Hepatitis B virus polymerase impairs interferon-α-induced STA T activation through inhibition of importin-α5 and protein kinase C-δ

Hepatology. 2013 Feb;57(2):470-82. doi: 10.1002/hep.26064.

Abstract

Treatment with exogenous interferon (IFN)-α is not effective in the majority of patients with chronic hepatitis B virus (HBV) infection. Recent evidence suggests that HBV has evolved strategies to block the nuclear translocation of signal transducer and activator of transcription (STAT) 1 to limit IFN-α-induced cellular antiviral responses. However, it remains unclear whether STAT1 translocation is impaired in chronic hepatitis B patients and what mechanisms are involved. Here we report that the expression of HBV polymerase (Pol) in human hepatic cell lines inhibited induction of IFN-stimulated genes and resulted in a weakened antiviral activity of IFN-α. Ectopic expression of Pol suppressed IFN-α-induced STAT1 serine 727 phosphorylation and STAT1/2 nuclear accumulation, whereas STAT1 tyrosine 701 phosphorylation, and STAT1-STAT2 heterodimer formation were not affected. Further studies demonstrated that Pol interacted with the catalytic domain of protein kinase C-δ (PKC-δ) and perturbed PKC-δ phosphorylation and its association with STAT1, which resulted in the suppression of STAT1 Ser727 phosphorylation. Moreover, Pol was found to interfere with nuclear transportation of STAT1/2 by competitively binding to the region of importin-α5 required for STAT1/2 recruitment. Truncation analysis suggested that the terminal protein and RNase H domains of Pol were able to bind to PKC-δ and importin-α5, respectively, and were responsible for the inhibition of IFN-α signaling. More importantly, the inhibition of STAT1 and PKC-δ phosphorylation were confirmed in a hydrodynamic-based HBV mouse model, and the blockage of IFN-α-induced STAT1/2 nuclear translocation was observed in HBV-infected cells from liver biopsies of chronic HBV patients.

Conclusions: These results demonstrate a role for Pol in HBV-mediated antagonization of IFN-α signaling and provide a possible molecular mechanism by which HBV resists the IFN therapy and maintains its persistence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Hep G2 Cells
  • Hepatitis B virus / enzymology
  • Humans
  • Interferon-alpha / pharmacology
  • Interferon-alpha / therapeutic use*
  • Mice
  • Phosphorylation
  • Protein Kinase C-delta / antagonists & inhibitors*
  • Protein Kinase C-delta / metabolism
  • RNA-Directed DNA Polymerase / metabolism*
  • STAT1 Transcription Factor / antagonists & inhibitors
  • STAT1 Transcription Factor / metabolism
  • STAT2 Transcription Factor / antagonists & inhibitors
  • Vesiculovirus / drug effects
  • alpha Karyopherins / antagonists & inhibitors*

Substances

  • Interferon-alpha
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • STAT2 Transcription Factor
  • STAT2 protein, human
  • alpha Karyopherins
  • Protein Kinase C-delta
  • RNA-Directed DNA Polymerase