A role for peroxisome proliferator-activated receptor gamma in resveratrol-induced colon cancer cell apoptosis

Molecular Nutrition and Food Research

Volumn 58, Issue 9, 2014, Pages 1785-1794

  Aires, Virginie ^a,b   Brassart, Bertrand ^c   Carlier, Annie ^c   Scagliarini, Alessandra ^a,b   Mandard, Stéphane ^a,b   Limagne, Emeric ^a,b   Solary, Eric ^d   Martiny, Laurent ^c   Tarpin, Michel ^c   Delmas, Dominique ^a,b  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b Institut Médical de Génétique et d Immunologie   (France)

^c UNIVERSITÉ DE REIMS CHAMPAGNE ARDENNE   (France)

^d INSERM   (France)

Author keywords

Apoptosis; Cell proliferation; Colon cancer; Polyphenols; PPAR; Resveratrol

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; 2-CHLORO-5-NITROBENZANILIDE; ANILIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RESVERATROL; ROSIGLITAZONE; STILBENE DERIVATIVE;

AGONISTS; ANTAGONISTS AND INHIBITORS; APOPTOSIS; CELL PROLIFERATION; COLONIC NEOPLASMS; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; PATHOLOGY; S PHASE CELL CYCLE CHECKPOINT; TUMOR CELL LINE;

ANILIDES; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; COLONIC NEOPLASMS; HUMANS; PPAR GAMMA; S PHASE CELL CYCLE CHECKPOINTS; STILBENES; THIAZOLIDINEDIONES;

EID: 84908220264     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201300962     Document Type: Article

References (43)

1. Lin, I. H., Ho, M. L., Chen, H. Y., Lee, H. S. et al., Smoking, green tea consumption, genetic polymorphisms in the insulin-like growth factors and lung cancer risk. PLoS One 2012, 7, e30951.
2. Sun, C. L., Yuan, J. M., Koh, W. P., Yu, M. C., Green tea, black tea and breast cancer risk: a meta-analysis of epidemiological studies. Carcinogenesis 2006, 27, 1310-1315.
3. Surh, Y. J., Cancer chemoprevention with dietary phytochemicals. Nat. Rev. Cancer 2003, 3, 768-780.
4. Renaud, S. C., Gueguen, R., Schenker, J., d'Houtaud, A., Alcohol and mortality in middle-aged men from eastern France. Epidemiology 1998, 9, 184-188.
5. Delmas, D., Solary, E., Latruffe, N., Resveratrol, a phytochemical inducer of multiple cell death pathways: apoptosis, autophagy and mitotic catastrophe. Curr. Med. Chem. 2011, 18, 1100-1121.
6. Baur, J. A., Sinclair, D. A., Therapeutic potential of resveratrol: the in vivo evidence. Nat. Rev. Drug. Discov. 2006, 5, 493-506.
7. Juan, M. E., Alfaras, I., Planas, J. M., Colorectal cancer chemoprevention by trans-resveratrol. Pharmacol. Res. 2012, 65, 584-591.
8. Ulrich, S., Loitsch, S. M., Rau, O., von Knethen, A. et al., peroxisome proliferator-activated receptor {gamma} as a molecular target of resveratrol-induced modulation of polyamine metabolism. Cancer Res. 2006, 66, 7348-7354.
9. Alfaras, I., Juan, M. E., Planas, J. M., trans-Resveratrol reduces precancerous colonic lesions in dimethylhydrazine-treated rats. J. Agric. Food Chem. 2010, 58, 8104-8110.
10. Tessitore, L., Davit, A., Sarotto, I., Caderni, G., Resveratrol depresses the growth of colorectal aberrant crypt foci by affecting bax and p21(CIP) expression. Carcinogenesis 2000, 21, 1619-1622.
11. Patel, K. R., Brown, V. A., Jones, D. J., Britton, R. G. et al., Clinical pharmacology of resveratrol and its metabolites in colorectal cancer patients. Cancer Res. 2010, 70, 7392-7399.
12. Colin, D., Gimazane, A., Lizard, G., Izard, J. C. et al., Effects of resveratrol analogs on cell cycle progression, cell cycle associated proteins and 5fluoro-uracil sensitivity in human derived colon cancer cells. Int. J. Cancer 2009, 124, 2780-2788.
13. Marel, A. K., Lizard, G., Izard, J. C., Latruffe, N. et al., Inhibitory effects of trans-resveratrol analogs molecules on the proliferation and the cell cycle progression of human colon tumoral cells. Mol. Nutr. Food Res. 2008, 52, 538-548.
14. Delmas, D., Rebe, C., Lacour, S., Filomenko, R. et al., Resveratrol-induced apoptosis is associated with Fas redistribution in the rafts and the formation of a death-inducing signaling complex in colon cancer cells. J. Biol. Chem. 2003, 278, 41482-41490.
15. Colin, D., Limagne, E., Jeanningros, S., Jacquel, A. et al., Endocytosis of resveratrol via lipid rafts and activation of downstream signaling pathways in cancer cells. Cancer Prev. Res. 2011, 4, 1095-1106.
16. Gurnell, M., Wentworth, J. M., Agostini, M., Adams, M. et al., A dominant-negative peroxisome proliferator-activated receptor gamma (PPARgamma) mutant is a constitutive repressor and inhibits PPARgamma-mediated adipogenesis. J. Biol. Chem. 2000, 275, 5754-5759.
17. Delmas, D., Passilly-Degrace, P., Jannin, B., Malki, M. C., Latruffe, N., Resveratrol, a chemopreventive agent, disrupts the cell cycle control of human SW480 colorectal tumor cells. Int. J. Mol. Med. 2002, 10, 193-199.
18. Delmas, D., Rebe, C., Micheau, O., Athias, A. et al., Redistribution of CD95, DR4 and DR5 in rafts accounts for the synergistic toxicity of resveratrol and death receptor ligands in colon carcinoma cells. Oncogene 2004, 23, 8979-8986.
19. Aires, V., Limagne, E., Cotte, A. K., Latruffe, N. et al., Resveratrol metabolites inhibit human metastatic colon cancer cells progression and synergize with chemotherapeutic drugs to induce cell death. Mol. Nutr. Food Res. 2013, 57, 170-181.
20. Delmas, D., Jannin, B., Malki, M. C., Latruffe, N., Inhibitory effect of resveratrol on the proliferation of human and rat hepatic derived cell lines. Oncol. Rep. 2000, 7, 847-852.
21. Seargent, J. M., Yates, E. A., Gill, J. H., GW9662, a potent antagonist of PPARgamma, inhibits growth of breast tumour cells and promotes the anticancer effects of the PPARgamma agonist rosiglitazone, independently of PPARgamma activation. Br. J. Pharmacol. 2004, 143, 933-937.
22. Leesnitzer, L. M., Parks, D. J., Bledsoe, R. K., Cobb, J. E. et al., Functional consequences of cysteine modification in the ligand binding sites of peroxisome proliferator activated receptors by GW9662. Biochemistry 2002, 41, 6640-6650.
23. Mueller, E., Smith, M., Sarraf, P., Kroll, T. et al., Effects of ligand activation of peroxisome proliferator-activated receptor gamma in human prostate cancer. Proc. Natl. Acad. Sci. USA 2000, 97, 10990-10995.
24. Cerbone, A., Toaldo, C., Minelli, R., Ciamporcero, E. et al., Rosiglitazone and AS601245 decrease cell adhesion and migration through modulation of specific gene expression in human colon cancer cells. PLoS One 2012, 7, e40149.
25. Jang, M., Cai, L., Udeani, G. O., Slowing, K. V. et al., Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 1997, 275, 218-220.
26. Ahmad, N., Katiyar, S. K., Mukhtar, H., Antioxidants in chemoprevention of skin cancer. Curr. Probl. Dermatol. 2001, 29, 128-139.
27. Kroon, P. A., Iyer, A., Chunduri, P., Chan, V. et al., The cardiovascular nutrapharmacology of resveratrol: pharmacokinetics, molecular mechanisms and therapeutic potential. Curr. Med. Chem. 2010, 17, 2442-2455.
28. Shih, A., Zhang, S., Cao, H. J., Boswell, S. et al., Inhibitory effect of epidermal growth factor on resveratrol-induced apoptosis in prostate cancer cells is mediated by protein kinase C-alpha. Mol. Cancer Ther. 2004, 3, 1355-1364.
29. Lin, H. Y., Shih, A., Davis, F. B., Tang, H. Y. et al., Resveratrol induced serine phosphorylation of p53 causes apoptosis in a mutant p53 prostate cancer cell line. J. Urol. 2002, 168, 748-755.
30. Heaney, A. P., Fernando, M., Melmed, S., PPAR-gamma receptor ligands: novel therapy for pituitary adenomas. J. Clin. Invest. 2003, 111, 1381-1388.
31. Yoshimura, R., Matsuyama, M., Segawa, Y., Hase, T. et al., Expression of peroxisome proliferator-activated receptors (PPARs) in human urinary bladder carcinoma and growth inhibition by its agonists. Int. J. Cancer 2003, 104, 597-602.
32. Michalik, L., Desvergne, B., Wahli, W., Peroxisome-proliferator-activated receptors and cancers: complex stories. Nat Rev. Cancer 2004, 4, 61-70.
33. Peters, J. M., Shah, Y. M., Gonzalez, F. J., The role of peroxisome proliferator-activated receptors in carcinogenesis and chemoprevention. Nat. Rev. Cancer 2012, 12, 181-195.
34. Koeffler, H. P., Peroxisome proliferator-activated receptor gamma and cancers. Clin. Cancer Res. 2003, 9, 1-9.
35. Sarraf, P., Mueller, E., Jones, D., King, F. J. et al., Differentiation and reversal of malignant changes in colon cancer through PPARgamma. Nat. Med. 1998, 4, 1046-1052.
36. Lamers, C., Schubert-Zsilavecz, M., Merk, D., Therapeutic modulators of peroxisome proliferator-activated receptors (PPAR): a patent review (2008-present). Expert Opin. Ther. Pat. 2012, 22, 803-841.
37. Roberts-Thomson, S. J., Peroxisome proliferator-activated receptors in tumorigenesis: targets of tumour promotion and treatment. Immunol. Cell Biol. 2000, 78, 436-441.
38. Bae, M. A., Song, B. J., Critical role of c-Jun N-terminal protein kinase activation in troglitazone-induced apoptosis of human HepG2 hepatoma cells. Mol. Pharmacol. 2003, 63, 401-408.
39. Farrow, B., Evers, B. M., Activation of PPARgamma increases PTEN expression in pancreatic cancer cells. Biochem. Biophys. Res. Commun. 2003, 301, 50-53.
40. Nagamine, M., Okumura, T., Tanno, S., Sawamukai, M. et al., PPAR gamma ligand-induced apoptosis through a p53-dependent mechanism in human gastric cancer cells. Cancer Sci. 2003, 94, 338-343.
41. Zhang, Q., Zhou, H., Zhai, S., Yan, B., Natural product-inspired synthesis of thiazolidine and thiazolidinone compounds and their anticancer activities. Curr. Pharm. Des. 2010, 16, 1826-1842.
42. Wei, S., Yang, J., Lee, S. L., Kulp, S. K. et al., PPARgamma-independent antitumor effects of thiazolidinediones. Cancer Lett. 2009, 276, 119-124.
43. Choi, J. H., Banks, A. S., Kamenecka, T. M., Busby, S. A. et al., Antidiabetic actions of a non-agonist PPARgamma ligand blocking Cdk5-mediated phosphorylation. Nature 2011, 477, 477-481.