H19 influenza A virus exhibits species-specific MHC class II receptor usage

Umut Karakus; Ignacio Mena; Jithesh Kottur; Sara S. El Zahed; Rocío Seoane; Soner Yildiz; Leanne Chen; Magdalena Plancarte; Le Ann Lindsay; Rebecca Halpin; Timothy B. Stockwell; David E. Wentworth; Geert Jan Boons; Florian Krammer; Silke Stertz; Walter Boyce; Robert P. de Vries; Aneel K. Aggarwal; Adolfo García-Sastre

doi:10.1016/j.chom.2024.05.018

H19 influenza A virus exhibits species-specific MHC class II receptor usage

Umut Karakus, Ignacio Mena, Jithesh Kottur, Sara S. El Zahed, Rocío Seoane, Soner Yildiz, Leanne Chen, Magdalena Plancarte, Le Ann Lindsay, Rebecca Halpin, Timothy B. Stockwell, David E. Wentworth, Geert Jan Boons, Florian Krammer, Silke Stertz, Walter Boyce, Robert P. de Vries, Aneel K. Aggarwal, Adolfo García-Sastre

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

2 Scopus citations

Abstract

Avian influenza A virus (IAV) surveillance in Northern California, USA, revealed unique IAV hemagglutinin (HA) genome sequences in cloacal swabs from lesser scaups. We found two closely related HA sequences in the same duck species in 2010 and 2013. Phylogenetic analyses suggest that both sequences belong to the recently discovered H19 subtype, which thus far has remained uncharacterized. We demonstrate that H19 does not bind the canonical IAV receptor sialic acid (Sia). Instead, H19 binds to the major histocompatibility complex class II (MHC class II), which facilitates viral entry. Unlike the broad MHC class II specificity of H17 and H18 from bat IAV, H19 exhibits a species-specific MHC class II usage that suggests a limited host range and zoonotic potential. Using cell lines overexpressing MHC class II, we rescued recombinant H19 IAV. We solved the H19 crystal structure and identified residues within the putative Sia receptor binding site (RBS) that impede Sia-dependent entry.

Original language	English
Pages (from-to)	1089-1102.e10
Journal	Cell Host and Microbe
Volume	32
Issue number	7
DOIs	https://doi.org/10.1016/j.chom.2024.05.018
State	Published - 10 Jul 2024

Keywords

HA structure
MHC class II
avian influenza virus surveillance
entry receptor
glycan array
hemagglutinin subtype H19
host range
influenza A virus
receptor binding site
recombinant H19 influenza A virus

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Karakus, U., Mena, I., Kottur, J., El Zahed, S. S., Seoane, R., Yildiz, S., Chen, L., Plancarte, M., Lindsay, L. A., Halpin, R., Stockwell, T. B., Wentworth, D. E., Boons, G. J., Krammer, F., Stertz, S., Boyce, W., de Vries, R. P., Aggarwal, A. K., & García-Sastre, A. (2024). H19 influenza A virus exhibits species-specific MHC class II receptor usage. Cell Host and Microbe, 32(7), 1089-1102.e10. https://doi.org/10.1016/j.chom.2024.05.018

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title = "H19 influenza A virus exhibits species-specific MHC class II receptor usage",

abstract = "Avian influenza A virus (IAV) surveillance in Northern California, USA, revealed unique IAV hemagglutinin (HA) genome sequences in cloacal swabs from lesser scaups. We found two closely related HA sequences in the same duck species in 2010 and 2013. Phylogenetic analyses suggest that both sequences belong to the recently discovered H19 subtype, which thus far has remained uncharacterized. We demonstrate that H19 does not bind the canonical IAV receptor sialic acid (Sia). Instead, H19 binds to the major histocompatibility complex class II (MHC class II), which facilitates viral entry. Unlike the broad MHC class II specificity of H17 and H18 from bat IAV, H19 exhibits a species-specific MHC class II usage that suggests a limited host range and zoonotic potential. Using cell lines overexpressing MHC class II, we rescued recombinant H19 IAV. We solved the H19 crystal structure and identified residues within the putative Sia receptor binding site (RBS) that impede Sia-dependent entry.",

keywords = "HA structure, MHC class II, avian influenza virus surveillance, entry receptor, glycan array, hemagglutinin subtype H19, host range, influenza A virus, receptor binding site, recombinant H19 influenza A virus",

author = "Umut Karakus and Ignacio Mena and Jithesh Kottur and {El Zahed}, {Sara S.} and Roc{\'i}o Seoane and Soner Yildiz and Leanne Chen and Magdalena Plancarte and Lindsay, {Le Ann} and Rebecca Halpin and Stockwell, {Timothy B.} and Wentworth, {David E.} and Boons, {Geert Jan} and Florian Krammer and Silke Stertz and Walter Boyce and {de Vries}, {Robert P.} and Aggarwal, {Aneel K.} and Adolfo Garc{\'i}a-Sastre",

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year = "2024",

month = jul,

day = "10",

doi = "10.1016/j.chom.2024.05.018",

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Karakus, U, Mena, I, Kottur, J, El Zahed, SS, Seoane, R, Yildiz, S, Chen, L, Plancarte, M, Lindsay, LA, Halpin, R, Stockwell, TB, Wentworth, DE, Boons, GJ, Krammer, F, Stertz, S, Boyce, W, de Vries, RP, Aggarwal, AK & García-Sastre, A 2024, 'H19 influenza A virus exhibits species-specific MHC class II receptor usage', Cell Host and Microbe, vol. 32, no. 7, pp. 1089-1102.e10. https://doi.org/10.1016/j.chom.2024.05.018

TY - JOUR

T1 - H19 influenza A virus exhibits species-specific MHC class II receptor usage

AU - Karakus, Umut

AU - Mena, Ignacio

AU - Kottur, Jithesh

AU - El Zahed, Sara S.

AU - Seoane, Rocío

AU - Yildiz, Soner

AU - Chen, Leanne

AU - Plancarte, Magdalena

AU - Lindsay, Le Ann

AU - Halpin, Rebecca

AU - Stockwell, Timothy B.

AU - Wentworth, David E.

AU - Boons, Geert Jan

AU - Krammer, Florian

AU - Stertz, Silke

AU - Boyce, Walter

AU - de Vries, Robert P.

AU - Aggarwal, Aneel K.

AU - García-Sastre, Adolfo

PY - 2024/7/10

Y1 - 2024/7/10

N2 - Avian influenza A virus (IAV) surveillance in Northern California, USA, revealed unique IAV hemagglutinin (HA) genome sequences in cloacal swabs from lesser scaups. We found two closely related HA sequences in the same duck species in 2010 and 2013. Phylogenetic analyses suggest that both sequences belong to the recently discovered H19 subtype, which thus far has remained uncharacterized. We demonstrate that H19 does not bind the canonical IAV receptor sialic acid (Sia). Instead, H19 binds to the major histocompatibility complex class II (MHC class II), which facilitates viral entry. Unlike the broad MHC class II specificity of H17 and H18 from bat IAV, H19 exhibits a species-specific MHC class II usage that suggests a limited host range and zoonotic potential. Using cell lines overexpressing MHC class II, we rescued recombinant H19 IAV. We solved the H19 crystal structure and identified residues within the putative Sia receptor binding site (RBS) that impede Sia-dependent entry.

AB - Avian influenza A virus (IAV) surveillance in Northern California, USA, revealed unique IAV hemagglutinin (HA) genome sequences in cloacal swabs from lesser scaups. We found two closely related HA sequences in the same duck species in 2010 and 2013. Phylogenetic analyses suggest that both sequences belong to the recently discovered H19 subtype, which thus far has remained uncharacterized. We demonstrate that H19 does not bind the canonical IAV receptor sialic acid (Sia). Instead, H19 binds to the major histocompatibility complex class II (MHC class II), which facilitates viral entry. Unlike the broad MHC class II specificity of H17 and H18 from bat IAV, H19 exhibits a species-specific MHC class II usage that suggests a limited host range and zoonotic potential. Using cell lines overexpressing MHC class II, we rescued recombinant H19 IAV. We solved the H19 crystal structure and identified residues within the putative Sia receptor binding site (RBS) that impede Sia-dependent entry.

KW - HA structure

KW - MHC class II

KW - avian influenza virus surveillance

KW - entry receptor

KW - glycan array

KW - hemagglutinin subtype H19

KW - host range

KW - influenza A virus

KW - receptor binding site

KW - recombinant H19 influenza A virus

UR - http://www.scopus.com/inward/record.url?scp=85197522616&partnerID=8YFLogxK

U2 - 10.1016/j.chom.2024.05.018

DO - 10.1016/j.chom.2024.05.018

M3 - Article

C2 - 38889725

AN - SCOPUS:85197522616

SN - 1931-3128

VL - 32

SP - 1089-1102.e10

JO - Cell Host and Microbe

JF - Cell Host and Microbe

IS - 7

ER -

H19 influenza A virus exhibits species-specific MHC class II receptor usage

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Keywords

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