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Molecular characterization of H10 subtype avian influenza viruses isolated from poultry in Eastern China

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Abstract

In recent years, avian-origin H10 influenza viruses have proved capable of infecting human beings, and they pose a potential public health threat. Seven H10 avian influenza viruses (AIVs), H10N3 (n = 2), H10N7 (n = 1), and H10N8 (n = 4), were isolated from chickens in Zhejiang Province, Eastern China, during surveillance of AIVs in live poultry markets in 2016 and 2017. Phylogenetic analysis indicated that Zhejiang H10 strains received gene segments from H10, H3, and H7 viruses from birds in East Asia. Animal inoculation tests showed that these isolates have low pathogenicity in mice and can replicate in this species. Our findings suggest these H10 AIVs have the ability to adapt to chicken or other poultry, and highlight the need of long-term surveillance.

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References

  1. Wu H, Lu R, Wu X, Peng X, Xu L, Cheng L, Lu X, Jin C, Xie T, Yao H, Wu N (2015) Novel reassortant H10N7 avian influenza viruses isolated from chickens in Eastern China. J Clin Virol 65:58–61

    Article  PubMed  CAS  Google Scholar 

  2. Zhang M, Zhang X, Xu K, Teng Q, Liu Q, Li X, Yang J, Xu J, Chen H, Li Z (2016) Characterization of the Pathogenesis of H10N3, H10N7, and H10N8 Subtype Avian Influenza Viruses Circulating in Ducks. Sci Rep 6:34489

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Wu H, Lu R, Wu X, Peng X, Xu L, Cheng L, Lu X, Jin C, Xie T, Yao H, Wu N (2015) Isolation and characterization of a novel H10N2 avian influenza virus from a domestic duck in Eastern China. Infect Genet Evol 29:1–5

    Article  PubMed  Google Scholar 

  4. Ma C, Lam TT, Chai Y, Wang J, Fan X, Hong W, Zhang Y, Li L, Liu Y, Smith DK, Webby RJ, Peiris JS, Zhu H, Guan Y (2015) Emergence and evolution of H10 subtype influenza viruses in poultry in China. J Virol 89:3534–3541

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Su C, Chen S, Liu X, Xu J, Huang K, Liu K, Huang J, Peng D (2013) Genome sequence of a novel H10N9 avian influenza virus isolated from chickens in a live poultry market in Eastern China. Genome Announc 1:e00386

    PubMed  PubMed Central  Google Scholar 

  6. Abolnik C, Gerdes GH, Sinclair M, Ganzevoort BW, Kitching JP, Burger CE, Romito M, Dreyer M, Swanepoel S, Cumming GS, Olivier AJ (2010) Phylogenetic analysis of influenza A viruses (H6N8, H1N8, H4N2, H9N2, H10N7) isolated from wild birds, ducks, and ostriches in South Africa from 2007 to 2009. Avian Dis 54:313–322

    Article  PubMed  Google Scholar 

  7. Karunakaran D, Hinshaw V, Poss P, Newman J, Halvorson D (1983) Influenza A outbreaks in Minnesota turkeys due to subtype H10N7 and possible transmission by waterfowl. Avian Dis 27:357–366

    Article  PubMed  CAS  Google Scholar 

  8. Ni X, He F, Hu M, Zhou X, Wang B, Feng C, Wu Y, Li Y, Tu J, Li H, Liu M, Chen H, Chen S (2015) Investigation of avian influenza virus in poultry and wild birds due to novel avian-origin influenza A(H10N8) in Nanchang City, China. Microbes Infect 17:48–53

    Article  PubMed  Google Scholar 

  9. Deng G, Shi J, Wang J, Kong H, Cui P, Zhang F, Tan D, Suzuki Y, Liu L, Jiang Y, Guan Y, Chen H (2015) Genetics, receptor binding, and virulence in mice of H10N8 influenza viruses isolated from ducks and chickens in live poultry markets in China. J Virol 89:6506–6510

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Englund L (2000) Studies on influenza viruses H10N4 and H10N7 of avian origin in mink. Vet Microbiol 74:101–107

    Article  PubMed  CAS  Google Scholar 

  11. Krog JS, Hansen MS, Holm E, Hjulsager CK, Chriel M, Pedersen K, Andresen LO, Abildstrom M, Jensen TH, Larsen LE (2015) Influenza A(H10N7) virus in dead harbor seals, Denmark. Emerg Infect Dis 21:684–687

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Wang N, Zou W, Yang Y, Guo X, Hua Y, Zhang Q, Zhao Z, Jin M (2012) Complete genome sequence of an H10N5 avian influenza virus isolated from pigs in central China. J Virol 86:13865–13866

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Arzey GG, Kirkland PD, Arzey KE, Frost M, Maywood P, Conaty S, Hurt AC, Deng YM, Iannello P, Barr I, Dwyer DE, Ratnamohan M, McPhie K, Selleck P (2012) Influenza virus A (H10N7) in chickens and poultry abattoir workers, Australia. Emerg Infect Dis 18:814–816

    Article  PubMed  PubMed Central  Google Scholar 

  14. 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 

  15. Jiao P, Cao L, Yuan R, Wei L, Song Y, Shen D, Gong L, Luo K, Ren T, Liao M (2012) Complete genome sequence of an H10N8 avian influenza virus isolated from a live bird market in Southern China. J Virol 86:7716

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. 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  PubMed  PubMed Central  CAS  Google Scholar 

  17. 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  PubMed  CAS  Google Scholar 

  18. Wu H, Peng X, Cheng L, Wu N (2015) Molecular characterization of novel reassortant H6N2 subtype avian influenza viruses isolated from poultry in Eastern China, in 2014. Infect Genet Evol 36:41–45

    Article  PubMed  CAS  Google Scholar 

  19. Wu H, Lu R, Peng X, Cheng L, Liu F, Wu N (2017) Characterization of novel reassortant influenza A (H5N2) viruses isolated from poultry in Eastern China, 2015. Front Microbiol 8:741

    Article  PubMed  PubMed Central  Google Scholar 

  20. 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  PubMed  CAS  Google Scholar 

  21. Bao Y, Bolotov P, Dernovoy D, Kiryutin B, Zaslavsky L, Tatusova T, Ostell J, Lipman D (2008) The influenza virus resource at the National Center for Biotechnology Information. J Virol 82:596–601

    Article  PubMed  CAS  Google Scholar 

  22. 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  PubMed  PubMed Central  CAS  Google Scholar 

  23. Gupta R JEaBS (2004) Prediction of N-glycosylation sites in human proteins; 2004. Database: NetNGlyc 1.0 [Internet]

  24. Tewawong N, Prachayangprecha S, Vichiwattana P, Korkong S, Klinfueng S, Vongpunsawad S, Thongmee T, Theamboonlers A, Poovorawan Y (2015) Assessing antigenic drift of seasonal influenza A (H3N2) and A(H1N1)pdm09 viruses. PLoS One 10:e0139958

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Suptawiwat O, Kongchanagul A, Chan-It W, Thitithanyanont A, Wiriyarat W, Chaichuen K, Songserm T, Suzuki Y, Puthavathana P, Auewarakul P (2008) A simple screening assay for receptor switching of avian influenza viruses. J Clin Virol 42:186–189

    Article  PubMed  CAS  Google Scholar 

  26. Zou S, Gao R, Zhang Y, Li X, Chen W, Bai T, Dong L, Wang D, Shu Y (2016) Molecular characterization of H6 subtype influenza viruses in southern China from 2009 to 2011. Emerg Microbes Infect 5:e73

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. 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  PubMed  CAS  Google Scholar 

  28. 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  CAS  Google Scholar 

  29. 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 

  30. Cao X, Yang F, Wu H, Xu L (2017) Genetic characterization of novel reassortant H5N6-subtype influenza viruses isolated from cats in eastern China. Arch Virol 162:3501–3505

    Article  PubMed  CAS  Google Scholar 

  31. Chang H, Dai F, Liu Z, Yuan F, Zhao S, Xiang X, Zou F, Zeng B, Fan Y, Duan G (2014) Seroprevalence survey of avian influenza A (H5) in wild migratory birds in Yunnan Province, Southwestern China. Virol J 11:18

    Article  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  33. Fouchier RA, Schneeberger PM, Rozendaal FW, Broekman JM, Kemink SA, Munster V, Kuiken T, Rimmelzwaan GF, Schutten M, Van Doornum GJ, Koch G, Bosman A, Koopmans M, Osterhaus AD (2004) Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci U S A 101:1356–1361

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Puzelli S, Rossini G, Facchini M, Vaccari G, Di Trani L, Di Martino A, Gaibani P, Vocale C, Cattoli G, Bennett M, McCauley JW, Rezza G, Moro ML, Rangoni R, Finarelli AC, Landini MP, Castrucci MR, Donatelli I (2014) Human infection with highly pathogenic A(H7N7) avian influenza virus, Italy, 2013. Emerg Infect Dis 20:1745–1749

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Wu H, Peng X, Xu L, Jin C, Cheng L, Lu X, Xie T, Yao H, Wu N (2014) Novel reassortant influenza A(H5N8) viruses in domestic ducks, eastern China. Emerg Infect Dis 20:1315–1318

    PubMed  PubMed Central  CAS  Google Scholar 

  36. Li M, Liu H, Bi Y, Sun J, Wong G, Liu D, Li L, Liu J, Chen Q, Wang H, He Y, Shi W, Gao GF, Chen J (2017) Highly pathogenic avian influenza A (H5N8) virus in wild migratory birds, Qinghai Lake. China, Emerg Infect Dis, p 23

    Google Scholar 

  37. Lee YJ, Kang HM, Lee EK, Song BM, Jeong J, Kwon YK, Kim HR, Lee KJ, Hong MS, Jang I, Choi KS, Kim JY, Lee HJ, Kang MS, Jeong OM, Baek JH, Joo YS, Park YH, Lee HS (2014) Novel reassortant influenza A(H5N8) viruses, South Korea, 2014. Emerg Infect Dis 20:1087–1089

    PubMed  PubMed Central  Google Scholar 

  38. Si YJ, Choi WS, Kim YI, Lee IW, Kwon HI, Park SJ, Kim EH, Kim SM, Kwon JJ, Song MS, Kim CJ, Choi YK (2016) Genetic characteristics of highly pathogenic H5N8 avian influenza viruses isolated from migratory wild birds in South Korea during 2014-2015. Arch Virol 161:2749–2764

    Article  PubMed  CAS  Google Scholar 

  39. Usui T, Soda K, Tomioka Y, Ito H, Yabuta T, Takakuwa H, Otsuki K, Ito T, Yamaguchi T (2016) Characterization of clade 2.3.4.4 H5N8 highly pathogenic avian influenza viruses from wild birds possessing atypical hemagglutinin polybasic cleavage sites. Virus Genes 53:44–51

    Article  PubMed  CAS  Google Scholar 

  40. Tanikawa T, Kanehira K, Tsunekuni R, Uchida Y, Takemae N, Saito T (2016) Pathogenicity of H5N8 highly pathogenic avian influenza viruses isolated from a wild bird fecal specimen and a chicken in Japan in 2014. Microbiol Immunol 60:243–252

    Article  PubMed  CAS  Google Scholar 

  41. Bouwstra RJ, Koch G, Heutink R, Harders F, van der Spek A, Elbers AR, Bossers A (2015) Phylogenetic analysis of highly pathogenic avian influenza A(H5N8) virus outbreak strains provides evidence for four separate introductions and one between-poultry farm transmission in the Netherlands, November 2014. Euro Surveill 20:21174

    Article  PubMed  Google Scholar 

  42. Adlhoch C, Gossner C, Koch G, Brown I, Bouwstra R, Verdonck F, Penttinen P, Harder T (2014) Comparing introduction to Europe of highly pathogenic avian influenza viruses A(H5N8) in 2014 and A(H5N1) in 2005. Euro Surveill 19:20996

    PubMed  CAS  Google Scholar 

  43. Lee DH, Sharshov K, Swayne DE, Kurskaya O, Sobolev I, Kabilov M, Alekseev A, Irza V, Shestopalov A (2017) Novel Reassortant Clade 2.3.4.4 Avian influenza A(H5N8) virus in wild aquatic Birds, Russia, 2016. Emerg Infect Dis 23:359–360

    Article  PubMed  PubMed Central  Google Scholar 

  44. Lee DH, Torchetti MK, Winker K, Ip HS, Song CS, Swayne DE (2015) Intercontinental spread of Asian-Origin H5N8 to North America through Beringia by migratory birds. J Virol 89:6521–6524

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Jhung MA, Nelson DI (2015) Outbreaks of avian influenza A (H5N2), (H5N8), and (H5N1) among birds—United States, December 2014-January 2015. MMWR Morb Mortal Wkly Rep 64:111

    PubMed  PubMed Central  Google Scholar 

  46. Stoute S, Chin R, Crossley B, Gabriel Senties-Cue C, Bickford A, Pantin-Jackwood M, Breitmeyer R, Jones A, Carnaccini S, Shivaprasad HL (2016) Highly pathogenic Eurasian H5N8 avian influenza outbreaks in two commercial poultry flocks in California. Avian Dis 60:688–693

    Article  PubMed  Google Scholar 

  47. Zhang H, Xu B, Chen Q, Chen J, Chen Z (2011) Characterization of an H10N8 influenza virus isolated from Dongting lake wetland. Virol J 8:42

    Article  PubMed  PubMed Central  Google Scholar 

  48. Matrosovich MN, Gambaryan AS, Teneberg S, Piskarev VE, Yamnikova SS, Lvov DK, Robertson JS, Karlsson KA (1997) Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology 233:224–234

    Article  PubMed  CAS  Google Scholar 

  49. Tzarum N, de Vries RP, Zhu X, Yu W, McBride R, Paulson JC, Wilson IA (2015) Structure and receptor binding of the hemagglutinin from a human H6N1 influenza virus. Cell Host Microbe 17:369–376

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Wei SH, Yang JR, Wu HS, Chang MC, Lin JS, Lin CY, Liu YL, Lo YC, Yang CH, Chuang JH, Lin MC, Chung WC, Liao CH, Lee MS, Huang WT, Chen PJ, Liu MT, Chang FY (2013) Human infection with avian influenza A H6N1 virus: an epidemiological analysis. Lancet Respir Med 1:771–778

    Article  PubMed  Google Scholar 

  51. Brookes DW, Miah S, Lackenby A, Hartgroves L, Barclay WS (2011) Pandemic H1N1 2009 influenza virus with the H275Y oseltamivir resistance neuraminidase mutation shows a small compromise in enzyme activity and viral fitness. J Antimicrob Chemother 66:466–470

    Article  PubMed  CAS  Google Scholar 

  52. Wang B, Dwyer DE, Blyth CC, Soedjono M, Shi H, Kesson A, Ratnamohan M, McPhie K, Cunningham AL, Saksena NK (2010) Detection of the rapid emergence of the H275Y mutation associated with oseltamivir resistance in severe pandemic influenza virus A/H1N1 09 infections. Antiviral Res 87:16–21

    Article  PubMed  CAS  Google Scholar 

  53. Durrant MG, Eggett DL, Busath DD (2015) Investigation of a recent rise of dual amantadine-resistance mutations in the influenza A M2 sequence. BMC Genet 16(Suppl 2):S3

    Article  PubMed  PubMed Central  Google Scholar 

  54. Schat KA, Bingham J, Butler JM, Chen LM, Lowther S, Crowley TM, Moore RJ, Donis RO, Lowenthal JW (2012) Role of position 627 of PB2 and the multibasic cleavage site of the hemagglutinin in the virulence of H5N1 avian influenza virus in chickens and ducks. PLoS One 7:e30960

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. 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  PubMed  PubMed Central  CAS  Google Scholar 

  56. 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  PubMed  PubMed Central  CAS  Google Scholar 

  57. Suptawiwat O, Boonarkart C, Chakritbudsabong W, Uiprasertkul M, Puthavathana P, Wiriyarat W, Auewarakul P (2015) The N-linked glycosylation site at position 158 on the head of hemagglutinin and the virulence of H5N1 avian influenza virus in mice. Arch Virol 160:409–415

    Article  PubMed  CAS  Google Scholar 

  58. Xiong X, McCauley JW, Steinhauer DA (2014) Receptor binding properties of the influenza virus hemagglutinin as a determinant of host range. Curr Top Microbiol Immunol 385:63–91

    PubMed  Google Scholar 

  59. Klimov A, Balish A, Veguilla V, Sun H, Schiffer J, Lu X, Katz JM, Hancock K (2012) Influenza virus titration, antigenic characterization, and serological methods for antibody detection. Methods Mol Biol 865:25–51

    Article  PubMed  CAS  Google Scholar 

  60. Li KS, Guan Y, Wang J, Smith GJ, Xu KM, Duan L, Rahardjo AP, Puthavathana P, Buranathai C, Nguyen TD, Estoepangestie AT, Chaisingh A, Auewarakul P, Long HT, Hanh NT, Webby RJ, Poon LL, Chen H, Shortridge KF, Yuen KY, Webster RG, Peiris JS (2004) Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 430:209–213

    Article  PubMed  CAS  Google Scholar 

  61. Koopmans M, Wilbrink B, Conyn M, Natrop G, van der Nat H, Vennema H, Meijer A, van Steenbergen J, Fouchier R, Osterhaus A, Bosman A (2004) Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. Lancet 363:587–593

    Article  PubMed  Google Scholar 

  62. Zhang T, Bi Y, Tian H, Li X, Liu D, Wu Y, Jin T, Wang Y, Chen Q, Chen Z, Chang J, Gao GF, Xu B (2014) Human infection with influenza virus A(H10N8) from live poultry markets, China, 2014. Emerg Infect Dis 20:2076–2079

    PubMed  PubMed Central  CAS  Google Scholar 

  63. To KK, Tsang AK, Chan JF, Cheng VC, Chen H, Yuen KY (2014) Emergence in China of human disease due to avian influenza A(H10N8)—cause for concern? J Infect 68:205–215

    Article  PubMed  Google Scholar 

  64. Xu Y, Cao H, Liu H, Sun H, Martin B, Zhao Y, Wang Q, Deng G, Xue J, Zong Y, Zhu J, Wen F, Long LP, Wong SS, Zhao N, Fu X, Liao M, Hu G, Webby R, Gao GF, Wan XF (2015) Identification of the source of A (H10N8) virus causing human infection. Infect Genet Evol 30:159–163

    Article  PubMed  CAS  Google Scholar 

  65. Qi W, Zhou X, Shi W, Huang L, Xia W, Liu D, Li H, Chen S, Lei F, Cao L, Wu J, He F, Song W, Li Q, Liao M, Liu M (2014) Genesis of the novel human-infecting influenza A(H10N8) virus and potential genetic diversity of the virus in poultry. China. Euro Surveill 19:20841

    Article  PubMed  Google Scholar 

  66. Su S, Qi W, Zhou P, Xiao C, Yan Z, Cui J, Jia K, Zhang G, Gray GC, Liao M, Li S (2014) First evidence of H10N8 Avian influenza virus infections among feral dogs in live poultry markets in Guangdong province, China. Clin Infect Dis 59:748–750

    Article  PubMed  Google Scholar 

  67. Wang M, Zhang W, Qi J, Wang F, Zhou J, Bi Y, Wu Y, Sun H, Liu J, Huang C, Li X, Yan J, Shu Y, Shi Y, Gao GF (2015) Structural basis for preferential avian receptor binding by the human-infecting H10N8 avian influenza virus. Nat Commun 6:5600

    Article  PubMed  CAS  Google Scholar 

  68. Shinya K, Hamm S, Hatta M, Ito H, Ito T, Kawaoka Y (2004) PB2 amino acid at position 627 affects replicative efficiency, but not cell tropism, of Hong Kong H5N1 influenza A viruses in mice. Virology 320:258–266

    Article  PubMed  CAS  Google Scholar 

  69. Ping J, Dankar SK, Forbes NE, Keleta L, Zhou Y, Tyler S, Brown EG (2010) PB2 and hemagglutinin mutations are major determinants of host range and virulence in mouse-adapted influenza A virus. J Virol 84:10606–10618

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Tan L, Su S, Smith DK, He S, Zheng Y, Shao Z, Ma J, Zhu H, Zhang G (2014) A combination of HA and PA mutations enhances virulence in a mouse-adapted H6N6 influenza A virus. J Virol 88:14116–14125

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. 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  PubMed  PubMed Central  CAS  Google Scholar 

  72. Wang C, Lee HH, Yang ZF, Mok CK, Zhang Z (2016) PB2-Q591K mutation determines the pathogenicity of avian H9N2 influenza viruses for mammalian species. PLoS One 11:e0162163

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Mok CK, Yen HL, Yu MY, Yuen KM, Sia SF, Chan MC, Qin G, Tu WW, Peiris JS (2011) Amino acid residues 253 and 591 of the PB2 protein of avian influenza virus A H9N2 contribute to mammalian pathogenesis. J Virol 85:9641–9645

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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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 (Y19H260021), and the Independent Task of State Key Laboratory for Diagnosis and Treatment of Infectious Diseases (Nos. 2017ZZ10 and 2018ZZ06).

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  1. State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital School of Medicine, Zhejiang University, Hangzhou, China

    Haibo Wu, Fan Yang, Fumin Liu, Xiuming Peng, Bin Chen, Linfang Cheng, Xiangyun Lu, Hangping Yao & Nanping Wu

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  1. Haibo Wu
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  2. Fan Yang
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Correspondence to Haibo Wu or Nanping Wu.

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

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Wu, H., Yang, F., Liu, F. et al. Molecular characterization of H10 subtype avian influenza viruses isolated from poultry in Eastern China. Arch Virol 164, 159–179 (2019). https://doi.org/10.1007/s00705-018-4019-z

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