Single mutation at the amino acid position 627 of PB2 that leads to increased virulence of an H5N1 avian influenza virus during adaptation in mice can be compensated by multiple mutations at other sites of PB2

Virus Research

Volumn 144, Issue 1-2, 2009, Pages 123-129

  Li, Junwei ^a   Ishaq, Musarat ^a   Prudence, Mabiala ^a   Xi, Xiao ^a   Hu, Tao ^a   Liu, Qingzhen ^a   Guo, Deyin ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

Adaptation; H5N1 influenza virus; Mice; PB2

Indexed keywords

GLUTAMIC ACID; HA PROTEIN; LYSINE; PB2 PROTEIN; PROTEIN M1; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ADAPTATION; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE MUTATION; GENETIC REASSORTMENT; HUMAN; HUMAN CELL; INFLUENZA VIRUS A H5N1; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERTANT; VIRUS INFECTIVITY; VIRUS MUTATION; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS VIRULENCE;

AMINO ACID SUBSTITUTION; ANIMALS; DNA MUTATIONAL ANALYSIS; INFLUENZA A VIRUS, H5N1 SUBTYPE; LUNG; MICE; MICE, INBRED BALB C; MUTATION, MISSENSE; REASSORTANT VIRUSES; RNA REPLICASE; SERIAL PASSAGE; SUPPRESSION, GENETIC; VIRAL PROTEINS; VIRULENCE;

ANIMALIA; AVIAN INFLUENZA VIRUS; MAMMALIA; MUS; ORTHOMYXOVIRIDAE;

EID: 69349096064     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2009.04.008     Document Type: Article

References (40)

1. Auewarakul P., Suptawiwat O., Kongchanagul A., Sangma C., Suzuki Y., Ungchusak K., Louisirirotchanakul S., Lerdsamran H., Pooruk P., Thitithanyanont A., Pittayawonganon C., Guo C.T., Hiramatsu H., Jampangern W., Chunsutthiwat S., and Puthavathana P. An avian influenza H5N1 virus that binds to a human-type receptor. J. Virol. 81 September (18) (2007) 9950-9955
2. Baranowski E., Ruiz-Jarabo C.M., and Domingo E. Evolution of cell recognition by viruses. Science 292 May (5519) (2001) 1102-1105
3. Beare A.S., and Webster R.G. Replication of avian influenza viruses in humans. Arch. Virol. 119 1-2 (1991) 37-42
4. Blok V., Cianci C., Tibbles K.W., Inglis S.C., Krystal M., and Digard P. Inhibition of the influenza virus RNA-dependent RNA polymerase by antisera directed against the carboxy-terminal region of the PB2 subunit. J. Gen. Virol. 77 May (Pt 5) (1996) 1025-1033
5. Brown E.G., and Bailly J.E. Genetic analysis of mouse-adapted influenza A virus identifies roles for the NA, PB1, and PB2 genes in virulence. Virus Res. 61 May (1) (1999) 63-76
6. Brown E.G., Liu H., Kit L.C., Baird S., and Nesrallah M. Pattern of mutation in the genome of influenza A virus on adaptation to increased virulence in the mouse lung: identification of functional themes. Proc. Natl. Acad. Sci. U.S.A. 98 June (12) (2001) 6883-6888
7. Clements M.L., Subbarao E.K., Fries L.F., Karron R.A., London W.T., and Murphy B.R. Use of single-gene reassortant viruses to study the role of avian influenza A virus genes in attenuation of wild-type human influenza A virus for squirrel monkeys and adult human volunteers. J. Clin. Microbiol. 30 March (3) (1992) 655-662
8. Detjen B.M., St Angelo C., Katze M.G., and Krug R.M. The three influenza virus polymerase (P) proteins not associated with viral nucleocapsids in the infected cell are in the form of a complex. J. Virol. 61 January (1) (1987) 16-22
9. Fouchier R.A., Schneeberger P.M., Rozendaal F.W., Broekman J.M., Kemink S.A., Munster V., Kuiken T., Rimmelzwaan G.F., Schutten M., Van Doornum G.J., Koch G., Bosman A., Koopmans M., and Osterhaus A.D. Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc. Natl. Acad. Sci. U.S.A. 101 February (5) (2004) 1356-1361
10. Gabriel G., Abram M., Keiner B., Wagner R., Klenk H.D., and Stech J. Differential polymerase activity in avian and mammalian cells determines host range of influenza virus. J. Virol. 81 September (17) (2007) 9601-9604
11. Gabriel G., Dauber B., Wolff T., Planz O., Klenk H.D., and Stech J. The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc. Natl. Acad. Sci. U.S.A. 102 December (51) (2005) 18590-18595
12. Gabriel G., Herwig A., and Klenk H.D. Interaction of polymerase subunit PB2 and NP with importin alpha1 is a determinant of host range of influenza A virus. PLoS Pathog. 4 February (2) (2008) e11
13. Gao P., Watanabe S., Ito T., Goto H., Wells K., McGregor M., Cooley A.J., and Kawaoka Y. Biological heterogeneity, including systemic replication in mice, of H5N1 influenza A virus isolates from humans in Hong Kong. J. Virol. 73 April (4) (1999) 3184-3189
14. Govorkova E.A., Rehg J.E., Krauss S., Yen H.L., Guan Y., Peiris M., Nguyen T.D., Hanh T.H., Puthavathana P., Long H.T., Buranathai C., Lim W., Webster R.G., and Hoffmann E. Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J. Virol. 79 February (4) (2005) 2191-2198
15. Harvey R., Martin A.C., Zambon M., and Barclay W.S. Restrictions to the adaptation of influenza a virus H5 hemagglutinin to the human host. J. Virol. 78 January (1) (2004) 502-507
16. Hatta M., Gao P., Halfmann P., and Kawaoka Y. Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293 September (5536) (2001) 1840-1842
17. Hatta M., Hatta Y., Kim J.H., Watanabe S., Shinya K., Nguyen T., Lien P.S., Le Q.M., and Kawaoka Y. Growth of H5N1 influenza A viruses in the upper respiratory tracts of mice. PLoS Pathog. 3 October (10) (2007) 1374-1379
18. Hoffmann E., Stech J., Guan Y., Webster R.G., and Perez D.R. Universal primer set for the full-length amplification of all influenza A viruses. Arch. Virol. 146 December (12) (2001) 2275-2289
19. Hoffmann E., Neumann G., Kawaoka Y., Hobom G., and Webster R.G. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc. Natl. Acad. Sci. U.S.A. 97 May (11) (2000) 6108-6113
20. Jiao P., Tian G., Li Y., Deng G., Jiang Y., Liu C., Liu W., Bu Z., Kawaoka Y., and Chen H. A single amino acid substitution in the NS1 protein changes the pathogenicity of H5N1 avian influenza viruses in mice. J. Virol. 82 February (3) (2008) 1146-1154
21. Katz J.M., Lu X., Tumpey T.M., Smith C.B., Shaw M.W., and Subbarao K. Molecular correlates of influenza A H5N1 virus pathogenesis in mice. J. Virol. 74 November (22) (2000) 10807-10810
22. Labadie K., Dos Santos Afonso E., Rameix-Welti M.A., van der Werf S., and Naffakh N. Host-range determinants on the PB2 protein of influenza A viruses control the interaction between the viral polymerase and nucleoprotein in human cells. Virology 362 June (2) (2007) 271-282
23. Li J., Cai H., Liu Q., and Guo D. Molecular and pathological characterization of two H5N1 avian influenza viruses isolated from wild ducks. Virus Genes 37 August (1) (2008) 88-95
24. Li Z., Chen H., Jiao P., Deng G., Tian G., Li Y., Hoffmann E., Webster R.G., Matsuoka Y., and Yu K. Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model. J. Virol. 79 September (18) (2005) 12058-12064
25. Mahy B.W., Barrett T., Briedis D.J., Brownson J.M., and Wolstenholme A.J. Influence of the host cell on influenza virus replication. Phil. Trans. R. Soc. Lond. B: Biol. Sci. 288 February (1029) (1980) 349-357
26. 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., Thawatsupha P., Chittaganpitch M., Waicharoen S., Nguyen D.T., Nguyen T., Nguyen H.H., Kim J.H., Hoang L.T., Kang C., Phuong L.S., Lim W., Zaki S., Donis R.O., Cox N.J., Katz J.M., and Tumpey T.M. Avian influenza (H5N1) viruses isolated from humans in Asia in 2004 exhibit increased virulence in mammals. Virology 79 September (18) (2005) 11788-11800
27. Mase M., Tanimura N., Imada T., Okamatsu M., Tsukamoto K., and Yamaguchi S. Recent H5N1 avian influenza A virus increases rapidly in virulence to mice after a single passage in mice. J. Gen. Virol. 87 December (Pt 12) (2006) 3655-3659
28. Murphy B.R., Hinshaw V.S., Sly D.L., London W.T., Hosier N.T., Wood F.T., Webster R.G., and Chanock R.M. Virulence of avian influenza A viruses for squirrel monkeys. Infect. Immun. 37 September (3) (1982) 1119-1126
29. Naffakh N., Massin P., Escriou N., Crescenzo-Chaigne B., and van der Werf S. Genetic analysis of the compatibility between polymerase proteins from human and avian strains of influenza A viruses. J. Gen. Virol. 81 May (Pt 5) (2000) 1283-1291
30. Neumann G., and Kawaoka Y. Host range restriction and pathogenicity in the context of influenza pandemic. Emerg. Infect. Dis. 12 June (6) (2006) 881-886
31. Penn C. The role of RNA segment 1 in an in vitro host restriction occurring in an avian influenza virus mutant. Virus Res. 12 April (4) (1989) 349-359
32. Rogers G.N., and Paulson J.C. Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 127 June (2) (1983) 361-373
33. Salomon R., Franks J., Govorkova E.A., Ilyushina N.A., Yen H.L., Hulse-Post D.J., Humberd J., Trichet M., Rehg J.E., Webby R.J., Webster R.G., and Hoffmann E. The polymerase complex genes contribute to the high virulence of the human H5N1 influenza virus isolate A/Vietnam/1203/04. J. Exp. Med. 203 March (3) (2006) 689-697
34. Seo S.H., Hoffmann E., and Webster R.G. Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat. Med. 8 September (9) (2002) 950-954
35. Shinya K., Hamm S., Hatta M., Ito H., Ito T., and Kawaoka Y. PB2 amino acid at position 627 affects replicative efficiency, but not cell tropism, of Hong Kong H5N1 influenza A viruses in mice. Virology 320 March (2) (2004) 258-266
36. Shinya K., Watanabe S., Ito T., Kasai N., and Kawaoka Y. Adaptation of an H7N7 equine influenza A virus in mice. J. Gen. Virol. 88 February (Pt 2) (2007) 547-553
37. Subbarao E.K., London W., and Murphy B.R. A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J. Virol. 67 April (4) (1993) 1761-1764
38. Taubenberger J.K., Reid A.H., Lourens R.M., Wang R., Jin G., and Fanning T.G. Characterization of the 1918 influenza virus polymerase genes. Nature 437 October (7060) (2005) 889-893
39. Yao Y., Mingay L.J., McCauley J.W., and Barclay W.S. Sequences in influenza A virus PB2 protein that determine productive infection for an avian influenza virus in mouse and human cell lines. J. Virol. 75 June (11) (2001) 5410-5415
40. Yen H.L., Lipatov A.S., Ilyushina N.A., Govorkova E.A., Franks J., Yilmaz N., Douglas A., Hay A., Krauss S., Rehg J.E., Hoffmann E., and Webster R.G. Inefficient transmission of H5N1 influenza viruses in a ferret contact model. J. Virol. 81 July (13) (2007) 6890-6898