Critical role for CD1d-restricted invariant NKT cells in stimulating intrahepatic CD8 T-cell responses to liver antigen

Gastroenterology. 2008 Jun;134(7):2132-43. doi: 10.1053/j.gastro.2008.02.037. Epub 2008 Feb 21.

Abstract

Background & aims: V alpha14 invariant natural killer T cells (iNKT) are localized in peripheral tissues such as the liver rather than lymphoid tissues. Therefore, their role in modulating the stimulation of conventional, major histocompatibility complex (MHC)-restricted T-cell responses has remained ambiguous. We here describe a role for V alpha14 iNKT cells in modulating conventional T-cell responses to antigen expressed in liver, using transferrin-mOVA (Tf-mOVA) mice.

Methods: Naïve ovalbumin-specific class I MHC-restricted T cells (OTI) were adoptively transferred into Tf-mOVA mice in the presence or absence of iNKT-cell agonist alpha-galactosylceramide, after which OTI T-cell priming, antigen-specific cytokine production, cytotoxic killing ability, and liver damage were analyzed.

Results: Transfer of OTI cells resulted in robust intrahepatic, antigen-specific proliferation of T cells. OTI T cells were activated in liver, and antigen-specific effector function was stimulated by coactivation of Valpha14 iNKT cells using alpha-galactosylceramide. This stimulation was absent in CD1d(-/-)Tf-mOVA mice, which lack V alpha14 iNKT cells, and was prevented when interferon-gamma and tumor necrosis factor-alpha production by V alpha14 iNKT cells was blocked.

Conclusions: CD1d-restricted V alpha14 iNKT cells stimulate intrahepatic CD8 T-cell effector responses to antigen expressed in liver. Our findings elucidate a previously unknown intervention point for targeted immunotherapy to autoimmune and possibly infectious liver diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer
  • Animals
  • Antibodies
  • Antigens, CD1 / genetics
  • Antigens, CD1 / metabolism*
  • Antigens, CD1d
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / metabolism
  • Cell Proliferation
  • Cells, Cultured
  • Cytotoxicity, Immunologic
  • Galactosylceramides / metabolism
  • Hepatitis, Autoimmune / genetics
  • Hepatitis, Autoimmune / immunology*
  • Hepatitis, Autoimmune / metabolism
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Interferon-gamma / immunology
  • Interferon-gamma / metabolism
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / metabolism
  • Liver / immunology*
  • Liver / metabolism
  • Liver / pathology
  • Lymph Nodes / immunology
  • Lymphocyte Activation*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Receptors, Antigen, T-Cell / metabolism
  • Serpins / genetics
  • Serpins / metabolism*
  • Transferrin / genetics
  • Transferrin / metabolism
  • Tumor Necrosis Factor-alpha / immunology
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Antibodies
  • Antigens, CD1
  • Antigens, CD1d
  • Galactosylceramides
  • Homeodomain Proteins
  • Receptors, Antigen, T-Cell
  • SERPIN-B5
  • Serpins
  • Transferrin
  • Tumor Necrosis Factor-alpha
  • alpha-galactosylceramide
  • RAG-1 protein
  • Interferon-gamma