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

  1. Mingyue Chen
  2. Yanli Lyu
  3. Fan Wu
  4. Ying Zhang
  5. Hongkui Li
  6. Rui Wang
  7. Yang Liu
  8. Xinyu Yang
  9. Liwei Zhou
  10. Ming Zhang
  11. Qi Tong
  12. Honglei Sun
  13. Juan Pu
  14. Jinhua Liu
  15. Yipeng Sun  Is a corresponding author
  1. China Agricultural University, China
  2. Chinese PLA General Hospital, China
  3. Liaoning Agricultural Development Service Center, China
  4. University of Georgia, United States

Abstract

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 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.

Data availability

Sequencing data have been deposited in GenBank under accession codes ON877531-ON878058.

The following data sets were generated
    1. Sun Y
    2. Chen M
    (2022) Primer sequences
    Dryad Digital Repository, doi:10.5061/dryad.4qrfj6qdf.

Article and author information

Author details

  1. Mingyue Chen

    National Key Laboratory of Veterinary Public Health Security, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Yanli Lyu

    National Key Laboratory of Veterinary Public Health Security, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Fan Wu

    National Key Laboratory of Veterinary Public Health Security, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Ying Zhang

    Department of Laboratory Medicine, Chinese PLA General Hospital, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Hongkui Li

    Liaoning Agricultural Development Service Center, Shenyang, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Rui Wang

    National Key Laboratory of Veterinary Public Health Security, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Yang Liu

    Veterinary Teaching Hospital, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Xinyu Yang

    National Key Laboratory of Veterinary Public Health Security, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Liwei Zhou

    National Key Laboratory of Veterinary Public Health Security, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Ming Zhang

    Department of Epidemiology and Biostatistics, University of Georgia, Athens, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Qi Tong

    National Key Laboratory of Veterinary Public Health Security, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  12. Honglei Sun

    National Key Laboratory of Veterinary Public Health Security, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  13. Juan Pu

    National Key Laboratory of Veterinary Public Health Security, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  14. Jinhua Liu

    National Key Laboratory of Veterinary Public Health Security, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  15. Yipeng Sun

    National Key Laboratory of Veterinary Public Health Security, China Agricultural University, Beijing, China
    For correspondence
    sypcau@163.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9399-0039

Funding

National Natural Science Foundation of China (Grant No. 32172838)

  • Yipeng Sun

National Natural Science Foundation of China (Grant No. 32192451)

  • Jinhua Liu

Higher Education Discipline Innovation Project (111 Project)

  • Yipeng Sun

This work was supported by the National Natural Science Foundation of China (32172838 and 32192451) and the 111 Project

Ethics

Animal experimentation: All experiments with live viruses were performed in animal biosafety level 2 (ABSL-2) environments. The present study was carried out in accordance with the Guide for the Care and Use of Laboratory Animals of the Ministry of Science and Technology of the People's Republic of China. The protocols for the animal studies were approved by the Committee on the Ethics of Laboratory Animals of China Agricultural University (approval SKLAB-B-2010-003).

Copyright

© 2023, Chen et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Mingyue Chen
  2. Yanli Lyu
  3. Fan Wu
  4. Ying Zhang
  5. Hongkui Li
  6. Rui Wang
  7. Yang Liu
  8. Xinyu Yang
  9. Liwei Zhou
  10. Ming Zhang
  11. Qi Tong
  12. Honglei Sun
  13. Juan Pu
  14. Jinhua Liu
  15. Yipeng Sun
(2023)
Increased public health threat of avian-origin H3N2 influenza virus caused by its evolution in dogs
eLife 12:e83470.
https://doi.org/10.7554/eLife.83470

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https://doi.org/10.7554/eLife.83470