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Accumulation of human-adapting mutations during circulation of A(H1N1)pdm09 influenza in humans in the UK

tetano

Editor, Senior Moderator
J Virol. 2014 Sep 10. pii: JVI.01636-14. [Epub ahead of print]
Accumulation of human-adapting mutations during circulation of A(H1N1)pdm09 influenza in humans in the UK.
Elderfield RA1, Watson SJ2, Godlee A3, Adamson WE4, Thompson CI5, Dunning J6, Fernandez-Alonso M1, Blumenkrantz D1, Hussell T3; The MOSAIC investigators, Zambon M5, Openshaw P6, Kellam P2, Barclay WS7.
Author information
Abstract

The influenza pandemic that emerged in 2009 provided an unprecedented opportunity to study adaptation of a virus recently acquired from an animal source during human transmission. In the UK, the novel virus spread in three temporally distinct waves between 2009 and 2011. Phylogenetic analysis of complete viral genomes showed that mutations accumulated over time. Second and third wave viruses replicated more rapidly in human airway epithelial (HAE) cells than first wave virus. In infected mice, weight loss varied between viral isolates from the same wave but showed no distinct pattern with wave, and did not correlate with viral load in the mouse lungs or severity of disease in the human donor. However, second and third wave viruses induced less interferon-α in the infected mouse lungs. NS1 protein, an interferon antagonist, had accumulated several mutations in second and third wave viruses. Recombinant viruses with third wave NS gene induced less interferon in human cells but this alone was did not account for increased virus fitness in HAE cells. Mutations in HA and NA genes in third wave viruses caused increased binding to α-2,6 sialic acid, and enhanced infectivity in human mucus. A recombinant virus with these two segments replicated more efficiently in HAE cells. A mutation in PA (N321K) enhanced polymerase activity of third wave viruses and also provided a replicative advantage in HAE cells. Therefore, multiple mutations allowed incremental changes in viral fitness which together may have contributed to the apparent increase in severity of A(H1N1)pdm09 influenza during successive waves.
IMPORTANCE:

Although most people infected with the 2009 pandemic influenza virus had mild or unapparent symptoms, some suffered severe and devastating disease. The reasons for this variability were unknown but the numbers of severe cases increased during successive waves of human infection in the UK. To determine the causes of this variation, we studied genetic changes in virus isolates from individual hospitalized patients. There were no consistent differences between these viruses and those circulating in the community, but we found multiple evolutionary changes that in combination over time increased the virus's ability to infect human cells. These adaptations may explain the remarkable ability of A(H1N1)pdm09 virus to continue to circulate despite widespread immunity, and the apparent increase in severity of influenza over successive waves of infection.

Copyright ? 2014, American Society for Microbiology. All Rights Reserved.

PMID:
25210166
[PubMed - as supplied by publisher]

http://www.ncbi.nlm.nih.gov/pubmed/25210166
 
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