Herpes simplex virus 1 serine/threonine kinase US3 hyperphosphorylates IRF3 and inhibits beta interferon production

J Virol. 2013 Dec;87(23):12814-27. doi: 10.1128/JVI.02355-13. Epub 2013 Sep 18.

Abstract

Viral infection initiates a series of signaling cascades that lead to the transcription of interferons (IFNs), finally inducing interferon-stimulated genes (ISGs) to eliminate viruses. Viruses have evolved a variety of strategies to modulate host IFN-mediated immune responses. Herpes simplex virus 1 (HSV-1) US3, a Ser/Thr kinase conserved in alphaherpesviruses, was previously reported to counteract host innate immunity; however, the molecular mechanism is elusive. In this study, we report that US3 blocks IFN-β production by hyperphosphorylating IFN regulatory factor 3 (IRF3). Ectopic expression of US3 protein significantly inhibited Sendai virus (SeV)-mediated activation of IFN-β and IFN-stimulated response element (ISRE) promoters and the transcription of IFN-β, ISG54, and ISG56. US3 was also shown to block SeV-induced dimerization and nuclear translocation of IRF3. The kinase activity was indispensable for its inhibitory function, as kinase-dead (KD) US3 mutants K220M and D305A could not inhibit IFN-β production. Furthermore, US3 interacted with and hyperphosphorylated IRF3 at Ser175 to prevent IRF3 activation. Finally, the US3 KD mutant viruses were constructed and denoted K220M or D305A HSV-1, respectively. Cells and mice infected with both mutant viruses produced remarkably larger amounts of IFN-β than those infected with wild-type HSV-1. For the first time, these findings provide convincing evidence that US3 hyperphosphorylates IRF3, blocks the production of IFN-β, and subverts host innate immunity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Motifs
  • Animals
  • Down-Regulation*
  • Female
  • Herpes Simplex / genetics*
  • Herpes Simplex / metabolism*
  • Herpes Simplex / virology
  • Herpesvirus 1, Human / enzymology*
  • Herpesvirus 1, Human / genetics
  • Humans
  • Interferon Regulatory Factor-3 / chemistry
  • Interferon Regulatory Factor-3 / genetics
  • Interferon Regulatory Factor-3 / metabolism*
  • Interferon-beta / genetics*
  • Interferon-beta / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Phosphorylation
  • Promoter Regions, Genetic
  • Protein Binding
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*
  • Viral Proteins / genetics
  • Viral Proteins / metabolism*

Substances

  • Interferon Regulatory Factor-3
  • Viral Proteins
  • Interferon-beta
  • Protein Serine-Threonine Kinases
  • US3 protein, Human herpesvirus 1