IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-34060-8.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-34060-8
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-34060-8?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Daniel Ellis & Julia Lederhofer & Oliver J. Acton & Yaroslav Tsybovsky & Sally Kephart & Christina Yap & Rebecca A. Gillespie & Adrian Creanga & Audrey Olshefsky & Tyler Stephens & Deleah Pettie & Mic, 2022. "Structure-based design of stabilized recombinant influenza neuraminidase tetramers," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Momei Zhou & Benjamin Vollmer & Emily Machala & Muyuan Chen & Kay Grünewald & Ann M. Arvin & Wah Chiu & Stefan L. Oliver, 2023. "Targeted mutagenesis of the herpesvirus fusogen central helix captures transition states," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Johannes P. M. Langedijk & Freek Cox & Nicole V. Johnson & Daan Overveld & Lam Le & Ward Hoogen & Richard Voorzaat & Roland Zahn & Leslie Fits & Jarek Juraszek & Jason S. McLellan & Mark J. G. Bakkers, 2024. "Universal paramyxovirus vaccine design by stabilizing regions involved in structural transformation of the fusion protein," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    4. Xiao Xiao & Arthur Fridman & Lu Zhang & Pavlo Pristatsky & Eberhard Durr & Michael Minnier & Aimin Tang & Kara S. Cox & Zhiyun Wen & Renee Moore & Dongrui Tian & Jennifer D. Galli & Scott Cosmi & Mich, 2022. "Profiling of hMPV F-specific antibodies isolated from human memory B cells," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    5. Mark J. G. Bakkers & Tina Ritschel & Machteld Tiemessen & Jacobus Dijkman & Angelo A. Zuffianò & Xiaodi Yu & Daan Overveld & Lam Le & Richard Voorzaat & Marlies M. Haaren & Martijn Man & Sem Tamara & , 2024. "Efficacious human metapneumovirus vaccine based on AI-guided engineering of a closed prefusion trimer," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Nicole V. Johnson & Revina C. Scherpenzeel & Mark J. G. Bakkers & Ajit R. Ramamohan & Daan Overveld & Lam Le & Johannes P. M. Langedijk & Joost A. Kolkman & Jason S. McLellan, 2024. "Structural basis for potent neutralization of human respirovirus type 3 by protective single-domain camelid antibodies," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Karen J. Gonzalez & Jiachen Huang & Miria F. Criado & Avik Banerjee & Stephen M. Tompkins & Jarrod J. Mousa & Eva-Maria Strauch, 2024. "A general computational design strategy for stabilizing viral class I fusion proteins," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    8. Ching-Lin Hsieh & Scott A. Rush & Concepcion Palomo & Chia-Wei Chou & Whitney Pickens & Vicente Más & Jason S. McLellan, 2022. "Structure-based design of prefusion-stabilized human metapneumovirus fusion proteins," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    9. Sonal V. Gidwani & Devarshi Brahmbhatt & Aaron Zomback & Mamie Bassie & Jennifer Martinez & Jian Zhuang & John Schulze & Jason S. McLellan & Roberto Mariani & Peter Alff & Daniela Frasca & Bonnie B. B, 2024. "Engineered dityrosine-bonding of the RSV prefusion F protein imparts stability and potency advantages," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    10. Kwinten Sliepen & Laura Radić & Joan Capella-Pujol & Yasunori Watanabe & Ian Zon & Ana Chumbe & Wen-Hsin Lee & Marlon Gast & Jelle Koopsen & Sylvie Koekkoek & Iván Moral-Sánchez & Philip J. M. Brouwer, 2022. "Induction of cross-neutralizing antibodies by a permuted hepatitis C virus glycoprotein nanoparticle vaccine candidate," Nature Communications, Nature, vol. 13(1), pages 1-16, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34060-8. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.