IL-21-induced Bepsilon cell apoptosis mediated by natural killer T cells suppresses IgE responses

J Exp Med. 2006 Dec 25;203(13):2929-37. doi: 10.1084/jem.20062206. Epub 2006 Dec 18.

Abstract

Epidemiological studies have suggested that the recent increase in the incidence and severity of immunoglobulin (Ig)E-mediated allergic disorders is inversely correlated with Mycobacterium bovis bacillus Calmette Guerin (BCG) vaccination; however, the underlying mechanisms remain uncertain. Here, we demonstrate that natural killer T (NKT) cells in mice and humans play a crucial role in the BCG-induced suppression of IgE responses. BCG-activated murine Valpha14 NKT cells, but not conventional CD4 T cells, selectively express high levels of interleukin (IL)-21, which preferentially induces apoptosis in Bepsilon cells. Signaling from the IL-21 receptor increases the formation of a complex between Bcl-2 and the proapoptotic molecule Bcl-2-modifying factor, resulting in Bepsilon cell apoptosis. Similarly, BCG vaccination induces IL-21 expression by human peripheral blood mononuclear cells (PBMCs) in a partially NKT cell-dependent fashion. BCG-activated PBMCs significantly reduce IgE production by human B cells. These findings provide new insight into the therapeutic effect of BCG in allergic diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Antibodies, Monoclonal / pharmacology
  • Antibody Formation / immunology
  • Antigens, CD1 / immunology
  • Antigens, CD1d
  • Apoptosis / immunology*
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / metabolism
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism
  • Female
  • Gene Expression
  • Humans
  • Immunoglobulin E / blood
  • Immunoglobulin E / immunology*
  • Interleukin-12 / genetics
  • Interleukin-12 / metabolism
  • Interleukin-12 / pharmacology
  • Interleukin-21
  • Interleukins / physiology*
  • Killer Cells, Natural / drug effects
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / metabolism
  • Liver / immunology
  • Liver / metabolism
  • Mice
  • Mice, Inbred BALB C
  • Mice, Knockout
  • Monocytes, Activated Killer / immunology
  • Mycobacterium bovis / immunology
  • Ovalbumin / immunology
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Receptors, Antigen, T-Cell, alpha-beta / genetics
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Antibodies, Monoclonal
  • Antigens, CD1
  • Antigens, CD1d
  • Bmf protein, mouse
  • CD1D protein, human
  • Interleukins
  • Proto-Oncogene Proteins c-bcl-2
  • Receptors, Antigen, T-Cell, alpha-beta
  • Interleukin-12
  • Immunoglobulin E
  • Ovalbumin
  • Interleukin-21