A 27-amino-acid deletion in the neuraminidase stalk supports replication of an avian H2N2 influenza A virus in the respiratory tract of chickens

Journal of Virology

Volumn 84, Issue 22, 2010, Pages 11831-11840

  Sorrell, Erin M ^a   Song, Haichen ^b   Pena, Lindomar ^a   Perez, Daniel R ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b ZOETIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMAGGLUTININ; SIALIDASE;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHICKEN; GENE DELETION; GENE MUTATION; GENETIC ANALYSIS; INFLUENZA VIRUS A H2N2; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; QUAIL; RESPIRATORY SYSTEM; SEQUENCE ANALYSIS; VIROGENESIS; VIRUS REPLICATION; VIRUS SHEDDING; VIRUS TRANSMISSION;

ANIMALS; CELL LINE; CHICKENS; INFLUENZA A VIRUS, H2N2 SUBTYPE; INFLUENZA IN BIRDS; MOLECULAR SEQUENCE DATA; NEURAMINIDASE; POULTRY DISEASES; QUAIL; RESPIRATORY SYSTEM; SEQUENCE DELETION; VIRAL PROTEINS; VIRUS REPLICATION;

ANAS PLATYRHYNCHOS; AVES; COTURNIX JAPONICA; GALLUS GALLUS; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE; PHASIANIDAE;

EID: 78049509775     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01460-10     Document Type: Article

References (46)

1. Air, G. M., W. G. Laver, and R. G. Webster. 1987. Antigenic variation in influenza viruses. Contrib. Microbiol. Immunol. 8:20-59.
2. Alexander, D. J., G. Parsons, and R. J. Manvell. 1986. Experimental assessment of the pathogenicity of eight avian influenza A viruses of H5 subtype for chickens, turkeys, ducks and quail. Avian Pathol. 15:647-662.
3. Baigent, S. J., R. C. Bethell, and J. W. McCauley. 1999. Genetic analysis reveals that both haemagglutinin and neuraminidase determine the sensitivity of naturally occurring avian influenza viruses to zanamivir in vitro. Virology 263:323-338.
4. Baigent, S. J., and J. W. McCauley. 2001. Glycosylation of haemagglutinin and stalk-length of neuraminidase combine to regulate the growth of avian influenza viruses in tissue culture. Virus Res. 79:177-185.
5. Banks, J., E. S. Speidel, E. Moore, L. Plowright, A. Piccirillo, I. Capua, P. Cordioli, A. Fioretti, and D. J. Alexander. 2001. Changes in the haemagglutinin and the neuraminidase genes prior to the emergence of highly pathogenic H7N1 avian influenza viruses in Italy. Arch. Virol. 146:963-973.
6. Campitelli, L., E. Mogavero, M. A. De Marco, M. Delogu, S. Puzelli, F. Frezza, M. Facchini, C. Chiapponi, E. Foni, P. Cordioli, R. Webby, G. Barigazzi, R. G. Webster, and I. Donatelli. 2004. Interspecies transmission of an H7N3 influenza virus from wild birds to intensively reared domestic poultry in Italy. Virology 323:24-36. (Pubitemid 38681017)
7. Castrucci, M. R., and Y. Kawaoka. 1993. Biologic importance of neuraminidase stalk length in influenza A virus. J. Virol. 67:759-764.
8. Chen, G. W., 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, and S. R. Shih. 2006. Genomic signatures of human versus avian influenza A viruses. Emerg. Infect. Dis. 12:1353-1360.
9. Chin, P. S., E. Hoffmann, R. Webby, R. G. Webster, Y. Guan, M. Peiris, and K. F. Shortridge. 2002. Molecular evolution of H6 influenza viruses from poultry in Southeastern China: prevalence of H6N1 influenza viruses possessing seven A/Hong Kong/156/97 (H5N1)-like genes in poultry. J. Virol. 76:507-516.
10. Colman, P. M. 1989. Neuraminidase: enzyme and antigen, p. 175-210. In R. M. Krug (ed.), The influenza viruses. Plenum Press, New York, NY.
11. Fitch, W. M., R. M. Bush, C. A. Bender, and N. J. Cox. 1997. Long term trends in the evolution of H(3) HA1 human influenza type A. Proc. Natl. Acad. Sci. U. S. A. 94:7712-7718.
12. Fraser, C., C. A. Donnelly, S. Cauchemez, W. P. Hanage, M. D. Van Kerkhove, T. D. Hollingsworth, J. Griffin, R. F. Baggaley, H. E. Jenkins, E. J. Lyons, T. Jombart, W. R. Hinsley, N. C. Grassly, F. Balloux, A. C. Ghani, N. M. Ferguson, A. Rambaut, O. G. Pybus, H. Lopez-Gatell, C. M. Alpuche- Aranda, I. B. Chapela, E. P. Zavala, D. M. Guevara, F. Checchi, E. Garcia, S. Hugonnet, and C. Roth. 2009. Pandemic potential of a strain of influenza A (H1N1): early findings. Science 324:1557-1561.
13. Giannecchini, S., L. Campitelli, L. Calzoletti, M. A. De Marco, A. Azzi, and I. Donatelli. 2006. Comparison of in vitro replication features of H7N3 influenza viruses from wild ducks and turkeys: potential implications for interspecies transmission. J. Gen. Virol. 87:171-175.
14. Guan, Y., K. F. Shortridge, S. Krauss, and R. G. Webster. 1999. Molecular characterization of H9N2 influenza viruses: were they the donors of the "internal" genes of H5N1 viruses in Hong Kong? Proc. Natl. Acad. Sci. U. S. A. 96:9363-9367.
15. Guo, Y. J., S. Krauss, D. A. Senne, I. P. Mo, K. S. Lo, X. P. Xiong, M. Norwood, K. F. Shortridge, R. G. Webster, and Y. Guan. 2000. Characterization of the pathogenicity of members of the newly established H9N2 influenza virus lineages in Asia. Virology 267:279-288.
16. Hatta, M., P. Gao, P. Halfmann, and Y. Kawaoka. 2001. Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293:1840-1842.
17. Hoffmann, E., S. Krauss, D. Perez, R. Webby, and R. G. Webster. 2002. Eight-plasmid system for rapid generation of influenza virus vaccines. Vaccine 20:3165-3170.
18. Hoffmann, E., J. Stech, Y. Guan, R. G. Webster, and D. R. Perez. 2001. Universal primer set for the full-length amplification of all influenza A viruses. Arch. Virol. 146:2275-2289.
19. Hossain, M. J., D. Hickman, and D. R. Perez. 2008. Evidence of expanded host range and mammalian-associated genetic changes in a duck H9N2 influenza virus following adaptation in quail and chickens. PLoS One 3:e3170.
20. Hulse-Post, D. J., J. Franks, K. Boyd, R. Salomon, E. Hoffmann, H. L. Yen, R. J. Webby, D. Walker, T. D. Nguyen, and R. G. Webster. 2007. Molecular changes in the polymerase genes (PA and PB1) associated with high pathogenicity of H5N1 influenza virus in mallard ducks. J. Virol. 81:8515-8524.
21. Laver, W. G. 1978. Crystallization and peptide maps of neuraminidase "heads" from H2N2 and H3N2 influenza virus strains. Virology 86:78-87.
22. Lin, Y. P., M. Shaw, V. Gregory, K. Cameron, W. Lim, A. Klimov, K. Subbarao, Y. Guan, S. Krauss, K. Shortridge, R. Webster, N. Cox, and A. Hay. 2000. Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proc. Natl. Acad. Sci. U. S. A. 97:9654-9658.
23. Liu, J. H., K. Okazaki, G. R. Bai, W. M. Shi, A. Mweene, and H. Kida. 2004. Interregional transmission of the internal protein genes of H2 influenza virus in migratory ducks from North America to Eurasia. Virus Genes 29:81-86.
24. Ma, W., A. L. Vincent, M. R. Gramer, C. B. Brockwell, K. M. Lager, B. H. Janke, P. C. Gauger, D. P. Patnayak, R. J. Webby, and J. A. Richt. 2007. Identification of H2N3 influenza A viruses from swine in the United States. Proc. Natl. Acad. Sci. U. S. A. 104:20949-20954.
25. Makarova, N. V., N. V. Kaverin, S. Krauss, D. Senne, and R. G. Webster. 1999. Transmission of Eurasian avian H2 influenza virus to shorebirds in North America. J. Gen. Virol. 80(Pt. 12):3167-3171.
26. Makarova, N. V., H. Ozaki, H. Kida, R. G. Webster, and D. R. Perez. 2003. Replication and transmission of influenza viruses in Japanese quail. Virology 310:8-15.
27. Massin, P., S. van der Werf, and N. Naffakh. 2001. Residue 627 of PB2 is a determinant of cold sensitivity in RNA replication of avian influenza viruses. J. Virol. 75:5398-5404. (Pubitemid 32448565)
28. Matrosovich, M., N. Zhou, Y. Kawaoka, and R. Webster. 1999. The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J. Virol. 73:1146-1155.
29. Munier, S., T. Larcher, F. Cormier-Aline, D. Soubieux, B. Su, L. Guigand, B. Labrosse, Y. Cherel, P. Quere, D. Marc, and N. Naffakh. 2010. A genetically engineered waterfowl influenza virus with a deletion in the stalk of the neuraminidase has increased virulence for chickens. J. Virol. 84:940-952.
30. Munster, V. J., E. de Wit, D. van Riel, W. E. Beyer, G. F. Rimmelzwaan, A. D. Osterhaus, T. Kuiken, and R. A. Fouchier. 2007. The molecular basis of the pathogenicity of the Dutch highly pathogenic human influenza A H7N7 viruses. J. Infect. Dis. 196:258-265.
31. Naffakh, N., P. Massin, N. Escriou, B. Crescenzo-Chaigne, and S. van der Werf. 2000. Genetic analysis of the compatibility between polymerase proteins from human and avian strains of influenza A viruses. J. Gen. Virol. 81:1283-1291.
32. Naffakh, N., A. Tomoiu, M. A. Rameix-Welti, and S. van der Werf. 2008. Host restriction of avian influenza viruses at the level of the ribonucleoproteins. Annu. Rev. Microbiol. 62:403-424.
33. Neumann, G., T. Watanabe, H. Ito, S. Watanabe, H. Goto, P. Gao, M. Hughes, D. R. Perez, R. Donis, E. Hoffmann, G. Hobom, and Y. Kawaoka. 1999. Generation of influenza A viruses entirely from cloned cDNAs. Proc. Natl. Acad. Sci. U. S. A. 96:9345-9350.
34. Perez, D. R., W. Lim, J. P. Seiler, G. Yi, M. Peiris, K. F. Shortridge, and R. G. Webster. 2003. Role of quail in the interspecies transmission of H9 influenza A viruses: molecular changes on HA that correspond to adaptation from ducks to chickens. J. Virol. 77:3148-3156.
35. Perez, D. R., R. J. Webby, E. Hoffmann, and R. G. Webster. 2003. Landbased birds as potential disseminators of avian mammalian reassortant influenza A viruses. Avian Dis. 47:1114-1117.
36. Schäfer, J. R., Y. Kawaoka, W. J. Bean, J. Suss, D. Senne, and R. G. Webster. 1993. Origin of the pandemic 1957 H2 influenza A virus and the persistence of its possible progenitors in the avian reservoir. Virology 194:781-788.
37. Shinde, V., C. B. Bridges, T. M. Uyeki, B. Shu, A. Balish, X. Xu, S. Lindstrom, L. V. Gubareva, V. Deyde, R. J. Garten, M. Harris, S. Gerber, S. Vagasky, F. Smith, N. Pascoe, K. Martin, D. Dufficy, K. Ritger, C. Conover, P. Quinlisk, A. Klimov, J. S. Bresee, and L. Finelli. 2009. Triple-reassortant swine influenza A (H1) in humans in the United States, 2005-2009. N. Engl. J. Med. 360:2616-2625.
38. Sorrell, E. M., and D. R. Perez. 2007. Adaptation of influenza A/Mallard/ Potsdam/178-4/83 H2N2 virus in Japanese quail leads to infection and transmission in chickens. Avian Dis. 51:264-268.
39. Spekreijse, D., A. Bouma, J. A. Stegeman, G. Koch, and M. C. de Jong. 20 June 2010. The effect of inoculation dose of a highly pathogenic avian influenza virus strain H5N1 on the infectiousness of chickens. Vet. Microbiol. doi:10.1016/j.vetmic.2010.06.012.
40. Steel, J., A. C. Lowen, S. Mubareka, and P. Palese. 2009. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog. 5:e1000252.
41. Tsuchiya, E., K. Sugawara, S. Hongo, Y. Matsuzaki, Y. Muraki, Z. N. Li, and K. Nakamura. 2001. Antigenic structure of the haemagglutinin of human influenza A/H2N2 virus. J. Gen. Virol. 82:2475-2484.
42. Wan, H., and D. R. Perez. 2007. Amino acid 226 in the hemagglutinin of H9N2 influenza viruses determines cell tropism and replication in human airway epithelial cells. J. Virol. 81:5181-5191.
43. Wan, H., and D. R. Perez. 2006. Quail carry sialic acid receptors compatible with binding of avian and human influenza viruses. Virology 346:278-286.
44. Webster, R. G. 1997. Predictions for future human influenza pandemics. J. Infect. Dis. 176(Suppl. 1):S14-S19.
45. Webster, R. G., W. G. Laver, G. M. Air, and G. C. Schild. 1982. Molecular mechanisms of variation in influenza viruses. Nature 296:115-121.
46. Yoshida, R., M. Igarashi, H. Ozaki, N. Kishida, D. Tomabechi, H. Kida, K. Ito, and A. Takada. 2009. Cross-protective potential of a novel monoclonal antibody directed against antigenic site B of the hemagglutinin of influenza A viruses. PLoS Pathog. 5:e1000350.