Regulating the balance between necroptosis, apoptosis and inflammation by inhibitors of apoptosis proteins

Immunology and Cell Biology

Volumn 95, Issue 2, 2017, Pages 160-165

  Vasilikos, Lazaros ^a   Spilgies, Lisanne M ^a   Knop, Janin ^a   Wong, Wendy Wei Lynn ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

INHIBITOR OF APOPTOSIS PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR 1;

APOPTOSIS; CELL DEATH; CELL SURVIVAL; GENETIC MODEL; HUMAN; INFLAMMATION; INTRACELLULAR SIGNALING; NECROPTOSIS; NONHUMAN; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; ANIMAL; BIOLOGICAL MODEL; METABOLISM; NECROSIS; PATHOLOGY;

ANIMALS; APOPTOSIS; CELL SURVIVAL; HUMANS; INFLAMMATION; INHIBITOR OF APOPTOSIS PROTEINS; MODELS, GENETIC; NECROSIS;

EID: 85008397719     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2016.118     Document Type: Review

References (87)

1. Crook NE, Clem RJ, Miller LK. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J Virol 1993; 67: 2168-2174.
2. Clem RJ, Miller LK. Control of programmed cell death by the baculovirus genes p35 and iap. Mol Cell Biol 1994; 14: 5212-5222.
3. Deveraux QL, Takahashi R, Salvesen GS, Reed JC. X-linked IAP is a direct inhibitor of cell-death proteases. Nature 1997; 388: 300-304.
4. Eckelman BP, Salvesen GS. The human anti-apoptotic proteins cIAP1 and cIAP2 bind but do not inhibit caspases. J Biol Chem 2006; 281: 3254-3260.
5. Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, Reid GE, et al. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 2000; 102: 43-53.
6. 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: 613-621.
7. Larisch S, Yi Y, Lotan R, Kerner H, Eimerl S, Tony Parks W, et al. A novel mitochondrial septin-like protein, ARTS, mediates apoptosis dependent on its P-loop motif. Nat Cell Biol 2000; 2: 915-921.
8. Du CY, Fang M, Li YC, Li L, Wang XD. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000; 102: 33-42.
9. Gyrd-Hansen M, Darding M, Miasari M, Santoro MM, Zender L, Xue W, et al. IAPs contain an evolutionarily conserved ubiquitin-binding domain that regulates NF-kappaB as well as cell survival and oncogenesis. Nat Cell Biol 2008; 10: 1309-1317.
10. Lopez J, John SW, Tenev T, Rautureau GJP, Hinds MG, Francalanci F, et al. CARDmediated autoinhibition of cIAP1's E3 ligase activity suppresses cell proliferation and migration. Mol Cell 2011; 42: 569-583.
11. Dubrez L, Berthelet J, Glorian V. IAP proteins as targets for drug development in oncology. Onco Targets Ther 2013; 9: 1285-1304.
12. Imoto I, Yang ZQ, Pimkhaokham A, Tsuda H, Shimada Y, Imamura M, et al. Identification of cIAP1 as a candidate target gene within an amplicon at 11q22 in esophageal squamous cell carcinomas. Cancer Res 2001; 61: 6629-6634.
13. Keats JJ, Fonseca R, Chesi M, Schop R, Baker A, Chng W-J, et al. Promiscuous mutations activate the noncanonical NF-kappaB pathway in multiple myeloma. Cancer Cell 2007; 12: 131-144.
14. 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: 11493-11498.
15. 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: 445-456.
16. 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: 682-693.
17. 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: 669-681.
18. Newton K, Manning G. Necroptosis and Inflammation. Annu Rev Biochem 2015; 85: 743-763.
19. Micheau O, Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 2003; 114: 181-190.
20. Pobezinskaya YL, Kim Y-S, Choksi S, Morgan MJ, Li T, Liu C, et al. The function of TRADD in signaling through tumor necrosis factor receptor 1 and TRIF-dependent Tolllike receptors. Nat Immunol 2008; 9: 1047-1054.
21. Ermolaeva MA, Michallet M-C, Papadopoulou N, Utermöhlen O, Kranidioti K, Kollias G, et al. Function of TRADD in tumor necrosis factor receptor 1 signaling and in TRIF-dependent inflammatory responses. Nat Immunol 2008; 9: 1037-1046.
22. 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.
23. Bertrand MJM, Lippens S, Staes A, Gilbert B, Roelandt R, De Medts J, et al. cIAP1/2 are direct E3 ligases conjugating diverse types of ubiquitin chains to receptor interacting proteins kinases 1 to 4 (RIP1-4). PLoS ONE 2011; 6: e22356.
24. O'Donnell MA, Legarda-Addison D, Skountzos P, Yeh WC, Ting AT. Ubiquitination of RIP1 regulates an NF-kappaB-independent cell-death switch in TNF signaling. Curr Biol 2007; 17: 418-424.
25. Dondelinger Y, Jouan-Lanhouet S, Divert T, Theatre E, Bertin J, Gough PJ, et al. NF-?Bindependent role of IKK?/IKK? in preventing RIPK1 kinase-dependent apoptotic and necroptotic cell death during TNF signaling. Mol Cell 2015; 60: 63-76.
26. Gerlach B, Cordier SM, Schmukle AC, Emmerich CH, Rieser E, Haas TL, et al. Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 2011; 471: 591-596.
27. Ea C-K, Deng L, Xia Z-P, Pineda G, Chen ZJ. Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol Cell 2006; 22: 245-257.
28. Li H, Kobayashi M, Blonska M, You Y, Lin X. Ubiquitination of RIP is required for tumor necrosis factor alpha-induced NF-kappaB activation. J Biol Chem 2006; 281: 13636-13643.
29. Micheau O, Lens S, Gaide O, Alevizopoulos K, Tschopp J. NF-kappaB signals induce the expression of c-FLIP. Mol Cell Biol 2001; 21: 5299-5305.
30. 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: 1371-1378.
31. O'Donnell MA, Perez-Jimenez E, Oberst A, Ng A, Massoumi R, Xavier R, et al. Caspase 8 inhibits programmed necrosis by processing CYLD. Nat Cell Biol 2011; 13: 1437-1442.
32. Pop C, Oberst A, Drag M, van Raam BJ, Riedl SJ, Green DR, et al. FLIP Linduces caspase 8 activity in the absence of interdomain caspase 8 cleavage and alters substrate specificity. Biochem J 2011; 433: 447-457.
33. Pop C, Fitzgerald P, Green DR, Salvesen GS. Role of proteolysis in caspase-8 activation and stabilization. Biochemistry 2007; 46: 4398-4407.
34. Hughes MA, Powley IR, Jukes-Jones R, Horn S, Feoktistova M, Fairall L, et al. Co-operative and hierarchical binding of c-FLIP and caspase-8: a unified model defines how c-FLIP isoforms differentially control cell fate. Mol Cell 2016; 61: 834-849.
35. Wang L, Du F, Wang X. TNF-alpha induces two distinct caspase-8 activation pathways. Cell 2008; 133: 693-703.
36. Jin Z, El-Deiry WS. Distinct signaling pathways in TRAIL-versus tumor necrosis factorinduced apoptosis. Mol Cell Biol 2006; 26: 8136-8148.
37. Dondelinger Y, Aguileta MA, Goossens V, Dubuisson C, Grootjans S, Dejardin E, et al. RIPK3 contributes to TNFR1-mediated RIPK1 kinase-dependent apoptosis in conditions of cIAP1/2 depletion or TAK1 kinase inhibition. Cell Death Differ 2013; 20: 1381-1392.
38. Kim JW, Choi EJ, Joe CO. Activation of death-inducing signaling complex (DISC) by pro-apoptotic C-terminal fragment of RIP. Oncogene 2000; 19: 4491-4499.
39. Martinon F, Holler N, Richard C, Tschopp J. Activation of a pro-apoptotic amplification loop through inhibition of NF-kappaB-dependent survival signals by caspase-mediated inactivation of RIP. FEBS Lett 2000; 468: 134-136.
40. Quarato G, Guy CS, Grace CR, Llambi F, Nourse A, Rodriguez DA, et al. Sequential engagement of distinct MLKL phosphatidylinositol-binding sites executes necroptosis. Mol Cell 2016; 61: 589-601.
41. Hildebrand JM, Tanzer MC, Lucet IS, Young SN, Spall SK, Sharma P, et al. Activation of the pseudokinase MLKL unleashes the four-helix bundle domain to induce membrane localization and necroptotic cell death. Proc Natl Acad Sci USA 2014; 111: 15072-15077.
42. Kaiser WJ, Upton JW, Long AB, Livingston-Rosanoff D, Daley-Bauer LP, Hakem R, et al. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 2011; 471: 368-372.
43. Oberst A, Dillon CP, Weinlich R, Mccormick LL, Fitzgerald P, Pop C, et al. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 2011; 471: 363-367.
44. Fulda S. Molecular pathways: targeting inhibitor of apoptosis proteins in cancer-from molecular mechanism to therapeutic application. Clin Cancer Res 2014; 20: 289-295.
45. Geserick P, Hupe M, Moulin M, Wong WW-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: 1037-1054.
46. Weber A, Kirejczyk Z, Besch R, Potthoff S, Leverkus M, Häcker G. Proapoptotic signalling through Toll-like receptor-3 involves TRIF-dependent activation of caspase-8 and is under the control of inhibitor of apoptosis proteins in melanoma cells. Cell Death Differ 2010; 17: 942-951.
47. 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: 449-463.
48. 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: 432-448.
49. Selmi T, Alecci C, dell' Aquila M, Montorsi L, Martello A, Guizzetti F, et al. ZFP36 stabilizes RIP1 via degradation of XIAP and cIAP2 thereby promoting ripoptosome assembly. BMC Cancer 2015; 15: 357-364.
50. Varfolomeev E, Goncharov T, Maecker H, Zobel K, Komuves LG, Deshayes K, et al. Cellular inhibitors of apoptosis are global regulators of NF-B and MAPK activation by members of the TNF family of receptors. Sci Signal 2012; 5: ra22.
51. Vince JE, Chau D, Callus B, Wong WW-L, Hawkins CJ, Schneider P, et al. TWEAK-FN14 signaling induces lysosomal degradation of a cIAP1-TRAF2 complex to sensitize tumor cells to TNF. J Cell Biol 2008; 182: 171-184.
52. Boutaffala L, Bertrand MJM, Remouchamps C, Seleznik G, Reisinger F, Janas M, et al. NIK promotes tissue destruction independently of the alternative NF-?B pathway through TNFR1/RIP1-induced apoptosis. Cell Death Differ 2015; 22: 2020-2033.
53. de Almagro MC, Goncharov T, Newton K, Vucic D. Cellular IAP proteins and LUBAC differentially regulate necrosome-associated RIP1 ubiquitination. Cell Death Dis 2015; 6: e1800.
54. Harlin H, Reffey SB, Duckett CS, Lindsten T, Thompson CB. Characterization of XIAPdeficient mice. Mol Cell Biol 2001; 21: 3604-3608.
55. Conze DB, Albert L, Ferrick DA, Goeddel DV, Yeh WC, Mak T, et al. Posttranscriptional downregulation of c-IAP2 by the ubiquitin protein ligase c-IAP1 in vivo. Mol Cell Biol 2005; 25: 3348-3356.
56. Conte D, Holcik M, Lefebvre C, LaCasse E, Picketts D, Wright K, et al. Inhibitor of apoptosis protein cIAP2 is essential for lipopolysaccharide-induced macrophage survival. Mol Cell Biol 2006; 26: 699.
57. Schile AJ, Garciá-Fernández M, Steller H. Regulation of apoptosis by XIAP ubiquitinligase activity. Genes Dev 2008; 22: 2256-2266.
58. Bauler LD, Duckett CS. O'Riordan MXD. XIAP regulates cytosol-specific innate immunity to Listeria infection. PLoS Pathog 2008; 4: e1000142.
59. Prakash H, Albrecht M, Becker D, Kuhlmann T, Rudel T. Deficiency of XIAP leads to sensitization for Chlamydophila pneumoniae pulmonary infection and dysregulation of innate immune response in mice. J Biol Chem 2010; 285: 20291-20302.
60. Moulin M, Anderton H, Voss AK, Thomas T, Wong WW-L, Bankovacki A, et al. IAPs limit activation of RIP kinases by TNF receptor 1 during development. EMBO J 2012; 31: 1679-1691.
61. Heard KN, Bertrand MJM, Barker PA. cIAP2 supports viability of mice lacking cIAP1 and XIAP. EMBO J 2015; 34: 2393-2395.
62. Kenneth N, Younger J, Hughes E, Marcotte D, Barker P, Saunders T, et al. An inactivating caspase-11 passenger mutation originating from the 129 murine strain in mice targeted for c-Iap1. Biochem J 2012; 443: 355-359.
63. Moulin M, Voss AK, Thomas T, Wong WW-L, Cook WD, Koentgen F, et al. Response to Heard, et al. EMBO J 2015; 34: 2396-2397.
64. Santoro MM, Samuel T, Mitchell T, Reed JC, Stainier DYR. Birc2 (cIap1) regulates endothelial cell integrity and blood vessel homeostasis. Nat Genet 2007; 39: 1397-1402.
65. Wong WW, Vince JE, Lalaoui N, Lawlor KE, Chau D, Bankovacki A, et al. cIAPs and XIAP regulate myelopoiesis through cytokine production in an RIPK1-and RIPK3-dependent manner. Blood 2014; 123: 2562-2572.
66. Lawlor KE, Khan N, Mildenhall A, Gerlic M, Croker BA, D'Cruz AA, et al. RIPK3 promotes cell death and NLRP3 inflammasome activation in the absence of MLKL. Nat Commun 2015; 6: 6282.
67. Gardam S, Turner VM, Anderton H, Limaye S, Basten A, Koentgen F, et al. Deletion of cIAP1 and cIAP2 in murine B lymphocytes constitutively activates cell survival pathways and inactivates the germinal center response. Blood 2011; 117: 4041-4051.
68. Rigaud S, Fondanèche M-C, Lambert N, Pasquier B, Mateo V, Soulas P, et al. XIAP deficiency in humans causes an X-linked lymphoproliferative syndrome. Nature 2006; 444: 110-114.
69. Marsh RA, Madden L, Kitchen BJ, Mody R, McClimon B, Jordan MB, et al. XIAP deficiency: a unique primary immunodeficiency best classified as X-linked familial hemophagocytic lymphohistiocytosis and not as X-linked lymphoproliferative disease. Blood 2010; 116: 1079-1082.
70. Horn PC, Belohradsky BH, Urban C, Weber-Mzell D, Meindl A, Schuster V. Two new families with X-linked inhibitor of apoptosis deficiency and a review of all 26 published cases. J Allergy Clin Immunol 2011; 127: 544-546.
71. Worthey EA, Mayer AN, Syverson GD, Helbling D, Bonacci BB, Decker B, et al. Making a definitive diagnosis: successful clinical application of whole exome sequencing in a child with intractable inflammatory bowel disease. Genet Med 2011; 13: 255-262.
72. Aguilar C, Lenoir C, Lambert N, Bègue B, Brousse N, Canioni D, et al. Characterization of Crohn disease in X-linked inhibitor of apoptosis-deficient male patients and female symptomatic carriers. J Allergy Clin Immunol 2014; 134: 1131-1141.e9.
73. Zeissig Y, Petersen B-S, Milutinovic S, Bosse E, Mayr G, Peuker K, et al. XIAP variants in male Crohn's disease. Gut 2015; 64: 66-76.
74. Gérart S, Siberil S, Martin E, Lenoir C, Aguilar C, Picard C, et al. Human iNKT and MAIT cells exhibit a PLZF-dependent proapoptotic propensity that is counterbalanced by XIAP. Blood 2013; 121: 614-623.
75. Damgaard RB, Nachbur U, Yabal M, Wong WW-L, Fiil BK, Kastirr M, et al. The ubiquitin ligase XIAP recruits LUBAC for NOD2 signaling in inflammation and innate immunity. Mol Cell 2012; 46: 746-758.
76. Bertrand MJM, Doiron K, Labbé K, Korneluk RG, Barker PA, Saleh M. Cellular inhibitors of apoptosis cIAP1 and cIAP2 are required for innate immunity signaling by the pattern recognition receptors NOD1 and NOD2. Immunity 2009; 30: 789-801.
77. Krieg A, Correa RG, Garrison JB, Le Negrate G, Welsh K, Huang Z, et al. XIAP mediates NOD signaling via interaction with RIP2. Proc Natl Acad Sci USA 2009; 106: 14524-14529.
78. Gentle IE, Moelter I, Lechler N, Bambach S, Vucikuja S, Häcker G, et al. Inhibitors of apoptosis proteins (IAPs) are required for effective T-cell expansion/survival during antiviral immunity in mice. Blood 2014; 123: 659-668.
79. Dougan M, Dougan S, Slisz J, Firestone B, Vanneman M, Draganov D, et al. IAP inhibitors enhance co-stimulation to promote tumor immunity. J Exp Med 2010; 207: 2195-2206.
80. Takeda AN, Oberoi-Khanuja TK, Glatz G, Schulenburg K, Scholz RP, Carpy A, et al. Ubiquitin-dependent regulation of MEKK2/3-MEK5-ERK5 signaling module by XIAP and cIAP1. EMBO J 2014; 33: 1784-1801.
81. Dogan T, Harms GS, Hekman M, Karreman C, Oberoi TK, Alnemri ES, et al. X-linked and cellular IAPs modulate the stability of C-RAF kinase and cell motility. Nat Cell Biol 2008; 10: 1447-1455.
82. Yabal M, Müller N, Adler H, Knies N, Groß CJ, Damgaard RB, et al. XIAP restricts TNFand RIP3-dependent cell death and inflammasome activation. Cell Rep 2014; 7: 1796-1808.
83. Vince JE, Wong WW-L, Gentle I, Lawlor KE, Allam R, O'Reilly L, et al. Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation. Immunity 2012; 36: 215-227.
84. Yatim N, Jusforgues-Saklani H, Orozco S, Schulz O, Barreira da Silva R, Reis e Sousa C, et al. RIPK1 and NF-?B signaling in dying cells determines cross-priming of CD8+ T cells. Science 2015; 350: 328-334.
85. Rébé C, Cathelin S, Launay S, Prévotat L, L'Ollivier C, Gyan E, et al. Caspase-8 prevents sustained activation of NF-kappaB in monocytes undergoing macrophagic differentiation. Blood 2007; 109: 1442-1450.
86. McComb S, Aguadé-Gorgorió J, Harder L, Marovca B, Cario G, Eckert C, et al. Activation of concurrent apoptosis and necroptosis by SMAC mimetics for the treatment of refractory and relapsed ALL. Sci Transl Med 2016; 8: 339ra70-339ra70.
87. Zhang T, Zhang Y, Cui M, Jin L, Wang Y, Lv F, et al. CaMKII is a RIP3 substrate mediating ischemia-and oxidative stress-induced myocardial necroptosis. Nat Med 2016; 22: 175-182.