Inhibition of dsRNA-induced signaling in hepatitis C virus-infected cells by NS3 protease-dependent and -independent mechanisms

Proc Natl Acad Sci U S A. 2006 May 30;103(22):8499-504. doi: 10.1073/pnas.0602957103. Epub 2006 May 17.

Abstract

The recent establishment of a robust hepatitis C virus (HCV) cell culture system permits analysis of virus-host interactions during HCV infection. Here, we report that HCV genotype 2a (JFH-1) infection fails to induce IFN-beta or IFN-stimulated gene expression in Huh-7 cells, and that it blocks IFN-beta and IFN-stimulated gene production after transfection of synthetic dsRNA. Overexpression of individual components of the dsRNA-signaling pathway in HCV-infected and uninfected cells indicates that HCV inhibits IFN-beta promoter activity by inactivating the mitochondrial antiviral signaling protein/IFN-beta promoter stimulator 1 (MAVS/IPS-1), while leaving the IFN-induced Janus kinases-signal transducers and activators of transcription (JAK-STAT) signaling pathway intact. We also show that MAVS/IPS-1-dependent IFN-beta promoter activity in HCV-infected cells is fully restored by the nonstructural protein 3 (NS3) protease inhibitor BILN2061. In contrast, synthetic dsRNA-induced IFN-beta promoter activity is not restored by BILN2061, although it is partially restored by overexpression of RIG-I. These results support recently reported evidence that the HCV NS3 protease blunts the ability of HCV to induce IFN-beta promoter activity by proteolytically cleaving MAVS/IPS-1. The results also suggest that HCV blocks the synthetic dsRNA-induced signaling pathway at a point upstream of MAVS/IPS-1, and that it does so by an NS3-independent mechanism.

Publication types

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

MeSH terms

  • Active Transport, Cell Nucleus
  • Carbamates / pharmacology
  • Cell Line, Tumor
  • Gene Expression Regulation, Viral
  • Hepacivirus / genetics*
  • Hepacivirus / physiology*
  • Humans
  • I-kappa B Kinase / genetics
  • I-kappa B Kinase / metabolism
  • Interferon Regulatory Factor-3 / metabolism
  • Interferon-Stimulated Gene Factor 3 / genetics
  • Interferon-Stimulated Gene Factor 3 / metabolism
  • Interferon-beta / biosynthesis
  • Macrocyclic Compounds / pharmacology
  • Promoter Regions, Genetic / genetics
  • Protease Inhibitors / pharmacology
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Protein-Tyrosine Kinases / metabolism
  • Quinolines / pharmacology
  • RNA, Double-Stranded / immunology*
  • RNA, Double-Stranded / physiology
  • Response Elements / genetics
  • Signal Transduction*
  • Thiazoles / pharmacology
  • Viral Nonstructural Proteins / antagonists & inhibitors
  • Viral Nonstructural Proteins / genetics
  • Viral Nonstructural Proteins / metabolism*

Substances

  • BILN 2061
  • Carbamates
  • Interferon Regulatory Factor-3
  • Interferon-Stimulated Gene Factor 3
  • Macrocyclic Compounds
  • NS3 protein, hepatitis C virus
  • Protease Inhibitors
  • Quinolines
  • RNA, Double-Stranded
  • Thiazoles
  • Viral Nonstructural Proteins
  • Interferon-beta
  • Protein-Tyrosine Kinases
  • Protein Serine-Threonine Kinases
  • TBK1 protein, human
  • I-kappa B Kinase