FOXP3+ Tregs require WASP to restrain Th2-mediated food allergy

Journal of Clinical Investigation

Volumn 126, Issue 10, 2016, Pages 4030-4044

  Lexmond, Willem S ^a,b   Goettel, Jeremy A ^a,b   Lyons, Jonathan J ^c   Jacobse, Justin ^a   Deken, Marion M ^a   Lawrence, Monica G ^d   DiMaggio, Thomas H ^c   Kotlarz, Daniel ^a,e   Garabedian, Elizabeth ^f   Sackstein, Paul ^c   Nelson, Celeste C ^c   Jones, Nina ^g   Stone, Kelly D ^c   Candotti, Fabio ^f   Rings, Edmond H H M ^h   Thrasher, Adrian J ⁱ   Milner, Joshua D ^c   Snapper, Scott B ^a,b,j   Fiebiger, Edda ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^e LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^f NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^g FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^h ERASMUS MEDICAL CENTER   (Netherlands)

ⁱ UNIVERSITY COLLEGE LONDON   (United Kingdom)

^j BRIGHAM AND WOMEN S HOSPITAL   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

FOOD ALLERGEN; IMMUNOGLOBULIN E; INTERLEUKIN 4; SOYBEAN PROTEIN; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; WISKOTT ALDRICH SYNDROME PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; TRANSCRIPTOME; WAS PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; EFFECTOR CELL; ENTERITIS; FEMALE; FOOD ALLERGY; GENE DELETION; HOUSING; HUMAN; HUMAN CELL; IMMUNE SYSTEM; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; MALE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; SENSITIZATION; TH1 CELL; TH17 CELL; TH2 CELL; WHEAT; WISKOTT ALDRICH SYNDROME; 129 MOUSE; ANIMAL; CELL DIFFERENTIATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MUTATION; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; FEMALE; FOOD HYPERSENSITIVITY; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNOGLOBULIN E; MALE; MICE, 129 STRAIN; MICE, KNOCKOUT; MUTATION; T-LYMPHOCYTES, REGULATORY; TH2 CELLS; TRANSCRIPTOME; WISKOTT-ALDRICH SYNDROME PROTEIN;

EID: 84991735297     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI85129     Document Type: Article

References (63)

1. Wynn TA. Type 2 cytokines: mechanisms and therapeutic strategies. Nat Rev Immunol. 2015;15(5):271-282.
2. Pulendran B, Artis D. New paradigms in type 2 immunity. Science. 2012;337(6093):431-435.
3. Palm NW, Rosenstein RK, Medzhitov R. Allergic host defences. Nature. 2012;484(7395):465-472.
4. Ramsdell F, Ziegler SF. FOXP3 and scurfy: how it all began. Nat Rev Immunol. 2014;14(5):343-349.
5. Suscovich TJ, Perdue NR, Campbell DJ. Type-1 immunity drives early lethality in scurfy mice. Eur J Immunol. 2012;42(9):2305-2310.
6. Lin W, et al. Allergic dysregulation and hyperimmunoglobulinemia E in Foxp3 mutant mice. J Allergy Clin Immunol. 2005;116(5):1106-1115.
7. Akdis CA, Akdis M. Mechanisms and treatment of allergic disease in the big picture of regulatory T cells. J Allergy Clin Immunol. 2009;123(4):735-747.
8. Dhainaut M, et al. Thymus-derived regulatory T cells restrain pro-inflammatory Th1 responses by downregulating CD70 on dendritic cells. EMBO J. 2015;34(10):1336-1348.
9. Josefowicz SZ, et al. Extrathymically generated regulatory T cells control mucosal TH2 inflammation. Nature. 2012;482(7385):395-399.
10. Yu F, Sharma S, Edwards J, Feigenbaum L, Zhu J. Dynamic expression of transcription factors T-bet and GATA-3 by regulatory T cells maintains immunotolerance. Nat Immunol. 2015;16(2):197-206.
11. Li X, Zheng Y. Regulatory T cell identity: formation and maintenance. Trends Immunol. 2015;36(6):344-353.
12. Josefowicz SZ, Lu LF, Rudensky AY. Regulatory T cells: mechanisms of differentiation and function. Annu Rev Immunol. 2012;30:531-564.
13. Ozcan E, Notarangelo LD, Geha RS. Primary immune deficiencies with aberrant IgE production. J Allergy Clin Immunol. 2008; 122(6):1054-1063.
14. Altered T-cell receptor signaling in the pathogenesis of allergic disease. J Allergy Clin Immunol. 2011;127(2):351-354.
15. Yong PF, Freeman AF, Engelhardt KR, Holland S, Puck JM, Grimbacher B. An update on the hyper-IgE syndromes. Arthritis Res Ther. 2012;14(6):228.
16. Liston A, Enders A, Siggs OM. Unravelling the association of partial T-cell immunodeficiency and immune dysregulation. Nat Rev Immunol. 2008;8(7):545-558.
17. Sassi A, et al. Hypomorphic homozygous mutations in phosphoglucomutase 3 (PGM3) impair immunity and increase serum IgE levels. J Allergy Clin Immunol. 2014;133(5):1410-1419.e1.
18. Zhang Y, et al. Autosomal recessive phosphoglucomutase 3 (PGM3) mutations link glycosylation defects to atopy, immune deficiency, autoimmunity, and neurocognitive impairment. J Allergy Clin Immunol. 2014;133(5):1400-1409.e1.
19. Thrasher AJ, Burns SO. WASP: a key immunological multitasker. Nat Rev Immunol. 2010;10(3):182-192.
20. Snapper SB, Rosen FS. The Wiskott-Aldrich syndrome protein (WASP): roles in signaling and cytoskeletal organization. Annu Rev Immunol. 1999;17:905-929.
21. Albert MH, Notarangelo LD, Ochs HD. Clinical spectrum, pathophysiology and treatment of the Wiskott-Aldrich syndrome. Curr Opin Hematol. 2011;18(1):42-48.
22. Tuano KS, Orange JS, Sullivan K, Cunningham-Rundles C, Bonilla FA, Davis CM. Food allergy in patients with primary immunodeficiency diseases: prevalence within the US Immunodeficiency Network (USIDNET). J Allergy Clin Immunol. 2015;135(1):273-275.
23. Salo PM, et al. Prevalence of allergic sensitization in the United States: results from the National Health and Nutrition Examination Survey (NHANES) 2005-2006. J Allergy Clin Immunol. 2014;134(2):350-359.
24. McGowan EC, Keet CA. Prevalence of self-reported food allergy in the National Health and Nutrition Examination Survey (NHANES) 2007-2010. J Allergy Clin Immunol. 2013;132(5):1216-1219.e5.
25. Eigenmann PA, Sicherer SH, Borkowski TA, Cohen BA, Sampson HA. Prevalence of IgEmediated food allergy among children with atopic dermatitis. Pediatrics. 1998;101(3):E8.
26. Snapper SB, et al. Wiskott-Aldrich syndrome protein-deficient mice reveal a role for WASP in T but not B cell activation. Immunity. 1998;9(1):81-91.
27. Nguyen DD, et al. Lymphocyte-dependent and Th2 cytokine-associated colitis in mice deficient in Wiskott-Aldrich syndrome protein. Gastroenterology. 2007;133(4):1188-1197.
28. Föger N, Jenckel A, Orinska Z, Lee KH, Chan AC, Bulfone-Paus S. Differential regulation of mast cell degranulation versus cytokine secretion by the actin regulatory proteins Coronin1a and Coronin1b. J Exp Med. 2011;208(9):1777-1787.
29. Burton OT, et al. Oral immunotherapy induces IgG antibodies that act through FcγRIIb to suppress IgE-mediated hypersensitivity. J Allergy Clin Immunol. 2014;134(6):1310-1317.e6.
30. Hogan SP, Wang YH, Strait R, Finkelman FD. Food-induced anaphylaxis: mast cells as modulators of anaphylactic severity. Semin Immunopathol. 2012;34(5):643-653.
31. Caffarelli C, Romanini E, Caruana P, Street ME, de' Angelis G. Clinical food hypersensitivity: the relevance of duodenal immunoglobulin E-positive cells. Pediatr Res. 1998;44(4):485-490.
32. Brandt EB, et al. Mast cells are required for experimental oral allergen-induced diarrhea. J Clin Invest. 2003;112(11):1666-1677.
33. Burton OT, et al. Direct effects of IL-4 on mast cells drive their intestinal expansion and increase susceptibility to anaphylaxis in a murine model of food allergy. Mucosal Immunol. 2013;6(4):740-750.
34. Platzer B, et al. Dendritic cell-bound IgE functions to restrain allergic inflammation at mucosal sites. Mucosal Immunol. 2015;8(3):516-532.
35. Khodoun MV, Strait R, Armstrong L, Yanase N, Finkelman FD. Identification of markers that distinguish IgE-from IgG-mediated anaphylaxis. Proc Natl Acad Sci U S A. 2011;108(30):12413-12418.
36. Stefka AT, et al. Commensal bacteria protect against food allergen sensitization. Proc Natl Acad Sci U S A. 2014;111(36):13145-13150.
37. Noval Rivas M, et al. A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis. J Allergy Clin Immunol. 2013;131(1):201-212.
38. Cahenzli J, Köller Y, Wyss M, Geuking MB, McCoy KD. Intestinal microbial diversity during early-life colonization shapes long-term IgE levels. Cell Host Microbe. 2013;14(5):559-570.
39. Maillard MH, et al. The Wiskott-Aldrich syndrome protein is required for the function of CD4(+)CD25(+)Foxp3(+) regulatory T cells. J Exp Med. 2007;204(2):381-391.
40. Westerberg L, Larsson M, Hardy SJ, Fernández C, Thrasher AJ, Severinson E. Wiskott-Aldrich syndrome protein deficiency leads to reduced B-cell adhesion, migration, and homing, and a delayed humoral immune response. Blood. 2005;105(3):1144-1152.
41. Humblet-Baron S, et al. Wiskott-Aldrich syndrome protein is required for regulatory T cell homeostasis. J Clin Invest. 2007;117(2):407-418.
42. Marangoni F, et al. WASP regulates suppressor activity of human and murine CD4(+)CD25(+) FOXP3(+) natural regulatory T cells. J Exp Med. 2007;204(2):369-380.
43. Weiss JM, et al. Neuropilin 1 is expressed on thymus-derived natural regulatory T cells, but not mucosa-generated induced Foxp3+ T reg cells. J Exp Med. 2012;209(10):1723-1742.
44. Yadav M, et al. Neuropilin-1 distinguishes natural and inducible regulatory T cells among regulatory T cell subsets in vivo. J Exp Med. 2012;209(10):1713-1722.
45. Nurieva RI, et al. Transcriptional regulation of th2 differentiation by inducible costimulator. Immunity. 2003;18(6):801-811.
46. Tindemans I, Serafini N, Di Santo JP, Hendriks RW. GATA-3 function in innate and adaptive immunity. Immunity. 2014;41(2):191-206.
47. Noval Rivas M, et al. Regulatory T cell reprogramming toward a Th2-cell-like lineage impairs oral tolerance and promotes food allergy. Immunity. 2015;42(3):512-523.
48. Ulges A, et al. Protein kinase CK2 enables regulatory T cells to suppress excessive TH2 responses in vivo. Nat Immunol. 2015;16(3):267-275.
49. Matalon O, Reicher B, Barda-Saad M. Wiskott-Aldrich syndrome protein-dynamic regulation of actin homeostasis: from activation through function and signal termination in T lymphocytes. Immunol Rev. 2013;256(1):10-29.
50. Massaad MJ, Ramesh N, Geha RS. Wiskott-Aldrich syndrome: a comprehensive review. Ann N Y Acad Sci. 2013;1285:26-43.
51. Sicherer SH, Sampson HA. Food allergy. J Allergy Clin Immunol. 2010;125(2 Suppl 2):S116-S125.
52. Wang J, Sampson HA. Food allergy. J Clin Invest. 2011;121(3):827-835.
53. Recher M, et al. B cell-intrinsic deficiency of the Wiskott-Aldrich syndrome protein (WASp) causes severe abnormalities of the peripheral B-cell compartment in mice. Blood. 2012;119(12):2819-2828.
54. Morales-Tirado V, et al. Critical requirement for the Wiskott-Aldrich syndrome protein in Th2 effector function. Blood. 2010;115(17):3498-3507.
55. Pivniouk VI, et al. Impaired signaling via the high-affinity IgE receptor in Wiskott-Aldrich syndrome protein-deficient mast cells. Int Immunol. 2003;15(12):1431-1440.
56. Sommers CL, et al. A LAT mutation that inhibits T cell development yet induces lymphoproliferation. Science. 2002;296(5575):2040-2043.
57. Aguado E, et al. Induction of T helper type 2 immunity by a point mutation in the LAT adaptor. Science. 2002;296(5575):2036-2040.
58. Barda-Saad M, Braiman A, Titerence R, Bunnell SC, Barr VA, Samelson LE. Dynamic molecular interactions linking the T cell antigen receptor to the actin cytoskeleton. Nat Immunol. 2005;6(1):80-89.
59. Zhang J, et al. Antigen receptor-induced activation and cytoskeletal rearrangement are impaired in Wiskott-Aldrich syndrome protein-deficient lymphocytes. J Exp Med. 1999;190(9):1329-1342.
60. Vahl JC, et al. Continuous T cell receptor signals maintain a functional regulatory T cell pool. Immunity. 2014;41(5):722-736.
61. Levine AG, Arvey A, Jin W, Rudensky AY. Continuous requirement for the TCR in regulatory T cell function. Nat Immunol. 2014;15(11):1070-1078.
62. Wada T, et al. Somatic mosaicism in Wiskott-Aldrich syndrome suggests in vivo reversion by a DNA slippage mechanism. Proc Natl Acad Sci U S A. 2001;98(15):8697-8702.
63. Milner JD, et al. Early-onset lymphoproliferation and autoimmunity caused by germline STAT3 gain-of-function mutations. Blood. 2015;125(4):591-599.