A critical role for cellular inhibitor of protein 2 (cIAP2) in colitis-associated colorectal cancer and intestinal homeostasis mediated by the inflammasome and survival pathways

Mucosal Immunology

Volumn 9, Issue 1, 2016, Pages 146-158

  Dagenais, M ^a   Dupaul Chicoine, J ^a   Champagne, C ^a   Skeldon, A ^a   Morizot, A ^a   Saleh, M ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; INHIBITOR OF APOPTOSIS PROTEIN 2; INTERLEUKIN 18; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK1 PROTEIN; UNCLASSIFIED DRUG; AZOXYMETHANE; BIRC3 PROTEIN, MOUSE; DODECYL SULFATE SODIUM; INFLAMMASOME; INHIBITOR OF APOPTOSIS PROTEIN; RIPK1 PROTEIN, MOUSE; UBIQUITIN PROTEIN LIGASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL PROLIFERATION; COLITIS; COLORECTAL CANCER; CONTROLLED STUDY; CYTOARCHITECTURE; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; ENZYME INHIBITION; HOMEOSTASIS; IMMUNOREGULATION; INTESTINAL HOMEOSTASIS; INTESTINE EPITHELIUM; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; TISSUE REGENERATION; TUMOR VOLUME; ANIMAL; CELL SURVIVAL; CHEMICALLY INDUCED; COLON; COLORECTAL TUMOR; DEFICIENCY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; MALE; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; AZOXYMETHANE; CELL DEATH; CELL SURVIVAL; COLITIS; COLON; COLORECTAL NEOPLASMS; GENE EXPRESSION REGULATION; HUMANS; INFLAMMASOMES; INHIBITOR OF APOPTOSIS PROTEINS; INTERLEUKIN-18; MALE; MICE; MICE, KNOCKOUT; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; SODIUM DODECYL SULFATE; UBIQUITIN-PROTEIN LIGASES;

EID: 84953238596     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2015.46     Document Type: Article

References (73)

1. Asquith, M., & Powrie, F. An innately dangerous balancing act: intestinal homeostasis, inflammation, and colitis-Associated cancer. J. Exp. Med. 207, 1573-1577 (2010
2. Dupaul-Chicoine, J., Dagenais, M., & Saleh, M. Crosstalk between the intestinal microbiota and the innate immune system in intestinal homeostasis and inflammatory bowel disease. Inflamm. Bowel Dis. 19, 2227-2237 (2013
3. Jostins L., et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491, 119-124 (2012
4. Saleh, M., & Trinchieri, G. Innate immune mechanisms of colitis and colitisassociated colorectal cancer. Nat. Rev. Immunol. 11, 9-20 (2011
5. Dagenais, M., Douglas, T., & Saleh, M. Role of programmed necrosis and cell death in intestinal inflammation. Curr. Opin. Gastroenterol. 30, 566-575 (2014
6. Neurath, M.F. Cytokines in inflammatory bowel disease. Nat. Rev. Immunol. 14, 329-342 (2014
7. Darding, M., & Meier, P. IAPs: guardians of RIPK1. Cell Death Differ. 19, 58-66 (2012
8. Bertrand M.J., et al. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol. Cell 30, 689-700 (2008
9. Dannappel M., et al. RIPK1 maintains epithelial homeostasis by inhibiting apoptosis and necroptosis. Nature 513, 90-94 (2014
10. Takahashi N., et al. RIPK1 ensures intestinal homeostasis by protecting the epithelium against apoptosis. Nature 513, 95-99 (2014
11. Vandenabeele, P., Galluzzi, L., Vanden Berghe, T., & Kroemer, G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 11, 700-714 (2010
12. Kaiser W.J., et al. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 471, 368-372 (2011
13. Oberst A., et al. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 471, 363-367 (2011
14. Varfolomeev, E.E., et al. Targeted disruption of the mouse caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity 9, 267-276 (1998
15. Yeh, W.C., et al. FADD: essential for embryo development and signaling from some, but not all, inducers of apoptosis. Science 279, 1954-1958 (1998
16. Yeh W.C., et al. Requirement for Casper (c-FLIP) in regulation of death receptor-induced apoptosis and embryonic development. Immunity 12, 633-642 (2000
17. Zhang, H., Zhou, X., McQuade, T., Li, J., Chan, F.K., & Zhang, J. Functional complementation between FADD and RIP1 in embryos and lymphocytes. Nature 471, 373-376 (2011
18. Gunther C., et al. Caspase-8 regulates TNF-Alpha-induced epithelial necroptosis and terminal ileitis. Nature 477, 335-339 (2011
19. Weinlich R., et al. Protective roles for caspase-8 and cFLIP in adult homeostasis. Cell Rep. 5, 340-348 (2013
20. Welz P.S., et al. FADD prevents RIP3-mediated epithelial cell necrosis and chronic intestinal inflammation. Nature 477, 330-334 (2011
21. Linkermann, A., & Green, D.R. Necroptosis. N. Engl. J. Med. 370, 455-465 (2014
22. Rodrigue-Gervais I.G., et al. Cellular inhibitor of apoptosis protein cIAP2 protects against pulmonary tissue necrosis during influenza virus infection to promote host survival. Cell Host Microbe 15, 23-35 (2014
23. Wallach, D., Kovalenko, A., & Kang, T.B. Necrosome-induced inflammation: must cells die for it? Trends Immunol. 32, 505-509 (2011
24. Kang, T.B., Yang, S.H., Toth, B., Kovalenko, A., & Wallach, D. Activation of the NLRP3 Inflammasome by Proteins That Signal for Necroptosis. Methods Enzymol. 545, 67-81 (2014
25. Gurung P., et al. FADDand caspase-8 mediate priming and activation of the canonical and noncanonical Nlrp3 inflammasomes. J. Immunol. 192, 1835-1846 (2014
26. Moulin M., et al. IAPs limit activation of RIP kinases by TNF receptor 1 during development. EMBO J. 31, 1679-1691 (2012
27. Bertrand, M.J., Doiron, K., Labbe, K., Korneluk, R.G., Barker, P.A., & Saleh, M Cellular inhibitors of apoptosis cIAP1 and cIAP2 are required for innate immunity signaling by the pattern recognition receptors NOD1 and NOD2 Immunity 30 789-801 2009
28. Tseng, P.H., Matsuzawa, A., Zhang, W., Mino, T., Vignali, D.A., & Karin, M. Different modes of ubiquitination of the adaptor TRAF3 selectively activate the expression of type I interferons and proinflammatory cytokines. Nat. Immunol. 11, 70-75 (2010
29. Labbe, K., McIntire, C.R., Doiron, K., Leblanc, P.M., & Saleh, M. Cellular inhibitors of apoptosis proteins cIAP1 and cIAP2 are required for efficient caspase-1 activation by the inflammasome. Immunity 35, 897-907 (2011
30. Petersen S.L., et al. Autocrine TNFalpha signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis. Cancer Cell 12, 445-456 (2007
31. Varfolomeev, E., et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell 131, 669-681 (2007
32. Vince J.E., et al. IAP antagonists target cIAP1 to induce TNFalphadependent apoptosis. Cell 131, 682-693 (2007
33. Beug S.T., et al. Smac mimetics and innate immune stimuli synergize to promote tumor death. Nat. Biotechnol. 32, 182-190 (2014
34. Seidelin, J.B., Vainer, B., Andresen, L., & Nielsen, O.H. Upregulation of cIAP2 in regenerating colonocytes in ulcerative colitis. Virchows Arch. 451, 1031-1038 (2007
35. Karasawa H., et al. Down-regulation of cIAP2 enhances 5-FU sensitivity through the apoptotic pathway in human colon cancer cells. Cancer Sci. 100, 903-913 (2009
36. Krajewska M., et al. Analysis of apoptosis protein expression in early-stage colorectal cancer suggests opportunities for new prognostic biomarkers. Clin. Cancer Res. 11, 5451-5461 (2005
37. Miura K., et al. Inhibitor of apoptosis protein family as diagnostic markers and therapeutic targets of colorectal cancer. Surg. Today 41, 175-182 (2011
38. Conte D., et al. Inhibitor of apoptosis protein cIAP2 is essential for lipopolysaccharide-induced macrophage survival. Mol. Cell. Biol. 26, 699-708 (2006
39. Kayagaki N., et al. Non-canonical inflammasome activation targets caspase-11. Nature 479, 117-121 (2011
40. 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. 443 355-359 2012
41. Gyrd-Hansen, M., & Meier, P. IAPs: from caspase inhibitors tomodulators of NF-kappaB, inflammation and cancer. Nat. Rev. Cancer 10, 561-574 (2010
42. Gonzalez-Lopez, M., 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. 21, 4332-4336 (2011
43. Huber S., et al. IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine. Nature 491, 259-263 (2012
44. Allen I.C., et al. The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitis-Associated cancer. J. Exp. Med. 207, 1045-1056 (2010
45. Dupaul-Chicoine, J., et al. Control of intestinal homeostasis, colitis, and colitis-Associated colorectal cancer by the inflammatory caspases. Immunity 32, 367-378 (2010
46. Elinav E., et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 145, 745-757 (2011
47. Salcedo R., et al. MyD88-mediated signaling prevents development of adenocarcinomas of the colon: role of interleukin 18. J. Exp. Med. 207, 1625-1636 (2010
48. Wlodarska M., et al. NLRP6 inflammasome orchestrates the colonic hostmicrobial interface by regulating goblet cell mucus secretion. Cell 156, 1045-1059 (2014
49. Zaki, M.H., Boyd, K.L., Vogel, P., Kastan, M.B., Lamkanfi, M., & Kanneganti, T.D. The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis. Immunity 32, 379-391 (2010a
50. Demon, D., Kuchmiy, A., Fossoul, A., Zhu, Q., Kanneganti, T.D., & Lamkanfi, M. Caspase-11 is expressed in the colonic mucosa and protects against dextran sodium sulfate-induced colitis. Mucosal Immunol. 7, 1480-1491 (2014
51. Oficjalska K., et al. Protective role for caspase-11 during acute experimental murine colitis. J. Immunol. 194, 1252-1260 (2015
52. Grivennikov S., et al. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-Associated cancer. Cancer Cell 15, 103-113 (2009
53. Putoczki T.L., et al. Interleukin-11 is the dominant IL-6 family cytokine during gastrointestinal tumorigenesis and can be targeted therapeutically. Cancer Cell 24, 257-271 (2013
54. Feoktistova, M., et al. cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol. Cell 43, 449-463 (2011
55. Tenev, T., et al. The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol. Cell 43, 432-448 (2011
56. Vanden Berghe, T., Linkermann, A., Jouan-Lanhouet, S., Walczak, H., & Vandenabeele, P. Regulated necrosis: the expanding network of nonapoptotic cell death pathways. Nat. Rev. Mol. Cell Biol. 15, 135-147 (2014
57. Duprez, L., Bertrand, M.J., Vanden Berghe, T., Dondelinger, Y., Festjens, N., & Vandenabeele, P. Intermediate domain of receptor-interacting protein kinase 1 (RIPK1) determines switch between necroptosis and RIPK1 kinase-dependent apoptosis. J. Biol. Chem. 287, 14863-14872 (2012
58. Basu R., et al. IL-1 signaling modulates activation of STAT transcription factors to antagonize retinoic acid signaling and control the TH17 cell-iTreg cell balance. Nat. Immunol. 16, 286-295 (2015
59. Zaki, M.H., Vogel, P., Body-Malapel, M., Lamkanfi, M., & Kanneganti, T.D. IL-18 production downstream of the Nlrp3 inflammasome confers protection against colorectal tumor formation. J. Immunol. 185, 4912-4920 (2010b
60. Greten F.R., et al. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-Associated cancer. Cell 118, 285-296 (2004
61. Qiu W., et al. An apoptosis-independent role of SMAC in tumor suppression. Oncogene 32, 2380-2389 (2013
62. Damgaard R.B., et al. Disease-causing mutations in the XIAP BIR2 domain impair NOD2-dependent immune signalling. EMBO Mol. Med. 5, 1278-1295 (2013
63. Filipovich, A.H., Zhang, K., Snow, A.L., & Marsh, R.A. X-linked lymphoproliferative syndromes: brothers or distant cousins? Blood 116, 3398-3408 (2010
64. Marsh R.A., et al. Allogeneic hematopoietic cell transplantation for XIAP deficiency: an international survey reveals poor outcomes. Blood 121, 877-883 (2013
65. 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 117, 1522-1529 (2011
66. Rigaud S., et al. XIAP deficiency in humans causes an X-linked lymphoproliferative syndrome. Nature 444, 110-114 (2006
67. Speckmann C., et al. X-linked inhibitor of apoptosis (XIAP) deficiency: the spectrum of presenting manifestations beyond hemophagocytic lymphohistiocytosis. Clin. Immunol. 149, 133-141 (2013
68. Yang X., et al. Clinical and genetic characteristics of XIAP deficiency in Japan. J. Clin. Immunol. 32, 411-420 (2012
69. Zeissig Y., et al. XIAP variants in male Crohns disease. Gut 64, 66-76 (2014
70. Nenci A., et al. Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 446, 557-561 (2007
71. Qiu W., et al. PUMA-mediated intestinal epithelial apoptosis contributes to ulcerative colitis in humans and mice. J. Clin. Invest. 121, 1722-1732 (2011
72. Qiu, W., Carson-Walter, E.B., Kuan, S.F., Zhang, L., & Yu, J. PUMA suppresses intestinal tumorigenesis in mice. Cancer Res. 69, 4999-5006 (2009
73. Newton, K., Sun, X., & Dixit, V.M. Kinase RIP3 is dispensable for normal NF-kappa Bs, signaling by the B-cell and T-cell receptors, tumor necrosis factor receptor 1, and Toll-like receptors 2 and 4. Mol. Cell. Biol. 24, 1464-1469 (2004