Zika virus (ZIKV) can be transmitted sexually with infection of the female reproductive tract (FRT) and the developing foetus in utero. Like many RNA viruses ZIKV abrogates type-I and type-III IFN antiviral responses that is mediated by viral non-structural (NS) proteins. However, we hypothesise that the constitutively expressed IFNε in the FRT can circumvent ZIKV mediated IFN evasion by constitutively protecting the FRT from infection
To explore the role of IFNε in vivo we intravaginally inoculated IFNε -/-, type-I IFN receptor KO (IFNAR1-/-) and WT mice with ZIKV (PRVABC59). IFNε-/- mice had increased viral burden in the uterus and ovary (qRT-PCR) and increased ZIKV in vaginal washes when compared to WT mice (plaque assay). We intravaginally administered 4 μg of recombinant IFNε to IFNε-/- mice that resulted in the restoration of antiviral activity compared to buffer treated controls. Furthermore, application of 100 μg IFNε neutralising antibody to WT mice increased their susceptibility to infection compared to isotype controls.
We demonstrated that in primary transformed FRT cell lines, IFNε induced the expression of hundreds of ISGs similar to the antiviral profile induced by IFNλ-III, not IFNα as expected (NextSeq550 V2.5, qRT-PCR). Interestingly, IFNε did not induce expression of IRF1 and displayed limited induction of pro-inflammatory cytokines compared to IFNα and IFNλ-III. Pre-treatment with IFNε in FRT cell lines inhibited ZIKV replication like IFNα and IFNλ-III (qRT-PCR, plaque assay). However, post-infection these antiviral responses were blocked via NS5 mediated STAT2 degradation. Conversely, the expression of IFNε was impervious to ZIKV NS4A, NS1 and NS5 mediated inhibition downstream of activated RIG-I that delayed the production of other type-I and III IFNs (qRT-PCR). Furthermore, we demonstrated by immunoblot that IFNε signals constitutively despite IFN induced receptor desensitisation that limits IFNα mediated signal transduction.
Collectively these findings highlight the unique biological role of constitutively expressed IFNε in prevention of ZIKV infections in the FRT. Importantly, this shifts our understanding of FRT innate immunity from reliance on reactionary responses to pre-emptive protection against viral infections. This knowledge will help to inform sexual health recommendations for ZIKV and other infections of the FRT.