Establishment and Lineage Replacement of H6 Influenza Viruses in Domestic Ducks in Southern China

Overview

Journal J Virol

Publisher American Society for Microbiology

Date 2012 Mar 23

PMID 22438558

Citations 53

Authors

Kai Huang

Huachen Zhu

Xiaohui Fan

Jia Wang

Chung-Lam Cheung

Lian Duan

Wenshan Hong

Yongmei Liu

Lifeng Li

David K Smith

Honglin Chen

Robert G Webster

Richard J Webby

Malik Peiris

Yi Guan

Affiliations

Soon will be listed here.

Abstract

Domestic ducks in southern China act as an important reservoir for influenza viruses and have also facilitated the establishment of multiple H6 influenza virus lineages. To understand the continuing evolution of these established lineages, 297 H6 viruses isolated from domestic ducks during 2006 and 2007 were genetically and antigenically analyzed. Phylogenetic analyses showed that group II duck H6 viruses had replaced the previously predominant group I lineage and extended their geographic distribution from coastal to inland regions. Group II H6 virus showed that the genesis and development of multiple types of deletions in the neuraminidase (NA) stalk region could occur in the influenza viruses from domestic ducks. A gradual replacement of the N2 NA subtype with N6 was observed. Significant antigenic changes occurred within group II H6 viruses so that they became antigenically distinguishable from group I and gene pool viruses. Gene exchange between group II H6 viruses and the established H5N1, H9N2, or H6N1 virus lineages in poultry in the region was very limited. These findings suggest that domestic ducks can facilitate significant genetic and antigenic changes in viruses established in this host and highlight gaps in our knowledge of influenza virus ecology and even the evolutionary behavior of this virus family in its aquatic avian reservoirs.

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References

Matrosovich M, Zhou N, Kawaoka Y, Webster R . The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J Virol. 1999; 73(2):1146-55. PMC: 103935. DOI: 10.1128/JVI.73.2.1146-1155.1999. View

Woolcock P, Suarez D, Kuney D . Low-pathogenicity avian influenza virus (H6N2) in chickens in California, 2000-02. Avian Dis. 2003; 47(3 Suppl):872-81. DOI: 10.1637/0005-2086-47.s3.872. View

Banks J, Speidel E, Moore E, Plowright L, Piccirillo A, Capua I . Changes in the haemagglutinin and the neuraminidase genes prior to the emergence of highly pathogenic H7N1 avian influenza viruses in Italy. Arch Virol. 2001; 146(5):963-73. DOI: 10.1007/s007050170128. View

Duan L, Zhu H, Wang J, Huang K, Cheung C, Peiris J . Influenza virus surveillance in migratory ducks and sentinel ducks at Poyang Lake, China. Influenza Other Respir Viruses. 2011; 5(Suppl 1):65-8. View

Munier S, Larcher T, Cormier-Aline F, Soubieux D, Su B, Guigand L . A genetically engineered waterfowl influenza virus with a deletion in the stalk of the neuraminidase has increased virulence for chickens. J Virol. 2009; 84(2):940-52. PMC: 2798369. DOI: 10.1128/JVI.01581-09. View

. Antigenic and genetic characteristics of zoonotic influenza viruses and development of candidate vaccine viruses for pandemic preparedness. Wkly Epidemiol Rec. 2012; 87(11):97-108. View

Guindon S, Gascuel O . A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003; 52(5):696-704. DOI: 10.1080/10635150390235520. View

Huang K, Bahl J, Fan X, Vijaykrishna D, Cheung C, Webby R . Establishment of an H6N2 influenza virus lineage in domestic ducks in southern China. J Virol. 2010; 84(14):6978-86. PMC: 2898240. DOI: 10.1128/JVI.00256-10. View

Zhang G, Kong W, Qi W, Long L, Cao Z, Huang L . Identification of an H6N6 swine influenza virus in southern China. Infect Genet Evol. 2011; 11(5):1174-7. PMC: 3104128. DOI: 10.1016/j.meegid.2011.02.023. View

10.

Webster R, BEAN W, Gorman O, Chambers T, Kawaoka Y . Evolution and ecology of influenza A viruses. Microbiol Rev. 1992; 56(1):152-79. PMC: 372859. DOI: 10.1128/mr.56.1.152-179.1992. View

11.

Duan L, Bahl J, Smith G, Wang J, Vijaykrishna D, Zhang L . The development and genetic diversity of H5N1 influenza virus in China, 1996-2006. Virology. 2008; 380(2):243-54. PMC: 2651962. DOI: 10.1016/j.virol.2008.07.038. View

12.

Zhao G, Lu X, Gu X, Zhao K, Song Q, Pan J . Molecular evolution of the H6 subtype influenza A viruses from poultry in eastern China from 2002 to 2010. Virol J. 2011; 8:470. PMC: 3213047. DOI: 10.1186/1743-422X-8-470. View

13.

Sorrell E, Song H, Pena L, Perez D . A 27-amino-acid deletion in the neuraminidase stalk supports replication of an avian H2N2 influenza A virus in the respiratory tract of chickens. J Virol. 2010; 84(22):11831-40. PMC: 2977859. DOI: 10.1128/JVI.01460-10. View

14.

Dugan V, Chen R, Spiro D, Sengamalay N, Zaborsky J, Ghedin E . The evolutionary genetics and emergence of avian influenza viruses in wild birds. PLoS Pathog. 2008; 4(5):e1000076. PMC: 2387073. DOI: 10.1371/journal.ppat.1000076. View

15.

Xu K, Li K, Smith G, Li J, Tai H, Zhang J . Evolution and molecular epidemiology of H9N2 influenza A viruses from quail in southern China, 2000 to 2005. J Virol. 2006; 81(6):2635-45. PMC: 1865985. DOI: 10.1128/JVI.02316-06. View

16.

Chenna R, Sugawara H, Koike T, Lopez R, Gibson T, Higgins D . Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 2003; 31(13):3497-500. PMC: 168907. DOI: 10.1093/nar/gkg500. View

17.

Lee M, Chang P, Shien J, Cheng M, Chen C, Shieh H . Genetic and pathogenic characterization of H6N1 avian influenza viruses isolated in Taiwan between 1972 and 2005. Avian Dis. 2007; 50(4):561-71. DOI: 10.1637/7640-050106R.1. View

18.

Cheung C, Vijaykrishna D, Smith G, Fan X, Zhang J, Bahl J . Establishment of influenza A virus (H6N1) in minor poultry species in southern China. J Virol. 2007; 81(19):10402-12. PMC: 2045442. DOI: 10.1128/JVI.01157-07. View

19.

Webby R, Woolcock P, Krauss S, Walker D, Chin P, Shortridge K . Multiple genotypes of nonpathogenic H6N2 influenza viruses isolated from chickens in California. Avian Dis. 2003; 47(3 Suppl):905-10. DOI: 10.1637/0005-2086-47.s3.905. View

20.

Li J, Dohna H, Cardona C, Miller J, Carpenter T . Emergence and genetic variation of neuraminidase stalk deletions in avian influenza viruses. PLoS One. 2011; 6(2):e14722. PMC: 3044137. DOI: 10.1371/journal.pone.0014722. View