Dengue virus nonstructural protein 5 adopts multiple conformations in solution

Biochemistry

Volumn 51, Issue 30, 2012, Pages 5921-5931

  Bussetta, Cécile ^a   Choi, Kyung H ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL DOMAINS; DENGUE VIRUS; EXTENDED FORM; FULL-LENGTH PROTEINS; GLOBULAR DOMAINS; MULTIPLE CONFORMATIONS; N-TERMINAL DOMAINS; NONSTRUCTURAL PROTEINS; O-METHYLTRANSFERASE; RELATIVE ORIENTATION; RNA-DEPENDENT RNA POLYMERASE; SMALL ANGLE X-RAY SCATTERING; STABLE STRUCTURES; STRUCTURAL DATA; STRUCTURE AND DYNAMICS; TWO DOMAINS; VIRAL GENOME; VIRAL RNA; WEAK INTERACTIONS;

EXPERIMENTS; RNA; VIRUSES;

PROTEINS;

MESSENGER RNA; NONSTRUCTURAL PROTEIN 5; VIRUS RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; DENGUE VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; RNA SYNTHESIS; SMALL ANGLE SCATTERING; VIRUS GENOME;

CRYSTALLOGRAPHY, X-RAY; DENGUE VIRUS; PROTEIN CONFORMATION; SOLUTIONS; VIRAL NONSTRUCTURAL PROTEINS; VIRAL PROTEINS; VIRUS REPLICATION;

DENGUE VIRUS;

EID: 84864436647     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300406n     Document Type: Article

References (57)

1. Gould, E. A. and Solomon, T. (2008) Pathogenic flaviviruses Lancet 371, 500-509
2. World Health Organization (2009) Dengue: Guidelines for diagnosis, treatment, prevention and control; World Health Organization, Geneva.
3. Mackenzie, J. S., Gubler, D. J., and Petersen, L. R. (2004) Emerging flaviviruses: The spread and resurgence of Japanese encephalitis, West Nile and dengue viruses Nat. Med. 10, S98-S109
4. Vasilakis, N. and Weaver, S. C. (2008) The history and evolution of human dengue emergence Adv. Virus Res. 72, 1-76
5. Rigau-Perez, J. G., Clark, G. G., Gubler, D. J., Reiter, P., Sanders, E. J., and Vorndam, A. V. (1998) Dengue and dengue haemorrhagic fever Lancet 352, 971-977
6. Paranjape, S. M. and Harris, E. (2010) Control of dengue virus translation and replication Curr. Top. Microbiol. Immunol. 338, 15-34
7. Khromykh, A. A., Kondratieva, N., Sgro, J. Y., Palmenberg, A., and Westaway, E. G. (2003) Significance in replication of the terminal nucleotides of the flavivirus genome J. Virol. 77, 10623-10629
8. Fernandez-Garcia, M. D., Mazzon, M., Jacobs, M., and Amara, A. (2009) Pathogenesis of flavivirus infections: Using and abusing the host cell Cell Host Microbe 5, 318-328
9. Perera, R. and Kuhn, R. J. (2008) Structural proteomics of dengue virus Curr. Opin. Microbiol. 11, 369-377
10. Bollati, M., Alvarez, K., Assenberg, R., Baronti, C., Canard, B., Cook, S., Coutard, B., Decroly, E., de Lamballerie, X., Gould, E. A., Grard, G., Grimes, J. M., Hilgenfeld, R., Jansson, A. M., Malet, H., Mancini, E. J., Mastrangelo, E., Mattevi, A., Milani, M., Moureau, G., Neyts, J., Owens, R. J., Ren, J., Selisko, B., Speroni, S., Steuber, H., Stuart, D. I., Unge, T., and Bolognesi, M. (2009) Structure and functionality in flavivirus NS-proteins: Perspectives for drug design Antiviral Res. 87, 125-148
11. Egloff, M. P., Decroly, E., Malet, H., Selisko, B., Benarroch, D., Ferron, F., and Canard, B. (2007) 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, 723-736
12. Issur, M., Geiss, B. J., Bougie, I., Picard-Jean, F., Despins, S., Mayette, J., Hobdey, S. E., and Bisaillon, M. (2009) The flavivirus NS5 protein is a true RNA guanylyltransferase that catalyzes a two-step reaction to form the RNA cap structure RNA 15, 2340-2350
13. Bollati, M., Milani, M., Mastrangelo, E., Ricagno, S., Tedeschi, G., Nonnis, S., Decroly, E., Selisko, B., de Lamballerie, X., Coutard, B., Canard, B., and Bolognesi, M. (2009) Recognition of RNA cap in the Wesselsbron virus NS5 methyltransferase domain: Implications for RNA-capping mechanisms in Flavivirus J. Mol. Biol. 385, 140-152
14. Liu, L., Dong, H., Chen, H., Zhang, J., Ling, H., Li, Z., Shi, P. Y., and Li, H. (2010) Flavivirus RNA cap methyltransferase: Structure, function, and inhibition Front. Biol. 5, 286-303
15. Cui, T., Sugrue, R. J., Xu, Q., Lee, A. K., Chan, Y. C., and Fu, J. (1998) Recombinant dengue virus type 1 NS3 protein exhibits specific viral RNA binding and NTPase activity regulated by the NS5 protein Virology 246, 409-417
16. Yon, C., Teramoto, T., Mueller, N., Phelan, J., Ganesh, V. K., Murthy, K. H., and Padmanabhan, R. (2005) Modulation of the nucleoside triphosphatase/RNA helicase and 5′-RNA triphosphatase activities of Dengue virus type 2 nonstructural protein 3 (NS3) by interaction with NS5, the RNA-dependent RNA polymerase J. Biol. Chem. 280, 27412-27419
17. Davidson, A. D. (2009) New Insights into Flavivirus Nonstructural Protein 5. In Advances in Virus Research, Chapter 2, pp 41-101, Academic Press, New York.
18. Kapoor, M., Zhang, L., Ramachandra, M., Kusukawa, J., Ebner, K. E., and Padmanabhan, R. (1995) Association between NS3 and NS5 proteins of dengue virus type 2 in the putative RNA replicase is linked to differential phosphorylation of NS5 J. Biol. Chem. 270, 19100-19106
19. Xu, T., Sampath, A., Chao, A., Wen, D., Nanao, M., Chene, P., Vasudevan, S. G., and Lescar, J. (2005) Structure of the dengue virus helicase/nucleoside triphosphatase catalytic domain at a resolution of 2.4 Å J. Virol. 79, 10278-10288
20. Luo, D., Xu, T., Hunke, C., Gruber, G., Vasudevan, S. G., and Lescar, J. (2008) Crystal structure of the NS3 protease-helicase from dengue virus J. Virol. 82, 173-183
21. Chernov, A. V., Shiryaev, S. A., Aleshin, A. E., Ratnikov, B. I., Smith, J. W., Liddington, R. C., and Strongin, A. Y. (2008) The two-component NS2B-NS3 proteinase represses DNA unwinding activity of the West Nile virus NS3 helicase J. Biol. Chem. 283, 17270-17278
22. Luo, D., Wei, N., Doan, D. N., Paradkar, P. N., Chong, Y., Davidson, A. D., Kotaka, M., Lescar, J., and Vasudevan, S. G. (2010) Flexibility between the protease and helicase domains of the dengue virus NS3 protein conferred by the linker region and its functional implications J. Biol. Chem. 285, 18817-18827
23. Selisko, B., Dutartre, H., Guillemot, J. C., Debarnot, C., Benarroch, D., Khromykh, A., Despres, P., Egloff, M. P., and Canard, B. (2006) Comparative mechanistic studies of de novo RNA synthesis by flavivirus RNA-dependent RNA polymerases Virology 351, 145-158
24. Assenberg, R., Mastrangelo, E., Walter, T. S., Verma, A., Milani, M., Owens, R. J., Stuart, D. I., Grimes, J. M., and Mancini, E. J. (2009) Crystal structure of a novel conformational state of the flavivirus NS3 protein: Implications for polyprotein processing and viral replication J. Virol. 83, 12895-12906
25. Egloff, M. P., Benarroch, D., Selisko, B., Romette, J. L., and Canard, B. (2002) An RNA cap (nucleoside-2′-O-)-methyltransferase in the flavivirus RNA polymerase NS5: Crystal structure and functional characterization EMBO J. 21, 2757-2768
26. Yap, T. L., Xu, T., Chen, Y. L., Malet, H., Egloff, M. P., Canard, B., Vasudevan, S. G., and Lescar, J. (2007) Crystal structure of the dengue virus RNA-dependent RNA polymerase catalytic domain at 1.85-angstrom resolution J. Virol. 81, 4753-4765
27. Cheng, X. and Roberts, R. J. (2001) AdoMet-dependent methylation, DNA methyltransferases and base flipping Nucleic Acids Res. 29, 3784-3795
28. Ray, D., Shah, A., Tilgner, M., Guo, Y., Zhao, Y., Dong, H., Deas, T. S., Zhou, Y., Li, H., and Shi, P. Y. (2006) 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, 8362-8370
29. Lo Conte, L., Ailey, B., Hubbard, T. J., Brenner, S. E., Murzin, A. G., and Chothia, C. (2000) SCOP: A structural classification of proteins database Nucleic Acids Res. 28, 257-259
30. Ferrer-Orta, C., Arias, A., Escarmis, C., and Verdaguer, N. (2006) A comparison of viral RNA-dependent RNA polymerases Curr. Opin. Struct. Biol. 16, 27-34
31. Choi, K. H. and Rossmann, M. G. (2009) RNA-dependent RNA polymerases from Flaviviridae Curr. Opin. Struct. Biol. 19, 746-751
32. Ferron, F., Bussetta, C., Dutartre, H., and Canard, B. (2005) The modeled structure of the RNA dependent RNA polymerase of GBV-C virus suggests a role for motif E in Flaviviridae RNA polymerases BMC Bioinf. 6, 255
33. Cameron, C. E., Moustafa, I. M., and Arnold, J. J. (2009) Dynamics: The missing link between structure and function of the viral RNA-dependent RNA polymerase? Curr. Opin. Struct. Biol. 19, 768-774
34. Szymanski, M. R., Jezewska, M. J., Bujalowski, P. J., Bussetta, C., Ye, M., Choi, K. H., and Bujalowski, W. (2011) Full-length dengue virus RNA-dependent RNA polymerase-RNA/DNA complexes: Stoichiometries, intrinsic affinities, cooperativities, base, and conformational specificities J. Biol. Chem. 286, 33095-33108
35. Malet, H., Egloff, M. P., Selisko, B., Butcher, R. E., Wright, P. J., Roberts, M., Gruez, A., Sulzenbacher, G., Vonrhein, C., Bricogne, G., Mackenzie, J. M., Khromykh, A. A., Davidson, A. D., and Canard, B. (2007) Crystal structure of the RNA polymerase domain of the West Nile virus non-structural protein 5 J. Biol. Chem. 282, 10678-10689
36. Hura, G. L., Menon, A. L., Hammel, M., Rambo, R. P., Poole, F. L., II, Tsutakawa, S. E., Jenney, F. E., Jr., Classen, S., Frankel, K. A., Hopkins, R. C., Yang, S. J., Scott, J. W., Dillard, B. D., Adams, M. W., and Tainer, J. A. (2009) Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS) Nat. Methods 6, 606-612
37. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H., and Svergun, D. I. (2003) PRIMUS: A Windows PC-based system for small-angle scattering data analysis J. Appl. Crystallogr. 36, 1277-1282
38. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria J. Appl. Crystallogr. 25, 495-503
39. Mertens, H. D. and Svergun, D. I. (2010) Structural characterization of proteins and complexes using small-angle X-ray solution scattering J. Struct. Biol. 172, 128-141
40. Mylonas, E. and Svergun, D. I. (2007) Accuracy of molecular mass determination of proteins in solution by small-angle X-ray scattering J. Appl. Crystallogr. 40, s245-s249
41. Svergun, D. I., Petoukhov, M. V., and Koch, M. H. (2001) Determination of domain structure of proteins from X-ray solution scattering Biophys. J. 80, 2946-2953
42. Volkov, V. V. and Svergun, D. I. (2003) Uniqueness of ab initio shape determination in small-angle scattering J. Appl. Crystallogr. 36, 860-864
43. Svergun, D., Barberato, C., and Koch, M. H. J. (1995) CRYSOL: A Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates J. Appl. Crystallogr. 28, 768-773
44. Kozin, M. B. and Svergun, D. I. (2001) Automated matching of high- and low-resolution structural models J. Appl. Crystallogr. 34, 33-41
45. Petoukhov, M. V. and Svergun, D. I. (2005) Global Rigid Body Modeling of Macromolecular Complexes against Small-Angle Scattering Data Biophys. J. 89, 1237-1250
46. Bernadó, P., Mylonas, E., Petoukhov, M. V., Blackledge, M., and Svergun, D. I. (2007) Structural Characterization of Flexible Proteins Using Small-Angle X-ray Scattering J. Am. Chem. Soc. 129, 5656-5664
47. Assenberg, R., Ren, J., Verma, A., Walter, T. S., Alderton, D., Hurrelbrink, R. J., Fuller, S. D., Bressanelli, S., Owens, R. J., Stuart, D. I., and Grimes, J. M. (2007) Crystal structure of the Murray Valley encephalitis virus NS5 methyltransferase domain in complex with cap analogues J. Gen. Virol. 88, 2228-2236
48. Geiss, B. J., Stahla, H., Hannah, A. M., Gari, A. M., and Keenan, S. M. (2009) Focus on flaviviruses: Current and future drug targets Future Med. Chem. 1, 327-344
49. Jansson, A. M., Jakobsson, E., Johansson, P., Lantez, V., Coutard, B., de Lamballerie, X., Unge, T., and Jones, T. A. (2009) Structure of the methyltransferase domain from the Modoc virus, a flavivirus with no known vector Acta Crystallogr. D65, 796-803
50. Bollati, M., Milani, M., Mastrangelo, E., de Lamballerie, X., Canard, B., and Bolognesi, M. (2009) Crystal structure of a methyltransferase from a no-known-vector Flavivirus Biochem. Biophys. Res. Commun. 382, 200-204
51. Vachette, P., Koch, M. H., and Svergun, D. I. (2003) Looking behind the beamstop: X-ray solution scattering studies of structure and conformational changes of biological macromolecules Methods Enzymol. 374, 584-615
52. Pilz, I. (1982) Small Angle X-ray Scattering. In Proteins (Glatter, O. and Kratky, O., Eds.) Chapter 8, pp 239-293, Academic Press Inc., London.
53. Putnam, C. D., Hammel, M., Hura, G. L., and Tainer, J. A. (2007) X-ray solution scattering (SAXS) combined with crystallography and computation: Defining accurate macromolecular structures, conformations and assemblies in solution Q. Rev. Biophys. 40, 191-285
54. George, R. A. and Heringa, J. (2002) An analysis of protein domain linkers: Their classification and role in protein folding Protein Eng. 15, 871-879
55. Bernadó, P. (2010) Effect of interdomain dynamics on the structure determination of modular proteins by small-angle scattering Eur. Biophys. J. 39, 769-780
56. Johansson, M., Brooks, A. J., Jans, D. A., and Vasudevan, S. G. (2001) A small region of the dengue virus-encoded RNA-dependent RNA polymerase, NS5, confers interaction with both the nuclear transport receptor importin-β and the viral helicase, NS3 J. Gen. Virol. 82, 735-745
57. Kroschewski, H., Lim, S. P., Butcher, R. E., Yap, T. L., Lescar, J., Wright, P. J., Vasudevan, S. G., and Davidson, A. D. (2008) Mutagenesis of the dengue virus type 2 NS5 methyltransferase domain J. Biol. Chem. 283, 19410-19421