IL-29 is the dominant type III interferon produced by hepatocytes during acute hepatitis C virus infection

Hepatology. 2012 Dec;56(6):2060-70. doi: 10.1002/hep.25897. Epub 2012 Nov 19.

Abstract

Early, vigorous intrahepatic induction of interferon (IFN)-stimulated gene (ISG) induction is a feature of hepatitis C virus (HCV) infection, even though HCV inhibits the induction of type I IFNs in vitro. To identify the cytokines and cells that drive ISG induction and mediate antiviral activity during acute HCV infection, type I and III IFN responses were studied in (1) serial liver biopsies and plasma samples obtained from 6 chimpanzees throughout acute HCV infection and (2) primary human hepatocyte (PHH) cultures upon HCV infection. Type I IFNs were minimally induced at the messenger RNA (mRNA) level in the liver and were undetectable at the protein level in plasma during acute HCV infection of chimpanzees. In contrast, type III IFNs, in particular, interleukin (IL)-29 mRNA and protein, were strongly induced and these levels correlated with ISG expression and viremia. However, there was no association between intrahepatic or peripheral type III IFN levels and the outcome of acute HCV infection. Infection of PHH with HCV recapitulated strong type III and weak type I IFN responses. Supernatants from HCV-infected PHH cultures mediated antiviral activity upon transfer to HCV-replicon-containing cells. This effect was significantly reduced by neutralization of type III IFNs and less by neutralization of type I IFNs. Furthermore, IL-29 production by HCV-infected PHH occurred independently from type I IFN signaling and was not enhanced by the presence of plasmacytoid dendritic cells.

Conclusion: Hepatocyte-derived type III IFNs contribute to ISG induction and antiviral activity, but are not the principal determinant of the outcome of HCV infection.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • Ape Diseases / immunology*
  • Ape Diseases / metabolism
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cells, Cultured
  • Chemokine CXCL10 / genetics
  • Chemokine CXCL10 / metabolism
  • Chemokine CXCL11 / genetics
  • Chemokine CXCL11 / metabolism
  • Coculture Techniques
  • Dendritic Cells
  • GTP-Binding Proteins / genetics
  • GTP-Binding Proteins / metabolism
  • Gene Expression Regulation / immunology*
  • Hepacivirus / physiology
  • Hepatitis C / immunology*
  • Hepatitis C / metabolism
  • Hepatitis C / veterinary*
  • Hepatocytes / immunology*
  • Hepatocytes / metabolism
  • Humans
  • Interferon-alpha / genetics
  • Interferon-alpha / metabolism
  • Interferon-beta / genetics
  • Interferon-beta / metabolism
  • Interferons
  • Interleukins / genetics
  • Interleukins / metabolism*
  • Myxovirus Resistance Proteins
  • Pan troglodytes
  • Polymorphism, Single Nucleotide
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins
  • Viremia / virology
  • Virus Replication

Substances

  • Adaptor Proteins, Signal Transducing
  • Carrier Proteins
  • Chemokine CXCL10
  • Chemokine CXCL11
  • IFIT1 protein, human
  • interferon-lambda, human
  • Interferon-alpha
  • Interleukins
  • Myxovirus Resistance Proteins
  • RNA, Messenger
  • RNA-Binding Proteins
  • Interferon-beta
  • Interferons
  • GTP-Binding Proteins