Listeria monocytogenes induces T cell receptor unresponsiveness through pore-forming toxin listeriolysin O

J Infect Dis. 2010 Dec 1;202(11):1698-707. doi: 10.1086/657145. Epub 2010 Oct 20.

Abstract

Background: The success of many pathogens relies on their ability to circumvent the innate and adaptive immune defenses. How bacterial pathogens subvert adaptive immune defenses is not clear. Cholesterol-dependent cytolysins (CDCs) represent an expansive family of homologous pore-forming toxins that are produced by more than 20 gram-positive bacterial species. Listeriolysin O (LLO), a prototype CDC, is the main virulence factor of Listeria monocytogenes.

Methods: We employed flow cytometric and microarray techniques to analyze the effect of LLO on T cell activation in vitro and in vivo.

Results: In vivo and in vitro proliferation of CD4(+) T cells upon T cell receptor (TCR) activation was highly diminished in the presence of LLO or wild-type L. monocytogenes but not in the presence of LLO-deficient L. monocytogenes. This block in T cell proliferation was specific to T cell activation via the TCR and not by phorbol 12-myristate 13-acetate-ionomycin, which bypasses the proximal TCR signaling event. The results of microarray analysis suggest that LLO-induced T cell unresponsiveness is due to the induction of a calcium-nuclear factor of activated T cells-dependent transcriptional program that drives the expression of negative regulators of TCR signaling.

Conclusion: These findings provide important insights into how bacterial toxins silence adaptive immune responses and thus enable prolonged survival of the pathogen in the host.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacterial Toxins / genetics
  • Bacterial Toxins / immunology*
  • CD4-Positive T-Lymphocytes
  • Disease Models, Animal
  • Flow Cytometry
  • Gene Expression
  • Heat-Shock Proteins / genetics
  • Heat-Shock Proteins / immunology*
  • Hemolysin Proteins / genetics
  • Hemolysin Proteins / immunology*
  • Listeria monocytogenes / immunology
  • Listeria monocytogenes / pathogenicity*
  • Mice
  • Mice, Inbred C57BL
  • Microarray Analysis
  • Receptors, Antigen, T-Cell / analysis*
  • Specific Pathogen-Free Organisms

Substances

  • Bacterial Toxins
  • Heat-Shock Proteins
  • Hemolysin Proteins
  • Receptors, Antigen, T-Cell
  • hlyA protein, Listeria monocytogenes