IFN-λ Inhibits MiR-122 Transcription through a Stat3-HNF4α Inflammatory Feedback Loop in an IFN-α Resistant HCV Cell Culture System

PLoS One. 2015 Dec 11;10(12):e0141655. doi: 10.1371/journal.pone.0141655. eCollection 2015.

Abstract

Background: HCV replication in persistently infected cell culture remains resistant to IFN-α/RBV combination treatment, whereas IFN-λ1 induces viral clearance. The antiviral mechanisms by which IFN-λ1 induces sustained HCV clearance have not been determined.

Aim: To investigate the mechanisms by which IFN-λ clears HCV replication in an HCV cell culture model.

Methods: IFN-α sensitive (S3-GFP) and resistant (R4-GFP) cells were treated with equivalent concentrations of either IFN-α or IFN-λ. The relative antiviral effects of IFN-α and IFN-λ1 were compared by measuring the HCV replication, quantification of HCV-GFP expression by flow cytometry, and viral RNA levels by real time RT-PCR. Activation of Jak-Stat signaling, interferon stimulated gene (ISG) expression, and miRNA-122 transcription in S3-GFP and R4-GFP cells were examined.

Results: We have shown that IFN-λ1 induces HCV clearance in IFN-α resistant and sensitive replicon cell lines in a dose dependent manner through Jak-Stat signaling, and induces STAT 1 and STAT 2 activation, ISRE-luciferase promoter activation and ISG expression. Stat 3 activation is also involved in IFN-λ1 induced antiviral activity in HCV cell culture. IFN-λ1 induced Stat 3 phosphorylation reduces the expression of hepatocyte nuclear factor 4 alpha (HNF4α) through miR-24 in R4-GFP cells. Reduced expression of HNF4α is associated with decreased expression of miR-122 resulting in an anti-HCV effect. Northern blot analysis confirms that IFN-λ1 reduces miR-122 levels in R4-GFP cells. Our results indicate that IFN-λ1 activates the Stat 3-HNF4α feedback inflammatory loop to inhibit miR-122 transcription in HCV cell culture.

Conclusions: In addition to the classical Jak-Stat antiviral signaling pathway, IFN-λ1 inhibits HCV replication through the suppression of miRNA-122 transcription via an inflammatory Stat 3-HNF4α feedback loop. Inflammatory feedback circuits activated by IFNs during chronic inflammation expose non-responders to the risk of hepatocellular carcinoma.

Publication types

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

MeSH terms

  • Antiviral Agents / pharmacology*
  • Cell Line, Tumor
  • Feedback, Physiological
  • Gene Expression Regulation
  • Hepacivirus / drug effects*
  • Hepacivirus / genetics
  • Hepacivirus / metabolism
  • Hepatocyte Nuclear Factor 4 / genetics*
  • Hepatocyte Nuclear Factor 4 / metabolism
  • Hepatocytes / drug effects
  • Hepatocytes / metabolism
  • Hepatocytes / virology
  • Host-Pathogen Interactions
  • Humans
  • Interferon-alpha / pharmacology
  • Interferons
  • Interleukins / pharmacology*
  • Janus Kinase 1 / genetics
  • Janus Kinase 1 / metabolism
  • MicroRNAs / antagonists & inhibitors*
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Phosphorylation
  • RNA, Viral / antagonists & inhibitors*
  • RNA, Viral / biosynthesis
  • Ribavirin / pharmacology
  • STAT2 Transcription Factor / genetics
  • STAT2 Transcription Factor / metabolism
  • STAT3 Transcription Factor / genetics*
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction
  • Virus Replication / drug effects

Substances

  • Antiviral Agents
  • HNF4A protein, human
  • Hepatocyte Nuclear Factor 4
  • interferon-lambda, human
  • Interferon-alpha
  • Interleukins
  • MIRN122 microRNA, human
  • MicroRNAs
  • RNA, Viral
  • STAT2 Transcription Factor
  • STAT2 protein, human
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Ribavirin
  • Interferons
  • Janus Kinase 1