A mechanism for priming and realignment during influenza A virus replication

Journal of Virology

Volumn 92, Issue 3, 2018, Pages

  Oymans, Judith ^a,c   te Velthuis, Aartjan J W ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

ApG; Influenza A virus; Priming loop; Realignment; RNA dependent RNA polymerase; Viral replication

Indexed keywords

HELIX LOOP HELIX PROTEIN; RNA DEPENDENT RNA POLYMERASE PB1 SUBUNIT; RNA DIRECTED RNA POLYMERASE; UNCLASSIFIED DRUG; VIRUS RNA; DNA DIRECTED RNA POLYMERASE; VIRAL PROTEIN;

ARTICLE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INFLUENZA A VIRUS; INTERNAL ELONGATION; NONHUMAN; PRIMING LOOP; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RNA SYNTHESIS; VIRAL PHENOMENA AND FUNCTIONS; VIRUS GENOME; VIRUS PRIMING; VIRUS REALIGNMENT; VIRUS REPLICATION; VIRUS TRANSCRIPTION; GENETIC TRANSCRIPTION; GENETICS; HEK293 CELL LINE; METABOLISM; PHYSIOLOGY;

DNA-DIRECTED RNA POLYMERASES; GENOME, VIRAL; HEK293 CELLS; HUMANS; INFLUENZA A VIRUS; PROMOTER REGIONS, GENETIC; RNA REPLICASE; RNA, VIRAL; TRANSCRIPTION, GENETIC; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 85040683970     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01773-17     Document Type: Article

References (40)

1. te Velthuis AJ, Fodor E. 2016. Influenza virus RNA polymerase: insights into the mechanisms of viral RNA synthesis. Nat Rev Microbiol 18: 479-493. https://doi.org/10.1038/nrmicro.2016.87
2. Fodor E. 2013. The RNA polymerase of influenza A virus: mechanisms of viral transcription and replication. Acta Virol 57:113-122. https://doi.org/ 10.4149/av_2013_02_113
3. York A, Hengrung N, Vreede FT, Huiskonen JT, Fodor E. 2013. Isolation and characterization of the positive-sense replicative intermediate of a negative-strand RNA virus. Proc Natl Acad Sci U S A 110:E4238-E4245. https://doi.org/10.1073/pnas.1315068110
4. Pflug A, Lukarska M, Resa-Infante P, Reich S, Cusack S. 2017. Structural insights into RNA synthesis by the influenza virus transcriptionreplication machine. Virus Res 234:103-117. https://doi.org/10.1016/j .virusres.2017.01.013
5. Reich S, Guilligay D, Pflug A, Malet H, Berger I, Crépin T, Hart D, Lunardi T, Nanao M, Ruigrok RW, Cusack S. 2014. Structural insight into capsnatching and RNA synthesis by influenza polymerase. Nature 516: 361-366. https://doi.org/10.1038/nature14009
6. Pflug A, Guilligay D, Reich S, Cusack S. 2014. Structure of influenza A polymerase bound to the viral RNA promoter. Nature 516:355-360. https://doi.org/10.1038/nature14008
7. Hengrung N, El Omari K, Serna Martin I, Vreede FT, Cusack S, Rambo RP, Vonrhein C, Bricogne G, Stuart DI, Grimes JM, Fodor E. 2015. Crystal structure of the RNA-dependent RNA polymerase from influenza C virus. Nature 527:114-117. https://doi.org/10.1038/nature15525
8. Parvin JD, Palese P, Honda A, Ishihama A, Krystal M. 1989. Promoter analysis of influenza virus RNA polymerase. J Virol 63:5142-5152
9. 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. https://doi .org/10.1099/0022-1317-76-9-2205
10. Fodor E, Pritlove DC, Brownlee GG. 1994. The influenza virus panhandle is involved in the initiation of transcription. J Virol 68:4092-4096
11. Thierry E, Guilligay D, Kosinski J, Bock T, Gaudon S, Round A, Pflug A, Hengrung N, El Omari K, Baudin F, Hart DJ, Beck M, Cusack S. 2016. Influenza polymerase can adopt an alternative configuration involving a radical repacking of PB2 domains. Mol Cell 61:125-137. https://doi.org/ 10.1016/j.molcel.2015.11.016
12. Robb NC, te Velthuis AJ, Wieneke R, Tampé R, Cordes T, Fodor E, Kapanidis AN. 2016. Single-molecule FRET reveals the pre-initiation and initiation conformations of influenza virus promoter, RNA. Nucleic Acids Res 44:10304-10315
13. te Velthuis A, Robb NC, Kapanidis AF, Fodor F. 2016. The role of the priming loop in influenza A virus RNA synthesis. Nat Microbiol 1:16029. https://doi.org/10.1038/nmicrobiol.2016.29
14. 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. https://doi.org/10.1128/JVI.80.5.2337-2348.2006
15. Martin A, Hoefs N, Tadewaldt J, Staeheli P, Schneider U. 2011. Genomic RNAs of Borna disease virus are elongated on internal template motifs after realignment of the 3= termini. Proc Natl Acad Sci U S A 108: 7206-7211. https://doi.org/10.1073/pnas.1016759108
16. Garcin D, Lezzi M, Dobbs M, Elliott RM, Schmaljohn C, Kang CY, Kolakofsky D. 1995. The 5= ends of Hantaan virus (Bunyaviridae) RNAs suggest a prime-and-realign mechanism for the initiation of RNA synthesis. J Virol 69:5754-5762
17. Oymans J, te Velthuis A. 2017. A mechanism for prime-realignment during influenza A virus replication. bioRxiv https://doi.org/10.1101/ 138487
18. Reich S, Guilligay D, Cusack S. 2017. An in vitro fluorescence based study of initiation of RNA synthesis by influenza B polymerase. Nucleic Acids Res 45:3353-3368. https://doi.org/10.1093/nar/gkx043
19. Vreede FT, Brownlee GG. 2007. Influenza virion-derived viral ribonucleoproteins synthesize both mRNA and cRNA in vitro. J Virol 81:2196-2204. https://doi.org/10.1128/JVI.02187-06
20. Jung TE, Brownlee GG. 2006. A new promoter-binding site in the PB1 subunit of the influenza A virus polymerase. J Gen Virol 87:679-688. https://doi.org/10.1099/vir.0.81453-0
21. Du Y, Wu NC, Jiang L, Zhang T, Gong D, Shu S, Wu TT, Sun R. 2016. Annotating protein functional residues by coupling high-throughput fitness profile and homologous-structure analysis. mBio 7:e01801-16. https://doi.org/10.1128/mBio.01801-16
22. Laurila MR, Makeyev EV, Bamford DH. 2002. Bacteriophage phi 6 RNAdependent RNA polymerase: molecular details of initiating nucleic acid synthesis without primer. J Biol Chem 277:17117-17124. https://doi.org/ 10.1074/jbc.M111220200
23. Hong Z, Cameron CE, Walker MP, Castro C, Yao N, Lau JY, Zhong W. 2001. A novel mechanism to ensure terminal initiation by hepatitis C virus NS5B polymerase. Virology 285:6-11. https://doi.org/10.1006/viro.2001 .0948
24. Mosley RT, Edwards TE, Murakami E, Lam AM, Grice RL, Du J, Sofia MJ, Furman PA, Otto MJ. 2012. Structure of hepatitis C virus polymerase in complex with primer-template RNA. J Virol 86:6503-6511. https://doi .org/10.1128/JVI.00386-12
25. Tomescu AI, Robb NC, Hengrung N, Fodor E, Kapanidis AN. 2014. Singlemolecule FRET reveals a corkscrew RNA structure for the polymerasebound influenza virus promoter. Proc Natl Acad Sci U S A 111: E3335-E3342. https://doi.org/10.1073/pnas.1406056111
26. Appleby TC, Perry JK, Murakami E, Barauskas O, Feng J, Cho A, Fox D, Wetmore DR, McGrath ME, Ray AS, Sofia MJ, Swaminathan S, Edwards TE. 2015. Structural basis for RNA replication by the hepatitis C virus polymerase. Science 347:771-775. https://doi.org/10.1126/science.1259210
27. Tao Y, Farsetta DL, Nibert ML, Harrison SC. 2002. RNA synthesis in a cage-structural studies of reovirus polymerase lambda3. Cell 111: 733-745. https://doi.org/10.1016/S0092-8674(02)01110-8
28. Nilsson BE, Te Velthuis AJ, Fodor E. 2017. Role of the PB2 627 domain in influenza A virus polymerase function. J Virol 91:e02467-16. https://doi .org/10.1128/JVI.02467-16
29. van Knippenberg I, Lamine M, Goldbach R, Kormelink R. 2005. Tomato spotted wilt virus transcriptase in vitro displays a preference for cap donors with multiple base complementarity to the viral template. Virology 335:122-130. https://doi.org/10.1016/j.virol.2005.01.041
30. Bouloy M, Pardigon N, Vialat P, Gerbaud S, Girard M. 1990. Characterization of the 5= and 3= ends of viral messenger RNAs isolated from BHK21 cells infected with Germiston virus (Bunyavirus). Virology 175: 50-58. https://doi.org/10.1016/0042-6822(90)90185-T
31. Duijsings D, Kormelink R, Goldbach R. 2001. In vivo analysis of the TSWV cap-snatching mechanism: single base complementarity and primer length requirements. EMBO J 20:2545-2552. https://doi.org/10.1093/ emboj/20.10.2545
32. Vreede FT, Jung TE, Brownlee GG. 2004. Model suggesting that replication of influenza virus is regulated by stabilization of replicative intermediates. J Virol 78:9568-9572. https://doi.org/10.1128/JVI.78.17.9568-9572.2004
33. 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. https://doi.org/10.1128/JVI.76.18.8989-9001 .2002
34. 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. https://doi.org/10.1128/JVI.79.13.8669-8674.2005
35. 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. https://doi.org/10.1128/JVI.00600-06
36. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. https://doi.org/10.1093/bioinformatics/btm404
37. Robert X, Gouet P. 2014. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42:W320-W324. https://doi.org/10.1093/nar/gku316
38. Kapanidis AN, Lee NK, Laurence TA, Doose S, Margeat E, Weiss S. 2004. Fluorescence-aided molecule sorting: analysis of structure and interactions by alternating-laser excitation of single molecules. Proc Natl Acad Sci U S A 101:8936-8941. https://doi.org/10.1073/pnas.0401690101
39. Santoso Y, Hwang LC, Le Reste L, Kapanidis AN. 2008. Red light, green light: probing single molecules using alternating-laser excitation. Biochem Soc Trans 36:738-744. https://doi.org/10.1042/BST0360738
40. te Velthuis AJW, Oymans J. 2018. Initiation, elongation, and realignment during influenza virus mRNA synthesis. J Virol 92:e01775-17. https://doi .org/10.1128/JVI.01775-17