NOXA-induced alterations in the Bax/Smac Axis enhance sensitivity of ovarian cancer cells to cisplatin

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Lin, Chao ^a   Zhao, Xin yu ^a   Li, Lei ^a   Liu, Huan yi ^b   Cao, Kang ^c   Wan, Yang ^a   Liu, Xin yu ^a   Nie, Chun lai ^a   Liu, Lei ^a   Tong, Ai ping ^a   Deng, Hong xin ^a   Li, Jiong ^a   Yuan, Zhu ^a   Wei, Yu quan ^a  

^a SICHUAN UNIVERSITY   (China)

^b CHENGDU MILITARY GENERAL HOSPITAL   (China)

^c CHENGDU MEDICAL COLLEGE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CISPLATIN; LIPOSOME; PLASMID DNA; PROTEIN BCL 2; PROTEIN NOXA; PROTEIN P53; RECOMBINANT PROTEIN NOXA; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; BAX PROTEIN, HUMAN; DIABLO PROTEIN, HUMAN; MITOCHONDRIAL PROTEIN; PMAIP1 PROTEIN, HUMAN; PROTEIN BAX; SIGNAL PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CELL COUNT; CELL GROWTH; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSOL; DRUG SENSITIVITY; GENE SILENCING; GENETIC VARIABILITY; HUMAN; HUMAN CELL; LIPOSOMAL GENE DELIVERY SYSTEM; MOUSE; NONHUMAN; OVARY CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; TREATMENT RESPONSE; UPREGULATION; ANIMAL; CANCER TRANSPLANTATION; DRUG EFFECT; DRUG SCREENING; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUDE MOUSE; OVARY TUMOR; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE, TUMOR; CISPLATIN; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, NUDE; MITOCHONDRIAL PROTEINS; NEOPLASM TRANSPLANTATION; OVARIAN NEOPLASMS; PROTO-ONCOGENE PROTEINS C-BCL-2; TRANSPLANTATION, HETEROLOGOUS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84860772981     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036722     Document Type: Article

References (44)

1. Salzberg M, Thurlimann B, Bonnefois H, Fink D, Rochlitz C, et al. (2005) Current concepts of treatment strategies in advanced or recurrent ovarian cancer. Oncology 68: 293-298.
2. Folkman J, (1995) Seminars in medicine of the Beth Israel Hospital, Boston: Clinical applications of research on angiogenesis. N Engl J Med 333: 1757-1763.
3. Johnstone RW, Ruefli AA, Lowe SW, (2002) Apoptosis: a link between cancer genetics and chemotherapy. Cell 108: 153-164.
4. Yu J, Zhang L, (2004) Apoptosis in human cancer cells. Curr Opin Oncol 16: 19-24.
5. Reles A, Wen WH, Schmider A, Gee C, Runnebaum IB, et al. (2001) Correlation of p53 Mutations with Resistance to Platinum-based Chemotherapy and Shortened Survival in Ovarian Cancer. Clin cancer Res 7: 2984-2997.
6. Al-Bahlani S, Fraser M, Wong AY, Sayan BS, Bergeron R, et al. (2011) P73 regulates cisplatin-induced apoptosis in ovarian cancer cells via a calcium/calpain-dependent mechanism, Oncogene 30: 4219-4230.
7. Muscolini M, Cianfrocca R, Sajeva A, Mozzetti S, Ferrandina G, et al. (2008) Trichostatin A up-regulates p73 and induces Bax-dependent apoptosis in cisplatin-resistant ovarian cancer cells, Mol Cancer Ther 7: 1410-1419.
8. Ibrahim N, He L, Leong CO, Xing D, Karlan BY, et al. (2010) BRCA1-Associated Epigenetic Regulation of p73 Mediates an Effector Pathway for Chemosensitivity in Ovarian Carcinoma, Cancer Res 70: 7155-7165.
9. Seo YW, Shin JN, Ko KH, Cha JH, Park JY, et al. (2003) The molecular mechanism of Noxa-induced mitochondrial dysfunction in p53-mediated cell death. J Biol Chem 278: 48292-48299.
10. Oda E, Ohki R, Murasawa H, Nemoto J, Shibue T, et al. (2000) Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 288: 1053-1058.
11. Hassan M, Alaoui A, Feyen O, Mirmohammadsadegh A, Essmann F, et al. (2008) The BH3-only member Noxa causes apoptosis in melanoma cells by multiple pathways. Oncogene 27: 4557-4568.
12. Suzuki S, Nakasato M, Shibue T, Koshima I, Taniguchi T, (2009) Therapeutic potential of proapoptotic molecule Noxa in the selective elimination of tumor cells. Cancer Sci 100: 759-769.
13. Debernardis D, Siré EG, De Feudis P, Vikhanskaya F, Valenti M, et al. (1997) p53 status does not affect sensitivity of human ovarian cancer cell lines to paclitaxel. Cancer Res. 57: 870-874.
14. De Feudis P, Debernardis D, Beccaglia P, Valenti M, Graniela Siré E, et al. (1997) DDP-induced cytotoxicity is not influenced by p53 in nine human ovarian cancer cell lines with different p53 status, Br J Cancer. 76: 474-479.
15. Gallardo D, Drazan KE, McBride WH, (1996) Adenovirus-based transfer of wild-type p53 gene increases ovarian tumor radiosensitivity. Cancer Res 56: 4891-4893.
16. Villedieu M, Louis MH, Dutoit S, Brotin E, Lincet H, et al. (2007) Absence of Bcl-xL down-regulation in response to cisplatin is associated with chemoresistance in ovarian carcinoma cells. Gynecol Oncol 105: 31-44.
17. Sasaki H, Sheng Y, Kotsuji F, Tsang BK, (2000) Down-regulation of X-linked inhibitor of apoptosis protein induces apoptosis in chemoresistant human ovarian cancer cells. Cancer Res 60: 5659-5666.
18. Williams J, Lucas PC, Griffith KA, Choi M, Fogoros S, et al. (2005) Expression of Bcl-xL in ovarian carcinoma is associated with chemoresistance and recurrent disease. Gynecol Oncol 96: 287-295.
19. Yuan Z, Liu H, Yan F, Wang Y, Gou L, 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.
20. Hu W, Wang F, Tang J, Liu X, Yuan Z, et al. (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.
21. Blezinger P, Wang J, Gondo M, Quezada A, Mehrens D, et al. (1999) Systemic inhibition of tumor growth and tumor metastases by intramuscular administration of the endostatin gene. Nat Biotechnol 17: 343-348.
22. Chen KF, Yeh PY, Yeh KH, Lu YS, Huang SY, et al. (2008) Down-regulation of phospho-Akt is a major molecular determinant of bortezomib-induced apoptosis in hepatocellular carcinoma cells. Cancer Res 68: 6698-6707.
23. Wei YQ, Zhao X, Kariya Y, Fukata H, Teshigawara K, et al. (1994) Induction of apoptosis by quercetin: involvement of heat shock protein. Cancer Res 54: 4952-4957.
24. Ruiz-Vela A, Opferman JT, Cheng EH, Korsmeyer SJ, (2005) Proapoptotic BAX and BAK control multiple initiator caspases. EMBO Rep 6: 379-385.
25. Leu JI, Dumont P, Hafey M, Murphy ME, George DL, (2004) Mitochondrial p53 activates Bak and causes disruption of a Bak-Mcl1 complex. Nat Cell Biol 6: 443-450.
26. Sauter BV, Martinet O, Zhang WJ, Mandeli J, Woo SL, (2000) Adenovirus-mediated gene transfer of endostatin in vivo results in high level of transgene expression and inhibition of tumor growth and metastases. Proc Natl Acad Sci U S A 97: 4802-4807.
27. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, et al. (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2: 183-192.
28. Daniel NN, Korsmeyer SJ, (2004) Cell death: critical control points. Cell 116: 205-219.
29. Labi V, Erlacher M, Kiessling S, Villunger A, (2006) BH3-only proteins in cell death ignition, malignant disease and anticancer therapy. Cell Death Diff 13: 1325-1338.
30. Kassim SK, Ali HS, Sallam MM, Fayed ST, Seada LS, et al. (1999) Increased bcl-2 expression is associated with primary resistance to chemotherapy in human epithelial ovarian cancer. Clin Biochem 32: 333-338.
31. Liu JR, Fletcher B, Page C, Hu C, Nunez G, et al. (1998) Bcl-xL is expressed in ovarian carcinoma and modulates chemoterapy-induced apoptosis. Gynecol Oncol 70: 398-403.
32. Dodier P, Piché A, (2006) Bcl-X(L) is functionally non-equivalent for the regulation of growth and survival in human ovarian cancer cells. Gynecol Oncol 100: 254-63.
33. Perego P, Giarola M, Righetti SC, Supino R, Caserini C, et al. (1996) Association between cisplatin resistance and mutation of p53 gene and reduced bax expression in ovarian carcinoma cell systems, Cancer Res. 56: 556-562.
34. Simonin K, Brotin E, Dufort S, Dutoit S, Goux D, et al. (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.
35. Yang Z, Schumaker LM, Egorin MJ, Zuhowski EG, Guo Z, et al. (2006) Cisplatin preferentially binds mitochondrial DNA and voltage-dependent anion channel protein in the mitochondrial membrane of head and neck squamous cell carcinoma: possible role in apoptosis. Clin Cancer Res 12: 5817-5825.
36. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, et al. (1997) Cytochrome C and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489.
37. Asselin E, Mills GB, Tsang BK, (2001) XIAP regulates Akt activity and caspase-3-dependent cleavage during cisplatin-induced apoptosis in human ovarian epithelial cancer cells. Cancer Res 61: 1862-1868.
38. Henkels KM, Turchi JJ, (1999) Cisplatin-induced apoptosis proceeds by caspase-3-dependent and-independent pathways in cisplatin-resistant and-sensitive human ovarian cancer cell lines. Cancer Res 59: 3077-3083.
39. Deng Y, Lin Y, Wu X, (2002) TRAIL-induced apoptosis requires Bax-dependent mitochondrial release of Smac/DIABLO. Genes Dev 16: 33-45.
40. Zhang L, Yu J, Park BH, Kinzler KW, Vogelstein B, (2000) Role of BAX in the apoptotic response to anticancer agents. Science 290: 989-992.
41. Yu J, Wang P, Ming L, Wood MA, Zhang L, (2007) SMAC/Diablo mediates the proapoptotic function of PUMA by regulating PUMA-induced mitochondrial events, Oncogene 26: 4189-4198.
42. Yang X, Fraser M, Moll UM, Basak A, Tsang BK, (2006) Akt-mediated cisplatin resistance in ovarian cancer: modulation of p53 action on caspase-dependent mitochondrial death pathway, Cancer Res 66: 3126-3136.
43. Fulda S, Wick W, Weller M, Debatin KM, (2002) Smac agonists sensitize for Apo2L/TRAIL- or anticancer druginduced apoptosis and induce regression of malignant glioma in vivo. Nat Med 8: 808-815.
44. Li L, Thomas RM, Suzuki H, De Brabander JK, Wang X, et al. (2004) A small molecule Smac mimic potentiates TRAIL- and TNF alpha-mediated cell death. Science 305: 1471-1474.