Influenza D virus diverges from its related influenza C virus in the recognition of 9-O-acetylated N-acetyl- or N-glycolyl-neuraminic acid-containing glycan receptors

Runxia Liu; Chithra Sreenivasan; Hai Yu; Zizhang Sheng; Simon J. Newkirk; Wenfeng An; David F. Smith; Xi Chen; Dan Wang; Feng Li

doi:10.1016/j.virol.2020.02.007

Influenza D virus diverges from its related influenza C virus in the recognition of 9-O-acetylated N-acetyl- or N-glycolyl-neuraminic acid-containing glycan receptors

Runxia Liu, Chithra Sreenivasan, Hai Yu, Zizhang Sheng, Simon J. Newkirk, Wenfeng An, David F. Smith, Xi Chen, Dan Wang, Feng Li

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

29 Scopus citations

Abstract

Influenza D virus (IDV) utilizes bovines as a primary reservoir with periodical spillover to other mammalian hosts. By using traditional hemagglutination assay coupled with sialoglycan microarray (SGM) platform and functional assays, we demonstrated that IDV is more efficient in recognizing both 9-O-acetylated N-acetylneuraminic acid (Neu5,9Ac₂) and 9-O-acetylated N-glycolylneuraminic acid (Neu5Gc9Ac) than influenza C virus (ICV), a ubiquitous human pathogen. ICV seems to strongly prefer Neu5,9Ac₂ over Neu5Gc9Ac. Since Neu5Gc9Ac is different from Neu5,9Ac₂ only by an additional oxygen in the group at the C5 position, our results reveal that the hydroxyl group in Neu5Gc9Ac plays a critical role in determining receptor binding specificity, which as a result may discriminate IDV from ICV in communicating with 9-O-acetylated SAs. These findings shall provide a framework for further investigation towards better understanding of how newly discovered multiple-species-infecting IDV exploits natural 9-O-acetylated SA variations to expand its host range.

Original language	English
Pages (from-to)	16-23
Number of pages	8
Journal	Virology
Volume	545
DOIs	https://doi.org/10.1016/j.virol.2020.02.007
State	Published - Jun 2020

Bibliographical note

Publisher Copyright:
© 2020

Funding

This work was partially supported by NIH grants R01AI141889 and R01AI130684 and NIH Grant GM62116 , by SDSU AES 3AH-477 , by National Science Foundation/EPSCoR ( http://www.nsf.gov/od/iia/programs/epscor/index.jsp ) award IIA-1335423, and by the state of South Dakota’s Governor’s Office of Economic Development as a South Dakota Research Innovation Center. We thank all the members of the Li and Wang laboratories for their input into this work. We thank Dr. Reinhard Vlasak at University of Salzburg, Austria, for many valuable suggestions about our experiments. We also thank Peter Palese (Mt. Sinai Medical School, New York) for providing the C/Johannesburg/1/66 virus. We thank the Consortium for Functional Glycomics (Core H) that conducted glycan microarray assays. which was supported by NIH Grant GM62116 . This work was partially supported by NIH grants R01AI141889 and R01AI130684 and NIH Grant GM62116, by SDSU AES 3AH-477, by National Science Foundation/EPSCoR (http://www.nsf.gov/od/iia/programs/epscor/index.jsp) award IIA-1335423, and by the state of South Dakota's Governor's Office of Economic Development as a South Dakota Research Innovation Center.We thank all the members of the Li and Wang laboratories for their input into this work. We thank Dr. Reinhard Vlasak at University of Salzburg, Austria, for many valuable suggestions about our experiments. We also thank Peter Palese (Mt. Sinai Medical School, New York) for providing the C/Johannesburg/1/66 virus. We thank the Consortium for Functional Glycomics (Core H) that conducted glycan microarray assays. which was supported by NIH Grant GM62116.

Funders	Funder number
National Science Foundation/EPSCoR
South Dakota's Governor's Office of Economic Development
National Science Foundation Arctic Social Science Program
National Institutes of Health (NIH)	R01AI141889, GM62116
National Institutes of Health (NIH)
National Institute of Allergy and Infectious Diseases	R01AI130684
National Institute of Allergy and Infectious Diseases
Office of Experimental Program to Stimulate Competitive Research	IIA-1335423
Office of Experimental Program to Stimulate Competitive Research
San Diego State University	AES 3AH-477
San Diego State University
South Dakota Governor's Office of Economic Development
UniversitÃ¤t Salzburg	C/Johannesburg/1/66
UniversitÃ¤t Salzburg

Keywords

Glycan receptors
Influenza C virus
Influenza D virus

ASJC Scopus subject areas

Virology

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10.1016/j.virol.2020.02.007

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title = "Influenza D virus diverges from its related influenza C virus in the recognition of 9-O-acetylated N-acetyl- or N-glycolyl-neuraminic acid-containing glycan receptors",

abstract = "Influenza D virus (IDV) utilizes bovines as a primary reservoir with periodical spillover to other mammalian hosts. By using traditional hemagglutination assay coupled with sialoglycan microarray (SGM) platform and functional assays, we demonstrated that IDV is more efficient in recognizing both 9-O-acetylated N-acetylneuraminic acid (Neu5,9Ac2) and 9-O-acetylated N-glycolylneuraminic acid (Neu5Gc9Ac) than influenza C virus (ICV), a ubiquitous human pathogen. ICV seems to strongly prefer Neu5,9Ac2 over Neu5Gc9Ac. Since Neu5Gc9Ac is different from Neu5,9Ac2 only by an additional oxygen in the group at the C5 position, our results reveal that the hydroxyl group in Neu5Gc9Ac plays a critical role in determining receptor binding specificity, which as a result may discriminate IDV from ICV in communicating with 9-O-acetylated SAs. These findings shall provide a framework for further investigation towards better understanding of how newly discovered multiple-species-infecting IDV exploits natural 9-O-acetylated SA variations to expand its host range.",

keywords = "Glycan receptors, Influenza C virus, Influenza D virus",

author = "Runxia Liu and Chithra Sreenivasan and Hai Yu and Zizhang Sheng and Newkirk, \{Simon J.\} and Wenfeng An and Smith, \{David F.\} and Xi Chen and Dan Wang and Feng Li",

note = "Publisher Copyright: {\textcopyright} 2020",

year = "2020",

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doi = "10.1016/j.virol.2020.02.007",

language = "English",

volume = "545",

pages = "16--23",

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AU - Liu, Runxia

AU - Sreenivasan, Chithra

AU - Yu, Hai

AU - Sheng, Zizhang

AU - Newkirk, Simon J.

AU - An, Wenfeng

AU - Smith, David F.

AU - Chen, Xi

AU - Wang, Dan

AU - Li, Feng

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N2 - Influenza D virus (IDV) utilizes bovines as a primary reservoir with periodical spillover to other mammalian hosts. By using traditional hemagglutination assay coupled with sialoglycan microarray (SGM) platform and functional assays, we demonstrated that IDV is more efficient in recognizing both 9-O-acetylated N-acetylneuraminic acid (Neu5,9Ac2) and 9-O-acetylated N-glycolylneuraminic acid (Neu5Gc9Ac) than influenza C virus (ICV), a ubiquitous human pathogen. ICV seems to strongly prefer Neu5,9Ac2 over Neu5Gc9Ac. Since Neu5Gc9Ac is different from Neu5,9Ac2 only by an additional oxygen in the group at the C5 position, our results reveal that the hydroxyl group in Neu5Gc9Ac plays a critical role in determining receptor binding specificity, which as a result may discriminate IDV from ICV in communicating with 9-O-acetylated SAs. These findings shall provide a framework for further investigation towards better understanding of how newly discovered multiple-species-infecting IDV exploits natural 9-O-acetylated SA variations to expand its host range.

AB - Influenza D virus (IDV) utilizes bovines as a primary reservoir with periodical spillover to other mammalian hosts. By using traditional hemagglutination assay coupled with sialoglycan microarray (SGM) platform and functional assays, we demonstrated that IDV is more efficient in recognizing both 9-O-acetylated N-acetylneuraminic acid (Neu5,9Ac2) and 9-O-acetylated N-glycolylneuraminic acid (Neu5Gc9Ac) than influenza C virus (ICV), a ubiquitous human pathogen. ICV seems to strongly prefer Neu5,9Ac2 over Neu5Gc9Ac. Since Neu5Gc9Ac is different from Neu5,9Ac2 only by an additional oxygen in the group at the C5 position, our results reveal that the hydroxyl group in Neu5Gc9Ac plays a critical role in determining receptor binding specificity, which as a result may discriminate IDV from ICV in communicating with 9-O-acetylated SAs. These findings shall provide a framework for further investigation towards better understanding of how newly discovered multiple-species-infecting IDV exploits natural 9-O-acetylated SA variations to expand its host range.

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Influenza D virus diverges from its related influenza C virus in the recognition of 9-O-acetylated N-acetyl- or N-glycolyl-neuraminic acid-containing glycan receptors

Abstract

Bibliographical note

Funding

Keywords

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