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[Cancer Research 58, 3344-3352, August 1, 1998]
© 1998 American Association for Cancer Research
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Ligand for Peroxisome Proliferator-activated Receptor {gamma} (Troglitazone) Has Potent Antitumor Effect against Human Prostate Cancer Both in Vitro and in Vivo1

Tetsuya Kubota2, Kozo Koshizuka, Elizabeth A. Williamson, Hiroya Asou, Jonathan W. Said, Stuart Holden, Isao Miyoshi and H. Phillip Koeffler

Division of Hematology/Oncology [T. K., K. K., E. A. W., H. A., H. P. K.], Division of Pathology [J. W. S.], Department of Surgery [S. H.], Cedars-Sinai Research Institute, UCLA School of Medicine, Los Angeles, California 90048, and Department of Medicine, Kochi Medical School, Kochi 783-8505, Japan [I. M.]

Troglitazone, a thiazolidinedione derivative, is a widely used antidiabetic drug that binds and activates peroxisome proliferator-activated receptor {gamma} (PPAR{gamma}) and enhances insulin sensitivity. It induces differentiation of adipocytes, which highly express PPAR{gamma}. We report that human prostate cancer cells expressed PPAR{gamma} at prominent levels and normal prostate tissues had very low expression. Dose-response clonogenic assays of the PC-3 prostate cancer cell line with troglitazone showed an antiproliferative effect (ED50, 3 x 10-7 M) and other PPAR{gamma} ligands (BRL49653: ED50, 8 x 10-8 M; 15-deoxy-{Delta}12,14-prostaglandin J2: ED50, 2 x 10-6 M; ciglitizone: ED50, not reached; indomethacin: ED50, not reached) showed similar effects. Combinations of troglitazone and a ligand specific for either retinoid X receptor or retinoic acid receptor did not show a synergistic effect. Pulse-exposure to troglitazone (10-5 M) for different durations showed that 4 days of pulse-exposure to the agent irreversibly inhibited 50% clonal growth of PC-3 cells. Interestingly, PC-3 cells cultured with troglitazone (10-5 M) showed dramatic morphological changes both by light and electron microscopy, suggesting that the cells became less malignant. Nevertheless, troglitazone did not affect either the cell cycle or several markers of differentiation. LNCaP cells constitutively produced prostate-specific antigen, and levels were markedly enhanced by all-trans-retinoic acid. Troglitazone (10-5 M, 4 days) decreased by 50% the levels of prostate-specific antigen produced by these cells. In vivo treatment of PC-3 tumors growing in male BNX triple immunodeficient mice with oral troglitazone (500 mg/kg/day) produced significant inhibition of tumor growth (P = 0.01). The only objective side effect of troglitazone in mice was the elevation of serum transaminases. Short-term culture of four surgically obtained human prostate cancer tumors with troglitazone (10-5 M, 4 days) produced marked and selective necrosis of the cancer cells (about 60%) but not the adjacent normal prostate cells. Taken together, these results suggest that troglitazone may be a useful therapeutic agent for the treatment of prostate cancer, especially in the setting of low disease burden.

1 This work was supported by NIH and United States Army grants and also in part by the CaP CURE Foundation and Parker Hughes Fund.

2 To whom requests for reprints should be addressed, at Division of Hematology/Oncology, Cedars-Sinai Medical Center, UCLA School of Medicine, 8700 Beverly Boulevard, Los Angeles, CA 90048. Phone: (310) 855-4609; Fax: (310) 659-9741.

Received 10/22/97. Accepted 6/ 2/98.




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 CarcinogenesisHome page
L. Pavan, A. Tarrade, A. Hermouet, C. Delouis, M. Titeux, M. Vidaud, P. Therond, D. Evain-Brion, and T. Fournier
Human invasive trophoblasts transformed with simian virus 40 provide a new tool to study the role of PPAR{gamma} in cell invasion process
Carcinogenesis, August 1, 2003; 24(8): 1325 - 1336.
[Abstract] [Full Text] [PDF]

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 J. Nutr.Home page
E. J. Kim, I.-J. Kang, H. J. Cho, W. K. Kim, Y.-L. Ha, and J. H. Y. Park
Conjugated Linoleic Acid Downregulates Insulin-Like Growth Factor-I Receptor Levels in HT-29 Human Colon Cancer Cells
J. Nutr., August 1, 2003; 133(8): 2675 - 2681.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. Landi, V. Moreno, L. Gioia-Patricola, E. Guino, M. Navarro, J. de Oca, G. Capella, and F. Canzian
Association of Common Polymorphisms in Inflammatory Genes Interleukin (IL)6, IL8, Tumor Necrosis Factor {alpha}, NFKB1, and Peroxisome Proliferator-activated Receptor {gamma} with Colorectal Cancer ,
Cancer Res., July 1, 2003; 63(13): 3560 - 3566.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
R. A. Gupta, P. Sarraf, E. Mueller, J. A. Brockman, J. J. Prusakiewicz, C. Eng, T. M. Willson, and R. N. DuBois
Peroxisome Proliferator-activated Receptor {gamma}-mediated Differentiation: A MUTATION IN COLON CANCER CELLS REVEALS DIVERGENT AND CELL TYPE-SPECIFIC MECHANISMS
J. Biol. Chem., June 13, 2003; 278(25): 22669 - 22677.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
D. Bruemmer, F. Yin, J. Liu, J. P. Berger, T. Kiyono, J. Chen, E. Fleck, A. J. Van Herle, B. M. Forman, and R. E. Law
Peroxisome Proliferator-Activated Receptor {gamma} Inhibits Expression of Minichromosome Maintenance Proteins in Vascular Smooth Muscle Cells
Mol. Endocrinol., June 1, 2003; 17(6): 1005 - 1018.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Gastrointest. Liver Physiol.Home page
H. J. Cho, W. K. Kim, E. J. Kim, K. C. Jung, S. Park, H. S. Lee, A. L. Tyner, and J. H. Y. Park
Conjugated linoleic acid inhibits cell proliferation and ErbB3 signaling in HT-29 human colon cell line
Am J Physiol Gastrointest Liver Physiol, June 1, 2003; 284(6): G996 - G1005.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
K. D. Houston, J. A. Copland, R. R. Broaddus, M. M. Gottardis, S. M. Fischer, and C. L. Walker
Inhibition of Proliferation and Estrogen Receptor Signaling by Peroxisome Proliferator-activated Receptor {gamma} Ligands in Uterine Leiomyoma
Cancer Res., March 15, 2003; 63(6): 1221 - 1227.
[Abstract] [Full Text] [PDF]

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 Am. J. Clin. Nutr.Home page
P. D Terry, T. E Rohan, and A. Wolk
Intakes of fish and marine fatty acids and the risks of cancers of the breast and prostate and of other hormone-related cancers: a review of the epidemiologic evidence
Am. J. Clinical Nutrition, March 1, 2003; 77(3): 532 - 543.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
C. Qin, R. Burghardt, R. Smith, M. Wormke, J. Stewart, and S. Safe
Peroxisome Proliferator-activated Receptor {gamma} Agonists Induce Proteasome-dependent Degradation of Cyclin D1 and Estrogen Receptor {alpha} in MCF-7 Breast Cancer Cells
Cancer Res., March 1, 2003; 63(5): 958 - 964.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
R. A. Gupta, P. Sarraf, J. A. Brockman, S. B. Shappell, L. A. Raftery, T. M. Willson, and R. N. DuBois
Peroxisome Proliferator-activated Receptor gamma and Transforming Growth Factor-beta Pathways Inhibit Intestinal Epithelial Cell Growth by Regulating Levels of TSC-22
J. Biol. Chem., February 21, 2003; 278(9): 7431 - 7438.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. J. Baek, L. C. Wilson, L. C. Hsi, and T. E. Eling
Troglitazone, a Peroxisome Proliferator-activated Receptor gamma (PPARgamma ) Ligand, Selectively Induces the Early Growth Response-1 Gene Independently of PPARgamma . A NOVEL MECHANISM FOR ITS ANTI-TUMORIGENIC ACTIVITY
J. Biol. Chem., February 14, 2003; 278(8): 5845 - 5853.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
J. C. Desmond, J. C. Mountford, M. T. Drayson, E. A. Walker, M. Hewison, J. P. Ride, Q. T. Luong, R. E. Hayden, E. F. Vanin, and C. M. Bunce
The Aldo-Keto Reductase AKR1C3 Is a Novel Suppressor of Cell Differentiation That Provides a Plausible Target for the Non-Cyclooxygenase-dependent Antineoplastic Actions of Nonsteroidal Anti-Inflammatory Drugs
Cancer Res., January 15, 2003; 63(2): 505 - 512.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
H. P. Koeffler
Peroxisome Proliferator-activated Receptor {gamma} and Cancers
Clin. Cancer Res., January 1, 2003; 9(1): 1 - 9.
[Abstract] [Full Text] [PDF]

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 ASH Education BookHome page
W. L. Carroll, D. Bhojwani, D.-J. Min, E. Raetz, M. Relling, S. Davies, J. R. Downing, C. L. Willman, and J. C. Reed
Pediatric Acute Lymphoblastic Leukemia
Hematology, January 1, 2003; 2003(1): 102 - 131.
[Abstract] [Full Text] [PDF]

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 Cancer Epidemiol. Biomarkers Prev.Home page
M. F. Leitzmann, M. J. Stampfer, J. Ma, J. M. Chan, G. A. Colditz, W. C. Willett, and E. Giovannucci
Aspirin Use in Relation to Risk of Prostate Cancer
Cancer Epidemiol. Biomarkers Prev., October 1, 2002; 11(10): 1108 - 1111.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
M. L. Martelli, R. Iuliano, I. Le Pera, I. Sama', C. Monaco, S. Cammarota, T. Kroll, L. Chiariotti, M. Santoro, and A. Fusco
Inhibitory Effects of Peroxisome Proliferator-Activated Receptor {gamma} on Thyroid Carcinoma Cell Growth
J. Clin. Endocrinol. Metab., October 1, 2002; 87(10): 4728 - 4735.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
J. Huang, W. C. Powell, A. C. Khodavirdi, J. Wu, T. Makita, R. D. Cardiff, M. B. Cohen, H. M. Sucov, and P. Roy-Burman
Prostatic Intraepithelial Neoplasia in Mice with Conditional Disruption of the Retinoid X Receptor{alpha} Allele in the Prostate Epithelium
Cancer Res., August 15, 2002; 62(16): 4812 - 4819.
[Abstract] [Full Text] [PDF]

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 Hum Exp ToxicolHome page
J D Tugwood and C T Montague
Biology and toxicology of PPARg ligands
Human and Experimental Toxicology, August 1, 2002; 21(8): 429 - 437.
[Abstract] [PDF]

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 Jpn J Clin OncolHome page
Y. Terashita, H. Sasaki, N. Haruki, T. Nishiwaki, H. Ishiguro, Y. Shibata, J. Kudo, S. Konishi, J. Kato, H. Koyama, et al.
Decreased Peroxisome Proliferator-activated Receptor Gamma Gene Expression is Correlated with Poor Prognosis in Patients with Esophageal Cancer
Jpn. J. Clin. Oncol., July 1, 2002; 32(7): 238 - 243.
[Abstract] [Full Text] [PDF]

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 Mol Hum ReprodHome page
L. Capparuccia, D. Marzioni, A. Giordano, F. Fazioli, M. De Nictolis, N. Busso, T. Todros, and M. Castellucci
PPAR{gamma} expression in normal human placenta, hydatidiform mole and choriocarcinoma
Mol. Hum. Reprod., June 1, 2002; 8(6): 574 - 579.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
J. Shao, H. Sheng, and R. N. DuBois
Peroxisome Proliferator-activated Receptors Modulate K-Ras-mediated Transformation of Intestinal Epithelial Cells
Cancer Res., June 1, 2002; 62(11): 3282 - 3288.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Y. Cui, K. Miyoshi, E. Claudio, U. K. Siebenlist, F. J. Gonzalez, J. Flaws, K.-U. Wagner, and L. Hennighausen
Loss of the Peroxisome Proliferation-activated Receptor gamma (PPARgamma ) Does Not Affect Mammary Development and Propensity for Tumor Formation but Leads to Reduced Fertility
J. Biol. Chem., May 10, 2002; 277(20): 17830 - 17835.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
R. C. Haydon, L. Zhou, T. Feng, B. Breyer, H. Cheng, W. Jiang, A. Ishikawa, T. Peabody, A. Montag, M. A. Simon, et al.
Nuclear Receptor Agonists As Potential Differentiation Therapy Agents for Human Osteosarcoma
Clin. Cancer Res., May 1, 2002; 8(5): 1288 - 1294.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
T. E. Akiyama, S. Sakai, G. Lambert, C. J. Nicol, K. Matsusue, S. Pimprale, Y.-H. Lee, M. Ricote, C. K. Glass, H. B. Brewer Jr., et al.
Conditional Disruption of the Peroxisome Proliferator-Activated Receptor {gamma} Gene in Mice Results in Lowered Expression of ABCA1, ABCG1, and apoE in Macrophages and Reduced Cholesterol Efflux
Mol. Cell. Biol., April 15, 2002; 22(8): 2607 - 2619.
[Abstract] [Full Text] [PDF]

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 GutHome page
M Toyoda, H Takagi, N Horiguchi, S Kakizaki, K Sato, H Takayama, and M Mori
A ligand for peroxisome proliferator activated receptor {gamma} inhibits cell growth and induces apoptosis in human liver cancer cells
Gut, April 1, 2002; 50(4): 563 - 567.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Gastrointest. Liver Physiol.Home page
J. Auwerx
Nuclear Receptors: I. PPARgamma in the gastrointestinal tract: gain or pain?
Am J Physiol Gastrointest Liver Physiol, April 1, 2002; 282(4): G581 - G585.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
L. Kopelovich, J. R. Fay, R. I. Glazer, and J. A. Crowell
Peroxisome Proliferator-activated Receptor Modulators As Potential Chemopreventive Agents
Mol. Cancer Ther., March 1, 2002; 1(5): 357 - 363.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
A. Diab, C. Deng, J. D. Smith, R. Z. Hussain, B. Phanavanh, A. E. Lovett-Racke, P. D. Drew, and M. K. Racke
Peroxisome Proliferator-Activated Receptor-{gamma} Agonist 15-Deoxy-{Delta}12,1412,14-Prostaglandin J2 Ameliorates Experimental Autoimmune Encephalomyelitis
J. Immunol., March 1, 2002; 168(5): 2508 - 2515.
[Abstract] [Full Text] [PDF]

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 Toxicol SciHome page
E. M. Wauson, A. S. Langan, and R. L. Vorce
Sodium Arsenite Inhibits and Reverses Expression of Adipogenic and Fat Cell-Specific Genes during in Vitro Adipogenesis
Toxicol. Sci., February 1, 2002; 65(2): 211 - 219.
[Abstract] [Full Text] [PDF]

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 CarcinogenesisHome page
K. Berge, K. J. Tronstad, E. N. Flindt, T. H. Rasmussen, L. Madsen, K. Kristiansen, and R. K. Berge
Tetradecylthioacetic acid inhibits growth of rat glioma cells ex vivo and in vivo via PPAR-dependent and PPAR-independent pathways
Carcinogenesis, November 1, 2001; 22(11): 1747 - 1755.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
I. TEGEDER, J. PFEILSCHIFTER, and G. GEISSLINGER
Cyclooxygenase-independent actions of cyclooxygenase inhibitors
FASEB J, October 1, 2001; 15(12): 2057 - 2072.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. S. Palakurthi, H. Aktas, L. M. Grubissich, R. M. Mortensen, and J. A. Halperin
Anticancer Effects of Thiazolidinediones Are Independent of Peroxisome Proliferator-activated Receptor {gamma} and Mediated by Inhibition of Translation Initiation
Cancer Res., August 1, 2001; 61(16): 6213 - 6218.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
K.-i. Nakashiro, Y. Hayashi, A. Kita, T. Tamatani, A. Chlenski, N. Usuda, K. Hattori, J. K. Reddy, and R. Oyasu
Role of Peroxisome Proliferator-Activated Receptor {gamma} and Its Ligands in Non-Neoplastic and Neoplastic Human Urothelial Cells
Am. J. Pathol., August 1, 2001; 159(2): 591 - 597.
[Abstract] [Full Text]

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 Cancer Res.Home page
T. Ikezoe, C. W. Miller, S. Kawano, A. Heaney, E. A. Williamson, J. Hisatake, E. Green, W. Hofmann, H. Taguchi, and H. P. Koeffle
Mutational Analysis of the Peroxisome Proliferator-activated Receptor {{gamma}} Gene in Human Malignancies
Cancer Res., July 1, 2001; 61(13): 5307 - 5310.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
K. Ohta, T. Endo, K. Haraguchi, J. M. Hershman, and T. Onaya
Ligands for Peroxisome Proliferator-Activated Receptor {{gamma}} Inhibit Growth and Induce Apoptosis of Human Papillary Thyroid Carcinoma Cells
J. Clin. Endocrinol. Metab., May 1, 2001; 86(5): 2170 - 2177.
[Abstract] [Full Text]

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 Pharmacol. Rev.Home page
S. C. Dixon, K. B. Knopf, and W. D. Figg
The Control of Prostate-Specific Antigen Expression and Gene Regulation by Pharmacological Agents
Pharmacol. Rev., March 1, 2001; 53(1): 73 - 92.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
R. Pili, M. P. Kruszewski, B. W. Hager, J. Lantz, and M. A. Carducci
Combination of Phenylbutyrate and 13-cis Retinoic Acid Inhibits Prostate Tumor Growth and Angiogenesis
Cancer Res., February 1, 2001; 61(4): 1477 - 1485.
[Abstract] [Full Text]

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 ANN INTERN MEDHome page
A. A. Parulkar, M. L. Pendergrass, R. Granda-Ayala, T. R. Lee, and V. A. Fonseca
Nonhypoglycemic Effects of Thiazolidinediones
Ann Intern Med, January 2, 2001; 134(1): 61 - 71.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. B. Shappell, R. A. Gupta, S. Manning, R. Whitehead, W. E. Boeglin, C. Schneider, T. Case, J. Price, G. S. Jack, T. M. Wheeler, et al.
15S-Hydroxyeicosatetraenoic Acid Activates Peroxisome Proliferator-activated Receptor {{gamma}} and Inhibits Proliferation in PC3 Prostate Carcinoma Cells
Cancer Res., January 1, 2001; 61(2): 497 - 503.
[Abstract] [Full Text]

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 Clin. Cancer Res.Home page
S. W. Han, M. E. Greene, J. Pitts, R. K. Wada, and N. Sidell
Novel Expression and Function of Peroxisome Proliferator-activated Receptor Gamma (PPAR{{gamma}}) in Human Neuroblastoma Cells
Clin. Cancer Res., January 1, 2001; 7(1): 98 - 104.
[Abstract] [Full Text]

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 ChestHome page
K.-i. Inoue, Y. Kawahito, and H. Sano
Endothelial Apoptosis
Chest, December 1, 2000; 118(6): 1839 - 1839.
[Full Text] [PDF]

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 Cancer Res.Home page
K. Izuishi, K. Kato, T. Ogura, T. Kinoshita, and H. Esumi
Remarkable Tolerance of Tumor Cells to Nutrient Deprivation: Possible New Biochemical Target for Cancer Therapy
Cancer Res., November 1, 2000; 60(21): 6201 - 6207.
[Abstract] [Full Text]

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 Cancer Res.Home page
J.-i. Hisatake, T. Ikezoe, M. Carey, S. Holden, S. Tomoyasu, and H. P. Koeffler
Down-Regulation of Prostate-specific Antigen Expression by Ligands for Peroxisome Proliferator-activated Receptor {{gamma}} in Human Prostate Cancer
Cancer Res., October 1, 2000; 60(19): 5494 - 5498.
[Abstract] [Full Text]

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 Cancer Res.Home page
W. Motomura, T. Okumura, N. Takahashi, T. Obara, and Y. Kohgo
Activation of Peroxisome Proliferator-activated Receptor {{gamma}} by Troglitazone Inhibits Cell Growth through the Increase of p27Kip1 in Human Pancreatic Carcinoma Cells
Cancer Res., October 1, 2000; 60(19): 5558 - 5564.
[Abstract] [Full Text]

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 ScienceHome page
T. G. Kroll, P. Sarraf, L. Pecciarini, C.-J. Chen, E. Mueller, B. M. Spiegelman, and J. A. Fletcher
PAX8-PPARgamma 1 Fusion in Oncogene Human Thyroid Carcinoma
Science, August 25, 2000; 289(5483): 1357 - 1360.
[Abstract] [Full Text]

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 Cell Growth Differ.Home page
S. J. Muga, P. Thuillier, A. Pavone, J. E. Rundhaug, W. E. Boeglin, M. Jisaka, A. R. Brash, and S. M. Fischer
8S-Lipoxygenase Products Activate Peroxisome Proliferator-activated Receptor {{alpha}} and Induce Differentiation in Murine Keratinocytes
Cell Growth Differ., August 1, 2000; 11(8): 447 - 454.
[Abstract] [Full Text]

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 Cancer Res.Home page
F. A. Attiga, P. M. Fernandez, A. T. Weeraratna, M. J. Manyak, and S. R. Patierno
Inhibitors of Prostaglandin Synthesis Inhibit Human Prostate Tumor Cell Invasiveness and Reduce the Release of Matrix Metalloproteinases
Cancer Res., August 1, 2000; 60(16): 4629 - 4637.
[Abstract] [Full Text]


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