Phosphate release contributes to the rate-limiting step for unwinding by an RNA helicase

Nucleic Acids Research

Volumn 38, Issue 4, 2009, Pages 1312-1324

  Wang, Qixin ^a,b   Arnold, Jamie J ^a   Uchida, Akira ^a   Raney, Kevin D ^c   Cameron, Craig E ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; NONSTRUCTURAL PROTEIN 3; PHOSPHATE; RNA; ADENOSINE TRIPHOSPHATASE; NS3 PROTEIN, HEPATITIS C VIRUS; OLIGORIBONUCLEOTIDE; RNA HELICASE; VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; ENZYME SUBSTRATE; HEPATITIS C VIRUS; HYDROLYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOSPHATE TRANSPORT; PRIORITY JOURNAL; BIOCATALYSIS; CHEMISTRY; KINETICS; METABOLISM; PROTEIN BINDING;

HEPATITIS C VIRUS;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; BIOCATALYSIS; KINETICS; OLIGORIBONUCLEOTIDES; PHOSPHATES; PROTEIN BINDING; RNA HELICASES; VIRAL NONSTRUCTURAL PROTEINS;

EID: 77950361633     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp1118     Document Type: Article

References (37)

1. Bleichert, F. and Baserga, S.J. (2007) The long unwinding road of RNA helicases. Mol. Cell, 27, 339-352.
2. Knipe, D.M., Howley, P.M., Griffin, D.E., Lamb, R.A., Martin, M.A., Roizman, B. and Straus, S.E. (2007) Field's Virology. Lippincott Williams and Wilkins, Philadelphia, PA.
3. Cheng, W., Dumont, S., Tinoco, I. Jr and Bustamante, C. (2007) NS3 helicase actively separates RNA strands and senses sequence barriers ahead of the opening fork. Proc. Natl Acad. Sci. USA, 104, 13954-13959.
4. Dumont, S., Cheng, W., Serebrov, V., Beran, R.K., Tinoco, I. Jr, Pyle, A.M. and Bustamante, C. (2006) RNA translocation and unwinding mechanism of HCV NS3 helicase and its coordination by ATP. Nature, 439, 105-108.
5. Levin, M.K., Gurjar, M. and Patel, S.S. (2005) A Brownian motor mechanism of translocation and strand separation by hepatitis C virus helicase. Nat. Struct. Mol. Biol., 12, 429-435.
6. Myong, S., Bruno, M.M., Pyle, A.M. and Ha, T. (2007) Spring-loaded mechanism of DNA unwinding by hepatitis C virus NS3 helicase. Science, 317, 513-516.
7. 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.
8. Serebrov, V., Beran, R.K. and Pyle, A.M. (2009) Establishing a mechanistic basis for the large kinetic steps of the NS3 helicase. J. Biol. Chem., 284, 2512-2521.
9. Serebrov, V. and Pyle, A.M. (2004) Periodic cycles of RNA unwinding and pausing by hepatitis C virus NS3 helicase. Nature, 430, 476-480.
10. Jennings, T.A., Chen, Y., Sikora, D., Harrison, M.K., Sikora, B., Huang, L., Jankowsky, E., Fairman, M.E., Cameron, C.E. and Raney, K.D. (2008) RNA unwinding activity of the hepatitis C virus NS3 helicase is modulated by the NS5B polymerase. Biochemistry, 47, 1126-1135.
11. Sikora, B., Chen, Y., Lichti, C.F., Harrison, M.K., Jennings, T.A., Tang, Y., Tackett, A.J., Jordan, J.B., Sakon, J., Cameron, C.E. et al. (2008) Hepatitis C virus NS3 helicase forms oligomeric structures that exhibit optimal DNA unwinding activity in vitro. J. Biol. Chem., 283, 11516-11525.
12. Pang, P.S., Jankowsky, E., Planet, P.J. and Pyle, A.M. (2002) The hepatitis C viral NS3 protein is a processive DNA helicase with cofactor enhanced RNA unwinding. EMBO J., 21, 1168-1176.
13. Donmez, I. and Patel, S.S. (2008) Coupling of DNA unwinding to nucleotide hydrolysis in a ring-shaped helicase. EMBO J., 27, 1718-1726.
14. Pyle, A.M. (2008) Translocation and unwinding mechanisms of RNA and DNA helicases. Annu. Rev. Biophys., 37, 317-336.
15. Arnold, J.J. and Cameron, C.E. (2000) Poliovirus RNA-dependent RNA polymerase (3D(pol)). Assembly of stable, elongation-competent complexes by using a symmetrical primer-template substrate (sym/sub). J. Biol. Chem., 275, 5329-5336.
16. Lohmann, V., Korner, F., Koch, J., Herian, U., Theilmann, L. and Bartenschlager, R. (1999) Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science, 285, 110-113.
17. Brune, M., Hunter, J.L., Corrie, J.E. and Webb, M.R. (1994) Direct, real-time measurement of rapid inorganic phosphate release using a novel fluorescent probe and its application to actomyosin subfragment 1 ATPase. Biochemistry, 33, 8262-8271.
18. Studier, F.W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif., 41, 207-234.
19. Lakowicz, J.R. (1999) Principles of Fluorescence Spectroscopy. Kluwer Academic, Plenum Publishers.
20. Tackett, A.J., Chen, Y., Cameron, C.E. and Raney, K.D. (2005) Multiple full-length NS3 molecules are required for optimal unwinding of oligonucleotide DNA in vitro. J. Biol. Chem., 280, 10797-10806.
21. Mackintosh, S.G., Lu, J.Z., Jordan, J.B., Harrison, M.K., Sikora, B., Sharma, S.D., Cameron, C.E., Raney, K.D. and Sakon, J. (2006) Structural and biological identification of residues on the surface of NS3 helicase required for optimal replication of the hepatitis C virus. J. Biol. Chem., 281, 3528-3535.
22. Donmez, I., Rajagopal, V., Jeong, Y.J. and Patel, S.S. (2007) Nucleic acid unwinding by hepatitis C virus and bacteriophage t7 helicases is sensitive to base pair stability. J. Biol. Chem., 282, 21116-21123.
23. Frick, D.N., Banik, S. and Rypma, R.S. (2007) Role of divalent metal cations in ATP hydrolysis catalyzed by the hepatitis C virus NS3 helicase: magnesium provides a bridge for ATP to fuel unwinding. J. Mol. Biol., 365, 1017-1032.
24. Locatelli, G.A., Spadari, S. and Maga, G. (2002) Hepatitis C virus NS3 ATPase/helicase: an ATP switch regulates the cooperativity among the different substrate binding sites. Biochemistry, 41, 10332-10342.
25. Porter, D.J. (1998) Inhibition of the hepatitis C virus helicase-associated ATPase activity by the combination of ADP, NaF, MgCl2, and poly(rU). Two ADP binding sites on the enzyme-nucleic acid complex. J. Biol. Chem., 273, 7390-7396.
26. Huang, L., Hwang, J., Sharma, S.D., Hargittai, M.R., Chen, Y., Arnold, J.J., Raney, K.D. and Cameron, C.E. (2005) Hepatitis C virus nonstructural protein 5A (NS5A) is an RNA-binding protein. J. Biol. Chem., 280, 36417-36428.
27. Rajagopal, V. and Patel, S.S. (2008) Single strand binding proteins increase the processivity of DNA unwinding by the hepatitis C virus helicase. J. Mol. Biol., 376, 69-79.
28. Ikeda, M., Yi, M., Li, K. and Lemon, S.M. (2002) Selectable subgenomic and genome-length dicistronic RNAs derived from an infectious molecular clone of the HCV-N strain of hepatitis C virus replicate efficiently in cultured Huh7 cells. J. Virol., 76, 2997-3006.
29. Pietschmann, T., Lohmann, V., Rutter, G., Kurpanek, K. and Bartenschlager, R. (2001) Characterization of cell lines carrying self-replicating hepatitis C virus RNAs. J. Virol., 75, 1252-1264.
30. Yi, M., Bodola, F. and Lemon, S.M. (2002) Subgenomic hepatitis C virus replicons inducing expression of a secreted enzymatic reporter protein. Virology, 304, 197-210.
31. Chen, Y., Potratz, J.P., Tijerina, P., Del Campo, M., Lambowitz, A.M. and Russell, R. (2008) DEAD-box proteins can completely separate an RNA duplex using a single ATP. Proc. Natl Acad. Sci. USA, 105, 20203-20208.
32. Liu, F., Putnam, A. and Jankowsky, E. (2008) ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding. Proc. Natl Acad. Sci. USA, 105, 20209-20214.
33. Yang, Q., Del Campo, M., Lambowitz, A.M. and Jankowsky, E. (2007) DEAD-box proteins unwind duplexes by local strand separation. Mol. Cell, 28, 253-263.
34. Gilbert, S.P., Webb, M.R., Brune, M. and Johnson, K.A. (1995) Pathway of processive ATP hydrolysis by kinesin. Nature, 373, 671-676.
35. Algire, M.A., Maag, D. and Lorsch, J.R. (2005) Pi release from eIF2, not GTP hydrolysis, is the step controlled by start-site selection during eukaryotic translation initiation. Mol. Cell, 20, 251-262.
36. Henn, A., Cao, W., Hackney, D.D. and De La Cruz, E.M. (2008) The ATPase cycle mechanism of the DEAD-box rRNA helicase, DbpA. J. Mol. Biol., 377, 193-205.
37. Cheng, Y. and Prusoff, W.H. (1973) Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem. Pharmacol., 22, 3099-3108.