Host restriction of influenza virus polymerase activity by PB2 627E is diminished on short viral templates in a nucleoprotein-independent manner

Journal of Virology

Volumn 88, Issue 1, 2014, Pages 339-344

  Paterson, Duncan ^a   te Velthuis, Aartjan J W ^a   Vreede, Frank T ^a   Fodor, Ervin ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOPROTEIN; RNA POLYMERASE; VIRUS RNA;

ANIMAL CELL; ARTICLE; AVIAN INFLUENZA VIRUS; CONTROLLED STUDY; ENZYME ACTIVITY; GENE MUTATION; HUMAN; HUMAN CELL; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; VIRAL GENETICS;

BASE SEQUENCE; DNA PRIMERS; DNA-DIRECTED RNA POLYMERASES; HEK293 CELLS; HUMANS; INFLUENZA A VIRUS; POLYMERASE CHAIN REACTION; RIBONUCLEOPROTEINS; TEMPLATES, GENETIC;

EID: 84890879650     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02022-13     Document Type: Article

References (35)

1. Sorrell E, Schrauwen E, Linster M, De Graaf M, Herfst S, Fouchier R. 2011. Predicting "airborne" influenza viruses: (trans-) mission impossible? Curr. Opin. Virol. 1:635-642. http://dx.doi.org/10.1016/j.coviro .2011.07.003.
2. Flick R, Neumann G, Hoffmann E, Neumeier E, Hobom G. 1996. Promoter elements in the influenza vRNA terminal structure. RNA 2:1046-1057.
3. Fodor E, Pritlove DC, Brownlee GG. 1994. The influenza virus panhandle is involved in the initiation of transcription. J. Virol. 68:4092-4096.
4. Fodor E. 2013. The RNA polymerase of influenza A virus: mechanisms of viral transcription and replication. Acta Virol. 57:113-122. http://dx.doi .org/10.4149/av_2013_02_113.
5. Krug R, Fodor E. 2013. The virus genome and its replication, p 57-66. In Webster RG, Monto AS, Braciale TJ, Lamb RA (ed), Textbook of influenza, 2nd ed. John Wiley & Sons, Ltd., New York, NY.
6. Resa-Infante P, Jorba N, Coloma R, Ortin J. 2011. The influenza virus RNA synthesis machine: advances in its structure and function. RNA Biol. 8:207-215. http://dx.doi.org/10.4161/rna.8.2.14513.
7. 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.
8. Chen G-W, Chang S-C, Mok C-K, Lo Y-L, Kung Y-N, Huang J-H, Shih Y-H, Wang J-Y, Chiang C, Chen C-J, Shih S-R. 2006. Genomic signatures of human versus avian influenza A viruses. Emerg. Infect. Dis. 12: 1353-1360. http://dx.doi.org/10.3201/eid1209.060276.
9. 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. http://dx.doi.org/10.1073/pnas.0911915106.
10. 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. http://dx.doi.org/10.1126/science.1062882.
11. Salomon R, Franks J, Govorkova EA, Ilyushina NA, Yen H-L, Hulse-Post DJ, Humberd J, Trichet M, Rehg JE, Webby RJ, Webster RG, Hoffmann E. 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. http://dx.doi.org/10.1084/jem.20051938.
12. Steel J, Lowen AC, 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. http://dx.doi.org/10.1371/journal .ppat.1000252.
13. Herfst S, Schrauwen EJA, Linster M, Chutinimitkul S, de Wit E, Munster VJ, Sorrell EM, Bestebroer TM, Burke DF, Smith DJ, Rimmelzwaan GF, Osterhaus ADME, Fouchier RAM. 2012. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336:1534-1541. http://dx.doi.org/10.1126/science.1213362.
14. Fouchier RAM, Schneeberger PM, Rozendaal FW, Broekman JM, Kemink SAG, Munster V, Kuiken T, Rimmelzwaan GF, Schutten M, van Doornum GJJ, Koch G, Bosman A, Koopmans M, Osterhaus ADME. 2004. 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. 101:1356-1361. http://dx.doi.org/10.1073/pnas .0308352100.
15. Gao P, Watanabe S, Ito T, Goto H, Wells K, McGregor M, Cooley AJ, Kawaoka Y. 1999. Biological heterogeneity, including systemic replication in mice, of H5N1 influenza A virus isolates from humans in Hong Kong. J. Virol. 73:3184-3189.
16. Kageyama T, Fujisaki S, Takashita E, Xu H, Yamada S, Uchida Y, Neumann G, Saito T, Kawaoka Y, Tashiro M. 2013. Genetic analysis of novel avian A(H7N9) influenza viruses isolated from patients in China, February to April 2013. Euro Surveill. 18(15):pii=20453. http://www .eurosurveillance.org/ViewArticle.aspx?ArticleId=20453.
17. Mehle A, Doudna JA. 2008. An inhibitory activity in human cells restricts the function of an avian-like influenza virus polymerase. Cell Host Microbe 4:111-122. http://dx.doi.org/10.1016/j.chom.2008.06.007.
18. Moncorgé O, Mura M, Barclay WS. 2010. Evidence for avian and human host cell factors that affect the activity of influenza virus polymerase. J. Virol. 84:9978-9986. http://dx.doi.org/10.1128/JVI.01134-10.
19. Labadie K, Dos Santos Afonso E, Rameix-Welti M-A, 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. http://dx.doi.org/10 .1016/j.virol.2006.12.027.
20. Ng AK-L, Chan W-H, Choi S-T, Lam MK-H, Lau K-F, Chan PK-S, Au SW-N, Fodor E, Shaw P-C. 2012. Influenza polymerase activity correlates with the strength of interaction between nucleoprotein and PB2 through the host-specific residue K/E627. PLoS One 7:e36415. http://dx.doi.org/10 .1371/journal.pone.0036415.
21. Rameix-Welti M-A, Tomoiu A, Afonso EDS, van der Werf S, Naffakh N. 2009. Avian influenza A virus polymerase association with nucleoprotein, but not polymerase assembly, is impaired in human cells during the course of infection. J. Virol. 83:1320-1331. http://dx.doi.org/10.1128/JVI .00977-08.
22. Turrell L, Lyall JW, Tiley LS, Fodor E, Vreede FT. 2013. The role and assembly mechanism of nucleoprotein in influenza A virus ribonucleoprotein complexes. Nat. Commun. 4:1591. http://dx.doi.org/10.1038 /ncomms2589.
23. Fodor E, Crow M, Mingay LJ, Deng T, Sharps J, Fechter P, Brownlee GG. 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. http://dx.doi.org/10.1128/JVI.76.18.8989-9001 .2002.
24. 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. http://dx.doi.org/10.1128/JVI.79.21.13811-13816.2005.
25. Robb NC, Smith M, Vreede FT, Fodor E. 2009. NS2/NEP protein regulates transcription and replication of the influenza virus RNA genome. J. Gen. Virol. 90:1398-1407. http://dx.doi.org/10.1099/vir.0 .009639-0.
26. 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. http://dx.doi.org/10.1128/JVI.79.13.8669-8674.2005.
27. 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. http://dx.doi.org/10.1128/JVI.00600-06.
28. 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. http://dx.doi.org/10.1128/JVI.75.11.5398 -5404.2001.
29. Aggarwal S, Dewhurst S, Takimoto T, Kim B. 2011. Biochemical impact of the host adaptation-associated PB2 E627K mutation on the temperature-dependent RNA synthesis kinetics of influenza A virus polymerase complex. J. Biol. Chem. 286:34504-34513. http://dx.doi.org/10.1074/jbc .M111.262048.
30. Resa-Infante P, Recuero-Checa MÁ, Zamarreño N, Llorca ó, Ortín J. 2010. Structural and functional characterization of an influenza virus RNA polymerase-genomic RNA complex. J. Virol. 84:10477-10487. http: //dx.doi.org/10.1128/JVI.01115-10.
31. Cauldwell AV, Moncorgé O, Barclay WS. 2013. Unstable polymerase-NP interaction is not responsible for avian influenza polymerase re-striction in human cells. J. Virol. 87:1278-1284. http://dx.doi.org/10.1128 /JVI.02597-12.
32. Crescenzo-Chaigne B, van der Werf S, Naffakh N. 2002. Differential effect of nucleotide substitutions in the 3= arm of the influenza A virus vRNA promoter on transcription/replication by avian and human polymerase complexes is related to the nature of PB2 amino acid 627. Virology 303:240-252. http://dx.doi.org/10.1006/viro.2002.1637.
33. Kuzuhara T, Kise D, Yoshida H, Horita T, Murazaki Y, Nishimura A, Echigo N, Utsunomiya H, Tsuge H. 2009. Structural basis of the influenza A virus RNA polymerase PB2 RNA-binding domain containing the pathogenicity-determinant lysine 627 residue. J. Biol. Chem. 284:6855-6860. http://dx.doi.org/10.1074/jbc.C800224200.
34. Fodor E, Seong BL, Brownlee GG. 1993. 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. 74:1327-1333. http://dx.doi.org/10.1099/0022-1317-74-7-1327.
35. Pritlove DC, Fodor E, Seong BL, Brownlee GG. 1995. In vitro transcription and polymerase binding studies of the termini of influenza A virus cRNA: evidence for a cRNA panhandle. J. Gen. Virol. 76:2205-2213. http: //dx.doi.org/10.1099/0022-1317-76-9-2205.