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An Influenza A virus can evolve to use human ANP32E through altering polymerase dimerization

Author

Listed:
  • Carol M. Sheppard

    (Imperial College London)

  • Daniel H. Goldhill

    (Imperial College London
    Royal Veterinary College)

  • Olivia C. Swann

    (Imperial College London)

  • Ecco Staller

    (University of Oxford)

  • Rebecca Penn

    (Imperial College London)

  • Olivia K. Platt

    (Imperial College London)

  • Ksenia Sukhova

    (Imperial College London)

  • Laury Baillon

    (Imperial College London)

  • Rebecca Frise

    (Imperial College London)

  • Thomas P. Peacock

    (Imperial College London)

  • Ervin Fodor

    (University of Oxford)

  • Wendy S. Barclay

    (Imperial College London)

Abstract

Human ANP32A and ANP32B are essential but redundant host factors for influenza virus genome replication. While most influenza viruses cannot replicate in edited human cells lacking both ANP32A and ANP32B, some strains exhibit limited growth. Here, we experimentally evolve such an influenza A virus in these edited cells and unexpectedly, after 2 passages, we observe robust viral growth. We find two mutations in different subunits of the influenza polymerase that enable the mutant virus to use a novel host factor, ANP32E, an alternative family member, which is unable to support the wild type polymerase. Both mutations reside in the symmetric dimer interface between two polymerase complexes and reduce polymerase dimerization. These mutations have previously been identified as adapting influenza viruses to mice. Indeed, the evolved virus gains the ability to use suboptimal mouse ANP32 proteins and becomes more virulent in mice. We identify further mutations in the symmetric dimer interface which we predict allow influenza to adapt to use suboptimal ANP32 proteins through a similar mechanism. Overall, our results suggest a balance between asymmetric and symmetric dimers of influenza virus polymerase that is influenced by the interaction between polymerase and ANP32 host proteins.

Suggested Citation

  • Carol M. Sheppard & Daniel H. Goldhill & Olivia C. Swann & Ecco Staller & Rebecca Penn & Olivia K. Platt & Ksenia Sukhova & Laury Baillon & Rebecca Frise & Thomas P. Peacock & Ervin Fodor & Wendy S. B, 2023. "An Influenza A virus can evolve to use human ANP32E through altering polymerase dimerization," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41308-4
    DOI: 10.1038/s41467-023-41308-4
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    References listed on IDEAS

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    1. Haitian Fan & Alexander P. Walker & Loïc Carrique & Jeremy R. Keown & Itziar Serna Martin & Dimple Karia & Jane Sharps & Narin Hengrung & Els Pardon & Jan Steyaert & Jonathan M. Grimes & Ervin Fodor, 2019. "Structures of influenza A virus RNA polymerase offer insight into viral genome replication," Nature, Nature, vol. 573(7773), pages 287-290, September.
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    Cited by:

    1. Benoît Arragain & Tim Krischuns & Martin Pelosse & Petra Drncova & Martin Blackledge & Nadia Naffakh & Stephen Cusack, 2024. "Structures of influenza A and B replication complexes give insight into avian to human host adaptation and reveal a role of ANP32 as an electrostatic chaperone for the apo-polymerase," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. Tim Krischuns & Benoît Arragain & Catherine Isel & Sylvain Paisant & Matthias Budt & Thorsten Wolff & Stephen Cusack & Nadia Naffakh, 2024. "The host RNA polymerase II C-terminal domain is the anchor for replication of the influenza virus genome," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

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