Guanylate binding proteins promote caspase-11-dependent pyroptosis in response to cytoplasmic LPS

Proc Natl Acad Sci U S A. 2014 Apr 22;111(16):6046-51. doi: 10.1073/pnas.1321700111. Epub 2014 Apr 8.

Abstract

IFN receptor signaling induces cell-autonomous immunity to infections with intracellular bacterial pathogens. Here, we demonstrate that IFN-inducible guanylate binding protein (Gbp) proteins stimulate caspase-11-dependent, cell-autonomous immunity in response to cytoplasmic LPS. Caspase-11-dependent pyroptosis is triggered in IFN-activated macrophages infected with the Gram-negative bacterial pathogen Legionella pneumophila. The rapid induction of pyroptosis in IFN-activated macrophages required a cluster of IFN-inducible Gbp proteins encoded on mouse chromosome 3 (Gbp(chr3)). Induction of pyroptosis in naive macrophages by infections with the cytosol-invading ΔsdhA L. pneumophila mutant was similarly dependent on Gbp(chr3), suggesting that these Gbp proteins play a role in the detection of bacteria accessing the cytosol. Cytoplasmic LPS derived from Salmonella ssp. or Escherichia coli has recently been shown to trigger caspase-11 activation and pyroptosis, but the cytoplasmic sensor for LPS and components of the caspase-11 inflammasome are not yet defined. We found that the induction of caspase-11-dependent pyroptosis by cytoplasmic L. pneumophila-derived LPS required Gbp(chr3) proteins. Similarly, pyroptosis induced by cytoplasmic LPS isolated from Salmonella was diminished in Gbp(chr3)-deficient macrophages. These data suggest a role for Gbp(chr3) proteins in the detection of cytoplasmic LPS and the activation of the noncanonical inflammasome.

Keywords: Nos2; cell death; immunity-related GTPases; interferon.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects*
  • Caspases / metabolism*
  • Caspases, Initiator
  • Cytoplasm / drug effects
  • Cytoplasm / metabolism*
  • Enzyme Activation / drug effects
  • GTP-Binding Proteins / metabolism*
  • Interferon-gamma / pharmacology
  • Legionella pneumophila / drug effects
  • Legionella pneumophila / growth & development
  • Legionella pneumophila / physiology
  • Legionnaires' Disease / microbiology
  • Legionnaires' Disease / pathology
  • Lipopolysaccharides / pharmacology*
  • Macrophage Activation / drug effects
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Macrophages / microbiology
  • Membrane Glycoproteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mutation / genetics
  • NADPH Oxidase 2
  • NADPH Oxidases / metabolism
  • Nitric Oxide Synthase Type II / metabolism
  • Salmonella typhimurium / drug effects
  • Salmonella typhimurium / physiology

Substances

  • Ifi1 protein, mouse
  • Lipopolysaccharides
  • Membrane Glycoproteins
  • Interferon-gamma
  • Nitric Oxide Synthase Type II
  • Nos2 protein, mouse
  • Cybb protein, mouse
  • NADPH Oxidase 2
  • NADPH Oxidases
  • Casp4 protein, mouse
  • Caspases
  • Caspases, Initiator
  • GTP-Binding Proteins