The N-terminal region of the PA subunit of the RNA polymerase of influenza A/HongKong/156/97 (H5N1) influences promoter binding

PLoS ONE

Volumn 4, Issue 5, 2009, Pages

  Kashiwagi, Takahito ^a,b   Leung, Bo Wah ^a,c   Deng, Tao ^a,d   Chen, Hualan ^e   Brownlee, George G ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^d NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

^e INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

RNA POLYMERASE; CROSS LINKING REAGENT; DNA DIRECTED RNA POLYMERASE; PA PROTEIN, INFLUENZA VIRUSES; RIBONUCLEOPROTEIN; RNA DIRECTED RNA POLYMERASE; VIRUS PROTEIN; VIRUS RNA;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME STRUCTURE; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLUENZA VIRUS A H5N1; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN BINDING; STRAIN DIFFERENCE; VIRUS ISOLATION; VIRUS STRAIN; VIRUS VIRULENCE; ANIMAL; CHICK EMBRYO; CHICKEN; CYTOLOGY; ENZYMOLOGY; GENETIC TRANSCRIPTION; GENETICS; KIDNEY; METABOLISM; PHYSIOLOGY; ULTRAVIOLET RADIATION; VIROLOGY; VIRUS REPLICATION;

ORTHOMYXOVIRIDAE;

ANIMALS; CHICK EMBRYO; CHICKENS; CROSS-LINKING REAGENTS; DNA-DIRECTED RNA POLYMERASES; HUMANS; INFLUENZA A VIRUS, H5N1 SUBTYPE; KIDNEY; PROMOTER REGIONS, GENETIC; RIBONUCLEOPROTEINS; RNA REPLICASE; RNA, VIRAL; TRANSCRIPTION, GENETIC; ULTRAVIOLET RAYS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 65549162170     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005473     Document Type: Article

References (66)

1. Palese P, Shaw ML (2007) Orthomyxoviridae: the viruses and their replication, In: Knipe DM, Howley RM, eds. Fields virology, 5 ed. Philadelphia, PA: Lippincott Williams & Wilkins. pp 1647-1689.
2. Fodor E, Brownlee GG (2002) Influenza virus replication. In: Potter CW, ed. Influenza. New York, NY: Elsevier. pp 1-29.
3. Bouloy M, Plotch SJ, Krug RM (1978) Globin mRNAs are primers for the transcription of influenza viral RNA in vitro. Proc. Natl. Acad. Sci. USA 75: 4886-4890.
4. Plotch SJ, Bouloy M, Krug RM (1979) Transfer of 5′-terminal cap of globin mRNA to influenza viral complementary RNA during transcription in vitro. Proc. Natl. Acad. Sci. USA 76: 1618-1622.
5. Fechter P, Brownlee GG (2005) Recognition of mRNA cap structures by viral and cellular proteins. J. Gen. Virol. 86: 1239-1249.
6. Hara K, Schmidt FI, Crow M, Brownlee GG (2006) 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, endonuclease activity, cap binding, and virion RNA promoter binding. J. Virol. 80: 7789-7798.
7. Plotch SJ, Bouloy M, Ulmanen I, Krug RM (1981) A unique cap(m7GpppXm)-dependent influenza virion endonuclease cleaves capped RNAs to generate the primers that initiate viral RNA transcription. Cell 23: 847-858.
8. Neumann G, Brownlee GG, Fodor E, Kawaoka Y (2004) Orthomyxovirus replication, transcription, and polyadenylation. Curr. Topics Microbiol. Immunol. 283: 121-143.
9. Area E, Martin-Benito J, Gastaminza P, Torreira E, Valpuesta JM, et al. (2004) 3D structure of the influenza virus polymerase complex: localization of subunit domains. Proc. Natl. Acad. Sci. USA 101: 308-313.
10. Ortin J, Parra F (2006) Structure and function of RNA replication. Ann. Rev. Microbiol. 60: 305-326.
11. Torreira E, Schoehn G, Fernandez Y, Jorba N, Ruigrok RW, et al. (2007) Three-dimensional model for the isolated recombinant influenza virus polymerase heterotrimer. Nucleic Acids Res. 35: 3774-3783.
12. He X, Zhou J, Bartlam M, Zhang R, Ma J, et al. (2008) Crystal structure of the polymerase PA(C)-PB1(N) complex from an avian influenza H5N1 virus. Nature 454: 1123-1126.
13. N reveals an endonuclease active site. Nature. In press.
14. Dias A, Bouvier D, Crépin T, McCarthy AA, Hart DJ, et al. (2009) The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature. In press.
15. Guilligay D, Tarendeau F, Resa-Infante P, Coloma R, Crepin T, et al. (2008) The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat. Struct. Mol. Biol. 15: 500-506.
16. Tarendeau F, Boudet J, Guilligay D, Mas PJ, Bougault CM, et al. (2007) Structure and nuclear import function of the C-terminal domain of influenza virus polymerase PB2 subunit. Nat. Struct. Mol. Biol. 14: 229-233.
17. Fodor E, Crow M, Mingay LJ, Deng T, Sharps J, et al. (2002) A single amino acid mutation in the PA subunit of the influenza virus RNA polymerase inhibits endonucleolytic cleavage of capped RNAs. J. Virol. 76: 8989-9001.
18. Honda A, Mizumoto K, Ishihama A (2002) Minimum molecular architectures for transcription and replication of the influenza virus. Proc. Natl. Acad. Sci. USA 99: 13166-13171.
19. Biswas SK, Nayak DP (1994) Mutational analysis of the conserved motifs of influenza A virus polymerase basic protein 1. J. Virol. 68: 1819-1826.
20. Li ML, Rao P, Krug RM (2001) The active sites of the influenza cap-dependent endonuclease are on different polymerase subunits. EMBO J. 20: 2078-2086.
21. Fechter P, Mingay L, Sharps J, Chambers A, Fodor E, et al. (2003) Two aromatic residues in the PB2 subunit of influenza A RNA polymerase are crucial for cap binding. J. Biol. Chem. 278: 20381-20388.
22. Lee MT, Bishop K, Medcalf L, Elton D, Digard P, et al. (2002) Definition of the minimal viral components required for the initiation of unprimed RNA synthesis by influenza virus RNA polymerase. Nucleic Acids Res. 30: 429-438.
23. Maier HJ, Kashiwagi T, Hara K, Brownlee GG (2008) Differential role of the influenza A virus polymerase PA subunit for vRNA and cRNA promoter binding. Virology 370: 194-204.
24. Hara K, Shiota M, Kido H, Ohtsu Y, Kashiwagi T, et al. (2001) Influenza virus RNA polymerase PA subunit is a novel serine protease with Ser624 at the active site. Genes Cells 6: 87-97.
25. Perales B, Sanz-Ezquerro JJ, Gastaminza P, Ortega J, Santaren JF, et al. (2000) The replication activity of influenza virus polymerase is linked to the capacity of the PA subunit to induce proteolysis. J. Virol. 74: 1307-1312.
26. Rodriguez A, Perez-Gonzalez A, Nieto A (2007) Influenza virus infection causes specific degradation of the largest subunit of cellular RNA polymerase II. J. Virol. 81: 5315-5324.
27. De BK, Brownlee GG, Kendal AP, Shaw MW (1988) Complete sequence of a cDNA clone of the hemagglutinin gene of influenza A/Chicken/Scotland/59 (H5N1) virus: comparison with contemporary North American and European strains. Nucleic Acids Res. 16: 4181-4182.
28. Wood GW, McCauley JW, Bashiruddin JB, Alexander DJ (1993) Deduced amino acid sequences at the haemagglutinin cleavage site of avian influenza A viruses of H5 and H7 subtypes. Arch. Virol. 130: 209-217.
29. Xu X, Subbarao EK, Cox NJ, 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.
30. Claas EC, de Jong JC, van Beek R, Rimmelzwaan GF, Osterhaus AD (1998) Human influenza virus A/HongKong/156/97 (H5N1) infection. Vaccine 16: 977-978.
31. Claas EC, Osterhaus AD, van Beek R, De Jong JC, Rimmelzwaan GF, et al. (1998) Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 351: 472-477.
32. Shortridge KF, Zhou NN, Guan Y, Gao P, Ito T, et al. (1998) Characterization of avian H5N1 influenza viruses from poultry in Hong Kong. Virology 252: 331-342.
33. Suarez DL, Perdue ML, Cox N, Rowe T, Bender C, et al. (1998) Comparisons of highly virulent H5N1 influenza A viruses isolated from humans and chickens from Hong Kong. J. Virol. 72: 6678-6688.
34. Abdel-Ghafar AN, Chotpitayasunondh T, Gao Z, Hayden FG, Nguyen DH, et al. (2008) Update on avian influenza A (H5N1) virus infection in humans. N. Engl. J. Med. 358: 261-273.
35. Li Y, Lin Z, Shi J, Qi Q, Deng G, et al. (2006) Detection of Hong Kong 97-like H5N1 influenza viruses from eggs of Vietnamese waterfowl. Arch. Virol. 151: 1615-1624.
36. Webster RG, Guan Y, Peiris M, Walker D, Krauss S, et al. (2002) Characterization of H5N1 influenza viruses that continue to circulate in geese in southeastern China. J. Virol. 76: 118-126.
37. Neumann G, Shinya K, Kawaoka Y (2007) Molecular pathogenesis of H5N1 influenza virus infections. Antivir. Ther. 12: 617-626.
38. Ito T, Suzuki Y, Suzuki T, Takada A, Horimoto T, et al. (2000) Recognition of N-glycolylneuraminic acid linked to galactose by the alpha 2, 3 linkage is associated with intestinal replication of influenza A virus in ducks. J. Virol. 74: 9300-9305.
39. Vines A, Wells K, Matrosovich M, Castrucci MR, Ito T, et al. (1998) The role of influenza A virus hemagglutinin residues 226 and 228 in receptor specificity and host range restriction. J. Virol. 72: 7626-7631.
40. 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.
41. Subbarao EK, London W, Murphy BR (1993) A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J. Virol. 67: 1761-1764.
42. Uyeki TM (2008) Global epidemiology of human infections with highly pathogenic avian influenza A (H5N1) viruses. Respirology 13 Suppl 1: S2-9.
43. Hulse-Post DJ, Franks J, Boyd K, Salomon R, Hoffmann E, et al. (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.
44. Wasilenko JL, Lee CW, Sarmento L, Spackman E, Kapczynski DR, et al. (2008) NP, PB1, and PB2 viral genes contribute to altered replication of H5N1 avian influenza viruses in chickens. J. Virol. 82: 4544-4553.
45. Brownlee GG, Sharps JL (2002) The RNA polymerase of influenza a virus is stabilized by interaction with its viral RNA promoter. J. Virol. 76: 7103-7113.
46. Fodor E, Mingay LJ, Crow M, Deng T, Brownlee GG (2003) A single amino acid mutation in the PA subunit of the influenza virus RNA polymerase promotes the generation of defective interfering RNAs. J. Virol. 77: 5017-5020.
47. Fodor E, Smith M (2004) The PA subunit is required for efficient nuclear accumulation of the PB1 subunit of the influenza A virus RNA polymerase complex. J. Virol. 78: 9144-9153.
48. Massin P, Rodrigues P, Marasescu M, van der Werf S, Naffakh N (2005) Cloning of the chicken RNA polymerase I promoter and use for reverse genetics of influenza A viruses in avian cells. J. Virol. 79: 13811-13816.
49. Labadie K, Dos Santos Afonso E, Rameix-Welti MA, van der Werf S, Naffakh N (2007) 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: 271-282.
50. Subbarao EK, Klimov A, Katz J, Regnery H, Lim W, et al. (1998) Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279: 393-396.
51. Tran TH, Nguyen TL, Nguyen TD, Luong TS, Pham PM, et al. (2004) Avian influenza A (H5N1) in 10 patients in Vietnam. N. Engl. J. Med. 350: 1179-1188.
52. Blom N, Gammeltoft S, Brunak S (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294: 1351-1362.
53. Chan AY, Vreede FT, Smith M, Engelhardt OG, Fodor E (2006) Influenza virus inhibits RNA polymerase II elongation. Virology 351: 210-217.
54. Huarte M, Sanz-Ezquerro JJ, Roncal F, Ortin J, Nieto A (2001) PA subunit from influenza virus polymerase complex interacts with a cellular protein with homology to a family of transcriptional activators. J. Virol. 75: 8597-8604.
55. Kawaguchi A, Nagata K (2007) De novo replication of the influenza virus RNA genome is regulated by DNA replicative helicase, MCM. EMBO J. 26: 4566-4575.
56. Hiromoto Y, Saito T, Lindstrom S, Nerome K (2000) Characterization of low virulent strains of highly pathogenic A/Hong Kong/156/97 (H5N1) virus in mice after passage in embryonated hens' eggs. Virology 272: 429-437.
57. Treanor J, Perkins M, Battaglia R, Murphy BR (1994) Evaluation of the genetic stability of the temperature-sensitive PB2 gene mutation of the influenza A/Ann Arbor/6/60 cold-adapted vaccine virus. J. Virol. 68: 7684-7688.
58. Deng T, Sharps J, Fodor E, Brownlee GG (2005) In vitro assembly of PB2 with a PB1-PA dimer supports a new model of assembly of influenza A virus polymerase subunits into a functional trimeric complex. J. Virol. 79: 8669-8674.
59. Bishop DH, Huddleston JA, Brownlee GG (1982) The complete sequence of RNA segment 2 of influenza A/NT/60/68 P1 protein. Nucleic Acids Res. 10: 1335-1343.
60. Bishop DH, Jones KL, Huddleston JA, Brownlee GG (1982) Influenza A virus evolution: complete sequences of influenza A/NT/60/68 RNA segment 3 and its predicted acidic P polypeptide compared with those of influenza A/PR/ 8/34. Virology 120: 481-489.
61. Jones KL, Huddleston JA, Brownlee GG (1983) The sequence of RNA segment 1 of influenza virus A/NT/60/68 and its comparison with the corresponding segment of strains A/PR/8/34 and A/WSN/33. Nucleic Acids Res. 11: 1555-1566.
62. Chen H, Deng G, Li Z, Tian G, Li Y, et al. (2004) The evolution of H5N1 influenza viruses in ducks in southern China. Proc. Natl. Acad. Sci. U.S.A. 101: 10452-10457.
63. Fan S, Deng G, Song J, Tian G, Suo Y, et al. (2009) Two amino acid residues in the matrix protein M1 contribute to the virulence difference of H5N1 avian influenza viruses in mice. Virology 384: 28-32.
64. Li KS, Guan Y, Wang J, Smith GJ, Xu KM, et al. (2004) Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 430: 209-213.
65. Deng T, Sharps JL, Brownlee GG (2006) Role of the influenza virus heterotrimeric RNA polymerase complex in the initiation of replication. J. Gen. Virol. 87: 3373-3377.
66. Deng T, Vreede FT, Brownlee GG (2006) 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. 80: 2337-2348.