Interferon-gamma inhibits interferon-alpha signalling in hepatic cells: evidence for the involvement of STAT1 induction and hyperexpression of STAT1 in chronic hepatitis C

Biochem J. 2004 Apr 1;379(Pt 1):199-208. doi: 10.1042/BJ20031495.

Abstract

IFN-gamma (interferon-gamma) modulates IFN-alpha therapy in chronic hepatitis C infection; however, the underlying mechanism remains unclear. Here we demonstrate that long-term (3-6 days) but not short-term (up to 1 day) IFN-gamma treatment of human hepatoma Hep3B cells attenuates IFN-alpha activation of STAT1 (signal transducers and activators of transcription factor 1), STAT2 and STAT3, but enhances IFN-gamma and interleukin 6 activation of STATs. Prolonged exposure to IFN-gamma also significantly induces STAT1 protein expression without affecting STAT2, STAT3 and ERK (extracellular-signal-regulated kinase) 1/2 protein expression. To determine the role of STAT1 protein overexpression in regulation of IFN-alpha signalling, Hep3B cells were stably transfected with wild-type STAT1. Overexpression of STAT1 via stable transfection enhances IFN-gamma activation of STAT1, but surprisingly attenuates IFN-alpha activation of STAT1, STAT2 and STAT3 without affecting Janus kinase activation. This STAT1-mediated inhibition does not require STAT1 tyrosine phosphorylation because overexpression of dominant-negative STAT1 with a mutation on tyrosine residue 701 also blocks IFN-alpha activation of STAT1, STAT2 and STAT3. Moreover, overexpression of STAT1 blocks IFN-alpha-activated STAT2 translocation from IFN-alpha receptor 2 to IFN-alpha receptor 1, a critical step in IFN-alpha signalling activation. Finally, significantly higher levels of STAT1 protein expression, which is probably induced by IFN-gamma, are detected in the majority of hepatitis C virus-infected livers compared with healthy controls. In conclusion, long-term IFN-gamma treatment inhibits IFN-alpha-activated signals most probably, at least in part, through the induction of STAT1 protein expression, which could partly contribute to IFN-alpha treatment failure in hepatitis C patients.

MeSH terms

  • Antiviral Agents / pharmacology*
  • Carcinoma, Hepatocellular / pathology
  • Carrier Proteins / biosynthesis
  • Carrier Proteins / genetics
  • Cell Cycle
  • Cell Line, Tumor / drug effects
  • Cell Line, Tumor / metabolism
  • DNA-Binding Proteins / biosynthesis
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • DNA-Binding Proteins / physiology*
  • Enzyme Activation / drug effects
  • Gene Expression Regulation / drug effects*
  • Genes, Reporter
  • Hepatitis C, Chronic / drug therapy*
  • Hepatitis C, Chronic / metabolism
  • Humans
  • Interferon-alpha / antagonists & inhibitors*
  • Interferon-alpha / physiology
  • Interferon-gamma / pharmacology*
  • Interleukin-6 / metabolism
  • Intracellular Signaling Peptides and Proteins*
  • Janus Kinase 1
  • Liver / drug effects
  • Liver / metabolism*
  • Liver Cirrhosis / metabolism
  • Liver Neoplasms / pathology
  • Membrane Proteins
  • Protein-Tyrosine Kinases / metabolism
  • RNA, Messenger / biosynthesis
  • Receptor, Interferon alpha-beta
  • Receptors, Interferon / metabolism
  • Recombinant Fusion Proteins / physiology
  • Repressor Proteins / biosynthesis
  • Repressor Proteins / genetics
  • STAT1 Transcription Factor
  • STAT2 Transcription Factor
  • STAT3 Transcription Factor
  • Signal Transduction
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling Proteins
  • TYK2 Kinase
  • Trans-Activators / biosynthesis
  • Trans-Activators / genetics
  • Trans-Activators / metabolism
  • Trans-Activators / physiology*
  • Transfection

Substances

  • Antiviral Agents
  • Carrier Proteins
  • DNA-Binding Proteins
  • Interferon-alpha
  • Interleukin-6
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • RNA, Messenger
  • Receptors, Interferon
  • Recombinant Fusion Proteins
  • Repressor Proteins
  • SOCS1 protein, human
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • STAT2 Transcription Factor
  • STAT2 protein, human
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling Proteins
  • Trans-Activators
  • Receptor, Interferon alpha-beta
  • Interferon-gamma
  • Protein-Tyrosine Kinases
  • JAK1 protein, human
  • Janus Kinase 1
  • TYK2 Kinase
  • TYK2 protein, human