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; LeAnn 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, LeAnn 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^*

^*Corresponding author for this work

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

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 & Microbe
Volume	32
Issue number	7
Early online date	13 Jun 2024
DOIs	https://doi.org/10.1016/j.chom.2024.05.018
Publication status	Published - 10 Jul 2024

Bibliographical note

Publisher Copyright:
© 2024 Elsevier Inc.

Funding

This research was partly funded by CRIPT (Center for Research on Influenza Pathogenesis and Transmission), an NIAID -funded Center of Excellence for Influenza Research and Response (CEIRR) contract number 75N93021C00014 (A.G.-S. and F.K.). This work was supported by a Postdoc.Mobility fellowship from the Swiss National Science Foundation to U.K. ( P500PB_206818 ). S.Y. received funding from the Swiss National Science Foundation Postdoc.Mobility fellowship ( P400PB_199292 ). R.P.d.V. is supported by the European Commission (ERC Starting Grant 802780 ). A.K.A. is supported by grant R35-GM13170 from the National Institutes of Health (NIH) . These data were generated while D.E.W. was employed at the J. Craig Venter Institute . The opinions expressed in this article are our own and do not reflect the view of the Centers for Disease Control and Prevention, the Department of Health and Human Services, or the U.S. Government. The sequencing study was funded by the National Institute of Allergy and Infectious Diseases and the National Institutes of Health under contract no. HHSN272200900007C , HHSN266200700005C , and HHSN272201400006C .

Funders	Funder number
European Commission
CRIPT
Engineering Research Centers	R35-GM13170, 802780
National Institutes of Health	HHSN272200900007C, HHSN266200700005C, HHSN272201400006C
National Institute of Allergy and Infectious Diseases	75N93021C00014
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung	P400PB_199292, P500PB_206818

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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10.1016/j.chom.2024.05.018

mmc2Final published version, 12.4 MBLicence: Taverne

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Karakus, U., Mena, I., Kottur, J., El Zahed, S. S., Seoane, R., Yildiz, S., Chen, L., Plancarte, M., Lindsay, L., 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 & Microbe, 32(7), 1089-1102.e10. https://doi.org/10.1016/j.chom.2024.05.018

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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.",

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Karakus, U, Mena, I, Kottur, J, El Zahed, SS, Seoane, R, Yildiz, S, Chen, L, Plancarte, M, Lindsay, L, Halpin, R, Stockwell, TB, Wentworth, DE, Boons, G-J, 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 & Microbe, vol. 32, no. 7, pp. 1089-1102.e10. https://doi.org/10.1016/j.chom.2024.05.018

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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, LeAnn

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

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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

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U2 - 10.1016/j.chom.2024.05.018

DO - 10.1016/j.chom.2024.05.018

M3 - Article

C2 - 38889725

SN - 1931-3128

VL - 32

SP - 1089-1102.e10

JO - Cell Host & Microbe

JF - Cell Host & Microbe

IS - 7

ER -

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

Abstract

Bibliographical note

Funding

Keywords

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