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Influenza A virus virulence depends on two amino acids in the N-terminal domain of its NS1 protein facilitating inhibition of PKR

tetano

Editor, Senior Moderator
J Virol. 2017 Mar 1. pii: JVI.00198-17. doi: 10.1128/JVI.00198-17. [Epub ahead of print]
[h=1]Influenza A virus virulence depends on two amino acids in the N-terminal domain of its NS1 protein facilitating inhibition of PKR.[/h] Schierhorn KL[SUP]1[/SUP], Jolmes F[SUP]2[/SUP], Bespalowa J[SUP]3[/SUP], Saenger S[SUP]1[/SUP], Peteranderl C[SUP]3[/SUP], Dzieciolowski J[SUP]4[/SUP], Budt M[SUP]1[/SUP], Pleschka S[SUP]4[/SUP], Herrmann A[SUP]2[/SUP], Herold S[SUP]3[/SUP], Wolff T[SUP]5[/SUP].
[h=3]Author information[/h]

[h=3]Abstract[/h] The RNA-dependent protein kinase (PKR) has broad antiviral activity inducing translational shut-down of viral and cellular genes and is therefore targeted by various viral proteins to facilitate pathogen propagation. The pleiotropic NS1 protein of influenza A virus acts as silencer of PKR activation and ascertains high level viral replication and virulence. However, the exact way of this inhibition remains controversial. To elucidate the structural requirements within the NS1 protein for PKR inhibition, we generated a set of mutant viruses identifying highly conserved arginine residues 35 and 46 within the NS1 N-terminus as being most critical not only for binding to and blocking activation of PKR, but also for efficient virus propagation. Biochemical and FRET-based interaction studies showed that mutation of each of R35 or R46 allowed formation of NS1 dimers, but eliminated any detectable binding to PKR as well as to dsRNA. Using in vitro and in vivo approaches of phenotypic restoration we demonstrate the essential role of the NS1 N-terminus for blocking PKR. The strong attenuation conferred by NS1 mutations R35A or R46A was substantially alleviated by stable knock-down of PKR in human cells. Intriguingly, both NS1 mutant viruses did not trigger any signs of disease in PKR[SUP]+/+[/SUP] mice, but replicated to high titers in lungs of PKR[SUP]-/-[/SUP] mice and caused lethal infections. These data not only establish the NS1 N-terminus as highly critical for neutralization of PKR's antiviral activity, but also identify this blockade as an indispensable contribution of NS1 to the viral life cycle.IMPORTANCE Influenza A virus inhibits activation of the RNA-dependent protein kinase PKR by means of its non-structural NS1 protein, but the underlying mode of inhibition is debated. Using mutational analysis, we identify arginine residues 35 and 46 within the N-terminal NS1 domain as highly critical for binding to and functional silencing of PKR. In addition, our data show that this is a main activity of the amino acids 35 and 46 as the strong attenuation of corresponding mutant viruses in human cells was rescued to a large extent by lowering PKR expression levels. Significantly, this corresponded with restoration of viral virulence for NS1 R35A and R46A mutant viruses in PKR[SUP]-/-[/SUP] mice. Therefore, our data establish a model in which the NS1 N-terminal domain engages in a binding interaction to inhibit activation of PKR and ensure efficient viral propagation and virulence.
Copyright ? 2017 American Society for Microbiology.


PMID: 28250123 DOI: 10.1128/JVI.00198-17
[PubMed - as supplied by publisher]
 
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