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Prevalence and mechanisms of evolutionary contingency in human influenza H3N2 neuraminidase

Author

Listed:
  • Ruipeng Lei

    (University of Illinois at Urbana-Champaign)

  • Timothy J. C. Tan

    (University of Illinois at Urbana-Champaign)

  • Andrea Hernandez Garcia

    (University of Illinois at Urbana-Champaign)

  • Yiquan Wang

    (University of Illinois at Urbana-Champaign)

  • Meghan Diefenbacher

    (University of Illinois at Urbana-Champaign)

  • Chuyun Teo

    (University of Illinois at Urbana-Champaign)

  • Gopika Gopan

    (University of Illinois at Urbana-Champaign)

  • Zahra Tavakoli Dargani

    (University of Illinois at Urbana-Champaign)

  • Qi Wen Teo

    (University of Illinois at Urbana-Champaign
    University of Illinois at Urbana-Champaign)

  • Claire S. Graham

    (University of Illinois at Urbana-Champaign)

  • Christopher B. Brooke

    (University of Illinois at Urbana-Champaign
    University of Illinois at Urbana-Champaign)

  • Satish K. Nair

    (University of Illinois at Urbana-Champaign
    University of Illinois at Urbana-Champaign
    University of Illinois at Urbana-Champaign)

  • Nicholas C. Wu

    (University of Illinois at Urbana-Champaign
    University of Illinois at Urbana-Champaign
    University of Illinois at Urbana-Champaign
    University of Illinois at Urbana-Champaign)

Abstract

Neuraminidase (NA) of human influenza H3N2 virus has evolved rapidly and been accumulating mutations for more than half-century. However, biophysical constraints that govern the evolutionary trajectories of NA remain largely elusive. Here, we show that among 70 natural mutations that are present in the NA of a recent human H3N2 strain, >10% are deleterious for an ancestral strain. By mapping the permissive mutations using combinatorial mutagenesis and next-generation sequencing, an extensive epistatic network is revealed. Biophysical and structural analyses further demonstrate that certain epistatic interactions can be explained by non-additive stability effect, which in turn modulates membrane trafficking and enzymatic activity of NA. Additionally, our results suggest that other biophysical mechanisms also contribute to epistasis in NA evolution. Overall, these findings not only provide mechanistic insights into the evolution of human influenza NA and elucidate its sequence-structure-function relationship, but also have important implications for the development of next-generation influenza vaccines.

Suggested Citation

  • Ruipeng Lei & Timothy J. C. Tan & Andrea Hernandez Garcia & Yiquan Wang & Meghan Diefenbacher & Chuyun Teo & Gopika Gopan & Zahra Tavakoli Dargani & Qi Wen Teo & Claire S. Graham & Christopher B. Broo, 2022. "Prevalence and mechanisms of evolutionary contingency in human influenza H3N2 neuraminidase," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34060-8
    DOI: 10.1038/s41467-022-34060-8
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    References listed on IDEAS

    as
    1. Susu Duan & Elena A. Govorkova & Justin Bahl & Hassan Zaraket & Tatiana Baranovich & Patrick Seiler & Kristi Prevost & Robert G. Webster & Richard J. Webby, 2014. "Epistatic interactions between neuraminidase mutations facilitated the emergence of the oseltamivir-resistant H1N1 influenza viruses," Nature Communications, Nature, vol. 5(1), pages 1-12, December.
    2. Anders Krarup & Daphné Truan & Polina Furmanova-Hollenstein & Lies Bogaert & Pascale Bouchier & Ilona J. M. Bisschop & Myra N. Widjojoatmodjo & Roland Zahn & Hanneke Schuitemaker & Jason S. McLellan &, 2015. "A highly stable prefusion RSV F vaccine derived from structural analysis of the fusion mechanism," Nature Communications, Nature, vol. 6(1), pages 1-12, November.
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