IFN-α-Induced Downregulation of miR-221 in Dendritic Cells: Implications for HCV Pathogenesis and Treatment

J Interferon Cytokine Res. 2015 Sep;35(9):698-709. doi: 10.1089/jir.2014.0211. Epub 2015 Jun 19.

Abstract

Although interferon (IFN)-α is known to exert immunomodulatory and antiproliferative effects on dendritic cells (DCs) through induction of protein-coding IFN-stimulated genes (ISGs), little is known about IFN-α-regulated miRNAs in DCs. Since several miRNAs are involved in regulating DC functions, it is important to investigate whether IFN-α's effects on DCs are mediated through miRNAs as well. In this study, we examined miRNA expression patterns in myeloid DCs (mDCs) and plasmacytoid DCs after exposing them to IFN-α. We report that IFN-α downregulates miR-221 in both DC subsets via inhibition of STAT3. We validated proapoptotic proteins BCL2L11 and CDKN1C as miR-221 targets suggesting that IFN-α can induce DC apoptosis via miR-221 downregulation. In addition, we validated another miR-221 target, SOCS1, which is known to be a negative regulator of JAK/STAT signaling. Consistent with this, miR-221 overexpression in mDCs enhanced the secretion of proinflammatory cytokines IL-6 and TNF-α. In peripheral blood mononuclear cells (PBMCs) of HIV-1/HCV co-infected individuals undergoing IFN-α-based treatment the baseline miR-221 expression was lower in non-responders compared with responders; and miR-221 expression directly correlated with DC frequency and IL-6/TNF-α secretion. In addition to PBMCs, we isolated total liver cells and kupffer cells from HCV-infected individuals and individuals with alcoholic cirrhosis. We found that both total liver cells and kupffer cells from HCV-infected individuals had significantly higher miR-221 levels compared with individuals with cirrhosis. Overall, we demonstrate that IFN-α exerts both antiproliferative and immunomodulatory effects on mDCs via miR-221 downregulation; and IFN-miR-221 axis can play important role in HCV pathogenesis and treatment.

Publication types

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

MeSH terms

  • Apoptosis / physiology
  • Dendritic Cells / metabolism*
  • Dendritic Cells / virology*
  • Down-Regulation / genetics*
  • HIV Infections / genetics
  • HIV Infections / metabolism
  • HIV Infections / virology
  • HIV-1 / pathogenicity
  • Hepacivirus / pathogenicity*
  • Hepatitis C / genetics
  • Hepatitis C / metabolism
  • Hepatitis C / virology
  • Hepatocytes / metabolism
  • Hepatocytes / virology
  • Humans
  • Interferon-alpha / metabolism*
  • Interleukin-6 / metabolism
  • Janus Kinases / metabolism
  • Kupffer Cells / metabolism
  • Kupffer Cells / virology
  • Leukocytes, Mononuclear / metabolism
  • Leukocytes, Mononuclear / virology
  • Liver / metabolism
  • Liver / virology
  • Liver Cirrhosis, Alcoholic / genetics
  • Liver Cirrhosis, Alcoholic / metabolism
  • Liver Cirrhosis, Alcoholic / virology
  • MicroRNAs / genetics*
  • STAT3 Transcription Factor / metabolism
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling Proteins / metabolism
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Interferon-alpha
  • Interleukin-6
  • MIRN221 microRNA, human
  • MicroRNAs
  • SOCS1 protein, human
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling Proteins
  • Tumor Necrosis Factor-alpha
  • Janus Kinases