Constitutive expression and distinct properties of IFN-epsilon protect the female reproductive tract from Zika virus infection

PLoS Pathog. 2023 Mar 10;19(3):e1010843. doi: 10.1371/journal.ppat.1010843. eCollection 2023 Mar.

Abstract

The immunological surveillance factors controlling vulnerability of the female reproductive tract (FRT) to sexually transmitted viral infections are not well understood. Interferon-epsilon (IFNɛ) is a distinct, immunoregulatory type-I IFN that is constitutively expressed by FRT epithelium and is not induced by pathogens like other antiviral IFNs α, β and λ. We show the necessity of IFNɛ for Zika Virus (ZIKV) protection by: increased susceptibility of IFNɛ-/- mice; their "rescue" by intravaginal recombinant IFNɛ treatment and blockade of protective endogenous IFNɛ by neutralising antibody. Complementary studies in human FRT cell lines showed IFNɛ had potent anti-ZIKV activity, associated with transcriptome responses similar to IFNλ but lacking the proinflammatory gene signature of IFNα. IFNɛ activated STAT1/2 pathways similar to IFNα and λ that were inhibited by ZIKV-encoded non-structural (NS) proteins, but not if IFNε exposure preceded infection. This scenario is provided by the constitutive expression of endogenous IFNε. However, the IFNɛ expression was not inhibited by ZIKV NS proteins despite their ability to antagonise the expression of IFNβ or λ. Thus, the constitutive expression of IFNɛ provides cellular resistance to viral strategies of antagonism and maximises the antiviral activity of the FRT. These results show that the unique spatiotemporal properties of IFNε provides an innate immune surveillance network in the FRT that is a significant barrier to viral infection with important implications for prevention and therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antiviral Agents / pharmacology
  • Female
  • Genitalia, Female
  • Humans
  • Immunologic Factors
  • Interferon-alpha / pharmacology
  • Mice
  • Zika Virus Infection*
  • Zika Virus* / genetics

Substances

  • Antiviral Agents
  • Immunologic Factors
  • Interferon-alpha
  • IFNE protein, human

Grants and funding

This research was funded by the National Health and Medical Research Council (NHMRC: nhmrc.gov.au) of Australia, awarded to M.R.B (APP1145613). Additionally, this work was supported by the Victorian State Government Operational Infrastructure Scheme. M.D.T was supported by an NHMRC Career Development Fellowship (APP1123319). Funding was also provided in part by the Division of Intramural Research, National Institutes of Health, National Institute of Allergy and Infectious Diseases. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.