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Emergence of amantadine-resistant avian influenza H5N1 virus in India

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Abstract

This study reports the genetic characterization of highly pathogenic avian influenza (HPAI) virus (subtype H5N1) isolated from poultry in West Bengal, India. We analyzed all the eight genome segments of two viruses isolated from chickens in January 2010 to understand their genetic relationship with other Indian H5N1 isolates and possible connection between different outbreaks. The hemagglutinin (HA) gene of the viruses showed multiple basic amino acids at the cleavage site, a marker for high virulence in chickens. Of greatest concern was that the viruses displayed amino acid substitution from serine-to-asparagine at position 31 of M2 ion channel protein suggesting emergence of amantadine-resistant mutants not previously reported in HPAI H5N1 outbreaks in India. Amino acid lysine at position 627 of the PB2 protein highlights the risk the viruses possess to mammals. In the phylogenetic trees, the viruses clustered within the lineage of avian isolates from India (2008–2009) and avian and human isolates from Bangladesh (2007–2009) in all the genes. Both these viruses were most closely related to the viruses from 2008 in West Bengal within the subclade 2.2.3 of H5N1 viruses.

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References

  1. X. Xu, E.K. Subbarao, N.J. Cox, Y. Guo, Virology 261, 15 (1999)

    Article  PubMed  CAS  Google Scholar 

  2. K.S. Li, Y. Guan, J. Wang, G.J. Smith, K.M. Xu, L. Duan, A.P. Rahardjo, P. Puthavathana, C. Buranathai, T.D. Nguyen, A.T. Estoepangestie, A. Chaisingh, P. Auewarakul, H.T. Long, N.T. Hanh, R.J. Webby, L.L. Poon, H. Chen, K.F. Shortridge, K.Y. Yuen, R.G. Webster, J.S. Peiris, Nature 430, 209 (2004)

    Article  PubMed  CAS  Google Scholar 

  3. H. Chen, G.J.D. Smith, K.S. Li, J. Wang, X.H. Fan, J.M. Rayner, D. Vijaykrishna, J.X. Zhang, L.J. Zhang, C.T. Guo, C.L. Cheung, K.M. Xu, L. Duan, K. Huang, K. Qin, Y.H.C. Leung, W.L. Wu, H.R. Lu, Y. Chen, N.S. Xia, T.S.P. Naipospos, K.Y. Yuen, S.S. Hassan, S. Bahri, T.D. Nguyen, R.G. Webster, J.S.M. Peiris, Y. Guan, Proc. Natl. Acad. Sci. USA 103, 2845 (2006)

    Article  PubMed  CAS  Google Scholar 

  4. H. Chen, G.J.D. Smith, S.Y. Zhang, K. Qin, J. Wang, K.S. Li, R.G. Webster, J.S.M. Peiris, Y. Guan, Nature 436, 191 (2005)

    Article  PubMed  CAS  Google Scholar 

  5. M.F. Ducatez, C.M. Olinger, A.A. Owoade, S. De Landtsheer, W. Ammerlaan, H.G. Niesters, A.D. Osterhaus, R.A. Fouchier, C.P. Muller, Nature 442, 37 (2006)

    Article  PubMed  CAS  Google Scholar 

  6. A.S. Lipatov, V.A. Evseenko, H.L. Yen, A.V. Zaykovskaya, A.G. Durimanov, S.I. Zolotykh, V. Netesov, I.G. Drozdov, G.G. Onishchenko, R.G. Webster, A.M. Shestopalov, Emerg. Infect. Dis. 13, 539 (2007)

    Article  PubMed  CAS  Google Scholar 

  7. S. Weber, H. Timm, E. Starick, M. Beer, O. Werner, B. Hoffmann, T.C. Mettenleiter, E. Mundt, J. Gen. Virol. 88, 554 (2007)

    Article  PubMed  CAS  Google Scholar 

  8. A.S. Abdel-Moneim, A.E. Abdel-Ghany, S.A. Shany, J. Biomed. Sci. 17, 25 (2010)

    Article  PubMed  Google Scholar 

  9. A. Amonsin, T. Songserm, S. Chutinimitkul, R. Jam-On, N. Sae-Heng, N. Pariyothorn, S. Payungporn, A. Theamboonlers, Y. Poovorawan, Arch. Virol. 152, 1925 (2007)

    Article  PubMed  CAS  Google Scholar 

  10. A. Amonsin, S. Payungporn, A. Theamboonlers, R. Thanawongnuwech, S. Suradhat, N. Pariyothorn, R. Tantilertcharoen, S. Damrongwantanapokin, C. Buranathai, A. Chaisingh, T. Songserm, Y. Poovorawan, Virology 344, 480 (2006)

    Article  PubMed  CAS  Google Scholar 

  11. J. Keawcharoen, K. Oraveerakul, T. Kuiken, R.A. Fouchier, A. Amonsin, S. Payungporn, S. Noppornpanth, S. Wattanodorn, A. Theambooniers, R. Tantilertcharoen, R. Pattanarangsan, N. Arya, P. Ratanakorn, D.M. Osterhaus, Y. Poovorawan, Emerg. Infect. Dis. 10, 2189 (2004)

    PubMed  Google Scholar 

  12. J.S. Peiris, J. De, Y. Guan, Clin. Microbiol. Rev. 20, 243 (2007)

    Article  PubMed  Google Scholar 

  13. K. Subbarao, A. Klimov, J. Katz, H. Regnery, W. Lim, H. Hall, M. Perdue, D. Swayne, C. Bender, J. Huang, M. Hemphill, T. Rowe, M. Shaw, X. Xu, K. Fukuda, N. Cox, Science 279, 393 (1998)

    Article  PubMed  CAS  Google Scholar 

  14. A.S. Monto, Vaccine 21, 1796 (2003)

    Article  PubMed  CAS  Google Scholar 

  15. C.L. Cheung, J.M. Rayner, G.J. Smith, P. Wang, T.S. Naipospos, J. Zhang, K.Y. Yuen, R.G. Webster, J.S. Peiris, Y. Guan, H. Chen, J. Infect. Dis. 193, 1626 (2006)

    Article  PubMed  CAS  Google Scholar 

  16. I. Monne, A. Fusaro, A. Hamad, M.H. AI-Blowi, M.M. Ismail, O.A. Khan, G. Dauphin, A. Tripodi, A. Salviato, S. Marangon, I. Capua, G. Cattoli, J. Gen. Virol. 89, 2691 (2008)

    Article  PubMed  CAS  Google Scholar 

  17. B. Pattnaik, A.K. Pateriya, R. Khandia, C. Tosh, S. Nagarajan, S. Gounalan, H.V. Murugkar, B.P. Shankar, N. Shrivastava, P. Behera, S. Bhagat, J.S.M. Peiris, H.K. Pradhan, Curr. Sci. 91, 77 (2006)

    CAS  Google Scholar 

  18. C. Tosh, H.V. Murugkar, S. Nagarajan, S. Bhatia, A.K. Pateriya, P. Behera, R. Jain, S. Kumar, R. Khandia, P.R. Vanamayya, S.C. Dubey, S.P.S. Ahlawat, Vet. Rec. 161, 279 (2007)

    Article  PubMed  CAS  Google Scholar 

  19. H.V. Murugkar, S. Nagarajan, C. Tosh, S. Bhatia, G. Venkatesh, R. Jain, S. Kumar, R. Khandia, M. Pandey, P. Behera, S. Tripathy, D.D. Kulkarni, S.C. Dubey, Vet. Rec. 162, 255 (2008)

    Article  PubMed  CAS  Google Scholar 

  20. S. Nagarajan, H.V. Murugkar, C. Tosh, P. Behera, R. Jain, S. Tripathi, R. Khandia, V. Gupta, D.D. Kulkarni, S.C. Dubey, Vet. Rec. 164, 128 (2009)

    Article  PubMed  CAS  Google Scholar 

  21. A.K. Chakrabarti, S.D. Pawar, S.S. Cherian, S.S. Koratkar, S.M. Jadhav, B. Pal, S. Raut, V. Thite, S.S. Kode, S.S. Keng, B.J. Payyapilly, J. Mullick, A.C. Mishra, PLoS ONE 4(11), e7846 (2009). doi:10.1371/journal.pone.0007846

    Article  PubMed  Google Scholar 

  22. A.C. Mishra, S.S. Cherian, A.K. Chakrabarti, S.D. Pawar, S.M. Jadhav, B. Pal, S. Raut, S. Koratkar, S.S. Kode, Virol. J. 6, 26 (2009)

    Article  PubMed  Google Scholar 

  23. S. Nagarajan, C. Tosh, H.V. Murugkar, G. Venkatesh, M. Katare, R. Jain, P. Behera, R. Khandia, S. Tripathi, D.D. Kulkarni, S.C. Dubey, Virus Genes 41, 30 (2010)

    Article  PubMed  CAS  Google Scholar 

  24. K. Ray, V.A. Potdar, S.S. Cherian, S.D. Pawar, S.M. Jadhav, S.R. Waregaonkar, A.A. Joshi, A.C. Mishra, Virus Genes 36, 345 (2008)

    Article  PubMed  CAS  Google Scholar 

  25. OIE (2010), http://www.oie.int/downld/Avian%20INFLUENZA/A2006_AI.php. Accessed 5 Feb 2010

  26. S. Nagarajan, K. Rajukumar, C. Tosh, V. Ramaswamy, K. Purohit, G. Saxena, P. Behera, B. Pattnaik, H.K. Pradhan, S.C. Dubey, Vet. Microbiol. 133, 154 (2009)

    Article  PubMed  CAS  Google Scholar 

  27. OIE, Chapter 2.3.4 (OIE, Paris, France, 2008)

    Google Scholar 

  28. E. Hoffmann, J. Stech, Y. Guan, R.G. Webster, D.R. Perez, Arch. Virol. 146, 2275 (2001)

    Article  PubMed  CAS  Google Scholar 

  29. T.A. Hall, Nucl. Acids Symp. Ser. 41, 95 (1999)

    CAS  Google Scholar 

  30. K. Tamura, J. Dudley, M. Nei, S. Kumar, Mol. Biol. Evol. 24, 1596 (2007)

    Article  PubMed  CAS  Google Scholar 

  31. L. Duan, J. Bahl, G.J.D. Smith, J. Wang, D. Vijaykrishna, L.J. Zhang, J.X. Zhang, K.S. Li, X.H. Fan, C.L. Cheung, K. Huang, L.L.M. Poon, K.F. Shortridge, R.G. Webster, J.S.M. Peiris, H. Chen, Y. Guan, Virology 380, 243 (2008)

    Article  PubMed  CAS  Google Scholar 

  32. WHO/OIE/FAO H5N1 Evolution working group. Emerg. Infect. Dis. 14 (2008), (http://www.cdc.gov/EID/content/14/7/e1.html)

  33. I.A. Rudneva, A.A. Kushch, O.V. Masalova, T.A. Timofeeva, R.R. Klimova, A.A. Shilov, A.V. Ignatieva, P.S. Krylov, N.V. Kaverin, Viral Immunol. 23, 181 (2010)

    Article  PubMed  CAS  Google Scholar 

  34. G.J. Smith, X.H. Fan, J. Wang, K.S. Li, K. Qin, J.X. Zhang, D. Vijaykrishna, C.L. Cheung, K. Huang, J.M. Rayner, J.S. Peiris, H. Chen, R.G. Webster, Y. Guan, Proc. Natl. Acad. Sci. USA 103, 16936 (2006)

    Article  PubMed  CAS  Google Scholar 

  35. W.L. Wu, Y. Chen, P. Wang, W. Song, S.-Y. Lau, J.M. Rayner, G.J.D. Smith, R.G. Webster, J.S.M. Peiris, T. Lin, N. Xia, Y. Guan, H. Chen, J. Virol. 82, 1798 (2008)

    Article  PubMed  CAS  Google Scholar 

  36. Y. Ha, D.J. Stevens, J.J. Skehel, D.C. Wiley, Proc. Natl. Acad. Sci. USA 98, 11181 (2001)

    Article  PubMed  CAS  Google Scholar 

  37. N.A. Ilyushina, J.P. Seiler, R.G. Webster, E.A. Govorkova, Antiviral Res. 82, A71 (2009)

    Article  Google Scholar 

  38. N.A. Ilyushina, E.A. Govorkova, R.G. Webster, Virology 341, 102 (2005)

    Article  PubMed  CAS  Google Scholar 

  39. A.C. Hurt, P. Selleck, N. Komadina, R. Shaw, L. Brown, I.G. Barr, Antiviral Res. 73, 228 (2007)

    Article  PubMed  CAS  Google Scholar 

  40. Q. He, J. Qiao, C. Dong, C. He, L. Zhao, Y. Tian, Antiviral Res. 77, 72 (2008)

    Article  PubMed  CAS  Google Scholar 

  41. T. Ziegler, M.L. Hemphill, M.L. Ziegler, G. Perez-Oronoz, A.I. Klimov, A.W. Hampson, H.L. Regnery, N.J. Cox, J. Infect. Dis. 180, 4 (1999)

    Article  Google Scholar 

  42. G. Gabriel, B. Dauber, T. Wolff, O. Planz, H.D. Klenk, J. Stech, Proc. Natl. Acad. Sci. USA 102, 18590 (2005)

    Article  PubMed  CAS  Google Scholar 

  43. M. Hatta, P. Gao, P. Halfmann, Y. Kawaoka, Science 293, 1840 (2001)

    Article  PubMed  CAS  Google Scholar 

  44. G.W. Chen, S.C. Chang, C.K. Mok, Y.L. Lo, Y.N. Kung, J.H. Huang, Y.H. Shih, J.Y. Wang, C. Chiang, C.J. Chen, S.R. Shih, Emerg. Infect. Dis. 12, 1353 (2006)

    PubMed  CAS  Google Scholar 

  45. S.H. Seo, E. Hoffmann, R.G. Webster, Nat. Med. 8, 950 (2002)

    Article  PubMed  CAS  Google Scholar 

  46. J.C. Obenauer, J. Denson, P.K. Mehta, X. Su, S. Mukatira, D.B. Finkelstein, X. Xu, J. Wang, J. Ma, Y. Fan, K.M. Rakestraw, R.G. Webster, E. Hoffmann, S. Krauss, J. Zheng, Z. Zhang, C.W. Naeve, Science 311, 1576 (2006)

    Article  PubMed  CAS  Google Scholar 

  47. D. Jackson, J.M. Hosain, D. Hickman, D.R. Perez, R.A. Lamb, Proc. Natl. Acad. Sci. USA 105, 4381 (2008)

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Director, Indian Veterinary Research Institute and Indian Council of Agricultural Research, New Delhi for providing necessary facilities to carry out this work. We also thank two anonymous referees for valuable suggestions on the improvement of the manuscript. We are thankful to the Department of Animal Husbandry, Dairying and Fisheries, Ministry of Agriculture, Government of India for financial support through CDDL for Avian influenza diagnosis and research grant. The authors wish to thank the State Animal Husbandry Department, West Bengal for providing the clinical materials.

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Authors and Affiliations

  1. High Security Animal Disease Laboratory, Indian Veterinary Research Institute, Anand Nagar, Bhopal, 462021, India

    C. Tosh, H. V. Murugkar, S. Nagarajan, S. Tripathi, M. Katare, R. Jain, R. Khandia, Z. Syed, P. Behera, S. Patil, D. D. Kulkarni & S. C. Dubey

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  1. C. Tosh
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  2. H. V. Murugkar
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  3. S. Nagarajan
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Correspondence to C. Tosh.

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11262_2010_534_MOESM1_ESM.ppt

Supplementary Figure S1. Phylogenetic relationships of the PB2 (a), PB1 (b), PA (c), NP (d), M (e) and NS (f) genes of representative influenza A viruses. The sequence regions compared were as follows: nucleotide positions 28-2304 of PB2, 25-2295 of PB1, 25-2172 of PA, 46-1539 of NP, 26-1006 of M and 27-869 of NS. The trees were rooted to A/goose/Guangdong/1/1996. Numbers near the node indicates bootstrap values of ≥70%. Scale bar indicates nucleotide substitutions per site. The Bangladesh/India sub-cluster is highlighted. *Indicate isolates sequenced in this study. (PPT 343 kb)

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Tosh, C., Murugkar, H.V., Nagarajan, S. et al. Emergence of amantadine-resistant avian influenza H5N1 virus in India. Virus Genes 42, 10–15 (2011). https://doi.org/10.1007/s11262-010-0534-z

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