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Published in: Virology Journal 1/2018

Open Access 01-12-2018 | Research

Isolation and characterization of novel reassortant H6N1 avian influenza viruses from chickens in Eastern China

Authors: Haibo Wu, Fan Yang, Fumin Liu, Rufeng Lu, Xiuming Peng, Bin Chen, Hangping Yao, Nanping Wu

Published in: Virology Journal | Issue 1/2018

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Abstract

Background

The H6N1 subtype of avian influenza viruses (AIVs) can infect people with an influenza-like illness; the H6N1 viruses possess the ability for zoonotic transmission from avians into mammals, and possibly pose a threat to human health.

Methods

In 2017, live poultry markets (LPMs) in Zhejiang Province were surveyed for AIVs. To better understand the genetic relationships between these strains from Eastern China and other AIVs, all gene segments of these strains were sequenced and compared with sequences available in GenBank. In this study, we analyzed the receptor-binding specificity, antigenic characteristics, and pathogenicity of these two H6N1 viruses.

Results

In 2017, two H6N1 AIVs were isolated from chickens during surveillance for AIVs in LPMs in Eastern China. Phylogenetic analysis showed that these strains shared genetic characteristics from H6, H10, H1, and H4 AIVs found in ducks and wild birds in East Asia. These AIV strains were able to replicate in mice without prior adaptation.

Conclusions

In this study, we report the discovery of new strains of H6N1 viruses from chickens with novel gene reassortments. Our results suggest that these chickens play an important role generating novel reassortments in AIVs, and emphasize the need for continued surveillance of AIV strains circulating in poultry.
Appendix
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Literature
1.
go back to reference Zhu X, Yu W, McBride R, Li Y, Chen LM, Donis RO, Tong S, Paulson JC, Wilson IA. Hemagglutinin homologue from H17N10 bat influenza virus exhibits divergent receptor-binding and pH-dependent fusion activities. Proc Natl Acad Sci U S A. 2013;110:1458–63.CrossRef Zhu X, Yu W, McBride R, Li Y, Chen LM, Donis RO, Tong S, Paulson JC, Wilson IA. Hemagglutinin homologue from H17N10 bat influenza virus exhibits divergent receptor-binding and pH-dependent fusion activities. Proc Natl Acad Sci U S A. 2013;110:1458–63.CrossRef
2.
go back to reference Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X, Recuenco S, Gomez J, et al. New world bats harbor diverse influenza a viruses. PLoS Pathog. 2013;9:e1003657.CrossRef Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X, Recuenco S, Gomez J, et al. New world bats harbor diverse influenza a viruses. PLoS Pathog. 2013;9:e1003657.CrossRef
3.
go back to reference Kawaoka Y, Chambers TM, Sladen WL, Webster RG. Is the gene pool of influenza viruses in shorebirds and gulls different from that in wild ducks? Virology. 1988;163:247–50.CrossRef Kawaoka Y, Chambers TM, Sladen WL, Webster RG. Is the gene pool of influenza viruses in shorebirds and gulls different from that in wild ducks? Virology. 1988;163:247–50.CrossRef
4.
go back to reference Liu M, He S, Walker D, Zhou N, Perez DR, Mo B, Li F, Huang X, Webster RG, Webby RJ. The influenza virus gene pool in a poultry market in south Central China. Virology. 2003;305:267–75.CrossRef Liu M, He S, Walker D, Zhou N, Perez DR, Mo B, Li F, Huang X, Webster RG, Webby RJ. The influenza virus gene pool in a poultry market in south Central China. Virology. 2003;305:267–75.CrossRef
5.
go back to reference Cardona C, Yee K, Carpenter T. Are live bird markets reservoirs of avian influenza? Poult Sci. 2009;88:856–9.CrossRef Cardona C, Yee K, Carpenter T. Are live bird markets reservoirs of avian influenza? Poult Sci. 2009;88:856–9.CrossRef
6.
go back to reference Xu KM, Li KS, Smith GJ, Li JW, Tai H, Zhang JX, Webster RG, Peiris JS, Chen H, Guan Y. Evolution and molecular epidemiology of H9N2 influenza a viruses from quail in southern China, 2000 to 2005. J Virol. 2007;81:2635–45.CrossRef Xu KM, Li KS, Smith GJ, Li JW, Tai H, Zhang JX, Webster RG, Peiris JS, Chen H, Guan Y. Evolution and molecular epidemiology of H9N2 influenza a viruses from quail in southern China, 2000 to 2005. J Virol. 2007;81:2635–45.CrossRef
7.
go back to reference Guo YJ, Krauss S, Senne DA, Mo IP, Lo KS, Xiong XP, Norwood M, Shortridge KF, Webster RG, Guan Y. Characterization of the pathogenicity of members of the newly established H9N2 influenza virus lineages in Asia. Virology. 2000;267:279–88.CrossRef Guo YJ, Krauss S, Senne DA, Mo IP, Lo KS, Xiong XP, Norwood M, Shortridge KF, Webster RG, Guan Y. Characterization of the pathogenicity of members of the newly established H9N2 influenza virus lineages in Asia. Virology. 2000;267:279–88.CrossRef
8.
go back to reference Gambaryan AS, Tuzikov AB, Pazynina GV, Desheva JA, Bovin NV, Matrosovich MN, Klimov AI. 6-sulfo sialyl Lewis X is the common receptor determinant recognized by H5, H6, H7 and H9 influenza viruses of terrestrial poultry. Virol J. 2008;5:85.CrossRef Gambaryan AS, Tuzikov AB, Pazynina GV, Desheva JA, Bovin NV, Matrosovich MN, Klimov AI. 6-sulfo sialyl Lewis X is the common receptor determinant recognized by H5, H6, H7 and H9 influenza viruses of terrestrial poultry. Virol J. 2008;5:85.CrossRef
9.
go back to reference Munster VJ, Baas C, Lexmond P, Waldenstrom J, Wallensten A, Fransson T, Rimmelzwaan GF, Beyer WE, Schutten M, Olsen B, et al. Spatial, temporal, and species variation in prevalence of influenza a viruses in wild migratory birds. PLoS Pathog. 2007;3:e61.CrossRef Munster VJ, Baas C, Lexmond P, Waldenstrom J, Wallensten A, Fransson T, Rimmelzwaan GF, Beyer WE, Schutten M, Olsen B, et al. Spatial, temporal, and species variation in prevalence of influenza a viruses in wild migratory birds. PLoS Pathog. 2007;3:e61.CrossRef
10.
go back to reference Krauss S, Obert CA, Franks J, Walker D, Jones K, Seiler P, Niles L, Pryor SP, Obenauer JC, Naeve CW, et al. Influenza in migratory birds and evidence of limited intercontinental virus exchange. PLoS Pathog. 2007;3:e167.CrossRef Krauss S, Obert CA, Franks J, Walker D, Jones K, Seiler P, Niles L, Pryor SP, Obenauer JC, Naeve CW, et al. Influenza in migratory birds and evidence of limited intercontinental virus exchange. PLoS Pathog. 2007;3:e167.CrossRef
11.
go back to reference Krauss S, Walker D, Pryor SP, Niles L, Chenghong L, Hinshaw VS, Webster RG. Influenza a viruses of migrating wild aquatic birds in North America. Vector Borne Zoonotic Dis. 2004;4:177–89.CrossRef Krauss S, Walker D, Pryor SP, Niles L, Chenghong L, Hinshaw VS, Webster RG. Influenza a viruses of migrating wild aquatic birds in North America. Vector Borne Zoonotic Dis. 2004;4:177–89.CrossRef
12.
go back to reference Kim HR, Lee YJ, Lee KK, Oem JK, Kim SH, Lee MH, Lee OS, Park CK. Genetic relatedness of H6 subtype avian influenza viruses isolated from wild birds and domestic ducks in Korea and their pathogenicity in animals. J Gen Virol. 2010;91:208–19.CrossRef Kim HR, Lee YJ, Lee KK, Oem JK, Kim SH, Lee MH, Lee OS, Park CK. Genetic relatedness of H6 subtype avian influenza viruses isolated from wild birds and domestic ducks in Korea and their pathogenicity in animals. J Gen Virol. 2010;91:208–19.CrossRef
13.
go back to reference Nam JH, Kim EH, Song D, Choi YK, Kim JK, Poo H. Emergence of mammalian species-infectious and -pathogenic avian influenza H6N5 virus with no evidence of adaptation. J Virol. 2011;85:13271–7.CrossRef Nam JH, Kim EH, Song D, Choi YK, Kim JK, Poo H. Emergence of mammalian species-infectious and -pathogenic avian influenza H6N5 virus with no evidence of adaptation. J Virol. 2011;85:13271–7.CrossRef
14.
go back to reference Huang K, Zhu H, Fan X, Wang J, Cheung CL, Duan L, Hong W, Liu Y, Li L, Smith DK, et al. Establishment and lineage replacement of H6 influenza viruses in domestic ducks in southern China. J Virol. 2012;86:6075–83.CrossRef Huang K, Zhu H, Fan X, Wang J, Cheung CL, Duan L, Hong W, Liu Y, Li L, Smith DK, et al. Establishment and lineage replacement of H6 influenza viruses in domestic ducks in southern China. J Virol. 2012;86:6075–83.CrossRef
15.
go back to reference Zhao G, Lu X, Gu X, Zhao K, Song Q, Pan J, Xu Q, Duan Z, Peng D, Hu S, et al. Molecular evolution of the H6 subtype influenza a viruses from poultry in eastern China from 2002 to 2010. Virol J. 2011;8:470.CrossRef Zhao G, Lu X, Gu X, Zhao K, Song Q, Pan J, Xu Q, Duan Z, Peng D, Hu S, et al. Molecular evolution of the H6 subtype influenza a viruses from poultry in eastern China from 2002 to 2010. Virol J. 2011;8:470.CrossRef
16.
go back to reference Wang G, Deng G, Shi J, Luo W, Zhang G, Zhang Q, Liu L, Jiang Y, Li C, Sriwilaijaroen N, et al. H6 influenza viruses pose a potential threat to human health. J Virol. 2014;88:3953–64.CrossRef Wang G, Deng G, Shi J, Luo W, Zhang G, Zhang Q, Liu L, Jiang Y, Li C, Sriwilaijaroen N, et al. H6 influenza viruses pose a potential threat to human health. J Virol. 2014;88:3953–64.CrossRef
17.
go back to reference Chin PS, Hoffmann E, Webby R, Webster RG, Guan Y, Peiris M, Shortridge KF. Molecular evolution of H6 influenza viruses from poultry in southeastern China: prevalence of H6N1 influenza viruses possessing seven a/Hong Kong/156/97 (H5N1)-like genes in poultry. J Virol. 2002;76:507–16.CrossRef Chin PS, Hoffmann E, Webby R, Webster RG, Guan Y, Peiris M, Shortridge KF. Molecular evolution of H6 influenza viruses from poultry in southeastern China: prevalence of H6N1 influenza viruses possessing seven a/Hong Kong/156/97 (H5N1)-like genes in poultry. J Virol. 2002;76:507–16.CrossRef
18.
go back to reference Wu H, Peng X, Cheng L, Wu N. Molecular characterization of novel reassortant H6N2 subtype avian influenza viruses isolated from poultry in eastern China, in 2014. Infect Genet Evol. 2015;36:41–5.CrossRef Wu H, Peng X, Cheng L, Wu N. Molecular characterization of novel reassortant H6N2 subtype avian influenza viruses isolated from poultry in eastern China, in 2014. Infect Genet Evol. 2015;36:41–5.CrossRef
19.
go back to reference Wu H, Lu R, Peng X, Cheng L, Jin C, Lu X, Xie T, Yao H, Wu N. Isolation and genetic characterization of novel reassortant H6N6 subtype avian influenza viruses isolated from chickens in eastern China. Arch Virol. 2016;161:1859–72.CrossRef Wu H, Lu R, Peng X, Cheng L, Jin C, Lu X, Xie T, Yao H, Wu N. Isolation and genetic characterization of novel reassortant H6N6 subtype avian influenza viruses isolated from chickens in eastern China. Arch Virol. 2016;161:1859–72.CrossRef
20.
go back to reference Xin L, Bai T, Zhou JF, Chen YK, Li XD, Zhu WF, Li Y, Tang J, Chen T, Qin K, et al. Seropositivity for avian influenza H6 virus among humans, China. Emerg Infect Dis. 2015;21:1267–9.CrossRef Xin L, Bai T, Zhou JF, Chen YK, Li XD, Zhu WF, Li Y, Tang J, Chen T, Qin K, et al. Seropositivity for avian influenza H6 virus among humans, China. Emerg Infect Dis. 2015;21:1267–9.CrossRef
21.
go back to reference Wei SH, Yang JR, Wu HS, Chang MC, Lin JS, Lin CY, Liu YL, Lo YC, Yang CH, Chuang JH, et al. Human infection with avian influenza a H6N1 virus: an epidemiological analysis. Lancet Respir Med. 2013;1:771–8.CrossRef Wei SH, Yang JR, Wu HS, Chang MC, Lin JS, Lin CY, Liu YL, Lo YC, Yang CH, Chuang JH, et al. Human infection with avian influenza a H6N1 virus: an epidemiological analysis. Lancet Respir Med. 2013;1:771–8.CrossRef
22.
go back to reference Shi W, Shi Y, Wu Y, Liu D, Gao GF. Origin and molecular characterization of the human-infecting H6N1 influenza virus in Taiwan. Protein Cell. 2013;4:846–53.CrossRef Shi W, Shi Y, Wu Y, Liu D, Gao GF. Origin and molecular characterization of the human-infecting H6N1 influenza virus in Taiwan. Protein Cell. 2013;4:846–53.CrossRef
23.
go back to reference Lin HT, Wang CH, Chueh LL, Su BL, Wang LC. Influenza A(H6N1) Virus in Dogs, Taiwan. Emerg Infect Dis. 2015;21:2154–7.CrossRef Lin HT, Wang CH, Chueh LL, Su BL, Wang LC. Influenza A(H6N1) Virus in Dogs, Taiwan. Emerg Infect Dis. 2015;21:2154–7.CrossRef
24.
go back to reference Cheng K, Yu Z, Gao Y, Xia X, He H, Hua Y, Chai H. Experimental infection of dogs with H6N1 avian influenza a virus. Arch Virol. 2014;159:2275–82.CrossRef Cheng K, Yu Z, Gao Y, Xia X, He H, Hua Y, Chai H. Experimental infection of dogs with H6N1 avian influenza a virus. Arch Virol. 2014;159:2275–82.CrossRef
25.
go back to reference Wang F, Qi J, Bi Y, Zhang W, Wang M, Zhang B, Liu J, Yan J, Shi Y, Gao GF. Adaptation of avian influenza a (H6N1) virus from avian to human receptor-binding preference. EMBO J. 2015;34:1661–73.CrossRef Wang F, Qi J, Bi Y, Zhang W, Wang M, Zhang B, Liu J, Yan J, Shi Y, Gao GF. Adaptation of avian influenza a (H6N1) virus from avian to human receptor-binding preference. EMBO J. 2015;34:1661–73.CrossRef
26.
go back to reference Huang K, Bahl J, Fan XH, Vijaykrishna D, Cheung CL, Webby RJ, Webster RG, Chen H, Smith GJ, Peiris JS, Guan Y. Establishment of an H6N2 influenza virus lineage in domestic ducks in southern China. J Virol. 2010;84:6978–86.CrossRef Huang K, Bahl J, Fan XH, Vijaykrishna D, Cheung CL, Webby RJ, Webster RG, Chen H, Smith GJ, Peiris JS, Guan Y. Establishment of an H6N2 influenza virus lineage in domestic ducks in southern China. J Virol. 2010;84:6978–86.CrossRef
27.
go back to reference Wu HB, Guo CT, Lu RF, Xu LH, Wo EK, You JB, Wang YT, Wang QG, Wu NP. Genetic characterization of subtype H1 avian influenza viruses isolated from live poultry markets in Zhejiang Province, China, in 2011. Virus Genes. 2012;44:441–9.CrossRef Wu HB, Guo CT, Lu RF, Xu LH, Wo EK, You JB, Wang YT, Wang QG, Wu NP. Genetic characterization of subtype H1 avian influenza viruses isolated from live poultry markets in Zhejiang Province, China, in 2011. Virus Genes. 2012;44:441–9.CrossRef
28.
go back to reference Wu H, Lu R, Peng X, Cheng L, Liu F, Wu N. Characterization of novel Reassortant influenza a (H5N2) viruses isolated from poultry in eastern China, 2015. Front Microbiol. 2017;8:741.CrossRef Wu H, Lu R, Peng X, Cheng L, Liu F, Wu N. Characterization of novel Reassortant influenza a (H5N2) viruses isolated from poultry in eastern China, 2015. Front Microbiol. 2017;8:741.CrossRef
29.
go back to reference Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR. Universal primer set for the full-length amplification of all influenza a viruses. Arch Virol. 2001;146:2275–89.CrossRef Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR. Universal primer set for the full-length amplification of all influenza a viruses. Arch Virol. 2001;146:2275–89.CrossRef
30.
go back to reference Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725–9.CrossRef Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725–9.CrossRef
31.
go back to reference Gupta R JEaBS: Prediction of N-glycosylation sites in human proteins; 2004. Database: NetNGlyc 1.0 [Internet]. 2004. Gupta R JEaBS: Prediction of N-glycosylation sites in human proteins; 2004. Database: NetNGlyc 1.0 [Internet]. 2004.
32.
go back to reference Tewawong N, Prachayangprecha S, Vichiwattana P, Korkong S, Klinfueng S, Vongpunsawad S, Thongmee T, Theamboonlers A, Poovorawan Y. Assessing antigenic drift of seasonal influenza a(H3N2) and a(H1N1)pdm09 viruses. PLoS One. 2015;10:e0139958.CrossRef Tewawong N, Prachayangprecha S, Vichiwattana P, Korkong S, Klinfueng S, Vongpunsawad S, Thongmee T, Theamboonlers A, Poovorawan Y. Assessing antigenic drift of seasonal influenza a(H3N2) and a(H1N1)pdm09 viruses. PLoS One. 2015;10:e0139958.CrossRef
33.
go back to reference Zou S, Gao R, Zhang Y, Li X, Chen W, Bai T, Dong L, Wang D, Shu Y. Molecular characterization of H6 subtype influenza viruses in southern China from 2009 to 2011. Emerg Microbes Infect. 2016;5:e73.CrossRef Zou S, Gao R, Zhang Y, Li X, Chen W, Bai T, Dong L, Wang D, Shu Y. Molecular characterization of H6 subtype influenza viruses in southern China from 2009 to 2011. Emerg Microbes Infect. 2016;5:e73.CrossRef
34.
go back to reference Suptawiwat O, Kongchanagul A, Chan-It W, Thitithanyanont A, Wiriyarat W, Chaichuen K, Songserm T, Suzuki Y, Puthavathana P, Auewarakul P. A simple screening assay for receptor switching of avian influenza viruses. J Clin Virol. 2008;42:186–9.CrossRef Suptawiwat O, Kongchanagul A, Chan-It W, Thitithanyanont A, Wiriyarat W, Chaichuen K, Songserm T, Suzuki Y, Puthavathana P, Auewarakul P. A simple screening assay for receptor switching of avian influenza viruses. J Clin Virol. 2008;42:186–9.CrossRef
35.
go back to reference Medeiros R, Escriou N, Naffakh N, Manuguerra JC, van der Werf S. Hemagglutinin residues of recent human a(H3N2) influenza viruses that contribute to the inability to agglutinate chicken erythrocytes. Virology. 2001;289:74–85.CrossRef Medeiros R, Escriou N, Naffakh N, Manuguerra JC, van der Werf S. Hemagglutinin residues of recent human a(H3N2) influenza viruses that contribute to the inability to agglutinate chicken erythrocytes. Virology. 2001;289:74–85.CrossRef
36.
go back to reference Liu Q, Zhou B, Ma W, Bawa B, Ma J, Wang W, Lang Y, Lyoo Y, Halpin RA, Lin X, et al. Analysis of recombinant H7N9 wild-type and mutant viruses in pigs shows that the Q226L mutation in HA is important for transmission. J Virol. 2014;88:8153–65.CrossRef Liu Q, Zhou B, Ma W, Bawa B, Ma J, Wang W, Lang Y, Lyoo Y, Halpin RA, Lin X, et al. Analysis of recombinant H7N9 wild-type and mutant viruses in pigs shows that the Q226L mutation in HA is important for transmission. J Virol. 2014;88:8153–65.CrossRef
37.
go back to reference Jin H, Wang D, Sun J, Cui Y, Chen G, Zhang X, Zhang J, Li X, Chai H, Gao Y, et al. Pathogenesis and phylogenetic analyses of two avian influenza H7N1 viruses isolated from wild birds. Front Microbiol. 2016;7:1066.PubMedPubMedCentral Jin H, Wang D, Sun J, Cui Y, Chen G, Zhang X, Zhang J, Li X, Chai H, Gao Y, et al. Pathogenesis and phylogenetic analyses of two avian influenza H7N1 viruses isolated from wild birds. Front Microbiol. 2016;7:1066.PubMedPubMedCentral
38.
go back to reference Chang H, Dai F, Liu Z, Yuan F, Zhao S, Xiang X, Zou F, Zeng B, Fan Y, Duan G. Seroprevalence survey of avian influenza a (H5) in wild migratory birds in Yunnan Province, southwestern China. Virol J. 2014;11:18.CrossRef Chang H, Dai F, Liu Z, Yuan F, Zhao S, Xiang X, Zou F, Zeng B, Fan Y, Duan G. Seroprevalence survey of avian influenza a (H5) in wild migratory birds in Yunnan Province, southwestern China. Virol J. 2014;11:18.CrossRef
39.
go back to reference Tan L, Su S, Smith DK, He S, Zheng Y, Shao Z, Ma J, Zhu H, Zhang G. A combination of HA and PA mutations enhances virulence in a mouse-adapted H6N6 influenza a virus. J Virol. 2014;88:14116–25.CrossRef Tan L, Su S, Smith DK, He S, Zheng Y, Shao Z, Ma J, Zhu H, Zhang G. A combination of HA and PA mutations enhances virulence in a mouse-adapted H6N6 influenza a virus. J Virol. 2014;88:14116–25.CrossRef
40.
go back to reference Wang J, Sun Y, Xu Q, Tan Y, Pu J, Yang H, Brown EG, Liu J. Mouse-adapted H9N2 influenza a virus PB2 protein M147L and E627K mutations are critical for high virulence. PLoS One. 2012;7:e40752.CrossRef Wang J, Sun Y, Xu Q, Tan Y, Pu J, Yang H, Brown EG, Liu J. Mouse-adapted H9N2 influenza a virus PB2 protein M147L and E627K mutations are critical for high virulence. PLoS One. 2012;7:e40752.CrossRef
41.
go back to reference Wu H, Peng X, Lu R, Xu L, Liu F, Cheng L, Lu X, Yao H, Wu N. Virulence of an H5N8 highly pathogenic avian influenza is enhanced by the amino acid substitutions PB2 E627K and HA A149V. Infect Genet Evol. 2017;54:347–54.CrossRef Wu H, Peng X, Lu R, Xu L, Liu F, Cheng L, Lu X, Yao H, Wu N. Virulence of an H5N8 highly pathogenic avian influenza is enhanced by the amino acid substitutions PB2 E627K and HA A149V. Infect Genet Evol. 2017;54:347–54.CrossRef
42.
go back to reference Reed L, Muench H. A simple method for estimating fifty percent endpoints. Am J Hyg. 1938;27:493–7. Reed L, Muench H. A simple method for estimating fifty percent endpoints. Am J Hyg. 1938;27:493–7.
43.
go back to reference Wu H, Peng X, Cheng L, Lu X, Jin C, Xie T, Yao H, Wu N. Genetic and molecular characterization of H9N2 and H5 avian influenza viruses from live poultry markets in Zhejiang Province, Eastern China. Sci Rep. 2015;5:17508.CrossRef Wu H, Peng X, Cheng L, Lu X, Jin C, Xie T, Yao H, Wu N. Genetic and molecular characterization of H9N2 and H5 avian influenza viruses from live poultry markets in Zhejiang Province, Eastern China. Sci Rep. 2015;5:17508.CrossRef
44.
go back to reference Horimoto T, Ito T, Alexander DJ, Kawaoka Y. Cleavability of hemagglutinin from an extremely virulent strain of avian influenza virus containing a unique cleavage site sequence. J Vet Med Sci. 1995;57:927–30.CrossRef Horimoto T, Ito T, Alexander DJ, Kawaoka Y. Cleavability of hemagglutinin from an extremely virulent strain of avian influenza virus containing a unique cleavage site sequence. J Vet Med Sci. 1995;57:927–30.CrossRef
45.
go back to reference Matrosovich MN, Gambaryan AS, Teneberg S, Piskarev VE, Yamnikova SS, Lvov DK, Robertson JS, Karlsson KA. 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. 1997;233:224–34.CrossRef Matrosovich MN, Gambaryan AS, Teneberg S, Piskarev VE, Yamnikova SS, Lvov DK, Robertson JS, Karlsson KA. 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. 1997;233:224–34.CrossRef
46.
go back to reference Tzarum N, de Vries RP, Zhu X, Yu W, McBride R, Paulson JC, Wilson IA. Structure and receptor binding of the hemagglutinin from a human H6N1 influenza virus. Cell Host Microbe. 2015;17:369–76.CrossRef Tzarum N, de Vries RP, Zhu X, Yu W, McBride R, Paulson JC, Wilson IA. Structure and receptor binding of the hemagglutinin from a human H6N1 influenza virus. Cell Host Microbe. 2015;17:369–76.CrossRef
47.
go back to reference Aoki FY, Boivin G, Roberts N. Influenza virus susceptibility and resistance to oseltamivir. Antivir Ther. 2007;12:603–16.PubMed Aoki FY, Boivin G, Roberts N. Influenza virus susceptibility and resistance to oseltamivir. Antivir Ther. 2007;12:603–16.PubMed
48.
go back to reference Deyde VM, Xu X, Bright RA, Shaw M, Smith CB, Zhang Y, Shu Y, Gubareva LV, Cox NJ, Klimov AI. Surveillance of resistance to adamantanes among influenza a(H3N2) and a(H1N1) viruses isolated worldwide. J Infect Dis. 2007;196:249–57.CrossRef Deyde VM, Xu X, Bright RA, Shaw M, Smith CB, Zhang Y, Shu Y, Gubareva LV, Cox NJ, Klimov AI. Surveillance of resistance to adamantanes among influenza a(H3N2) and a(H1N1) viruses isolated worldwide. J Infect Dis. 2007;196:249–57.CrossRef
49.
go back to reference Schat KA, Bingham J, Butler JM, Chen LM, Lowther S, Crowley TM, Moore RJ, Donis RO, Lowenthal JW. 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. 2012;7:e30960.CrossRef Schat KA, Bingham J, Butler JM, Chen LM, Lowther S, Crowley TM, Moore RJ, Donis RO, Lowenthal JW. 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. 2012;7:e30960.CrossRef
50.
go back to reference Bussey KA, Bousse TL, Desmet EA, Kim B, Takimoto T. PB2 residue 271 plays a key role in enhanced polymerase activity of influenza a viruses in mammalian host cells. J Virol. 2010;84:4395–406.CrossRef Bussey KA, Bousse TL, Desmet EA, Kim B, Takimoto T. PB2 residue 271 plays a key role in enhanced polymerase activity of influenza a viruses in mammalian host cells. J Virol. 2010;84:4395–406.CrossRef
51.
go back to reference Zhang Y, Zhu J, Li Y, Bradley KC, Cao J, Chen H, Jin M, Zhou H. Glycosylation on hemagglutinin affects the virulence and pathogenicity of pandemic H1N1/2009 influenza a virus in mice. PLoS One. 2013;8:e61397.CrossRef Zhang Y, Zhu J, Li Y, Bradley KC, Cao J, Chen H, Jin M, Zhou H. Glycosylation on hemagglutinin affects the virulence and pathogenicity of pandemic H1N1/2009 influenza a virus in mice. PLoS One. 2013;8:e61397.CrossRef
52.
go back to reference Suptawiwat O, Boonarkart C, Chakritbudsabong W, Uiprasertkul M, Puthavathana P, Wiriyarat W, Auewarakul P. 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. 2015;160:409–15.CrossRef Suptawiwat O, Boonarkart C, Chakritbudsabong W, Uiprasertkul M, Puthavathana P, Wiriyarat W, Auewarakul P. 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. 2015;160:409–15.CrossRef
53.
go back to reference Xiong X, McCauley JW, Steinhauer DA. Receptor binding properties of the influenza virus hemagglutinin as a determinant of host range. Curr Top Microbiol Immunol. 2014;385:63–91.PubMed Xiong X, McCauley JW, Steinhauer DA. Receptor binding properties of the influenza virus hemagglutinin as a determinant of host range. Curr Top Microbiol Immunol. 2014;385:63–91.PubMed
54.
go back to reference Klimov A, Balish A, Veguilla V, Sun H, Schiffer J, Lu X, Katz JM, Hancock K. Influenza virus titration, antigenic characterization, and serological methods for antibody detection. Methods Mol Biol. 2012;865:25–51.CrossRef Klimov A, Balish A, Veguilla V, Sun H, Schiffer J, Lu X, Katz JM, Hancock K. Influenza virus titration, antigenic characterization, and serological methods for antibody detection. Methods Mol Biol. 2012;865:25–51.CrossRef
55.
go back to reference Hotta K, Takakuwa H, Le QM, Phuong SL, Murase T, Ono E, Ito T, Otsuki K, Yamashiro T. Isolation and characterization of H6N1 and H9N2 avian influenza viruses from ducks in Hanoi, Vietnam. Virus Res. 2012;163:448–53.CrossRef Hotta K, Takakuwa H, Le QM, Phuong SL, Murase T, Ono E, Ito T, Otsuki K, Yamashiro T. Isolation and characterization of H6N1 and H9N2 avian influenza viruses from ducks in Hanoi, Vietnam. Virus Res. 2012;163:448–53.CrossRef
56.
go back to reference Myers KP, Setterquist SF, Capuano AW, Gray GC. Infection due to 3 avian influenza subtypes in United States veterinarians. Clin Infect Dis. 2007;45:4–9.CrossRef Myers KP, Setterquist SF, Capuano AW, Gray GC. Infection due to 3 avian influenza subtypes in United States veterinarians. Clin Infect Dis. 2007;45:4–9.CrossRef
57.
go back to reference Zhang G, Kong W, Qi W, Long LP, Cao Z, Huang L, Qi H, Cao N, Wang W, Zhao F, et al. Identification of an H6N6 swine influenza virus in southern China. Infect Genet Evol. 2011;11:1174–7.CrossRef Zhang G, Kong W, Qi W, Long LP, Cao Z, Huang L, Qi H, Cao N, Wang W, Zhao F, et al. Identification of an H6N6 swine influenza virus in southern China. Infect Genet Evol. 2011;11:1174–7.CrossRef
58.
go back to reference Yuan R, Zou L, Kang Y, Wu J, Zeng X, Lu J, Liang L, Song Y, Zhang X, Ni H, et al. Reassortment of avian influenza a/H6N6 viruses from live poultry Markets in Guangdong, China. Front Microbiol. 2016;7:65.PubMedPubMedCentral Yuan R, Zou L, Kang Y, Wu J, Zeng X, Lu J, Liang L, Song Y, Zhang X, Ni H, et al. Reassortment of avian influenza a/H6N6 viruses from live poultry Markets in Guangdong, China. Front Microbiol. 2016;7:65.PubMedPubMedCentral
59.
go back to reference Xie Z, Xie L, Zhou C, Liu J, Pang Y, Deng X, Fan Q. Complete genome sequence analysis of an H6N1 avian influenza virus isolated from Guangxi pockmark ducks. J Virol. 2012;86:13868–9.CrossRef Xie Z, Xie L, Zhou C, Liu J, Pang Y, Deng X, Fan Q. Complete genome sequence analysis of an H6N1 avian influenza virus isolated from Guangxi pockmark ducks. J Virol. 2012;86:13868–9.CrossRef
60.
go back to reference Yuan J, Zhang L, Kan X, Jiang L, Yang J, Guo Z, Ren Q. Origin and molecular characteristics of a novel 2013 avian influenza a(H6N1) virus causing human infection in Taiwan. Clin Infect Dis. 2013;57:1367–8.CrossRef Yuan J, Zhang L, Kan X, Jiang L, Yang J, Guo Z, Ren Q. Origin and molecular characteristics of a novel 2013 avian influenza a(H6N1) virus causing human infection in Taiwan. Clin Infect Dis. 2013;57:1367–8.CrossRef
61.
go back to reference Belser JA, Gustin KM, Pearce MB, Maines TR, Zeng H, Pappas C, Sun X, Carney PJ, Villanueva JM, Stevens J, et al. Pathogenesis and transmission of avian influenza a (H7N9) virus in ferrets and mice. Nature. 2013;501:556–9.CrossRef Belser JA, Gustin KM, Pearce MB, Maines TR, Zeng H, Pappas C, Sun X, Carney PJ, Villanueva JM, Stevens J, et al. Pathogenesis and transmission of avian influenza a (H7N9) virus in ferrets and mice. Nature. 2013;501:556–9.CrossRef
62.
go back to reference Brown EG. Increased virulence of a mouse-adapted variant of influenza a/FM/1/47 virus is controlled by mutations in genome segments 4, 5, 7, and 8. J Virol. 1990;64:4523–33.PubMedPubMedCentral Brown EG. Increased virulence of a mouse-adapted variant of influenza a/FM/1/47 virus is controlled by mutations in genome segments 4, 5, 7, and 8. J Virol. 1990;64:4523–33.PubMedPubMedCentral
63.
go back to reference Yao Y, Wang H, Chen Q, Zhang H, Zhang T, Chen J, Xu B, Sun B, Chen Z. Characterization of low-pathogenic H6N6 avian influenza viruses in Central China. Arch Virol. 2013;158:367–77.CrossRef Yao Y, Wang H, Chen Q, Zhang H, Zhang T, Chen J, Xu B, Sun B, Chen Z. Characterization of low-pathogenic H6N6 avian influenza viruses in Central China. Arch Virol. 2013;158:367–77.CrossRef
64.
go back to reference Yu Z, Cheng K, Xin Y, Sun W, Li X, Huang J, Zhang K, Yang S, Wang T, Zheng X, et al. Multiple amino acid substitutions involved in the adaptation of H6N1 avian influenza virus in mice. Vet Microbiol. 2014;174:316–21.CrossRef Yu Z, Cheng K, Xin Y, Sun W, Li X, Huang J, Zhang K, Yang S, Wang T, Zheng X, et al. Multiple amino acid substitutions involved in the adaptation of H6N1 avian influenza virus in mice. Vet Microbiol. 2014;174:316–21.CrossRef
65.
go back to reference Cheng K, Yu Z, Chai H, Sun W, Xin Y, Zhang Q, Huang J, Zhang K, Li X, Yang S, et al. PB2-E627K and PA-T97I substitutions enhance polymerase activity and confer a virulent phenotype to an H6N1 avian influenza virus in mice. Virology. 2014;468-470:207–13.CrossRef Cheng K, Yu Z, Chai H, Sun W, Xin Y, Zhang Q, Huang J, Zhang K, Li X, Yang S, et al. PB2-E627K and PA-T97I substitutions enhance polymerase activity and confer a virulent phenotype to an H6N1 avian influenza virus in mice. Virology. 2014;468-470:207–13.CrossRef
66.
go back to reference Ni F, Kondrashkina E, Wang Q. Structural and functional studies of influenza virus a/H6 hemagglutinin. PLoS One. 2015;10:e0134576.CrossRef Ni F, Kondrashkina E, Wang Q. Structural and functional studies of influenza virus a/H6 hemagglutinin. PLoS One. 2015;10:e0134576.CrossRef
67.
go back to reference Cheung CL, Vijaykrishna D, Smith GJ, Fan XH, Zhang JX, Bahl J, Duan L, Huang K, Tai H, Wang J, et al. Establishment of influenza a virus (H6N1) in minor poultry species in southern China. J Virol. 2007;81:10402–12.CrossRef Cheung CL, Vijaykrishna D, Smith GJ, Fan XH, Zhang JX, Bahl J, Duan L, Huang K, Tai H, Wang J, et al. Establishment of influenza a virus (H6N1) in minor poultry species in southern China. J Virol. 2007;81:10402–12.CrossRef
Metadata
Title
Isolation and characterization of novel reassortant H6N1 avian influenza viruses from chickens in Eastern China
Authors
Haibo Wu
Fan Yang
Fumin Liu
Rufeng Lu
Xiuming Peng
Bin Chen
Hangping Yao
Nanping Wu
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2018
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-018-1063-y

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