Evolution of highly pathogenic avian H5N1 influenza viruses and the emergence of dominant variants

Journal of General Virology

Volumn 91, Issue 8, 2010, Pages 1984-1995

  Neumann, Gabriele ^a   Green, Margaret A ^b   Macken, Catherine A ^b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMAGGLUTININ; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; GENE SEQUENCE; GENETIC REASSORTMENT; GENOTYPE; INFLUENZA VIRUS A H5N1; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENETIC TREE; POINT MUTATION; PRIORITY JOURNAL; ANIMAL; AVIAN INFLUENZA; BIOLOGY; BIRD; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; MOLECULAR EPIDEMIOLOGY; PHYLOGENY; POULTRY; SEQUENCE HOMOLOGY; VIROLOGY;

AVES; ORTHOMYXOVIRIDAE;

ANIMALS; BIRDS; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; GENOTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA IN BIRDS; MOLECULAR EPIDEMIOLOGY; PHYLOGENY; POULTRY; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; VIRAL PROTEINS;

EID: 77955298876     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.020750-0     Document Type: Article

References (55)

1. Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J. & Wheeler, D. L. (2008). GenBank. Nucleic Acids Res 36, D25-D30.
2. Chen, W., Calvo, P. A., Malide, D., Gibbs, J., Schubert, U., Bacik, I., Basta, S., O'Neill, R., Schickli, J. & other authors (2001). A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 7, 1306-1312. (Pubitemid 34007934)
3. Chen, H., Deng, G., Li, Z., Tian, G., Li, Y., Jiao, P., Zhang, L., Liu, Z., Webster, R. G. & Yu, K. (2004). The evolution of H5N1 influenza viruses in ducks in southern China. Proc Natl Acad Sci U S A 101, 10452-10457. (Pubitemid 38924946)
4. Chen, H., Smith, G. J., Zhang, S. Y., Qin, K., Wang, J., Li, K. S., Webster, R. G., Peiris, J. S. & Guan, Y. (2005). Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature 436, 191-192. (Pubitemid 41021261)
5. Chen, H., Li, Y., Li, Z., Shi, J., Shinya, K., Deng, G., Qi, Q., Tian, G., Fan, S. & other authors (2006a). Properties and dissemination of H5N1 viruses isolated during an influenza outbreak in migratory waterfowl in western China. J Virol 80, 5976-5983.
6. Chen, H., Smith, G. J., Li, K. S., Wang, J., Fan, X. H., Rayner, J. M., Vijaykrishna, D., Zhang, J. X., Zhang, L. J. & other authors (2006b). Establishment of multiple sublineages of H5N1 influenza virus in Asia: implications for pandemic control. Proc Natl Acad Sci U S A 103, 2845-2850. (Pubitemid 43306637)
7. Cheung, C. L., Vijaykrishna, D., Smith, G. J., Fan, X. H., Zhang, J. X., Bahl, J., Duan, L., Huang, K., Tai, H. & other authors (2007). Establishment of influenza A virus (H6N1) in minor poultry species in southern China. J Virol 81, 10402-10412.
8. Claas, E. C., de Jong, J. C., Van Beek, R., Rimmelzwaan, G. F. & Osterhaus, A. D. (1998a). Human influenza virus A/HongKong/156/97 (H5N1) infection. Vaccine 16, 977-978. (Pubitemid 28276010)
9. Claas, E. C., Osterhaus, A. D., Van Beek, R., de Jong, J. C., Rimmelzwaan, G. F., Senne, D. A., Krauss, S., Shortridge, K. F. & Webster, R. G. (1998b). Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 351, 472-477. (Pubitemid 28070093)
10. Crescenzo-Chaigne, B., Naffakh, N. & van der Werf, S. (1999). Comparative analysis of the ability of the polymerase complexes of influenza viruses type A, B and C to assemble into functional RNPs that allow expression and replication of heterotypic model RNA templates in vivo. Virology 265, 342-353. (Pubitemid 30022228)
11. de Jong, J. C., Claas, E. C., Osterhaus, A. D., Webster, R. G. & Lim, W. L. (1997). A pandemic warning? Nature 389, 554.
12. Duan, L., Bahl, J., Smith, G. J., Wang, J., Vijaykrishna, D., Zhang, L. J., Zhang, J. X., Li, K. S., Fan, X. H. & other authors (2008). The development and genetic diversity of H5N1 influenza virus in China, 1996-2006. Virology 380, 243-254.
13. Dugan, V. G., Chen, R., Spiro, D. J., Sengamalay, N., Zaborsky, J., Ghedin, E., Nolting, J., Swayne, D. E., Runstadler, J. A. & other authors (2008). The evolutionary genetics and emergence of avian influenza viruses in wild birds. PLoS Pathog 4, e1000076. (Pubitemid 351811513)
14. Felsenstein, J. (2004). Inferring Phylogenies. Sunderland, MA: Sinauer Associates.
15. Gabriel, G., Dauber, B., Wolff, T., Planz, O., Klenk, H. D. & Stech, J. (2005). The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci U S A 102, 18590-18595. (Pubitemid 43011270)
16. Garten, R. J., Davis, C. T., Russell, C. A., Shu, B., Lindstrom, S., Balish, A., Sessions, W. M., Xu, X., Skepner, E. & other authors (2009). Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325, 197-201.
17. Guan, Y., Shortridge, K. F., Krauss, S. & Webster, R. G. (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.
18. Guan, Y., Peiris, J. S., Lipatov, A. S., Ellis, T.M., Dyrting, K. C., Krauss, S., Zhang, L. J., Webster, R. G. & Shortridge, K. F. (2002a). Emergence of multiple genotypes of H5N1 avian influenza viruses in Hong Kong SAR. Proc Natl Acad Sci U S A 99, 8950-8955. (Pubitemid 34693664)
19. Guan, Y., Peiris, M., Kong, K. F., Dyrting, K. C., Ellis, T. M., Sit, T., Zhang, L. J. & Shortridge, K. F. (2002b). H5N1 influenza viruses isolated from geese in Southeastern China: evidence for genetic reassortment and interspecies transmission to ducks. Virology 292, 16-23. (Pubitemid 34925834)
20. Guan, Y., Poon, L. L., Cheung, C. Y., Ellis, T. M., Lim, W., Lipatov, A. S., Chan, K. H., Sturm-Ramirez, K. M., Cheung, C. L. & other authors (2004). H5N1 influenza: a protean pandemic threat. Proc Natl Acad Sci U S A 101, 8156-8161. (Pubitemid 38698070)
21. Guindon, S. & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52, 696-704. (Pubitemid 37365050)
22. Hatta, M., Gao, P., Halfmann, P. & Kawaoka, Y. (2001). Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293, 1840-1842. (Pubitemid 32845783)
23. Hoffmann, E., Stech, J., Leneva, I., Krauss, S., Scholtissek, C., Chin, P. S., Peiris, M., Shortridge, K. F. & Webster, R. G. (2000). Characterization of the influenza A virus gene pool in avian species in southern China: was H6N1 a derivative or a precursor of H5N1? J Virol 74, 6309-6315.
24. Jackson, D., Hossain, M. J., Hickman, D., Perez, D. R. & Lamb, R. A. (2008). A new influenza virus virulence determinant: the NS1 protein four C-terminal residues modulate pathogenicity. Proc Natl Acad Sci U S A 105, 4381-4386. (Pubitemid 351754389)
25. Li, K. S., Guan, Y., Wang, J., Smith, G. J., Xu, K. M., Duan, L., Rahardjo, A. P., Puthavathana, P., Buranathai, C. & other authors (2004). Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 430, 209-213. (Pubitemid 38902429)
26. Li, Z., Chen, H., Jiao, P., Deng, G., Tian, G., Li, Y., Hoffmann, E., Webster, R. G., Matsuoka, Y. & Yu, K. (2005). Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model. J Virol 79, 12058-12064. (Pubitemid 41279322)
27. Liu, J., Xiao, H., Lei, F., Zhu, Q., Qin, K., Zhang, X. W., Zhang, X. L., Zhao, D., Wang, G. & other authors (2005). Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 309, 1206. (Pubitemid 41170907)
28. Lu, G., Rowley, T., Garten, R. & Donis, R. O. (2007). FluGenome: a web tool for genotyping influenza A virus. Nucleic Acids Res 35, W275-W279.
29. Macken, C. A., Webby, R. J. & Bruno, W. J. (2006). Genotype turnover by reassortment of replication complex genes from avian influenza A virus. J Gen Virol 87, 2803-2815.
30. Massin, P., van der Werf, S. & Naffakh, N. (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)
31. Mazur, I., Anhlan, D., Mitzner, D., Wixler, L., Schubert, U. & Ludwig, S. (2008). The proapoptotic influenza A virus protein PB1-F2 regulates viral polymerase activity by interaction with the PB1 protein. Cell Microbiol 10, 1140-1152. (Pubitemid 351524278)
32. McAuley, J. L., Hornung, F., Boyd, K. L., Smith, A. M., McKeon, R., Bennink, J., Yewdell, J. W. & McCullers, J. A. (2007). Expression of the 1918 influenza A virus PB1-F2 enhances the pathogenesis of viral and secondary bacterial pneumonia. Cell Host Microbe 2, 240-249. (Pubitemid 47500821)
33. Naffakh, N., Massin, P., Escriou, N., Crescenzo-Chaigne, B. & van der Werf, S. (2000). Genetic analysis of the compatibility between polymerase proteins from human and avian strains of influenza A viruses. J Gen Virol 81, 1283-1291. (Pubitemid 30232714)
34. Nelson, M. I., Viboud, C., Simonsen, L., Bennett, R. T., Griesemer, S. B., St George, K., Taylor, J., Spiro, D. J., Sengamalay, N. A. & other authors (2008). Multiple reassortment events in the evolutionary history of H1N1 influenza A virus since 1918. PLoS Pathog 4, e1000012.
35. Neumann, G., Noda, T. & Kawaoka, Y. (2009). Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459, 931-939.
36. Novel Swine-Origin Influenza A (H1N1) Virus Investigation Team & other authors (2009). Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med 360, 2605-2615.
37. Obenauer, J. C., Denson, J., Mehta, P. K., Su, X., Mukatira, S., Finkelstein, D. B., Xu, X., Wang, J., Ma, J. & other authors (2006). Large-scale sequence analysis of avian influenza isolates. Science 311, 1576-1580.
38. Palese, P. & Shaw, M. (2007). Orthomyxoviridae: The viruses and their replication. In Fields Virology, 5th edn, pp. 1647-1689. Edited by D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman & S. E. Straus. Philadelphia, PA: Wolters Kluwer, Lippincott Williams & Wilkins.
39. Salomon, R., Franks, J., Govorkova, E. A., Ilyushina, N. A., Yen, H. L., Hulse-Post, D. J., Humberd, J., Trichet, M., Rehg, J. E. & other authors (2006). The polymerase complex genes contribute to the high virulence of the human H5N1 influenza virus isolate A/Vietnam/1203/04. J Exp Med 203, 689-697.
40. Shinya, K., Hamm, S., Hatta, M., Ito, H., Ito, T. & Kawaoka, Y. (2004). 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. (Pubitemid 38315152)
41. Smith, G. J., Fan, X. H., Wang, J., Li, K. S., Qin, K., Zhang, J. X., Vijaykrishna, D., Cheung, C. L., Huang, K. & other authors (2006a). Emergence and predominance of an H5N1 influenza variant in China. Proc Natl Acad Sci U S A 103, 16936-16941. (Pubitemid 44737356)
42. Smith, G. J., Naipospos, T. S., Nguyen, T. D., de Jong, M. D., Vijaykrishna, D., Usman, T. B., Hassan, S. S., Nguyen, T. V., Dao, T. V. & other authors (2006b). Evolution and adaptation of H5N1 influenza virus in avian and human hosts in Indonesia and Vietnam. Virology 350, 258-268. (Pubitemid 44218982)
43. Smith, G. J., Vijaykrishna, D., Ellis, T. M., Ellis, T. M., Dyrting, K. C., Leung, Y. H., Bahl, J., Wong, C. W., Kai, H. & other authors (2009). Characterization of avian influenza viruses A (H5N1) from wild birds, Hong Kong, 2004-2008. Emerg Infect Dis 15, 402-407.
44. Subbarao, K., Klimov, A., Katz, J., Regnery, H., Lim, W., Hall, H., Perdue, M., Swayne, D., Bender, C. & other authors (1998). Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279, 393-396. (Pubitemid 28063376)
45. Sweet, T. M., Maassab, H. F. & Herlocher, M. L. (2004). Reverse genetics studies of attenuation of the ca A/AA/6/60 influenza virus: the role of the matrix gene. Biomed Pharmacother 58, 509-515.
46. Van Hoeven, N., Pappas, C., Belser, J. A., Maines, T. R., Zeng, H., Garcia-Sastre, A., Sasisekharan, R., Katz, J. M. & Tumpey, T. M. (2009). Human HA and polymerase subunit PB2 proteins confer transmission of an avian influenza virus through the air. Proc Natl Acad Sci U S A 106, 3366-3371.
47. Vijaykrishna, D., Bahl, J., Riley, S., Duan, L., Zhang, J. X., Chen, H., Peiris, J. S., Smith, G. J. & Guan, Y. (2008). Evolutionary dynamics and emergence of panzootic H5N1 influenza viruses. PLoS Pathog 4, e1000161.
48. Wan, X. F., Nguyen, T., Davis, C. T., Smith, C. B., Zhao, Z. M., Carrel, M., Inui, K., Do, H. T., Mai, D. T. & other authors (2008). Evolution of highly pathogenic H5N1 avian influenza viruses in Vietnam between 2001 and 2007. PLoS One 3, e3462.
49. Watanabe, T., Watanabe, S., Shinya, K., Kim, J. H., Hatta, M. & Kawaoka, Y. (2009). Viral RNA polymerase complex promotes optimal growth of 1918 virus in the lower respiratory tract of ferrets. Proc Natl Acad Sci U S A 106, 588-592.
50. WHO (2008). Toward a unified nomenclature system for highly pathogenic avian influenza virus (H5N1). Emerg Infect Dis 14, e1. (Pubitemid 351920470)
51. WHO Global Influenza Program Surveillance Network (2005). Evolution of H5N1 avian influenza viruses in Asia. Emerg Infect Dis 11, 1515-1521. (Pubitemid 41384335)
52. Wright, P. F., Neumann, G. & Kawaoka, Y. (2007). Orthomyxoviruses. In Fields Virology, 5th edn, pp. 1691-1740. Edited by D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman & S. E. Straus. Philadelphia, PA: Wolters Kluwer, Lippincott Williams & Wilkins.
53. Xu, X., Subbarao, K., Cox, N. J. & Guo, Y. (1999). 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. (Pubitemid 29395053)
54. Xu, K. M., Smith, G. J., Bahl, J., Duan, L., Tai, H., Vijaykrishna, D., Wang, J., Zhang, J. X., Li, K. S. & other authors (2007). The genesis and evolution of H9N2 influenza viruses in poultry from southern China, 2000 to 2005. J Virol 81, 10389-10401.
55. Zamarin, D., Garcia-Sastre, A., Xiao, X., Wang, R. & Palese, P. (2005). Influenza virus PB1-F2 protein induces cell death through mitochondrial ANT3 and VDAC1. PLoS Pathog 1, e4.