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.
References
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
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
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
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
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
Cardona C, Yee K, Carpenter T (2009) Are live bird markets reservoirs of avian influenza? Poult Sci 88:856–859
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Reed L, Muench H (1938) A simple method for estimating fifty percent endpoints. Am J Hyg 27:493–497
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
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
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
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
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
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
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
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).
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-017-3487-x