carcinoma cells were treated with discodermolide at concentrations higher than 8nM, accelerated cell aging was observed by a functional $-galactosidase activity at pH=6. When the cells were treated with IC50 concentrations of doxorubicin, Taxol and discodermolide, only the latter two resulted in aberrant mitosis. However only discodermolide produced an aging associated $galactosidase activity (Horwitz et al, 2005).

Coumarin-derived discodermolide analogues (Figure 12) possessing equivalent antiproliferative activity to the natural product have been described; the complete C-1 to C-7 fragment was replaced with a coumarin moiety in these compounds (Shaw et al, 2007). Photoaffinity-labeled discodermolide analogues have been used to investigate their binding site in tubulin; all promoted microtubule polymerization in the absence of GTP. The analogue, C19[4-(4-3H-benzoyl-phenyl)-carbamate] -discodermolide (Figure 12) had the highest extent of photoincorporation, it was more cytotoxic than discodermolide, could displace [3H]Taxol from microtubules, and bound amino acid residues 355-359, in !-tubulin, which is in close proximity to the Taxol binding site (Xia et al, 2006).

intravenously (IV). After injection, they are eventually metabolized by the liver and excreted. They work in a cellcycle specific manner, halting mitosis of affected cells and causing cell death. The mechanism of action involves binding to the tubulin monomers and keeping the microtubules (spindle fibers) from forming. These alkaloids also seem to interfere with cells' ability to synthesize DNA and RNA. Although the plant has medical uses, it can produce many serious side effects if smoked or ingested.

There are four major vinca alkaloids in clinical use: Vinblastine, vinorelbine, vincristine and vindesine.

A. Vinblastine Vinblastine (Velban, Velsar), a vinca alkaloid acts as an inhibitor of tubulin polymerization and mitosis. This contrasts the stabilization of tubulin polymers by taxanes.

It also seems to exert its anticancer properties by interfering with glutamic acid metabolism (specifically, the pathways leading from glutamic acid to the Krebs cycle and to urea formation). Vinblastine treatment suppresses angiogenesis (Albertsson et al, 2008).

Vinblastine (Figure 13), is approved by FDA for multiple hematologic and solid tumors. It is most often used in Hodgkin's disease, non-Hodgkin's lymphoma, breast cancer, and germ cell tumors. Because it is a vesicant, extravasation precautions are required during administration.

The major adverse effect of vinblastine is hematologic toxicity which occurs much more frequently than with vincristine therapy.

Leukopenia (granulocytopenia) occurs most commonly and is usually the dose-limiting factor in vinblastine therapy. Other side effects include nausea, vomiting and constipation, dyspnea, chest or tumor pain, wheezing and fever during administration. Some rare cases of syndrome of inappropriate antidiuretic hormone secretion as well as angina pectoris have been reported (Gobbi et al, 2005; Connors, 2005).

Vinblastine induced an accumulation of the G2/M cells with the appearance of aneugenic micronuclei during monocyte-macrophage differentiation induced in a monocytic cell line by phorbol 12-myristate 13-acetate (PMA). Actinomycin D on the contrary, induced under similar conditions a drastic reduction of the G2/M cells (Spano et. al, 2007). Apoptosis is not a major mechanism of cell death induced by etoposide, vinblastine and estramustine in prostate cell lines and appeared to be independent of p53 status and bax/bcl-2 expression (Serafin and Bohm, 2005).

1. Mechanisms of vinblastine Vinblastine is a microtubule-depolymerizing drug.

The X-ray structure of vinblastine bound to tubulin in a complex with the RB3 protein stathmin-like domain (RB3SLD) showed that vinblastine introduces a wedge at the interface of two tubulin molecules and thus interferes with tubulin assembly; furthermore, EM studies showed that vinblastine induced tubulin self-association into spiral aggregates at the expense of microtubule growth in a

VI. Vinca alkaloids The Vinca alkaloids are a subset of drugs that are derived from the periwinkle plant, Catharanthus roseus (also Vinca rosea, Lochnera rosea, and Ammocallis rosea).

While it has been historically used to treat numerous diseases, it has most recently been employed for its anticancer properties. All vinca alkaloids are administered 330

Gene Therapy and Molecular Biology Vol 12, page 331 reaction that appears to be regulated by the C-terminus of $-tubulin and is enhanced by GDP and GTP. Vinblastine also arrests the cell cycle in G2/M-phase by blocking mitotic spindle formation. Triggers Raf-1 activation, phosphorylation of bcl-2-family proteins, induction of p53 expression, and apoptosis in several tumor cell lines (Rai and Wolff, 1998). Vinblastine and the amino-terminal part of RB3-SLD binding sites share a hydrophobic groove on the alpha-tubulin surface that is located at an intermolecular contact in microtubules. Drugs designed to perturb microtubule dynamics by interfacial interference at this site of !-tubulin, can be an attractive anticancer target (Gigant et al, 2005).

Efflux of the P-glycoprotein substrate vinblastine sulfate through Caco-2 cell monolayers was reduced by polyoxyethylene 40 stearate (PS40) thus enhancing the antitumor activity of vinblastine (Luo et al, 2007).

2. Regimens containing vinblastine Advanced urothelial cancer is treated with conventional frontline chemotherapy with gemcitabine and cisplatin; however, traditional or dose-dense methotrexate, vinblastine, doxorubicin and cisplatin regimens are also in current use (Sonpavde et al, 2008).

3. Preclinical regimens containing vinblastine A significant synergistic effect of vinblastine and HSV-Tk/GCV "suicide" gene therapy mediated by human serum albumin (HSA)-associated lipoplexes has been found in cell cultures (Faneca et al, 2008).

A novel way of diminishing cellular resistance to vinblastine has been suggested: Alterations in DNA methylation of the mdr-1 gene promoter are known to be linked to mdr-1 gene expression and related to intracellular S-adenosyl-methionine; cobalamin, a cofactor of methionine-synthase, downregulates mdr-1 gene expression, as well as P-glycoprotein expression and function, and significantly increases cytotoxicity of vinblastine (Marguerite et al, 2007).

Tubulin, the major protein of microtubules, is posttranslationally modified by palmitoylation; this modification is inhibited in vitro by stoichiometric levels of vinblastine; a low, clinically relevant dose of vinblastine, inhibited palmitoylation of tubulin in human leukemic lymphocytes, microtubules were disassembled and cells became apoptotic (Caron and Herwood, 2007).

4. Reactive oxygen species (ROS), vinblastine and apoptosis Reactive oxygen species (ROS), such as superoxide anion radicals (O2-) and hydrogen peroxide (H2O2) are potentially harmful by-products of normal cellular metabolism; ROS is generated by all aerobic organisms and it seems to be indispensable for signal transduction pathways. Overproduction of reactive oxygen species initiate lethal chain reactions involving oxidation and damage to cellular structures, that are crucial for integrity and survival.

OH N

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H C2H5 N

H3CO

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OCOCH3 COOCH3

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Vinblastine

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Vindesine

Figure 13. Structures of vinblastine, vinorelbine, vincristine and vindesine.Structural differences are marked in red.

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OH CONH2

Boulikas and Tsogas: Microtubule-targeting anticancer drugs page Vinblastine, cisplatin, mitomycin C, doxorubicin, camptothecin, inostamycin, neocarzinostatin and other anticancer drugs exhibit antitumor activity via ROSdependent activation of apoptotic cell death. The "oxidation therapy of cancer" has been attempted either by inducing the generation of ROS in solid tumors by delivery for example, H2O2, or by inhibiting the antioxidative enzyme (defense) system of tumor cells.

However no successful and practical results were obtained probably because of the lack of tumor selective ROS delivery and in induction of severe side effects. Delivering PEGylated enzymes generating reactive oxygen species, such as xanthine oxidase and D-amino acid oxidase (DAO) is an interesting approach. In addition, a PEGylated zinc protoporphyrin (PEG-ZnPP) and a highly water soluble micellar formulation of ZnPP based on amphiphilic styrene maleic acid copolymer were prepared, which were potent inhibitors of heme oxygenase-1 for oxidation therapy of cancer (Fang et al, 2007).

Whereas antioxidative enzymes such as catalase and SOD are down-regulated in most solid tumors in vivo, heme oxygenase-1 is highly upregulated exerting antiapoptosis in tumors and therefore, its targeting by zinc protoporphyrin might find application as an anticancer drug (Fang et al, 2007).

interdigitation, since cholesterol interrupts the upraise of enthalpy change (Koukoulitsa et al, 2006).

Vinorelbine has a number of side-effects that can limit its use: Lowered resistance to infection, bruising or bleeding, anemia, constipation, diarrhea, nausea, numbness or tingling in hands or feet (peripheral neuropathy), tiredness and a general feeling of weakness (asthenia), inflammation of the vein into which it was injected (phlebitis). Less common effects are hair loss and allergic reaction.

C. Vincristine Vincristine (Oncovin, Vincasar), (Figure 13), is another vinca alkaloid compound that inhibits tubulin polymerization. As it is a vesicant it should be administered with extravasation precautions. It is FDA approved to treat acute leukemia, rhabdomyosarcoma, neuroblastoma, Wilmâ&#x20AC;&#x2122;s tumor, Hodgkin's disease and other lymphomas.

Vincristine is administrated intravenously.

Peripheral neuropathy is the dose limiting side effect, because of this, people with neuromuscular disorders should steer clear of this drug if possible. Likewise, people with some forms of Charcot-Marie-Tooth syndrome should avoid vincristine. Other side effects include mild myelosuppression, constipation -rather commonly-, autonomic neuropathy, CNS toxicity, nausea and vomiting. There have been reported a few cases of acute cardiopulmonary or pain symptoms during administration as well as transient elevation of liver function tests (Pappo et al, 2007; Chow et al, 2006).

As the microtubule is a dynamic protein, constantly polymerizing and depolymerizing, vinca alkaloid poisoned dimers could easily be incorporated into the microtubule polymer, preventing further growth. The incorporation of vincristine onto the heterodimer is rapidly reversible, and appears to occur at two sites per tubulin dimer. At higher concentrations of drug, microtubular crystals are formed, consisting of two intertwined helices of tubulin. Arrests cell cycle in G2/M-phase by blocking mitotic spindle formation. Triggers Raf-1 activation, phosphorylation of bcl-2-family proteins, induction of p53 expression, and apoptosis in several tumor cell lines. Inhibits VEGF production in leukemia cell lines. MRP1 transports vincristine in an ATP- and GSH-dependent manner induces the destabilization of polymerized tubulin, by binding to a site recently localized on !-tubulin, and has a high affinity for the protein.

Accidental injection of vinca alkaloids into the spinal canal (intrathecal administration) is highly dangerous, with a mortality rate approaching 100%. The medical literature documents cases of ascending paralysis due to massive encephalopathy and spinal nerve demyelination, accompanied by intractable pain, almost uniformly leading to death; a handful of survivors were left with devastating neurological damage with no hope of recovery. Rescue treatments consist of washout of the cerebrospinal fluid and administration of protective medications. A significant series of inadvertent intrathecal vincristine administration occurred in China in 2007 when batches of cytarabine and methotrexate (both often used intrathecally) manufactured

B. Vinorelbine Vinorelbine (Navelbine, Figure 13) is a semisynthetic vinca alkaloid that acts the same way as Vinblastine.

Vinorelbine and mitoxantrone (a topoisomerase II inhibitor) have both been demonstrated to have significant antitumor activity in patients with breast cancer. Vinorelbine is approved from the FDA for the treatment of relapsed metastatic breast cancer and for NSCLC either as a single agent or combined with a platinating agent. It is a mild vesicant, requiring extravasation precautions. Myelosuppression -mostly leucopenia- is the dose limiting effect. Not significant nausea and vomiting are reported as well neuropathy -but milder than it is observed with vinblastine- and tumor pain during administration. Acute reaction, such as dyspnea, chest pain and wheezing has been reported during administration but can be prevented in some cases by premedication with corticosteroids (Zelek et al, 2001; Gridelli et al, 2003; Georgoulias et al, 2005).

1. Vinorelbine mechanisms In addition to exerting its antitumor activity by interfering with the polymerization of tubulin, vinorelbine showed antiproliferative effects in human osteosarcoma cells inducing apoptosis without affecting phosphorylation of Bcl-2 but rather by down-regulation of cyclin D1 and up-regulation of p53 expression in wild-type cells; in p53 negative osteosarcoma cells, however, vinorelbine showed no alteration in cyclin D1 (Roncuzzi et al, 2006).

The total enthalpy change in dipalmytoylphosphatidylcholine (DPPC) bilayers was increased by vinorelbine indicating a partial interdigitation of the lipid alkyl chains. The presence of cholesterol in Vinorelbine-DPPC bilayers induced an obstruction of the

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Gene Therapy and Molecular Biology Vol 12, page 333 by the company Shanghai Hualian were found to be contaminated with vincristine.

On the basis of encouraging preclinical activity vinflunine has been selected for clinical development in patients with a wide spectrum of solid tumors. Clinically significant activity has been seen in phase II studies, mainly in the treatment of transitional cell carcinoma of the urothelial tract, non-small cell lung cancer, and carcinoma of the breast. Vinflunine is currently in phase III trial assessment in patients with (second line) transitional cell carcinoma of the urothelium and first-line advanced breast cancer. The efficacy of vinflunine in patients with advanced non-small cell lung cancer previously treated with a platinum-containing regimen was confirmed by a large phase III trial (Nguyen et al, 2008).

In a phase II study the efficacy of vinflunine against malignant pleural mesothelioma (MPM) was assessed.

Patients with a histologically confirmed diagnosis of MPM were eligible for enrollment onto this multicenter phase II trial if they had not received prior chemotherapy or radiotherapy and had measurable lesions by Response Evaluation Criteria in Solid Tumors (RECIST). Vinflunine 320 mg/m2 by 10-minute intravenous infusion was administered on day 1 of 21-day cycles. A response rate of 13.8% was found. The median survival was 10.8 months.

The most common adverse events were anemia, neutropenia, fatigue, constipation, and nausea. Of grade 3 and 4 toxicities, neutropenia and constipation were the most common (45% and 9% of patients, respectively) (Talbot et al, 2007).

D. Vindesine Vindesine (Eldisine and Fildesin) has a serum halflife of about 24 hours and is administered at a dose of 3 milligrams per square meter of body surface. Its toxicity and side effects are similar to those of vinblastine.

Vindesine (Figure 13) is used mainly to treat melanoma and lung cancers (carcinomas) and, with other drugs, to treat uterine cancers.

A study published in 2006 reported the effects of vindesine and gemcitabine on patients with advanced nonsmall cell lung cancer (NSCLC). 44 patients (36 males and 8 females with a median age of 70 years and a median Karnofsky performance score of 60) were recruited between January 1998 and June 2001. 9 patients (20.5%) were stage IIIB patients and 35 (79.5%) were stage IV patients. 20 patients (45.5%) had squamous carcinoma and 24 (54.5%) non-squamous carcinoma. The patients received gemcitabine 1000 mg/m2 and vindesine 3mg/m2 (max 5mg) on days 1 and 8 every 3 weeks, and were all evaluable for response and toxicity: 17 (38.6%) were partial responders, 17 (38.6%) experienced stable disease, and 10 (22.3%) progressive disease. Grade 3-4 anemia, neutropenia and thrombocytopenia were observed in, respectively, 6.8, 9.1 and 2.3% of the patients, and grade 2-3 fatigue, paresthesias and skin toxicity in, respectively, 11.4, 20.4 and 2.3%. After a median follow-up of 54 months, 43/44 patients died; median survival was 12 months, and a clinical benefit was observed in 54.5% of cases. Gemcitabine plus vindesine proved to be an active and well-tolerated schedule (Cetto et al, 2006).

VII. Other tubulin polymerization inhibitors A. Tubulysin A Tubulysin A (Figure 15A) is a highly cytotoxic peptide from myxobacteria with antimitotic activity.

Tubulysin A inhibited tubulin polymerization more efficiently than vinblastine, induced depolymerization of isolated microtubule preparations and triggered the apoptotic process (Figure 15B); electron microscopy studies showed that tubulysin A induced the formation of rings, double rings, and pinwheel structures. The mode of action of tubulysin A resembled that of peptide antimitotics dolastatin 10, phomopsin A, and hemiasterlin (Khalil et al, 2006).

E. Vinflunine Vinflunine is a novel third generation vinca alkaloid with superior antitumor activity in preclinical models, a more favorable toxicity profile compared to the other vinca alkaloids and with radiosensitizing potential (Simoens et al, 2006, 2008). Vinflunine (Javlor) is the first fluorinated microtubule inhibitor and is obtained by semisynthesis using superacidic chemistry to selectively introduce two fluorine atoms at the 20' position of the catharanthine moiety (Figure 14).

Its mechanism of action differs from other members of the vinca alkaloid class in terms of tubulin-binding affinity, microtubule dynamics, spiral formation, and intracellular accumulation. Vinflunine altered adhesion site targeting by microtubules and suppressed the microtubule (+) end pause that occurs at adhesion sites during endothelial cell migration; it has, therefore, an antiangiogenesis potential (HonorĂŠ et al, 2008). The high antitumor activity of vinflunine is not well understood since it binds to tubulin with an overall affinity severalfold lower than that of vinblastine or vincristine; vinflunine suppressed calmodulin interaction with the microtubule-associated protein STOP (stable tubule only polypeptide); this finding and the different binding modes of vinflunine and vinblastine to calmodulin could explain the remarkable antitumor activity of vinflunine (Makarov et al, 2007).

H N

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H C2H5 N CH3

H OH

OCOCH3 COOCH3

Vinflunine Figure 14. Structure of Vinflunine with the differences marked red.

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Figure 15. (Top) Structure of Tubulisin A. (A, B) Tubulysin induces a depletion of microtubules. PtK2 potoroo kidney cells were cultured in the absence and presence of tubulysin A (59 nm) for 4 h. (A) The control sample shows the normal microtubular network (green) in interphase cells and two mitotic bipolar spindles. Chromosomes and nuclei are stained blue. B ( ) In tubulysin treated cells the microtubule network is less dense and the centrosomes become visible. The mitotic cell in the middle shows metaphase chromosomes and few longer microtubules that do not form a mitotic spindle. From Khalil MW, Sasse F, L端nsdorf H, Elnakady YA, Reichenbach H Mechanism of action of tubulysin, an antimitotic peptide from myxobacteria. Chembiochem. 2006, 7, 678-683. Copyright Wiley-VCH Verlag GmbH & Co.KGaA. Reproduced with permission.

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