Increased public health threat of avian-origin H3N2 influenza virus caused by its evolution in dogs

Mingyue Chen; Yanli Lyu; Fan Wu; Ying Zhang; Hongkui Li; Rui Wang; Yang Liu; Xinyu Yang; Liwei Zhou; Ming Zhang; Qi Tong; Honglei Sun; Juan Pu; Jinhua Liu; Yipeng Sun

doi:10.7554/eLife.83470

eLife (Apr 2023)

Increased public health threat of avian-origin H3N2 influenza virus caused by its evolution in dogs

Mingyue Chen,
Yanli Lyu,
Fan Wu,
Ying Zhang,
Hongkui Li,
Rui Wang,
Yang Liu,
Xinyu Yang,
Liwei Zhou,
Ming Zhang,
Qi Tong,
Honglei Sun,
Juan Pu,
Jinhua Liu,
Yipeng Sun

Affiliations

Mingyue Chen: National Key Laboratory of Veterinary Public Health Security, Key Laboratory for Prevention and Control of Avian Influenza and Other Major Poultry Diseases and Key Laboratory of Animal Epidemiology of Ministry of Agriculture and Rural Affairs, College of Veterinary Medicine, China Agricultural University, Beijing, China
Yanli Lyu: National Key Laboratory of Veterinary Public Health Security, Key Laboratory for Prevention and Control of Avian Influenza and Other Major Poultry Diseases and Key Laboratory of Animal Epidemiology of Ministry of Agriculture and Rural Affairs, College of Veterinary Medicine, China Agricultural University, Beijing, China; Veterinary Teaching Hospital, China Agricultural University, Beijing, China
Fan Wu: National Key Laboratory of Veterinary Public Health Security, Key Laboratory for Prevention and Control of Avian Influenza and Other Major Poultry Diseases and Key Laboratory of Animal Epidemiology of Ministry of Agriculture and Rural Affairs, College of Veterinary Medicine, China Agricultural University, Beijing, China; Veterinary Teaching Hospital, China Agricultural University, Beijing, China
Ying Zhang: Department of Laboratory Medicine, the First Medical Centre, Chinese People's Liberation Army (PLA) General Hospital, Beijing, China
Hongkui Li: Liaoning Agricultural Development Service Center, Shenyang, China
Rui Wang: National Key Laboratory of Veterinary Public Health Security, Key Laboratory for Prevention and Control of Avian Influenza and Other Major Poultry Diseases and Key Laboratory of Animal Epidemiology of Ministry of Agriculture and Rural Affairs, College of Veterinary Medicine, China Agricultural University, Beijing, China
Yang Liu: Veterinary Teaching Hospital, China Agricultural University, Beijing, China
Xinyu Yang: National Key Laboratory of Veterinary Public Health Security, Key Laboratory for Prevention and Control of Avian Influenza and Other Major Poultry Diseases and Key Laboratory of Animal Epidemiology of Ministry of Agriculture and Rural Affairs, College of Veterinary Medicine, China Agricultural University, Beijing, China
Liwei Zhou: National Key Laboratory of Veterinary Public Health Security, Key Laboratory for Prevention and Control of Avian Influenza and Other Major Poultry Diseases and Key Laboratory of Animal Epidemiology of Ministry of Agriculture and Rural Affairs, College of Veterinary Medicine, China Agricultural University, Beijing, China; Veterinary Teaching Hospital, China Agricultural University, Beijing, China
Ming Zhang: Department of Epidemiology and Biostatistics, University of Georgia, Athens, United States
Qi Tong: National Key Laboratory of Veterinary Public Health Security, Key Laboratory for Prevention and Control of Avian Influenza and Other Major Poultry Diseases and Key Laboratory of Animal Epidemiology of Ministry of Agriculture and Rural Affairs, College of Veterinary Medicine, China Agricultural University, Beijing, China
Honglei Sun: National Key Laboratory of Veterinary Public Health Security, Key Laboratory for Prevention and Control of Avian Influenza and Other Major Poultry Diseases and Key Laboratory of Animal Epidemiology of Ministry of Agriculture and Rural Affairs, College of Veterinary Medicine, China Agricultural University, Beijing, China
Juan Pu: National Key Laboratory of Veterinary Public Health Security, Key Laboratory for Prevention and Control of Avian Influenza and Other Major Poultry Diseases and Key Laboratory of Animal Epidemiology of Ministry of Agriculture and Rural Affairs, College of Veterinary Medicine, China Agricultural University, Beijing, China
Jinhua Liu: National Key Laboratory of Veterinary Public Health Security, Key Laboratory for Prevention and Control of Avian Influenza and Other Major Poultry Diseases and Key Laboratory of Animal Epidemiology of Ministry of Agriculture and Rural Affairs, College of Veterinary Medicine, China Agricultural University, Beijing, China
Yipeng Sun: ORCiD; National Key Laboratory of Veterinary Public Health Security, Key Laboratory for Prevention and Control of Avian Influenza and Other Major Poultry Diseases and Key Laboratory of Animal Epidemiology of Ministry of Agriculture and Rural Affairs, College of Veterinary Medicine, China Agricultural University, Beijing, China

DOI: https://doi.org/10.7554/eLife.83470
Journal volume & issue: Vol. 12

Abstract

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Influenza A viruses in animal reservoirs repeatedly cross species barriers to infect humans. Dogs are the closest companion animals to humans, but the role of dogs in the ecology of influenza viruses is unclear. H3N2 avian influenza viruses were transmitted to dogs around 2006 and have formed stable lineages. The long-term epidemic of avian-origin H3N2 virus in canines offers the best models to investigate the effect of dogs on the evolution of influenza viruses. Here, we carried out a systematic and comparative identification of the biological characteristics of H3N2 canine influenza viruses (CIVs) isolated worldwide over 10 years. We found that, during adaptation in dogs, H3N2 CIVs became able to recognize the human-like SAα2,6-Gal receptor, showed gradually increased hemagglutination (HA) acid stability and replication ability in human airway epithelial cells, and acquired a 100% transmission rate via respiratory droplets in a ferret model. We also found that human populations lack immunity to H3N2 CIVs, and even preexisting immunity derived from the present human seasonal influenza viruses cannot provide protection against H3N2 CIVs. Our results showed that canines may serve as intermediates for the adaptation of avian influenza viruses to humans. Continuous surveillance coordinated with risk assessment for CIVs is necessary.

Published in eLife

ISSN: 2050-084X (Online)
Publisher: eLife Sciences Publications Ltd
Country of publisher: United Kingdom
LCC subjects: Medicine; Science: Biology (General)
Website: https://elifesciences.org

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