Modulation of immune signalling by inhibitors of apoptosis

Trends in Immunology

Volumn 33, Issue 11, 2012, Pages 535-545

  Beug, Shawn T ^a   Cheung, Herman H ^a,c   LaCasse, Eric C ^a   Korneluk, Robert G ^a,b  

^a CHILDREN S HOSPITAL OF EASTERN ONTARIO   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c ONTARIO INSTITUTE FOR CANCER RESEARCH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; INHIBITOR OF APOPTOSIS PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN 1; INHIBITOR OF APOPTOSIS PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE; NEURONAL APOPTOSIS INHIBITORY PROTEIN; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; UBIQUITIN PROTEIN LIGASE; X LINKED INHIBITOR OF APOPTOSIS;

ADAPTIVE IMMUNITY; HUMAN; IMMUNOMODULATION; INNATE IMMUNITY; NONHUMAN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

ADAPTIVE IMMUNITY; ANIMALS; APOPTOSIS; HUMANS; IMMUNITY, INNATE; INHIBITOR OF APOPTOSIS PROTEINS; NF-KAPPA B; SIGNAL TRANSDUCTION;

EID: 84867902828     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2012.06.004     Document Type: Review

References (102)

1. Baud V., Karin M. Is NF-kappaB a good target for cancer therapy? Hopes and pitfalls. Nat. Rev. Drug Discov. 2009, 8:33-40.
2. Mace P.D., et al. Assembling the building blocks: structure and function of inhibitor of apoptosis proteins. Cell Death Differ. 2010, 17:46-53.
3. Mehrotra S., et al. IAP regulation of metastasis. Cancer Cell 2010, 17:53-64.
4. Bertrand M.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.
5. Petersen S.L., et al. Autocrine TNFalpha signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis. Cancer Cell 2007, 12:445-456.
6. Varfolomeev E., et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell 2007, 131:669-681.
7. Vince J.E., et al. IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis. Cell 2007, 131:682-693.
8. Fulda S., Vucic D. Targeting IAP proteins for therapeutic intervention in cancer. Nat. Rev. Drug Discov. 2012, 11:109-124.
9. Dickens L.S., et al. The 'complexities' of life and death: death receptor signalling platforms. Exp. Cell Res. 2012, 318:1269-1277.
10. Tseng P.H., et al. Different modes of ubiquitination of the adaptor TRAF3 selectively activate the expression of type I interferons and proinflammatory cytokines. Nat. Immunol. 2010, 11:70-75.
11. Zarnegar B.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.
12. Dougan M., et al. IAP inhibitors enhance co-stimulation to promote tumor immunity. J. Exp. Med. 2010, 207:2195-2206.
13. Muller-Sienerth N., et al. SMAC mimetic BV6 induces cell death in monocytes and maturation of monocyte-derived dendritic cells. PLoS ONE 2010, 6:e21556.
14. Mayer B.A., et al. Inhibitor of apoptosis proteins as novel targets in inflammatory processes. Arterioscler. Thromb. Vasc. Biol. 2011, 31:2240-2250.
15. Mao A.P., et al. Virus-triggered ubiquitination of TRAF3/6 by cIAP1/2 is essential for induction of interferon-beta (IFN-beta) and cellular antiviral response. J. Biol. Chem. 2010, 285:9470-9476.
16. Bertrand M.J., et al. 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.
17. Krieg A., et al. XIAP mediates NOD signaling via interaction with RIP2. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:14524-14529.
18. Bauler L.D., et al. XIAP regulates cytosol-specific innate immunity to Listeria infection. PLoS Pathog. 2008, 4:e1000142.
19. Prakash H., et al. 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.
20. Zamboni D.S., et al. The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat. Immunol. 2006, 7:318-325.
21. Vinzing M., et al. NAIP and Ipaf control Legionella pneumophila replication in human cells. J. Immunol. 2008, 180:6808-6815.
22. Labbe K., et al. Cellular inhibitors of apoptosis proteins cIAP1 and cIAP2 are required for efficient caspase-1 activation by the inflammasome. Immunity 2011, 35:897-907.
23. Gardam S., 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.
24. Vallabhapurapu S., et al. Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-kappa B signaling. Nat. Immunol. 2008, 9:1364-1370.
25. Filipovich A.H. The expanding spectrum of hemophagocytic lymphohistiocytosis. Curr. Opin. Allergy Clin. Immunol. 2011, 11:512-516.
26. Ganesan S., et al. NF-kappaB/Rel proteins and the humoral immune responses of Drosophila melanogaster. Curr. Top. Microbiol. Immunol. 2010, 349:25-60.
27. Vince J.E., et al. Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation. Immunity 2012, 36:215-227.
28. Hayden M.S., Ghosh S. NF-kappaB in immunobiology. Cell Res. 2011, 21:223-244.
29. Mahoney D.J., et al. Both cIAP1 and cIAP2 regulate TNFalpha-mediated NF-kappaB activation. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:11778-11783.
30. Varfolomeev E., et al. c-IAP1 and c-IAP2 are critical mediators of tumor necrosis factor alpha (TNFalpha)-induced NF-kappaB activation. J. Biol. Chem. 2008, 283:24295-24299.
31. Gaither A., 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.
32. Damgaard R.B., et al. The ubiquitin ligase XIAP recruits LUBAC for NOD2 signaling in inflammation and innate immunity. Mol. Cell 2012, 46:1-13.
33. Yang Y.B., et al. NOD2 pathway activation by MDP or Mycobacterium tuberculosis infection involves the stable polyubiquitination of Rip2. J. Biol. Chem. 2007, 282:36223-36229.
34. Kenneth N.S., 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.
35. Kayagaki N., et al. Non-canonical inflammasome activation targets caspase-11. Nature 2011, 479:117-121.
36. Kofoed E.M., Vance R.E. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 2011, 477:592-595.
37. Zhao Y., et al. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 2011, 477:596-600.
38. Diez E., et al. Birc1e is the gene within the Lgn1 locus associated with resistance to Legionella pneumophila. Nat. Genet. 2003, 33:55-60.
39. Wright E.K., et al. Naip5 affects host susceptibility to the intracellular pathogen Legionella pneumophila. Curr. Biol. 2003, 13:27-36.
40. Lightfield K.L., et al. Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat. Immunol. 2008, 9:1171-1178.
41. Romanish M.T., et al. A novel protein isoform of the multicopy human NAIP gene derives from intragenic Alu SINE promoters. PLoS ONE 2009, 4:e5761.
42. Oshiumi H., et al. Riplet/RNF135, a RING finger protein, ubiquitinates RIG-I to promote interferon-beta induction during the early phase of viral infection. J. Biol. Chem. 2009, 284:807-817.
43. Gack M.U., et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 2007, 446:916-920.
44. Parvatiyar K., et al. TAX1BP1 and A20 inhibit antiviral signaling by targeting TBK1-IKKi kinases. J. Biol. Chem. 2010, 285:14999-15009.
45. Nakhaei P., et al. I kappa B kinase epsilon-dependent phosphorylation and degradation of X-linked inhibitor of apoptosis sensitizes cells to virus-induced apoptosis. J. Virol. 2012, 86:726-737.
46. White C.L., et al. Phosphatidylinositol 3-kinase signaling delays Sendai virus-induced apoptosis by preventing XIAP degradation. J. Virol. 2011, 85:5224-5227.
47. Varfolomeev E., et al. Cellular inhibitors of apoptosis are global regulators of NF-kappaB and MAPK activation by members of the TNF family of receptors. Sci. Signal. 2012, 5:ra22.
48. Keats J.J., et al. Promiscuous mutations activate the noncanonical NF-kappaB pathway in multiple myeloma. Cancer Cell 2007, 12:131-144.
49. Annunziata C.M., et al. Frequent engagement of the classical and alternative NF-kappaB pathways by diverse genetic abnormalities in multiple myeloma. Cancer Cell 2007, 12:115-130.
50. Rigaud S., et al. XIAP deficiency in humans causes an X-linked lymphoproliferative syndrome. Nature 2006, 444:110-114.
51. Pachlopnik Schmid J., et al. Clinical similarities and differences of patients with X-linked lymphoproliferative syndrome type 1 (XLP-1/SAP deficiency) versus type 2 (XLP-2/XIAP deficiency). Blood 2010, 117:1522-1529.
52. Worthey E.A., 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.
53. Yang X., et al. Clinical and genetic characteristics of XIAP deficiency in Japan. J. Clin. Immunol. 2012, 32:411-420.
54. Marsh R.A., et al. Patients with X-linked lymphoproliferative disease due to BIRC4 mutation have normal invariant natural killer T-cell populations. Clin. Immunol. 2009, 132:116-123.
55. Rumble J.M., et al. Phenotypic differences between mice deficient in XIAP and SAP, two factors targeted in X-linked lymphoproliferative syndrome (XLP). Cell. Immunol. 2009, 259:82-89.
56. Flygare J.A., Fairbrother W.J. Small-molecule pan-IAP antagonists: a patent review. Expert Opin. Ther. Patents 2010, 20:251-267.
57. Darding M., et al. Molecular determinants of Smac mimetic induced degradation of cIAP1 and cIAP2. Cell Death Differ. 2011, 18:1376-1386.
58. Dueber E.C., et al. Antagonists induce a conformational change in cIAP1 that promotes autoubiquitination. Science 2011, 334:376-380.
59. Feltham R., et al. Smac mimetics activate the E3 ligase activity of cIAP1 protein by promoting RING domain dimerization. J. Biol. Chem. 2011, 286:17015-17028.
60. Vince J.E., et al. TWEAK-FN14 signaling induces lysosomal degradation of a cIAP1-TRAF2 complex to sensitize tumor cells to TNFalpha. J. Cell Biol. 2008, 182:171-184.
61. Lightfield K.L., et al. Differential requirements for NAIP5 in activation of the NLRC4 inflammasome. Infect. Immun. 2011, 79:1606-1614.
62. Conze D.B., et al. Posttranscriptional downregulation of c-IAP2 by the ubiquitin protein ligase c-IAP1 in vivo. Mol. Cell. Biol. 2005, 25:3348-3356.
63. Yang Y., et al. Ubiquitin protein ligase activity of IAPs and their degradation in proteasomes in response to apoptotic stimuli. Science 2000, 288:874-877.
64. Prakash H., et al. cIAP-1 controls innate immunity to C. pneumoniae pulmonary infection. PLoS ONE 2009, 4:e6519.
65. McComb S., et al. cIAP1 and cIAP2 limit macrophage necroptosis by inhibiting Rip1 and Rip3 activation. Cell Death Differ. 2012, 10.1038/cdd.2012.59.
66. Conte D., et al. Inhibitor of apoptosis protein cIAP2 is essential for lipopolysaccharide-induced macrophage survival. Mol. Cell. Biol. 2006, 26:699-708.
67. Conze D.B., et al. Non-canonical NF-kappaB activation and abnormal B cell accumulation in mice expressing ubiquitin protein ligase-inactive c-IAP2. PLoS Biol. 2010, 8:e1000518.
68. Baens M., et al. Selective expansions of marginal zone B cells in Emicro-AP12-MALT1 mice is linked to enhanced IkappaB kinase gamma polyubiquitination. Cancer Res. 2006, 66:5270-5277.
69. Sagaert X., et al. Splenic marginal zone lymphoma-like features in API2-MALT1 transgenic mice that are exposed to antigenic stimulation. Haematologica 2006, 91:1693-1696.
70. Harlin H., et al. Characterization of XIAP-deficient mice. Mol. Cell. Biol. 2001, 21:3604-3608.
71. Jost P.J., et al. XIAP discriminates between type I and type II FAS-induced apoptosis. Nature 2009, 460:1035-1039.
72. Conte D., et al. Thymocyte-targeted overexpression of xiap transgene disrupts T lymphoid apoptosis and maturation. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:5049-5054.
73. Moore C.S., et al. Increased X-linked inhibitor of apoptosis protein (XIAP) expression exacerbates experimental autoimmune encephalomyelitis (EAE). J. Neuroimmunol. 2008, 203:79-93.
74. Schile A.J., et al. Regulation of apoptosis by XIAP ubiquitin-ligase activity. Genes Dev. 2008, 22:2256-2266.
75. Garcia-Fernandez M., et al. Sept4/ARTS is required for stem cell apoptosis and tumor suppression. Genes Dev. 2010, 24:2282-2293.
76. Leung C.G., et al. Requirements for survivin in terminal differentiation of erythroid cells and maintenance of hematopoietic stem and progenitor cells. J. Exp. Med. 2007, 204:1603-1611.
77. Conway E.M., et al. Deficiency of survivin in transgenic mice exacerbates Fas-induced apoptosis via mitochondrial pathways. Gastroenterology 2002, 123:619-631.
78. Uren A.G., et al. Survivin and the inner centromere protein INCENP show similar cell-cycle localization and gene knockout phenotype. Curr. Biol. 2000, 10:1319-1328.
79. Hikita S., et al. Overexpression of TIAP/m-survivin in thymocytes enhances cell proliferation. Mol. Immunol. 2002, 39:289-298.
80. Small S., et al. Overexpression of survivin initiates hematologic malignancies in vivo. Leukemia 2010, 24:1920-1926.
81. Boniotto M., et al. Population variation in NAIP functional copy number confers increased cell death upon Legionella pneumophila infection. Hum. Immunol. 2011, 73:196-200.
82. Braggio E., et al. Identification of copy number abnormalities and inactivating mutations in two negative regulators of nuclear factor-kappaB signaling pathways in Waldenstrom's macroglobulinemia. Cancer Res. 2009, 69:3579-3588.
83. Rossi D., et al. Alteration of BIRC3 and multiple other NF-kappaB pathway genes in splenic marginal zone lymphoma. Blood 2011, 118:4930-4934.
84. Rossi D., et al. Disruption of BIRC3 associates with fludarabine chemorefractoriness in TP53 wild-type chronic lymphocytic leukemia. Blood 2012, 119:2854-2862.
85. Dierlamm J., et al. The apoptosis inhibitor gene AP12 and a novel 18q gene, MLT, are recurrently rearranged in the t(11;18)(q21;q21) associated with mucosa-associated lymphoid tissue lymphomas. Blood 1999, 93:3601-3609.
86. Izumiyama K., et al. Stability and subcellular localization of API2-MALT1 chimeric protein involved in t(11;18) (q21;q21) MALT lymphoma. Oncogene 2003, 22:8085-8092.
87. Noels H., et al. A novel TRAF6 binding site in MALT1 defines distinct mechanisms of NF-kappa B activation by API2-MALT1 fusions. J. Biol. Chem. 2007, 282:10180-10189.
88. Garrison J.B., et al. TRAF2-binding BIR1 domain of c-IAP2/MALT1 fusion protein is essential for activation of NF-kappaB. Oncogene 2009, 28:1584-1593.
89. Coornaert B., et al. T cell antigen receptor stimulation induces MALT1 paracaspase-mediated cleavage of the NF-kappaB inhibitor A20. Nat. Immunol. 2008, 9:263-271.
90. Hosokowa Y. Anti-apoptotic action of AP12-MALT1 fusion protein involved in t(11;18)(q21;q21) MALT lymphoma. Apoptosis 2005, 10:25-34.
91. Staal J., et al. Regulation of NF-kappaB signaling by caspases and MALT1 paracaspase. Cell Res. 2011, 21:40-54.
92. Lucas P.C., et al. A dual role for the API2 moiety in API2-MALT1-dependent NF-kappaB activation: heterotypic oligomerization and TRAF2 recruitment. Oncogene 2007, 26:5643-5654.
93. Ho L., et al. MALT1 and the API2-MALT1 fusion act between CD40 and IKK and confer NF-kappa B-dependent proliferative advantage and resistance against FAS-induced cell death in B cells. Blood 2005, 105:2891-2899.
94. Rosebeck S., et al. Cleavage of NIK by the API2-MALT1 fusion oncoprotein leads to noncanonical NF-kappaB activation. Science 2011, 331:468-472.
95. Murga Penas E.M., et al. The translocations t(6;18;11)(q24;q21;q21) and t(11;14;18)(q21;q32;q21) lead to a fusion of the API2 and MALT1 genes and occur in MALT lymphomas. Haematologica 2007, 92:405-409.
96. Marsh R.A., et al. A rapid flow cytometric screening test for X-linked lymphoproliferative disease due to XIAP deficiency. Cytometry B Clin. Cytom. 2009, 76:334-344.
97. Rezaei N., et al. X-linked lymphoproliferative syndrome: a genetic condition typified by the triad of infection, immunodeficiency and lymphoma. Br. J. Haematol. 2010, 152:13-30.
98. Ferretti M., et al. The 423Q polymorphism of the X-linked inhibitor of apoptosis gene influences monocyte function and is associated with periodic fever. Arthritis Rheum. 2009, 60:3476-3484.
99. Zhizhuo H., et al. Screening the PRF1, UNC13D, STX11, SH2D1A, XIAP, and ITK gene mutations in Chinese children with Epstein-Barr virus-associated hemophagocytic lymphohistiocytosis. Pediatr. Blood Cancer 2012, 58:410-414.
100. Marsh R.A., 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.
101. Rigaud S., et al. Human X-linked variable immunodeficiency caused by a hypomorphic mutation in XIAP in association with a rare polymorphism in CD40LG. Blood 2011, 118:252-261.
102. Zhao M., et al. A novel XIAP mutation in a Japanese boy with recurrent pancytopenia and splenomegaly. Haematologica 2010, 95:688-689.