Wiskott-aldrich syndrome protein deficiency in innate immune cells leads to mucosal immune dysregulation and colitis in mice

Gastroenterology

Volumn 143, Issue 3, 2012, Pages

  Nguyen, Deanna D ^a,b   Wurbel, Marc Andre ^b,c   Goettel, Jeremy A ^b,c   Eston, Michelle A ^a   Ahmed, Osub S ^c   Marin, Romela ^a   Boden, Elisa K ^a,b   Villablanca, Eduardo J ^a,b   Paidassi, Helena ^a,b   Ahuja, Vineet ^a,b   Reinecker, Hans Christian ^a,b   Fiebiger, Edda ^b,c   Lacyhulbert, Adam ^a,b   Horwitz, Bruce H ^b,d   Mora, J Rodrigo ^a,b   Snapper, Scott B ^a,b,c,d  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Antigen Presenting Cells; Immunodeficiency; Inflammatory Bowel Disease; Mouse Model

Indexed keywords

CD103 ANTIGEN; INTERLEUKIN 10; TRANSCRIPTION FACTOR FOXP3; WISKOTT ALDRICH SYNDROME PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL EXPANSION; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; IMMUNE DYSREGULATION; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; LYMPHOCYTE FUNCTION; MESENTERY LYMPH NODE; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE;

EID: 84865461925     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2012.06.008     Document Type: Article

References (44)

1. S. Wirtz, M.F. Neurath Mouse models of inflammatory bowel disease Adv Drug Deliv Rev 59 2007 1073 1083 (Pubitemid 47615208)
2. C.L. Maynard, C.T. Weaver Intestinal effector T cells in health and disease Immunity 31 2009 389 400
3. K.R. Siddiqui, S. Laffont, F. Powrie E-cadherin marks a subset of inflammatory dendritic cells that promote T cell-mediated colitis Immunity 32 2010 557 567
4. B. Liu, S.L. Tonkonogy, R.B. Sartor Antigen-presenting cell production of IL-10 inhibits T-helper 1 and 17 cell responses and suppresses colitis in mice Gastroenterology 141 2011 653 662 662 e14
5. M. Murai, O. Turovskaya, G. Kim Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis Nat Immunol 10 2009 1178 1184
6. W.S. Garrett, S. Punit, C.A. Gallini Colitis-associated colorectal cancer driven by T-bet deficiency in dendritic cells Cancer Cell 16 2009 208 219
7. A. Lacy-Hulbert, A.M. Smith, H. Tissire Ulcerative colitis and autoimmunity induced by loss of myeloid alphav integrins Proc Natl Acad Sci U S A 104 2007 15823 15828 (Pubitemid 350035383)
8. M.A. Travis, B. Reizis, A.C. Melton Loss of integrin alpha(v)beta8 on dendritic cells causes autoimmunity and colitis in mice Nature 449 2007 361 365 (Pubitemid 47443473)
9. H.H. Uhlig, B.S. McKenzie, S. Hue Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology Immunity 25 2006 309 318
10. K. Takeda, B.E. Clausen, T. Kaisho Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils Immunity 10 1999 39 49 (Pubitemid 29077382)
11. L.S. Westerberg, C. Klein, S.B. Snapper Breakdown of T cell tolerance and autoimmunity in primary immunodeficiencylessons learned from monogenic disorders in mice and men Curr Opin Immunol 20 2008 646 654
12. K.H. Hsieh, M.H. Chang, C.Y. Lee Wiskott-Aldrich syndrome and inflammatory bowel disease Ann Allergy 60 1988 429 431
13. C. Folwaczny, C. Ruelfs, J. Walther Ulcerative colitis in a patient with Wiskott-Aldrich syndrome Endoscopy 34 2002 840 841
14. S. Dupuis-Girod, J. Medioni, E. Haddad Autoimmunity in Wiskott-Aldrich syndrome: risk factors, clinical features, and outcome in a single-center cohort of 55 patients Pediatrics 111 2003 e622 e627
15. S.B. Snapper, F.S. Rosen, E. Mizoguchi Wiskott-Aldrich syndrome protein-deficient mice reveal a role for WASP in T but not B cell activation Immunity 9 1998 81 90
16. D.D. Nguyen, M.H. Maillard, V. Cotta-de-Almeida Lymphocyte-dependent and Th2 cytokine-associated colitis in mice deficient in Wiskott-Aldrich syndrome protein Gastroenterology 133 2007 1188 1197 (Pubitemid 47494455)
17. A. Franke, T. Balschun, T.H. Karlsen Sequence variants in IL10, ARPC2 and multiple other loci contribute to ulcerative colitis susceptibility Nat Genet 40 2008 1319 1323
18. A.J. Thrasher, S.O. Burns WASP: a key immunological multitasker Nat Rev Immunol 10 2010 182 192
19. M.H. Maillard, V. Cotta-de-Almeida, F. Takeshima The Wiskott-Aldrich syndrome protein is required for the function of CD4(+)CD25(+)Foxp3(+) regulatory T cells J Exp Med 204 2007 381 391 (Pubitemid 46294553)
20. F. Marangoni, S. Trifari, S. Scaramuzza WASP regulates suppressor activity of human and murine CD4(+)CD25(+)FOXP3(+) natural regulatory T cells J Exp Med 204 2007 369 380 (Pubitemid 46294552)
21. S. Humblet-Baron, B. Sather, S. Anover Wiskott-Aldrich syndrome protein is required for regulatory T cell homeostasis J Clin Invest 117 2007 407 418 (Pubitemid 46203969)
22. M. Adriani, J. Aoki, R. Horai Impaired in vitro regulatory T cell function associated with Wiskott-Aldrich syndrome Clin Immunol 124 2007 41 48 (Pubitemid 46936247)
23. L.S. Westerberg, M.A. de la Fuente, F. Wermeling WASP confers selective advantage for specific hematopoietic cell populations and serves a unique role in marginal zone B-cell homeostasis and function Blood 112 2008 4139 4147
24. S. Burns, A.J. Thrasher, M.P. Blundell Configuration of human dendritic cell cytoskeleton by Rho GTPases, the WAS protein, and differentiation Blood 98 2001 1142 1149
25. G. Bouma, S. Burns, A.J. Thrasher Impaired T-cell priming in vivo resulting from dysfunction of WASp-deficient dendritic cells Blood 110 2007 4278 4284 (Pubitemid 351377792)
26. S.B. Snapper, P. Meelu, D. Nguyen WASP deficiency leads to global defects of directed leukocyte migration in vitro and in vivo J Leukoc Biol 77 2005 993 998 (Pubitemid 40770852)
27. S. de Noronha, S. Hardy, J. Sinclair Impaired dendritic-cell homing in vivo in the absence of Wiskott-Aldrich syndrome protein Blood 105 2005 1590 1597 (Pubitemid 40223679)
28. S. Tsuboi, J. Meerloo Wiskott-Aldrich syndrome protein is a key regulator of the phagocytic cup formation in macrophages J Biol Chem 282 2007 34194 34203 (Pubitemid 350159472)
29. M. Locci, E. Draghici, F. Marangoni The Wiskott-Aldrich syndrome protein is required for iNKT cell maturation and function J Exp Med 206 2009 735 742
30. J. Pulecio, E. Tagliani, A. Scholer Expression of Wiskott-Aldrich syndrome protein in dendritic cells regulates synapse formation and activation of naive CD8+ T cells J Immunol 181 2008 1135 1142
31. G. Bouma, A. Mendoza-Naranjo, M.P. Blundell Cytoskeletal remodeling mediated by WASP in dendritic cells is necessary for normal immune synapse formation and T-cell priming Blood 118 2011 2492 2501
32. J.D. Milner, J.M. Ward, A. Keane-Myers Lymphopenic mice reconstituted with limited repertoire T cells develop severe, multiorgan, Th2-associated inflammatory disease Proc Natl Acad Sci U S A 104 2007 576 581 (Pubitemid 46123067)
33. K.J. Maloy Induction and regulation of inflammatory bowel disease in immunodeficient mice by distinct CD4+ T-cell subsets Methods Mol Biol 380 2007 327 335 (Pubitemid 350183337)
34. J.L. Coombes, K.R. Siddiqui, C.V. Arancibia-Carcamo A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism J Exp Med 204 2007 1757 1764 (Pubitemid 47236314)
35. K. Fujimoto, T. Karuppuchamy, N. Takemura A new subset of CD103+CD8alpha+ dendritic cells in the small intestine expresses TLR3, TLR7, and TLR9 and induces Th1 response and CTL activity J Immunol 186 2011 6287 6295
36. K.J. Maloy, F. Powrie Intestinal homeostasis and its breakdown in inflammatory bowel disease Nature 474 2011 298 306
37. S. Agarwal, C. Cunningham-Rundles Autoimmunity in common variable immunodeficiency Curr Allergy Asthma Rep 9 2009 347 352
38. C.J. Winstead, J.M. Fraser, A. Khoruts Regulatory CD4+CD25+Foxp3+ T cells selectively inhibit the spontaneous form of lymphopenia-induced proliferation of naive T cells J Immunol 180 2008 7305 7317
39. J. Suffner, K. Hochweller, M.C. Kuhnle Dendritic cells support homeostatic expansion of Foxp3+ regulatory T cells in Foxp3.LuciDTR mice J Immunol 184 2010 1810 1820
40. D. Zicha, W.E. Allen, P.M. Brickell Chemotaxis of macrophages is abolished in the Wiskott-Aldrich syndrome Br J Haematol 101 1998 659 665 (Pubitemid 28308514)
41. J.H. Niess, G. Adler Enteric flora expands gut lamina propria CX3CR1+ dendritic cells supporting inflammatory immune responses under normal and inflammatory conditions J Immunol 184 2010 2026 2037
42. N. Mach, S. Gillessen, S.B. Wilson Differences in dendritic cells stimulated in vivo by tumors engineered to secrete granulocyte-macrophage colony-stimulating factor or Flt3-ligand Cancer Res 60 2000 3239 3246 (Pubitemid 30407923)
43. D.D. Nguyen, M.H. Maillard, V. Cotta-de-Almeida Lymphocyte-dependent and Th2 cytokine-associated colitis in mice deficient in Wiskott-Aldrich syndrome protein Gastroenterology 133 2007 1188 1197 (Pubitemid 47494455)
44. M.F. Tomczak, S.E. Erdman, A. Davidson Inhibition of Helicobacter hepaticus-induced colitis by IL-10 requires the p50/p105 subunit of NF-kappa B J Immunol 177 2006 7332 7339 (Pubitemid 44715103)