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Genetic characterization of the NS gene indicates co-circulation of two sub-lineages of highly pathogenic avian influenza virus of H5N1 subtype in Northern Europe in 2006

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Abstract

The non-structural (NS) gene of highly pathogenic avian influenza viruses of the H5N1 subtype (HPAI-H5N1) isolated in Baltic Sea area of Sweden in 2006 was studied. The phylogenetic analysis data demonstrated that two distinct sub-lineages of HPAI-H5N1 were circulating during the outbreak in Northern Europe in Spring 2006. Sub-lineage I viruses fell into the same clade as viruses found in Denmark and Germany and formed a sub-clade which also included viruses isolated in the Russian Federation in late 2005. Sub-lineage II viruses formed a sub-clade closely related to European, Middle Eastern and African isolates reported in 2006. Analysis of the inferred amino acid sequences of the NS1 protein showed a deletion of five amino acids at positions 80–84. No viruses represented in this study contained Glu92 in the NS1 and all isolates contained the avian-like ESKV amino acid sequences at the NS1 C-terminal end. Sub-lineage I isolates contained unique substitutions V194I in NS1 and G63E in Nuclear export protein (NEP).

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References

  1. X. Xu, K. Subbatao, N.J. Cox, Y. Guo, Virology 261, 15–19 (1999)

    Article  PubMed  CAS  Google Scholar 

  2. K. Subbarao, A. Klimov, J. Katz, H. Regnery, W. Lim, H. Hall, M. Perdue, D. Swayne, C. Bender, J. Huang, M. Hemphil, T. Rowe, M. Shaw, X. Xu, K. Fukuda, N.J. Cox, Science 279, 393–396 (1998)

    Article  PubMed  CAS  Google Scholar 

  3. L.D. Sims, J. Domenech, C. Benigno, S. Kahn, A. Kamata, J. Lubroth, V. Martin, P. Roeder, Vet. Rec. 157, 159–164 (2005)

    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, 191–192 (2005)

    Article  PubMed  CAS  Google Scholar 

  5. T.M. Ellis, R.B. Bousfield, L.A. Bisset, K.C. Dyrting, G.S.M. Luk, S.T. Tsim, K. Sturm-Ramirez, R.G. Webster, Y. Guan, J.S.M. Peiris, Avian Pathol. 33, 492–505 (2004)

    Article  PubMed  Google Scholar 

  6. World Health Organization (http://www.who.int/csr/disease/avian_influenza/timeline2007_06_21.pdf). Accessed 21 June 2007

  7. S. Weber, T. Harder, E. Starick, M. Beer, O. Werner, B. Hoffmann, T.C. Mettenleiter, E. Mundt, J. Gen. Virol. 88, 554–558 (2007)

    Article  PubMed  CAS  Google Scholar 

  8. K. Bragstad, P.H. Jorgensen, K. Handberg, A.S. Hammer, S. Kabell, A. Fomsgaard, Virol. J. 4:43 doi: 10.1186/1743-422x-4-43 (2007)

  9. M. Hatta, P. Gao, P. Halfmann, Y. Kawaoka, Science 293, 1840–1842 (2001)

    Article  PubMed  CAS  Google Scholar 

  10. T. Kuiken, E.C. Holmes, J. MacCauley, G.F. Rimmelzwaan, C.S. Williams, B.T. Grenfell, Science 312, 394–397 (2006)

    Article  PubMed  CAS  Google Scholar 

  11. A. Garcia-Sastre, Virology 279, 375–384 (2001)

    Article  PubMed  CAS  Google Scholar 

  12. R.M. Krug, W. Yuan, D.L. Noah, A.G. Latham, Virology 309, 181–189 (2003)

    Article  PubMed  CAS  Google Scholar 

  13. S. Li, J.Y. Min, R.M. Krug, G.C. Sen, Virology 349, 13–21 (2006)

    Article  PubMed  CAS  Google Scholar 

  14. J.Y. Min, R.M. Krug, Proc. Natl. Acad. Sci. USA 103, 7100–7105 (2006)

    Article  PubMed  CAS  Google Scholar 

  15. J. Talon, C.M. Horvath, R. Polley, C.F. Basler, T. Muster, P. Palese, A. Garcia-Sastre, J. Virol. 74, 7989–7996 (2000)

    Article  PubMed  CAS  Google Scholar 

  16. M. Mibayashi, L. Martinez-Sobrido, Y.M. Loo, W.B. Cardenas, M. Gale, A. Garcia-Sastre, J. Virol. 81, 514–524 (2007)

    Article  PubMed  CAS  Google Scholar 

  17. E. Bucher, H. Hemmes, P. De Haan, R. Goldbach, M. Prins, J. Gen. Virol. 85, 983–991 (2004)

    Article  PubMed  CAS  Google Scholar 

  18. W.X. Li, H. Li, R. Lu, F. Li, M. Dus, P. Atkinson, E.W.A. Brydon, K.L. Johanson, A. Garcia-Sastre, L.A. Ball, P. Palese, S.W. Ding, Proc. Natl. Acad. Sci. USA 101, 1350–1355 (2004)

    Article  PubMed  CAS  Google Scholar 

  19. T. Aragon, S. De La Luna, L. Carrasco, J. Ortin, A. Nieto, Mol. Cell. Biol. 20, 6259–6268 (2000)

    Article  PubMed  CAS  Google Scholar 

  20. N. Satterly, P.L. Tsai, J. Van Deursen, D.R. Nussenzveig, Y. Wang, P.A. Faria, A. Levay, D.A. Levy, B.M.A. Fontoura, Proc. Natl. Acad. Sci. USA 104, 1853–1858 (2007)

    Article  PubMed  CAS  Google Scholar 

  21. M.E. Nemeroff, S.M.L. Barabino, Y. Li, W. Keller, R.M. Krug, Mol. Cell 1, 991–1000 (1998)

    Article  PubMed  CAS  Google Scholar 

  22. Z. Chen, Y. Li, R.M. Krug, EMBO J. 18, 2273–2283 (1999)

    Article  PubMed  CAS  Google Scholar 

  23. Y. Li, Z.Y. Chen, W. Wang, C.C. Baker, R.M. Krug, RNA 7, 920–931 (2001)

    Article  PubMed  CAS  Google Scholar 

  24. Y. Qiu, R.M. Krug, J. Virol. 68, 2425–2432 (1994)

    PubMed  CAS  Google Scholar 

  25. R.A. Lamb, C.J. Lai, Cell 21, 475–485 (1980)

    Article  PubMed  CAS  Google Scholar 

  26. G. Neumann, M.T. Hughes, Y. Kawaoka, EMBO J. 19, 6751–6758 (2000)

    Article  PubMed  CAS  Google Scholar 

  27. H. Akarsu, W.P. Burmeister, C. Petosa, I. Petit, C.W. Muller, W.H. Ruigrok, F. Baudin, EMBO J. 22, 4646–4655 (2003)

    Article  PubMed  CAS  Google Scholar 

  28. E. Spackman, D.A. Senne, L.L. Bulaga, T.J. Myers, M.L. Perdue, L.P. Garber, K. Lohman, L.T. Daum, D.L. Suarez, Avian Dis. 47, 1079–1082 (2003)

    Article  PubMed  CAS  Google Scholar 

  29. M.J. Slomka, V.J. Coward, J. Banks, B.Z. Ouml ndt, I.H. Brown, J. Voermans, G. Koch, K.J. Handberg, P.H. Oslash rgensen, M. Cherbonnel-Pansart, V. Jestin, G. Cattoli, I. Capua, A. Ejdersund, N.P. Thor Eacute, G. Czifra, Avian Dis. 51, 227–234 (2007)

    Article  PubMed  CAS  Google Scholar 

  30. Influenza Virus Resource at National Center for Biotechnology Information (http://www.ncbi.nlm.nih.gov/genomes/FLU/). Accessed 20 June 2007

  31. T.A. Hall, Nucleic Acids Symposium Series. (Oxford University Press, Oxford, 1999), pp. 95–98

    Google Scholar 

  32. S. Kumar, K. Tamura, M. Nei, Bioinformatics 5, 150–163 (2004)

    Article  PubMed  CAS  Google Scholar 

  33. F. Ronquist, J.P. Huelsenbeck, Bioinformatics 19, 1572–1574 (2003)

    Article  PubMed  CAS  Google Scholar 

  34. D.A. Senne, B. Paniagrahy, Y. Kawaoka, J.E. Pearson, J. Suss, M. Lipkind, H. Kida, R.G. Webster, Avian Dis. 40, 425–437 (1996)

    Article  PubMed  CAS  Google Scholar 

  35. S.L. Salzberg, C. Kingsford, G. Cattoli, D.J. Spiro, D.A. Janies, M.M. Aly, I.H. Brown, E. Couacy-Hymann, G.M. De Mia et al., Emerg. Infect. Dis. 13, 713–718 (2007)

    PubMed  CAS  Google Scholar 

  36. E. Hatada, R. Fukuda, J. Gen. Virol. 73, 3325–3329 (1992)

    PubMed  CAS  Google Scholar 

  37. W. Wang, K. Riedel, P. Lynch, C.Y. Chien, G.T. Montelione, R.M. Krug, RNA 5, 195–205 (1999)

    Article  PubMed  CAS  Google Scholar 

  38. H.L. Chen, G.H. Deng, Z.J. Li, G.B. Tian, Y.B. Li, P. Jiao, L. Zhang, Z. Liu, R.G. Webster, K. Yu, Proc. Natl. Acad. Sci. USA 101, 10452–10457 (2004)

    Article  PubMed  CAS  Google Scholar 

  39. S. Seo, E. Hoffmann, R.G. Webster, Nat. Med. 8, 950–954 (2002)

    Article  PubMed  CAS  Google Scholar 

  40. Z. Li, Y. Jiang, P. Jiao, A. Wang, F. Zhao, G. Tian, X. Wang, K. Yu, Z. Bu, H. Chen, J. Virol. 80, 11115–11123 (2006)

    Article  PubMed  CAS  Google Scholar 

  41. G. Kochs, A. Garcia-Sastre, L. Martinez-Sobrido, J. Virol. 81, 7011–7021 (2007)

    Article  PubMed  CAS  Google Scholar 

  42. 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, 1576–1580 (2006)

    Article  PubMed  CAS  Google Scholar 

  43. S. Ludwig, U. Schultz, J. Mandler, W.M. Fitch, C. Scholtissek, Virology 183, 566–577 (1991)

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We would like to thank Professor Berndt Klingeborn for helpful scientific discussions and constant support. Many thanks are due to Natasha Dahnberg for help with layout of the figures. Our appreciation also goes to Dr. Neil LeBlanc for critical review of the manuscript. The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (Formas), financially supported this work.

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Authors and Affiliations

  1. Department of Virology, Joint Research and Development in Virology, National Veterinary Institute (SVA) and the Swedish University of Agricultural Sciences (SLU), Ulls väg 2B, 751 89, Uppsala, Sweden

    Siamak Zohari, Peter Gyarmati, Peter Thorén, Sándor Belák & Mikael Berg

  2. Division of Parasitology and Virology, Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences (SLU), Uppsala, Sweden

    Siamak Zohari, Peter Gyarmati, Peter Thorén, Sándor Belák & Mikael Berg

  3. Department of Virology, National Veterinary Institute (SVA), Ulls väg 2B, 751 89, Uppsala, Sweden

    György Czifra

  4. Department of Wildlife, Fish and Environment, National Veterinary Institute (SVA), Ulls väg 2B, 751 89, Uppsala, Sweden

    Caroline Bröjer

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  1. Siamak Zohari
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Correspondence to Siamak Zohari.

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Zohari, S., Gyarmati, P., Thorén, P. et al. Genetic characterization of the NS gene indicates co-circulation of two sub-lineages of highly pathogenic avian influenza virus of H5N1 subtype in Northern Europe in 2006. Virus Genes 36, 117–125 (2008). https://doi.org/10.1007/s11262-007-0188-7

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