Recognition of RNA Cap in the Wesselsbron Virus NS5 Methyltransferase Domain: Implications for RNA-Capping Mechanisms in Flavivirus

Journal of Molecular Biology

Volumn 385, Issue 1, 2009, Pages 140-152

  Bollati, Michela ^a   Milani, Mario ^a   Mastrangelo, Eloise ^a   Ricagno, Stefano ^a   Tedeschi, Gabriella ^a   Nonnis, Simona ^a   Decroly, Etienne ^b   Selisko, Barbara ^b   de Lamballerie, Xavier ^c   Coutard, Bruno ^b   Canard, Bruno ^b   Bolognesi, Martino ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b Centre National de la Recherche Scientifique   (France)

^c Aix Marseille University IRD 190 Inserm 1207   (France)

Author keywords

Flavivirus; guanylyltransferase; methyltransferase; RNA capping; viral enzyme structure

Indexed keywords

CAPPED RNA; GUANINE; GUANOSINE PHOSPHATE; GUANOSINE TRIPHOSPHATE; LYSINE; METHYLTRANSFERASE; NONSTRUCTURAL PROTEIN 5; S ADENOSYLHOMOCYSTEINE; S ADENOSYLMETHIONINE; SINEFUNGIN;

ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME MECHANISM; ENZYME STRUCTURE; FLAVIVIRUS; METHYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN RNA BINDING; RNA BINDING; RNA CAPPING; WESSELBRON FLAVIVIRUS;

FLAVIVIRUS; WESSELSBRON VIRUS;

EID: 57749204973     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.10.028     Document Type: Article

References (39)

1. Chambers T.J., Hahn C.S., Galler R., and Rice C.M. Flavivirus genome organization, expression, and replication. Annu. Rev. Microbiol. 44 (1990) 649-688
2. Furuichi Y., LaFiandra A., and Shatkin A.J. 5(-Terminal structure and mRNA stability. Nature 266 (1977) 235-241
3. Shuman S. Structure, mechanism, and evolution of the mRNA capping apparatus. Prog. Nucleic Acid Res. Mol. Biol. 66 (2001) 1-40
4. Zhou Y., Ray D., Zhao Y., Dong H., Ren S., Li Z., et al. Structure and function of Flavivirus NS5 methyltransferase. J. Virol. 81 (2007) 3891-3903
5. Ray D., Shah A., Tilgner M., Guo Y., Zhao Y., Dong H., et al. West Nile virus 5(-cap structure is formed by sequential guanine N-7 and ribose 2(-O methylations by nonstructural protein 5. J. Virol. 80 (2006) 8362-8370
6. Assenberg R., Ren J., Verma A., Walter T.S., Alderton D., Hurrelbrink R.J., et al. Crystal structure of the Murray Valley encephalitis virus NS5 methyltransferase domain in complex with cap analogues. J. Gen. Virol. 88 (2007) 2228-2236
7. Egloff M.-P., Decroly E., Malet H., Selisko B., Benarroch D., Ferron F., and Canard B. Structural and functional analysis of methylation and 5(-RNA sequence requirements of short capped RNAs by the methyltransferase domain of dengue virus NS5. J. Mol. Biol. 372 (2007) 23-36
8. Morvan J., Fontanille D., Digoutte J.P., and Coulanges P. The Wesselsbron virus, a new arbovirus for Madagascar. Arch. Inst. Pasteur Madagascar 57 1 (1990) 183-192
9. Mastrangelo E., Bollati M., Milani M., Selisko B., Peyrane F., Canard B., et al. Crystal structure and activity of Kunjin virus NS3 helicase; protease and helicase domain assembly in the full length NS3 protein. Protein Sci. 16 (2007) 1133-1145
10. Faumann E.B., Blumental R.M., and Cheng X. Structure and evolution of AdoMet-dependent methyltransferases. In: Cheng X., and Blumental R.M. (Eds). S-Adenosylmethionine-Dependent Methyltransferases: Structure and Functions (1999), World Scientific Publishing, Singapore 1-38
11. Egloff M.P., Benarroch D., Selisko B., Romette J.L., and Canard B. An RNA cap (nucleoside-2(-O-)-methyltransferase in the Flavivirus RNA polymerase NS5: crystal structure and functional characterization. EMBO J. 21 (2002) 2757-2768
12. Kabsch W., and Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolicy 22 (1983) 2577-2637
13. Malet H., Egloff M.-P., Selisko B., Butcher R.E., Wright P.J., Roberts M., et al. Crystal structure of the RNA polymerase domain of the West Nile virus non-structural protein 5. J. Biol. Chem. 282 (2007) 10678-10689
14. Yap T.L., Xu T., Chen Y.L., Malet H., Egloff M.-P., Canard B., et al. Crystal structure of the dengue virus RNA-dependent RNA polymerase catalytic domain at 1.85-angstrom resolution. J. Virol. 81 (2007) 4753-4765
15. Dong H., Ren S., Zhang B., Zhou Y., Puig-Basagoiti F., Li H., and Shi P.-Y. West Nile virus methyltransferase catalyzes two methylations of the viral RNA cap through a substrate repositioning mechanism. J. Virol. 82 (2008) 4295-4307
16. Deguchi T., and Barchas J. Enhancement of transmethylation by adenosylhomocysteinase. J. Biol. Chem. 10 (1971) 3175-3181
17. Dong H., Ray D., Ren S., Zhang B., Puig-Basagoiti F., Takagi Y., et al. Distinct RNA elements confer specificity to Flavivirus RNA cap methylation events. J. Virol. 81 (2007) 4412-4421
18. Shuman S., and Hurwitz J. Mechanism of mRNA capping by vaccinia virus guanylyltransferase: characterization of an enzyme-guanylate intermediate. Proc. Natl Acad. Sci. USA 78 (1981) 187-191
19. Shuman S., Surks M., Furneaux H., and Hurwitz J. Purification and characterization of a GTP-pyrophosphate exchange activity from vaccinia virions. Association of the GTP-pyrophosphate exchange activity with vaccinia mRNA guanylyltransferase. RNA (guanine-7-)methyltransferase complex (capping enzyme). J. Biol. Chem. 255 (1980) 11588-11598
20. Mizumoto K., and Kaziro Y. Messenger RNA capping enzymes from eukaryotic cells. Prog. Nucleic Acid Res. Mol. Biol. 34 (1987) 1-28
21. Ahola T., Laakkonen P., Vihinen H., and Kaariainen L. Critical residues of Semliki Forest virus RNA capping enzyme involved in methyltransferase and guanylyltransferase-like activities. J. Virol. 71 (1997) 392-397
22. Guarino L.A., Jin J., and Dong W. Guanylyltransferase activity of the LEF-4 subunit of baculovirus RNA polymerase. J. Virol. 72 (1998) 10003-10010
23. Hakansson K., and Wigley D.B. Structure of a complex between a cap analogue and mRNA guanylyl transferase demonstrates the structural chemistry of RNA capping. Biochemistry 95 (1998) 1505-1510
24. Fresco L.D., and Buratowski S. Active site of the mRNA-capping enzyme guanylyltransferase from Saccharomyces cerevisiae: similarity to the nucleotidyl attachment motif of DNA and RNA ligases. Proc. Natl Acad. Sci. USA 91 (1994) 6624-6628
25. Fausnaugh J., and Shatkin A.J. Active site localization in a viral mRNA capping enzyme. J. Biol. Chem. 265 (1990) 7669-7672
26. Roth M.J., and Hurwitz J. RNA capping by the vaccinia virus guanylyltransferase. Structure of enzyme-guanylate intermediate. J. Biol. Chem. 259 (1984) 13488-13494
27. Sawaya R., and Shuman S. Mutational analysis of the guanylyltransferase component of mammalian mRNA capping enzyme. Biochemistry 42 (2003) 8240-8249
28. Wang S.P., Deng L., Ho C.K., and Shuman S. Phylogeny of mRNA capping enzymes. Proc. Natl Acad. Sci. USA 94 (1997) 9573-9578
29. Ferre-D'Amare A.R., and Burley S.K. Use of dynamic light scattering to assess crystallizability of macromolecules and macromolecular assemblies. Structure 25 (1994) 357-359
30. Zulauf M., and D'Arcy A. Light scattering of proteins as a criterion for crystallization. J. Cryst. Growth 122 (1992) 102-106
31. Steller I., Bolotovsky R., and Rossmann M. An algorithm for automatic indexing of oscillation images using Fourier analysis. J. Appl. Crystallogr. 30 (1997) 1036-1040
32. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D 50 (1994) 760-763
33. Vagin A., and Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30 (1997) 1022-1025
34. Winn M.D., Isupov M.N., and Murshudov G.N. Use of TLS parameter to model anisotropic displacement in macromolecular refinement. Acta Crystallogr. Sect. D 57 (2001) 122-133
35. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D 60 (2004) 2126-2132
36. Blanc E., Roversi P., Vonrhein C., Flensburg C., Lea S.M., and Bricogne G. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. Sect. D 60 (2004) 2210-2221
37. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291
38. 7MeGpppA-capped RNAs and HPLC-monitoring of methyltransfer reactions at the guanine-N7 and adenosine-2(O positions. Nucleic Acids Res. 35 (2007) e26
39. Berman H.M., Westbrook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., et al. The Protein Data Bank. Nucleic Acids Res. 28 (2000) 235-242