Invariant NKT cells regulate experimental autoimmune uveitis through inhibition of Th17 differentiation

Eur J Immunol. 2011 Feb;41(2):392-402. doi: 10.1002/eji.201040569. Epub 2010 Dec 29.

Abstract

Although NKT cells have been implicated in diverse immunomodulatory responses, the effector mechanisms underlying the NKT cell-mediated regulation of pathogenic T helper cells are not well understood. Here, we show that invariant NKT cells inhibited the differentiation of CD4(+) T cells into Th17 cells both in vitro and in vivo. The number of IL-17-producing CD4(+) T cells was reduced following co-culture with purified NK1.1(+) TCR(+) cells from WT, but not from CD1d(-/-) or Jα18(-/-) , mice. Co-cultured NKT cells from either cytokine-deficient (IL-4(-/-) , IL-10(-/-) , or IFN-γ(-/-) ) or WT mice efficiently inhibited Th17 differentiation. The contact-dependent mechanisms of NKT cell-mediated regulation of Th17 differentiation were confirmed using transwell co-culture experiments. On the contrary, the suppression of Th1 differentiation was dependent on IL-4 derived from the NKT cells. The in vivo regulatory capacity of NKT cells on Th17 cells was confirmed using an experimental autoimmune uveitis model induced with human IRBP(1-20) (IRBP, interphotoreceptor retinoid-binding protein) peptide. NKT cell-deficient mice (CD1d(-/-) or Jα18(-/-) ) demonstrated an increased disease severity, which was reversed by the transfer of WT or cytokine-deficient (IL-4(-/-) , IL-10(-/-) , or IFN-γ(-/-) ) NKT cells. Our results indicate that invariant NKT cells inhibited autoimmune uveitis predominantly through the cytokine-independent inhibition of Th17 differentiation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer
  • Animals
  • Antigens, CD1d / genetics
  • Antigens, CD1d / metabolism
  • Autoimmune Diseases / genetics
  • Autoimmune Diseases / immunology*
  • Autoimmune Diseases / metabolism
  • Autoimmune Diseases / pathology
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / metabolism
  • CD4-Positive T-Lymphocytes / pathology
  • Cell Communication / immunology
  • Cell Count
  • Cell Differentiation / immunology*
  • Cytokines / genetics
  • Cytokines / immunology
  • Disease Models, Animal
  • Eye / pathology
  • Eye Proteins / immunology
  • Interleukin-4 / metabolism
  • Lymphocyte Activation / immunology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Natural Killer T-Cells / immunology*
  • Natural Killer T-Cells / metabolism
  • Natural Killer T-Cells / pathology
  • Natural Killer T-Cells / transplantation
  • Ovalbumin / immunology
  • Peptide Fragments / immunology
  • Retinol-Binding Proteins / immunology
  • Th1 Cells / immunology
  • Th1 Cells / metabolism
  • Th17 Cells / immunology*
  • Th17 Cells / metabolism
  • Uveitis / genetics
  • Uveitis / immunology*
  • Uveitis / metabolism
  • Uveitis / pathology
  • Vaccination

Substances

  • Antigens, CD1d
  • Cd1d1 protein, mouse
  • Cytokines
  • Eye Proteins
  • OVA 323-339
  • Peptide Fragments
  • Retinol-Binding Proteins
  • interstitial retinol-binding protein
  • Interleukin-4
  • Ovalbumin