Therapeutic small molecules target inhibitor of apoptosis proteins in cancers with deregulation of extrinsic and intrinsic cell death pathways

Clinical Cancer Research

Volumn 23, Issue 6, 2017, Pages 1379-1387

  Derakhshan, Adeeb ^a   Chen, Zhong ^a   Van Waes, Carter ^a  

^a NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; ASTX 660; BIRINAPANT; CASPASE 3; CASPASE 7; CASPASE 8; CASPASE 9; CUDC 427; CYTOCHROME C; DEBIO 1143; FAS ASSOCIATED DEATH DOMAIN PROTEIN; GDC 0152; GDC 0917; HGS 1029; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN; N BENZHYDRYL DECAHYDRO 5 [2 (METHYLAMINO)PROPIONAMIDO] 3 (3 METHYLBUTANOYL) 6 OXOPYRROLO[1,2 A][1,5]DIAZOCINE 8 CARBOXAMIDE; N [1 CYCLOHEXYL 2 [2 [4 (4 FLUOROBENZOYL) 2 THIAZOLYL] 1 PYRROLIDINYL] 2 OXOETHYL] 2 (METHYLAMINO)PROPANAMIDE; PEPTIDOMIMETIC AGENT; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; UNCLASSIFIED DRUG; AMYLIN RECEPTOR AGONIST; DIABLO PROTEIN, HUMAN; FADD PROTEIN, HUMAN; MITOCHONDRIAL PROTEIN; SIGNAL PEPTIDE; TNFSF10 PROTEIN, HUMAN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

APOPTOSIS; ARTICLE; CANCER SURVIVAL; CELL DEATH; CELL SURVIVAL; COPY NUMBER VARIATION; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; MITOCHONDRIAL PERMEABILITY; MOLECULAR DYNAMICS; NECROPTOSIS; NONHUMAN; OUTCOME ASSESSMENT; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UBIQUITINATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HEAD AND NECK TUMOR; PATHOLOGY; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE;

AMYLIN RECEPTOR AGONISTS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAD AND NECK NEOPLASMS; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MITOCHONDRIAL PROTEINS; NF-KAPPA B; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85016152858     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-16-2172     Document Type: Article

References (74)

1. The future of cancer genomics. Nat Med 2015;21:99.
2. Hoadley KA, Yau C, Wolf DM, Cherniack AD, Tamborero D, Ng S, et al. Multiplatform analysis of 12 cancer types reveals molecular classification within and across tissues of origin. Cell 2014;158:929-44.
3. The Cancer Genome Atlas Network. Comprehensive genomic characterization of head and neck squamous cell carcinomas. Nature 2015;517: 576-82.
4. Eytan DF, Snow GE, Carlson S, Derakhshan A, Saleh A, Schiltz S, et al. SMAC mimetic birinapant plus radiation eradicates human head and neck cancers with genomic amplifications of cell death genes FADD and BIRC2. Cancer Res 2016;76:5442-54.
5. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
6. Hengartner MO. The biochemistry of apoptosis. Nature 2000;407:770-6.
7. Degterev A, Boyce M, Yuan J. A decade of caspases. Oncogene 2003; 22:8543-67.
8. Fulda S. Targeting extrinsic apoptosis in cancer: challenges and opportunities. Semin Cell Dev Biol 2015;39:20-5.
9. Kischkel FC,Hellbardt S, Behrmann I, Germer M, PawlitaM, Krammer PH, et al. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 1995;14:5579-88.
10. Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol 2007;35:495-516.
11. Lee E-W, Kim J-H, Ahn Y-H, Seo J, Ko A, Jeong M, et al. Ubiquitination and degradation of the FADD adaptor protein regulate death receptor-mediated apoptosis and necroptosis. Nat Commun 2012;3:978.
12. Tait SWG, Green DR. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 2010;11:621-32.
13. 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.
14. Crook NE, Clem RJ, Miller LK. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J Virol 1993;67:2168-74.
15. Miller LK. An exegesis of IAPs: salvation and surprises from BIR motifs. Trends Cell Biol 1999;9:323-8.
16. Vaux DL, Silke J. IAPs, RINGs and ubiquitylation. Nat Rev Mol Cell Biol 2005;6:287-97.
17. Salvesen GS, Duckett CS. IAP proteins: blocking the road to death's door. Nat Rev Mol Cell Biol 2002;3:401-10.
18. Eckelman BP, Salvesen GS. The human anti-apoptotic proteins cIAP1 and cIAP2 bind but do not inhibit caspases. J Biol Chem 2006;281: 3254-60.
19. Choi YE, Butterworth M,Malladi S, Duckett CS, Cohen GM, Bratton SB. The E3 ubiquitin ligase cIAP1 binds and ubiquitinates caspase-3 and-7 via unique mechanisms at distinct steps in their processing. J Biol Chem 2009;284:12772-82.
20. Eckelman BP, Salvesen GS, Scott FL. Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family.EMBORep 2006;7:988-94.
21. Shiozaki EN, Chai J, Rigotti DJ, Riedl SJ, Li P, Srinivasula SM, et al. Mechanism of XIAP-mediated inhibition of caspase-9. Mol Cell 2003; 11:519-27.
22. Riedl SJ, Renatus M, Schwarzenbacher R, Zhou Q, Sun C, Fesik SW, et al. Structural basis for the inhibition of caspase-3 by XIAP. Cell 2001;104: 791-800.
23. Chai J, Shiozaki E, Srinivasula SM, Wu Q, Datta P, Alnemri ES, et al. Structural basis of caspase-7 inhibition by XIAP. Cell 2001;104:769-80.
24. Vucic D, Dixit VM, Wertz IE. Ubiquitylation in apoptosis: a post-translational modification at the edge of life and death. Nat Rev Mol Cell Biol 2011;12:439-52.
25. Bertrand MJM, Milutinovic S, Dickson KM, Ho WC, Boudreault A, Durkin J, et al. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol Cell 2008;30:689-700.
26. Dynek JN, Goncharov T, Dueber EC, Fedorova AV, Izrael-Tomasevic A, Phu L, et al. c-IAP1 and UbcH5 promote K11-linked polyubiquitination of RIP1 in TNF signalling. EMBO J 2010;29:4198-209.
27. Barnhart BC, Peter ME. The TNF receptor 1: a split personality complex. Cell 2003;114:148-50.
28. Schütze S, Tchikov V, Schneider-Brachert W. Regulation of TNFR1 and CD95 signalling by receptor compartmentalization. Nat Rev Mol Cell Biol 2008;9:655-62.
29. Pasparakis M, Vandenabeele P. Necroptosis and its role in inflammation. Nature 2015;517:311-20.
30. Declercq W, Vanden Berghe T, Vandenabeele P. RIP kinases at the crossroads of cell death and survival. Cell 2009;138:229-32.
31. Gilmore TD. Introduction to NF-kappaB: players, pathways, perspectives. Oncogene 2006;25:6680-4.
32. 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.
33. Zarnegar BJ, Wang Y, Mahoney DJ, Dempsey PW, Cheung HH, He J, et al. Noncanonical NF-kappaB activation requires coordinated assembly of a regulatory complex of the adaptors cIAP1, cIAP2, TRAF2 and TRAF3 and the kinase NIK. Nat Immunol 2008;9:1371-8.
34. Sun S-C.Non-canonical NF-kB signaling pathway. Cell Res 2011;21: 71-85.
35. Vallabhapurapu S, Matsuzawa A, Zhang W, Tseng P-H, Keats JJ, Wang H, et al. Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-kappaB signaling. Nat Immunol 2008;9:1364-70.
36. Häcker H, Karin M. Regulation and function of IKK and IKK-related kinases. Sci STKE 2006;2006:re13.
37. Liu H, Sidiropoulos P, Song G, Pagliari LJ, Birrer MJ, Stein B, et al. TNFalpha gene expression in macrophages: regulation by NF-kappa B is independent of c-Jun or C/EBP beta. J Immunol 2000;164:4277-85.
38. Vande Walle L, Lamkanfi M, Vandenabeele P. The mitochondrial serine protease HtrA2/Omi: an overview. Cell Death Differ 2008;15:453-60.
39. Gottfried Y, Rotem A, Lotan R, Steller H, Larisch S. Themitochondrial ARTS protein promotes apoptosis through targeting XIAP. EMBO J 2004; 23:1627-35.
40. Straszewski-Chavez SL, Visintin IP, KarassinaN, LosG, Liston P,Halaban R, et al. XAF1mediates tumor necrosis factor-alpha-induced apoptosis and Xlinked inhibitor of apoptosis cleavage by acting through themitochondrial pathway. J Biol Chem 2007;282:13059-72.
41. 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.
42. Chai J, Du C, Wu JW, Kyin S, Wang X, Shi Y. Structural and biochemical basis of apoptotic activation by Smac/DIABLO. Nature 2000;406:855-62.
43. Liu Z, Sun C, Olejniczak ET, Meadows RP, Betz SF, Oost T, et al. Structural basis for binding of Smac/DIABLO to the XIAP BIR3 domain. Nature 2000;408:1004-8.
44. Vince JE, Wong WW-L, Khan N, Feltham R, Chau D, Ahmed AU, et al. IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis. Cell 2007;131:682-93.
45. Fulda S, Vucic D. Targeting IAP proteins for therapeutic intervention in cancer. Nat Rev Drug Discov 2012;11:109-24.
46. Bai L, Smith DC, Wang S. Small-molecule SMAC mimetics as new cancer therapeutics. Pharmacol Ther 2014;144:82-95.
47. Fulda S. Smac mimetics as IAP antagonists. Semin Cell Dev Biol 2015;39:132-8.
48. Gaither A, Porter D, Yao Y, Borawski J, Yang G, Donovan J, et al. A Smac mimetic rescue screen reveals roles for inhibitor of apoptosis proteins in tumor necrosis factor-alpha signaling. Cancer Res 2007;67:11493-8.
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-a-dependent manner. Cell Death Differ 2010;17:1645-54.
50. Collart MA, Baeuerle P, Vassalli P. Regulation of tumor necrosis factor alpha transcription in macrophages: involvement of four kappa B-like motifs and of constitutive and inducible forms of NF-kappa B. Mol Cell Biol 1990;10:1498-506.
51. Geserick P, Hupe M, Moulin M, WongWW-L, Feoktistova M, Kellert B, et al. Cellular IAPs inhibit a cryptic CD95-induced cell death by limiting RIP1 kinase recruitment. J Cell Biol 2009;187:1037-54.
52. Finlay D, VamosM, González-López M, Ardecky RJ,Ganji SR, YuanH, et al. Small-molecule IAP antagonists sensitize cancer cells to TRAIL-induced apoptosis: roles of XIAP and cIAPs. Mol Cancer Ther 2014;13:5-15.
53. Lu J, McEachern D, Sun H, Bai L, Peng Y, Qiu S, et al. Therapeutic potential and molecular mechanism of a novel, potent, nonpeptide, Smac mimetic SM-164 in combination with TRAIL for cancer treatment. Mol Cancer Ther 2011;10:902-14.
54. Lee E-W, Seo J, Jeong M, Lee S, Song J. The roles of FADD in extrinsic apoptosis and necroptosis. BMB Rep 2012;45:496-508.
55. Hu WH, Johnson H, Shu HB. Activation of NF-kappaB by FADD, casper, and caspase-8. J Biol Chem 2000;275:10838-44.
56. Rasamny JJ, Allak A, Krook KA, Jo VY, Policarpio-Nicolas ML, Sumner HM, et al. Cyclin D1 and FADD as biomarkers in head and neck squamous cell carcinoma. Otolaryngol Head Neck Surg 2012;146:923-31.
57. Lin RJ, Lubpairee T, Liu KY, Anderson DW, Durham S, Poh CF. Cyclin D1 overexpression is associated with poor prognosis in oropharyngeal cancer. J Otolaryngol 2013;42:23.
58. Musgrove EA, Caldon CE, Barraclough J, Stone A, Sutherland RL. Cyclin D as a therapeutic target in cancer. Nat Rev Cancer 2011;11:558-72.
59. Matzinger O, Viertl D, Tsoutsou P, Kadi L, Rigotti S, Zanna C, et al. The radiosensitizing activity of the SMAC-mimetic, Debio 1143, is TNFamediated in head and neck squamous cell carcinoma. Radiother Oncol 2015;116:495-503.
60. Yang J, McEachern D, Li W, Davis MA, Li H, Morgan MA, et al. Radiosensitization of head and neck squamous cell carcinoma by a SMACmimetic compound, SM-164, requires activation of caspases. Mol Cancer Ther 2011;10:658-69.
61. Eytan DF, Snow GE, Carlson SG, Schiltz S, Chen Z, Van Waes C. Combination effects of SMAC mimetic birinapant with TNFa, TRAIL, and docetaxel in preclinical models of HNSCC. Laryngoscope 2015;125: E118-124.
62. Sprowl JA, Reed K, Armstrong SR, Lanner C, Guo B, Kalatskaya I, et al. Alterations in tumor necrosis factor signaling pathways are associated with cytotoxicity and resistance to taxanes: a study in isogenic resistant tumor cells. Breast Cancer Res 2012;14:R2.
63. Sun Q, Zheng X, Zhang L, Yu J. Smac modulates chemosensitivity in head and neck cancer cells through the mitochondrial apoptotic pathway. Clin Cancer Res 2011;17:2361-72.
64. RaulfN, El-Attar R, Kulms D, Lecis D, Delia D, Walczak H, et al.Differential response of head and neck cancer cell lines to TRAIL or Smac mimetics is associated with the cellular levels and activity of caspase-8 and caspase-10. Br J Cancer 2014;111:1955-64.
65. Brands RC, Herbst F, Hartmann S, Seher A, Linz C, Kübler AC, et al. Cytotoxic effects of SMAC-mimetic compound LCL161 in head and neck cancer cell lines. Clin Oral Investig 2016;20:2325-32
66. Fulda S. Promises and challenges of smac mimetics as cancer therapeutics. Clin Cancer Res 2015;21:5030-6.
67. Hurwitz HI, Smith DC, Pitot HC, Brill JM, Chugh R, Rouits E, et al. Safety, pharmacokinetics, and pharmacodynamic properties of oral DEBIO1143 (AT-406) in patients with advanced cancer: results of a first-in-man study. Cancer Chemother Pharmacol 2015;75:851-9.
68. Amaravadi RK, Schilder RJ, Martin LP, Levin M, Graham MA, Weng DE, et al. A phase I study of the SMAC-mimetic birinapant in adults with refractory solid tumors or lymphoma. Mol Cancer Ther 2015;14:2569-75.
69. Infante JR, Dees EC, Olszanski AJ, Dhuria SV, Sen S, Cameron S, et al. Phase I dose-escalation study of LCL161, an oral inhibitor of apoptosis proteins inhibitor, in patients with advanced solid tumors. J Clin Oncol 2014; 32:3103-10.
70. Cai Q, Sun H, Peng Y, Lu J, Nikolovska-Coleska Z, McEachern D, et al. A potent and orally active antagonist (SM-406/AT-406) of multiple inhibitor of apoptosis proteins (IAPs) in clinical development for cancer treatment. J Med Chem 2011;54:2714-26.
71. Wong H, Gould SE, Budha N, Darbonne WC, Kadel EEIII, La H, et al. Learning and confirming with preclinical studies: modeling and simulation in the discovery of GDC-0917, an inhibitor of apoptosis proteins antagonist. Drug Metab Dispos 2013;41:2104-13.
72. Flygare JA, BeresiniM, Budha N, ChanH, Chan IT, Cheeti S, et al.Discovery of a potent small-molecule antagonist of inhibitor of apoptosis (IAP) proteins and clinical candidate for the treatment of cancer (GDC-0152). J Med Chem 2012;55:4101-13.
73. Benetatos CA, Mitsuuchi Y, Burns JM, Neiman EM, Condon SM, YuG, et al. Birinapant (TL32711), a bivalent SMAC mimetic, targets TRAF2-associated cIAPs, abrogates TNF-induced NF-kB activation, and is active in patientderived xenograft models. Mol Cancer Ther 2014;13:867-79.
74. Ward G, Ahn M, Chessari G, Graham B, Hearn K, Johnson CN, et al. Characterization of the activity of potent XIAP/cIAP1 dual antagonists in melanoma models. Poster presented at 3rd British Association for Cancer Research: Advances in Cancer Drug Discovery; 2014 Mar 30-Apr 1; Homerton College, Cambridge, United Kingdom.