Initiation, elongation, and realignment during influenza virus mRNA synthesis

Journal of Virology

Volumn 92, Issue 3, 2018, Pages

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

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Influenza A virus; Priming loop; Realignment; Replication; RNA dependent RNA polymerase; Transcription; Viral transcription

Indexed keywords

MESSENGER RNA; SINGLE STRANDED RNA; VIRUS RNA; RNA DIRECTED RNA POLYMERASE; VIRAL PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BASE PAIRING; CONTROLLED STUDY; DNA TEMPLATE; IN VITRO STUDY; INFLUENZA A VIRUS; MESSENGER RNA SYNTHESIS; MOLECULAR WEIGHT; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RNA 3' END PROCESSING; SANGER SEQUENCING; SEGMENTAL DUPLICATION; SEQUENCE ALIGNMENT; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; VIRUS REPLICATION; VIRUS TRANSCRIPTION; WILD TYPE; ANIMAL; CHEMISTRY; GENETIC TRANSCRIPTION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; PHYSIOLOGY; SF9 CELL LINE;

ANIMALS; HEK293 CELLS; HUMANS; INFLUENZA A VIRUS; RNA REPLICASE; RNA, MESSENGER; RNA, VIRAL; SF9 CELLS; TRANSCRIPTION, GENETIC; VIRAL PROTEINS;

EID: 85040676791     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01775-17     Document Type: Article

References (30)

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. 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
4. 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
5. 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
6. 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
7. Oymans J, te Velthuis AJW. 2018. A mechanism for priming and realignment during influenza A virus replication. J Virol 92:e01773-17. https://doi.org/10.1128/JVI.01773-17
8. Lukarska M, Fournier G, Pflug A, Resa-Infante P, Reich S, Naffakh N, Cusack S. 2017. Structural basis of an essential interaction between influenza polymerase, Pol II CTD. 2016. Nature 541:117-121. https://doi .org/10.1038/nature20594
9. Martínez-Alonso M, Hengrung N, Fodor E. 2016. RNA-free and ribonucleoprotein-associated influenza virus polymerases directly bind the serine-5-phosphorylated carboxyl-terminal domain of host polymerase RNA II. J Virol 90:6014-6021. https://doi.org/10.1128/JVI.00494-16
10. Chung TD, Cianci C, Hagen M, Terry B, Matthews JT, Krystal M, Colonno RJ. 1994. Biochemical studies on capped RNA primers identify a class of oligonucleotide inhibitors of the influenza virus RNA polymerase. Proc Natl Acad Sci U S A 91:2372-2376. https://doi.org/10.1073/pnas.91.6 .2372
11. Datta K, Wolkerstorfer A, Szolar OH, Cusack S, Klumpp K. 2013. Characterization of PA-N terminal domain of influenza A polymerase reveals sequence specific RNA cleavage. Nucleic Acids Res 41:8289-8299. https://doi.org/10.1093/nar/gkt603
12. Hagen M, Tiley L, Chung TD, Krystal M. 1995. The role of template-primer interactions in cleavage and initiation by the influenza virus polymerase. J Gen Virol 76(Part 3):603-611
13. 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
14. Geerts-Dimitriadou C, Goldbach R, Kormelink R. 2011. Preferential use of RNA leader sequences during influenza A transcription initiation in vivo. Virology 409:27-32. https://doi.org/10.1016/j.virol.2010.09.006
15. Koppstein D, Ashour J, Bartel DP. 2015. Sequencing the cap-snatching repertoire of H1N1 influenza provides insight into the mechanism of viral transcription initiation. Nucleic Acids Res 43:5052-5064. https://doi .org/10.1093/nar/gkv333
16. Krug RM, Broni BA, LaFiandra AJ, Morgan MA, Shatkin AJ. 1980. Priming and inhibitory activities of RNAs for the influenza viral transcriptase do not require base pairing with the virion template, RNA. Proc Natl Acad Sci U S A 77:5874-5878. https://doi.org/10.1073/pnas.77.10.5874
17. Sikora D, Rocheleau L, Brown EG, Pelchat M. 2014. Deep sequencing reveals the eight facets of the influenza A/HongKong/1/1968 (H3N2) virus cap-snatching process. Sci Rep 4:6181. https://doi.org/10.1038/ srep06181
18. Geerts-Dimitriadou C, Zwart MP, Goldbach R, Kormelink R. 2011. Basepairing promotes leader selection to prime in vitro influenza genome transcription. Virology 409:17-26. https://doi.org/10.1016/j.virol.2010.09 .003
19. te Velthuis AJW, Oymans J. 2017. Initiation, elongation and realignment during influenza virus mRNA synthesis. bioRxiv https://doi.org/10.1101/ 197210
20. 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
21. 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
22. Kerry PS, Willsher N, Fodor E. 2008. A cluster of conserved basic amino acids near the C-terminus of the PB1 subunit of the influenza virus RNA polymerase is involved in the regulation of viral transcription. Virology 373:202-210. https://doi.org/10.1016/j.virol.2007.11.030
23. Lee MT, Bishop K, Medcalf L, Elton D, Digard P, Tiley L. 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. https://doi.org/10.1093/nar/30.2.429
24. te Velthuis AJ. 2014. Common and unique features of viral RNAdependent polymerases. Cell Mol Life Sci 71:4403-4420. https://doi.org/ 10.1007/s00018-014-1695-z
25. Lee M-K, Bae S-H, Park C-J, Cheong H-K, Cheong C, Choi B-S. 2003. A single-nucleotide natural variation (U4 to C4) in an influenza A virus promoter exhibits a large structural change: implications for differential viral RNA synthesis by RNA-dependent RNA polymerase. Nucleic Acids Res 31:1216-1223. https://doi.org/10.1093/nar/gkg214
26. 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
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. https://doi.org/10.1128/JVI.00600-06
28. 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
29. 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
30. 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