XIAP deficiency syndrome in humans

Seminars in Cell and Developmental Biology

Volumn 39, Issue , 2015, Pages 115-123

  Latour, Sylvain ^a   Aguilar, Claire ^a  

^a IMAGINE INSTITUTE   (France)

Author keywords

HLH hemophagocytic lymphohistiocytosis; IBD inflammatory bowel disease; Immunodeficiency; Inflammation; Innate immunity; XIAP X linked inhibitor of apoptosis

Indexed keywords

AZATHIOPRINE; CORTICOSTEROID; CRYOPYRIN; CYCLOSPORIN; CYTOKINE; ETOPOSIDE; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; MESALAZINE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ANTIBODY; X LINKED INHIBITOR OF APOPTOSIS; XIAP PROTEIN, HUMAN;

CLINICAL FEATURE; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; EPSTEIN BARR VIRUS; GENE MUTATION; HEMOPHAGOCYTIC SYNDROME; HUMAN; INFLAMMATORY BOWEL DISEASE; INNATE IMMUNITY; LYMPHOPROLIFERATIVE DISEASE; NONHUMAN; REVIEW; X CHROMOSOME LINKED DISORDER; X LINKED INHIBITOR OF APOPTOSIS DEFICIENCY; ANIMAL; GENETICS; IMMUNOLOGY; INFLAMMATION; PATHOLOGY;

HUMAN HERPESVIRUS 4;

ANIMALS; GENETIC DISEASES, X-LINKED; HUMANS; IMMUNITY, INNATE; INFLAMMATION; LYMPHOPROLIFERATIVE DISORDERS; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 84928208327     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2015.01.015     Document Type: Review

References (83)

1. Rigaud S., Fondaneche 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.
2. Tangye S.G. XLP: clinical features and molecular etiology due to mutations in SH2D1A encoding SAP. J Clin Immunol 2014, 34:772-779.
3. Usmani G.N., Woda B.A., Newburger P.E. Advances in understanding the pathogenesis of HLH. Br J Haematol 2013, 161:609-622.
4. Janka G.E. Familial and acquired hemophagocytic lymphohistiocytosis. Annu Rev Med 2012, 63:233-246.
5. Eckelman B.P., Salvesen G.S., Scott F.L. Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep 2006, 7:988-994.
6. Galban S., Duckett C.S. XIAP as a ubiquitin ligase in cellular signaling. Cell Death Differ 2009, 17:54-60.
7. Kenneth N.S., Duckett C.S. IAP proteins: regulators of cell migration and development. Curr Opin Cell Biol 2012, 24:871-875.
8. Wang C., Deng L., Hong M., Akkaraju G.R., Inoue J., Chen Z.J. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 2001, 412:346-351.
9. Gyrd-Hansen M., Darding M., Miasari M., Santoro M.M., 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. 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 2009, 30:789-801.
11. Philpott D.J., Sorbara M.T., Robertson S.J., Croitoru K., Girardin S.E. NOD proteins: regulators of inflammation in health and disease. Nat Rev Immunol 2014, 14:9-23.
12. Sabbah A., Chang T.H., Harnack R., Frohlich V., Tominaga K., Dube P.H., et al. Activation of innate immune antiviral responses by Nod2. Nat Immunol 2009, 10:1073-1080.
13. Kapoor A., Forman M., Arav-Boger R. Activation of nucleotide oligomerization domain 2 (NOD2) by human cytomegalovirus initiates innate immune responses and restricts virus replication. PLOS ONE 2014, 9:e92704.
14. Park J.H., Kim Y.G., Shaw M., Kanneganti T.D., Fujimoto Y., Fukase K., et al. Nod1/RICK and TLR signaling regulate chemokine and antimicrobial innate immune responses in mesothelial cells. J Immunol 2007, 179:514-521.
15. Hasegawa M., Fujimoto Y., Lucas P.C., Nakano H., Fukase K., Nunez G., et al. A critical role of RICK/RIP2 polyubiquitination in Nod-induced NF-kappaB activation. EMBO J 2008, 27:373-383.
16. Krieg A., Correa R.G., Garrison J.B., Le Negrate G., Welsh K., Huang Z., et al. XIAP mediates NOD signaling via interaction with RIP2. Proc Natl Acad Sci U S A 2009, 106:14524-14529.
17. Damgaard R.B., Nachbur U., Yabal M., Wong W.W., Fiil B.K., Kastirr M., et al. The ubiquitin ligase XIAP Recruits LUBAC for NOD2 signaling in inflammation and innate immunity. Mol Cell 2012, 46:1-13.
18. Damgaard R.B., Fiil B.K., Speckmann C., Yabal M., Stadt U.Z., Bekker-Jensen S., et al. Disease-causing mutations in the XIAP BIR2 domain impair NOD2-dependent immune signalling. EMBO Mol Med 2013, 5:1278-1295.
19. Hsieh W.C., Chuang Y.T., Chiang I.H., Hsu S.C., Miaw S.C., Lai M.Z. Inability to resolve specific infection generates innate immunodeficiency syndrome in Xiap-/- mice. Blood 2014, 124:2847-2857.
20. Moulin M., Anderton H., Voss A.K., Thomas T., Wong W.W., Bankovacki A., et al. IAPs limit activation of RIP kinases by TNF receptor 1 during development. EMBO J 2012, 31:1679-1691.
21. Bertrand M.J., Milutinovic S., Dickson K.M., Ho W.C., 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.
22. Vanden Berghe T., Linkermann A., Jouan-Lanhouet S., Walczak H., Vandenabeele P. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat Rev Mol Cell Biol 2014, 15:135-147.
23. Yabal M., Muller N., Adler H., Knies N., Gross C.J., Damgaard R.B., et al. XIAP restricts TNF- and RIP3-dependent cell death and inflammasome activation. Cell Rep 2014, 7:1796-1808.
24. Vince J.E., Wong W.W., Gentle I., Lawlor K.E., Allam R., O'Reilly L., et al. Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation. Immunity 2012, 36:215-227.
25. Wong W.W., Vince J.E., Lalaoui N., Lawlor K.E., 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.
26. Abulafia D.P., de Rivero Vaccari J.P., Lozano J.D., Lotocki G., Keane R.W., Dietrich W.D. Inhibition of the inflammasome complex reduces the inflammatory response after thromboembolic stroke in mice. J Cereb Blood Flow Metab 2009, 29:534-544.
27. de Rivero Vaccari J.P., Lotocki G., Marcillo A.E., Dietrich W.D., Keane R.W. A molecular platform in neurons regulates inflammation after spinal cord injury. J Neurosci 2008, 28:3404-3414.
28. Harlin H., Reffey S.B., Duckett C.S., Lindsten T., Thompson C.B. Characterization of XIAP-deficient mice. Mol Cell Biol 2001, 21:3604-3608.
29. Olayioye M.A., Kaufmann H., Pakusch M., Vaux D.L., Lindeman G.J., Visvader J.E. XIAP-deficiency leads to delayed lobuloalveolar development in the mammary gland. Cell Death Differ 2005, 12:87-90.
30. Bauler L.D., Duckett C.S., O'Riordan M.X. XIAP regulates cytosol-specific innate immunity to Listeria infection. PLoS Pathog 2008, 4:e1000142.
31. 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.
32. Andree M., Seeger J.M., Schull S., Coutelle O., Wagner-Stippich D., Wiegmann K., et al. BID-dependent release of mitochondrial SMAC dampens XIAP-mediated immunity against Shigella. EMBO J 2014, 33:2171-2187.
33. Girardin S.E., Tournebize R., Mavris M., Page A.L., Li X., Stark G.R., et al. CARD4/Nod1 mediates NF-kappaB and JNK activation by invasive Shigella flexneri. EMBO Rep 2001, 2:736-742.
34. Bai L., Smith D.C., Wang S. Small-molecule SMAC mimetics as new cancer therapeutics. Pharmacol Ther 2014, 144:82-95.
35. Gentle I.E., Moelter I., Lechler N., Bambach S., Vucikuja S., Hacker 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.
36. Pachlopnik Schmid J., Canioni D., Moshous D., Touzot F., Mahlaoui N., Hauck F., 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 2011, 117:1522-1529.
37. Marsh R.A., Madden L., Kitchen B.J., Mody R., McClimon B., Jordan M.B., 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, 7:1079-1082.
38. Yang X., Kanegane H., Nishida N., Imamura T., Hamamoto K., Miyashita R., et al. Clinical and genetic characteristics of XIAP deficiency in Japan. J Clin Immunol 2012, 32:411-420.
39. Horn P.C., Belohradsky B.H., 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.
40. Speckmann C., Lehmberg K., Albert M.H., Damgaard R.B., Fritsch M., Gyrd-Hansen M., et al. X-linked inhibitor of apoptosis (XIAP) deficiency: the spectrum of presenting manifestations beyond hemophagocytic lymphohistiocytosis. Clin Immunol 2013, 149:133-141.
41. Rigaud S., Lopez-Granados E., Siberil S., Gloire G., Lambert N., Lenoir C., 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.
42. Worthey E.A., Mayer A.N., Syverson G.D., Helbling D., Bonacci B.B., 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.
43. Aguilar C., Lenoir C., Lambert N., Begue 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, (June). pii:S0091-6749(14)00606-X. 10.1016/j.jaci.2014.04.031.
44. Zeissig Y., Petersen B.S., Milutinovic S., Bosse E., Mayr G., Peuker K., et al. XIAP variants in male Crohn's disease. Gut 2014, 2014(February). 10.1136/gutjnl-2013-306520.
45. Speckmann C., Ehl S. XIAP deficiency is a mendelian cause of late-onset IBD. Gut 2013, (December). [Epub ahead of print]. 10.1136/gutjnl-2013-306474.
46. Zhao M., Kanegane H., Ouchi K., Imamura T., Latour S., Miyawaki T. A novel XIAP mutation in a Japanese boy with recurrent pancytopenia and splenomegaly. Haematologica 2009, 95:688-689.
47. Ammann S., Elling R., Gyrd-Hansen M., Duckers G., Bredius R., Burns S.O., et al. A new functional assay for the diagnosis of X-linked inhibitor of apoptosis (XIAP) deficiency. Clin Exp Immunol 2014, [Epub ahead of print]. 10.1111/cei.12306.
48. Wada T., Kanegane H., Ohta K., Katoh F., Imamura T., Nakazawa Y., et al. Sustained elevation of serum interleukin-18 and its association with hemophagocytic lymphohistiocytosis in XIAP deficiency. Cytokine 2014, 65:74-78.
49. Beser O.F., Conde C.D., Kutlu T., Cokugras F.C., Boztug K., Erkan T. Inflammatory bowel disease with lethal disease course caused by a nonsense mutation in BIRC4 Encoding X-linked inhibitor of apoptosis protein (XIAP). J Pediatr Gastroenterol Nutr 2014, 10.1097/MPG.0000000000000504.
50. Pedersen J., LaCasse E.C., Seidelin J.B., Coskun M., Nielsen O.H. Inhibitors of apoptosis (IAPs) regulate intestinal immunity and inflammatory bowel disease (IBD) inflammation. Trends Mol Med 2014, 20:652-665.
51. Marsh R.A., Villanueva J., Kim M.O., Zhang K., Marmer D., Risma K.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.
52. Henter J.I., Horne A., Arico M., Egeler R.M., Filipovich A.H., Imashuku S., et al. HLH-2004: diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer 2007, 48:124-131.
53. Marsh R.A., Rao K., Satwani P., Lehmberg K., Muller I., Li D., et al. Allogeneic hematopoietic cell transplantation for XIAP deficiency: an international survey reveals poor outcomes. Blood 2013, 121:877-883.
54. Worth A.J., Nikolajeva O., Chiesa R., Rao K., Veys P., Amrolia P.J. Successful stem cell transplant with antibody-based conditioning for XIAP deficiency with refractory hemophagocytic lymphohistiocytosis. Blood 2013, 121:4966-4968.
55. Tsuma Y., Imamura T., Ichise E., Sakamoto K., Ouchi K., Osone S., et al. Successful treatment of idiopathic colitis related to XIAP deficiency with allo-HSCT using reduced-intensity conditioning. Pediatr Transplant 2015, 19:E25-E28.
56. Varghese A.S., Lee H., Bonney D., Hughes S., Wynn R. Complications of reduced intensity conditioning HSCT for XIAP deficiency (Alloimmune Cytopenias and HLH) successfully managed with donor lymphocyte infusion. J Pediatr Hematol Oncol 2014, 10.1097/MPH.0000000000000191.
57. Bouillet P., O'Reilly L.A. CD95, BIM and T cell homeostasis. Nat Rev Immunol 2009, 9:514-519.
58. Paulsen M., Ussat S., Jakob M., Scherer G., Lepenies I., Schutze S., et al. Interaction with XIAP prevents full caspase-3/-7 activation in proliferating human T lymphocytes. Eur J Immunol 2008, 38:1979-1987.
59. Gerart 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.
60. van de Veerdonk F.L., Netea M.G., Dinarello C.A., Joosten L.A. Inflammasome activation and IL-1beta and IL-18 processing during infection. Trends Immunol 2011, 32:110-116.
61. Lopez-Granados E., Stacey M., Kienzler A.K., Sierro S., Willberg C.B., Fox C.P., et al. A mutation in X-linked inhibitor of apoptosis (G466X) leads to memory inflation of Epstein-Barr virus-specific T cells. Clin Exp Immunol 2014, 178:470-482.
62. Latour S. Natural killer T cells and X-linked lymphoproliferative syndrome. Curr Opin Allergy Clin Immunol 2007, 7:510-514.
63. Diana J., Lehuen A. NKT cells: friend or foe during viral infections. Eur J Immunol 2009, 39:3283-3291.
64. Chung B.K., Tsai K., Allan L.L., Zheng D.J., Nie J.C., Biggs C.M., et al. Innate immune control of EBV-infected B cells by invariant natural killer T cells. Blood 2013, 122:2600-2608.
65. Veillette A., Perez-Quintero L.A., Latour S. X-linked lymphoproliferative syndromes and related autosomal recessive disorders. Curr Opin Allergy Clin Immunol 2013, 13:614-622.
66. Romberg N., Al Moussawi K., Nelson-Williams C., Stiegler A.L., Loring E., Choi M., et al. Mutation of NLRC4 causes a syndrome of enterocolitis and autoinflammation. Nat Genet 2014, 46:1135-1139.
67. Canna S.W., de Jesus A.A., Gouni S., Brooks S.R., Marrero B., Liu Y., et al. An activating NLRC4 inflammasome mutation causes autoinflammation with recurrent macrophage activation syndrome. Nat Genet 2014, 46:1140-1146.
68. Levy R., Gerard L., Kuemmerle-Deschner J., Lachmann H.J., Kone-Paut I., Cantarini L., et al. Phenotypic and genotypic characteristics of cryopyrin-associated periodic syndrome: a series of 136 patients from the Eurofever Registry. Ann Rheum Dis 2014, 10.1136/annrheumdis-2013-204991.
69. Hugot J.P., Chamaillard M., Zouali H., Lesage S., Cezard J.P., Belaiche J., et al. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 2001, 411:599-603.
70. Jostins L., Ripke S., Weersma R.K., Duerr R.H., McGovern D.P., Hui K.Y., et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 2012, 491:119-124.
71. Ogura Y., Bonen D.K., Inohara N., Nicolae D.L., Chen F.F., Ramos R., et al. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 2001, 411:603-606.
72. Strober W., Asano N., Fuss I., Kitani A., Watanabe T. Cellular and molecular mechanisms underlying NOD2 risk-associated polymorphisms in Crohn's disease. Immunol Rev 2014, 260:249-260.
73. Glocker E.O., Kotlarz D., Klein C., Shah N., Grimbacher B. IL-10 and IL-10 receptor defects in humans. Ann N Y Acad Sci 2011, 1246:102-107.
74. Marks D.J., Harbord M.W., MacAllister R., Rahman F.Z., Young J., Al-Lazikani B., et al. Defective acute inflammation in Crohn's disease: a clinical investigation. Lancet 2006, 367:668-678.
75. Smith A.M., Rahman F.Z., Hayee B., Graham S.J., Marks D.J., Sewell G.W., et al. Disordered macrophage cytokine secretion underlies impaired acute inflammation and bacterial clearance in Crohn's disease. J Exp Med 2009, 206:1883-1897.
76. Casanova J.L., Abel L. Revisiting Crohn's disease as a primary immunodeficiency of macrophages. J Exp Med 2009, 206:1839-1843.
77. Marks D.J., Miyagi K., Rahman F.Z., Novelli M., Bloom S.L., Segal A.W. Inflammatory bowel disease in CGD reproduces the clinicopathological features of Crohn's disease. Am J Gastroenterol 2009, 104:117-124.
78. Ashida H., Ogawa M., Mimuro H., Kobayashi T., Sanada T., Sasakawa C. Shigella are versatile mucosal pathogens that circumvent the host innate immune system. Curr Opin Immunol 2011, 23:448-455.
79. Gunther C., Martini E., Wittkopf N., Amann K., Weigmann B., Neumann H., et al. Caspase-8 regulates TNF-alpha-induced epithelial necroptosis and terminal ileitis. Nature 2011, 477:335-339.
80. Serriari N.E., Eoche M., Lamotte L., Lion J., Fumery M., Marcelo P., et al. Innate mucosal-associated invariant T (MAIT) cells are activated in inflammatory bowel diseases. Clin Exp Immunol 2014, 176:266-274.
81. Ruijing X., Mengjun W., Xiaoling Z., Shu P., Mei W., Yingcheng Z., et al. Jalpha33+ MAIT cells play a protective role in TNBS induced intestinal inflammation. Hepatogastroenterology 2012, 59:762-767.
82. An D., Oh S.F., Olszak T., Neves J.F., Avci F.Y., Erturk-Hasdemir D., et al. Sphingolipids from a symbiotic microbe regulate homeostasis of host intestinal natural killer T cells. Cell 2014, 156:123-133.
83. Olszak T., Neves J.F., Dowds C.M., Baker K., Glickman J., Davidson N.O., et al. Protective mucosal immunity mediated by epithelial CD1d and IL-10. Nature 2014, 509:497-502.