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Characterization of reassortant H1-subtype avian influenza viruses isolated from poultry in Zhejiang Province in China from 2013 to 2015

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Abstract

From 2013 to 2015, 32 H1-subtype avian influenza viruses (AIVs), H1N2 (n = 12), H1N3 (n = 14), H1N4 (n = 4) and H1N9 (n = 2), were isolated from poultry in Zhejiang Province in eastern China. These strains were characterized by whole-genome sequencing with subsequent phylogenetic analysis and genetic comparison. Phylogenetic analysis of all eight viral genes showed that these strains clustered in the AIV Eurasian lineage. These strains were found to be minimally pathogenic in mice and were able to replicate in mice without prior adaptation. Continued surveillance is needed, considering the important role of poultry in AIV reassortment.

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References

  1. Zhu X, Yu W, McBride R, Li Y, Chen LM, Donis RO, Tong S, Paulson JC, Wilson IA (2013) Hemagglutinin homologue from H17N10 bat influenza virus exhibits divergent receptor-binding and pH-dependent fusion activities. Proc Natl Acad Sci USA 110:1458–1463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X, Recuenco S, Gomez J, Chen LM, Johnson A, Tao Y, Dreyfus C, Yu W, McBride R, Carney PJ, Gilbert AT, Chang J, Guo Z, Davis CT, Paulson JC, Stevens J, Rupprecht CE, Holmes EC, Wilson IA, Donis RO (2013) New world bats harbor diverse influenza A viruses. PLoS Pathog 9:e1003657

    Article  PubMed  PubMed Central  Google Scholar 

  3. Kawaoka Y, Chambers TM, Sladen WL, Webster RG (1988) Is the gene pool of influenza viruses in shorebirds and gulls different from that in wild ducks? Virology 163:247–250

    Article  CAS  PubMed  Google Scholar 

  4. Gambaryan AS, Tuzikov AB, Pazynina GV, Desheva JA, Bovin NV, Matrosovich MN, Klimov AI (2008) 6-Sulfo sialyl Lewis X is the common receptor determinant recognized by H5, H6, H7 and H9 influenza viruses of terrestrial poultry. Virol J 5:85

    Article  PubMed  PubMed Central  Google Scholar 

  5. Liu M, He S, Walker D, Zhou N, Perez DR, Mo B, Li F, Huang X, Webster RG, Webby RJ (2003) The influenza virus gene pool in a poultry market in South central china. Virology 305:267–275

    Article  CAS  PubMed  Google Scholar 

  6. Cardona C, Yee K, Carpenter T (2009) Are live bird markets reservoirs of avian influenza? Poult Sci 88:856–859

    Article  CAS  PubMed  Google Scholar 

  7. Wu HB, Guo CT, Lu RF, Xu LH, Wo EK, You JB, Wang YT, Wang QG, Wu NP (2012) Genetic characterization of subtype H1 avian influenza viruses isolated from live poultry markets in Zhejiang Province, China, in 2011. Virus Genes 44:441–449

    Article  CAS  PubMed  Google Scholar 

  8. Hai-bo W, Chao-tan G, Ru-feng L, Li-hua X, En-kang W, Jin-biao Y, Yi-ting W, Qiao-gang W, Nan-ping W (2012) Characterization of a highly pathogenic H5N1 avian influenza virus isolated from ducks in Eastern China in 2011. Arch Virol 157:1131–1136

    Article  PubMed  Google Scholar 

  9. Kang HM, Jeong OM, Kim MC, Kwon JS, Paek MR, Choi JG, Lee EK, Kim YJ, Kwon JH, Lee YJ (2010) Surveillance of avian influenza virus in wild bird fecal samples from South Korea, 2003–2008. J Wildl Dis 46:878–888

    Article  CAS  PubMed  Google Scholar 

  10. Peng Y, Xie ZX, Liu JB, Pang YS, Deng XW, Xie ZQ, Xie LJ, Fan Q, Luo SS (2013) Epidemiological surveillance of low pathogenic avian influenza virus (LPAIV) from poultry in Guangxi Province, Southern China. PLoS One 8:e77132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Stincarelli M, Arvia R, De Marco MA, Clausi V, Corcioli F, Cotti C, Delogu M, Donatelli I, Azzi A, Giannecchini S (2013) Reassortment ability of the 2009 pandemic H1N1 influenza virus with circulating human and avian influenza viruses: public health risk implications. Virus Res 175:151–154

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  13. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Chen Y, Liang W, Yang S, Wu N, Gao H, Sheng J, Yao H, Wo J, Fang Q, Cui D, Li Y, Yao X, Zhang Y, Wu H, Zheng S, Diao H, Xia S, Chan KH, Tsoi HW, Teng JL, Song W, Wang P, Lau SY, Zheng M, Chan JF, To KK, Chen H, Li L, Yuen KY (2013) Human infections with the emerging avian influenza A H7N9 virus from wet market poultry: clinical analysis and characterisation of viral genome. Lancet 381:1916–1925

    Article  CAS  PubMed  Google Scholar 

  15. Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K, Xu X, Lu H, Zhu W, Gao Z, Xiang N, Shen Y, He Z, Gu Y, Zhang Z, Yang Y, Zhao X, Zhou L, Li X, Zou S, Zhang Y, Yang L, Guo J, Dong J, Li Q, Dong L, Zhu Y, Bai T, Wang S, Hao P, Yang W, Han J, Yu H, Li D, Gao GF, Wu G, Wang Y, Yuan Z, Shu Y (2013) Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med 368:1888–1897

    Article  CAS  PubMed  Google Scholar 

  16. Lam TT, Wang J, Shen Y, Zhou B, Duan L, Cheung CL, Ma C, Lycett SJ, Leung CY, Chen X, Li L, Hong W, Chai Y, Zhou L, Liang H, Ou Z, Liu Y, Farooqui A, Kelvin DJ, Poon LL, Smith DK, Pybus OG, Leung GM, Shu Y, Webster RG, Webby RJ, Peiris JS, Rambaut A, Zhu H, Guan Y (2013) The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature 502:241–244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Zhang Y, Zhu J, Li Y, Bradley KC, Cao J, Chen H, Jin M, Zhou H (2013) Glycosylation on hemagglutinin affects the virulence and pathogenicity of pandemic H1N1/2009 influenza A virus in mice. PLoS One 8:e61397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Bussey KA, Bousse TL, Desmet EA, Kim B, Takimoto T (2010) PB2 residue 271 plays a key role in enhanced polymerase activity of influenza A viruses in mammalian host cells. J Virol 84:4395–4406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Czudai-Matwich V, Otte A, Matrosovich M, Gabriel G, Klenk HD (2014) PB2 mutations D701N and S714R promote adaptation of an influenza H5N1 virus to a mammalian host. J Virol 88:8735–8742

    Article  PubMed  PubMed Central  Google Scholar 

  20. Wang J, Sun Y, Xu Q, Tan Y, Pu J, Yang H, Brown EG, Liu J (2012) Mouse-adapted H9N2 influenza A virus PB2 protein M147L and E627K mutations are critical for high virulence. PLoS One 7:e40752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Song W, Wang P, Mok BW, Lau SY, Huang X, Wu WL, Zheng M, Wen X, Yang S, Chen Y, Li L, Yuen KY, Chen H (2014) The K526R substitution in viral protein PB2 enhances the effects of E627K on influenza virus replication. Nat Commun 5:5509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Reed L, Muench H (1938) A simple method for estimating fifty percent endpoints. Am J Hyg 27:493–497

    Google Scholar 

  23. Medeiros R, Escriou N, Naffakh N, Manuguerra JC, van der Werf S (2001) Hemagglutinin residues of recent human A(H3N2) influenza viruses that contribute to the inability to agglutinate chicken erythrocytes. Virology 289:74–85

    Article  CAS  PubMed  Google Scholar 

  24. Liu Q, Zhou B, Ma W, Bawa B, Ma J, Wang W, Lang Y, Lyoo Y, Halpin RA, Lin X, Stockwell TB, Webby R, Wentworth DE, Richt JA (2014) Analysis of recombinant H7N9 wild-type and mutant viruses in pigs shows that the Q226L mutation in HA is important for transmission. J Virol 88:8153–8165

    Article  PubMed  PubMed Central  Google Scholar 

  25. Jin H, Wang D, Sun J, Cui Y, Chen G, Zhang X, Zhang J, Li X, Chai H, Gao Y, Li Y, Hua Y (2016) Pathogenesis and phylogenetic analyses of two avian influenza H7N1 viruses isolated from wild birds. Front Microbiol 7:1066

    PubMed  PubMed Central  Google Scholar 

  26. Chen H, Yuan H, Gao R, Zhang J, Wang D, Xiong Y, Fan G, Yang F, Li X, Zhou J, Zou S, Yang L, Chen T, Dong L, Bo H, Zhao X, Zhang Y, Lan Y, Bai T, Dong J, Li Q, Wang S, Li H, Gong T, Shi Y, Ni X, Li J, Fan J, Wu J, Zhou X, Hu M, Wan J, Yang W, Li D, Wu G, Feng Z, Gao GF, Wang Y, Jin Q, Liu M, Shu Y (2014) Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study. Lancet 383:714–721

    Article  PubMed  Google Scholar 

  27. Shi W, Shi Y, Wu Y, Liu D, Gao GF (2013) Origin and molecular characterization of the human-infecting H6N1 influenza virus in Taiwan. Protein Cell 4:846–853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hai-bo W, Ru-feng L, En-kang W, Jin-biao Y, Yi-ting W, Qiao-gang W, Li-hua X, Nan-ping W, Chao-tan G (2012) Sequence and phylogenetic analysis of H7N3 avian influenza viruses isolated from poultry in China in 2011. Arch Virol 157:2017–2021

    Article  PubMed  Google Scholar 

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Corresponding author

Correspondence to Nanping Wu.

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Funding

This study was funded by grants from the National Science Foundation of the People’s Republic of China (81502852), Zhejiang Provincial Natural Science Foundation of China (LY15H190003), and the Independent Task of State Key Laboratory for Diagnosis and Treatment of Infectious Diseases (Nos. 2016ZZ03 and 2017ZZ10).

Conflict of interest

The authors declare that they had no conflict of interest.

Ethical approval

The animal experiment was approved by the First Affiliated Hospital, School of Medicine, Zhejiang University (No. 2015-15).

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Wu, H., Lu, R., Peng, X. et al. Characterization of reassortant H1-subtype avian influenza viruses isolated from poultry in Zhejiang Province in China from 2013 to 2015. Arch Virol 162, 3493–3500 (2017). https://doi.org/10.1007/s00705-017-3487-x

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  • DOI: https://doi.org/10.1007/s00705-017-3487-x

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