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PMID: 22993206 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Th17 cells upregulate polymeric Ig receptor and intestinal IgA and contribute to intestinal homeostasis.

Journal of immunology (Baltimore, Md. : 1950) ·Vol. 189 ·No. 9 ·2012-11-01 ·Pages 4666-73

Cao AT, Yao S, Gong B, Elson CO, Cong Y

Abstract

Although CD4(+) Th17 cells are enriched in normal intestines, their role in regulation of the host response to microbiota, and whether and how they contribute to intestinal homeostasis, is still largely unknown. It is also unclear whether Th17 cells regulate intestinal IgA production, which is also abundant in the intestinal lumen and has a crucial role as the first defense line in host response to microbiota. In this study, we found that intestinal polymeric Ig receptor (pIgR) and IgA production was impaired in T cell-deficient TCR-βxδ(-/-) mice. Repletion of TCR-βxδ(-/-) mice with Th17 cells from CBir1 flagellin TCR transgenic mice, which are specific for a commensal Ag, increased intestinal pIgR and IgA. The levels of intestinal pIgR and IgA in B6.IL-17R (IL-17R(-/-)) mice were lower than wild type mice. Treatment of colonic epithelial HT-29 cells with IL-17 increased pIgR expression. IL-17R(-/-) mice demonstrated systemic antimicroflora Ab response. Consistently, administering dextran sulfate sodium (DSS) to C57BL/6 mice after treatment with IL-17-neutralizing Ab resulted in more severe intestinal inflammation compared with control Ab. Administering DSS to IL-17R(-/-) mice resulted in increased weight loss and more severe intestinal inflammation compared with wild type mice, indicating a protective role of Th17 cells in intestinal inflammation. Individual mice with lower levels of pIgR and intestinal-secreted IgA correlated with increased weight loss at the end of DSS administration. Collectively, our data reveal that microbiota-specific Th17 cells contribute to intestinal homeostasis by regulating intestinal pIgR expression and IgA secretion.

MeSH Terms
Animals Colitis/chemically induced,genetics,immunology Dextran Sulfate/administration & dosage,toxicity Drug Administration Schedule HT29 Cells Homeostasis/drug effects,genetics,immunology Humans Immunoglobulin A/biosynthesis Intestinal Mucosa/immunology,metabolism,pathology Mice Mice, Inbred C57BL Mice, Knockout Mice, Transgenic Receptors, Interleukin/deficiency,genetics Receptors, Polymeric Immunoglobulin/biosynthesis Th17 Cells/immunology,metabolism,pathology Up-Regulation/drug effects,genetics,immunology
Chemicals
IL17RC protein, human Immunoglobulin A Receptors, Interleukin Receptors, Polymeric Immunoglobulin Dextran Sulfate
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Cao Anthony T
Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX 77555, USA.
Yao Suxia
Gong Bin
Elson Charles O
Cong Yingzi
References (45)
45 references, click to expand
  1. Regulation of innate and adaptive immunity by the commensal microbiota.
    Curr Opin Immunol. 2011 Jun;23(3):353-60 PMID: 21466955
  2. De novo synthesized RelB mediates TNF-induced up-regulation of the human polymeric Ig receptor.
    J Immunol. 2004 Aug 1;173(3):1849-57 PMID: 15265917
  3. A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota.
    Proc Natl Acad Sci U S A. 2009 Nov 17;106(46):19256-61 PMID: 19889972
  4. Involvement of IL-17A in the pathogenesis of DSS-induced colitis in mice.
    Biochem Biophys Res Commun. 2008 Dec 5;377(1):12-6 PMID: 18796297
  5. Monoclonal anti-interleukin 23 reverses active colitis in a T cell-mediated model in mice.
    Gastroenterology. 2007 Jun;132(7):2359-70 PMID: 17570211
  6. Bacterial flagellin is a dominant antigen in Crohn disease.
    J Clin Invest. 2004 May;113(9):1296-306 PMID: 15124021
  7. Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22.
    J Exp Med. 2009 Jan 16;206(1):35-41 PMID: 19114665
  8. CD4+ T cells reactive to enteric bacterial antigens in spontaneously colitic C3H/HeJBir mice: increased T helper cell type 1 response and ability to transfer disease.
    J Exp Med. 1998 Mar 16;187(6):855-64 PMID: 9500788
  9. Apathogenic, intestinal, segmented, filamentous bacteria stimulate the mucosal immune system of mice.
    Infect Immun. 1993 Jan;61(1):303-6 PMID: 8418051
  10. Experimental models of inflammatory bowel disease.
    Gastroenterology. 1995 Oct;109(4):1344-67 PMID: 7557106
  11. Interleukin-17-producing gammadelta T cells selectively expand in response to pathogen products and environmental signals.
    Immunity. 2009 Aug 21;31(2):321-30 PMID: 19682928
  12. Critical role of IL-17 receptor signaling in acute TNBS-induced colitis.
    Inflamm Bowel Dis. 2006 May;12(5):382-8 PMID: 16670527
  13. A protective function for interleukin 17A in T cell-mediated intestinal inflammation.
    Nat Immunol. 2009 Jun;10(6):603-9 PMID: 19448631
  14. Secretory component delays the conversion of secretory IgA into antigen-binding competent F(ab')2: a possible implication for mucosal defense.
    J Immunol. 1998 Nov 15;161(10):5445-53 PMID: 9820520
  15. Neutralization of interleukin-17 aggravates dextran sulfate sodium-induced colitis in mice.
    Clin Immunol. 2004 Jan;110(1):55-62 PMID: 14962796
  16. Treg cell-IgA axis in maintenance of host immune homeostasis with microbiota.
    Int Immunopharmacol. 2011 May;11(5):589-92 PMID: 21111079
  17. The biology of intestinal immunoglobulin A responses.
    Immunity. 2008 Jun;28(6):740-50 PMID: 18549797
  18. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine.
    Cell Host Microbe. 2008 Oct 16;4(4):337-49 PMID: 18854238
  19. Th17 cells induce colitis and promote Th1 cell responses through IL-17 induction of innate IL-12 and IL-23 production.
    J Immunol. 2011 Jun 1;186(11):6313-8 PMID: 21531892
  20. Intestinal bacterial colonization induces mutualistic regulatory T cell responses.
    Immunity. 2011 May 27;34(5):794-806 PMID: 21596591
  21. Requirement for both JAK-mediated PI3K signaling and ACT1/TRAF6/TAK1-dependent NF-kappaB activation by IL-17A in enhancing cytokine expression in human airway epithelial cells.
    J Immunol. 2007 Nov 15;179(10):6504-13 PMID: 17982039
  22. Late developmental plasticity in the T helper 17 lineage.
    Immunity. 2009 Jan 16;30(1):92-107 PMID: 19119024
  23. Regulation of the polymeric Ig receptor by signaling through TLRs 3 and 4: linking innate and adaptive immune responses.
    J Immunol. 2005 Jul 1;175(1):376-84 PMID: 15972671
  24. Cutting edge: regulatory T cells induce CD4+CD25-Foxp3- T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta.
    J Immunol. 2007 Jun 1;178(11):6725-9 PMID: 17513718
  25. Novel functions of the polymeric Ig receptor: well beyond transport of immunoglobulins.
    Trends Immunol. 2003 Feb;24(2):55-8 PMID: 12547499
  26. Long-term exposure of the HT-29 human intestinal epithelial cell line to TNF causes sustained up-regulation of the polymeric Ig receptor and proinflammatory genes through transcriptional and posttranscriptional mechanisms.
    J Immunol. 2005 Jun 1;174(11):7278-84 PMID: 15905574
  27. Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut.
    Immunity. 2008 Aug 15;29(2):261-71 PMID: 18656387
  28. Tight mucosal compartmentation of the murine immune response to antigens of the enteric microbiota.
    Gastroenterology. 2006 Jun;130(7):2050-9 PMID: 16762628
  29. Absence of epithelial immunoglobulin A transport, with increased mucosal leakiness, in polymeric immunoglobulin receptor/secretory component-deficient mice.
    J Exp Med. 1999 Oct 4;190(7):915-22 PMID: 10510081
  30. Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease.
    Nature. 2008 Jan 10;451(7175):211-5 PMID: 18185592
  31. Increased expression of interleukin 17 in inflammatory bowel disease.
    Gut. 2003 Jan;52(1):65-70 PMID: 12477762
  32. Microbial lipopeptides induce the production of IL-17 in Th cells.
    J Immunol. 2000 Dec 1;165(11):6107-15 PMID: 11086043
  33. Induction of colonic regulatory T cells by indigenous Clostridium species.
    Science. 2011 Jan 21;331(6015):337-41 PMID: 21205640
  34. Adaptive immunity in the host-microbiota dialog.
    Mucosal Immunol. 2011 Jan;4(1):15-21 PMID: 20944557
  35. Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system.
    Infect Immun. 1999 Apr;67(4):1992-2000 PMID: 10085047
  36. Isolation of flagellated bacteria implicated in Crohn's disease.
    Inflamm Bowel Dis. 2007 Oct;13(10):1191-201 PMID: 17712838
  37. Generation of mucosal dendritic cells from bone marrow reveals a critical role of retinoic acid.
    J Immunol. 2010 Nov 15;185(10):5915-25 PMID: 20944006
  38. Contribution of polymeric immunoglobulin receptor to regulation of intestinal inflammation in dextran sulfate sodium-induced colitis.
    J Gastroenterol Hepatol. 2006 Sep;21(9):1372-80 PMID: 16911679
  39. Regulation of the polymeric immunoglobulin receptor by the classical and alternative NF-κB pathways in intestinal epithelial cells.
    Mucosal Immunol. 2011 Jul;4(4):468-78 PMID: 21451502
  40. Requirement for Runx proteins in IgA class switching acting downstream of TGF-beta 1 and retinoic acid signaling.
    J Immunol. 2010 Mar 15;184(6):2785-92 PMID: 20142360
  41. The biological functions of T helper 17 cell effector cytokines in inflammation.
    Immunity. 2008 Apr;28(4):454-67 PMID: 18400188
  42. Cutting edge: lung mucosal Th17-mediated responses induce polymeric Ig receptor expression by the airway epithelium and elevate secretory IgA levels.
    J Immunol. 2009 Apr 15;182(8):4507-11 PMID: 19342622
  43. The regulation of IgA class switching.
    Nat Rev Immunol. 2008 Jun;8(6):421-34 PMID: 18483500
  44. Induction of intestinal Th17 cells by segmented filamentous bacteria.
    Cell. 2009 Oct 30;139(3):485-98 PMID: 19836068
  45. T helper 1 and T helper 2 cells are pathogenic in an antigen-specific model of colitis.
    J Exp Med. 2002 Jan 7;195(1):71-84 PMID: 11781367
Article Info
Journal
Journal of immunology (Baltimore, Md. : 1950)
Abbr.
J Immunol
ISSN
1550-6606
Published
2012-11-01
Epub
2012-00-19
Pages
4666-73
Language
English
Region
United States
NLM ID
2985117R
PMCID
PMC3478497
Subset
IM
Grants
NIAID NIH HHS · AI083484 · United States
NIDDK NIH HHS · DK071176 · United States
NIDDK NIH HHS · R01 DK079918 · United States
NIDDK NIH HHS · DK079918 · United States
NIDDK NIH HHS · P01 DK071176 · United States
NIAID NIH HHS · R21 AI083484 · United States
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