Artificial hybrids of influenza a virus RNA polymerase reveal PA subunit modulates its thermal sensitivity

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Kashiwagi, Takahito ^a   Hara, Koyu ^a   Nakazono, Yoko ^a   Hamada, Nobuyuki ^a   Watanabe, Hiroshi ^a  

^a KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY RNA; MESSENGER RNA; RIBONUCLEOPROTEIN; RNA POLYMERASE; RNA POLYMERASE PA SUBUNIT; RNA POLYMERASE PB1 SUBUNIT; RNA POLYMERASE PB2 SUBUNIT; UNCLASSIFIED DRUG; VIRUS ENZYME; VIRUS RNA; DNA DIRECTED RNA POLYMERASE; VIRUS PROTEIN;

ARTICLE; ARTIFICIAL HYBRIDIZATION; CONTROLLED STUDY; ENZYME ACTIVITY; HEAT SHOCK; INFLUENZA VIRUS A; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS A H5N1; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; RNA REPLICATION; RNA TRANSCRIPTION; STEADY STATE; TEMPERATURE SENSITIVITY; TEMPERATURE STRESS; VIRUS HYBRID; BODY TEMPERATURE; CELL LINE; CHEMISTRY; COLD; ENZYMOLOGY; GENETICS; HEAT; HUMAN; METABOLISM; PANDEMIC; PLASMID; TEMPERATURE;

INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

BODY TEMPERATURE; CELL LINE; COLD TEMPERATURE; DNA-DIRECTED RNA POLYMERASES; HOT TEMPERATURE; HUMANS; INFLUENZA A VIRUS; MUTAGENESIS; PANDEMICS; PLASMIDS; RIBONUCLEOPROTEINS; TEMPERATURE; VIRAL PROTEINS;

EID: 78650092717     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015140     Document Type: Article

References (51)

1. Centers for Disease Control and Prevention (CDC) (2009) Update: novel influenza A (H1N1) virus infection - Mexico, March-May, 2009. MMWR Morb Mortal Wkly Rep 58: 585-589.
2. Centers for Disease Control and Prevention (CDC) (2009) Update: novel influenza A (H1N1) virus infections - worldwide, May 6, 2009. MMWR Morb Mortal Wkly Rep 58: 453-458.
3. World Health Organization (WHO) (2010) Pandemic (H1N1) 2009. http://wwwwhoint/csr/disease/swineflu/en/indexhtml.
4. Itoh Y, Shinya K, Kiso M, Watanabe T, Sakoda Y, et al. (2009) In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature 460: 1021-1025.
5. Dawood FS, Jain S, Finelli L, Shaw MW, Lindstrom S, et al. (2009) Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med 360: 2605-2615.
6. Peiris JS, Poon LL, Guan Y (2009) Emergence of a novel swine-origin influenza A virus (S-OIV) H1N1 virus in humans. J Clin Virol 45: 169-173.
7. Danishuddin M, Khan SN, Khan AU (2009) Phylogenetic analysis of surface proteins of novel H1N1 virus isolated from 2009 pandemic. Bioinformation 4: 94-97.
8. Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, et al. (2009) Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325: 197-201.
9. Smith GJ, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, et al. (2009) Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459: 1122-1125.
10. Pappaioanou M (2009) Highly pathogenic H5N1 avian influenza virus: cause of the next pandemic? Comp Immunol Microbiol Infect Dis 32: 287-300.
11. Palese P, Shaw ML (2007) Orthomyxoviridae: the viruses and their replication. In: Knipe DM, Howley PM, eds. Fields virology. 5 ed. Philadelphia: Lippincott Williams & Wilkins. pp 1647-1689.
12. Gabriel G, Herwig A, Klenk HD (2008) Interaction of polymerase subunit PB2 and NP with importin alpha1 is a determinant of host range of influenza A virus. PLoS Pathog 4: e11.
13. Resa-Infante P, Jorba N, Zamarreno N, Fernandez Y, Juarez S, et al. (2008) The host-dependent interaction of alpha-importins with influenza PB2 polymerase subunit is required for virus RNA replication. PLoS One 3: e3904.
14. 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.
15. 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.
16. Fodor E, Brownlee GG (2002) Influenza virus replication. In: Potter CW, ed. Influenza. New York: Elsevier. pp 1-29.
17. Yuan P, Bartlam M, Lou Z, Chen S, Zhou J, et al. (2009) Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 458: 909-913.
18. 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.
19. 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.
20. Kuzuhara T, Kise D, Yoshida H, Horita T, Murazaki Y, et al. (2009) Crystallization and X-ray diffraction analysis of the RNA primer/promoterbinding domain of influenza A virus RNA-dependent RNA polymerase PB2. Acta Crystallogr Sect F Struct Biol Cryst Commun 65: 144-146.
21. 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.
22. 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.
23. Bradel-Tretheway BG, Kelley Z, Chakraborty-Sett S, Takimoto T, Kim B, et al. (2008) The human H5N1 influenza A virus polymerase complex is active in vitro over a broad range of temperatures, in contrast to the WSN complex, and this property can be attributed to the PB2 subunit. J Gen Virol 89: 2923-2932.
24. Cox NJ, Kitame F, Kendal AP, Maassab HF, Naeve C (1988) Identification of sequence changes in the cold-adapted, live attenuated influenza vaccine strain, A/Ann Arbor/6/60 (H2N2). Virology 167: 554-567.
25. 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.
26. Odagiri T, Tosaka A, Ishida N, Maassab HF (1986) Biological characteristics of a cold-adapted influenza A virus mutation residing on a polymerase gene. Arch Virol 88: 91-104.
27. Kiseleva IV, Voeten JT, Teley LC, Larionova NV, Drieszen-van der Cruijsen SK, et al. (2010) PB2 and PA genes control the expression of the temperature-sensitive phenotype of cold-adapted B/USSR/60/69 influenza master donor virus. J Gen Virol 91: 931-937.
28. Dias A, Bouvier D, Crepin T, McCarthy AA, Hart DJ, et al. (2009) The capsnatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458: 914-918.
29. 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. Journal of Virology 76: 8989-9001.
30. 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. Journal of Virology 80: 7789-7798.
31. Kashiwagi T, Leung BW, Deng T, Chen H, Brownlee GG (2009) The Nterminal region of the PA subunit of the RNA polymerase of influenza A/ HongKong/156/97 (H5N1) influences promoter binding. PLoS One 4: e5473.
32. 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.
33. 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.
34. 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.
35. Sanz-Ezquerro JJ, Zurcher T, de la Luna S, Ortin J, Nieto A (1996) The aminoterminal one-third of the influenza virus PA protein is responsible for the induction of proteolysis. J Virol 70: 1905-1911.
36. Song MS, Pascua PN, Lee JH, Baek YH, Lee OJ, et al. (2009) The polymerase acidic protein gene of influenza a virus contributes to pathogenicity in a mouse model. J Virol 83: 12325-12335.
37. Dalton RM, Mullin AE, Amorim MJ, Medcalf E, Tiley LS, et al. (2006) Temperature sensitive influenza A virus genome replication results from low thermal stability of polymerase-cRNA complexes. Virol J 3: 58.
38. 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. Journal of Virology 79: 8669-8674.
39. Leung BW, Chen H, Brownlee GG (2010) Correlation between polymerase activity and pathogenicity in two duck H5N1 influenza viruses suggests that the polymerase contributes to pathogenicity. Virology 401: 96-106.
40. Toyoda T, Adyshev DM, Kobayashi M, Iwata A, Ishihama A (1996) Molecular assembly of the influenza virus RNA polymerase: determination of the subunitsubunit contact sites. J Gen Virol 77(Pt 9): 2149-2157.
41. Deng T, Sharps JL, Brownlee GG (2006) Role of the influenza virus heterotrimeric RNA polymerase complex in the initiation of replication. Journal of General Virology 87: 3373-3377.
42. 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. Journal of Virology 80: 2337-2348.
43. Chase G, Deng T, Fodor E, Leung BW, Mayer D, et al. (2008) Hsp90 inhibitors reduce influenza virus replication in cell culture. Virology 377: 431-439.
44. Momose F, Naito T, Yano K, Sugimoto S, Morikawa Y, et al. (2002) Identification of Hsp90 as a stimulatory host factor involved in influenza virus RNA synthesis. J Biol Chem 277: 45306-45314.
45. Naito T, Momose F, Kawaguchi A, Nagata K (2007) Involvement of Hsp90 in assembly and nuclear import of influenza virus RNA polymerase subunits. J Virol 81: 1339-1349.
46. Hirayama E, Atagi H, Hiraki A, Kim J (2004) Heat shock protein 70 is related to thermal inhibition of nuclear export of the influenza virus ribonucleoprotein complex. J Virol 78: 1263-1270.
47. Mehle A, Doudna JA (2009) Adaptive strategies of the influenza virus polymerase for replication in humans. Proc Natl Acad Sci U S A 106: 21312-21316.
48. Dubois MF, Bellier S, Seo SJ, Bensaude O (1994) Phosphorylation of the RNA polymerase II largest subunit during heat shock and inhibition of transcription in HeLa cells. J Cell Physiol 158: 417-426.
49. Engelhardt OG, Smith M, Fodor E (2005) Association of the influenza A virus RNA-dependent RNA polymerase with cellular RNA polymerase II. J Virol 79: 5812-5818.
50. 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.
51. Perez-Gonzalez A, Rodriguez A, Huarte M, Salanueva IJ, Nieto A (2006) hCLE/CGI-99, a human protein that interacts with the influenza virus polymerase, is a mRNA transcription modulator. J Mol Biol 362: 887-900.