Sensitivity of the polymerase of vesicular stomatitis virus to 2′ substitutions in the template and nucleotide triphosphate during initiation and elongation

Journal of Biological Chemistry

Volumn 289, Issue 14, 2014, Pages 9961-9969

  Morin, Benjamin ^a   Whelan, Sean P J ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; ELONGATION; MACHINERY; NUCLEOTIDES; POLYMERS; PROTEINS; VIRUSES;

CATALYTIC SUBUNITS; NUCLEOCAPSID PROTEINS; NUCLEOTIDE TRIPHOSPHATES; PROMOTER SEQUENCES; RIBONUCLEOPROTEIN COMPLEX; RNA SYNTHESIS; RNA-DEPENDENT RNA POLYMERASE; VESICULAR STOMATITIS VIRUS;

RNA;

DEOXYGUANOSINE TRIPHOSPHATE; GENOMIC RNA; LARGE PROTEIN; NUCLEOCAPSID PROTEIN; NUCLEOSIDE TRIPHOSPHATE; PHOSPHOPROTEIN; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; DNA SEQUENCE; ENZYME ACTIVE SITE; ENZYME MODIFICATION; ENZYME STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PURIFICATION; RIBONUCLEIC ACID TEMPLATE; RNA STRUCTURE; RNA SYNTHESIS; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; VESICULAR STOMATITIS VIRUS;

ENZYME INHIBITORS; NEGATIVE-STRAND RNA VIRUSES; NUCLEOSIDE NUCLEOTIDE ANALOGS; RNA; RNA POLYMERASE;

ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; CYTARABINE; PROMOTER REGIONS, GENETIC; RNA REPLICASE; RNA, VIRAL; SF9 CELLS; SPODOPTERA; TRANSCRIPTION ELONGATION, GENETIC; TRANSCRIPTION INITIATION, GENETIC; VESICULOVIRUS; VIRAL PROTEINS; ZALCITABINE;

EID: 84898077396     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.542761     Document Type: Article

References (32)

1. Li, J., Fontaine-Rodriguez, E. C., and Whelan, S. P. (2005) Amino acid residues within conserved domainVIof the vesicular stomatitis virus large polymerase protein essential for mRNA cap methyltransferase activity. J. Virol. 79, 13373-13384
2. Li, J., Rahmeh, A., Morelli, M., and Whelan, S. P.(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
3. Li, J., Wang, J. T., and Whelan, S. P. (2006) A unique strategy for mRNA cap methylation used by vesicular stomatitis virus. Proc. Natl. Acad. Sci. U.S.A. 103, 8493-8498
4. Ogino, T., and Banerjee, A. K. (2007) Unconventional mechanism of mRNA capping by the RNA-dependent RNA polymerase of vesicular stomatitis virus. Mol. Cell 25, 85-97
5. Sleat, D. E., and Banerjee, A. K. (1993) Transcriptional activity and muta-tional analysis of recombinant vesicular stomatitis virus RNA polymerase. J. Virol. 67, 1334-1339
6. Rahmeh, A. A., Schenk, A.D., Danek, E.I., Kranzusch, P. J., Liang, B., Walz, T., and Whelan, S. P. (2010) Molecular architecture of the vesicular stomatitis virus RNA polymerase. Proc. Natl. Acad. Sci. U.S.A. 107, 20075-20080
7. Morin, B., Rahmeh, A. A., and Whelan, S. P. (2012) Mechanism of RNA synthesis initiation by the vesicular stomatitis virus polymerase. EMBO J. 31, 1320-1329
8. Rahmeh, A. A., Morin, B., Schenk, A. D., Liang, B., Heinrich, B. S., Brusic, V., Walz, T., and Whelan, S. P. (2012) Critical phosphoprotein elements that regulate polymerase architecture and function in vesicular stomatitis virus. Proc. Natl. Acad. Sci. U.S.A. 109, 14628-14633
9. Albertini, A. A., Wernimont, A. K., Muziol, T., Ravelli, R. B., Clapier, C. R., Schoehn, G., Weissenhorn, W., and Ruigrok, R. W. (2006) Crystal structure of the rabies virus nucleoprotein-RNA complex. Science 313, 360-363
10. Green, T. J., Zhang, X., Wertz, G. W., and Luo, M. (2006) Structure of the vesicular stomatitis virus nucleoprotein-RNA complex. Science 313, 357-360
11. Tawar, R. G., Duquerroy, S., Vonrhein, C, Varela, P. F., Damier-Piolle, L., Castagné, N., MacLellan, K., Bedouelle, H., Bricogne, G., Bhella, D., Eléouët, J. F., and Rey, F. A. (2009) Crystal structure of a nucleocapsid-like nucleoprotein-RNA complex of respiratory syncytial virus. Science 326, 1279-1283
12. Kranzusch, P. J., and Whelan, S. P. (2011) Arenavirus Z protein controls viral RNA synthesis by locking a polymerase-promoter complex. Proc. Natl. Acad. Sci. U.S.A. 108, 19743-19748
13. Noton, S. L., Deflubé, L. R., Tremaglio, C. Z., and Fearns, R. (2012) The respiratory syncytial virus polymerase has multiple RNA synthesis activities at the promoter. PLoS Pathog. 8, e1002980
14. 2+. Biochemistry 43, 5138-5148
15. Gohara, D. W., Arnold, J. J., and Cameron, C. E. (2004) Poliovirus RNA-dependent RNA polymerase (3Dpol). Kinetic, thermodynamic, and structural analysis of ribonucleotide selection. Biochemistry 43, 5149-5158
16. Gohara, D. W., Crotty, S., Arnold, J. J., Yoder, J. D., Andino, R., and Cameron, C E. (2000) Poliovirus RNA-dependent RNA polymerase (3Dpol). Structural, biochemical, and biological analysis of conserved structural motifs A and B. J. Biol. Chem. 275, 25523-25532
17. Ng, K. K., Arnold, J. J., and Cameron, C. E. (2008) Structure-function relationships among RNA-dependent RNA polymerases. Curr. Top. Microbiol. Immunol. 320, 137-156
18. Zamyatkin, D. F., Parra, F., Alonso, J. M., Harki, D. A., Peterson, B. R., Grochulski, P., and Ng, K. K. (2008) Structural insights into mechanisms of catalysis and inhibition in Norwalk virus polymerase. J. Biol. Chem. 283, 7705-7712
19. Butcher, S. J., Grimes, J. M., Makeyev, E. V., Bamford, D. H., and Stuart, D. I. (2001) A mechanism for initiating RNA-dependent RNA polymerization. Nature 410, 235-240
20. Ferrer-Orta, C, Arias, A., Escarmís, C, and Verdaguer, N. (2006) A comparison of viral RNA-dependent RNA polymerases. Curr. Opin. Struct. Biol. 16, 27-34
21. Tao, Y., Farsetta, D. L., Nibert, M. L., and Harrison, S. C. (2002) RNA synthesis in a cage. Structural studies of reovirus polymerase A3. Cell 111, 733-745
22. Schubert, M., and Lazzarini, R. A. (1982) In vitro transcription of vesicular stomatitis virus. Incorporation of deoxyguanosine and deoxycytidine, and formation of deoxyguanosine caps. J. Biol. Chem. 257, 2968-2973
23. Kao, C C, Singh, P., and Ecker, D. J. (2001) De novo initiation of viral RNA-dependent RNA synthesis. Virology 287, 251-260
24. Steitz, T. A. (1998) A mechanism for all polymerases. Nature 391, 231-232
25. van Dijk, A. A., Makeyev, E. V., and Bamford, D. H. (2004) Initiation of viral RNA-dependent RNA polymerization. J. Gen. Virol. 85, 1077-1093
26. Sofia, M. J., Chang, W., Furman, P. A., Mosley, R. T., and Ross, B. S. (2012) Nucleoside, nucleotide, and non-nucleoside inhibitors of hepatitis C virus NS5B RNA-dependent RNA-polymerase. J. Med. Chem. 55, 2481-2531
27. Ferrer-Orta, C, Arias, A., Perez-Luque, R., Escarmís, C, Domingo, E., and Verdaguer, N. (2004) Structure of foot-and-mouth disease virus RNA-dependent RNA polymerase and its complex with a template-primer RNA. J. Biol. Chem. 279, 47212-47221
28. Gong, P., and Peersen, O. B. (2010) Structural basis for active site closure by the poliovirus RNA-dependent RNA polymerase. Proc. Natl. Acad. Sci. U.S.A. 107, 22505-22510
29. Yin, Y. W., and Steitz, T. A. (2002) Structural basis for the transition from initiation to elongation transcription in T7 RNA polymerase. Science 298, 1387-1395
30. Siegel, R. W., Bellon, L., Beigelman, L., and Kao, C. C. (1999) Use of DNA, RNA, and chimeric templates by a viral RNA-dependent RNA polymer-ase. Evolutionary implications for the transition from the RNA to the DNA world. J. Virol. 73, 6424-6429
31. Tayon, R., Jr., Kim, M. J., and Kao, C. C. (2001) Completion of RNA synthesis by viral RNA replicases. Nucleic Acids Res. 29, 3576-3582
32. Zhong, W., Gutshall, L. L., and Del Vecchio, A. M. (1998) Identification and characterization of an RNA-dependent RNA polymerase activity within the nonstructural protein 5B region of bovine viral diarrhea virus. J. Virol. 72, 9365-9369