Granzyme A produced by γ(9)δ(2) T cells induces human macrophages to inhibit growth of an intracellular pathogen

PLoS Pathog. 2013 Jan;9(1):e1003119. doi: 10.1371/journal.ppat.1003119. Epub 2013 Jan 10.

Abstract

Human γ(9)δ(2) T cells potently inhibit pathogenic microbes, including intracellular mycobacteria, but the key inhibitory mechanism(s) involved have not been identified. We report a novel mechanism involving the inhibition of intracellular mycobacteria by soluble granzyme A. γ(9)δ(2) T cells produced soluble factors that could pass through 0.45 µm membranes and inhibit intracellular mycobacteria in human monocytes cultured below transwell inserts. Neutralization of TNF-α in co-cultures of infected monocytes and γ(9)δ(2) T cells prevented inhibition, suggesting that TNF-α was the critical inhibitory factor produced by γ(9)δ(2) T cells. However, only siRNA- mediated knockdown of TNF-α in infected monocytes, but not in γ(9)δ(2) T cells, prevented mycobacterial growth inhibition. Investigations of other soluble factors produced by γ(9)δ(2) T cells identified a highly significant correlation between the levels of granzyme A produced and intracellular mycobacterial growth inhibition. Furthermore, purified granzyme A alone induced inhibition of intracellular mycobacteria, while knockdown of granzyme A in γ(9)δ(2) T cell clones blocked their inhibitory effects. The inhibitory mechanism was independent of autophagy, apoptosis, nitric oxide production, type I interferons, Fas/FasL and perforin. These results demonstrate a novel microbial defense mechanism involving granzyme A-mediated triggering of TNF-α production by monocytes leading to intracellular mycobacterial growth suppression. This pathway may provide a protective mechanism relevant for the development of new vaccines and/or immunotherapies for macrophage-resident chronic microbial infections.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Cells, Cultured
  • Gene Expression Regulation, Bacterial
  • Gene Knockdown Techniques
  • Granzymes / genetics
  • Granzymes / metabolism*
  • Granzymes / pharmacology
  • Host-Pathogen Interactions
  • Humans
  • Macrophages / enzymology*
  • Macrophages / immunology
  • Macrophages / microbiology
  • Monocytes / enzymology*
  • Monocytes / immunology
  • Monocytes / microbiology
  • Mycobacterium / drug effects
  • Mycobacterium / physiology*
  • Neutralization Tests
  • RNA, Small Interfering / genetics
  • Receptors, Antigen, T-Cell, gamma-delta / immunology
  • Receptors, Antigen, T-Cell, gamma-delta / metabolism
  • T-Lymphocyte Subsets / enzymology*
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / microbiology
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • RNA, Small Interfering
  • Receptors, Antigen, T-Cell, gamma-delta
  • Tumor Necrosis Factor-alpha
  • Granzymes