Prdx4 limits caspase-1 activation and restricts inflammasome-mediated signaling by extracellular vesicles

EMBO J. 2019 Oct 15;38(20):e101266. doi: 10.15252/embj.2018101266. Epub 2019 Sep 23.

Abstract

Inflammasomes are cytosolic protein complexes, which orchestrate the maturation of active IL-1β by proteolytic cleavage via caspase-1. Although many principles of inflammasome activation have been described, mechanisms that limit inflammasome-dependent immune responses remain poorly defined. Here, we show that the thiol-specific peroxidase peroxiredoxin-4 (Prdx4) directly regulates IL-1β generation by interfering with caspase-1 activity. We demonstrate that caspase-1 and Prdx4 form a redox-sensitive regulatory complex via caspase-1 cysteine 397 that leads to caspase-1 sequestration and inactivation. Mice lacking Prdx4 show an increased susceptibility to LPS-induced septic shock. This effect was phenocopied in mice carrying a conditional deletion of Prdx4 in the myeloid lineage (Prdx4-ΔLysMCre). Strikingly, we demonstrate that Prdx4 co-localizes with inflammasome components in extracellular vesicles (EVs) from inflammasome-activated macrophages. Purified EVs are able to transmit a robust IL-1β-dependent inflammatory response in vitro and also in recipient mice in vivo. Loss of Prdx4 boosts the pro-inflammatory potential of EVs. These findings identify Prdx4 as a critical regulator of inflammasome activity and provide new insights into remote cell-to-cell communication function of inflammasomes via macrophage-derived EVs.

Keywords: IL-1β; Prdx4; caspase-1; extracellular vesicle; inflammasome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caspase 1 / genetics
  • Caspase 1 / metabolism*
  • Cytokines / metabolism
  • Extracellular Vesicles / metabolism*
  • Female
  • Inflammasomes / immunology*
  • Inflammasomes / metabolism
  • Lipopolysaccharides / toxicity
  • Macrophages / immunology*
  • Macrophages / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Peroxiredoxins / physiology*
  • Shock, Septic / chemically induced
  • Shock, Septic / immunology
  • Shock, Septic / pathology
  • Shock, Septic / prevention & control*
  • Signal Transduction

Substances

  • Cytokines
  • Inflammasomes
  • Lipopolysaccharides
  • Peroxiredoxins
  • Prdx4 protein, mouse
  • Casp1 protein, mouse
  • Caspase 1