Bacteria-triggered CD4(+) T regulatory cells suppress Helicobacter hepaticus-induced colitis

J Exp Med. 2002 Aug 19;196(4):505-15. doi: 10.1084/jem.20020556.

Abstract

We have previously demonstrated that interleukin (IL)-10-deficient (IL-10 knockout [KO]) but not wild-type (WT) mice develop colitis after infection with Helicobacter hepaticus. Here, we show that infected recombination activating gene (RAG) KO mice develop intestinal inflammation after reconstitution with CD4(+) T cells from IL-10 KO animals and that the cotransfer of CD4(+) T cells from H. hepaticus-infected but not uninfected WT mice prevents this colitis. The disease-protective WT CD4(+) cells are contained within the CD45RB(low) fraction and unexpectedly were found in both the CD25(+) and the CD25(-) subpopulations of these cells, their frequency being higher in the latter. The mechanism by which CD25(+) and CD25(-) CD45RB(low) CD4(+) cells block colitis involves IL-10 and not transforming growth factor (TGF)-beta, as treatment with anti-IL-10R but not anti-TGF-beta monoclonal antibody abrogated their protective effect. In vitro, CD45RB(low) CD4(+) cells from infected WT mice were shown to produce IL-10 and suppress interferon-gamma production by IL-10 KO CD4(+) cells in an H. hepaticus antigen-specific manner. Together, our data support the concept that H. hepaticus infection results in the induction in WT mice of regulatory T cells that prevent bacteria-induced colitis. The induction of such cells in response to gut flora may be a mechanism protecting normal individuals against inflammatory bowel disease.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Adoptive Transfer
  • Animals
  • Antigens, Bacterial / immunology
  • Biomarkers
  • CD4-Positive T-Lymphocytes / cytology
  • CD4-Positive T-Lymphocytes / immunology*
  • Colitis / immunology*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / immunology
  • Female
  • Helicobacter / immunology
  • Helicobacter Infections / immunology*
  • Interleukin-10 / genetics
  • Interleukin-10 / immunology
  • Interleukin-4 / genetics
  • Interleukin-4 / immunology
  • Leukocyte Common Antigens / immunology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Receptors, Interleukin-2
  • Transforming Growth Factor beta / immunology

Substances

  • Antigens, Bacterial
  • Biomarkers
  • DNA-Binding Proteins
  • Rag2 protein, mouse
  • Receptors, Interleukin-2
  • Transforming Growth Factor beta
  • V(D)J recombination activating protein 2
  • Interleukin-10
  • Interleukin-4
  • Leukocyte Common Antigens