Virus Genes

, Volume 36, Issue 2, pp 345–353 | Cite as

Characterization of the complete genome of influenza A (H5N1) virus isolated during the 2006 outbreak in poultry in India

  • Koninika Ray
  • Varsha A. Potdar
  • Sarah S. Cherian
  • Shailesh D. Pawar
  • Santosh M. Jadhav
  • Shamal R. Waregaonkar
  • Anshu A. Joshi
  • Akhilesh C. Mishra
Article

Abstract

An outbreak of highly pathogenic avian influenza A (H5N1) virus in poultry was reported from Nandurbar and Jalgaon districts of Maharashtra and adjoining areas of Uchhal in Gujarat and Burhanpur in Madhya Pradesh in India from January to April, 2006. In the present study, the full genome of two previously uncharacterized strains of H5N1 viruses isolated at the National Institute of Virology (NIV), Pune, from post-mortem tissues of chicken collected from Navapur, Nandurbar district during the outbreak, has been presented. All the genes belong to clade 2.2 of the Z genotype and are close to the 2006 isolates from Iran, Afghanistan, Mongolia, Italy, and Krasnodar. In a study reported earlier, based on the partial gene sequences of HA, the authors (Pattnaik et al.) hypothesized that the viruses in Jalgaon and Navapur, causing outbreaks 12 days apart, were introduced at different times from different sources. However, our Navapur isolates are closer to the isolate reported from Jalgaon than that from Navapur. Molecular markers suggest that the isolates are sensitive to both drugs Oseltamivir and Amantadine. Amino acid residues responsible for pathogenesis, glycosylation, and receptor binding have also been discussed. The relationship between the Indian viruses and those in the East Africa/West-Asia flyway of migratory birds and the position of Nandurbar in this route suggests that the viruses in India may have been introduced through migratory birds although the role of trade as a possible route of introduction of the virus cannot be ruled out.

Keywords

Highly Pathogenic Avian Influenza (HPAI) H5N1 India Clade 2.2 Poultry 

Notes

Acknowledgments

The work described was supported by the Intramural Grant of the National Institute of Virology, Pune (Indian Council of Medical Research, Government of India). The authors wish to thank Dr. A. Chakrabarty, Mr. A. Walimbe, Mr. G. Prabhakar, Mr. N. Mishra, and Mr. S. Ranawade for scientific discussions, bioinformatics analyses and help in the laboratory. We are grateful to Drs. M. Chadhha and D. Mourya for their support.

References

  1. 1.
    X. Xu, K. Subbarao, N.J. Cox, Y. Guo, Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: similarity of its hemagglutinin gene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong. Virology 261, 15–19 (1999)PubMedCrossRefGoogle Scholar
  2. 2.
    K.S. Li, Y. Guan, J. Wang et al., Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 430, 209–213 (2004)PubMedCrossRefGoogle Scholar
  3. 3.
    H. Chen, G.J.D. Smith, S.Y. Zhang, K. Qin, J. Wang, K.S. Li, et al., Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature 436, 191–192 (2005)PubMedCrossRefGoogle Scholar
  4. 4.
    World Organization for Animal Health (2006) Update on avian influenza in animals (Type H5), available at http://www.oie.int/downld/avianinfluenza/A_AI-Asia.htm. Accessed 21 Nov 2006
  5. 5.
    H. Chen, Y. Li, Z. Li, J. Shi, K. Shinya, G. Deng et al., Properties and dissemination of H5N1 viruses isolated during an influenza outbreak in migratory waterfowl in Western China. J. Virol. 80, 5976–5983 (2006)PubMedCrossRefGoogle Scholar
  6. 6.
    G.J. Smith, X.H. Fan, J. Wang, et al., Emergence and predominance of an H5N1 influenza variant in China. Proc. Natl. Acad. Sci. U.S.A. 103, 16936–16941 (2006)PubMedCrossRefGoogle Scholar
  7. 7.
    Avian Influenza in India, Follow-up report No. 4 (final report) http://www.oie.int/eng/info/hebdo/AIS_05.HTM#Sec5. Vol. 19, No. 33, Accessed 17 Aug 2006
  8. 8.
    B. Pattnaik, A.K. Pateriya, R. Khandia, C. Tosh, S. Nagarajan, S. Gounalan, et al., Phylogenetic analysis revealed genetic similarity of the H5N1 avian influenza viruses isolated from HPAI outbreaks in chickens in Maharashtra, India with those isolated from swan in Italy and Iran in 2006. Curr. Sci. 91, 77–81 (2006)Google Scholar
  9. 9.
    R. Webster, N. Cox, K. Stöhr, Laboratory procedures, in WHO Manual on Animal Influenza Diagnosis and Surveillance, 2nd edn. 15–65 (2002)Google Scholar
  10. 10.
    A.P. Kendal, M.S. Pereira, J.J. Skehel, Hemagglutinin inhibition. in Concepts and Procedures for Laboratory-Based Influenza Surveillance, ed. by A.P. Kendal, M.S. Pereira, J.J. Skehel, (Centers for Disease Control and Prevention an Pan American Health Organization, Atlanta, 1982), pp. B17–B35Google Scholar
  11. 11.
    Recommended laboratory tests to identify avian influenza A virus in specimens from humans. WHO June 2005. Available at http://www.who.int/csr/disease/avian_influenza/guidelines/avian-labtests2.pdf. Accessed 21 Nov 2006
  12. 12.
    E. Hoffmann, J. Stech, Y. Guan, R.G. Webster, D.R. Perez, Universal primer set for the full-length amplification of all influenza A viruses. Arch. Virol. 146, 2275–2289 (2001)PubMedCrossRefGoogle Scholar
  13. 13.
    The World Health Organization Global Influenza Program Surveillance Network, Evolution of H5N1 avian influenza viruses in Asia. Emerg. Infect. Dis. 11, 1515–1521 (2005)Google Scholar
  14. 14.
    D.G. Higgins, J.D. Thompson, T.J. Gibson, Using CLUSTAL for multiple sequence alignments. Meth. Enzymol. 2666, 383–402 (1996)CrossRefGoogle Scholar
  15. 15.
    S. Kumar, K. Tamura, M. Nei, MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5, 150–163 (2004)PubMedCrossRefGoogle Scholar
  16. 16.
    D.L. Swofford, PAUP*: Phylogenetic Analysis Using Parsimony (and other methods) 4.0 Beta. (Sinauer Associates, Sunderland, MA, 2002)Google Scholar
  17. 17.
    E. De Castro, C.J.A. Sigrist, A. Gattiker, V. Bulliard, S. Petra, Langendijk-Genevaux PS et al. ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res. 34, W362–W365 (2006)PubMedCrossRefGoogle Scholar
  18. 18.
    J. Stevens, O. Blixt, T.M. Tumpey, J.K. Taubenberger, J.C. Paulson, I.A. Wilson, Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 312, 404–412 (2006)PubMedCrossRefGoogle Scholar
  19. 19.
    R.J. Russell, L.F. Haire, D.J. Stevens, P.J. Collins, Y.P. Lin, G.M. Blackburn, A.J. Hay, S.J. Gamblin, J.J. Skehel, The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature 443, 45–49 (2006)PubMedCrossRefGoogle Scholar
  20. 20.
    A. Sali, T.L. Blundell, Comparative protein modeling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779–815 (1993)PubMedCrossRefGoogle Scholar
  21. 21.
    N. Guex M.C. Peitsch, SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18, 2714 (1997)CrossRefGoogle Scholar
  22. 22.
    M. Shaw L. Cooper, X. Xu et al., Molecular changes associated with the transmission of avian influenza A H5N1 and H9N2 viruses to humans. J. Med. Virol. 66, 107–114 (2002)CrossRefGoogle Scholar
  23. 23.
    G. Gabriel, B. Dauber, T. Wolff, O. Planz, H.D. Klenk, J. Stech, The viral polymerase mediates adaptation of an avian inßuenza virus to a mammalian host. Proc. Natl. Acad. Sci. U.S.A. 102, 18590–18595 (2005)PubMedCrossRefGoogle Scholar
  24. 24.
    J.M. Katz, X. Lu, T.M. Tumpey, C.B. Smith, M.W. Shaw, K. Subbarao, Molecular correlates of influenza A H5N1 virus pathogenesis in mice. J. Virol. 74, 10807–10810 (2000)PubMedCrossRefGoogle Scholar
  25. 25.
    A.S. Lipatov, S. Andreansky, R.J. Webby, D.J. Hulse, J.E. Rehg, S.S. Krause, et al., Pathogenesis of Hong Kong H5N1 influenza virus NS gene reassortants in mice: the role of cytokines and B- and T-cell responses. J. Gen. Virol. 86, 1121–1130 (2005)PubMedCrossRefGoogle Scholar
  26. 26.
    H. Suzuki, R. Saito, H. Masuda, H. Oshitani, M. Sato, I. Sato, Emergence of amantadine-resistant influenza A viruses: epidemiological study. J. Infect. Chemother. 9, 195–200 (2003)PubMedCrossRefGoogle Scholar
  27. 27.
    S.L. Salzberg, C. Kingsford, G. Cattoli, D.J. Spiro, D.A. Janies, M.M. Aly, et al., Genome analysis linking recent European and African influenza (H5N1) viruses. Emerg. Infect. Dis. 13(5), 713–718 (2007)PubMedGoogle Scholar
  28. 28.
    P. Puthavathana, P. Auewarakul, P.C. Charoenying, K. Sangsiriwut, P. Pooruk, K. Boonnak, et al., Molecular characterization of the complete genome of human influenza H5N1 virus isolates from Thailand. J. Gen. Virol. 86, 423–433 (2005)PubMedCrossRefGoogle Scholar
  29. 29.
    M.N. Matrosovich, N. Zhou, Y. Kawaoka, R. Webster, The surface glycoproteins of H5 influenza viruses isolated from humans, chicken, and wild aquatic birds have distinguishable properties. J. Virol. 73, 1146–1155 (1999)PubMedGoogle Scholar
  30. 30.
    H.K. Iwatsuki, R. Kanazawa, S. Sugii, Y. Kawaoka, T. Horimoto, The index influenza A virus subtype H5N1 isolated from a human in 1997 differs in its receptor binding properties from a virulent influenza virus. J. Gen. Virol. 85, 1001–1005 (2004)CrossRefGoogle Scholar
  31. 31.
    M.N. Matrosovich, T.Y. Matrosovich, T. Gray, N.A. Roberts, H.D. Klenk, Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc. Natl. Acad. Sci. U.S.A. 101, 4620–4624 (2004)PubMedCrossRefGoogle Scholar
  32. 32.
    J.A. Kim, S.Y. Ryu, S.H. Seo, Cells in the respiratory and intestinal tracts of chicken have different proportions of both human and avian influenza virus receptors. J. Microbiol. 43, 366–369 (2005)PubMedGoogle Scholar
  33. 33.
    O. Werner T.C. Harder, Avian influenza. in Influenza Report 2006, ed. by B.S. Kamps C. Hoffmann W. Preiser (Flying Publisher, Paris, 2006) pp. 48–86Google Scholar
  34. 34.
    K. Shinya, S. Hamm, M. Hatta, H. Ito, T. Ito, Y. Kawaoka, 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 (2004)PubMedCrossRefGoogle Scholar
  35. 35.
    Z. Li, H. Chen, P. Jiao, G. Deng, G. Tian, Y. Li et al., Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model. J. Virol. 79, 12058–12064 (2005)PubMedCrossRefGoogle Scholar
  36. 36.
    W.J. Bean, S.C. Threlkeld, R.G. Webster, Biologic potential of amantadine-resistant influenza A virus in an avian model. J. Infect. Dis. 159, 1050–1056 (1989)PubMedGoogle Scholar
  37. 37.
    G. Boivin, N. Goyette, H. Bernatchez, Prolonged excretion of amantadine-resistant influenza A virus quasi species after cessation of antiviral therapy in an immunocompromised patient. Clin. Infect. Dis. 34, E23–E25 (2002)PubMedCrossRefGoogle Scholar
  38. 38.
    C. Sweet F.G. Hayden K.J. Jakeman S. Grambas A.J. Hay, Virulence of rimantadine-resistant human influenza A (H3N2) viruses in ferrets. J. Infect. Dis. 162 969–972 (1991)Google Scholar
  39. 39.
    F.G. Hayden, R.B. Belshe, R.D. Clover, A.J. Hay, M.G. Oakes, W. Soo, Emergence and apparent transmission of rimantadine-resistant influenza A virus in families. N. Engl. J. Med. 321, 1696–1702 (1989)PubMedCrossRefGoogle Scholar
  40. 40.
    WHO inter-country-consultation: influenza A/H5N1 in humans in Asia: Manila, Philippines, http://www.who.int/csr/resources/publications/influenza/WHO_CDS_CSR_GIP_2005_7/en/. Accessed 6–7 May 2005
  41. 41.
    M.A. Rameix-Welti, F. Agou, P. Buchy, S. Mardy, J.T. Aubin, M.S. Véron et al., Natural variation can significantly alter the sensitivity of influenza A (H5N1) viruses to oseltamivir. Antimicrob. Agents Chemother. 50, 3809–3815 (2006)PubMedCrossRefGoogle Scholar
  42. 42.
    B. Olsen, V. Munster, A. Wallensten, J. Waldenström, A.D.M.E. Osterhaus, R.A.M. Fouchier, Global patterns of influenza A virus in wild birds. Science 312, 384–388 (2006)PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Koninika Ray
    • 1
  • Varsha A. Potdar
    • 2
  • Sarah S. Cherian
    • 2
  • Shailesh D. Pawar
    • 1
  • Santosh M. Jadhav
    • 2
  • Shamal R. Waregaonkar
    • 2
  • Anshu A. Joshi
    • 2
  • Akhilesh C. Mishra
    • 2
  1. 1.Microbial Containment ComplexNational Institute of VirologyPuneIndia
  2. 2.National Institute of VirologyPuneIndia

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