An in vitro RNA synthesis assay for rabies virus defines ribonucleoprotein interactions critical for polymerase activity

Journal of Virology

Volumn 91, Issue 1, 2017, Pages

  Morin, Benjamin ^a,c   Liang, Bo ^a   Gardner, Erica ^a   Ross, Robin A ^a,b   Whelan, Sean P J ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c Antigenics Inc   (United States)

Author keywords

In vitro; Phosphoprotein; Polymerase; Rabies; Ribavirin

Indexed keywords

RIBONUCLEOPROTEIN; RNA DIRECTED RNA POLYMERASE; DNA DIRECTED RNA POLYMERASE; L PROTEIN, RABIES VIRUS; NUCLEOCAPSID PROTEIN; NUCLEOTIDE; P PHOSPHOPROTEIN, RABIES VIRUS; PHOSPHOPROTEIN; RECOMBINANT PROTEIN; RIBAVIRIN 5'-TRIPHOSPHATE; VIRAL PROTEIN; VIRUS RNA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; IN VITRO STUDY; LIMIT OF QUANTITATION; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RABIES VIRUS; RNA SYNTHESIS; VESICULOVIRUS; VIRUS REPLICATION; BACULOVIRIDAE; BIOASSAY; ESCHERICHIA COLI; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROMOTER REGION; RHABDOVIRIDAE;

BACULOVIRIDAE; BIOLOGICAL ASSAY; DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI; GENE EXPRESSION; GENE EXPRESSION REGULATION, VIRAL; NUCLEOCAPSID PROTEINS; NUCLEOTIDES; PHOSPHOPROTEINS; PROMOTER REGIONS, GENETIC; RABIES VIRUS; RECOMBINANT PROTEINS; RHABDOVIRIDAE; RIBONUCLEOPROTEINS; RNA REPLICASE; RNA, VIRAL; VESICULOVIRUS; VIRAL PROTEINS; VIRAL STRUCTURAL PROTEINS;

EID: 85008219763     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01508-16     Document Type: Article

References (38)

1. Knobel DL, Cleaveland S, Coleman PG, Fevre EM, Meltzer MI, Miranda ME, Shaw A, Zinsstag J, Meslin FX. 2005. Re-evaluating the burden of rabies in Africa and Asia. Bull World Health Organ 83:360-368.
2. WHO. 2014. Rabies. World Health Organization, Geneva, Switzerland. http://www.who.int/rabies/en/. Accessed 14 August 2014.
3. Albertini AA, Wernimont AK, Muziol T, Ravelli RB, Clapier CR, Schoehn G, Weissenhorn W, Ruigrok RW. 2006. Crystal structure of the rabies virus nucleoprotein-RNA complex. Science 313:360-363. https://doi.org/10.1126/science.1125280.
4. Green TJ, Zhang X, Wertz GW, Luo M. 2006. Structure of the vesicular stomatitis virus nucleoprotein-RNA complex. Science 313:357-360. https://doi.org/10.1126/science.1126953.
5. Morin B, Kranzusch PJ, Rahmeh AA, Whelan SP. 2013. The polymerase of negative-stranded RNA viruses. Curr Opin Virol 3:103-110. https://doi.org/10.1016/j.coviro.2013.03.008.
6. Ruigrok RW, Crepin T, Kolakofsky D. 2011. Nucleoproteins and nucleocapsids of negative-strand RNA viruses. Curr Opin Microbiol 14:504-510. https://doi.org/10.1016/j.mib.2011.07.011.
7. Tawar RG, Duquerroy S, Vonrhein C, Varela PF, Damier-Piolle L, Castagne N, MacLellan K, Bedouelle H, Bricogne G, Bhella D, Eleouet JF, Rey FA. 2009 Crystal structure of a nucleocapsid-like nucleoprotein-RNA complex of respiratory syncytial virus. Science 326:1279-1283. https://doi.org/10.1126/science.1177634.
8. Li J, Fontaine-Rodriguez EC, Whelan SP. 2005. Amino acid residues within conserved domain VI of the vesicular stomatitis virus large polymerase protein essential for mRNA cap methyltransferase activity. J Virol 79:13373-13384. https://doi.org/10.1128/JVI.79.21.13373-13384.2005.
9. Li J, Rahmeh A, Morelli M, Whelan SP. 2008. A conserved motif in region V of the large polymerase proteins of nonsegmented negative-sense RNA viruses that is essential for mRNA capping. J Virol 82:775-784. https://doi.org/10.1128/JVI.02107-07.
10. Li J, Wang JT, Whelan SP. 2006. A unique strategy for mRNA cap methylation used by vesicular stomatitis virus. Proc Natl Acad Sci U S A 103:8493-8498. https://doi.org/10.1073/pnas.0509821103.
11. Ogino M, Ito N, Sugiyama M, Ogino T. 2016. The rabies virus L protein catalyzes mRNA capping with GDP polyribonucleotidyltransferase activity. Viruses 8:E144. https://doi.org/10.3390/v8050144.
12. Ogino T, Banerjee AK. 2007. Unconventional mechanism of mRNA capping by the RNA-dependent RNA polymerase of vesicular stomatitis virus. Mol Cell 25:85-97. https://doi.org/10.1016/j.molcel.2006.11.013.
13. Sleat DE, Banerjee AK. 1993. Transcriptional activity and mutational analysis of recombinant vesicular stomatitis virus RNA polymerase. J Virol 67:1334-1339.
14. Liang B, Li Z, Jenni S, Rahmeh AA, Morin BM, Grant T, Grigorieff N, Harrison SC, Whelan SP. 2015. Structure of the L protein of vesicular stomatitis virus from electron cryomicroscopy. Cell 162:314-327. https://doi.org/10.1016/j.cell.2015.06.018.
15. Rahmeh AA, Schenk AD, Danek EI, Kranzusch PJ, Liang B, Walz T, Whelan SP. 2010. Molecular architecture of the vesicular stomatitis virus RNA polymerase. Proc Natl Acad Sci U S A 107:20075-20080. https://doi.org/10.1073/pnas.1013559107.
16. Morin B, Rahmeh AA, Whelan SP. 2012. Mechanism of RNA synthesis initiation by the vesicular stomatitis virus polymerase. EMBO J 31: 1320-1329. https://doi.org/10.1038/emboj.2011.483.
17. Green TJ, Luo M. 2009. Structure of the vesicular stomatitis virus nucleocapsid in complex with the nucleocapsid-binding domain of the small polymerase cofactor, P. Proc Natl Acad Sci U S A 106:11713-11718. https://doi.org/10.1073/pnas.0903228106.
18. Ivanov I, Crepin T, Jamin M, Ruigrok RW. 2010. Structure of the dimerization domain of the rabies virus phosphoprotein. J Virol 84:3707-3710. https://doi.org/10.1128/JVI.02557-09.
19. Leyrat C, Yabukarski F, Tarbouriech N, Ribeiro EA, Jr, Jensen MR, Blackledge M, Ruigrok RW, Jamin M. 2011. Structure of the vesicular stomatitis virus N(0)-P complex. PLoS Pathog 7:e1002248. https://doi.org/10.1371/journal.ppat.1002248.
20. Chenik M, Chebli K, Gaudin Y, Blondel D. 1994. In vivo interaction of rabies virus phosphoprotein (P) and nucleoprotein (N): existence of two N-binding sites on P protein. J Gen Virol 75:2889-2896. https://doi.org/10.1099/0022-1317-75-11-2889.
21. Chenik M, Schnell M, Conzelmann KK, Blondel D. 1998. Mapping the interacting domains between the rabies virus polymerase and phosphoprotein. J Virol 72:1925-1930.
22. Fu ZF, Zheng Y, Wunner WH, Koprowski H, Dietzschold B. 1994. Both the N-and the C-terminal domains of the nominal phosphoprotein of rabies virus are involved in binding to the nucleoprotein. Virology 200: 590-597. https://doi.org/10.1006/viro.1994.1222.
23. Gerard FC, Ribeiro Ede A, Jr, Leyrat C, Ivanov I, Blondel D, Longhi S, Ruigrok RW, Jamin M. 2009. Modular organization of rabies virus phosphoprotein. J Mol Biol 388:978-996. https://doi.org/10.1016/j.jmb.2009.03.061.
24. Liu P, Yang J, Wu X, Fu ZF. 2004. Interactions amongst rabies virus nucleoprotein, phosphoprotein and genomic RNA in virus-infected and transfected cells. J Gen Virol 85:3725-3734. https://doi.org/10.1099/vir.0.80325-0.
25. Mavrakis M, Iseni F, Mazza C, Schoehn G, Ebel C, Gentzel M, Franz T, Ruigrok RW. 2003. Isolation and characterisation of the rabies virus N degrees-P complex produced in insect cells. Virology 305:406-414. https://doi.org/10.1006/viro.2002.1748.
26. Mavrakis M, McCarthy AA, Roche S, Blondel D, Ruigrok RW. 2004. Structure and function of the C-terminal domain of the polymerase cofactor of rabies virus. J Mol Biol 343:819-831. https://doi.org/10.1016/j.jmb.2004.08.071.
27. Mavrakis M, Mehouas S, Real E, Iseni F, Blondel D, Tordo N, Ruigrok RW. 2006 Rabies virus chaperone: identification of the phosphoprotein peptide that keeps nucleoprotein soluble and free from non-specific RNA. Virology 349:422-429. https://doi.org/10.1016/j.virol.2006.01.030.
28. Baltimore D, Huang AS, Stampfer M. 1970. Ribonucleic acid synthesis of vesicular stomatitis virus. II. An RNA polymerase in the virion. Proc Natl Acad Sci U S A 66:572-576. https://doi.org/10.1073/pnas.66.2.572.
29. Emerson SU, Wagner RR. 1973. L protein requirement for in vitro RNA synthesis by vesicular stomatitis virus. J Virol 12:1325-1335.
30. Rahmeh AA, Morin B, Schenk AD, Liang B, Heinrich BS, Brusic V, Walz T, Whelan SP. 2012. Critical phosphoprotein elements that regulate polymerase architecture and function in vesicular stomatitis virus. Proc Natl Acad Sci U S A 109:14628-14633. https://doi.org/10.1073/pnas.1209147109.
31. Morin B, Whelan SP. 2014. Sensitivity of the polymerase of vesicular stomatitis virus to 2' substitutions in the template and nucleotide triphosphate during initiation and elongation. J Biol Chem 289: 9961-9969. https://doi.org/10.1074/jbc.M113.542761.
32. Deval J, Hong J, Wang G, Taylor J, Smith LK, Fung A, Stevens SK, Liu H, Jin Z, Dyatkina N, Prhavc M, Stoycheva AD, Serebryany V, Liu J, Smith DB, Tam Y, Zhang Q, Moore ML, Fearns R, Chanda SM, Blatt LM, Symons JA, Beigelman L. 2015. Molecular basis for the selective inhibition of respiratory syncytial virus RNA polymerase by 2'-fluoro-4'-chloromethylcytidine triphosphate. PLoS Pathog 11:e1004995. https://doi.org/10.1371/journal.ppat.1004995.
33. Crotty S, Cameron CE, Andino R. 2001. RNA virus error catastrophe: direct molecular test by using ribavirin. Proc Natl Acad Sci U S A 98:6895-6900. https://doi.org/10.1073/pnas.111085598.
34. Graci JD, Cameron CE. 2006. Mechanisms of action of ribavirin against distinct viruses. Rev Med Virol 16:37-48. https://doi.org/10.1002/rmv.483.
35. Noton SL, Deflube LR, Tremaglio CZ, Fearns R. 2012. The respiratory syncytial virus polymerase has multiple RNA synthesis activities at the promoter. PLoS Pathog 8:e1002980. https://doi.org/10.1371/journal.ppat.1002980.
36. Canter DM, Perrault J. 1996. Stabilization of vesicular stomatitis virus L polymerase protein by P protein binding: a small deletion in the C-terminal domain of L abrogates binding. Virology 219:376-386. https://doi.org/10.1006/viro.1996.0263.
37. Warrell MJ, White NJ, Looareesuwan S, Phillips RE, Suntharasamai P, Chanthavanich P, Riganti M, Fisher-Hoch SP, Nicholson KG, Manatsathit S, Vannaphan S, Warrell DA. 1989. Failure of interferon alfa and tribavirin in rabies encephalitis. BMJ 299:830-833. https://doi.org/10.1136/bmj.299.6703.830.
38. Kuraku S, Zmasek CM, Nishimura O, Katoh K. 2013. aLeaves facilitates on-demand exploration of metazoan gene family trees on MAFFT sequence alignment server with enhanced interactivity. Nucleic Acids Res 41:W22-W28. https://doi.org/10.1093/nar/gkt389.