HCV-induced miR-21 contributes to evasion of host immune system by targeting MyD88 and IRAK1

PLoS Pathog. 2013;9(4):e1003248. doi: 10.1371/journal.ppat.1003248. Epub 2013 Apr 25.

Abstract

Upon recognition of viral components by pattern recognition receptors, such as the toll-like receptors (TLRs) and retinoic acid-inducible gene I (RIG-I)-like helicases, cells are activated to produce type I interferon (IFN) and proinflammatory cytokines. These pathways are tightly regulated by the host to prevent an inappropriate cellular response, but viruses can modulate these pathways to proliferate and spread. In this study, we revealed a novel mechanism in which hepatitis C virus (HCV) evades the immune surveillance system to proliferate by activating microRNA-21 (miR-21). We demonstrated that HCV infection upregulates miR-21, which in turn suppresses HCV-triggered type I IFN production, thus promoting HCV replication. Furthermore, we demonstrated that miR-21 targets two important factors in the TLR signaling pathway, myeloid differentiation factor 88 (MyD88) and interleukin-1 receptor-associated kinase 1 (IRAK1), which are involved in HCV-induced type I IFN production. HCV-mediated activation of miR-21 expression requires viral proteins and several signaling components. Moreover, we identified a transcription factor, activating protein-1 (AP-1), which is partly responsible for miR-21 induction in response to HCV infection through PKCε/JNK/c-Jun and PKCα/ERK/c-Fos cascades. Taken together, our results indicate that miR-21 is upregulated during HCV infection and negatively regulates IFN-α signaling through MyD88 and IRAK1 and may be a potential therapeutic target for antiviral intervention.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Vesicular Transport / genetics
  • Cell Line, Tumor
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • HEK293 Cells
  • Hepacivirus / genetics
  • Hepacivirus / immunology*
  • Hepacivirus / pathogenicity
  • Hepatitis C / immunology
  • Humans
  • Immune Evasion*
  • Interferon Regulatory Factor-3 / genetics
  • Interferon-alpha / biosynthesis
  • Interferon-alpha / metabolism
  • Interleukin-1 Receptor-Associated Kinases / genetics
  • Interleukin-1 Receptor-Associated Kinases / metabolism*
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • MAP Kinase Signaling System
  • MicroRNAs / genetics
  • MicroRNAs / immunology
  • MicroRNAs / metabolism*
  • Myeloid Differentiation Factor 88 / genetics
  • Myeloid Differentiation Factor 88 / metabolism*
  • Phosphorylation
  • Protein Kinase C / metabolism
  • Proto-Oncogene Proteins c-fos / metabolism
  • RNA Helicases / metabolism
  • RNA Interference
  • RNA, Small Interfering
  • Serine Endopeptidases / metabolism
  • Toll-Like Receptor 7 / metabolism
  • Up-Regulation
  • Viral Nonstructural Proteins / metabolism

Substances

  • Adaptor Proteins, Vesicular Transport
  • IRF3 protein, human
  • Interferon Regulatory Factor-3
  • Interferon-alpha
  • MIRN21 microRNA, human
  • MYD88 protein, human
  • MicroRNAs
  • Myeloid Differentiation Factor 88
  • NS3 protein, flavivirus
  • NS4A protein, flavivirus
  • NS5 protein, flavivirus
  • Proto-Oncogene Proteins c-fos
  • RNA, Small Interfering
  • TICAM1 protein, human
  • TLR7 protein, human
  • Toll-Like Receptor 7
  • Viral Nonstructural Proteins
  • IRAK1 protein, human
  • Interleukin-1 Receptor-Associated Kinases
  • Protein Kinase C
  • Extracellular Signal-Regulated MAP Kinases
  • JNK Mitogen-Activated Protein Kinases
  • Serine Endopeptidases
  • RNA Helicases

Grants and funding

This work was supported by research grants from Major State Basic Research Development Program (973 Program) (2012CB518900 and 2009CB522506), National Natural Science Foundation of China (31230005, 812111146, and 81171525), National Mega Project on Major Infectious Disease Prevention (2012ZX10002006-003 and 2012ZX10004-207), National Mega Project on Major Drug Development (2011ZX09401-302). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.