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Genetic characterization of canine influenza A virus (H3N2) in Thailand

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Abstract

In January 2012, several clinical cases of dogs with flu-like symptoms, including coughing, sneezing, nasal discharge, and fever, were reported in a small-animal hospital located in Bangkok, Thailand. One influenza A virus was identified and characterized as an avian-like influenza virus H3N2. The virus was named A/canine/Thailand/CU-DC5299/12. A phylogenetic analysis indicated that the canine virus belonged to an avian Eurasian lineage and was genetically related to the canine influenza viruses H3N2 from China and Korea. This canine virus displays a unique genetic signature with two amino acid insertions in the NA protein, which is similar to the canine influenza viruses from eastern China (Zhejiang and Jiangsu). This study constitutes the first report of H3N2 canine influenza virus infection in a small-animal hospital in Thailand.

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References

  1. P.C. Crawford, E.J. Dubovi, W.L. Castleman, I. Stephenson, E.P. Gibbs, L. Chen, C. Smith, R.C. Hill, P. Ferro, J. Pompey, R.A. Bright, M.J. Medina, C.M. Johnson, C.W. Olsen, N.J. Cox, A.I. Klimov, J.M. Katz, R.O. Donis, Transmission of equine influenza virus to dogs. Science 310(5747), 482–485 (2005)

    Article  CAS  PubMed  Google Scholar 

  2. D. Song, B. Kang, C. Lee, K. Jung, G. Ha, D. Kang, S. Park, B. Park, J. Oh, Transmission of avian influenza virus (H3N2) to dogs. Emerg. Infect. Dis. 14(5), 741–746 (2008)

    Article  PubMed  Google Scholar 

  3. G.J. Zhan, Z.S. Ling, Y.L. Zhu, S.J. Jiang, Z.J. Xie, Genetic characterization of a novel influenza A virus H5N2 isolated from a dog in China. Vet. Microbiol. 155(2–4), 409–416 (2012)

    CAS  PubMed  Google Scholar 

  4. D. Song, C. Lee, B. Kang, K. Jung, T. Oh, H. Kim, B. Park, J. Oh, Experimental infection of dogs with avian-origin canine influenza A virus (H3N2). Emerg. Infect. Dis. 15(1), 56–58 (2009)

    Article  PubMed  Google Scholar 

  5. D.S. Song, D.J. An, H.J. Moon, M.J. Yeom, H.Y. Jeong, W.S. Jeong, S.J. Park, H.K. Kim, S.Y. Han, J.S. Oh, B.K. Park, J.K. Kim, H. Poo, R.G. Webster, K. Jung, B.K. Kang, Interspecies transmission of the canine influenza H3N2 virus to domestic cats in South Korea. J. Gen. Virol. 92(Pt 10), 2350–2355 (2011)

    Article  CAS  PubMed  Google Scholar 

  6. C. Lee, D. Song, B. Kang, D. Kang, J. Yoo, K. Jung, G. Na, K. Lee, B. Park, J. Oh, A serological survey of avian origin canine H3N2 influenza virus in dogs in Korea. Vet. Microbiol. 137(3–4), 359–362 (2009)

    Article  PubMed  Google Scholar 

  7. D. Song, H.J. Moon, D.J. An, H.Y. Jeoung, H. Kim, M.J. Yeom, M. Hong, J.H. Nam, S.J. Park, B.K. Park, J.S. Oh, M. Song, R.G. Webster, J.K. Kim, B.K. Kang, A novel reassortant canine H3N1 influenza virus between pandemic H1N1 and canine H3N2 influenza viruses in Korea. J. Gen. Virol. 93(Pt 3), 551–554 (2012)

    Article  CAS  PubMed  Google Scholar 

  8. S. Li, Z. Shi, P. Jiao, G. Zhang, Z. Zhong, W. Tian, L.P. Long, Z. Cai, X. Zhu, M. Liao, X.F. Wan, Avian-origin H3N2 canine influenza A viruses in southern China. Infect. Genet. Evol. 10(8), 1286–1288 (2010)

    Article  PubMed Central  PubMed  Google Scholar 

  9. Y. Lin, Y.B. Zhao, X.J. Zeng, C.P. Lu, Y.J. Liu, Complete genome sequence of an H3N2 canine influenza virus from dogs in Jiangsu, China. J. Virol. 86(20), 11402 (2012)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. T. Songserm, A. Amonsin, R. Jam-on, N. Sae-Heng, N. Pariyothorn, S. Payungporn, A. Theamboonlers, S. Chutinimitkul, R. Thanawongnuwech, Y. Poovorawan, Fatal avian influenza A H5N1 in a dog. Emerg. Infect. Dis. 12(11), 1744–1747 (2006)

    Article  PubMed  Google Scholar 

  11. A. Amonsin, T. Songserm, S. Chutinimitkul, R. Jam-On, N. Sae-Heng, N. Pariyothorn, S. Payungporn, A. Theamboonlers, Y. Poovorawan, Genetic analysis of influenza A virus (H5N1) derived from domestic cat and dog in Thailand. Arch. Virol. 152(10), 1925–1933 (2007)

    Article  CAS  PubMed  Google Scholar 

  12. T. Songsermn, A. Amonsin, R. Jam-on, N. Sae-Heng, N. Meemak, N. Pariyothorn, S. Payungporn, A. Theamboonlers, Y. Poovorawan, Avian influenza H5N1 in naturally infected domestic cat. Emerg. Infect. Dis. 12(4), 681–683 (2006)

    Article  Google Scholar 

  13. R. Thanawongnuwech, A. Amonsin, R. Tantilertcharoen, S. Damrongwatanapokin, A. Theamboonlers, S. Payungporn, K. Nanthapornphiphat, S. Ratanamungklanon, E. Tunak, T. Songserm, V. Vivatthanavanich, T. Lekdumrongsak, S. Kesdangsakonwut, S. Tunhikorn, Y. Poovorawan, Probable tiger-to-tiger transmission of avian influenza H5N1. Emerg. Infect. Dis. 11(5), 699–701 (2005)

    Article  PubMed  Google Scholar 

  14. P. De Benedictis, T.C. Anderson, A. Perez, E. Viale, C. Veggiato, S. Tiozzo Caenazzo, P.C. Crawford, I. Capua, A diagnostic algorithm for detection of antibodies to influenza A viruses in dogs in Italy (2006–2008). J. Vet. Diagn. Invest. 22(6), 914–920 (2010)

    Article  PubMed  Google Scholar 

  15. W.G. Dundon, P. De Benedictis, E. Viale, I. Capua, Serologic evidence of pandemic (H1N1) 2009 infection in dogs, Italy. Emerg. Infect. Dis. 16(12), 2019–2021 (2010)

    Article  PubMed  Google Scholar 

  16. E. Spackman, D.A. Senne, T.J. Myers, L.L. Bulaga, L.P. Garber, M.L. Perdue, K. Lohman, L.T. Daum, D.L. Suarez, Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the avian H5 and H7 hemagglutinin subtypes. J. Clin. Microbiol. 40(9), 3256–3260 (2002)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. K. Tsukamoto, H. Ashizawa, K. Nakanishi, N. Kaji, K. Suzuki, M. Okamatsu, S. Yamaguchi, M. Mase, Subtyping of avian influenza viruses H1 to H15 on the basis of hemagglutinin genes by PCR assay and molecular determination of pathogenic potential. J. Clin. Microbiol. 46(9), 3048–3055 (2008)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. K. Tsukamoto, T. Ashizawa, K. Nakanishi, N. Kaji, K. Suzuki, M. Shishido, M. Okamatsu, M. Mase, Use of reverse transcriptase PCR to subtype N1 to N9 neuraminidase genes of avian influenza viruses. J. Clin. Microbiol. 47(7), 2301–2303 (2009)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. E. Hoffmann, J. Stech, Y. Guan, R.G. Webster, D.R. Perez, Universal primer set for the full-length amplification of all influenza A viruses. Arch. Virol. 146(12), 2275–2289 (2001)

    Article  CAS  PubMed  Google Scholar 

  20. K. Tamura, J. Dudley, M. Nei, S. Kumar, MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24(8), 1596–1599 (2007)

    Article  CAS  PubMed  Google Scholar 

  21. J.P. Huelsenbeck, F. Ronquist, MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8), 754–755 (2001)

    Article  CAS  PubMed  Google Scholar 

  22. A.J. Caton, G.G. Brownlee, J.W. Yewdell, W. Gerhard, The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell 31(2 Pt 1), 417–427 (1982)

    Article  CAS  PubMed  Google Scholar 

  23. K. Nakajima, E. Nobusawa, K. Tonegawa, S. Nakajima, Restriction of amino acid change in influenza A virus H3HA: comparison of amino acid changes observed in nature and in vitro. J. Virol. 77(18), 10088–10098 (2003)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. D.A. Steinhauer, Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology 258(1), 1–20 (1999)

    Article  CAS  PubMed  Google Scholar 

  25. I.A. Wilson, N.J. Cox, Structural basis of immune recognition of influenza virus hemagglutinin. Annu. Rev. Immunol. 8, 737–771 (1990)

    Article  CAS  PubMed  Google Scholar 

  26. A.C. Shih, T.C. Hsiao, M.S. Ho, W.H. Li, Simultaneous amino acid substitutions at antigenic sites drive influenza A hemagglutinin evolution. Proc. Natl. Acad. Sci. USA 104(15), 6283–6288 (2007)

    Article  CAS  PubMed  Google Scholar 

  27. I.T. Schulze, Effects of glycosylation on the properties and functions of influenza virus hemagglutinin. J. Infect. Dis. 176(Suppl 1), S24–S28 (1997)

    Article  PubMed  Google Scholar 

  28. L.J. Mitnaul, M.N. Matrosovich, M.R. Castrucci, A.B. Tuzikov, N.V. Bovin, D. Kobasa, Y. Kawaoka, Balanced hemagglutinin and neuraminidase activities are critical for efficient replication of influenza A virus. J. Virol. 74(13), 6015–6020 (2000)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. G.M. Air, M.C. Els, L.E. Brown, W.G. Laver, R.G. Webster, Location of antigenic sites on the three-dimensional structure of the influenza N2 virus neuraminidase. Virology 145(2), 237–248 (1985)

    Article  CAS  PubMed  Google Scholar 

  30. P.M. Colman, J.N. Varghese, W.G. Laver, Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature 303(5912), 41–44 (1983)

    Article  CAS  PubMed  Google Scholar 

  31. J. Li, H. zu Dohna, N.L. Anchell, S.C. Adams, N.T. Dao, Z. Xing, C.J. Cardona, Adaptation and transmission of a duck-origin avian influenza virus in poultry species. Virus Res. 147(1), 40–46 (2010)

    Article  CAS  PubMed  Google Scholar 

  32. J. Li, H. Zu Dohna, C.J. Cardona, J. Miller, T.E. Carpenter, Emergence and genetic variation of neuraminidase stalk deletions in avian influenza viruses. PLoS ONE 6(2), e14722 (2011)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. M.R. Castrucci, Y. Kawaoka, Biologic importance of neuraminidase stalk length in influenza A virus. J. Virol. 67(2), 759–764 (1993)

    CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This study has been funded in whole with federal funds from the National Institute of Allergy and Infectious Disease, National Institute of Health, Department of Health and Human Services, under Contract No. HHSN266200700007c. The study contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIH. The authors would like to thank Chulalongkorn University for its financial support in the Center of Excellence for Emerging and Re-emerging Infectious Diseases in Animals. The authors would like to thank also the National Research University of CHE and the Ratchadaphiseksomphot Endowment Fund of Chulalongkorn University (HR1155A and RES560530129) for the grant of support to AA. The authors would like to thank Ms. Petra Hirsch for reviewing the manuscript.

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The authors declare that they have no conflict of interests.

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Correspondence to Alongkorn Amonsin.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11262_2013_978_MOESM1_ESM.pptx

Phylogenetic analysis of the six internal genes of influenza A viruses. The Thai canine influenza H3N2 virus is presented as a circle. Supplementary material 1 (PPTX 256 kb)

11262_2013_978_MOESM2_ESM.pptx

The deduced amino acid sequences of the HA1 protein of a Thai canine influenza H3N2 viruses compared with canine, feline and avian H3N2 viruses. Supplementary material 2 (PPTX 620 kb)

11262_2013_978_MOESM3_ESM.pptx

The deduced amino acid sequences at the NA protein of a Thai canine influenza H3N2 viruses compared with canine, feline and avian H3N2 viruses. Supplementary material 3 (PPTX 731 kb)

11262_2013_978_MOESM4_ESM.docx

Nucleotide and amino acid identities (%) of the Thai canine H3N2 virus (CU-DC5299) compared with reference viruses. Supplementary material 4 (DOCX 100 kb)

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Bunpapong, N., Nonthabenjawan, N., Chaiwong, S. et al. Genetic characterization of canine influenza A virus (H3N2) in Thailand. Virus Genes 48, 56–63 (2014). https://doi.org/10.1007/s11262-013-0978-z

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  • DOI: https://doi.org/10.1007/s11262-013-0978-z

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