RNA viruses promote activation of the NLRP3 inflammasome through cytopathogenic effect-induced potassium efflux

Cell Death Dis. 2019 Apr 25;10(5):346. doi: 10.1038/s41419-019-1579-0.

Abstract

Early detection of viruses by the innate immune system is crucial for host defense. The NLRP3 inflammasome, through activation of caspase-1, promotes the maturation of IL-1β and IL-18, which are critical for antiviral immunity and inflammatory response. However, the mechanism by which viruses activate this inflammasome is still debated. Here, we report that the replication of cytopathogenic RNA viruses such as vesicular stomatitis virus (VSV) or encephalomyocarditis virus (EMCV) induced a lytic cell death leading to potassium efflux, the common trigger of NLRP3 inflammasome activation. This lytic cell death was not prevented by a chemical or genetic inhibition of apoptosis, pyroptosis, or necroptosis but required the viral replication. Hence, the viruses that stimulated type I IFNs production after their sensing did not activate NLRP3 inflammasome due to an inhibition of their replication. In contrast, NLRP3 inflammasome activation induced by RNA virus infection was stimulated in IFNAR-deficient or MAVS-deficient cells consequently to an increased viral replication and ensuing lytic cell death. Therefore, in a context of inefficient IFN response, viral replication-induced lytic cell death activates of the NLRP3 inflammasome to fight against infection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / deficiency
  • Adaptor Proteins, Signal Transducing / genetics
  • Animals
  • Bone Marrow Cells / cytology
  • Dynamins / antagonists & inhibitors
  • Dynamins / genetics
  • Dynamins / metabolism
  • Encephalomyocarditis virus / physiology*
  • Humans
  • Inflammasomes / metabolism
  • Interleukin-1beta / analysis
  • Interleukin-1beta / metabolism
  • Lipopolysaccharides / pharmacology
  • Macrophages / cytology
  • Macrophages / metabolism
  • Macrophages / virology
  • Mice
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism*
  • Necroptosis
  • Potassium / metabolism*
  • RNA Interference
  • RNA, Small Interfering / metabolism
  • Receptor, Interferon alpha-beta / deficiency
  • Receptor, Interferon alpha-beta / genetics
  • Vesiculovirus / physiology*
  • Virus Replication

Substances

  • Adaptor Proteins, Signal Transducing
  • IPS-1 protein, mouse
  • Ifnar2 protein, mouse
  • Inflammasomes
  • Interleukin-1beta
  • Lipopolysaccharides
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • RNA, Small Interfering
  • Receptor, Interferon alpha-beta
  • Dnm1l protein, mouse
  • Dynamins
  • Potassium