Inducible interleukin 32 (IL-32) exerts extensive antiviral function via selective stimulation of interferon λ1 (IFN-λ1)

J Biol Chem. 2013 Jul 19;288(29):20927-20941. doi: 10.1074/jbc.M112.440115. Epub 2013 May 31.

Abstract

Interleukin (IL)-32 has been recognized as a proinflammatory cytokine that participates in responses to viral infection. However, little is known about how IL-32 is induced in response to viral infection and the mechanisms of IL-32-mediated antiviral activities. We discovered that IL-32 is elevated by hepatitis B virus (HBV) infection both in vitro and in vivo and that HBV induced IL-32 expression at the level of both transcription and post-transcription. Furthermore, microRNA-29b was found to be a key factor in HBV-regulated IL-32 expression by directly targeting the mRNA 3'-untranslated region of IL-32. Antiviral analysis showed that IL-32 was not sufficient to alter HBV replication in HepG2.2.15 cells. To mimic the viremic phase of viral infection, freshly isolated peripheral blood mononuclear cells were treated with IL-32γ, the secretory isoform, and the supernatants were used for antiviral assays. Surprisingly, these supernatants exhibited extensive antiviral activity against multiplex viruses besides HBV. Thus, we speculated that the IL-32γ-treated peripheral blood mononuclear cells produced and secreted an unknown antiviral factor. Using antibody neutralization assays, we identified the factor as interferon (IFN)-λ1 and not IFN-α. Further studies indicated that IL-32γ effectively inhibited HBV replication in a hydrodynamic injection mouse model. Clinical data showed that elevated levels of IFN-λ1 both in serum and liver tissue of HBV patients were positively correlated to the increased levels of IL-32. Our results demonstrate that elevated IL-32 levels during viral infection mediate antiviral effects by stimulating the expression of IFN-λ1.

Keywords: Cytokines/Interferon; Gene Regulation; Host-Pathogen Interactions; Infectious Diseases; Interleukin; Viral Immunology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antiviral Agents / metabolism*
  • Binding Sites
  • Cell Line
  • Gene Expression Regulation / drug effects
  • Hepatitis B virus / drug effects
  • Hepatitis B virus / physiology*
  • Hepatitis B, Chronic / genetics
  • Hepatitis B, Chronic / immunology
  • Hepatitis B, Chronic / pathology
  • Hepatitis B, Chronic / virology
  • Humans
  • Hydrodynamics
  • Interferons
  • Interleukins / genetics
  • Interleukins / metabolism*
  • Interleukins / pharmacology
  • Leukocytes, Mononuclear / drug effects
  • Leukocytes, Mononuclear / metabolism
  • Leukocytes, Mononuclear / virology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / metabolism
  • NF-kappa B / metabolism
  • Recombinant Proteins / pharmacology
  • Transcription, Genetic / drug effects
  • Virus Replication / drug effects

Substances

  • Antiviral Agents
  • interferon-lambda, human
  • IL32 protein, human
  • Interleukins
  • MIRN29a microRNA, human
  • MicroRNAs
  • NF-kappa B
  • Recombinant Proteins
  • Interferons