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
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
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.
