MicroRNA-18a enhances the interleukin-6-mediated production of the acute-phase proteins fibrinogen and haptoglobin in human hepatocytes

J Biol Chem. 2011 Nov 18;286(46):40142-50. doi: 10.1074/jbc.M111.251793. Epub 2011 Sep 27.

Abstract

The acute-phase response is an inflammatory process triggered mainly by the cytokine IL-6. Signaling of IL-6 is transduced by activation of STAT3 (signal transducer and activator of transcription 3), which rapidly induces the production of acute-phase proteins such as haptoglobin and fibrinogen. Another target of the IL-6/STAT3 signal transduction pathway is the microRNA cluster miR-17/92. Here, we investigated the interplay of miR-17/92 and STAT3 signaling and its impact on the acute-phase response in primary human hepatocytes and hepatoma (HepG2) cells. Employing a reporter gene system consisting of STAT3-sensitive promoter sequences, we show that the miR-17/92 cluster member miR-18a enhanced the transcriptional activity of STAT3. IL-6 stimulation experiments in miR-18a-overexpressing hepatocytes and HepG2 cells revealed an augmented acute-phase response indicated by increased expression and secretion of haptoglobin and fibrinogen. This effect was due, at least in part, to repression of PIAS3 (protein inhibitor of activated STAT, 3), a repressor of STAT3 activity, which we identified as a novel direct target of miR-18a. Finally, we demonstrate that the expression of miR-17/92 in primary hepatocytes and HepG2 cells is modulated by IL-6. Our data reveal, for the first time, a microRNA-mediated positive feedback loop of IL-6 signal transduction leading to an enhanced acute-phase response in human hepatocytes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Fibrinogen / biosynthesis*
  • Haptoglobins / biosynthesis*
  • Hep G2 Cells
  • Hepatocytes / metabolism*
  • Humans
  • Interleukin-6 / metabolism*
  • Interleukin-6 / pharmacology
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Molecular Chaperones / genetics
  • Molecular Chaperones / metabolism
  • Protein Inhibitors of Activated STAT / genetics
  • Protein Inhibitors of Activated STAT / metabolism
  • STAT3 Transcription Factor / genetics
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • Transcription, Genetic / drug effects
  • Transcription, Genetic / physiology

Substances

  • HP protein, human
  • Haptoglobins
  • IL6 protein, human
  • Interleukin-6
  • MIRN18A microRNA, human
  • MicroRNAs
  • Molecular Chaperones
  • PIAS3 protein, human
  • Protein Inhibitors of Activated STAT
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Fibrinogen