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Variability of NS1 proteins among H9N2 avian influenza viruses isolated in Israel during 2000–2009

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Abstract

The main aims of the present study were to characterize NS1 protein from H9N2 avian influenza viruses (AIVs) isolated in Israel and to investigate the possibility to use NS1-based indirect ELISA. To achieve these purposes, the non-structural gene (NS1) of 79 AIVs of the H9N2 subtype isolated in Israel in 2000–2009 was sequenced and genetically analyzed. The phylogenetic analysis demonstrated that four distinct introductions of H9N2 occurred in Israel during this period. Analysis of the inferred amino acid sequences of the NS1 proteins showed high, about 10%, differences between viruses of the 3rd and 4th introductions. Antibodies against NS1 protein in immune sera were tested by means of indirect ELISA using recombinant NS1 as antigen. Immune sera were obtained from experimentally H9N2-infected chicken after infection on 4, 7, 10, 14, and 21 days. All sera from chickens experimentally infected with 3rd- or 4th-introduction AIV contained anti-NS1 antibodies that were detected by enzyme-linked immunosorbent assay (NS1-ELISA) even though the recombinant NS1 used as antigen for NS1-ELISA differed significantly in its amino acid sequences from the NS1 protein of AIV that caused infection in experimental birds. These findings indicate that the sites of the NS1 protein by which viruses belonging to 3rd and 4th introduction are out of antigenic epitope positions were responsible for the results of NS1-based iELISA.

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References

  1. J.A. Richt, A. Garcia-Sastre, Curr. Top. Microbiol. Immunol. 333, 177–195 (2009)

    Article  CAS  PubMed  Google Scholar 

  2. C. Ehrhardt, R. Seyer, E.R. Hrincius, T. Eierhoff, T. Wolff, S. Ludwig, Microbes Infect. 12, 81–87 (2010)

    Article  CAS  PubMed  Google Scholar 

  3. T. Wolff, F. Zielecki, M. Abt, D. Voss, I. Semmler, M. Matthaei, Biol. Chem. 389, 1299–1305 (2008)

    Article  CAS  PubMed  Google Scholar 

  4. M.U. Gack, R.A. Albrecht, T. Urano, K.-S. Inn, I.-Ch. Huang, E. Carnero, M. Farzan, S. Inoue, J.U. Jung, A. Garcia-Sastre, Cell Host Microbe 5, 439–449 (2009)

    Article  CAS  PubMed  Google Scholar 

  5. K. Das, L.C. Ma, R. Xiao, B. Radvansky, J. Aramini, L. Zhao, J. Marklund, R.L. Kuo, K.Y. Twu, E. Arnold, R.M. Krug, G.T. Montelione, Proc. Natl. Acad. Sci. USA 105, 13093–13098 (2008)

    Article  CAS  PubMed  Google Scholar 

  6. Z. Xing, C.J. Cardona, S. Adams, Z. Yang, J. Li, D. Perez, P.R. Woolcock, J. Gen. Virol. 90, 1109–1118 (2009)

    Article  CAS  PubMed  Google Scholar 

  7. Zhirnov, H.D. Klenk, Apoptosis 12, 1419–1432 (2007)

    Article  CAS  PubMed  Google Scholar 

  8. C. Ehrhardt, S. Ludwig, Cell Microbiol. 11, 863–871 (2009)

    Article  CAS  PubMed  Google Scholar 

  9. 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  CAS  PubMed  Google Scholar 

  10. T.M. Tumpey, R. Alvarez, D.E. Swayne, D.L. Suarez, J. Clin. Microbiol. 43, 676–683 (2005)

    Article  CAS  PubMed  Google Scholar 

  11. C. Banet-Noach, A. Panshin, N. Golender, L. Simanov, E. Rozenblut, S. Pokamunski, M. Pirak, Y. Tendler, M. García, B. Gelman, R. Pasternak, s. Perk, Virus Genes 34, 157–168 (2007)

    Article  CAS  PubMed  Google Scholar 

  12. N. Golender, A. Panshin, C. Banet-Noach, S. Nagar, S. Pokamunski, M. Pirak, Y. Tendler, I. Davidson, M. García, S. Perk, Virus Genes 37, 289–297 (2008)

    Article  CAS  PubMed  Google Scholar 

  13. OIE Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, 6th edn. (World Organization for Animal Health, Paris, France, 2008), pp. 465–481

  14. E. Hoffmann, J. Stech, Y. Guan, R.G. Webster, D.R. Perez, Arch. Virol. 146, 2275–2289 (2001)

    Article  CAS  PubMed  Google Scholar 

  15. Y. Guan, J.S. Peiris, A.S. Lipatov, T.M. Ellis, K.C. Dyrting, S. Krauss, L.J. Zhang, R.G. Webster, K.F. Shortridge, Proc. Natl. Acad. Sci. USA 99, 8950–8955 (2002)

    Article  CAS  PubMed  Google Scholar 

  16. T.A. Hall, Nucleic Acids Symp. Ser. 41, 95–98 (1999)

    CAS  Google Scholar 

  17. R. Chenna, H. Sugawara, T. Koike, R. Lopez, T.J. Gibson, D.G. Higgins, J.D. Thompson, Nucleic Acids Res. 31, 3497–3500 (2003)

    Article  CAS  PubMed  Google Scholar 

  18. K. Tamura, J. Dudley, M. Nei, S. Kumar, Mol. Biol. Evol. 24, 1596–1599 (2007)

    Article  CAS  PubMed  Google Scholar 

  19. B.A. Jameson, H. Wolf, Comput. Appl. Biosci. 4, 181–186 (1988)

    CAS  PubMed  Google Scholar 

  20. S. Perk, C. Banet-Noach, N. Golender, L. Simanov, E. Rozenblut, S. Nagar, S. Pokamunski, M. Pirak, Y. Tendler, M. García, A. Panshin, Virus Genes 35, 497–502 (2007)

    Article  CAS  PubMed  Google Scholar 

  21. S. Perk, N. Golender, E. Lapin, S. Pokamunski, E. Berman, Y. Tendler, M. Bellaiche, A. Panshin, I. Davidson, Comp. Immunol. Microbiol. Infect. Dis. [Epub ahead of print] (2009)

  22. K.M. Xu, G.J. Smith, J. Bahl, L. Duan, H. Tai, D. Vijaykrishna, J. Wang, J.X. Zhang, K.S. Li, X.H. Fan, R.G. Webster, H. Chen, J.S. Peiris, Y. Guan, J. Virol. 81, 10389–10401 (2007)

    Article  CAS  PubMed  Google Scholar 

  23. B.G. Hale, R.E. Randall, J. Ortín, D. Jackson, J. Gen. Virol. 89, 2359–2376 (2008)

    Article  CAS  PubMed  Google Scholar 

  24. J.-X. Long, D.-X. Peng, Y.-L. Liu, Y.-T. Wu, X.-F. Liu, Virus Genes 36, 471–478 (2008)

    Article  CAS  PubMed  Google Scholar 

  25. L. Duan, J. Bahl, G.J. Smith, J. Wang, D. Vijaykrishna, L.J. Zhang, J.X. Zhang, K.S. Li, X.H. Fan, C.L. Cheung, K. Huang, L.L. Poon, K.F. Shortridge, R.G. Webster, J.S. Peiris, H. Chen, Y. Guan, Virology 380, 243–254 (2008)

    Article  CAS  PubMed  Google Scholar 

  26. P. Zhang, Y. Tang, X. Liu, W. Liu, X. Zhang, H. Liu, D. Peng, S. Gao, Y. Wu, L. Zhang, S. Lu, X. Liu, J. Virol. 83, 8428–8438 (2009)

    Article  CAS  PubMed  Google Scholar 

  27. M. Iqbal, T. Yaqub, K. Reddy, J. W. McCauley, PLoS One 11, 4, e5788 (2009)

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

    Article  CAS  PubMed  Google Scholar 

  29. 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  CAS  PubMed  Google Scholar 

  30. D.A. Buonagurio, S. Nakada, J.D. Parvin, M. Krystal, P. Palese, W.M. Fitch, Science 232, 980–982 (1986)

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  32. D.L. Suarez, M.L. Perdue, Virus Res. 54, 59–69 (1998)

    Article  CAS  PubMed  Google Scholar 

  33. J.J. Treanor, M.H. Synder, W.T. London, B.R. Murphy, Virology 171, 1–9 (1989)

    Article  CAS  PubMed  Google Scholar 

  34. C.J. Hackett, D. Horowitz, M. Wysocka, S.B. Dillon, J. Gen. Virol. 73, 1339–1343 (1992)

    Article  CAS  PubMed  Google Scholar 

  35. J. Jameson, J. Cruz, F.A. Ennis, J. Virol. 72, 8682–8689 (1998)

    CAS  PubMed  Google Scholar 

  36. Z. Tan, S. Akerstrom, B.Y. Wee, S.K. Lal, A. Mirazimi, Y.J. Tan, J. Med. Virol. 82, 467–475 (2010)

    Article  CAS  PubMed  Google Scholar 

  37. L.E. Brown, V.S. Hinshaw, R.G. Webster, Virology 130, 134–143 (1983)

    Article  CAS  PubMed  Google Scholar 

  38. J.A. van der Goot, B. Engel, S.G. van de Water, W. Buist, M.C. de Jong, G. Koch, M. van Boven, A. Stegeman, Vaccine 28, 1771–1777 (2010)

    Article  PubMed  Google Scholar 

  39. W.G. Dundon, S. Maniero, A. Toffan, I. Capua, G. Cattoli, Avian Dis. 51(1 Suppl), 209–212 (2007)

    Article  PubMed  Google Scholar 

  40. D.S. Watson, S.M. Reddy, V. Brahmakshatriya, B. Lupiani, J. Immunol. Methods 340, 123–131 (2009)

    CAS  PubMed  Google Scholar 

  41. G. Avellaneda, E. Mundr, C.-W. Lee, S. Jadhao, D. Suarez, Avian Dis. 54, 278–286 (2010)

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Mrs. Rivi Ascarelli-Goell, MSc, Mrs. Magda David, MSc, and Mrs. Faina Golender for excellent technical assistance. This study was supported by the Kameya Grant of the Israel Ministry of Absorption, by Research Grant No. IS-3679-05 from BARD, the United States-Israel Binational Agricultural Research and Development Fund, and by Grant No. 847-0319 from the Poultry Association of the Israel Ministry of Agriculture and Rural Development.

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Authors and Affiliations

  1. Kimron Veterinary Institute, P.O. Box 12, 50250, Bet Dagan, Israel

    A. Panshin, N. Golender, I. Davidson, S. Nagar, A. Alturi & S. Perk

  2. University of Georgia, Athens, GA, USA

    M. Garsia, M. W. Jackwood & E. Mundt

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  1. A. Panshin
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  2. N. Golender
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  3. I. Davidson
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Correspondence to A. Panshin.

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Panshin, A., Golender, N., Davidson, I. et al. Variability of NS1 proteins among H9N2 avian influenza viruses isolated in Israel during 2000–2009. Virus Genes 41, 396–405 (2010). https://doi.org/10.1007/s11262-010-0522-3

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  • DOI: https://doi.org/10.1007/s11262-010-0522-3

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