Small-molecule IAP antagonists sensitize cancer cells to TRAIL-induced apoptosis: Roles of XIAP and cIAPs

Molecular Cancer Therapeutics

Volumn 13, Issue 1, 2013, Pages 5-15

  Finlay, Darren ^a   Vamos, Mitchell ^a   González López, Marcos ^a   Ardecky, Robert J ^a   Ganji, Santhi Reddy ^a   Yuan, Hongbin ^a   Su, Ying ^a   Cooley, Trina R ^a   Hauser, Curt T ^a   Welsh, Kate ^a   Reed, John C ^a,b   Cosford, Nicholas D P ^a   Vuori, Kristiina ^a  

^a BURNHAM INSTITUTE   (United States)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CASPASE 8; INHIBITOR OF APOPTOSIS PROTEIN; MLS 0390969; MLS 0390982; MLS 0391011; PROTEIN INHIBITOR; SB 1 0636457; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CHEMOSENSITIZATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG EFFICACY; DRUG POTENCY; DRUG STRUCTURE; FEMALE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CASPASE 8; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MOLECULAR TARGETED THERAPY; NEOPLASMS; SIGNAL TRANSDUCTION; SMALL MOLECULE LIBRARIES; TNF-RELATED APOPTOSIS-INDUCING LIGAND; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 84892578403     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-13-0153     Document Type: Article

References (43)

1. Zheng L, Bidere N, Staudt D, Cubre A, Orenstein J, Chan FK, et al. Competitive control of independent programs of tumor necrosis factor receptor-induced cell death by TRADD and RIP1. Mol Cell Biol 2006; 26:3505-13.
2. Heyninck K, Beyaert R. Crosstalk between NF-κB-activating and apoptosis-inducing proteins of the TNF-receptor complex. Mol Cell Biol Res Commun 2001;4:259-65.
3. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, et al. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat. Med 1999;5:157-163.
4. Takeda K, Smyth MJ, Cretney E, Hayakawa Y, Kayagaki N, Yagita H, et al. Critical role for tumor necrosis factor-related apoptosis-inducing ligand in immune surveillance against tumor development. J Exp Med 2002;195:161-9.
5. Finnberg N, Klein-Szanto AJ, El-Deiry WS. TRAIL-R deficiency in mice promotes susceptibility to chronic inflammation and tumorigenesis. J Clin Invest 2008;118:111-23.
6. Cretney E, Takeda K, Yagita H, Glaccum M, Peschon JJ, Smyth MJ. Increased susceptibility to tumor initiation and metastasis in TNFrelated apoptosis-inducing ligand-deficient mice. J Immunol 2002; 168:1356-61.
7. Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, et al. Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 1999;104:155-62.
8. Mahalingam D, Oldenhuis CN, Szegezdi E, Giles FJ, de Vries EG, de Jong S, et al. Targeting trail towards the clinic. Curr Drug Targets 2011;12:2079-90.
9. Thorburn A, Behbakht K, Ford H. TRAIL receptor-targeted therapeutics: resistance mechanisms and strategies to avoid them. Drug Resist Updat 2008;11:17-24.
10. Dean EJ, Ranson M, Blackhall F, Dive C. X-linked inhibitor of apoptosis protein as a therapeutic target. Expert Opin Ther Targets 2007;11: 1459-71.
11. Deveraux QL, Reed JC. IAP family proteins-suppressors of apoptosis. Genes Dev 1999;13:239-52.
12. LaCasse EC, Mahoney DJ, Cheung HH, Plenchette S, Baird S, Korneluk RG. IAP-targeted therapies for cancer. Oncogene 2008;27: 6252-75.
13. Pop C, Salvesen GS. Human caspases: activation, specificity, and regulation. J Biol Chem 2009;284:21777-81.
14. Riedl SJ, Renatus M, Schwarzenbacher R, Zhou Q, Sun C, Fesik SW. Structural basis for the inhibition of caspase-3 by XIAP. Cell 2001; 104:791-800.
15. 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.
16. Srinivasula SM, Hegde R, Saleh A, Datta P, Shiozaki E, Chai J. A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature. 2001;410: 112-6.
17. Shiozaki EN, Shi Y. Caspases, IAPs and Smac/DIABLO: mechanisms from structural biology. Trends Biochem Sci 2004;29:486-94.
18. 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.
19. Zobel K, Wang L, Varfolomeev E, Franklin MC, Elliott LO, Wallweber HJ, et al. Design, synthesis, and biological activity of a potent Smac mimetic that sensitizes cancer cells to apoptosis by antagonizing IAPs. ACS Chem Biol 2006;1:525-33.
20. Li L, Thomas RM, Suzuki H, De Brabander JK, Wang X, Harran PG. A small molecule Smac mimic potentiates TRAIL- and TNFα-mediated cell death. Science 2004;305:1471-4.
21. Petersen SL, Wang L, Yalcin-Chin A, Li L, Peyton M, Minna J, et al. Autocrine TNFα signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis. Cancer Cell 2007;12: 445-56.
22. 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.
23. Dueber EC, Schoeffler AJ, Lingel A, Elliott JM, Fedorova AV, Giannetti AM, et al. Antagonists induce a conformational change in cIAP1 that promotes autoubiquitination. Science 2011;334:376-80.
24. Feltham R, Bettjeman B, Budhidarmo R, Mace PD, Shirley S, Condon SM, et al. Smacmimetics activate the E3 ligase activity of cIAP1 protein by promoting RING domain dimerization. J Biol Chem 2011; 286:17015-28.
25. Sun M, Song L, Li Y, Zhou T, Jope RS. Identification of an antiapoptotic protein complex at death receptors. Cell Death Differ 2008;15: 1887-900.
26. Sun SC. Non-canonical NF-κB signaling pathway. Cell Res 2011;21: 71-85.
27. Wang L, Du F, Wang X. TNF-α induces two distinct caspase-8 activation pathways. Cell 2008;133:693-703.
28. Feoktistova M, Geserick P, Kellert B, Dimitrova DP, Langlais C, Hupe M, et al. cIAPs block ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol Cell 2011;43:449-63.
29. Tenev T, Bianchi K, Darding M, Broemer M, Langlais C, Wallberg F, et al. The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol Cell 2011;43: 432-48.
30. González-López M, Welsh K, Finlay D, Ardecky RJ, Ganji SR, Su Y, et al. Design, synthesis and evaluation of monovalent Smac mimetics that bind to the BIR2 domain of the anti-apoptotic protein XIAP. Bioorg Med Chem Lett 2011;21:4332-6.
31. Vamos M, Welsh K, Finlay D, Lee PS, Mace PD, Snipas SJ, et al. Expedient synthesis of highly potent antagonists of inhibitor of apoptosis proteins (IAPs) with unique selectivity for ML-IAP. ACS Chem. Biol 2013;8:725-732.
32. Finlay D, Richardson RD, Landberg LK, Howes AL, Vuori K. Novel HTS strategy identifies TRAIL-sensitizing compounds acting specifically through the caspase-8 apoptotic axis. PLoS One 2010;5: e13375.
33. Finlay D, Vuori K. Novel non-catalytic role for caspase-8 in promoting src mediated-adhesion and Erk signaling in neuroblastoma cells. Cancer Res 2007;67:11704-11711.
34. Finlay D, Howes A., and Vuori K. Critical role for caspase-8 in EGF signaling. Cancer Res 2009;69:5023-5029.
35. Yadav VR, Prasad S, Gupta SC, Sung B, Phatak SS, Zhang S, et al. 3- Formylchromone interacts with cysteine 38 in p65 protein and with cysteine 179 in IκBα kinase, leading to down-regulation of nuclear factor-κB (NF-κB)-regulated gene products and sensitization of tumor cells. J Biol Chem 2012;287:245-56.
36. Park CM, Sun C, Olejniczak ET, Wilson AE, Meadows RP, Betz SF, et al. Non-peptidic small molecule inhibitors of XIAP. Bioorg Med Chem Lett 2005;15:771-5.
37. Boatright KM, Renatus M, Scott FL, Sperandio S, Shin H, Pedersen IM, et al. A unified model for apical caspase activation. Mol Cell 2003;11:529-41.
38. Varfolomeev E, Blankenship JW, Wayson SM, Fedorova AV, Kayagaki N, Garg P, et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-κB activation, and TNFα-dependent apoptosis. Cell 2007;131: 669-81.
39. Sun H, Liu L, Lu J, Qiu S, Yang CY, Yi H, et al. Cyclopeptide Smac mimetics as antagonists of IAP proteins. Bioorg Med Chem Lett 2010;20:3043-6.
40. Huerta-Yepez S, Vega M, Jazirehi A, Garban H, Hongo F, Cheng G, et al. Nitric oxide sensitizes prostate carcinoma cell lines to TRAILmediated apoptosis via inactivation of NF-κB and inhibition of Bcl-xl expression. Oncogene 2004;23:4993-5003.
41. Ammann JU, Haag C, Kasperczyk H, Debatin KM, Fulda S. Sensitization of neuroblastoma cells for TRAIL-induced apoptosis by NF-κB inhibition. Int J Cancer 2009;124:1301-11.
42. Allensworth JL, Aird KM, Aldrich AJ, Batinic-Haberle I, Devi GR. XIAP inhibition and generation of reactive oxygen species enhances TRAIL sensitivity in inflammatory breast cancer cells. Mol Cancer Ther 2012;11:1518-27.
43. Wang CY, Mayo MW, Korneluk RG, Goeddel DV, Baldwin AS Jr. NF-κB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 1998;281:1680-1683.