Adaptive immunity and enhanced CD8+ T cell response to Listeria monocytogenes in the absence of perforin and IFN-gamma

J Immunol. 2000 Jun 15;164(12):6444-52. doi: 10.4049/jimmunol.164.12.6444.

Abstract

Single Ag-specific CD8+ T cells from IFN-gamma-deficient (GKO) or perforin-deficient (PKO) mice provide substantial immunity against murine infection with Listeria monocytogenes. To address the potential for redundancy between perforin and IFN-gamma as CD8+ T cell effector mechanisms, we generated perforin/IFN-gamma (PKO/GKO) double-deficient mice. PKO/GKO-derived CD8+ T cells specific for the immunodominant listeriolysin O (LLO91-99) epitope provide immunity to LM infection similar to that provided by Ag-matched wild-type (WT) CD8+ T cells in the liver but reduced in the spleen. Strikingly, polyclonal CD8+ T cells from immunized PKO/GKO mice were approximately 100-fold more potent in reducing bacterial numbers than the same number of polyclonal CD8+ T cells from immunized WT mice. This result is probably quantitative, because the frequency of the CD8+ T cell response against the immunodominant LLO91-99 epitope is >4.5-fold higher in PKO/GKO mice than WT mice at 7 days after identical immunizations. Moreover, PKO/GKO mice can be immunized by a single infection with attenuated Listeria to resist >80,000-fold higher challenges with virulent organisms than naive PKO/GKO mice. These data demonstrate that neither perforin nor IFN-gamma is required for the development or expression of adaptive immunity to LM. In addition, the results suggest the potential for perforin and IFN-gamma to regulate the magnitude of the CD8+ T cell response to infection.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Bacterial Proteins / genetics
  • Bacterial Proteins / immunology
  • Bacterial Toxins*
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / metabolism
  • CD8-Positive T-Lymphocytes / transplantation
  • Cell Line
  • Cytotoxicity, Immunologic / genetics
  • Epitopes, T-Lymphocyte / immunology
  • Genetic Predisposition to Disease
  • Heat-Shock Proteins / immunology
  • Hemolysin Proteins
  • Immunity, Innate / genetics
  • Interferon-gamma / deficiency*
  • Interferon-gamma / genetics*
  • Listeria monocytogenes / genetics
  • Listeria monocytogenes / immunology
  • Listeria monocytogenes / pathogenicity
  • Listeriosis / genetics
  • Listeriosis / immunology*
  • Listeriosis / microbiology
  • Membrane Glycoproteins / deficiency*
  • Membrane Glycoproteins / genetics*
  • Membrane Proteins / genetics
  • Membrane Proteins / immunology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Knockout
  • Perforin
  • Pore Forming Cytotoxic Proteins
  • T-Lymphocyte Subsets / immunology
  • Tumor Necrosis Factor-alpha / biosynthesis
  • Virulence / immunology
  • fas Receptor / physiology

Substances

  • Bacterial Proteins
  • Bacterial Toxins
  • Epitopes, T-Lymphocyte
  • Heat-Shock Proteins
  • Hemolysin Proteins
  • Membrane Glycoproteins
  • Membrane Proteins
  • Pore Forming Cytotoxic Proteins
  • Tumor Necrosis Factor-alpha
  • fas Receptor
  • Perforin
  • actA protein, Listeria monocytogenes
  • Interferon-gamma
  • hlyA protein, Listeria monocytogenes