Deciphering the molecular basis for nucleotide selection by the West Nile virus RNA helicase

Nucleic Acids Research

Volumn 38, Issue 16, 2010, Pages 5493-5506

  Despins, Simon ^a   Issur, Moheshwarnath ^a   Bougie, Isabelle ^a   Bisaillon, Martin ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALANINE; AMINO ACID; ARGININE; ASPARAGINE; PURINE DERIVATIVE; RNA HELICASE; GUANOSINE TRIPHOSPHATE; NS3 PROTEIN, FLAVIVIRUS; NUCLEOTIDE; SERINE PROTEINASE; VIRUS PROTEIN;

AMINO ACID ANALYSIS; ARTICLE; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME BINDING; HYDROLYSIS; INHIBITION KINETICS; MOLECULAR MECHANICS; NUCLEIC ACID ANALYSIS; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STRUCTURE; STRUCTURAL HOMOLOGY; WEST NILE FLAVIVIRUS; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION;

WEST NILE VIRUS;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; CATALYTIC DOMAIN; GUANOSINE TRIPHOSPHATE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEOTIDES; RNA HELICASES; SERINE ENDOPEPTIDASES; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY; VIRAL NONSTRUCTURAL PROTEINS; WEST NILE VIRUS;

EID: 77956533034     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq276     Document Type: Article

References (50)

1. de la Cruz, J., Kressler, D., Tollervey, D. and Linder,p. (1998) Dob1p (Mtr4p) is a putative ATP-dependent RNA helicase required for the 3′ end formation of 5.8S rRNA in Saccharomyces cerevisiae. EMBO J., 17, 1128-1140.
2. Fuller-pace, F.V. (1994) RNA helicases: modulators of RNA structure. Trends Cell Biol., 4, 271-274.
3. Gorbalenya, A.E. and Koonin, E.V. (1993) Helicases: amino acid sequence comparisons and structure-function relationship. Curr. Opin. Struct. Biol., 3, 419-429.
4. Hodgman, T.C. (1988) A new superfamily of replicative proteins. Nature, 333, 22-23.
5. Ha, T., Rasnik, I., Cheng, W., Babcock, H.P., Gauss, G.H., Lohman, T.M. and Chu, S. (2002) Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase. Nature, 419, 638-641.
6. Lohman, T.M. and Bjornson, K.P. (1996) Mechanisms of helicase-catalyzed DNA unwinding. Annu. Rev. Biochem., 65, 169-214.
7. Maluf, N.K., Fischer, C.J. and Lohman, T.M. (2003) A dimer of Escherichia coli UvrD is the active form of the helicase in vitro. J. Mol. Biol., 325, 913-935.
8. Patel, S.S. and Picha, K.M. (2000) Structure and function of hexameric helicases. Annu. Rev. Biochem., 69, 651-697.
9. Soultanas, P. and Wigley, D.B. (2000) DNA helicases: "inching forward". Curr. Opin. Struct. Biol., 10, 124-128.
10. Hall, M.C. and Matson, S.W. (1999) Helicase motifs: the engine that powers DNA unwinding. Mol. Microbiol., 34, 867-877.
11. Subramanya, H.S., Bird, L.E., Brannigan, J.A. and Wigley, D.B. (1996) Crystal structure of a DExx box DNA helicase. Nature, 384, 379-383.
12. Koroloev, S., Hsieh, J., Gauss, G.H., Lohman, T.M. and Waksman, G. (1997) Major domain swiveling revealed by the crystal structures of complexes of E. coli Rep helicase bound to single-stranded DNA and ADP. Cell, 90, 635-647.
13. Yao, N., Hesson, T., Cable, M., Hong, Z., Kwong, A.D., Le, H.V. and Weber,p.C. (1997) Structure of the hepatitis C virus RNA helicase domain. Nat. Struct. Biol., 4, 463-467.
14. Kim, J.L., Morgenstern, K.A., Griffith, J.P., Dwyer, M.D., Thomson, J.A., Murcko, M.A., Lin, C. and Caron, P.R. (1998) Hepatitis C virus NS3 RNA helicase domain with a bound oligonucleotide: the crystal structure provides insights into the mode of unwinding. Structure, 6, 89-100.
15. Velankar, S.S., Soultanas, P., Dillingham, M.S., Subramanya, H.S. and Wigley, D.B. (1999) Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell, 97, 75-84.
16. Kwong, A.D., Rao, B.G. and Jeang, K.T. (2005) Viral and cellular RNA helicases as antiviral targets. Nat. Rev. Drug Disc., 4, 845-853.
17. Frick, D.N. and Lam, A.M.I. (2006) Understanding helicases as a means of virus control. Curr. Pharm. Des., 12, 1315-1338.
18. Grassmann, C.W., Isken, O. and Behrens, S.E. (1999) Assignment of the multifunctional NS3 protein of bovine viral diarrhea virus during RNA replication: an in vivo and in vitro study. J. Virol., 73, 9196-9205.
19. Gwack, Y., Kim, D.W., Han, J.H. and Choe, J. (1996) Characterization of RNA binding activity and RNA helicase activity of the hepatitis C virus NS3 protein. Biochem. Biophys. Res. Commun., 225, 654-659.
20. Utama, A., Shimizu, H., Morikawa, S., Hasebe, F., Morita, K., Igarashi, A., Hatsu, M., Takamizawa, K. and Miyamura, T. (2000) Identification and characterization of the RNA helicase activity of Japanese encephalitis virus NS3 protein. FEBS Lett., 465, 74-78.
21. Utama, A., Shimizu, H., Hasebe, F., Morita, K., Igarashi, A., Shoji, I., Matsuura, Y., Hatsu, M., Takamizawa, K. and Hagiwara, A. (2000) Role of the DExH motif of the Japanese encephalitis virus and hepatitis C virus NS3 proteins in the ATPase and RNA helicase activities. Virology, 273, 316-324.
22. Borowski, P., Mueller, O., Niebuhr, A., Kalitzky, M., Hwang, L.H., Schmitz, H., Siwecka, M.A. and Kulikowsk, T. (2000) ATP-binding domain of NTPase/helicase as a target for hepatitis C antiviral therapy. Acta Biochim. Pol., 47, 173-180.
23. Kim, D.W., Gwack, Y., Han, J.H. and Choe, J. (1995) C-terminal domain of the hepatitis C virus NS3 protein contains an RNA helicase activity. Biochem. Biophys. Res. Commun., 215, 160-166.
24. 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.
25. Sarbah, S. and Younossi, Z. (2000) Hepatitis C: an update on the silent epidemic. J. Clin. Gastro., 30, 125-143.
26. Hayes, E.B. and Gubler, D.J. (2006) West Nile virus: epidemiology and clinical features of an emerging epidemic in the United States. Annu. Rev. Med., 57, 181-194.
27. Wu, J., Bera, A.K., Kuhn, R.J. and Smith, J.L. (2005) Structure of the Flavivirus helicase: implications for catalytic activity, protein interactions, and proteolytic processing. J. Virol., 79, 10268-10277.
28. Luo, D., Xu, T., Watson, R.P., Scherer-Becker, D., Sampath, A., Jahnke, W., Yeong, S.S., Wang, C.H., Lim, S.P. and Strongin, A. (2008) Insights into RNA unwinding and ATP hydrolysis by the flavivirus NS3 protein. EMBO J., 27, 3209-3219.
29. 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.
30. 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-beta and the viral helicase, NS3. J. Gen. Virol., 82, 735-745.
31. Tuteja, N. and Tuteja, R. (2004) Unraveling DNA helicases. Motif, structure, mechanism and function. Eur. J. Biochem., 271, 1849-1863.
32. Tanner, N.K. and Linder, P. (2001) DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol. Cell, 8, 251-262.
33. Tanner, N.K., Cordin, O., Banroques, J., Doère, M. and Linder, P. (2003) The Q motif: a newly identified motif in DEAD box helicases may regulate ATP binding and hydrolysis. Mol. Cell, 11, 127-138.
34. Belon, C.A. and Frick, D.N. (2009) Fuel specificity of the hepatitis C virus NS3 helicase. J. Mol. Biol., 388, 851-864.
35. Suzich, J.A., Tamura, J.K., Palmer-Hill, F., Warrener, P., Grakoui, A., Rice, C.M., Feinstone, S.M. and Collett, M.S. (1993) Hepatitis C virus NS3 protein polynucleotide-stimulated nucleoside triphosphatase and comparison with the related pestivirus and flavivirus enzymes. J. Virol., 67, 6152-6158.
36. Preugschat, F., Averett, D.R., Clarke, B.E. and Porter, D.J. (1996) A steady-state and pre-steady-state kinetic analysis of the NTPase activity associated with the hepatitis C virus NS3 helicase domain. J. Biol. Chem., 271, 24449-24457.
37. Wardell, A.D., Errington, W., Ciaramella, G., Merson, J. and McGarvey, M.J. (1999) Characterization and mutational analysis of the helicase and NTPase activities of hepatitis C virus full-length NS3 protein. J. Gen. Virol., 80, 701-709.
38. Lam, A.M., Keeney, D., Eckert, P.Q. and Frick, D.N. (2003) Hepatitis C virus NS3 ATPases/helicases from different genotypes exhibit variations in enzymatic properties. J. Virol., 77, 3950-3961.
39. Bougie, I. and Bisaillon, M. (2009) Metal ion-binding studies highlight important differences between flaviviral RNA polymerases. Biochem. Biophys. Acta, 1794, 50-60.
40. Benzaghou, I., Bougie, I., Picard-Jean, F. and Bisaillon, M. (2006) Energetics of RNA binding by the West Nile virus RNA triphosphatase. FEBS Lett., 580, 867-877.
41. Schwede, T., Kopp, J., Guex, N. and Peitsch, M.C. (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res., 31, 3381-3385.
42. Zhou, P., Tian, F., Lv, F. and Shang, Z. (2009) Geometric characteristics of hydrogen bonds involving sulfur atoms in proteins. Proteins, 76, 151-163.
43. Lee, J.Y. and Yang, W. (2006) UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke. Cell, 127, 1349-1360.
44. Theis, K., Chen, P.J., Skorvaga, M., Van Houten, B. and Kisker, C. (1999) Crystal structure of UvrB, a DNA helicase adapted for nucleotide excision repair. EMBO J., 18, 6899-6907.
45. Rudolph, M.G., Heissmann, R., Wittmann, J.G. and Klostermeier, D. (2006) Crystal structure and nucleotide binding of the Thermus thermophilus RNA helicase Hera N-terminal domain. J. Mol. Biol., 361, 731-743.
46. Cordin, O., Tanner, N.K., Moere, M., Linder, P. and Banroques, J. (2004) The newly discovered Q motif of DEAD-box RNA helicases regulates RNA-binding and helicase activity. EMBO J., 23, 2478-2487.
47. Sinha, K.M., Glickman, M.S. and Shuman, S. (2009) Mutational analysis of Mycobacterium UvrD1 identifies functional groups required for ATP hydrolysis, DNA unwinding, and chemomechanical coupling. Biochemistry, 48, 4019-4030.
48. Nobeli, I., Laskowski, R.A., Valdar, W.S. and Thornton, J.M. (2001) On the molecular discrimination between adenine and guanine by proteins. Nucleic Acids Res., 29, 4294-4309.
49. Day, C.W., Smee, D.F., Julander, J.G., Yamshchikov, V.F., Sidwell, R.W. and Morrey, J.D. (2005) Error-prone replication of West Nile virus caused by ribavirin. Antiviral Res., 67, 38-45.
50. Graci, J.D. and Cameron, C.E. (2008) Therapeutically targeting RNA viruses via lethal mutagenesis. Future Virol., 3, 553-566.