PB1-mediated virulence attenuation of H5N1 influenza virus in mice is associated with PB2

Journal of General Virology

Volumn 92, Issue 6, 2011, Pages 1435-1444

  Li, Jing ^a   Li, Yongqiang ^a   Hu, Yi ^a   Chang, Guohui ^a   Sun, Wei ^a   Yang, Yinhui ^a   Kang, Xiaoping ^a   Wu, Xiaoyan ^a   Zhu, Qingyu ^a  

^a BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEOPROTEIN; RNA DIRECTED RNA POLYMERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ENZYME ACTIVITY; INFLUENZA A (H5N1); INFLUENZA VIRUS A H5N1; LUNG INFECTION; MOUSE; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; VIRUS GENOME; VIRUS ISOLATION; VIRUS RECOMBINANT; VIRUS VIRULENCE; WILD TYPE;

ANIMALS; CELL LINE; FEMALE; HUMANS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA, HUMAN; LUNG; MICE; MICE, INBRED BALB C; MUTATION; VIRAL PROTEINS; VIRULENCE; VIRUS REPLICATION;

AVIAN INFLUENZA VIRUS; MAMMALIA; MUS; ORTHOMYXOVIRIDAE;

EID: 79956298345     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.030718-0     Document Type: Article

References (56)

1. Bender, C., Hall, H., Huang, J., Klimov, A., Cox, N., Hay, A., Gregory, V., Cameron, K., Lim, W. & Subbarao, K. (1999). Characterization of the surface proteins of influenza A (H5N1) viruses isolated from humans in 1997-1998. Virology 254, 115-123.
2. Bornholdt, Z. A. & Prasad, B. V. V. (2008). X-ray structure of NS1 from a highly pathogenic H5N1 influenza virus. Nature 456, 985-988.
3. Bright, R. A., Ross, T. M., Subbarao, K., Robinson, H. L. & Katz, J. M. (2003). Impact of glycosylation on the immunogenicity of a DNAbased influenza H5 HA vaccine. Virology 308, 270-278.
4. CDC (1997). Isolation of avian influenza A(H5N1) viruses from humans-Hong Kong, May-December 1997. MMWR Morb Mortal Wkly Rep 46, 1204-1207.
5. CDC (1998). Update: isolation of avian influenza A(H5N1) viruses from humans-Hong Kong, 1997-1998. MMWR Morb Mortal Wkly Rep 46, 1245-1247.
6. Chen, R. & Holmes, E. C. (2006). Avian influenza virus exhibits rapid evolutionary dynamics. Mol Biol Evol 23, 2336-2341.
7. 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.
8. Chen, H., Bright, R. A., Subbarao, K., Smith, C., Cox, N. J., Katz, J. M. & Matsuoka, Y. (2007). Polygenic virulence factors involved in pathogenesis of 1997 Hong Kong H5N1 influenza viruses in mice. Virus Res 128, 159-163.
9. Conenello, G. M., Zamarin, D., Perrone, L. A., Tumpey, T. & Palese, P. (2007). A single mutation in the PB1-F2 of H5N1 (HK/97) and 1918 influenza A viruses contributes to increased virulence. PLoS Pathog 3, 1414-1421.
10. de Jong, M. D., Simmons, C. P., Thanh, T. T., Hien, V. M., Smith, G. J. D., Chau, T. N., Hoang, D. M., Chau, N. V., Khanh, T. H. & other authors (2006). Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12, 1203-1207.
11. 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.
12. Govorkova, E. A., Rehg, J. E., Krauss, S., Yen, H. L., Guan, Y., Peiris, M., Nguyen, T. D., Hanh, T. H., Puthavathana, P. & other authors (2005). Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J Virol 79, 2191-2198.
13. Gu, J., Xie, Z., Gao, Z., Liu, J., Korteweg, C., Ye, J., Lau, L. T., Lu, J., Gao, Z. & other authors (2007). H5N1 infection of the respiratory tract and beyond: a molecular pathology study. Lancet 370, 1137-1145.
14. Guan, Y., Peiris, J. S. M., Lipatov, A. S., Ellis, T. M., Dyrting, K. C., Krauss, S., Zhang, L. J., Webster, R. G. & Shortridge, K. F. (2002). Emergence of multiple genotypes of H5N1 avian influenza viruses in Hong Kong SAR. Proc Natl Acad Sci U S A 99, 8950-8955.
15. Guan, Y., Poon, L. L. M., 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.
16. 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.
17. Hoffmann, E., Neumann, G., Kawaoka, Y., Hobom, G. & Webster, R. G. (2000). A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci U S A 97, 6108-6113.
18. Honda, A., Mizumoto, K. & Ishihama, A. (2002). Minimum molecular architectures for transcription and replication of the influenza virus. Proc Natl Acad Sci U S A 99, 13166-13171.
19. Horimoto, T. & Kawaoka, Y. (1994). Reverse genetics provides direct evidence for a correlation of hemagglutinin cleavability and virulence of an avian influenza A virus. J Virol 68, 3120-3128.
20. 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.
21. Jiao, P., Tian, G., Li, Y., Deng, G., Jiang, Y., Liu, C., Liu, W., Bu, Z., Kawaoka, Y. & Chen, H. (2008). A single-amino-acid substitution in the NS1 protein changes the pathogenicity of H5N1 avian influenza viruses in mice. J Virol 82, 1146-1154.
22. Katz, J. M., Lu, X., Tumpey, T. M., Smith, C. B., Shaw, M. W. & Subbarao, K. (2000). Molecular correlates of influenza A H5N1 virus pathogenesis in mice. J Virol 74, 10807-10810.
23. Le, Q. M., Sakai-Tagawa, Y., Ozawa, M., Ito, M. & Kawaoka, Y. (2009). Selection of H5N1 influenza virus PB2 during replication in humans. J Virol 83, 5278-5281.
24. Lee, M. S., Deng, M. C., Lin, Y. J., Chang, C. Y., Shieh, H. K., Shiau, J. Z. & Huang, C. C. (2007). Characterization of an H5N1 avian influenza virus from Taiwan. Vet Microbiol 124, 193-201.
25. Lee, S. M. Y., Gardy, J. L., Cheung, C. Y., Cheung, T. K. W., Hui, K. P. Y., Ip, N. Y., Guan, Y., Hancock, R. E. W. & Peiris, J. S. M. (2009). Systems-level comparison of host-responses elicited by avian H5N1 and seasonal H1N1 influenza viruses in primary human macrophages. PLoS ONE 4, e8072.
26. 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.
27. Long, J. X., Peng, D. X., Liu, Y. L., Wu, Y. T. & Liu, X. F. (2008). Virulence of H5N1 avian influenza virus enhanced by a 15-nucleotide deletion in the viral nonstructural gene. Virus Genes 36, 471-478.
28. Lycett, S. J., Ward, M. J., Lewis, F. I., Poon, A. F. Y., Kosakovsky Pond, S. L. & Brown, A. J. (2009). Detection of mammalian virulence determinants in highly pathogenic avian influenza H5N1 viruses: multivariate analysis of published data. J Virol 83, 9901-9910.
29. Maines, T. R., Lu, X. H., Erb, S. M., Edwards, L., Guarner, J., Greer, P. W., Nguyen, D. C., Szretter, K. J., Chen, L. M. & other authors (2005). Avian influenza (H5N1) viruses isolated fromhumans in Asia in 2004 exhibit increased virulence in mammals. J Virol 79, 11788-11800.
30. Mase, M., Tanimura, N., Imada, T., Okamatsu, M., Tsukamoto, K. & Yamaguchi, S. (2006). Recent H5N1 avian influenza A virus increases rapidly in virulence to mice after a single passage in mice. J Gen Virol 87, 3655-3659.
31. Matrosovich, M., Zhou, N., Kawaoka, Y. & Webster, R. (1999). The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J Virol 73, 1146-1155.
32. McAuley, J. L., Zhang, K. & McCullers, J. A. (2010). The effects of influenza A virus PB1-F2 protein on polymerase activity are strain specific and do not impact pathogenesis. J Virol 84, 558-564.
33. Min, J. Y., Li, S., Sen, G. C. & Krug, R. M. (2007). A site on the influenza A virus NS1 protein mediates both inhibition of PKR activation and temporal regulation of viral RNA synthesis. Virology 363, 236-243.
34. Mok, C. K. P., Lee, D. C. W., Cheung, C. Y., Peiris, M. & Lau, A. S. Y. (2007). Differential onset of apoptosis in influenza A virus H5N1- and H1N1-infected human blood macrophages. J Gen Virol 88, 1275-1280.
35. 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.
36. Nishimura, H., Itamura, S., Iwasaki, T., Kurata, T. & Tashiro, M. (2000). Characterization of human influenza A (H5N1) virus infection in mice: neuro-, pneumo- and adipotropic infection. J Gen Virol 81, 2503-2510.
37. Perez, J. T., Varble, A., Sachidanandam, R., Zlatev, I., Manoharan, M., García-Sastre, A. & ten Oever, B. R. (2010). Influenza A virusgenerated small RNAs regulate the switch from transcription to replication. Proc Natl Acad Sci U S A 107, 11525-11530.
38. Poole, E. L., Medcalf, L., Elton, D. & Digard, P. (2007). Evidence that the C-terminal PB2-binding region of the influenza A virus PB1 protein is a discrete alpha-helical domain. FEBS Lett 581, 5300-5306.
39. Reed, L. J. & Muench, H. (1938). A simple method of estimating fifty percent endpoints. Am J Hyg 27, 493-497.
40. Rimmelzwaan, G. F., Kuiken, T., van Amerongen, G., Bestebroer, T. M., Fouchier, R. A. & Osterhaus, A. D. (2001). Pathogenesis of influenza A (H5N1) virus infection in a primate model. J Virol 75, 6687-6691.
41. Rimmelzwaan, G. F., van Riel, D., Baars, M., Bestebroer, T. M., van Amerongen, G., Fouchier, R. A., Osterhaus, A. D. & Kuiken, T. (2006). Influenza A virus (H5N1) infection in cats causes systemic disease with potential novel routes of virus spread within and between hosts. Am J Pathol 168, 176-183, quiz 364.
42. 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.
43. Seo, S. H., Hoffmann, E. & Webster, R. G. (2002). Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat Med 8, 950-954.
44. 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.
45. Shinya, K., Hatta, M., Yamada, S., Takada, A., Watanabe, S., Halfmann, P., Horimoto, T., Neumann, G., Kim, J. H. & other authors (2005). Characterization of a human H5N1 influenza A virus isolated in 2003. J Virol 79, 9926-9932.
46. Smith, G. J. D., Naipospos, T. S. P., Nguyen, T. D., de Jong, M. D., Vijaykrishna, D., Usman, T. B., Hassan, S. S., Nguyen, T. V., Dao, T. V. & other authors (2006). Evolution and adaptation of H5N1 influenza virus in avian and human hosts in Indonesia and Vietnam. Virology 350, 258-268.
47. Steel, J., Lowen, A. C., Mubareka, S. & Palese, P. (2009). Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog 5, e1000252.
48. Subbarao, K. & Shaw, M. W. (2000). Molecular aspects of avian influenza (H5N1) viruses isolated from humans. Rev Med Virol 10, 337-348.
49. Subbarao, E. K., London, W. & Murphy, B. R. (1993). A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J Virol 67, 1761-1764.
50. Sugiyama, K., Obayashi, E., Kawaguchi, A., Suzuki, Y., Tame, J. R., Nagata, K. & Park, S. Y. (2009). Structural insight into the essential PB1-PB2 subunit contact of the influenza virus RNA polymerase. EMBO J 28, 1803-1811.
51. Uiprasertkul, M. P., Puthavathana, P., Sangsiriwut, K., Pooruk, P., Srisook, K., Peiris, M., Nicholls, J. M., Chokephaibulkit, K., Vanprapar, N. & Auewarakul, P. (2005). Influenza A H5N1 replication sites in humans. Emerg Infect Dis 11, 1036-1041.
52. Uiprasertkul, M. P., Kitphati, R., Puthavathana, P., Kriwong, R., Kongchanagul, A., Ungchusak, K., Angkasekwinai, S., Chokephaibulkit, K., Srisook, K. &other authors (2007). Apoptosis and pathogenesis of avian influenza A (H5N1) virus in humans. Emerg Infect Dis 13, 708-712.
53. Vijaykrishna, D., Bahl, J., Riley, S., Duan, L., Zhang, J. X., Chen, H., Peiris, J. S. M., Smith, G. J. D. & Guan, Y. (2008). Evolutionary dynamics and emergence of panzootic H5N1 influenza viruses. PLoS Pathog 4, e1000161.
54. WHO (2011). Cumulative number of confirmed human cases of avian influenza A/(H5N1) reported to WHO. Updated 13 January 2011. http://www.who.int/csr/disease/avian_influenza/country/cases_table_2011_01_13/en/index.html
55. Yen, H. L., Lipatov, A. S., Ilyushina, N. A., Govorkova, E. A., Franks, J., Yilmaz, N., Douglas, A., Hay, A., Krauss, S. & other authors (2007). Inefficient transmission of H5N1 influenza viruses in a ferret contact model. J Virol 81, 6890-6898.
56. Zitzow, L. A., Rowe, T., Morken, T., Shieh, W. J., Zaki, S. & Katz, J. M. (2002). Pathogenesis of avian influenza A (H5N1) viruses in ferrets. J Virol 76, 4420-4429.