JNK- and Akt-mediated Puma expression in the apoptosis of cisplatin-resistant ovarian cancer cells

Biochemical Journal

Volumn 444, Issue 2, 2012, Pages 291-301

  Zhao, Zhiwei ^a   Wang, Jingjing ^a   Tang, Jingsheng ^b   Liu, Xinyu ^a   Zhong, Qian ^c   Wang, Fang ^a   Hu, Wenbin ^a   Yuan, Zhu ^a   Nie, Chunlai ^a   Wei, Yuquan ^a  

^a SICHUAN UNIVERSITY   (China)

^b ChongQing NewFine Biology Technology   (China)

^c SICHUAN UNIVERSITY   (China)

Author keywords

Akt dephosphorylation; c Jun N terminal kinase (JNK) activation; Cisplatin resistant; Ovarian cancer; Puma

Indexed keywords

BETULIC ACID; CISPLATIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; PROTEIN BAX; PROTEIN KINASE B; PUMA PROTEIN;

APOPTOSIS; ARTICLE; CANCER CELL; CELL DEATH; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RNA TRANSPORT;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL LINE, TUMOR; CISPLATIN; DRUG RESISTANCE, NEOPLASM; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; OVARIAN NEOPLASMS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 84860847695     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111855     Document Type: Article

References (43)

1. Jemal, A., Siegel, R., Ward, E., Murray, T., Xu, J., Smigal, C. and Thun, M. J. (2006) Cancer statistics, 2006. Ca-Cancer J. Clin. 56, 106-130
2. Pisha, E., Chai, H., Lee, I. S., Chagwedera, T. E., Farnsworth, N. R., Cordell, G. A., Beecher, C. W., Fong, H. H., Kinghorn, A. D., Brown, D. M. et al. (1995) Discovery of betulinic acid as a selective inhibitor of human melanoma that functions by induction of apoptosis. Nat. Med. 1, 1046-1051
3. Kessler, J. H., Mullauer, F. B., de Roo, G. M. and Medema, J. P. (2007) Broad in vitro efficacy of plant-derived betulinic acid against cell lines derived from the most prevalent human cancer types. Cancer Lett. 251, 132-145 (Pubitemid 46589768)
4. Fulda, S., Susin, S. A., Kroemer, G. and Debatin, K. M. (1998) Molecular ordering of apoptosis induced by anticancer drugs in neuroblastoma cells. Cancer Res. 58, 4453-4460 (Pubitemid 28450051)
5. Fulda, S. and Debatin, K. M. (2005) Sensitization for anticancer drug-induced apoptosis by betulinic acid. Neoplasia 7, 162-170 (Pubitemid 40315993)
6. Fulda, S., Friesen, C., Los, M., Scaffidi, C., Mier, W., Benedict, M., Nunez, G., Krammer, P. H., Peter, M. E. and Debatin, K. M. (1997) Betulinic acid triggers CD95 (APO-1/Fas)-and p53-independent apoptosis via activation of caspases in neuroectodermal tumors. Cancer Res. 57, 4956-4964 (Pubitemid 27469008)
7. Adams, J. M. and Cory, S. (2007) The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 26, 1324-1337 (Pubitemid 46328466)
8. Siddik, Z. H. (2003) Cisplatin: mode of cytotoxic action and molecular basis of resistance. Oncogene 22, 7265-7279
9. Villedieu, M., Louis, M. H., Dutoit, S., Brotin, E., Lincet, H., Duigou, F., Staedel, C., Gauduchon, P. and Poulain, L. (2007) Absence of Bcl-xL down-regulation in response to cisplatin is associated with chemoresistance in ovarian carcinoma cells. Gynecol. Oncol. 105, 31-44 (Pubitemid 46441466)
10. Marone, M., Scambia, G., Mozzetti, S., Ferrandina, G., Iacovella, S., De Pasqua, A., Benedetti-Panici, P. and Mancuso, S. (1998) Bcl-2, Bax, Bcl-XL, and Bcl-XS expression in normal and neoplastic ovarian tissues. Clin. Cancer Res. 4, 517-524 (Pubitemid 28122771)
11. Yu, J., Wang, Z., Kinzler, K. W., Vogelstein, B. and Zhang, L. (2003) PUMA mediates the apoptotic response to p53 in colorectal cancer cells. Proc. Natl. Acad. Sci. U.S.A. 100, 1931-1936 (Pubitemid 36254551)
12. Yu, J., Wang, P., Ming, L., Wood, M. A. and Zhang, L. (2007) SMAC/Diablo mediates the proapoptotic function of PUMA by regulating PUMA-induced mitochondrial events. Oncogene 26, 4189-4198 (Pubitemid 46975795)
13. Fraser, M., Bai, T. and Tsang, B. K. (2008) Akt promotes cisplatin resistance in human ovarian cancer cells through inhibition of p53 phosphorylation and nuclear function. Int. J. Cancer 122, 534-546 (Pubitemid 350308944)
14. Chen, K. F., Yeh, P. Y., Yeh, K. H., Lu, Y. S., Huang, S. Y. and Cheng, A. L. (2008) Down-regulation of phospho-Akt is a major molecular determinant of bortezomib-induced apoptosis in hepatocellular carcinoma cells. Cancer Res. 68, 6698-6707
15. Yuan, Z., Cao, K., Lin, C., Li, L., Liu, H. Y., Zhao, X. Y., Liu, L., Deng, H. X., Li, J., Nie, C. L. and Wei, Y. Q. (2011) PUMA chemosensitizes intrinsically resistant ovarian cancer cells to cisplatin by lowering the threshold set by Bcl-xL and Mcl-1. Mol. Med. 17, 1262-1274
16. Godwin, A. K., Meister, A., O'Dwyer, P. J., Huang, C. S., Hamilton, T. C. and Anderson, M. E. (1992) High resistance to cisplatin in human ovarian cancer cell lines is associated with marked increase of glutathione synthesis. Proc. Natl. Acad. Sci. U.S.A. 89, 3070-3074
17. Yuan, Z., Liu, H., Yan, F., Wang, Y., Gou, L., Nie, C., Ding, Z., Lai, S., Zhao, Y., Zhao, X. et al. (2009) Improved therapeutic efficacy against murine carcinoma by combining honokiol with gene therapy of PNAS-4, a novel pro-apoptotic gene. Cancer Sci. 100, 1757-1766
18. Nie, C., Tian, C., Zhao, L., Petit, P. X., Mehrpour, M. and Chen, Q. (2008) Cysteine 62 of Bax is critical for its conformational activation and its proapoptotic activity in response to H2O2-induced apoptosis. J. Biol. Chem. 283, 15359-15369
19. Hu, W., Wang, F., Tang, J., Liu, X., Yuan, Z., Nie, C. and Wei, Y. (2012) Pro-apoptotic protein, Smac, mediates apoptosis in cisplatin-resistant ovarian cancer cells when treated with the anti-tumor agent, At101. J. Biol. Chem. 287, 68-80
20. Hauck, L., Harms, C., Grothe, D., An, J., Gertz, K., Kronenberg, G., Dietz, R., Endres, M. and von Harsdorf, R. (2007) Critical role for FoxO3a-dependent regulation of p21CIP1/WAF1 in response to statin signaling in cardiac myocytes. Circ. Res. 100, 50-60 (Pubitemid 46066773)
21. Cazanave, S. C., Mott, J. L., Elmi, N. A., Bronk, S. F., Werneburg, N. W., Akazawa, Y., Kahraman, A., Garrison, S. P., Zambetti, G. P., Charlton, M. R. and Gores, G. J. (2009) JNK1-dependent PUMA expression contributes to hepatocyte lipoapoptosis. J. Biol. Chem. 284, 26591-26602
22. Yuan, Z., Wang, F., Zhao, Z., Zhao, X., Qiu, J., Nie, C. and Wei, Y. (2011) BIM-mediated Akt phosphorylation is a key modulator of arsenic trioxide-induced apoptosis in cisplatin-sensitive and -resistant ovarian cancer cells. PLoS ONE 6, e20586
23. Tacka, K. A., Szalda, D., Souid, A. K., Goodisman, J. and Dabrowiak, J. C. (2004) Experimental and theoretical studies on the pharmacodynamics of cisplatin in Jurkat cells. Chem. Res. Toxicol. 17, 1434-1444 (Pubitemid 39532312)
24. Rudin, C. M., Yang, Z., Schumaker, L. M., VanderWeele, D. J., Newkirk, K., Egorin, M. J., Zuhowski, E. G. and Cullen, K. J. (2003) Inhibition of glutathione synthesis reverses Bcl-2-mediated cisplatin resistance. Cancer Res. 63, 312-318 (Pubitemid 36152486)
25. Williams, J., Lucas, P. C., Griffith, K. A., Choi, M., Fogoros, S., Hu, Y. Y. and Liu, J. R. (2005) Expression of Bcl-xL in ovarian carcinoma is associated with chemoresistance and recurrent disease. Gynecol. Oncol. 96, 287-295 (Pubitemid 40127123)
26. Simonin, K., Brotin, E., Dufort, S., Dutoit, S., Goux, D., N'Diaye, M., Denoyelle, C., Gauduchon, P. and Poulain, L. (2009) Mcl-1 is an important determinant of the apoptotic response to the BH3-mimetic molecule HA14-1 in cisplatin-resistant ovarian carcinoma cells. Mol. Cancer Ther. 8, 3162-3170
27. Fulda, S. (2008) Betulinic acid for cancer treatment and prevention. Int. J. Mol. Sci. 9, 1096-1107
28. Selzer, E., Pimentel, E., Wacheck, V., Schlegel, W., Pehamberger, H., Jansen, B. and Kodym, R. (2000) Effects of betulinic acid alone and in combination with irradiation in human melanoma cells. J. Invest. Dermatol. 114, 935-940 (Pubitemid 30252714)
29. Selzer, E., Thallinger, C., Hoeller, C., Oberkleiner, P., Wacheck, V., Pehamberger, H. and Jansen, B. (2002) Betulinic acid-induced Mcl-1 expression in human melanoma: mode of action and functional significance. Mol. Med. 8, 877-884 (Pubitemid 36223142)
30. Villunger, A., Michalak, E. M., Coultas, L., Mullauer, F., Bock, G., Ausserlechner, M. J., Adams, J. M. and Strasser, A. (2003) p53- and drug-induced apoptotic responses mediated by BH3-only proteins Puma and Noxa. Science 302, 1036-1038 (Pubitemid 37386194)
31. Cregan, S. P., Arbour, N. A., Maclaurin, J. G., Callaghan, S. M., Fortin, A., Cheung, E. C., Guberman, D. S., Park, D. S. and Slack, R. S. (2004) p53 activation domain 1 is essential for PUMA upregulation and p53-mediated neuronal cell death. J. Neurosci. 24, 10003-10012 (Pubitemid 39463582)
32. Nakano, K. and Vousden, K. H. (2001) PUMA, a novel proapoptotic gene, is induced by p53. Mol. Cell 7, 683-694 (Pubitemid 32706359)
33. Siddik, Z. H., Mims, B., Lozano, G. and Thai, G. (1998) Independent pathways of p53 induction by cisplatin and X-rays in a cisplatin-resistant ovarian tumor cell line. Cancer Res. 58, 698-703 (Pubitemid 28099480)
34. Shaw, T. J., Lacasse, E. C., Durkin, J. P. and Vanderhyden, B. C. (2008) Downregulation of XIAP expression in ovarian cancer cells induces cell death in vitro and in vivo. Int. J. Cancer 122, 1430-1434 (Pubitemid 351287247)
35. You, H., Pellegrini, M., Tsuchihara, K., Yamamoto, K., Hacker, G., Erlacher, M., Villunger, A. and Mak, T. W. (2006) FOXO3a-dependent regulation of Puma in response to cytokine/growth factor withdrawal. J. Exp. Med. 203, 1657-1663 (Pubitemid 44036270)
36. Rieber, M. and Rieber, M. S. (2006) Signalling responses linked to betulinic acid-induced apoptosis are antagonized by MEK inhibitor U0126 in adherent or 3D spheroid melanoma irrespective of p53 status. Int. J. Cancer 118, 1135-1143 (Pubitemid 43185599)
37. She, Q. B., Solit, D. B., Ye, Q., O'Reilly, K. E., Lobo, J. and Rosen, N. (2005) The BAD protein integrates survival signaling by EGFR/MAPK and PI3K/Akt kinase pathways in PTEN-deficient tumor cells. Cancer Cell 8, 287-297 (Pubitemid 41443414)
38. Sunters, A., Madureira, P. A., Pomeranz, K. M., Aubert, M., Brosens, J. J., Cook, S. J., Burgering, B. M., Coombes, R. C. and Lam, E. W. (2006) Paclitaxel-induced nuclear translocation of FOXO3a in breast cancer cells is mediated by c-Jun NH2-terminal kinase and Akt. Cancer Res. 66, 212-220 (Pubitemid 43166027)
39. Whitfield, J., Neame, S. J., Paquet, L., Bernard, O. and Ham, J. (2001) Dominant-negative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron 29, 629-643 (Pubitemid 32323937)
40. Eferl, R., Ricci, R., Kenner, L., Zenz, R., David, J. P., Rath, M. and Wagner, E. F. (2003) Liver tumor development. c-Jun antagonizes the proapoptotic activity of p53. Cell 112, 181-192 (Pubitemid 36144108)
41. Valis, K., Prochazka, L., Boura, E., Chladova, J., Obsil, T., Rohlena, J., Truksa, J., Dong, L. F., Ralph, S. J. and Neuzil, J. (2011) Hippo/Mst1 stimulates transcription of the proapoptotic mediator NOXA in a FoxO1-dependent manner. Cancer Res. 71, 946-954
42. Wong, H. K., Fricker, M., Wyttenbach, A., Villunger, A., Michalak, E. M., Strasser, A. and Tolkovsky, A. M. (2005) Mutually exclusive subsets of BH3-only proteins are activated by the p53 and c-Jun N-terminal kinase/c-Jun signaling pathways during cortical neuron apoptosis induced by arsenite. Mol. Cell Biol. 25, 8732-8747 (Pubitemid 41369190)
43. Wang, J., Zhou, J. Y. and Wu, G. S. (2011) Bim protein degradation contributes to cisplatin resistance. J. Biol. Chem. 286, 22384-22392