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Human-type sialic acid receptors contribute to avian influenza A virus binding and entry by hetero-multivalent interactions

Author

Listed:
  • Mengying Liu

    (Utrecht University)

  • Liane Z. X. Huang

    (Utrecht University)

  • Anthony A. Smits

    (Utrecht University)

  • Christian Büll

    (University of Copenhagen
    Radboud University)

  • Yoshiki Narimatsu

    (University of Copenhagen)

  • Frank J. M. Kuppeveld

    (Utrecht University)

  • Henrik Clausen

    (University of Copenhagen)

  • Cornelis A. M. Haan

    (Utrecht University)

  • Erik Vries

    (Utrecht University)

Abstract

Establishment of zoonotic viruses, causing pandemics like the Spanish flu and Covid-19, requires adaptation to human receptors. Pandemic influenza A viruses (IAV) that crossed the avian-human species barrier switched from binding avian-type α2-3-linked sialic acid (2-3Sia) to human-type 2-6Sia receptors. Here, we show that this specificity switch is however less dichotomous as generally assumed. Binding and entry specificity were compared using mixed synthetic glycan gradients of 2-3Sia and 2-6Sia and by employing a genetically remodeled Sia repertoire on the surface of a Sia-free cell line and on a sialoglycoprotein secreted from these cells. Expression of a range of (mixed) 2-3Sia and 2-6Sia densities shows that non-binding human-type receptors efficiently enhanced avian IAV binding and entry provided the presence of a low density of high affinity avian-type receptors, and vice versa. Considering the heterogeneity of sialoglycan receptors encountered in vivo, hetero-multivalent binding is physiologically relevant and will impact evolutionary pathways leading to host adaptation.

Suggested Citation

  • Mengying Liu & Liane Z. X. Huang & Anthony A. Smits & Christian Büll & Yoshiki Narimatsu & Frank J. M. Kuppeveld & Henrik Clausen & Cornelis A. M. Haan & Erik Vries, 2022. "Human-type sialic acid receptors contribute to avian influenza A virus binding and entry by hetero-multivalent interactions," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31840-0
    DOI: 10.1038/s41467-022-31840-0
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    1. Xiaoli Xiong & Peter J. Coombs & Stephen R. Martin & Junfeng Liu & Haixia Xiao & John W. McCauley & Kathrin Locher & Philip A. Walker & Patrick J. Collins & Yoshihiro Kawaoka & John J. Skehel & Steven, 2013. "Receptor binding by a ferret-transmissible H5 avian influenza virus," Nature, Nature, vol. 497(7449), pages 392-396, May.
    2. Meng Liu & Azzurra Apriceno & Miguel Sipin & Edoardo Scarpa & Laura Rodriguez-Arco & Alessandro Poma & Gabriele Marchello & Giuseppe Battaglia & Stefano Angioletti-Uberti, 2020. "Combinatorial entropy behaviour leads to range selective binding in ligand-receptor interactions," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
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