Varicella-Zoster virus ORF9 is an antagonist of the DNA sensor cGAS

EMBO J. 2022 Jul 18;41(14):e109217. doi: 10.15252/embj.2021109217. Epub 2022 Jun 7.

Abstract

Varicella-Zoster virus (VZV) causes chickenpox and shingles. Although the infection is associated with severe morbidity in some individuals, molecular mechanisms that determine innate immune responses remain poorly defined. We found that the cGAS/STING DNA sensing pathway was required for type I interferon (IFN) induction during VZV infection and that recognition of VZV by cGAS restricted its replication. Screening of a VZV ORF expression library identified the essential VZV tegument protein ORF9 as a cGAS antagonist. Ectopically or virally expressed ORF9 bound to endogenous cGAS leading to reduced type I IFN responses to transfected DNA. Confocal microscopy revealed co-localisation of cGAS and ORF9. ORF9 and cGAS also interacted directly in a cell-free system and phase-separated together with DNA. Furthermore, ORF9 inhibited cGAMP production by cGAS. Taken together, these results reveal the importance of the cGAS/STING DNA sensing pathway for VZV recognition and identify a VZV immune antagonist that partially but directly interferes with DNA sensing via cGAS.

Keywords: DNA sensing; ORF9; Varicella-Zoster virus; cGAS; phase separation.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • DNA / metabolism
  • Herpesvirus 3, Human* / genetics
  • Herpesvirus 3, Human* / immunology
  • Humans
  • Immunity, Innate
  • Interferon Type I* / immunology
  • Membrane Proteins / immunology
  • Nucleotidyltransferases* / antagonists & inhibitors
  • Nucleotidyltransferases* / immunology
  • Viral Proteins* / immunology

Substances

  • Interferon Type I
  • Membrane Proteins
  • STING1 protein, human
  • Viral Proteins
  • DNA
  • Nucleotidyltransferases
  • cGAS protein, human