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

Producción científica: Article › revisión exhaustiva

30 Citas (Scopus)

Resumen

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.

Idioma original	English
Páginas (desde-hasta)	16-23
Número de páginas	8
Publicación	Virology
Volumen	545
DOI	https://doi.org/10.1016/j.virol.2020.02.007
Estado	Published - jun 2020

Nota bibliográfica

Publisher Copyright:
© 2020

Financiación

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.

Financiadores	Número del financiador
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 Institute of Allergy and Infectious F32-AI286447 Cydney N. Johnson Diseases National Institute of Allergy and Infectious R01AI168214 Jason W. Rosch Diseases National Institute of Allergy and Infectious P30 Cydney N. Johnson Diseases National Institute of Allergy and Infectious R00-AI166116 Christopher D. Radka Diseases National Institute of Allergy and Infectious T32-AI106700 Cydney N. Johnson Diseases National Institute of Allergy and Infectious R01AI192221 Jason W. Rosch Diseases National Inst...	R01AI130684
Office of Experimental Program to Stimulate Competitive Research	IIA-1335423
San Diego State University	AES 3AH-477
South Dakota Governor's Office of Economic Development
UniversitÃ¤t Salzburg	C/Johannesburg/1/66

ASJC Scopus subject areas

Virology

Acceder al documento

10.1016/j.virol.2020.02.007

Otros archivos y enlaces

Citar esto

@article{fb6c99a1eba24e9797f5aad538358ba5,

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",

month = jun,

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

language = "English",

volume = "545",

pages = "16--23",

}

TY - JOUR

T1 - 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

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

PY - 2020/6

Y1 - 2020/6

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.

KW - Glycan receptors

KW - Influenza C virus

KW - Influenza D virus

UR - https://www.scopus.com/pages/publications/85081021159

UR - https://www.scopus.com/pages/publications/85081021159#tab=citedBy

U2 - 10.1016/j.virol.2020.02.007

DO - 10.1016/j.virol.2020.02.007

M3 - Article

C2 - 32174455

AN - SCOPUS:85081021159

SN - 0042-6822

VL - 545

SP - 16

EP - 23

JO - Virology

JF - Virology

ER -

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

Resumen

Nota bibliográfica

Financiación

ASJC Scopus subject areas

Acceder al documento

Otros archivos y enlaces

Huella

Citar esto