Hepatitis C virus NS3/4A protease inhibits complement activation by cleaving complement component 4

PLoS One. 2013 Dec 12;8(12):e82094. doi: 10.1371/journal.pone.0082094. eCollection 2013.

Abstract

Background: It has been hypothesized that persistent hepatitis C virus (HCV) infection is mediated in part by viral proteins that abrogate the host immune response, including the complement system, but the precise mechanisms are not well understood. We investigated whether HCV proteins are involved in the fragmentation of complement component 4 (C4), composed of subunits C4α, C4β, and C4γ, and the role of HCV proteins in complement activation.

Methods: Human C4 was incubated with HCV nonstructural (NS) 3/4A protease, core, or NS5. Samples were separated by sodium dodecyl sulfate-polyacrylamide gel electrophoresis and then subjected to peptide sequencing. The activity of the classical complement pathway was examined using an erythrocyte hemolysis assay. The cleavage pattern of C4 in NS3/4A-expressing and HCV-infected cells, respectively, was also examined.

Results: HCV NS3/4A protease cleaved C4γ in a concentration-dependent manner, but viral core and NS5 did not. A specific inhibitor of NS3/4A protease reduced C4γ cleavage. NS3/4A protease-mediated cleavage of C4 inhibited classical pathway activation, which was abrogated by a NS3/4A protease inhibitor. In addition, co-transfection of cells with C4 and wild-type NS3/4A, but not a catalytic-site mutant of NS3/4A, produced cleaved C4γ fragments. Such C4 processing, with a concomitant reduction in levels of full-length C4γ, was also observed in HCV-infected cells expressing C4.

Conclusions: C4 is a novel cellular substrate of the HCV NS3/4A protease. Understanding disturbances in the complement system mediated by NS3/4A protease may provide new insights into the mechanisms underlying persistent HCV infection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Carrier Proteins / metabolism*
  • Cell Line, Tumor
  • Complement Activation* / drug effects
  • Complement C4 / chemistry
  • Complement C4 / metabolism*
  • Hemolysis / drug effects
  • Hepatitis C / virology
  • Humans
  • Intracellular Signaling Peptides and Proteins
  • Molecular Sequence Data
  • Oligopeptides / pharmacology
  • Protease Inhibitors / pharmacology
  • Sheep
  • Viral Nonstructural Proteins / metabolism*

Substances

  • Carrier Proteins
  • Complement C4
  • Intracellular Signaling Peptides and Proteins
  • NS3 protein, hepatitis C virus
  • NS4A cofactor peptide, Hepatitis C virus
  • Oligopeptides
  • Protease Inhibitors
  • Viral Nonstructural Proteins
  • telaprevir

Grants and funding

This study was supported by a Grant-in-Aid for Research on Hepatitis and BSE from the Ministry of Health, Labour and Welfare of Japan; a grant for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan; and a grant from the Miyazaki Prefecture Collaboration of Regional Entities for the Advancement of Technological Excellence. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.