N-Glycolylneuraminic Acid as a Receptor for Influenza A Viruses

Frederik Broszeit; Netanel Tzarum; Xueyong Zhu; Nikoloz Nemanichvili; Dirk Eggink; Tim Leenders; Zeshi Li; Lin Liu; Margreet A. Wolfert; Andreas Papanikolaou; Carles Martínez-Romero; Ivan A. Gagarinov; Wenli Yu; Adolfo García-Sastre; Tom Wennekes; Masatoshi Okamatsu; Monique H. Verheije; Ian A. Wilson; Geert Jan Boons; Robert P. de Vries

doi:10.1016/j.celrep.2019.05.048

N-Glycolylneuraminic Acid as a Receptor for Influenza A Viruses

Frederik Broszeit, Netanel Tzarum, Xueyong Zhu, Nikoloz Nemanichvili, Dirk Eggink, Tim Leenders, Zeshi Li, Lin Liu, Margreet A. Wolfert, Andreas Papanikolaou, Carles Martínez-Romero, Ivan A. Gagarinov, Wenli Yu, Adolfo García-Sastre, Tom Wennekes, Masatoshi Okamatsu, Monique H. Verheije, Ian A. Wilson, Geert Jan Boons, Robert P. de Vries^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

64 Scopus citations

Abstract

A species barrier for the influenza A virus is the differential expression of sialic acid, which can either be α2,3-linked for avians or α2,6-linked for human viruses. The influenza A virus hosts also express other species-specific sialic acid derivatives. One major modification at C-5 is N-glycolyl (NeuGc), instead of N-acetyl (NeuAc). N-glycolyl is mammalian specific and expressed in pigs and horses, but not in humans, ferrets, seals, or dogs. Hemagglutinin (HA) adaptation to either N-acetyl or N-glycolyl is analyzed on a sialoside microarray containing both α2,3- and α2,6-linkage modifications on biologically relevant N-glycans. Binding studies reveal that avian, human, and equine HAs bind either N-glycolyl or N-acetyl. Structural data on N-glycolyl binding HA proteins of both H5 and H7 origin describe this specificity. Neuraminidases can cleave N-glycolyl efficiently, and tissue-binding studies reveal strict species specificity. The exclusive manner in which influenza A viruses differentiate between N-glycolyl and N-acetyl is indicative of selection.

Original language	English
Pages (from-to)	3284-3294.e6
Journal	Cell Reports
Volume	27
Issue number	11
DOIs	https://doi.org/10.1016/j.celrep.2019.05.048
State	Published - 11 Jun 2019
Externally published	Yes

Bibliographical note

Publisher Copyright:
© 2019 The Authors

Keywords

crystal structure
glycan-array
hemagglutinin
influenza A virus
neuraminidase
receptor-binding
sialic acid

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.celrep.2019.05.048

Cite this

Broszeit, F., Tzarum, N., Zhu, X., Nemanichvili, N., Eggink, D., Leenders, T., Li, Z., Liu, L., Wolfert, M. A., Papanikolaou, A., Martínez-Romero, C., Gagarinov, I. A., Yu, W., García-Sastre, A., Wennekes, T., Okamatsu, M., Verheije, M. H., Wilson, I. A., Boons, G. J., & de Vries, R. P. (2019). N-Glycolylneuraminic Acid as a Receptor for Influenza A Viruses. Cell Reports, 27(11), 3284-3294.e6. https://doi.org/10.1016/j.celrep.2019.05.048

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title = "N-Glycolylneuraminic Acid as a Receptor for Influenza A Viruses",

abstract = "A species barrier for the influenza A virus is the differential expression of sialic acid, which can either be α2,3-linked for avians or α2,6-linked for human viruses. The influenza A virus hosts also express other species-specific sialic acid derivatives. One major modification at C-5 is N-glycolyl (NeuGc), instead of N-acetyl (NeuAc). N-glycolyl is mammalian specific and expressed in pigs and horses, but not in humans, ferrets, seals, or dogs. Hemagglutinin (HA) adaptation to either N-acetyl or N-glycolyl is analyzed on a sialoside microarray containing both α2,3- and α2,6-linkage modifications on biologically relevant N-glycans. Binding studies reveal that avian, human, and equine HAs bind either N-glycolyl or N-acetyl. Structural data on N-glycolyl binding HA proteins of both H5 and H7 origin describe this specificity. Neuraminidases can cleave N-glycolyl efficiently, and tissue-binding studies reveal strict species specificity. The exclusive manner in which influenza A viruses differentiate between N-glycolyl and N-acetyl is indicative of selection.",

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author = "Frederik Broszeit and Netanel Tzarum and Xueyong Zhu and Nikoloz Nemanichvili and Dirk Eggink and Tim Leenders and Zeshi Li and Lin Liu and Wolfert, {Margreet A.} and Andreas Papanikolaou and Carles Mart{\'i}nez-Romero and Gagarinov, {Ivan A.} and Wenli Yu and Adolfo Garc{\'i}a-Sastre and Tom Wennekes and Masatoshi Okamatsu and Verheije, {Monique H.} and Wilson, {Ian A.} and Boons, {Geert Jan} and {de Vries}, {Robert P.}",

note = "Publisher Copyright: {\textcopyright} 2019 The Authors",

year = "2019",

month = jun,

day = "11",

doi = "10.1016/j.celrep.2019.05.048",

language = "אנגלית",

volume = "27",

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Broszeit, F, Tzarum, N, Zhu, X, Nemanichvili, N, Eggink, D, Leenders, T, Li, Z, Liu, L, Wolfert, MA, Papanikolaou, A, Martínez-Romero, C, Gagarinov, IA, Yu, W, García-Sastre, A, Wennekes, T, Okamatsu, M, Verheije, MH, Wilson, IA, Boons, GJ & de Vries, RP 2019, 'N-Glycolylneuraminic Acid as a Receptor for Influenza A Viruses', Cell Reports, vol. 27, no. 11, pp. 3284-3294.e6. https://doi.org/10.1016/j.celrep.2019.05.048

TY - JOUR

T1 - N-Glycolylneuraminic Acid as a Receptor for Influenza A Viruses

AU - Broszeit, Frederik

AU - Tzarum, Netanel

AU - Zhu, Xueyong

AU - Nemanichvili, Nikoloz

AU - Eggink, Dirk

AU - Leenders, Tim

AU - Li, Zeshi

AU - Liu, Lin

AU - Wolfert, Margreet A.

AU - Papanikolaou, Andreas

AU - Martínez-Romero, Carles

AU - Gagarinov, Ivan A.

AU - Yu, Wenli

AU - García-Sastre, Adolfo

AU - Wennekes, Tom

AU - Okamatsu, Masatoshi

AU - Verheije, Monique H.

AU - Wilson, Ian A.

AU - Boons, Geert Jan

AU - de Vries, Robert P.

PY - 2019/6/11

Y1 - 2019/6/11

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KW - crystal structure

KW - glycan-array

KW - hemagglutinin

KW - influenza A virus

KW - neuraminidase

KW - receptor-binding

KW - sialic acid

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JO - Cell Reports

JF - Cell Reports

IS - 11

ER -

N-Glycolylneuraminic Acid as a Receptor for Influenza A Viruses

Abstract

Bibliographical note

Keywords

UN SDGs

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