PcrA helicase tightly couples ATP hydrolysis to unwinding double-stranded DNA, modulated by the initiator protein for plasmid replication, RepD

Biochemistry

Volumn 48, Issue 27, 2009, Pages 6326-6334

  Slatter, Andrew F ^a   Thomas, Christopher D ^b   Webb, Martin R ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ATP HYDROLYSIS; BASE PAIRS; COUPLING RATIOS; DNA HELICASE; DOUBLE STRANDED DNA; HELICASE; PROCESSIVITY; SINGLE MOLECULE; SINGLE-STRANDED DNA;

DNA; HYDROLYSIS; NUCLEIC ACIDS; OLIGONUCLEOTIDES;

GENES;

ADENOSINE TRIPHOSPHATE; DOUBLE STRANDED DNA; HELICASE; OLIGONUCLEOTIDE; PROTEIN PCRA; PROTEIN REPD; UNCLASSIFIED DRUG;

ARTICLE; BASE PAIRING; COVALENT BOND; DNA REPLICATION ORIGIN; GENE; HYDROLYSIS; MOLECULAR RECOGNITION; ORID GENE; PLASMID; PRIORITY JOURNAL; PROTEIN DNA BINDING;

ADENOSINE TRIPHOSPHATE; BACILLUS STEAROTHERMOPHILUS; BACTERIAL PROTEINS; BASE SEQUENCE; DNA; DNA HELICASES; DNA PRIMERS; HYDROLYSIS; KINETICS; PLASMIDS; POLYMERASE CHAIN REACTION;

EID: 67650066482     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900101h     Document Type: Article

References (32)

1. Dillingham, M. S., Wigley, D. B., and Webb, M. R. (2000) Demonstration of unidirectional single-stranded DNA translocation by PcrA helicase: measurement of step size and translocation speed. Biochemistry 39, 205-212.
2. Soultanas, P., Dillingham, M. S., Papadopoulos, F., Phillips, S. E., Thomas, C. D., and Wigley, D. B. (1999) Plasmid replication initiator protein RepD increases the processivity of PcrA DNA helicase. Nucleic Acids Res. 27, 1421-1428.
3. Niedziela-Majka, A., Chesnik, M. A., Tomko, E. J., and Lohman, T. M. (2007) Bacillus stearothermophilus PcrA monomer is a single-stranded DNA translocase but not a processive helicase in vitro. J. Biol. Chem. 282, 27076-27085.
4. 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.
5. Subramanya, H. S., Bird, L. E., Brannigan, J. A., and Wigley, D. B. (1996) Crystal structure of DExx box DNA helicase. Nature 384, 379-383.
6. Dillingham, M. S., Soultanas, P., Wiley, P., Webb, M. R., and Wigley, D. B. (2001) Defining the roles of individual residues in the single-stranded DNA binding site of PcrA helicase. Proc. Natl. Acad. Sci. U.S.A. 98, 8381-8387.
7. Yang, Y., Dou, S.-X., Ren, H., Wang, P.-Y., Zhang, X.-D., Qian, M., Pan, B.-Y., and Xi, X. G. (2008) Evidence for a functional dimeric form of the PcrA helicase in DNA unwinding. Nucleic Acids Res. 36, 1976-1989.
8. Bird, L. E., Brannigan, J. A., Subramanya, H. S., and Wigley, D. B. (1998) Characterisation of Bacillus stearothermophilus PcrA helicase: evidence against an active rolling mechanism. Nucleic Acids Res. 26, 2686-2693.
9. Levin, M. K., Wang, Y. H., and Patel, S. S. (2004) The functional interaction of the hepatitis C virus helicase molecules is responsible for unwinding processivity. J. Biol. Chem. 279, 26005-26012.
10. Byrd, A. K., and Raney, K. D. (2005) Increasing the length of the single-stranded overhang enhances unwinding of duplex DNA by bacteriophage T4 Dda helicase. Biochemistry 44, 12990-12997.
11. Iordanescu, S., and Bargonetti, J. (1989) Staphylococcus aureus chromosomal mutations that decrease efficiency of Rep utilization in replication of pT181 and related plasmids. J. Bacteriol. 171, 4501-4503.
12. Khan, S. A. (1997) Rolling-circle replication of bacterial plasmids. Microbiol. Mol. Biol. Rev. 61, 442-455.
13. Gennaro, M. L., Iordanescu, S., Novick, R. P., Murray, R. W., Steck, T. R., and Khan, S. A. (1989) Functional organization of the plasmid pT181 replication origin. J. Mol. Biol. 205, 355-362.
14. Noirot, P., Bargonetti, J., and Novick, R. P. (1990) Initiation of rolling-circle replication in pT181 plasmid: initiator protein enhances cruciform extrusion at the origin. Proc. Natl. Acad. Sci. U.S.A. 87, 8560-8564.
15. Thomas, C. D., Balson, D. F., and Shaw, W. V. (1990) In vitro studies of the initiation of Staphylococcal plasmid replication. Specificity of RepD for its origin (oriD) and characterization of the RepD-ori tyrosyl ester intermediate. J. Biol. Chem. 265, 5519-5530.
16. Projan, S. J., Kornblum, J., Moghazeh, S. L., Edelman, I., Gennaro, M. L., and Novick, R. P. (1985) Comparative sequence and functional analysis of pT181 and pC221, cognate plasmid replicons from Staphylococcus aureus. Mol. Gen. Genet. 199, 452-464.
17. Thomas, C. D., Nikiforov, T. T., Connolly, B. A., and Shaw, W. V. (1995) Determination of sequence specificity between a plasmid replication initiator protein and the origin of replication. J. Mol. Biol. 254, 381-391.
18. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4, 2411-2423.
19. Dillingham, M. S., Tibbles, K. L., Hunter, J. L., Bell, J. C., Kowalczykowski, S. C., and Webb, M. R. (2008) Fluorescent single-stranded DNA binding protein as a probe for sensitive, real time assays of helicase activity. Biophys. J. 95, 3330-3339.
20. Webb, M. R. (2003) A Fluorescent Sensor to Assay Inorganic Phosphate, in Kinetic Analysis: A Practical Approach (Johnson, K. A., Ed.) pp 131-152, Oxford University Press, Oxford, U.K.
21. Brune, M., Hunter, J. L., Howell, S. A., Martin, S. R., Hazlett, T. L., Corrie, J. E. T., and Webb, M. R. (1998) Mechanism of inorganic phosphate interaction with phosphate binding protein from Escherichia coli. Biochemistry 37, 10370-10380.
22. Jacques, L. B. (1977) Determination of heparin and related sulfated mucopolysaccharides. Methods Biochem. Anal. 24, 203-312.
23. Brownbridge, G. G., Lowe, P. N., Moore, K. J. M., Skinner, R. H., and Webb, M. R. (1993) Interaction of GTPase activating proteins (GAPs) with p21ras measured by a novel fluorescence anisotropy method. Essential role of Arg-903 of GAP in activation of GTP hydrolysis on p21ras. J. Biol. Chem. 268, 10914-10919.
24. Leatherbarrow, R. J. (2001) Grafit Version 5 , Erithacus Software Ltd., Horley, U.K.
25. Eccleston, J. F., Hutchinson, J. P., and White, H. D. (2001) Stopped-Flow Techniques, in Protein Ligand Interactions: Structure and Spectroscopy. A Practical Approach Series (Harding, S. E., and Chowdry, B. Z., Eds.) pp 201-237, Oxford University Press, Oxford, U.K.
26. Dillingham, M. S., Wigley, D. B., and Webb, M. R. (2002) Direct measurement of single stranded DNA translocation by PcrA helicase using the fluorescent base analogue 2-aminopurine. Biochemistry 41, 643-651.
27. Martinez-Senac, M. M., and Webb, M. R. (2005) Mechanism of translocation and kinetics of DNA unwinding by the helicase RecG. Biochemistry 44, 16967-16976.
28. Zhang, W., Dillingham, M. S., Thomas, C. D., Allen, S., Roberts, C. J., and Soultanas, P. (2007) Directional loading and stimulation of PcrA helicase by the replication initiator protein RepD. J. Mol. Biol. 371, 336-348.
29. Tomko, E. J., Fischer, C. J., Niedziela-Majka, A., and Lohman, T. M. (2007) A nonuniform stepping mechanism for E. coli UvrD monomer translocation along single-stranded DNA. Mol. Cell 26, 335-347
30. Cheng, W., Brendza, K. M., Gauss, G. H., Korolev, S., Waksman, G., and Lohman, T. M. (2002) The 2B domain of the Escherichia coli Rep protein is not required for DNA helicase activity. Proc. Natl. Acad. Sci. U.S.A. 99, 16006-16011
31. Khan, S. A., Carleton, S. M., and Novick, R. P. (1981) Replication of plasmid pT181 DNA in vitro: requirement for a plasmid-encoded product. Proc. Natl. Acad. Sci. U.S.A. 78, 4902-4906.
32. Bruck, I., Georgescu, R. E., and O'Donnell, M. (2005) Conserved interactions in the Staphylococcus aureus DNA PolC chromosome replication machine. J. Biol. Chem. 280, 18152-18162.