Smac modulates chemosensitivity in head and neck cancer cells through the mitochondrial apoptotic pathway

Clinical Cancer Research

Volumn 17, Issue 8, 2011, Pages 2361-2372

  Sun, Quanhong ^a,b   Zheng, Xingnan ^a,b   Zhang, Lin ^a,b   Yu, Jian ^a,b  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CISPLATIN; CYTOCHROME C; FLUOROURACIL; GEMCITABINE; GT A; GT C; INHIBITOR OF APOPTOSIS PROTEIN; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SMAC MIMETIC; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CHEMOSENSITIVITY; CHEMOSENSITIZATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG POTENTIATION; DRUG RESPONSE; ENZYME ACTIVATION; ENZYME RELEASE; FEMALE; GENE; GENE OVEREXPRESSION; GENE SILENCING; HEAD AND NECK CANCER; HUMAN; HUMAN CELL; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL APOPTOTIC PATHWAY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE GENE; TUMOR XENOGRAFT;

ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; BIOMIMETIC MATERIALS; BLOTTING, WESTERN; CASPASE 3; CELL LINE, TUMOR; CYTOCHROMES C; DEOXYCYTIDINE; DRUG SYNERGISM; ENZYME ACTIVATION; FEMALE; HEAD AND NECK NEOPLASMS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, NUDE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 79954623871     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-10-2262     Document Type: Article

References (52)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin 2009;59:225-49.
2. Airoldi M, Cattel L, Cortesina G, Giordano C, Passera R, Pedani F, et al. Gemcitabine and vinorelbine in recurrent head and neck cancer: pharmacokinetic and clinical results. Anticancer Res 2003;23:2845-52. (Pubitemid 36969822)
3. Jiang Y, Wei YQ, Luo F, Zou LQ, Liu JY, Peng F, et al. Gemcitabine and cisplatin in advanced nasopharyngeal carcinoma: a pilot study. Cancer Invest 2005;23:123-8. (Pubitemid 40463909)
4. Aguilar-Ponce J, Granados-García M, Villavicencio V, Poitevin-Chacón A, Green D, Dueñas-González A, et al. Phase II trial of gemcitabine concurrent with radiation for locally advanced squamous cell carcinoma of the head and neck. Ann Oncol 2004;15:301-6. (Pubitemid 38262632)
5. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70. (Pubitemid 30046295)
6. Johnstone RW, Ruefli AA, Lowe SW. Apoptosis: a link between cancer genetics and chemotherapy. Cell 2002;108:153-64. (Pubitemid 34161136)
7. Yu J, Zhang L. Apoptosis in human cancer cells. Curr Opin Oncol 2004;16:19-24. (Pubitemid 38703467)
8. Ragin CC, Modugno F, Gollin SM. The epidemiology and risk factors of head and neck cancer: a focus on human papillomavirus. J Dent Res 2007;86:104-14.
9. Yu J, Zhang L. The transcriptional targets of p53 in apoptosis control. Biochem Biophys Res Commun 2005;331:851-8. (Pubitemid 40615516)
10. Adams JM, Cory S. The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 2007;26:1324-37. (Pubitemid 46328466)
11. Trask DK, Wolf GT, Bradford CR, Fisher SG, Devaney K, Johnson M, et al. Expression of Bcl-2 family proteins in advanced laryngeal squamous cell carcinoma: correlation with response to chemotherapy and organ preservation. Laryngoscope 2002;112:638-44. (Pubitemid 34285929)
12. Kalyankrishna S, Grandis JR. Epidermal growth factor receptor biology in head and neck cancer. J Clin Oncol 2006;24:2666-72. (Pubitemid 46622088)
13. Lippert BM, Knauer SK, Fetz V, Mann W, Stauber RH. Dynamic survivin in head and neck cancer: molecular mechanism and therapeutic potential. Int J Cancer 2007;121:1169-74. (Pubitemid 47293781)
14. Salvesen GS, Duckett CS. IAP proteins: blocking the road to death's door. Nat Rev Mol Cell Biol 2002;3:401-10. (Pubitemid 34685698)
15. Velculescu VE, Madden SL, Zhang L, Lash AE, Yu J, Rago C, et al. Analysis of human transcriptomes. Nat Genet 1999;23:387-8.
16. LaCasse EC, Mahoney DJ, Cheung HH, Plenchette S, Baird S, Korneluk RG. IAP-targeted therapies for cancer. Oncogene 2008;27:6252-75.
17. Du C, Fang M, Li Y, Li L, Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000;102:33-42.
18. Okada H, Suh WK, Jin J, Woo M, Du C, Elia A, et al. Generation and characterization of Smac/DIABLO-deficient mice. Mol Cell Biol 2002;22:3509-17. (Pubitemid 34453989)
19. Bank A, Wang P, Du C, Yu J, Zhang L. SMAC mimetics sensitize nonsteroidal anti-inflammatory drug-induced apoptosis by promoting caspase-3-mediated cytochrome c release. Cancer Res 2008;68:276-84. (Pubitemid 351380129)
20. Oost TK, Sun C, Armstrong RC, Al-Assaad AS, Betz SF, Deckwerth TL, et al. Discovery of potent antagonists of the antiapoptotic protein XIAP for the treatment of cancer. J Med Chem 2004;47:4417-26. (Pubitemid 39096830)
21. Li L, Thomas RM, Suzuki H, De Brabander JK, Wang X, Harran PG. A small molecule Smac mimic potentiates TRAIL-and TNF alpha mediated cell death. Science 2004;305:1471-4. (Pubitemid 39167668)
22. Sun H, Nikolovska-Coleska Z, Yang CY, Xu L, Liu M, Tomita Y, et al. Structure-based design of potent, conformationally constrained Smac mimetics. J Am Chem Soc 2004;126:16686-7. (Pubitemid 40069464)
23. Varfolomeev E, Blankenship JW, Wayson SM, Fedorova AV, Kayagaki N, Garg P, et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell 2007;131:669-81. (Pubitemid 350087204)
24. Vince JE, Wong WW, Khan N, Feltham R, Chau D, Ahmed AU, et al. IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis. Cell 2007;131:682-93. (Pubitemid 350103599)
25. Petersen SL, Wang L, Yalcin-Chin A, Li L, Peyton M, Minna J, et al. Autocrine TNFalpha signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis. Cancer Cell 2007;12:445-56. (Pubitemid 350064365)
26. Wang L, Du F, Wang X. TNF-alpha induces two distinct caspase-8 activation pathways. Cell 2008;133:693-703. (Pubitemid 351636305)
27. Yu J, Wang Z, Kinzler KW, Vogelstein B, Zhang L. PUMA mediates the apoptotic response to p53 in colorectal cancer cells. Proc Natl Acad Sci U S A 2003;100:1931-6. (Pubitemid 36254551)
28. Sun Q, Sakaida T, Yue W, Gollin SM, Yu J. Chemosensitization of head and neck cancer cells by PUMA. Mol Cancer Ther 2007;6:3180-8.
29. Ming L, Wang P, Bank A, Yu J, Zhang L. PUMA dissociates Bax and BCL-XL to induce apoptosis in colon cancer cells. J Biol Chem 2006;281:16034-42. (Pubitemid 43848497)
30. Kohli M, Yu J, Seaman C, Bardelli A, Kinzler KW, Vogelstein B, et al. SMAC/Diablo-dependent apoptosis induced by nonsteroidal anti-inflammatory drugs (NSAIDs) in colon cancer cells. Proc Natl Acad Sci U S A 2004;101:16897-902. (Pubitemid 39601335)
31. Sun Q, Ming L, Thomas SM, Wang Y, Chen ZG, Ferris RL, et al. PUMA mediates EGFR tyrosine kinase inhibitor-induced apoptosis in head and neck cancer cells. Oncogene 2009;18:2348-57.
32. Yang QH, Du C. Smac/DIABLO selectively reduces the levels of c-IAP1 and c-IAP2 but not that of XIAP and livin in HeLa cells. J Biol Chem 2004;279:16963-70. (Pubitemid 38560449)
33. Rolff J, Dorn C, Merk J, Fichtner I. Response of patient-derived nonsmall cell lung cancer xenografts to classical and targeted therapies is not related to multidrug resistance markers. J Oncol 2009;2009:814140.
34. Chen Q, Gong B, Almasan A. Distinct stages of cytochrome c release from mitochondria: evidence for a feedback amplification loop linking caspase activation to mitochondrial dysfunction in genotoxic stress induced apoptosis. Cell Death Differ 2000;7:227-33. (Pubitemid 30150790)
35. Yu J, Wang P, Ming L, Wood MA, Zhang L. SMAC/Diablo mediates the proapoptotic function of PUMA by regulating PUMA-induced mitochondrial events. Oncogene 2007;26:4189-98. (Pubitemid 46975795)
36. Wu G, Chai J, Suber TL, Wu JW, Du C, Wang X, et al. Structural basis of IAP recognition by Smac/DIABLO. Nature 2000;408:1008-12. (Pubitemid 32101651)
37. Song Z, Yao X, Wu M. Direct interaction between survivin and Smac/DIABLO is essential for the anti-apoptotic activity of survivin during taxol-induced apoptosis. J Biol Chem 2003;278:23130-40. (Pubitemid 36830379)
38. Dohi T, Beltrami E, Wall NR, Plescia J, Altieri DC. Mitochondrial survivin inhibits apoptosis and promotes tumorigenesis. J Clin Invest 2004;114:1117-27. (Pubitemid 39578701)
39. Fulda S, Wick W, Weller M, Debatin KM. Smac agonists sensitize for Apo2L/TRAIL-or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat Med 2002;8:808-15.
40. Zhao J, Jin J, Zhang X, Shi M, Dai J, Wu M, et al. Transfection of Smac sensitizes tumor cells to etoposide-induced apoptosis and eradicates established human hepatoma in vivo. Cancer Gene Ther 2006;13:420-7.
41. Giagkousiklidis S, Vogler M, Westhoff MA, Kasperczyk H, Debatin KM, Fulda S. Sensitization for gamma-irradiation-induced apoptosis by second mitochondria-derived activator of caspase. Cancer Res 2005;65:10502-13. (Pubitemid 41743746)
42. Costa DB, Halmos B, Kumar A, Schumer ST, Huberman MS, Boggon TJ, et al. BIM mediates EGFR tyrosine kinase inhibitor-induced apoptosis in lung cancers with oncogenic EGFR mutations. PLoS Med 2007;4:1669-79; discussion 1680.
43. Cragg MS, Kuroda J, Puthalakath H, Huang DC, Strasser A. Gefitinib induced killing of NSCLC cell lines expressing mutant EGFR requires BIM and can be enhanced by BH3 mimetics. PLoS Med 2007;4:1681-89; discussion 1690.
44. Gong Y, Somwar R, Politi K, Balak M, Chmielecki J, Jiang X, et al. Induction of BIM is essential for apoptosis triggered by EGFR kinase inhibitors in mutant EGFR-dependent lung adenocarcinomas. PLoS Med 2007;4:e294.
45. Yu J, Yue W, Wu B, Zhang L. PUMA sensitizes lung cancer cells to chemotherapeutic agents and irradiation. Clin Cancer Res 2006;12:2928-36.
46. Rocco JW, Leong CO, Kuperwasser N, De Young MP, Ellisen LW. p63 mediates survival in squamous cell carcinoma by suppression of p73-dependent apoptosis. Cancer Cell 2006;9:45-56. (Pubitemid 43069510)
47. Barbieri CE, Barton CE, Pietenpol JA. Delta Np63 alpha expression is regulated by the phosphoinositide 3-kinase pathway. J Biol Chem 2003;278:51408-14. (Pubitemid 38020380)
48. Lassus P, Opitz-Araya X, Lazebnik Y. Requirement for caspase-2 in stress-induced apoptosis before mitochondrial permeabilization. Science 2002;297:1352-4. (Pubitemid 34913174)
49. Probst BL, Liu L, Ramesh V, Li L, Sun H, Minna JD, et al. Smac mimetics increase cancer cell response to chemotherapeutics in a TNF-alpha-dependent manner. Cell Death Differ 2010;17:1645-54.
50. Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K, Takahashi R. A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol Cell 2001;8:613-21. (Pubitemid 32946938)
51. Fesik SW. Promoting apoptosis as a strategy for cancer drug discovery. Nat Rev Cancer 2005;5:876-85. (Pubitemid 41746032)
52. Zhang L, Ming L, Yu J. BH3 mimetics to improve cancer therapy; mechanisms and examples. Drug Resist Updat 2007;10:207-17. (Pubitemid 351163146)