Nonredundant roles for CD1d-restricted natural killer T cells and conventional CD4+ T cells in the induction of immunoglobulin E antibodies in response to interleukin 18 treatment of mice

J Exp Med. 2003 Apr 21;197(8):997-1005. doi: 10.1084/jem.20021701. Epub 2003 Apr 14.

Abstract

Interleukin (IL)-18 synergizes with IL-12 to promote T helper cell (Th)1 responses. Somewhat paradoxically, IL-18 administration alone strongly induces immunoglobulin (Ig)E production and allergic inflammation, indicating a role for IL-18 in the generation of Th2 responses. The ability of IL-18 to induce IgE is dependent on CD4+ T cells, IL-4, and signal transducer and activator of transcription (stat)6. Here, we show that IL-18 fails to induce IgE both in CD1d-/- mice that lack natural killer T (NKT) cells and in class II-/- mice that lack conventional CD4+ T cells. However, class II-/- mice reconstituted with conventional CD4+ T cells show the capacity to produce IgE in response to IL-18. NKT cells express high levels of IL-18 receptor (R)alpha chain and produce significant amounts of IL-4, IL-9, and IL-13, and induce CD40 ligand expression in response to IL-2 and IL-18 stimulation in vitro. In contrast, conventional CD4+ T cells express low levels of IL-18Ralpha and poorly respond to IL-2 and IL-18. Nevertheless, conventional CD4+ T cells are essential for B cell IgE responses after the administration of IL-18. These findings indicate that NKT cells might be the major source of IL-4 in response to IL-18 administration and that conventional CD4+ T cells demonstrate their helper function in the presence of NKT cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, CD1 / genetics
  • Antigens, CD1 / metabolism*
  • Antigens, CD1d
  • B-Lymphocytes / cytology
  • B-Lymphocytes / immunology
  • B-Lymphocytes / metabolism
  • CD4-Positive T-Lymphocytes / cytology
  • CD4-Positive T-Lymphocytes / immunology*
  • CD4-Positive T-Lymphocytes / metabolism
  • CD40 Ligand / metabolism
  • Cells, Cultured
  • Female
  • Immunoglobulin E / biosynthesis*
  • Immunoglobulin E / immunology*
  • Interleukin-13 / metabolism
  • Interleukin-18 / immunology*
  • Interleukin-18 / metabolism
  • Interleukin-18 Receptor alpha Subunit
  • Interleukin-2 / metabolism
  • Interleukin-4 / metabolism
  • Interleukin-9 / metabolism
  • Killer Cells, Natural / cytology
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / metabolism
  • Lymphocyte Activation
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Receptors, Interleukin / genetics
  • Receptors, Interleukin / metabolism
  • Receptors, Interleukin-18
  • Th2 Cells / immunology
  • Th2 Cells / metabolism

Substances

  • Antigens, CD1
  • Antigens, CD1d
  • Il18r1 protein, mouse
  • Interleukin-13
  • Interleukin-18
  • Interleukin-18 Receptor alpha Subunit
  • Interleukin-2
  • Interleukin-9
  • Receptors, Interleukin
  • Receptors, Interleukin-18
  • CD40 Ligand
  • Interleukin-4
  • Immunoglobulin E