Influenza A virus polymerase: A determinant of host range and pathogenicity

Monographs in Virology

Volumn 27, Issue , 2008, Pages 187-194

  Stech, Jürgen ^a  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AVES; INFLUENZA A VIRUS; INFLUENZAVIRUS A; MAMMALIA;

EID: 50549085301     PISSN: 00770965     EISSN: 16623851     Source Type: Book Series    
DOI: 10.1159/000151620     Document Type: Article

References (82)

1. Page MG, Ruck BJ, Brammer KW: Characterization of the ribonucleic acid product synthesized by on influenza A2 virus-induced ribonucleic acid polymerase in vitro. Biochem J 1968;109:43P.
2. Bishop DH, Obijeski JF, Simpson RW: Transcription of the influenza ribonucleic acid genome by a virion polymerase. II. Nature of the in vitro polymerase product. J Virol 1971;8:74-80.
3. Bishop DH, Obijeski JF, Simpson RW: Transcription of the influenza ribonucleic acid genome by a virion polymerase. I. Optimal conditions for in vitro activity of the ribonucleic acid-dependent ribonucleic acid polymerase. J Virol 1971;8:66-73.
4. Bishop DH, Roy P, Bean WJ Jr, Simpson RW: Transcription of the influenza ribonucleic acid genome by a virion polymerase. 3. Completeness of the transcription process. J Virol 1972;10:689-697.
5. Compans RW, Caliguiri LA: Isolation and properties of an RNA polymerase from influenza virusinfected cells. J Virol 1973;11:441-448.
6. Skehel JJ: RNA-dependent RNA polymerase activity of the influenza virus. Virology 1971;45:793-796.
7. Area E, Martin-Benito J, Gastaminza P, Torreira E, Valpuesta JM, Carrascosa JL, Ortin J: 3D structure of the influenza virus polymerase complex: localization of subunit domains. Proc Natl Acad Sci USA 2004;101:308-313.
8. Detjen BM, St Angelo C, Katze MG, Krug RM: 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 1987;61:16-22.
9. Digard P, Blok VC, Inglis SC: Complex formation between influenza virus polymerase proteins expressed in Xenopus oocytes. Virology 1989;171:162-169.
10. Inglis SC, Carroll AR, Lamb RA, Mahy BW: Polypeptides specified by the influenza virus genome I. Evidence for eight distinct gene products specified by fowl plague virus. Virology 1976;74:489-503.
11. Inglis SC, McGeoch DJ, Mahy BW: Polypeptides specified by the influenza virus genoma. 2. Assignment of protein coding functions to individual genome segments by in vitro translation. Virology 1977;78:522-536.
12. Palese P, Ritchey MB, Schulman JL: Mapping of the influenza virus genome. II. Identification of the P1, P2, and P3 genes. Virology 1977;76:114-121.
13. Nath ST, Nayak DP: Function of two discrete regions is required for nuclear localization of polymerase basic protein 1 of A/WSN/33 influenza virus (H1 N1). Mol Cell Biol 1990;10:4139-4145.
14. Mukaigawa J, Nayak DP: Two signals mediate nuclear localization of influenza virus (A/WSN/33) polymerase basic protein 2. J Virol 1991;65:245-253.
15. Nieto A, de la Luna S, Barcena J, Portela A, Valcarcel J, Melero JA, Ortin J: Nudear transport of influenza virus polymerase PA protein. Virus Res 1992;24:65-75.
16. Fodor E, Smith M: The PA subunit is required for efficient nuclear accumulation of the FBI subunit of the influenza A virus RNA polymerase complex. J Virol 2004;78:9144-9153.
17. Mayer D, Molawi K, Martinez-Sobrido L, Ghanem A, Thomas S, Baginsky S, Grossmann J, Garcia-Sastre A, Schwemmle M: Identification of cellular interaction partners of the influenza virus ribonucleoprotein complex and polymerase complex using proteomic-based approaches. J Proteome Res 2007;6: 672-682.
18. Engelhardt OG, Smith M, Fodor E: Association of the influenza A virus RNA-dependent RNA polymerase with cellular RNA polymerase II. J Virol 2005;79:5812-5818.
19. Deng T, Engelhardt OG, Thomas B, Akoulitchev AV, Brownlee GG, Fodor E: Role of ran binding protein 5 in nuclear import and assembly of the influenza virus RNA polymerase complex. J Virol 2006;80:11911-11919.
20. Ye Q, Krug RM, Tao YJ: The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA. Nature 2006;444:1078-1082.
21. Hay AJ, Lomniczi B, Bellamy AR, Skehel JJ: Transcription of the influenza virus genome. Virology 1977;83:337-355.
22. Blaas D, Patzelt E, Kuechler E: Identification of the cap binding protein of influenza virus. Nudeic Acids Res 1982;10:4803-4812.
23. Blaas D, Patzelt E, Kuechler E: Cap-recognizing protein of influenza virus. Virology 1982;116:339-348.
24. Fechter P, Mingay L, Sharps J, Chambers A, Fodor E, Brownlee GG: Two aromatic residues in the PB2 subunit of influenza A RNA polymerase are crucial for cap binding. J Biol Chem 2003;278:20381-20388.
25. Li ML, Ramirez BC, Krug RM: RNA-dependent activation of primer RNA production by influenza virus polymerase: different regions of the same protein subunit constitute the two required RNA-binding sites. EMBO J 1998;17:5844-5852.
26. 7GpppNm) on RNAs and in initiating viral RNA transcription. Proc Natl Acad Sci USA 1981;78:7355-7359.
27. Hara K, Schmidt FI, Crow M, Brownlee GG: Amino acid residues in the N-terminal region of the PA subunit of influenza A virus RNA polymerase play a critical role in protein stability, endonudease activity, cap binding, and virion RNA promoter binding. J Virol 2006;80:7789-7798.
28. Li ML, Rao P, Krug RM: The active sites of the influenza cap-dependent endonudease are on different polymerase subunits. EMBO J 2001;20:2078-2086.
29. Shi L, Summers DF, Peng Q, Galarz JM: Influenza A virus RNA polymerase subunit PB2 is the endonudease which cleaves host cell mRNA and functions only as the trimeric enzyme. Virology 1995;208:38-47.
30. Poon LL, Pritlove DC, Fodor E, Brownlee GG: Direct evidence that the poly(A) tail of influenza A virus mRNA is synthesized by reiterative copying of a U track in the virion RNA template. J Virol 1999;73: 3473-3476.
31. Zheng H, Lee HA, Palese P, Garcia-Sastre A: Influenza A virus RNA polymerase has the ability to stutter at the polyadenylation site of a viral RNA template during RNA replication. J Virol 1999;73:5240-5243.
32. Li X, Palese P: Characterization of the polyadenylation signal of influenza virus RNA. J Virol 1994;68:1245-1249.
33. Luo GX, Luytjes W, Enami M, Palese P: The polyadenylation signal of influenza virus RNA involves a stretch of uridines followed by the RNA duplex of the panhandle structure. J Virol 1991;65: 2861-2867.
34. Poon LL, Pritlove DC, Sharps J, Brownlee GG: The RNA polymerase of influenza virus, bound to the 5′ end of virion RNA, acts in cis to polyadenylate mRNA. J Virol 1998;72:8214-8219.
35. Hay AJ, Skehel JJ, McCauley J: Characterization of influenza virus RNA complete transcripts. Virology 1982;116:517-522.
36. Deng T, Vreede FT, Brownlee GG: Different de novo initiation strategies are used by influenza virus RNA polymerase on its cRNA and viral RNA promoters during viral RNA replication. J Virol 2006;80:2337-2348.
37. Skehel JJ, Hay AJ: Nucleotide sequences at the 5' termini of influenza virus RNAs and their transcripts. Nucleic Acids Res 1978;5:1207-1219.
38. Desselberger U, Racaniello VR, Zazra JJ, Palese P: The 3′- and 5′-terminal sequences of influenza A, B and C virus RNA segments are highly conserved and show partial inverted complementarity. Gene 1980;8:315-328.
39. Hsu MT, Parvin JD, Gupta S, Krystal M, Palese P: Genomic RNAs of influenza viruses are held in a circular conformation in virions and in infected cells by a terminal panhandle. Proc Natl Acad Sci USA 1987;84:8140-8144.
40. Kim HJ, Fodor E, Brownlee GG, Seong BL: Mutational analysis of the RNA-fork model of the influenza A virus vRNA promoter in vivo. J Gen Virol 1997;78:353-357.
41. Fodor E, Seong BL, Brownlee GG: Photochemical cross-linking of influenza A polymerase to its virion RNA promoter defines a polymerase binding site at residues 9 to 12 of the promoter. J Gen Virol 1993;74:1327-1333.
42. Flick R, Hobom G: Interaction of influenza virus polymerase with viral RNA in the 'corkscrew' conformation. J Gen Virol 1999;80:2565-2572.
43. Azzeh M, Flick R, Hobom G: Functional analysis of the influenza A virus cRNA promoter and construction of an ambisense transcription system. Virology 2001;289:400-410.
44. Crow M, Deng T, Addley M, Brownlee GG: Mutational analysis of the influenza virus cRNA promoter and identification of nucleotides critical for replication. J Virol 2004;78:6263-6270.
45. Flick R, Neumann G, Hoffmann E, Neumeier E, Hobom G: Promoter elements in the influenza vRNA terminal structure. RNA 1996;2:1046-1057.
46. Barrett T, Wolstenholme AJ, Mahy BW: Transcription and replication of influenza virus RNA. Virology 1979;98:211-225.
47. Hatada E, Hasegawa M, Mukaigawa J, Shimizu K, Fukuda R: Control of influenza virus gene expression: quantitative analysis of each viral RNA species in infected cells. J Biochem 1989;105:537-546.
48. Taylor JM, Illmensee R, Litwin S, Herring L, Broni B, Krug RM: Use of specific radioactive probes to study transcription and replication of the influenza virus genome. J Virol 1977;21:530-540.
49. Vreede FT, Jung TE, Brownlee GG: Model suggesting that replication of influenza virus is regulated by stabilization of replicative intermediates. J Virol 2004;78:9568-9572.
50. Vreede FT, Brownlee GG: Influenza virion-derived viral ribonudeoproteins synthesize both mRNA and cRNA in vitro. J Virol 2007;81:2196-2204.
51. Rott R, Orlich M, Scholtissek C: Correlation of pathogenicity and gene constellation of influenza A viruses. III. Non-pathogenic recombinants derived from highly pathogenic parent strains. J Gen Virol 1979;44:471-477.
52. Scholtissek C, Vallbracht A, Flehmig B, Rott R: Correlation of pathogenicity and gene constellation of influenza A viruses. II. Highly neurovirulent recombinants derived from non-neurovirulent or weakly neuro-virulent parent virus strains. Virology 1979;95:492-500.
53. Vallbracht A, Scholtissek C, Flehmig B, Gerth HJ: Recombination of influenza A strains with fowl plague virus can change pneumotropism for mice to a generalized infection with involvement of the central nervous system. Virology 1980;107:452-460.
54. Snyder MH, Buckler-White AJ, London WT, Tierney EL, Murphy BR: The avian influenza virus nudeoprotein gene and a specific constellation of avian and human virus polymerase genes each specify attenuation of avian-human influenza A/Pintail/79 reassortant viruses for monkeys. J Virol 1987;61:2857-2863.
55. Hoffmann E, Neumann G, Kawaoka Y, Hobom G, Webster RG: A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci USA 2000;97:6108-6113.
56. Neumann G, Watanabe T, Ito H, Watanabe S, Goto H, Gao P, Hughes M, Perez DR, Donis R, Hoffmann E, Hobom G, Kawaoka Y: Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci USA 1999;96:9345-9350.
57. Fodor E, Devenish L, Engelhardt OG, Palese P, Brownlee GG, Garcia-Sastre A: Rescue of influenza A virus from recombinant DNA. J Virol 1999;73:9679-9682.
58. Subbarao EK, London W, Murphy BR: A single amino add in the FB2 gene of influenza A virus is a determinant of host range. J Virol 1993;67:1761-1764.
59. Massin P, van der WS, Naffakh N: Residue 627 of PB2 is a determinant of cold sensitivity in RNA replication of avian influenza viruses. J Virol 2001;75:5398-5404.
60. Gao P, Watanabe S, Ito T, Goto H, Wells K, McGregor M, Cooley AJ, Kawaoka Y: Biological heterogeneity, including systemic replication in mice, of H5N1 influenza A virus isolates from humans in Hong Kong. J Virol 1999;73:3184-189.
61. Hatte M, Gao P, Halfmann P, Kawaoka Y: Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 2001;293:1840-1842.
62. Salomon R, Franks J, Govorkova EA, Ilyushina NA, Yen HL, Hulse-Post DJ, Humberd J, Trichet M, Rehg JE, Webby RJ, Webster RG, 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 2006;203:689-697.
63. Shinya K, Hamm S, Hatt M, Ito H, Ito T, 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 2004;320:258-266.
64. Govorkova EA, Rehg JE, Krauss S, Yen HL, Guan Y, Peiris M, Nguyen TD, Hanh TH, Puthavathana P, Long HT, Buranathai C, Lim W, Webster RG, Hoffmann E: Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J Virol 2005;79:2191-2198.
65. Puthavathana P, Auewarakul P, Charoenying PC, Sangsiriwut K, Pooruk P, Boonnak K, Khanyok R, Thawachsupa P, Kijphati R, Sawanpanyalert P: Molecular characterization of the complete genome of human influenza H5N1 virus isolates from Thailand. J Gen Virol 2005;86:423-433.
66. De Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN, Hoang DM, Chau NV, Khanh TH, Dong VC, Qui PT, Cam BV, Ha do Q, Guan Y, Peiris JS, Chinh NT, Hien TT, Farrar J: Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 2006;12:1203-1207.
67. Fouchier RA, Schneeberger PM, Rozendaal FW, Broekman JM, Kemink SA, Munster V, Kuiken T, Rimmelzwaan GF, Schutten M, Van Doornum GJ, Koch G, Bosman A, Koopmans M, Osterhaus AD: Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci USA 2004;101:1356-1361.
68. Taubenberger JK, Reid AH, Lourens RM, Wang R, Jin G, Fanning TG: Characterization of the 1918 influenza virus polymerase genes. Nature 2005;437:889-893.
69. Gabriel G, Dauber B, Wolff T, Planz O, Klenk HD, Stech J: The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci USA 2005;102:18590-18595.
70. Brown EG, Liu H, Kit LC, Baird S, 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 USA 2001;98:6883-6888.
71. Hiromoto Y, Saito T, Lindstrom S, Nerome K: Characterization of low virulent strains of highly pathogenic A/Hong Kong/156/97 (H5N1) virus in mice after passage in embryonated hens' eggs. Virology 2000;272:429-437.
72. Naffakh N, Massin P, Escriou N, Crescenzo-Chaigne B, van der Werf S: Genetic analysis of the compatibility between polymerase proteins from human and avian strains of influenza A viruses. J Gen Virol 2000;81:1283-1291.
73. Li Z, Chen H, Jiao P, Deng G, Tian G, Li Y, Hoffmann E, Webster RG, Matsuoka Y, Yu K: Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model. J Virol 2005;79:12058-12064.
74. Hatta M, Asano Y, Masunaga K, Ito T, Okazaki K, Toyoda T, Kawaoka Y, Ishihama A, Kida H: Mapping of functional domains on the influenza A virus RNA polymerase PB2 molecule using monoclonal antibodies. Arch Virol 2000;145:1947-1961.
75. Ludwig S, Stitz L, Planz O, Van H, Fitch WM, Scholtissek C: European swine virus as a possible source for the next influenza pandemic? Virology 1995;212:555-561.
76. Schultz U, Fitch WM, Ludwig S, Mandler J, Scholtissek C: Evolution of pig influenza viruses. Virology 1991;183:61-73.
77. Guan Y, Peiris JS, Lipatov AS, Ellis TM, Dyrting KC, Krauss S, Zhang LJ, Webster RG, Shortridge KF: Emergence of multiple genotypes of H5N1 avian influenza viruses in Hong Kong SAR. Proc Natl Acad Sci USA 2002;99:8950-8955.
78. Xu X, Subbarao, Cox NJ, Guo Y: 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 1999;261:15-19.
79. Choi YK, Ozaki H, Webby RJ, Webster RG, Peiris JS, Poon L, Butt C, Leung YH, Guan Y: Continuing evolution of H9N2 influenza viruses in Southeastern China. J Virol 2004;78:8609-8614.
80. Guan Y, Shortridge KF, Krauss S, Webster RG: Molecular characterization of H9N2 influenza viruses: were they the donors of the 'internal' genes of H5N1 viruses in Hong Kong? Proc Natl Acad Sci USA 1999;96:9363-9367.
81. Hoffmann E, Stech J, Leneva I, Krauss S, Scholtissek C, Chin PS, Peiris M, Shortridge KF, Webster RG: 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 2000;74:6309-6315.
82. Gabriel G, Abram M, Keiner B, Wagner R, Klenk HD, Stech J: Differential polymerase activity in avian and mammalian cells determines host range of influenza virus. J Virol 2007;81:9601-9604.