Inflammatory bowel disease: Is it a primary immunodeficiency?

Cellular and Molecular Life Sciences

Volumn 69, Issue 1, 2012, Pages 41-48

  Glocker, Erik ^a   Grimbacher, Bodo ^a,b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

CGD; Crohn's disease; IL10 deficiency; IL10R deficiency; Immunodeficiency; Inflammatory bowel disease; IPEX; Wiskott Aldrich syndrome

Indexed keywords

INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR; INTERLEUKIN 12; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

B LYMPHOCYTE; CHRONIC GRANULOMATOUS DISEASE; CROHN DISEASE; CYTOKINE RELEASE; DENDRITIC CELL; DISEASE ASSOCIATION; DISEASE MODEL; ENTERITIS; GENE MUTATION; GENETIC IDENTIFICATION; HUMAN; IMMUNE DEFICIENCY; IPEX SYNDROME; MACROPHAGE; MONOCYTE; MUCOSAL IMMUNITY; NONHUMAN; REVIEW; T LYMPHOCYTE; WISKOTT ALDRICH SYNDROME;

COLITIS, ULCERATIVE; CROHN DISEASE; GENES, X-LINKED; GRANULOMATOUS DISEASE, CHRONIC; HUMANS; INTERLEUKIN-10; INTESTINAL MUCOSA; RECEPTORS, INTERLEUKIN-10; WISKOTT-ALDRICH SYNDROME; WISKOTT-ALDRICH SYNDROME PROTEIN; X-LINKED COMBINED IMMUNODEFICIENCY DISEASES;

BACTERIA (MICROORGANISMS);

EID: 84856217966     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-011-0837-9     Document Type: Review

References (111)

1. DK Podolsky 2002 Inflammatory bowel disease N Engl J Med 347 417 429 12167685 1:CAS:528:DC%2BD38XlvFKrt7s%3D (Pubitemid 34851835)
2. DC Baumgart SR Carding 2007 Inflammatory bowel disease: cause and immunobiology Lancet 369 1627 1640 17499605 1:CAS:528:DC%2BD2sXltF2qsrc%3D (Pubitemid 46722636)
3. C Romano A Famiani R Gallizzi, et al. 2008 Indeterminate colitis: a distinctive clinical pattern of inflammatory bowel disease in children Pediatrics 122 e1278 e1281 19047226
4. RJ Xavier DK Podolsky 2007 Unravelling the pathogenesis of inflammatory bowel disease Nature 448 427 434 17653185 1:CAS:528:DC%2BD2sXotFajurs%3D (Pubitemid 47123518)
5. MJ Carter AJ Lobo 2004 Travis SP; IBD Section, British Society of Gastroenterology. Guidelines for the management of inflammatory bowel disease in adults Gut 53 Suppl 5 V1 V16 15306569
6. MA Engel MF Neurath 2010 New pathophysiological insights and modern treatment of IBD J Gastroenterol 45 571 583 20213337 1:CAS:528: DC%2BC3cXntlKqtLo%3D
7. SD Spencer F Di Marco J Hooley, et al. 1998 The orphan receptor CRF2-4 is an essential subunit of the interleukin 10 receptor J Exp Med 187 571 578 9463407 1:CAS:528:DyaK1cXhtFCqtb8%3D (Pubitemid 28093359)
8. A Mizoguchi E Mizoguchi 2008 Inflammatory bowel disease, past, present and future: lessons from animal models J Gastroenterol 43 1 17 18297430 (Pubitemid 351324980)
9. CO Elson Y Cong VJ McCracken RA Dimmitt RG Lorenz CT Weaver 2005 Experimental models of inflammatory bowel disease reveal innate, adaptive, and regulatory mechanisms of host dialogue with the microbiota Immunol Rev 206 260 276 16048554 (Pubitemid 41105175)
10. AB Onderdonk JA Hermos JG Bartlett 1977 The role of the intestinal microflora in experimental colitis Am J Clin Nutr 30 1819 1825 920642 1:CAS:528:DyaE1cXoslWitA%3D%3D (Pubitemid 8212710)
11. M Barnes F Powrie 2009 Regulatory T cells reinforce intestinal homeostasis Immunity 31 401 411 19766083 1:CAS:528:DC%2BD1MXhsVejt7fN
12. D Artis 2008 Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut Nat Rev Immunol 8 411 420 18469830 1:CAS:528:DC%2BD1cXmt1OjtrY%3D (Pubitemid 351733416)
13. EK Boden SB Snapper 2008 Regulatory T cells in inflammatory bowel disease Curr Opin Gastroenterol 24 733 741 19125486
14. JD Fontenot MA Gavin AY Rudensky 2003 Foxp3 programs the development and function of CD4+ CD25+ regulatory T cells Nat Immunol 4 330 336 12612578 1:CAS:528:DC%2BD3sXitlyqs74%3D (Pubitemid 36432314)
15. MO Li YY Wan RA Flavell 2007 T cell-produced transforming growth factor-beta1 controls T cell tolerance and regulates Th1- and Th17-cell differentiation Immunity 26 579 591 17481928 1:CAS:528:DC%2BD2sXmt1ajs7k%3D (Pubitemid 46756347)
16. YP Rubtsov JP Rasmussen EY Chi J Fontenot L Castelli X Ye P Treuting L Siewe A Roers WR Henderson Jr W Muller AY Rudensky 2008 Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces Immunity 28 546 558 18387831 1:CAS:528:DC%2BD1cXkvV2it7c%3D
17. JH Cho 2008 The genetics and immunopathogenesis of inflammatory bowel disease Nat Rev Immunol 8 458 466 18500230 1:CAS:528:DC%2BD1cXmt1Ojt7o%3D (Pubitemid 351733422)
18. J Van Limbergen DC Wilson J Satsangi 2009 The genetics of Crohn's disease Annu Rev Genomics Hum Genet 10 89 116 19453248
19. JC Barrett S Hansoul DL Nicolae, et al. 2008 Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease Nat Genet 40 955 962 18587394 1:CAS:528:DC%2BD1cXptFSqs7k%3D
20. J Hampe A Franke P Rosenstiel, et al. 2007 A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1 Nat Genet 39 207 211 17200669 1:CAS:528:DC%2BD2sXpvFerug%3D%3D (Pubitemid 46184351)
21. M Parkes JC Barrett NJ Prescott, et al. 2007 Sequence variants in the autophagy gene IRGM and multiple other replicating loci contribute to Crohn's disease susceptibility Nat Genet 39 830 832 17554261 1:CAS:528: DC%2BD2sXmvFKlsL4%3D (Pubitemid 47014496)
22. K Cadwell JY Liu SL Brown, et al. 2008 A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells Nature 456 259 263 18849966 1:CAS:528:DC%2BD1cXhtlKmtL%2FI
23. JP Hugot M Chamaillard H Zouali, et al. 2001 Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease Nature 411 599 603 11385576 1:CAS:528:DC%2BD3MXksVShtLY%3D (Pubitemid 32531408)
24. M Economou TA Trikalinos KT Loizou, et al. 2004 Differential effects of NOD2 variants on Crohn's disease risk and phenotype in diverse populations: a metaanalysis Am J Gastroenterol 99 2393 2404 15571588 1:CAS:528: DC%2BD2MXmsFyquw%3D%3D (Pubitemid 40039371)
25. M Pierik S Joossens K Van Steen, et al. 2006 Toll-like receptor-1, -2, and -6 polymorphisms influence disease extension in inflammatory bowel diseases Inflamm Bowel Dis 12 1 8 16374251 (Pubitemid 43032444)
26. DA van Heel SA Fisher A Kirby, et al. 2004 Inflammatory bowel disease susceptibility loci defined by genome scan meta-analysis of 1952 affected relative pairs Hum Mol Genet 13 763 770 14976156 (Pubitemid 38455963)
27. RH Duerr KD Taylor SR Brant, et al. 2006 A genome-wide association study identifies IL23R as an inflammatory bowel disease gene Science 314 1461 1463 17068223 1:CAS:528:DC%2BD28Xht1CntrjF (Pubitemid 44871953)
28. J Glas J Seiderer M Wetzke, et al. 2007 rs1004819 is the main disease-associated IL23R variant in German Crohn's disease patients: combined analysis of IL23R, CARD15, and OCTN1/2 variants PLoS One 2 e819 17786191
29. SA Fisher M Tremelling CA Anderson, et al. 2008 Genetic determinants of ulcerative colitis include the ECM1 locus and five loci implicated in Crohn's disease Nat Genet 40 710 712 18438406 1:CAS:528:DC%2BD1cXmsVejsb8%3D (Pubitemid 351748865)
30. KD Taylor SR Targan L Mei, et al. 2008 IL23R haplotypes provide a large population attributable risk for Crohn's disease Inflamm Bowel Dis 14 1185 1191 18470928
31. M Stoll B Corneliussen CM Costello, et al. 2004 Genetic variation in DLG5 is associated with inflammatory bowel disease Nat Genet 36 476 480 15107852 1:CAS:528:DC%2BD2cXjsFSnt7w%3D (Pubitemid 38620031)
32. A Kaser AH Lee A Franke, et al. 2008 XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease Cell 134 743 756 18775308 1:CAS:528:DC%2BD1cXhtFCqs7nJ
33. A Zhernakova EM Festen L Franke, et al. 2008 Genetic analysis of innate immunity in Crohn's disease and ulcerative colitis identifies two susceptibility loci harboring CARD9 and IL18RAP Am J Hum Genet 82 1202 1210 18439550 1:CAS:528:DC%2BD1cXlvFeqtL8%3D
34. EO Glocker D Kotlarz K Boztug, et al. 2009 Inflammatory bowel disease and mutations affecting the interleukin-10 receptor N Engl J Med 361 2033 2045 19890111 1:CAS:528:DC%2BD1MXhsVequ7bM
35. Glocker EO, Frede N, Perro M, et al. Severe early-onset colitis due to a mutation in interleukin-10. The Lancet (accepted)
36. IO Akman BE Ostrov S Neudorf 1998 Autoimmune manifestations of the Wiskott-Aldrich syndrome Semin Arthritis Rheum 27 218 225 9514127 1:STN:280:DyaK1c7ntlSlsg%3D%3D (Pubitemid 28154647)
37. DJB Marks AW Segal 2008 Innate immunity in inflammatory bowel disease: a disease hypothesis J Pathol 214 260 266 18161747 1:CAS:528:DC%2BD1cXhvFCkt7c%3D (Pubitemid 351160162)
38. DJB Marks K Miyagi FZ Rahman, et al. 2009 Inflammatory bowel disease in CGD reproduces the clinicopathological features of Crohn's disease Am J Gastroenterol 104 117 124 19098859 1:CAS:528:DC%2BD1MXht1Shsw%3D%3D
39. FZ Rahman DJB Marks BH Hayee, et al. 2008 Phagocytic dysfunction and inflammatory bowel disease Inflamm Bowel Dis 14 1443 1452 18421761
40. G Bouma W Strober 2003 The immunological and genetic basis of inflammatory bowel disease Nat Rev Immunol 3 521 533 12876555 1:CAS:528:DC%2BD3sXls1Smtr4%3D (Pubitemid 37328672)
41. AW Segal G Loewi 1976 Neutrophil dysfunction in Crohn's disease Lancet 308 219 221
42. DJB Marks MWN Harbord R MacAllister, et al. 2006 Defective acute inflammation in Crohn's disease: a clinical investigation Lancet 367 668 678 16503465 1:CAS:528:DC%2BD28XhslylsbY%3D (Pubitemid 43289157)
43. AM Smith FZ Rahman BH Hayee, et al. 2009 Disordered macrophage cytokine secretion underlies impaired acute inflammation and bacterial clearance in Crohn's disease J Exp Med 206 1883 1897 19652016 1:CAS:528:DC%2BD1MXhtVyitLnP
44. JL Casanova L Abel 2009 Revisiting Crohn's disease as a primary immunodeficiency of macrophages J Exp Med 206 1839 1843 19687225 1:CAS:528:DC%2BD1MXhtVyitLjE
45. K Ephgrave 2007 Extra-intestinal manifestations of Crohn's disease Surg Clin North Am 87 673 680 17560419 (Pubitemid 46873666)
46. KW Moore R de Waal Malefyt RL Coffman A O'Garra 2001 Interleukin-10 and the interleukin-10 receptor Annu Rev Immunol 19 683 765 11244051 1:CAS:528:DC%2BD3MXivFKgu70%3D (Pubitemid 32368050)
47. C Bogdan Y Vodovotz C Nathan 1991 Macrophage deactivation by interleukin 10 J Exp Med 174 1549 1555 1744584 1:CAS:528:DyaK3MXmtlSiu78%3D
48. R de Waal Malefyt J Haanen H Spits, et al. 1991 Interleukin-10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via down regulation of class II major histocompatibility complex expression J Exp Med 174 915 924 1655948
49. LM Williams G Ricchetti U Sarma, et al. 2004 Interleukin-10 suppression of myeloid cell activation-a continuing puzzle Immunology 113 281 292 15500614 1:CAS:528:DC%2BD2cXpvV2jtbY%3D (Pubitemid 39472144)
50. R Kühn J Lohler D Rennick, et al. 1993 Interleukin-10-deficient mice develop chronic enterocolitis Cell 75 263 274 8402911 (Pubitemid 23320290)
51. DJ Berg R Kühn K Rajewsky, et al. 1995 Interleukin-10 is a central regulator of the response to LPS in murine models of endotoxic shock and the Shwartzman reaction but not endotoxin tolerance J Clin Invest 96 2339 2347 7593621 1:CAS:528:DyaK28XltF2hsg%3D%3D
52. A Franke T Balschun TH Karlsen, et al. 2008 Sequence variants in IL10, ARPC2 and multiple other loci contribute to ulcerative colitis susceptibility Nat Genet 40 1319 1323 18836448 1:CAS:528:DC%2BD1cXhtlSkurjI
53. K van der Linde PP Boor LA Sandkuijl, et al. 2003 A Gly15Arg mutation in the interleukin-10 gene reduces secretion of interleukin-10 in Crohn disease Scand J Gastroenterol 38 611 617 12825869 (Pubitemid 36724040)
54. E Noguchi Y Homma X Kang, et al. 2009 A Crohn's disease-associated NOD2 mutation suppresses transcription of human IL10 by inhibiting activity of the nuclear ribonucleoprotein hnRNP-A1 Nat Immunol 10 471 479 19349988 1:CAS:528:DC%2BD1MXktVKgurw%3D
55. SE Girardin JP Hugot PJ Sansonetti 2003 Lessons from Nod2 studies: towards a link between Crohn's disease and bacterial sensing Trends Immunol 24 652 658 14644139 1:CAS:528:DC%2BD3sXptlyhsr4%3D (Pubitemid 37485915)
56. Y Ogura DK Bonen N Inohara, et al. 2001 A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease Nature 411 603 606 11385577 1:CAS:528:DC%2BD3MXksVShur8%3D (Pubitemid 32531409)
57. RP Donnelly H Dickensheets DS Finbloom 1999 The interleukin-10 signal transduction pathway and regulation of gene expression in mononuclear phagocytes J Interferon Cytokine Res 19 563 573 10433356 1:CAS:528:DyaK1MXks1aiur8%3D (Pubitemid 29331308)
58. SV Kotenko CD Krause LS Izotova, et al. 1997 Identification and functional characterization of a second chain of the interleukin-10 receptor complex The EMBO J 16 5894 5903 1:CAS:528:DyaK2sXntVKgsL8%3D (Pubitemid 27427285)
59. JJ O'Shea PJ Murray 2008 Cytokine signaling modules in inflammatory responses Immunity 28 477 487 18400190 (Pubitemid 351467044)
60. L Williams L Bradley A Smith B Foxwell 2004 Signal transducer and activator of transcription 3 is the dominant mediator of the anti-inflammatory effects of IL-10 in human macrophages J Immunol 172 567 576 14688368 1:CAS:528:DC%2BD3sXpvFegs74%3D (Pubitemid 38020514)
61. K Wolk R Sabat 2006 Interleukin-22: A novel T- and NK-cell derived cytokine that regulates the biology of tissue cells Cytokine & Growth Factor Rev 17 367 380 1:CAS:528:DC%2BD28XhtFSktb%2FL (Pubitemid 44572879)
62. S Commins JW Steinke L Borish 2008 The extended IL-10 superfamily: IL-10, IL-19, IL-20, IL-22, IL-24, IL-26, IL-28, and IL-29 J Allergy Clin Immunol 121 1108 1111 18405958 1:CAS:528:DC%2BD1cXlslKltLY%3D
63. RP Donnelly F Sheikh SV Kotenko H Dickensheets 2004 The expanded family of class II cytokines that share the IL-10 receptor-2(IL-10R2) chain J Leukoc Biol 76 314 321 15123776 1:CAS:528:DC%2BD2cXmtlKrs70%3D (Pubitemid 39006944)
64. K Sugimoto A Ogawa E Mizoguchi, et al. 2008 IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis J Clin Invest 118 534 544 18172556 1:CAS:528:DC%2BD1cXhsFOmsr8%3D (Pubitemid 351206544)
65. LA Zenewicz GD Yancopoulos DM Valenzuela, et al. 2008 Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease Immunity 29 947 957 19100701 1:CAS:528:DC%2BD1MXhtlymtQ%3D%3D
66. Y Zheng PA Valdez DM Danilenko, et al. 2008 Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens Nat Med 14 282 289 18264109 1:CAS:528:DC%2BD1cXivFOrtLw%3D (Pubitemid 351347912)
67. K Wolk S Kunz E Witte M Friedrich K Asadullah R Sabat 2004 IL-22 increases the innate immunity of tissues Immunity 21 241 254 15308104 1:CAS:528:DC%2BD2cXnsVKlt7k%3D (Pubitemid 39094053)
68. K Wolk E Witte E Wallace WD Döcke S Kunz K Asadullah HD Volk W Sterry R Sabat 2006 IL-22 regulates the expression of genes responsible for antimicrobial defense, cellular differentiation, and mobility in keratinocytes: a potential role in psoriasis Eur J Immunol 36 1309 1323 16619290 1:CAS:528:DC%2BD28Xlt1ekurY%3D
69. JK Kolls PB McCray Jr YR Chan 2008 Cytokine-mediated regulation of antimicrobial proteins Nat Rev Immunol 8 829 835 18949018 1:CAS:528: DC%2BD1cXht12isLbI
70. SV Kotenko G Gallagher VV Baurin, et al. 2003 IFN-λs mediate antiviral protection through a distinct class II cytokine receptor complex Nat Immunol 4 69 77 12483210 1:CAS:528:DC%2BD38Xps1eltL8%3D (Pubitemid 36109115)
71. P Sheppard W Kindsvogel W Xu, et al. 2003 IL-28, IL-29 and their class II cytokine receptor IL-28R Nat Immunol 4 63 68 12469119 1:CAS:528: DC%2BD38Xps1elt7c%3D (Pubitemid 36104710)
72. KJ Maloy L Salaun R Cahill, et al. 2003 CD4 + CD25 + T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms J Exp Med 197 111 119 12515818 1:CAS:528:DC%2BD3sXjslWltg%3D%3D (Pubitemid 36110262)
73. S Read V Malmström F Powrie 2000 Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25(+)CD4(+) regulatory cells that control intestinal inflammation J Exp Med 192 295 302 10899916 1:CAS:528:DC%2BD3cXkvFGiu7Y%3D (Pubitemid 30470312)
74. C Mottet HH Uhlig F Powrie 2003 Cutting edge: cure of colitis by CD4+ CD25+ regulatory T cells J Immunol 170 3939 3943 12682220 1:CAS:528: DC%2BD3sXislektbk%3D (Pubitemid 36428153)
75. M Feuerer JA Hill D Mathis C Benoist 2009 Foxp3+ regulatory T cells: differentiation, specification, subphenotypes Nat Immunol 10 689 695 19536194 1:CAS:528:DC%2BD1MXnsVagsL4%3D
76. SZ Josefowicz A Rudensky 2009 Control of regulatory T cell lineage commitment and maintenance Immunity 30 616 625 19464984 1:CAS:528: DC%2BD1MXosVCks7o%3D
77. CW Lio CS Hsieh 2008 A two-step process for thymic regulatory T cell development Immunity 28 100 111 18199417 1:CAS:528:DC%2BD1cXht1Ont78%3D
78. F Powrie MW Leach S Mauze, et al. 1993 Phenotypically distinct subsets of CD4+ T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice Int Immunol 5 1461 1471 7903159 1:STN:280:DyaK2c%2Fotlektg%3D%3D (Pubitemid 23325202)
79. CL Bennett R Yoshioka H Kiyosawa, et al. 2000 X-Linked syndrome of polyendocrinopathy, immune dysfunction, and diarrhea maps to Xp11.23-Xq13.3 Am J Hum Genet 66 461 468 10677306 1:CAS:528:DC%2BD3cXitFyitr0%3D (Pubitemid 30468824)
80. BR Powell NR Buist P Stenzel 1982 An X-linked syndrome of diarrhea, polyendocrinopathy, and fatal infection in infancy J Pediatr 100 731 737 7040622 1:STN:280:DyaL387mvFKruw%3D%3D (Pubitemid 12155977)
81. SF Ziegler 2006 FOXP3: of mice and men Annu Rev Immunol 24 209 226 16551248 1:CAS:528:DC%2BD28XkvFSqt7s%3D
82. D Moraes-Vasconcelos BT Costa-Carvalho TR Torgerson HD Ochs 2008 Primary immune deficiency disorders presenting as autoimmune diseases: IPEX and APECED J Clin Immunol 28 Suppl 1 S11 S19 18264745 1:CAS:528:DC%2BD1cXptFyqs7g%3D
83. E Gambineri TR Torgerson HD Ochs 2003 Immune dysregulation, polyendocrinopathy, enteropathy, and X-linked inheritance (IPEX), a syndrome of systemic autoimmunity caused by mutations of FOXP3, a critical regulator of T cell homeostasis Curr Opin Rheumatol 15 430 435 12819471 1:CAS:528: DC%2BD3sXltFKjsb8%3D (Pubitemid 36774255)
84. DS Nieves RP Phipps SJ Pollock, et al. 2004 Dermatologic and immunologic findings in the immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome Arch Dermatol 140 466 472 15096376 (Pubitemid 38469251)
85. TR Torgerson HD Ochs 2007 Immune dysregulation, polyendocrinopathy, enteropathy, X-linked: forkhead box protein 3 mutations and lack of regulatory T cells J Allergy Clin Immunol 120 744 750 17931557 1:CAS:528:DC%2BD2sXhtFKitrnM (Pubitemid 47531861)
86. ML Heltzer JK Choi HD Ochs, et al. 2007 A potential screening tool for IPEX syndrome Pediatr Dev Pathol 10 98 105 17378693 1:CAS:528: DC%2BD2sXjvFOhs7w%3D (Pubitemid 46580400)
87. CL Bennett HD Ochs 2001 IPEX is a unique X-linked syndrome characterized by immune dysfunction, polyendocrinopathy, enteropathy, and a variety of autoimmune phenomena Curr Opin Pediatr 13 533 538 11753102 1:STN:280: DC%2BD38%2Fgt1GrtQ%3D%3D (Pubitemid 34015524)
88. BT Costa-Carvalho MI de Moraes-Pinto LC de Almeida, et al. 2008 A remarkable depletion of both naïve CD4+ and CD8+ with high proportion of memory T cells in an IPEX infant with a FOXP3 mutation in the forkhead domain Scand J Immunol 68 85 91 18489537 1:CAS:528:DC%2BD1cXovFertLo%3D (Pubitemid 351798396)
89. N Watanabe YH Wang HK Lee, et al. 2005 Hassall's corpuscles instruct dendritic cells to induce CD4+ CD25+ regulatory T cells in human thymus Nature 436 1181 1185 16121185 1:CAS:528:DC%2BD2MXovVOgtrw%3D (Pubitemid 41232298)
90. JR Korzenik 2007 Is Crohn's disease due to defective immunity? Gut 56 2 5 17172582 1:CAS:528:DC%2BD2sXhtF2qs7k%3D (Pubitemid 46044879)
91. AJ Thrasher NH Keep F Wientjes AW Segal 1994 Chronic granulomatous disease Biochim Biophys Acta 1227 1 24 7918677 1:CAS:528:DyaK2cXmslOltLo%3D (Pubitemid 24320379)
92. AW Segal A Abo 1993 The biochemical basis of the NADPH oxidase of phagocytes Trends Biochem Sci 18 43 47 8488557 1:CAS:528:DyaK3sXisFSitbc%3D (Pubitemid 23145110)
93. AW Segal 2005 How neutrophils kill microbes Annu Rev Immunol 23 197 223 15771570 1:CAS:528:DC%2BD2MXktFOjtbY%3D (Pubitemid 40563169)
94. BH Segal LR Romani 2009 Invasive aspergillosis in chronic granulomatous disease Med Mycol 47 Suppl 1 S282 S290 19296367 1:CAS:528:DC%2BD1MXms1OnsLw%3D
95. MJ Stasia XJ Li 2008 Genetics and immunopathology of chronic granulomatous disease Semin Immunopathol 30 209 235 18509647
96. SL Werlin MJ Chusid J Caya HW Oechler 1982 Colitis in chronic granulomatous disease Gastroenterology 82 328 331 6119271 1:STN:280: DyaL38%2Fps1WjsQ%3D%3D (Pubitemid 12213647)
97. BE Marciano SD Rosenzweig DE Kleiner, et al. 2004 Gastrointestinal involvement in chronic granulomatous disease Pediatrics 114 462 468 15286231 (Pubitemid 39006676)
98. LS Westerberg P Meelu M Baptista, et al. 2010 Activating WASP mutations associated with X-linked neutropenia result in enhanced actin polymerization, altered cytoskeletal responses, and genomic instability in lymphocytes J Exp Med 207 1145 1152 20513746 1:CAS:528:DC%2BC3cXns1Sntb0%3D
99. AJ Thrasher SO Burns 2010 WASP: a key immunological multitasker Nat Rev Immunol 10 182 192 20182458 1:CAS:528:DC%2BC3cXitlOjsr0%3D
100. M Symons JM Derry B Karlak, et al. 1996 Wiskott-Aldrich syndrome protein, a novel effector for the GTPase CDC42Hs, is implicated in actin polymerization Cell 84 723 734 8625410 1:CAS:528:DyaK28Xhs1Cgu7k%3D (Pubitemid 26094202)
101. L Blanchoin KJ Amann HN Higgs, et al. 2000 Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASP/Scar proteins Nature 404 1007 1011 10801131 1:CAS:528:DC%2BD3cXjtFyntbo%3D (Pubitemid 30243596)
102. HD Ochs AJ Thrasher 2006 The Wiskott-Aldrich syndrome J Allergy Clin Immunol 117 725 738 16630926 1:CAS:528:DC%2BD28Xjslels7w%3D (Pubitemid 44313817)
103. A Villa L Notarangelo P Macchi, et al. 1995 X-linked thrombocytopenia and Wiskott-Aldrich syndrome are allelic diseases with mutations in the WASP gene Nat Genet 9 414 417 7795648 1:CAS:528:DyaK2MXkvV2ju78%3D
104. LD Notarangelo C Mazza S Giliani, et al. 2002 Missense mutations of the WASP gene cause intermittent X-linked thrombocytopenia Blood 99 2268 2269 11877312 1:CAS:528:DC%2BD38XitF2mtr4%3D (Pubitemid 34525521)
105. K Devriendt AS Kim G Mathijs, et al. 2001 Constitutively activating mutation in WASP causes X-linked severe congenital neutropenia Nat Genet 27 313 317 11242115 1:CAS:528:DC%2BD3MXhslOisL4%3D (Pubitemid 32201854)
106. A Wiskott 1937 Familiarer, angeborener Morbus Werlhofii? Monastsschr Kinderheilkd 68 212 216
107. RA Aldrich AG Steinberg DC Campbell 1954 Pedigree demonstrating a sex-linked recessive condition characterized by draining ears, eczematoid dermatitis and bloody diarrhea Pediatrics 13 133 139 13133561 1:STN:280:DyaG2c%2FltlCitA%3D%3D
108. KE Sullivan CA Mullen RM Blaese JA Winkelstein 1994 A multiinstitutional survey of the Wiskott-Aldrich syndrome J Pediatr 125 876 885 7996359 1:STN:280:DyaK2M%2FovVyhtw%3D%3D (Pubitemid 24379120)
109. Z Cannioto I Berti S Martelossi, et al. 2009 IBD and IBD mimicking enterocolitis in children younger than 2 years of age Eur J Pediatr 168 149 155 18546019 1:STN:280:DC%2BD1M%2FhsVGltQ%3D%3D
110. S Dupuis-Girod J Medioni E Haddad, et al. 2003 Autoimmunity in Wiskott-Aldrich syndrome: risk factors, clinical features, and outcome in a single-center cohort of 55 patients Pediatrics 111 5 Pt 1 e622 e627 12728121
111. J Rohr U Pannicke M Döring, et al. 2010 Chronic inflammatory bowel disease as key manifestation of atypical ARTEMIS deficiency J Clin Immunol 30 314 320 19967552 1:CAS:528:DC%2BC3cXjs1aqu7w%3D