Regulation of IRF-3-dependent innate immunity by the papain-like protease domain of the severe acute respiratory syndrome coronavirus

J Biol Chem. 2007 Nov 2;282(44):32208-21. doi: 10.1074/jbc.M704870200. Epub 2007 Aug 30.

Abstract

Severe acute respiratory syndrome coronavirus (SARS-CoV) is a novel coronavirus that causes a highly contagious respiratory disease, SARS, with significant mortality. Although factors contributing to the highly pathogenic nature of SARS-CoV remain poorly understood, it has been reported that SARS-CoV infection does not induce type I interferons (IFNs) in cell culture. However, it is uncertain whether SARS-CoV evades host detection or has evolved mechanisms to counteract innate host defenses. We show here that infection of SARS-CoV triggers a weak IFN response in cultured human lung/bronchial epithelial cells without inducing the phosphorylation of IFN-regulatory factor 3 (IRF-3), a latent cellular transcription factor that is pivotal for type I IFN synthesis. Furthermore, SARS-CoV infection blocked the induction of IFN antiviral activity and the up-regulation of protein expression of a subset of IFN-stimulated genes triggered by double-stranded RNA or an unrelated paramyxovirus. In searching for a SARS-CoV protein capable of counteracting innate immunity, we identified the papain-like protease (PLpro) domain as a potent IFN antagonist. The inhibition of the IFN response does not require the protease activity of PLpro. Rather, PLpro interacts with IRF-3 and inhibits the phosphorylation and nuclear translocation of IRF-3, thereby disrupting the activation of type I IFN responses through either Toll-like receptor 3 or retinoic acid-inducible gene I/melanoma differentiation-associated gene 5 pathways. Our data suggest that regulation of IRF-3-dependent innate antiviral defenses by PLpro may contribute to the establishment of SARS-CoV infection.

Publication types

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

MeSH terms

  • Animals
  • Bronchi / cytology
  • Bronchi / immunology
  • Bronchi / virology
  • Cell Line
  • Humans
  • Immunity, Innate*
  • Interferon Regulatory Factor-3 / immunology*
  • Interferon Type I / immunology
  • Peptide Hydrolases / chemistry
  • Peptide Hydrolases / immunology*
  • Protein Structure, Tertiary
  • Severe Acute Respiratory Syndrome / immunology*
  • Severe Acute Respiratory Syndrome / virology
  • Severe acute respiratory syndrome-related coronavirus / enzymology*
  • Severe acute respiratory syndrome-related coronavirus / immunology*
  • Viral Proteins / chemistry
  • Viral Proteins / immunology*

Substances

  • Interferon Regulatory Factor-3
  • Interferon Type I
  • Viral Proteins
  • Peptide Hydrolases