Encephalomyocarditis virus disrupts stress granules, the critical platform for triggering antiviral innate immune responses

J Virol. 2013 Sep;87(17):9511-22. doi: 10.1128/JVI.03248-12. Epub 2013 Jun 19.

Abstract

In response to stress, cells induce ribonucleoprotein aggregates, termed stress granules (SGs). SGs are transient loci containing translation-stalled mRNA, which is eventually degraded or recycled for translation. Infection of some viruses, including influenza A virus with a deletion of nonstructural protein 1 (IAVΔNS1), induces SG-like protein aggregates. Previously, we showed that IAVΔNS1-induced SGs are required for efficient induction of type I interferon (IFN). Here, we investigated SG formation by different viruses using green fluorescent protein (GFP)-tagged Ras-Gap SH3 domain binding protein 1 (GFP-G3BP1) as an SG probe. HeLa cells stably expressing GFP-G3BP1 were infected with different viruses, and GFP fluorescence was monitored live with time-lapse microscopy. SG formations by different viruses was classified into 4 different patterns: no SG formation, stable SG formation, transient SG formation, and alternate SG formation. We focused on encephalomyocarditis virus (EMCV) infection, which exhibited transient SG formation. We found that EMCV disrupts SGs by cleavage of G3BP1 at late stages of infection (>8 h) through a mechanism similar to that used by poliovirus. Expression of a G3BP1 mutant that is resistant to the cleavage conferred persistent formation of SGs as well as an enhanced induction of IFN and other cytokines at late stages of infection. Additionally, knockdown of endogenous G3BP1 blocked SG formation with an attenuated induction of IFN and potentiated viral replication. Taken together, our findings suggest a critical role of SGs as an antiviral platform and shed light on one of the mechanisms by which a virus interferes with host stress and subsequent antiviral responses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Carrier Proteins / antagonists & inhibitors
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cytokines / genetics
  • DNA Helicases
  • DNA Viruses / pathogenicity
  • Encephalomyocarditis virus / immunology*
  • Encephalomyocarditis virus / pathogenicity*
  • Encephalomyocarditis virus / physiology
  • Gene Expression
  • Gene Knockdown Techniques
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • HeLa Cells
  • Host-Pathogen Interactions / genetics
  • Host-Pathogen Interactions / immunology
  • Humans
  • Immunity, Innate / genetics
  • Interferons / genetics
  • Mutation
  • Poly-ADP-Ribose Binding Proteins
  • RNA Helicases
  • RNA Recognition Motif Proteins
  • RNA Viruses / pathogenicity
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Ribonucleoproteins / immunology
  • Ribonucleoproteins / metabolism*
  • Stress, Physiological
  • Virus Replication

Substances

  • Carrier Proteins
  • Cytokines
  • Poly-ADP-Ribose Binding Proteins
  • RNA Recognition Motif Proteins
  • Recombinant Fusion Proteins
  • Ribonucleoproteins
  • Green Fluorescent Proteins
  • Interferons
  • DNA Helicases
  • G3BP1 protein, human
  • RNA Helicases