Influenza D binding properties vary amongst the two major virus clades and wildlife species

Nikoloz Nemanichvili; Alinda J Berends; Ilhan Tomris; Karen N Barnard; Colin R Parrish; Andrea Gröne; Jolianne M Rijks; Monique H Verheije; Robert P de Vries

doi:10.1016/j.vetmic.2021.109298

Influenza D binding properties vary amongst the two major virus clades and wildlife species

Nikoloz Nemanichvili, Alinda J Berends, Ilhan Tomris, Karen N Barnard, Colin R Parrish, Andrea Gröne, Jolianne M Rijks, Monique H Verheije, Robert P de Vries

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

Abstract

The influenza D virus (IDV) uses a trimeric hemagglutinin-esterase fusion protein (HEF) for attachment to 9-O-acetylated sialic acid receptors on the cell surface of host species. So far research has revealed that farm animals such as cattle, domestic pigs, goats, sheep and horses contain the necessary receptors on the epithelial surface of the respiratory tract to accommodate binding of the IDV HEF protein of both worldwide clades D/Oklahoma (D/OK) and D/Oklahoma/660 (D/660). More recently, seroprevalence studies have identified IDV-seropositive wildlife such as wild boar, deer, dromedaries, and small ruminants. However, no research has thus far been conducted in wildlife to reveal the distribution of acetylated sialic acid receptors that accommodate binding of IDV. Using our previously developed tissue microarray (TMA) system, we developed TMAs containing respiratory tissues of various wild and domestic species including wild boar, deer, dromedary, springbok, water buffalo, tiger, hedgehog, and Asian elephant. Protein histochemical staining of these TMAs with HEF proteins showed no receptor binding for wild Suidae, Cervidae and tiger. However, receptors were present in dromedary, springbok, water buffalo, Asian elephant, and hedgehog. In contrast to previously tested farm animals, a difference in host tropism was observed between the D/OK and D/660 clade HEF proteins in Asian elephant, and water buffalo. These results show that IDV can attach to the respiratory tract of wildlife which might facilitate transmission of IDV between wildlife and domestic animals.

Original language	English
Article number	109298
Pages (from-to)	1-8
Journal	Veterinary Microbiology
Volume	264
Early online date	7 Dec 2021
DOIs	https://doi.org/10.1016/j.vetmic.2021.109298
Publication status	Published - Jan 2022

Bibliographical note

Funding Information:
This research was partially funded by the European Food Safety Authority under Grant Agreement Number GA/EFSA/AFSCO/2017/01-GA04 , entitled ‘Risk assessment for influenza D in Europe’. Robert P. de Vries is a recipient of an ERC Starting Grant from the European Commission ( 802780 ) and a Beijerinck Premium of the Royal Dutch Academy of Sciences .

Funding Information:
We would like to thank the Centre for Cell Imaging at the Faculty of Veterinary Medicine, Utrecht University for use of the microscopy facilities and 3D printing services provided. We would also like to thank the Veterinary Pathologic Diagnostic Centre at the Faculty of Veterinary Medicine, Utrecht University for their assistance in acquiring and processing all the required animal tissues. We also thank Lisanne van der Voort of the Utrecht University, Faculty of Veterinary Medicine, Communications & Marketing Department for her graphical designs of the pictograms. We would also like to thank Rogier Sanders of the Amsterdam Medical Centre, Department of Medical Microbiology and Infection Prevention for gifting the codon-optimized cDNA open reading frames of full-length HKU1 spike protein. We also thank Wendy Weichert of the Cornell University, Department of Microbiology and Immunology College of Veterinary Medicine for her time and assistance in obtaining the MDCK ?CaSD1 cell line. We would finally like to thank Mariette F. Ducatez of the French National Re-search Institute for Agriculture, Food and the Environment for her guidance and input. This research was partially funded by the European Food Safety Authority under Grant Agreement Number GA/EFSA/AFSCO/2017/01-GA04, entitled ?Risk assessment for influenza D in Europe?. Robert P. de Vries is a recipient of an ERC Starting Grant from the European Commission (802780) and a Beijerinck Premium of the Royal Dutch Academy of Sciences.

Publisher Copyright:
© 2021 The Author(s)

Keywords

9-O-acetylated sialic acid
Host tropism
Influenza D
Tissue microarray
Wildlife

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1-s2.0-S0378113521003217-mainFinal published version, 8.88 MBLicence: CC BY

Cite this

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title = "Influenza D binding properties vary amongst the two major virus clades and wildlife species",

abstract = "The influenza D virus (IDV) uses a trimeric hemagglutinin-esterase fusion protein (HEF) for attachment to 9-O-acetylated sialic acid receptors on the cell surface of host species. So far research has revealed that farm animals such as cattle, domestic pigs, goats, sheep and horses contain the necessary receptors on the epithelial surface of the respiratory tract to accommodate binding of the IDV HEF protein of both worldwide clades D/Oklahoma (D/OK) and D/Oklahoma/660 (D/660). More recently, seroprevalence studies have identified IDV-seropositive wildlife such as wild boar, deer, dromedaries, and small ruminants. However, no research has thus far been conducted in wildlife to reveal the distribution of acetylated sialic acid receptors that accommodate binding of IDV. Using our previously developed tissue microarray (TMA) system, we developed TMAs containing respiratory tissues of various wild and domestic species including wild boar, deer, dromedary, springbok, water buffalo, tiger, hedgehog, and Asian elephant. Protein histochemical staining of these TMAs with HEF proteins showed no receptor binding for wild Suidae, Cervidae and tiger. However, receptors were present in dromedary, springbok, water buffalo, Asian elephant, and hedgehog. In contrast to previously tested farm animals, a difference in host tropism was observed between the D/OK and D/660 clade HEF proteins in Asian elephant, and water buffalo. These results show that IDV can attach to the respiratory tract of wildlife which might facilitate transmission of IDV between wildlife and domestic animals.",

keywords = "9-O-acetylated sialic acid, Host tropism, Influenza D, Tissue microarray, Wildlife",

author = "Nikoloz Nemanichvili and Berends, {Alinda J} and Ilhan Tomris and Barnard, {Karen N} and Parrish, {Colin R} and Andrea Gr{\"o}ne and Rijks, {Jolianne M} and Verheije, {Monique H} and {de Vries}, {Robert P}",

note = "Funding Information: This research was partially funded by the European Food Safety Authority under Grant Agreement Number GA/EFSA/AFSCO/2017/01-GA04 , entitled {\textquoteleft}Risk assessment for influenza D in Europe{\textquoteright}. Robert P. de Vries is a recipient of an ERC Starting Grant from the European Commission ( 802780 ) and a Beijerinck Premium of the Royal Dutch Academy of Sciences . Funding Information: We would like to thank the Centre for Cell Imaging at the Faculty of Veterinary Medicine, Utrecht University for use of the microscopy facilities and 3D printing services provided. We would also like to thank the Veterinary Pathologic Diagnostic Centre at the Faculty of Veterinary Medicine, Utrecht University for their assistance in acquiring and processing all the required animal tissues. We also thank Lisanne van der Voort of the Utrecht University, Faculty of Veterinary Medicine, Communications & Marketing Department for her graphical designs of the pictograms. We would also like to thank Rogier Sanders of the Amsterdam Medical Centre, Department of Medical Microbiology and Infection Prevention for gifting the codon-optimized cDNA open reading frames of full-length HKU1 spike protein. We also thank Wendy Weichert of the Cornell University, Department of Microbiology and Immunology College of Veterinary Medicine for her time and assistance in obtaining the MDCK ?CaSD1 cell line. We would finally like to thank Mariette F. Ducatez of the French National Re-search Institute for Agriculture, Food and the Environment for her guidance and input. This research was partially funded by the European Food Safety Authority under Grant Agreement Number GA/EFSA/AFSCO/2017/01-GA04, entitled ?Risk assessment for influenza D in Europe?. Robert P. de Vries is a recipient of an ERC Starting Grant from the European Commission (802780) and a Beijerinck Premium of the Royal Dutch Academy of Sciences. Publisher Copyright: {\textcopyright} 2021 The Author(s)",

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AU - Parrish, Colin R

AU - Gröne, Andrea

AU - Rijks, Jolianne M

AU - Verheije, Monique H

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Influenza D binding properties vary amongst the two major virus clades and wildlife species

Abstract

Bibliographical note

Keywords

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