Home LiteratureArticle Details
PMID: 19889972 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota.

Cong Y, Feng T, Fujihashi K, Schoeb TR, Elson CO

Abstract

A T cell receptor transgenic mouse line reactive to a microbiota flagellin, CBir1, was used to define mechanisms of host microbiota homeostasis. Intestinal IgA, but not serum IgA, was found to block mucosal flagellin uptake and systemic T cell activation in mice. Depletion of CD4(+)CD25(+) Tregs decreased IgA(+) B cells, total IgA, and CBir1-specific IgA in gut within days. Repletion of T cell-deficient mice with either CD4(+)CD25(+) or CD4(+)foxp3(+) Tregs restored intestinal IgA to a much greater extent than their reciprocal CD4(+) subsets, indicating that Tregs are the major helper cells for IgA responses to microbiota antigens such as flagellin. We propose that the major role of this coordinated Treg-IgA response is to maintain commensalism with the microbiota.

MeSH Terms
Animals Antigens, Bacterial/immunology B-Lymphocytes/immunology Flagellin/immunology Forkhead Transcription Factors/immunology Immunoglobulin A/biosynthesis,immunology Interleukin-2 Receptor alpha Subunit/immunology Intestines/immunology,microbiology Lymphocyte Depletion Mice Mice, Transgenic Mucous Membrane/immunology Receptors, Antigen, T-Cell, alpha-beta/genetics T-Lymphocytes, Regulatory/immunology
Chemicals
Antigens, Bacterial CBir1 flagellin Forkhead Transcription Factors Foxp3 protein, mouse Immunoglobulin A Interleukin-2 Receptor alpha Subunit Receptors, Antigen, T-Cell, alpha-beta Flagellin
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Cong Yingzi
Departments of Medicine and Microbiology, Pediatric Dentistry, and Genetics, University of Alabama at Birmingham, AL 35294, USA. [email protected]
Feng Ting
Fujihashi Kohtaro
Schoeb Trenton R
Elson Charles O
References (39)
39 references, click to expand
  1. Bacterial-reactive T regulatory cells inhibit pathogenic immune responses to the enteric flora.
    J Immunol. 2002 Dec 1;169(11):6112-9 PMID: 12444113
  2. Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response.
    Nat Cell Biol. 1999 Sep;1(5):260-6 PMID: 10559937
  3. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut.
    Proc Natl Acad Sci U S A. 2004 Feb 17;101(7):1981-6 PMID: 14766966
  4. Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3- precursor cells in the absence of interleukin 10.
    Nat Immunol. 2007 Sep;8(9):931-41 PMID: 17694059
  5. IgA response to symbiotic bacteria as a mediator of gut homeostasis.
    Cell Host Microbe. 2007 Nov 15;2(5):328-39 PMID: 18005754
  6. TGF-beta1 maintains suppressor function and Foxp3 expression in CD4+CD25+ regulatory T cells.
    J Exp Med. 2005 Apr 4;201(7):1061-7 PMID: 15809351
  7. The regulation of IgA class switching.
    Nat Rev Immunol. 2008 Jun;8(6):421-34 PMID: 18483500
  8. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL.
    Nat Immunol. 2002 Sep;3(9):822-9 PMID: 12154359
  9. B cell-specific deficiency for Smad2 in vivo leads to defects in TGF-beta-directed IgA switching and changes in B cell fate.
    J Immunol. 2006 Feb 15;176(4):2389-96 PMID: 16455997
  10. The biology of intestinal immunoglobulin A responses.
    Immunity. 2008 Jun;28(6):740-50 PMID: 18549797
  11. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5.
    Nat Immunol. 2008 Jul;9(7):769-76 PMID: 18516037
  12. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells.
    Science. 2006 Nov 17;314(5802):1157-60 PMID: 17110582
  13. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria.
    Science. 2004 Mar 12;303(5664):1662-5 PMID: 15016999
  14. TACI and BAFF-R mediate isotype switching in B cells.
    J Exp Med. 2005 Jan 3;201(1):35-9 PMID: 15630136
  15. Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA.
    Nat Immunol. 2004 Jan;5(1):104-12 PMID: 14691478
  16. Monoclonal anti-interleukin 23 reverses active colitis in a T cell-mediated model in mice.
    Gastroenterology. 2007 Jun;132(7):2359-70 PMID: 17570211
  17. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid.
    J Exp Med. 2007 Aug 6;204(8):1775-85 PMID: 17620362
  18. Prokaryotic regulation of epithelial responses by inhibition of IkappaB-alpha ubiquitination.
    Science. 2000 Sep 1;289(5484):1560-3 PMID: 10968793
  19. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae.
    Cell Host Microbe. 2007 Aug 16;2(2):119-29 PMID: 18005726
  20. Regulatory T cells suppress systemic and mucosal immune activation to control intestinal inflammation.
    Immunol Rev. 2006 Aug;212:256-71 PMID: 16903919
  21. TGF-beta receptor controls B cell responsiveness and induction of IgA in vivo.
    Immunity. 2000 Oct;13(4):443-51 PMID: 11070163
  22. The immune geography of IgA induction and function.
    Mucosal Immunol. 2008 Jan;1(1):11-22 PMID: 19079156
  23. Tight mucosal compartmentation of the murine immune response to antigens of the enteric microbiota.
    Gastroenterology. 2006 Jun;130(7):2050-9 PMID: 16762628
  24. Perspectives on mucosal vaccines: is mucosal tolerance a barrier?
    J Immunol. 2007 Nov 1;179(9):5633-8 PMID: 17947632
  25. CD4+CD25bright T cells in human intestinal lamina propria as regulatory cells.
    J Immunol. 2004 Sep 1;173(5):3119-30 PMID: 15322172
  26. Bacterial flagellin is a dominant antigen in Crohn disease.
    J Clin Invest. 2004 May;113(9):1296-306 PMID: 15124021
  27. Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility.
    Nat Immunol. 2003 Dec;4(12):1247-53 PMID: 14625549
  28. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice.
    Nat Immunol. 2007 Feb;8(2):191-7 PMID: 17136045
  29. A microbial symbiosis factor prevents intestinal inflammatory disease.
    Nature. 2008 May 29;453(7195):620-5 PMID: 18509436
  30. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells.
    Nature. 2003 Jul 3;424(6944):88-93 PMID: 12840763
  31. TGF-beta receptor signaling is critical for mucosal IgA responses.
    J Immunol. 2004 Sep 1;173(5):3305-9 PMID: 15322193
  32. Intestinal bacteria trigger T cell-independent immunoglobulin A(2) class switching by inducing epithelial-cell secretion of the cytokine APRIL.
    Immunity. 2007 Jun;26(6):812-26 PMID: 17570691
  33. Mucosal B cells: phenotypic characteristics, transcriptional regulation, and homing properties.
    Immunol Rev. 2005 Aug;206:32-63 PMID: 16048541
  34. Regulation of IgA production by naturally occurring TNF/iNOS-producing dendritic cells.
    Nature. 2007 Aug 23;448(7156):929-33 PMID: 17713535
  35. CD4+CD25+ regulatory T cells in the small intestinal lamina propria show an effector/memory phenotype.
    Int Immunol. 2008 Mar;20(3):307-15 PMID: 18184698
  36. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases.
    Proc Natl Acad Sci U S A. 2007 Aug 21;104(34):13780-5 PMID: 17699621
  37. Ecological and evolutionary forces shaping microbial diversity in the human intestine.
    Cell. 2006 Feb 24;124(4):837-48 PMID: 16497592
  38. Distinct populations of dendritic cells are present in the subepithelial dome and T cell regions of the murine Peyer's patch.
    J Exp Med. 1996 Jan 1;183(1):237-47 PMID: 8551227
  39. 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. 2007 Aug 6;204(8):1757-64 PMID: 17620361
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2009-11-17
Epub
2009-00-04
Pages
19256-61
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2780781
Subset
IM
Grants
NIDDK NIH HHS · DK064400 · United States
NIDDK NIH HHS · R24 DK064400 · United States
NCRR NIH HHS · RR-20136 · United States
NCRR NIH HHS · C06 RR020136 · United States
NIDDK NIH HHS · R01 DK079918 · United States
NIDDK NIH HHS · DK079918 · United States
NIDDK NIH HHS · P01 DK071176 · United States
NIDDK NIH HHS · DK06400 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]