Virologica Sinica

, Volume 31, Issue 4, pp 300–305 | Cite as

Highly pathogenic avian influenza H5N1 Clade 2.3.2.1c virus in migratory birds, 2014–2015

  • Yuhai Bi
  • Jianjun Chen
  • Zhenjie Zhang
  • Mingxin Li
  • Tianlong Cai
  • Kirill Sharshov
  • Ivan Susloparov
  • Alexander Shestopalov
  • Gary Wong
  • Yubang He
  • Zhi Xing
  • Jianqing Sun
  • Di Liu
  • Yingxia Liu
  • Lei Liu
  • Wenjun Liu
  • Fumin Lei
  • Weifeng Shi
  • George F. Gao
Research Article

Abstract

A novel Clade 2.3.2.1c H5N1 reassortant virus caused several outbreaks in wild birds in some regions of China from late 2014 to 2015. Based on the genetic and phylogenetic analyses, the viruses possess a stable gene constellation with a Clade 2.3.2.1c HA, a H9N2-derived PB2 gene and the other six genes of Asian H5N1-origin. The Clade 2.3.2.1c H5N1 reassortants displayed a high genetic relationship to a human H5N1 strain (A/Alberta/01/2014). Further analysis showed that similar viruses have been circulating in wild birds in China, Russia, Dubai (Western Asia), Bulgaria and Romania (Europe), as well as domestic poultry in some regions of Africa. The affected areas include the Central Asian, East Asian-Australasian, West Asian-East African, and Black Sea/Mediterranean flyways. These results show that the novel Clade 2.3.2.1c reassortant viruses are circulating worldwide and may have gained a selective advantage in migratory birds, thus posing a serious threat to wild birds and potentially humans.

Keywords

H5N1 highly pathogenic avian influenza virus Clade 2.3.2.1c outbreak migratory birds 

Supplementary material

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References

  1. Bi Y, Zhang Z, Liu W, Yin Y, Hong J, Li X, Wang H, Wong G, Chen J, Li Y, Ru W, Gao R, Liu D, Liu Y, Zhou B, Gao GF, Shi W, Lei F. 2015a. Highly Pathogenic Avian Influenza A(H5N1) Virus Struck Migratory Birds in China in 2015. Sci Rep, 5: 12986CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bi YH, Mei K, Shi WF, Liu D, Yu XL, Gao ZM, Zhao LH, Gao GF, Chen JJ, Chen QJ. 2015b. Two novel reassortants of avian influenza A (H5N6) virus in China. J Gen Virol, 96: 975–981.CrossRefPubMedGoogle Scholar
  3. Cauldwell AV, Long JS, Moncorgé O, Barclay WS. 2014. Viral determinants of influenza A virus host range. J Gen Virol, 95: 1193–1210.CrossRefPubMedGoogle Scholar
  4. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res, 32: 1792–1797.CrossRefPubMedPubMedCentralGoogle Scholar
  5. FAO. 2015). H5N1 HPAI spread in Nigeria and increased risk for neighbouring countries in West Africa. http://www.fao.org/3/ai4561e.pdf.Google Scholar
  6. Hatta M, Gao P, Halfmann P, Kawaoka Y. 2001. Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science, 293: 1840–1842.CrossRefPubMedGoogle Scholar
  7. Hay AJ, Wolstenholme AJ, Skehel JJ, Smith MH. 1985. The molecular basis of the specific anti-influenza action of amantadine. The EMBO J, 4: 3021–3024.PubMedGoogle Scholar
  8. Hu X, Liu D, Wang M, Yang L, Zhu Q, Li L, Gao GF. 2011. Clade 2.3.2 avian influenza virus (H5N1), Qinghai Lake region, China, 2009–2010. Emerg Infect Dis, 17: 560–562.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 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.Google Scholar
  10. Liu J, Xiao H, Lei F, Zhu Q, Qin K, Zhang XW, Zhang XL, Zhao D, Wang G, Feng Y, Ma J, Liu W, Wang J, Gao GF. 2005. Highly pathogenic H5N1 influenza virus infection in migratory birds. Science, 309: 1206.CrossRefPubMedGoogle Scholar
  11. Matsuoka Y, Swayne DE, Thomas C, Rameix-Welti M-A, Naffakh N, Warnes C, Altholtz M, Donis R, Subbarao K. 2009. Neuraminidase stalk length and additional glycosylation of the hemagglutinin influence the virulence of influenza H5N1 viruses for mice. J Virol, 83: 4704–4708.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Mok CKP, Yen HL, Yu MYM, Yuen KM, Sia SF, Chan MCW, Qin G, Tu WW, Peiris JSM. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Monne I, Meseko C, Joannis T, Shittu I, Ahmed M, Tassoni L, Fusaro A, Cattoli G. 2015. Highly pathogenic avian influenza A (H5N1) Virus in poultry, Nigeria, 2015. Emerg Infect Dis, 21: 1275–1277.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Naguib MM, Kinne J, Chen H, Chan KH, Joseph S, Wong PC, Woo PC, Wernery R, Beer M, Wernery U, Harder TC. 2015. Outbreaks of highly pathogenic avian influenza H5N1 Clade 2.3.2.1c in hunting falcons and kept wild birds in Dubai implicate intercontinental virus spread. J Gen Virol, 96: 3212–3212.CrossRefPubMedGoogle Scholar
  15. Pabbaraju K, Tellier R, Wong S, Li Y, Bastien N, Tang JW, Drews SJ, Jang Y, Davis CT, Fonseca K, Tipples GA. 2014. Full-genome analysis of avian influenza A(H5N1) virus from a human, North America, 2013. Emerg Infect Dis, 20: 887–891.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Pinto LH, Holsinger LJ, Lamb RA. 1992. Influenza virus M2 protein has ion channel activity. Cell, 69: 517–528.CrossRefPubMedGoogle Scholar
  17. Sakoda Y, Ito H, Uchida Y, Okamatsu M, Yamamoto N, Soda K, Nomura N, Kuribayashi S, Shichinohe S, Sunden Y, Umemura T, Usui T, Ozaki H, Yamaguchi T, Murase T, Ito T, Saito T, Takada A, Kida H. 2012. Reintroduction of H5N1 highly pathogenic avian influenza virus by migratory water birds, causing poultry outbreaks in the 2010–2011 winter season in Japan. J Gen Virol, 93: 541–550.CrossRefPubMedGoogle Scholar
  18. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30: 1312–1313.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Stevens J, Blixt O, Tumpey TM, Taubenberger JK, Paulson JC, Wilson IA. 2006. Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science, 312: 404–410.CrossRefPubMedGoogle Scholar
  20. Subbarao EK, London W, Murphy BR. 1993. A single amino-acid in the Pb2-Gene of influenza a virus is a determinant of host range. J Virol, 67: 1761–1764.PubMedPubMedCentralGoogle Scholar
  21. Verhagen JH, Herfst S, Fouchier RAM. 2015. How a virus travels the world. Science, 347: 616–617.CrossRefPubMedGoogle Scholar
  22. Wang G, Zhan D, Li L, Lei F, Liu B, Liu D, Xiao H, Feng Y, Li J, Yang B, Yin Z, Song X, Zhu X, Cong Y, Pu J, Wang J, Liu J, Gao GF, Zhu Q. 2008. H5N1 avian influenza re-emergence of Lake Qinghai: phylogenetic and antigenic analyses of the newly isolated viruses and roles of migratory birds in virus circulation. J Gen Virol, 89: 697–702.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Webster RG, Peiris M, Chen H, Guan Y. 2006. H5N1 outbreaks and enzootic influenza. Emerg Infect Dis, 12: 3–8.CrossRefPubMedPubMedCentralGoogle Scholar
  24. World Health Organization (WHO. 2014). Revised and updated nomenclature for highly pathogenic avian influenza A (H5N1) viruses. Influenza Other Respir Viruses, 8: 384–388.CrossRefGoogle Scholar
  25. Zhang W, Shi Y, Lu XS, Shu YL, Qi JX, Gao GF. 2013. An airborne transmissible avian influenza H5 hemagglutinin seen at the atomic level. Science, 340: 1463–1467.CrossRefPubMedGoogle Scholar
  26. Zhou B, Pearce MB, Li Y, Wang JR, Mason RJ, Tumpey TM, Wentworth DE. 2013. Asparagine substitution at PB2 residue 701 enhances the replication, pathogenicity, and transmission of the 2009 pandemic H1N1 influenza A virus. PloS One, 8.Google Scholar
  27. Zhou H, Yu Z, Hu Y, Tu J, Zou W, Peng Y, Zhu J, Li Y, Zhang A, Yu Z. 2009. The special neuraminidase stalk-motif responsible for increased virulence and pathogenesis of H5N1 influenza A virus. PLoS One, 4: e6277.CrossRefGoogle Scholar

Copyright information

© Wuhan Institute of Virology, CAS and Springer Science+Business Media Singapore 2016

Authors and Affiliations

  • Yuhai Bi
    • 1
    • 3
    • 6
  • Jianjun Chen
    • 2
    • 7
  • Zhenjie Zhang
    • 4
  • Mingxin Li
    • 2
  • Tianlong Cai
    • 5
  • Kirill Sharshov
    • 7
  • Ivan Susloparov
    • 7
  • Alexander Shestopalov
    • 7
  • Gary Wong
    • 3
  • Yubang He
    • 8
  • Zhi Xing
    • 8
  • Jianqing Sun
    • 8
  • Di Liu
    • 3
  • Yingxia Liu
    • 1
  • Lei Liu
    • 1
  • Wenjun Liu
    • 3
    • 6
  • Fumin Lei
    • 5
    • 6
  • Weifeng Shi
    • 4
  • George F. Gao
    • 1
    • 3
    • 6
    • 9
  1. 1.Shenzhen Key Laboratory of Pathogen and Immunity, State Key Discipline of Infectious DiseaseShenzhen Third People’s HospitalShenzhenChina
  2. 2.CAS Key Laboratory of Special Pathogens and BiosafetyWuhan Institute of Virology Chinese Academy of SciencesWuhanChina
  3. 3.CAS Key Laboratory of Pathogenic Microbiology and Immunology (CASPMI), Institute of MicrobiologyChinese Academy of SciencesBeijingChina
  4. 4.Institute of Pathogen BiologyTaishan Medical CollegeTaishanChina
  5. 5.CAS Key Laboratory of Zoological Systematics and Evolution, Institute of ZoologyChinese Academy of SciencesBeijingChina
  6. 6.Center for Influenza Research and Early-warning (CASCIRE)Chinese Academy of SciencesBeijingChina
  7. 7.Research Institute of Experimental and Clinical MedicineNovosibirsk State UniversityNovosibirskRussia
  8. 8.Qinghai Lake National Nature ReserveState Forestry AdministrationXiningChina
  9. 9.Office of Director-General, Chinese Center for Disease Control and Prevention (China CDC), and Collaborative Innovation Center for Diagnosis and Treatment of Infectious DiseaseZhejiang UniversityHangzhouChina

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