Dual-specificity phosphatase 6 regulates CD4+ T-cell functions and restrains spontaneous colitis in IL-10-deficient mice

Mucosal Immunol. 2015 May;8(3):505-15. doi: 10.1038/mi.2014.84. Epub 2014 Sep 17.

Abstract

Mitogen-activated protein kinase (MAPK) phosphatases are dual-specificity phosphatases (DUSPs) that dephosphorylate phosphothreonine and phosphotyrosine residues within MAPKs. DUSP6 preferentially dephosphorylates extracellular signal-regulated kinases 1 and 2 (ERK1/2) rendering them inactive. Here, we study the role of DUSP6 in CD4(+) T-cell function, differentiation, and inflammatory profile in the colon. Upon T-cell receptor (TCR) stimulation, DUSP6 knockout (Dusp6(-/-)) CD4(+) T cells showed increased ERK1/2 activation, proliferation, T helper 1 differentiation, and interferon-γ production, as well as a marked decrease in survival, interleukin- 17A (IL-17A) secretion, and regulatory T-cell function. To analyze the role of DUSP6 in vivo, we employed the Il10(-/-) model of colitis and generated Il10(-/-)/Dusp6(-/-) double-knockout mice. Il10(-/-)/Dusp6(-/-) mice suffered from accelerated and exacerbated spontaneous colitis, which was prevented by ERK1/2 inhibition. ERK1/2 inhibition also augmented regulatory T-cell differentiation in vitro and in vivo in both C57Bl/6 and Dusp6(-/-) mice. In summary, DUSP6 regulates CD4(+) T-cell activation and differentiation by inhibiting the TCR-dependent ERK1/2 activation. DUSP6 might therefore be a potential intervention target for limiting aberrant T-cell responses in T-cell-mediated diseases, such as inflammatory bowel disease.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Benzamides / pharmacology
  • Cell Differentiation
  • Cell Proliferation
  • Colitis / genetics
  • Colitis / immunology*
  • Colitis / pathology
  • Colon / immunology*
  • Colon / pathology
  • Diphenylamine / analogs & derivatives
  • Diphenylamine / pharmacology
  • Disease Models, Animal
  • Dual Specificity Phosphatase 6 / deficiency
  • Dual Specificity Phosphatase 6 / genetics
  • Dual Specificity Phosphatase 6 / immunology*
  • Gene Expression Regulation
  • Immunity, Mucosal
  • Interferon-gamma / genetics
  • Interferon-gamma / immunology
  • Interleukin-10 / deficiency
  • Interleukin-10 / genetics
  • Interleukin-10 / immunology*
  • Interleukin-17 / genetics
  • Interleukin-17 / immunology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitogen-Activated Protein Kinase 1 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 1 / genetics
  • Mitogen-Activated Protein Kinase 1 / immunology
  • Mitogen-Activated Protein Kinase 3 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 3 / genetics
  • Mitogen-Activated Protein Kinase 3 / immunology
  • Receptors, Antigen, T-Cell / genetics
  • Receptors, Antigen, T-Cell / immunology
  • Signal Transduction
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / pathology
  • Th1 Cells / immunology*
  • Th1 Cells / pathology

Substances

  • Benzamides
  • IL10 protein, mouse
  • Interleukin-17
  • Receptors, Antigen, T-Cell
  • Interleukin-10
  • Interferon-gamma
  • mirdametinib
  • Diphenylamine
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Dual Specificity Phosphatase 6
  • Dusp6 protein, mouse