Pegylated IFN-α regulates hepatic gene expression through transient Jak/STAT activation

J Clin Invest. 2014 Apr;124(4):1568-81. doi: 10.1172/JCI70408. Epub 2014 Feb 24.

Abstract

The use of pegylated interferon-α (pegIFN-α) has replaced unmodified recombinant IFN-α for the treatment of chronic viral hepatitis. While the superior antiviral efficacy of pegIFN-α is generally attributed to improved pharmacokinetic properties, the pharmacodynamic effects of pegIFN-α in the liver have not been studied. Here, we analyzed pegIFN-α-induced signaling and gene regulation in paired liver biopsies obtained prior to treatment and during the first week following pegIFN-α injection in 18 patients with chronic hepatitis C. Despite sustained high concentrations of pegIFN-α in serum, the Jak/STAT pathway was activated in hepatocytes only on the first day after pegIFN-α administration. Evaluation of liver biopsies revealed that pegIFN-α induces hundreds of genes that can be classified into four clusters based on different temporal expression profiles. In all clusters, gene transcription was mainly driven by IFN-stimulated gene factor 3 (ISGF3). Compared with conventional IFN-α therapy, pegIFN-α induced a broader spectrum of gene expression, including many genes involved in cellular immunity. IFN-induced secondary transcription factors did not result in additional waves of gene expression. Our data indicate that the superior antiviral efficacy of pegIFN-α is not the result of prolonged Jak/STAT pathway activation in hepatocytes, but rather is due to induction of additional genes that are involved in cellular immune responses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Antiviral Agents / pharmacology
  • Endopeptidases / genetics
  • Endopeptidases / metabolism
  • Female
  • Gene Expression / drug effects
  • Hepatitis C, Chronic / drug therapy
  • Hepatitis C, Chronic / genetics
  • Hepatitis C, Chronic / metabolism
  • Humans
  • Immunity, Cellular / drug effects
  • Immunity, Cellular / genetics
  • Interferon alpha-2
  • Interferon-Stimulated Gene Factor 3, gamma Subunit / genetics
  • Interferon-Stimulated Gene Factor 3, gamma Subunit / metabolism
  • Interferon-alpha / pharmacology*
  • Janus Kinases / genetics
  • Janus Kinases / metabolism*
  • Kinetics
  • Liver / drug effects*
  • Liver / immunology
  • Liver / metabolism*
  • Male
  • Middle Aged
  • Polyethylene Glycols / pharmacology*
  • Recombinant Proteins / pharmacology
  • STAT Transcription Factors / genetics
  • STAT Transcription Factors / metabolism*
  • STAT1 Transcription Factor / genetics
  • STAT1 Transcription Factor / metabolism
  • Signal Transduction / drug effects
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling 3 Protein
  • Suppressor of Cytokine Signaling Proteins / genetics
  • Suppressor of Cytokine Signaling Proteins / metabolism
  • Ubiquitin Thiolesterase

Substances

  • Antiviral Agents
  • IRF9 protein, human
  • Interferon alpha-2
  • Interferon-Stimulated Gene Factor 3, gamma Subunit
  • Interferon-alpha
  • Recombinant Proteins
  • SOCS1 protein, human
  • SOCS3 protein, human
  • STAT Transcription Factors
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling 3 Protein
  • Suppressor of Cytokine Signaling Proteins
  • Polyethylene Glycols
  • Janus Kinases
  • Endopeptidases
  • USP18 protein, human
  • Ubiquitin Thiolesterase
  • peginterferon alfa-2b