The rabies virus L protein catalyzes mRNA capping with GDP polyribonucleotidyltransferase activity

Viruses

Volumn 8, Issue 5, 2016, Pages

  Ogino, Minako ^a   Ito, Naoto ^b   Sugiyama, Makoto ^b   Ogino, Tomoaki ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GIFU UNIVERSITY   (Japan)

Author keywords

GDP polyribonucleotidyltransferase; L protein; mRNA capping; Rabies virus

Indexed keywords

DIHYDROLIPOAMIDE DEHYDROGENASE; GUANOSINE DIPHOSPHATE POLYRIBONUCLEOTIDYLTRANSFERASE; GUANOSINE TRIPHOSPHATE; MESSENGER RNA; RECOMBINANT PROTEIN; RNA POLYMERASE; RNA RECOGNITION MOTIF PROTEIN; UNCLASSIFIED DRUG; VIRUS ENZYME; DNA DIRECTED RNA POLYMERASE; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE; L PROTEIN, RABIES VIRUS; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; VIRAL PROTEIN; VIRUS RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOCATALYST; CONTROLLED STUDY; COVALENT BOND; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC POLYMORPHISM; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN HYDROLYSIS; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; PROTEIN RNA BINDING; RABIES VIRUS; RNA CAPPING; SITE DIRECTED MUTAGENESIS; WESTERN BLOTTING; ENZYMOLOGY; GENETICS; METABOLISM;

DNA-DIRECTED RNA POLYMERASES; GTP PHOSPHOHYDROLASES; GUANOSINE DIPHOSPHATE; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RABIES VIRUS; RECOMBINANT PROTEINS; RNA, MESSENGER; RNA, VIRAL; VIRAL PROTEINS;

EID: 84969560104     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v8050144     Document Type: Article

References (32)

1. Albertini, A.A.; Ruigrok, R.W.; Blondel, D. Rabies virus transcription and replication. Adv. Virus Res. 2011, 79, 1-22
2. Davis, B.M.; Rall, G.F.; Schnell, M.J. Everything you always wanted to know about rabies virus (but were afraid to ask). Annu. Rev. Virol. 2015, 2, 451-471
3. Lankester, F.; Hampson, K.; Lembo, T.; Palmer, G.; Taylor, L.; Cleaveland, S. Infectious Disease. Implementing Pasteur’s vision for rabies elimination. Science 2014, 345, 1562-1564
4. Johnson, N.; Vos, A.; Freuling, C.; Tordo, N.; Fooks, A.R.; Muller, T. Human rabies due to lyssavirus infection of bat origin. Vet. Microbiol. 2010, 142, 151-159
5. Villarreal, L.P.; Holland, J.J. Transcribing complexes in cells infected by vesicular stomatitis virus and rabies virus. J. Virol. 1974, 14, 441-450
6. Kawai, A. Transcriptase activity associated with rabies virion. J. Virol. 1977, 24, 826-835
7. Poch, O.; Blumberg, B.M.; Bougueleret, L.; Tordo, N. Sequence comparison of five polymerases (L proteins) of unsegmented negative-strand RNA viruses: Theoretical assignment of functional domains. J. Gen. Virol. 1990, 71, 1153-1162
8. Bujnicki, J.M.; Rychlewski, L. In silico identification, structure prediction and phylogenetic analysis of the 21-O-ribose (cap 1) methyltransferase domain in the large structural protein of ssRNA negative-strand viruses. Protein Eng. 2002, 15, 101-108
9. Ogino, T.; Banerjee, A.K. An unconventional pathway of mRNA cap formation by vesiculoviruses. Virus Res. 2011, 162, 100-109
10. Abraham, G.; Banerjee, A.K. Sequential transcription of the genes of vesicular stomatitis virus. Proc. Natl. Acad. Sci. USA 1976, 73, 1504-1508
11. Ball, L.A.; White, C.N. Order of transcription of genes of vesicular stomatitis virus. Proc. Natl. Acad. Sci. USA 1976, 73, 442-446
12. Testa, D.; Chanda, P.K.; Banerjee, A.K. Unique mode of transcription in vitro by Vesicular stomatitis virus. Cell 1980, 21, 267-275
13. Emerson, S.U. Reconstitution studies detect a single polymerase entry site on the vesicular stomatitis virus genome. Cell 1982, 31, 635-642
14. Banerjee, A.K.; Rhodes, D.P. In vitro synthesis of RNA that contains polyadenylate by virion-associated RNA polymerase of vesicular stomatitis virus. Proc. Natl. Acad. Sci. USA 1973, 70, 3566-3570
15. Abraham, G.; Rhodes, D.P.; Banerjee, A.K. The 51 terminal structure of the methylated mRNA synthesized in vitro by vesicular stomatitis virus. Cell 1975, 5, 51-58
16. Ogino, T.; Banerjee, A.K. Unconventional mechanism of mRNA capping by the RNA-dependent RNA polymerase of vesicular stomatitis virus. Mol. Cell 2007, 25, 85-97
17. Ogino, T.; Banerjee, A.K. Formation of guanosine(51)tetraphospho(51)adenosine cap structure by an unconventional mRNA capping enzyme of vesicular stomatitis virus. J. Virol. 2008, 82, 7729-7734
18. Ogino, T.; Banerjee, A.K. The HR motif in the RNA-dependent RNA polymerase L protein of Chandipura virus is required for unconventional mRNA-capping activity. J. Gen. Virol. 2010, 91, 1311-1134
19. Ogino, T.; Yadav, S.P.; Banerjee, A.K. Histidine-mediated RNA transfer to GDP for unique mRNA capping by vesicular stomatitis virus RNA polymerase. Proc. Natl. Acad. Sci. USA 2010, 107, 3463-3468
20. Shuman, S. Structure, mechanism, and evolution of the mRNA capping apparatus. Prog. Nucleic Acid Res. Mol. Biol. 2001, 66, 1-40
21. Ogino, T. Capping of vesicular stomatitis virus pre-mRNA is required for accurate selection of transcription stop-start sites and virus propagation. Nucleic Acids Res. 2014, 42, 12112-12125
22. Neubauer, J.; Ogino, M.; Green, T.J.; Ogino, T. Signature motifs of GDP polyribonucleotidyltransferase, a non-segmented negative strand RNA viral mRNA capping enzyme, domain in the L protein are required for covalent enzyme-pRNA intermediate formation. Nucleic Acids Res. 2016, 44, 330-341
23. Li, J.; Rahmeh, A.; Morelli, M.; Whelan, S.P. 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. 2008, 82, 775-784
24. Ogino, T.; Banerjee, A.K. mRNA capping by vesicular stomatitis virus and other related viruses. In Negative Strand RNA Virus; Luo, M., Ed.; World Scientific: Singapore, 2011; pp. 79-94.
25. Liang, B.; Li, Z.; Jenni, S.; Rahmeh, A.A.; Morin, B.M.; Grant, T.; Grigorieff, N.; Harrison, S.C.; Whelan, S.P. Structure of the L protein of vesicular stomatitis virus from electron cryomicroscopy. Cell 2015, 162, 314-327
26. Ito, N.; Takayama, M.; Yamada, K.; Sugiyama, M.; Minamoto, N. Rescue of rabies virus from cloned cDNA and identification of the pathogenicity-related gene: Glycoprotein gene is associated with virulence for adult mice. J. Virol. 2001, 75, 9121-9128
27. Ogino, T. In vitro capping and transcription of rhabdoviruses. Methods 2013, 59, 188-198
28. Bourhy, H.; Kissi, B.; Tordo, N. Molecular diversity of the Lyssavirus genus. Virology 1993, 194, 70-81
29. Schnell, M.J.; Conzelmann, K.K. Polymerase activity of in vitro mutated rabies virus L protein. Virology 1995, 214, 522-530
30. Venkatesan, S.; Moss, B. Donor and acceptor specificities of HeLa cell mRNA guanylyltransferase. J. Biol. Chem. 1980, 255, 2835-2842
31. Martin, S.A.; Moss, B. mRNA guanylyltransferase and mRNA (guanine-7-)-methyltransferase from vaccinia virions. Donor and acceptor substrate specificites. J. Biol. Chem. 1976, 251, 7313-7321
32. Furuichi, Y.; Muthukrishnan, S.; Tomasz, J.; Shatkin, A.J. Mechanism of formation of reovirus mRNA 51-terminal blocked and methylated sequence, m7GpppGmpC. J. Biol. Chem. 1976, 251, 5043-5053