Suppressor of cytokine signaling-1 ameliorates dextran sulfate sodium-induced colitis in mice

Int Immunol. 2008 Jun;20(6):753-62. doi: 10.1093/intimm/dxn033. Epub 2008 Apr 1.

Abstract

Inflammatory bowel disease (IBD) is a chronic disorder of the gastrointestinal tract. Although the etiology and pathogenesis of IBD remain unknown, pro-inflammatory cytokines including IFN-gamma play an important role in the development of IBD. Suppressor of cytokine signaling-1 (SOCS-1) is a crucial inhibitor of cytokine signaling, particularly of IFN-gamma. In this study, we investigated the role of SOCS-1 in the development of murine dextran sulfate sodium (DSS)-induced colitis, a model of colitis resembling human IBD. SOCS-1 heterozygous (SOCS-1(+/-)) and wild-type (WT) mice were given 3% DSS dissolved in drinking water for 5 days. Activation and expression of signal transducers and activators of transcription (STAT) in colonic tissues were assessed by western blot analysis. The expression of CD4, IFN-gamma, IL-4, IL-17 and Forkhead box P3 (Foxp3) in colonic lamina propria lymphocytes was analyzed by flow cytometry and cytokine concentrations in serum were measured. DSS-treated SOCS-1(+/-) mice developed more severe colitis than DSS-treated WT mice. Enhanced activation of STAT1, a higher ratio of CD4(+)IFN-gamma(+) T cells and a lower frequency of Foxp3(+) regulatory T (Treg) cells, were observed in the colon of DSS-treated SOCS-1(+/-) mice compared with DSS-treated WT mice. DSS-treated SOCS-1(+/-) mice showed higher levels of IFN-gamma in sera than did DSS-treated WT mice. Furthermore, T cell-specific SOCS-1-conditional knockout mice developed more severe colitis than control mice after DSS administration. Our findings suggest that SOCS-1, particularly in T cells, prevents the development of DSS-induced colitis in mice by inhibiting IFN-gamma/STAT1 signaling and by subsequently regulating Treg cell development.

MeSH terms

  • Animals
  • CD4-Positive T-Lymphocytes / metabolism
  • CD4-Positive T-Lymphocytes / pathology
  • Colitis / chemically induced*
  • Colitis / immunology*
  • Colitis / metabolism
  • Colitis / pathology
  • Dextran Sulfate / toxicity*
  • Disease Models, Animal
  • Forkhead Transcription Factors / biosynthesis*
  • Forkhead Transcription Factors / immunology
  • Inflammatory Bowel Diseases / immunology
  • Interferon-gamma / blood
  • Mice
  • Mice, Knockout
  • Mucous Membrane / immunology
  • Mucous Membrane / metabolism
  • Mucous Membrane / pathology
  • STAT1 Transcription Factor / biosynthesis*
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling Proteins / genetics
  • Suppressor of Cytokine Signaling Proteins / immunology*
  • Suppressor of Cytokine Signaling Proteins / metabolism
  • T-Lymphocytes, Regulatory / metabolism
  • T-Lymphocytes, Regulatory / pathology

Substances

  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • STAT1 Transcription Factor
  • Socs1 protein, mouse
  • Stat1 protein, mouse
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling Proteins
  • Interferon-gamma
  • Dextran Sulfate