Specific T cells restore the autophagic flux inhibited by Mycobacterium tuberculosis in human primary macrophages

J Infect Dis. 2012 May 1;205(9):1425-35. doi: 10.1093/infdis/jis226. Epub 2012 Mar 29.

Abstract

Background: Autophagy inhibits survival of intracellular Mycobacterium tuberculosis when induced by rapamycin or interferon γ (IFN-γ), but it remains unclear whether M. tuberculosis itself can induce autophagy and whether T cells play a role in M. tuberculosis-mediated autophagy. The aim of this study was to evaluate the impact of M. tuberculosis on autophagy in human primary macrophages and the role of specific T cells in this process.

Methods: M. tuberculosis (H37Rv)-infected macrophages were incubated with naive or M. tuberculosis-specific T cells. Autophagy was evaluated at 4 hours and 8 hours after infection by analyzing the levels of LC3-II (a hallmark of autophagy) and p62 (a protein degraded by autophagy). M. tuberculosis survival was evaluated by counting the colony-forming units.

Results: M. tuberculosis infection of macrophages inhibited the autophagic process at 8 hours after infection. Naive T cells could not rescue this block, whereas M. tuberculosis-specific T cells restored autophagy degradation, accompanied by enhanced bacterial killing. Notably, the effect of M. tuberculosis-specific T cells was not affected by neutralization of endogenous IFN-γ and tumor necrosis factor α and was blocked by preventing contact between macrophages and T cells, suggesting that cell-cell interaction is crucial.

Conclusions: M. tuberculosis inhibits autophagy in human primary macrophages, and specific T cells can restore functional autophagic flux through cell-cell contact.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism
  • Autophagy / immunology*
  • Blotting, Western
  • Cell Communication
  • Humans
  • Interferon-gamma / antagonists & inhibitors
  • Interferon-gamma / metabolism
  • Macrophages / immunology
  • Macrophages / microbiology*
  • Microscopy, Confocal
  • Mycobacterium tuberculosis / immunology*
  • Mycobacterium tuberculosis / pathogenicity
  • Phagosomes / metabolism
  • Real-Time Polymerase Chain Reaction
  • Sequestosome-1 Protein
  • Stem Cells / metabolism
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism
  • Tuberculosis / metabolism
  • Tuberculosis / pathology
  • Tumor Necrosis Factor-alpha / antagonists & inhibitors
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • SQSTM1 protein, human
  • Sequestosome-1 Protein
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma