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Glycan remodeled erythrocytes facilitate antigenic characterization of recent A/H3N2 influenza viruses

Author

Listed:
  • Frederik Broszeit

    (Utrecht University)

  • Rosanne J. Beek

    (Utrecht University)

  • Luca Unione

    (Utrecht University)

  • Theo M. Bestebroer

    (Erasmus MC)

  • Digantkumar Chapla

    (University of Georgia)

  • Jeong-Yeh Yang

    (University of Georgia)

  • Kelley W. Moremen

    (University of Georgia)

  • Sander Herfst

    (Erasmus MC)

  • Ron A. M. Fouchier

    (Erasmus MC)

  • Robert P. Vries

    (Utrecht University)

  • Geert-Jan Boons

    (Utrecht University
    University of Georgia
    Utrecht University
    University of Georgia)

Abstract

During circulation in humans and natural selection to escape antibody recognition for decades, A/H3N2 influenza viruses emerged with altered receptor specificities. These viruses lost the ability to agglutinate erythrocytes critical for antigenic characterization and give low yields and acquire adaptive mutations when cultured in eggs and cells, contributing to recent vaccine challenges. Examination of receptor specificities of A/H3N2 viruses reveals that recent viruses compensated for decreased binding of the prototypic human receptor by recognizing α2,6-sialosides on extended LacNAc moieties. Erythrocyte glycomics shows an absence of extended glycans providing a rationale for lack of agglutination by recent A/H3N2 viruses. A glycan remodeling approach installing functional receptors on erythrocytes, allows antigenic characterization of recent A/H3N2 viruses confirming the cocirculation of antigenically different viruses in humans. Computational analysis of HAs in complex with sialosides having extended LacNAc moieties reveals that mutations distal to the RBD reoriented the Y159 side chain resulting in an extended receptor binding site.

Suggested Citation

  • Frederik Broszeit & Rosanne J. Beek & Luca Unione & Theo M. Bestebroer & Digantkumar Chapla & Jeong-Yeh Yang & Kelley W. Moremen & Sander Herfst & Ron A. M. Fouchier & Robert P. Vries & Geert-Jan Boon, 2021. "Glycan remodeled erythrocytes facilitate antigenic characterization of recent A/H3N2 influenza viruses," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-25713-1
    DOI: 10.1038/s41467-021-25713-1
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    Cited by:

    1. Simon P. J. Jong & Zandra C. Felix Garza & Joseph C. Gibson & Sarah Leeuwen & Robert P. Vries & Geert-Jan Boons & Marliek Hoesel & Karen Haan & Laura E. Groeningen & Katina D. Hulme & Hugo D. G. Willi, 2024. "Determinants of epidemic size and the impacts of lulls in seasonal influenza virus circulation," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    2. Ruipeng Lei & Weiwen Liang & Wenhao O. Ouyang & Andrea Hernandez Garcia & Chika Kikuchi & Shengyang Wang & Ryan McBride & Timothy J. C. Tan & Yuanxin Sun & Chunke Chen & Claire S. Graham & Lucia A. Ro, 2024. "Epistasis mediates the evolution of the receptor binding mode in recent human H3N2 hemagglutinin," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    3. Chika Kikuchi & Aristotelis Antonopoulos & Shengyang Wang & Tadashi Maemura & Rositsa Karamanska & Chiara Lee & Andrew J. Thompson & Anne Dell & Yoshihiro Kawaoka & Stuart M. Haslam & James C. Paulson, 2023. "Glyco-engineered MDCK cells display preferred receptors of H3N2 influenza absent in eggs used for vaccines," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Luca Unione & Augustinus N. A. Ammerlaan & Gerlof P. Bosman & Elif Uslu & Ruonan Liang & Frederik Broszeit & Roosmarijn Woude & Yanyan Liu & Shengzhou Ma & Lin Liu & Marcos Gómez-Redondo & Iris A. Ber, 2024. "Probing altered receptor specificities of antigenically drifting human H3N2 viruses by chemoenzymatic synthesis, NMR, and modeling," Nature Communications, Nature, vol. 15(1), pages 1-12, December.

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