Inhibitor of apoptosis proteins as intracellular signaling intermediates

FEBS Journal

Volumn 283, Issue 2, 2016, Pages 221-231

  Kocab, Andrew J ^a,b   Duckett, Colin S ^b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

apoptosis; caspases; cd30; cell signaling; inhibitor of apoptosis protein (IAP); NF B; Smac; Smac mimetic; tumor necrosis factor (TNF); ubiquitin mediated signaling

Indexed keywords

CASPASE; CASPASE 8; CYTOCHROME C; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN 1; INHIBITOR OF APOPTOSIS PROTEIN 2; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; TUMOR NECROSIS FACTOR RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; UBIQUITIN PROTEIN LIGASE E3; X LINKED INHIBITOR OF APOPTOSIS; DIABLO PROTEIN, HUMAN; MITOCHONDRIAL PROTEIN; MOLECULAR LIBRARY; SIGNAL PEPTIDE;

APOPTOSIS; CELL DEATH; CELL DIFFERENTIATION; CELL FATE; CELL PROLIFERATION; COMPLEX FORMATION; DNA DAMAGE; HUMAN; INTRACELLULAR SIGNALING; MITOCHONDRIAL PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REVIEW; RIBOSOME; UBIQUITINATION; ANIMAL; ANTAGONISTS AND INHIBITORS; METABOLISM; MOLECULAR LIBRARY; MOLECULAR MIMICRY; PHARMACOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CASPASES; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MITOCHONDRIAL PROTEINS; MOLECULAR MIMICRY; RECEPTORS, TUMOR NECROSIS FACTOR; SIGNAL TRANSDUCTION; SMALL MOLECULE LIBRARIES;

EID: 84957445203     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13554     Document Type: Review

References (86)

1. Scott FL, Denault JB, Riedl SJ, Shin H, Renatus M, &, Salvesen GS, (2005) XIAP inhibits caspase-3 and -7 using two binding sites: evolutionarily conserved mechanism of IAPs. EMBO J 24, 645-655.
2. Wilkinson JC, Wilkinson AS, Galban S, Csomos RA, &, Duckett CS, (2008) Apoptosis-inducing factor is a target for ubiquitination through interaction with XIAP. Mol Cell Biol 28, 237-247.
3. Dueber EC, Schoeffler AJ, Lingel A, Elliott JM, Fedorova AV, Giannetti AM, Zobel K, Maurer B, Varfolomeev E, Wu P, et al,. (2011) Antagonists induce a conformational change in cIAP1 that promotes autoubiquitination. Science 334, 376-380.
4. Phillips AH, Schoeffler AJ, Matsui T, Weiss TM, Blankenship JW, Zobel K, Giannetti AM, Dueber EC, &, Fairbrother WJ, (2014) Internal motions prime cIAP1 for rapid activation. Nat Struct Mol Biol 21, 1068-1074.
5. Lopez J, John SW, Tenev T, Rautureau GJ, Hinds MG, Francalanci F, Wilson R, Broemer M, Santoro MM, Day CL, et al,. (2011) CARD-mediated autoinhibition of cIAP1's E3 ligase activity suppresses cell proliferation and migration. Mol Cell 42, 569-583.
6. Budhidarmo R, &, Day CL, (2014) The ubiquitin-associated domain of cellular inhibitor of apoptosis proteins facilitates ubiquitylation. J Biol Chem 289, 25721-25736.
7. Gyrd-Hansen M, Darding M, Miasari M, Santoro MM, Zender L, Xue W, Tenev T, da Fonseca PC, Zvelebil M, Bujnicki JM, et al,. (2008) IAPs contain an evolutionarily conserved ubiquitin-binding domain that regulates NF-κB as well as cell survival and oncogenesis. Nat Cell Biol 10, 1309-1317.
8. Blankenship JW, Varfolomeev E, Goncharov T, Fedorova AV, Kirkpatrick DS, Izrael-Tomasevic A, Phu L, Arnott D, Aghajan M, Zobel K, et al,. (2009) Ubiquitin binding modulates IAP antagonist-stimulated proteasomal degradation of c-IAP1 and c-IAP2. Biochem J 417, 149-160.
9. Deveraux QL, Roy N, Stennicke HR, Van Arsdale T, Zhou Q, Srinivasula SM, Alnemri ES, Salvesen GS, &, Reed JC, (1998) IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J 17, 2215-2223.
10. Deveraux QL, Takahashi R, Salvesen GS, &, Reed JC, (1997) X-linked IAP is a direct inhibitor of cell-death proteases. Nature 388, 300-304.
11. Salvesen GS, &, Duckett CS, (2002) IAP proteins: blocking the road to death's door. Nat Rev Mol Cell Biol 3, 401-410.
12. Duckett CS, Li F, Wang Y, Tomaselli KJ, Thompson CB, &, Armstrong RC, (1998) Human IAP-like protein regulates programmed cell death downstream of Bcl-xL and cytochrome c. Mol Cell Biol 18, 608-615.
13. Tait SW, &, Green DR, (2010) Mitochondria and cell death: outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 11, 621-632.
14. Samuel T, Welsh K, Lober T, Togo SH, Zapata JM, &, Reed JC, (2006) Distinct BIR domains of cIAP1 mediate binding to and ubiquitination of tumor necrosis factor receptor-associated factor 2 and second mitochondrial activator of caspases. J Biol Chem 281, 1080-1090.
15. Yang QH, &, Du C, (2004) 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 279, 16963-16970.
16. Du C, Fang M, Li Y, Li L, &, Wang X, (2000) Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102, 33-42.
17. Wu G, Chai J, Suber TL, Wu JW, Du C, Wang X, &, Shi Y, (2000) Structural basis of IAP recognition by Smac/DIABLO. Nature 408, 1008-1012.
18. Csomos RA, Wright CW, Galban S, Oetjen KA, &, Duckett CS, (2009) Two distinct signalling cascades target the NF-κB regulatory factor c-IAP1 for degradation. Biochem J 420, 83-91.
19. Eckelman BP, &, Salvesen GS, (2006) The human anti-apoptotic proteins cIAP1 and cIAP2 bind but do not inhibit caspases. J Biol Chem 281, 3254-3260.
20. Silke J, &, Brink R, (2010) Regulation of TNFRSF and innate immune signalling complexes by TRAFs and cIAPs. Cell Death Differ 17, 35-45.
21. Feoktistova M, Geserick P, Kellert B, Dimitrova DP, Langlais C, Hupe M, Cain K, MacFarlane M, Hacker G, &, Leverkus M, (2011) cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol Cell 43, 449-463.
22. Tenev T, Bianchi K, Darding M, Broemer M, Langlais C, Wallberg F, Zachariou A, Lopez J, MacFarlane M, Cain K, et al,. (2011) The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol Cell 43, 432-448.
23. Gyrd-Hansen M, &, Meier P, (2010) IAPs: from caspase inhibitors to modulators of NF-κB, inflammation and cancer. Nat Rev Cancer 10, 561-574.
24. Burstein E, Ganesh L, Dick RD, van De Sluis B, Wilkinson JC, Klomp LW, Wijmenga C, Brewer GJ, Nabel GJ, &, Duckett CS, (2004) A novel role for XIAP in copper homeostasis through regulation of MURR1. EMBO J 23, 244-254.
25. Mufti AR, Burstein E, Csomos RA, Graf PC, Wilkinson JC, Dick RD, Challa M, Son JK, Bratton SB, Su GL, et al,. (2006) XIAP is a copper binding protein deregulated in Wilson's disease and other copper toxicosis disorders. Mol Cell 21, 775-785.
26. Brady GF, Galban S, Liu X, Basrur V, Gitlin JD, Elenitoba-Johnson KS, Wilson TE, &, Duckett CS, (2010) Regulation of the copper chaperone CCS by XIAP-mediated ubiquitination. Mol Cell Biol 30, 1923-1936.
27. Samuel T, Okada K, Hyer M, Welsh K, Zapata JM, &, Reed JC, (2005) cIAP1 localizes to the nuclear compartment and modulates the cell cycle. Cancer Res 65, 210-218.
28. Cartier J, Berthelet J, Marivin A, Gemble S, Edmond V, Plenchette S, Lagrange B, Hammann A, Dupoux A, Delva L, et al,. (2011) Cellular inhibitor of apoptosis protein-1 (cIAP1) can regulate E2F1 transcription factor-mediated control of cyclin transcription. J Biol Chem 286, 26406-26417.
29. Oberoi TK, Dogan T, Hocking JC, Scholz RP, Mooz J, Anderson CL, Karreman C, Meyer zu Heringdorf D, Schmidt G, Ruonala M, et al,. (2012) IAPs regulate the plasticity of cell migration by directly targeting Rac1 for degradation. EMBO J 31, 14-28.
30. Kenneth NS, &, Duckett CS, (2012) IAP proteins: regulators of cell migration and development. Curr Opin Cell Biol 24, 871-875.
31. Heride C, Urbe S, &, Clague MJ, (2014) Ubiquitin code assembly and disassembly. Curr Biol 24, R215-R220.
32. Varfolomeev E, Goncharov T, Fedorova AV, Dynek JN, Zobel K, Deshayes K, Fairbrother WJ, &, Vucic D, (2008) c-IAP1 and c-IAP2 are critical mediators of tumor necrosis factor α (TNFα)-induced NF-κB activation. J Biol Chem 283, 24295-24299.
33. Bertrand MJ, Milutinovic S, Dickson KM, Ho WC, Boudreault A, Durkin J, Gillard JW, Jaquith JB, Morris SJ, &, Barker PA, (2008) cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol Cell 30, 689-700.
34. Walczak H, (2011) TNF and ubiquitin at the crossroads of gene activation, cell death, inflammation, and cancer. Immunol Rev 244, 9-28.
35. Hayden MS, &, Ghosh S, (2008) Shared principles in NF-κB signaling. Cell 132, 344-362.
36. Sun SC, (2012) The noncanonical NF-κB pathway. Immunol Rev 246, 125-140.
37. Perkins ND, (2007) Integrating cell-signalling pathways with NF-κB and IKK function. Nat Rev Mol Cell Biol 8, 49-62.
38. Scheidereit C, (2006) IκB kinase complexes: gateways to NF-κB activation and transcription. Oncogene 25, 6685-6705.
39. Vallabhapurapu S, Matsuzawa A, Zhang W, Tseng PH, Keats JJ, Wang H, Vignali DA, Bergsagel PL, &, Karin M, (2008) Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-κB signaling. Nat Immunol 9, 1364-1370.
40. Wertz IE, &, Dixit VM, (2010) Regulation of death receptor signaling by the ubiquitin system. Cell Death Differ 17, 14-24.
41. Hacker H, Tseng PH, &, Karin M, (2011) Expanding TRAF function: TRAF3 as a tri-faced immune regulator. Nat Rev Immunol 11, 457-468.
42. Croft M, Duan W, Choi H, Eun SY, Madireddi S, &, Mehta A, (2012) TNF superfamily in inflammatory disease: translating basic insights. Trends Immunol 33, 144-152.
43. Hsu H, Xiong J, &, Goeddel DV, (1995) The TNF receptor 1-associated protein TRADD signals cell death and NF-κB activation. Cell 81, 495-504.
44. Micheau O, &, Tschopp J, (2003) Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114, 181-190.
45. Vince JE, Pantaki D, Feltham R, Mace PD, Cordier SM, Schmukle AC, Davidson AJ, Callus BA, Wong WW, Gentle IE, et al,. (2009) TRAF2 must bind to cellular inhibitors of apoptosis for tumor necrosis factor (TNF) to efficiently activate NF-κB and to prevent TNF-induced apoptosis. J Biol Chem 284, 35906-35915.
46. Dynek JN, Goncharov T, Dueber EC, Fedorova AV, Izrael-Tomasevic A, Phu L, Helgason E, Fairbrother WJ, Deshayes K, Kirkpatrick DS, et al,. (2010) c-IAP1 and UbcH5 promote K11-linked polyubiquitination of RIP1 in TNF signaling. EMBO J 29, 4198-4209.
47. Wang C, Deng L, Hong M, Akkaraju GR, Inoue JI, &, Chen ZJ, (2001) TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412, 346-351.
48. Haas TL, Emmerich CH, Gerlach B, Schmukle AC, Cordier SM, Rieser E, Feltham R, Vince J, Warnken U, Wenger T, et al,. (2009) Recruitment of the linear ubiquitin chain assembly complex stabilizes the TNF-R1 signaling complex and is required for TNF-mediated gene induction. Mol Cell 36, 831-844.
49. Gerlach B, Cordier SM, Schmukle AC, Emmerich CH, Rieser E, Haas TL, Webb AI, Rickard JA, Anderton H, Wong WW, et al,. (2011) Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 471, 591-596.
50. Yang J, Lin Y, Guo Z, Cheng J, Huang J, Deng L, Liao W, Chen Z, Liu ZG, &, Su B, (2001) The essential role of MEKK3 in TNF-induced NF-κB activation. Nat Immunol 2, 620-624.
51. Takaesu G, Surabhi RM, Park KJ, Ninomiya-Tsuji J, Matsumoto K, &, Gaynor RB, (2003) TAK1 is critical for IκB kinase-mediated activation of the NF-κB pathway. J Mol Biol 326, 105-115.
52. Zarnegar BJ, Wang Y, Mahoney DJ, Dempsey PW, Cheung HH, He J, Shiba T, Yang X, Yeh WC, Mak TW, et al,. (2008) Noncanonical NF-κB activation requires coordinated assembly of a regulatory complex of the adaptors cIAP1, cIAP2, TRAF2 and TRAF3 and the kinase NIK. Nat Immunol 9, 1371-1378.
53. Vallabhapurapu S, &, Karin M, (2009) Regulation and function of NF-κB transcription factors in the immune system. Annu Rev Immunol 27, 693-733.
54. Malinin NL, Boldin MP, Kovalenko AV, &, Wallach D, (1997) MAP3K-related kinase involved in NF-κB induction by TNF, CD95, and IL-1. Nature 385, 540-544.
55. Liao G, Zhang M, Harhaj EW, &, Sun SC, (2004) Regulation of the NF-κB-inducing kinase by tumor necrosis factor receptor-associated factor 3-induced degradation. J Biol Chem 279, 26243-26250.
56. Varfolomeev E, Blankenship JW, Wayson SM, Fedorova AV, Kayagaki N, Garg P, Zobel K, Dynek JN, Elliott LO, Wallweber HJ, et al,. (2007) IAP antagonists induce autoubiquitination of c-IAPs, NF-κB activation, and TNFα-dependent apoptosis. Cell 131, 669-681.
57. Duckett CS, &, Thompson CB, (1997) CD30-dependent degradation of TRAF2: implications for negative regulation of TRAF signaling and the control of cell survival. Genes Dev 11, 2810-2821.
58. Varfolomeev E, Goncharov T, Maecker H, Zobel K, Komuves LG, Deshayes K, &, Vucic D, (2012) Cellular inhibitors of apoptosis are global regulators of NF-κB and MAPK activation by members of the TNF family of receptors. Sci Signal 5, ra22.
59. Wright CW, Rumble JM, &, Duckett CS, (2007) CD30 activates both the canonical and alternative NF-κB pathways in anaplastic large cell lymphoma cells. J Biol Chem 282, 10252-10262.
60. Schimmer AD, Welsh K, Pinilla C, Wang Z, Krajewska M, Bonneau MJ, Pedersen IM, Kitada S, Scott FL, Bailly-Maitre B, et al,. (2004) Small-molecule antagonists of apoptosis suppressor XIAP exhibit broad antitumor activity. Cancer Cell 5, 25-35.
61. Li L, Thomas RM, Suzuki H, de Brabander JK, Wang X, &, Harran PG, (2004) A small molecule Smac mimetic potentiates TRAIL- and TNFα-mediated cell death. Science 305, 1471-1474.
62. Sun H, Nikolovska-Coleska Z, Yang CY, Xu L, Liu M, Tomita Y, Pan H, Yoshioka Y, Krajewski K, Roller PP, et al,. (2004) Structure-based design of potent, conformationally constrained Smac mimetics. J Am Chem Soc 126, 16686-16687.
63. Vince JE, Wong WW, Khan N, Feltham R, Chau D, Ahmed AU, Benetatos CA, Chunduru SK, Condon SM, McKinlay M, et al,. (2007) IAP antagonists target cIAP1 to induce TNFα-dependent apoptosis. Cell 131, 682-693.
64. Darding M, Feltham R, Tenev T, Bianchi K, Benetatos C, Silke J, &, Meier P, (2011) Molecular determinants of Smac mimetic induced degradation of cIAP1 and cIAP2. Cell Death Differ 18, 1376-1386.
65. Lu J, Bai L, Sun H, Nikolovska-Coleska Z, McEachern D, Qiu S, Miller RS, Yi H, Shangary S, Sun Y, et al,. (2008) SM-164: a novel, bivalent Smac mimetic that induces apoptosis and tumor regression by concurrent removal of the blockade of cIAP-1/2 and XIAP. Cancer Res 68, 9384-9393.
66. Petersen SL, Wang L, Yalcin-Chin A, Li L, Peyton M, Minna J, Harran P, &, Wang X, (2007) Autocrine TNFα signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis. Cancer Cell 12, 445-456.
67. Darding M, &, Meier P, (2012) IAPs: guardians of RIPK1. Cell Death Differ 19, 58-66.
68. Ichim G, Lopez J, Ahmed SU, Muthalagu N, Giampazolias E, Delgado ME, Haller M, Riley JS, Mason SM, Athineos D, et al,. (2015) Limited mitochondrial permeabilization causes DNA damage and genomic instability in the absence of cell death. Mol Cell 57, 860-872.
69. Ditzel M, Wilson R, Tenev T, Zachariou A, Paul A, Deas E, &, Meier P, (2003) Degradation of DIAP1 by the N-end rule pathway is essential for regulating apoptosis. Nat Cell Biol 5, 467-473.
70. Kocab AJ, Veloso A, Paulsen MT, Ljungman M, &, Duckett CS, (2015) Effects of physiological and synthetic IAP antagonism on c-IAP-dependent signaling. Oncogene, 34, 5472-5481.
71. Saracino F, Bassler J, Muzzini D, Hurt E, &, Agostoni Carbone ML, (2004) The yeast kinase Swe1 is required for proper entry into cell cycle after arrest due to ribosome biogenesis and protein synthesis defects. Cell Cycle 3, 648-654.
72. Verbin RS, &, Farber E, (1967) Effect of cycloheximide on the cell cycle of the crypts of the small intestine of the rat. J Cell Biol 35, 649-658.
73. Medrano EE, &, Pardee AB, (1980) Prevalent deficiency in tumor cells of cycloheximide-induced cell cycle arrest. Proc Natl Acad Sci USA 77, 4123-4126.
74. Darzynkiewicz Z, Williamson B, Carswell EA, &, Old LJ, (1984) Cell cycle-specific effects of tumor necrosis factor. Cancer Res 44, 83-90.
75. Ehrhardt H, Wachter F, Grunert M, &, Jeremias I, (2013) Cell cycle-arrested tumor cells exhibit increased sensitivity towards TRAIL-induced apoptosis. Cell Death Dis 4, e661.
76. Vandenabeele P, Galluzzi L, Vanden Berghe T, &, Kroemer G, (2010) Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol 11, 700-714.
77. Oeckinghaus A, Hayden MS, &, Ghosh S, (2011) Crosstalk in NF-κB signaling pathways. Nat Immunol 12, 695-708.
78. Shalini S, Dorstyn L, Dawar S, &, Kumar S, (2015) Old, new and emerging functions of caspases. Cell Death Differ 22, 526-539.
79. Thornberry NA, Bull HG, Calaycay JR, Chapman KT, Howard AD, Kostura MJ, Miller DK, Molineaux SM, Weidner JR, Aunins J, et al,. (1992) A novel heterodimeric cysteine protease is required for interleukin-1β processing in monocytes. Nature 356, 768-774.
80. Ghayur T, Banerjee S, Hugunin M, Butler D, Herzog L, Carter A, Quintal L, Sekut L, Talanian R, Paskind M, et al,. (1997) Caspase-1 processes IFN-γ-inducing factor and regulates LPS-induced IFN-γ production. Nature 286, 619-623.
81. Fernando P, Kelly JF, Balazsi K, Slack RS, &, Megeney LA, (2002) Caspase-3 activity is required for skeletal muscle differentiation. Proc Natl Acad Sci USA 99, 11025-11030.
82. Maelfait J, Vercammen E, Janssens S, Schotte P, Haegman M, Magez S, &, Beyaert R, (2008) Stimulation of Toll-like receptor 3 and 4 induces interleukin-1β maturation by caspase-8. J Exp Med 205, 1967-1973.
83. Vince JE, Wong WW, Gentle I, Lawlor KE, Allam R, O'Reilly L, Mason K, Gross O, Ma S, Guarda G, et al,. (2012) Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation. Immunity 36, 215-227.
84. Allam R, Lawlor KE, Yu EC, Mildenhall AL, Moujalled DM, Lewis RS, Ke F, Mason KD, White MJ, Stacey KJ, et al,. (2014) Mitochondrial apoptosis is dispensable for NLRP3 inflammasome activation but non-apoptotic caspase-8 is required for inflammasome priming. EMBO Rep 15, 982-990.
85. Rebe C, Cathelin S, Launay S, Filomenko R, Prevotat L, L'Ollivier C, Gyan E, Micheau O, Grant S, Dubart-Kupperschmitt A, et al,. (2007) Caspase-8 prevents sustained activation of NF-κB in monocytes undergoing macrophagic differentiation. Blood 109, 1442-1450.
86. Kang TB, Ben-Moshe T, Varfolomeev EE, Pewzner-Jung Y, Yogev N, Jurewicz A, Waisman A, Brenner O, Haffner R, Gustafsson E, et al,. (2004) Caspase-8 serves both apoptotic and nonapoptotic roles. J Immunol 173, 2976-2984.