Fluorescent single-stranded DNA binding protein as a probe for sensitive, real-time assays of helicase activity

Biophysical Journal

Volumn 95, Issue 7, 2008, Pages 3330-3339

  Dillingham, Mark S ^a   Tibbles, Katherine L ^b   Hunter, Jackie L ^b   Bell, Jason C ^c   Kowalczykowski, Stephen C ^c   Webb, Martin R ^b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COUMARIN DERIVATIVE; DNA BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; FLUORESCENT DYE; HELICASE; SINGLE STRANDED DNA; SSB PROTEIN, E COLI; TRYPTOPHAN;

ARTICLE; BIOASSAY; CHEMISTRY; ENZYME SPECIFICITY; FLUORESCENCE; KINETICS; METABOLISM; METHODOLOGY; OSMOLARITY; TIME;

BIOLOGICAL ASSAY; COUMARINS; DNA HELICASES; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; ESCHERICHIA COLI PROTEINS; FLUORESCENCE; FLUORESCENT DYES; KINETICS; OSMOLAR CONCENTRATION; SUBSTRATE SPECIFICITY; TIME FACTORS; TRYPTOPHAN;

EID: 55949111485     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.133512     Document Type: Article

References (38)

1. Singleton, M. R., M. S. Dillingham, and D. B. Wigley. 2007. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 76:23-50.
2. Myong, S., M. M. Bruno, A. M. Pyle, and T. Ha. 2007. Spring-loaded mechanism of DNA unwinding by hepatitis C virus NS3 helicase. Science. 317:513-516.
3. Martinez-Senac, M. M., and M. R. Webb. 2005. Mechanism of translocation and kinetics of DNA unwinding by the helicase RecG. Biochemistry. 44:16967-16976.
4. Lucius, A. L., C. J. Wong, and T. M. Lohman. 2004. Fluorescence stopped-flow studies of single turnover kinetics of E. coli RecBCD helicase-catalyzed DNA unwinding. J. Mol. Biol. 339:731-750.
5. Roman, L. J., and S. C. Kowalczykowski. 1989. Characterization of the helicase activity of the Escherichia coli RecBCD enzyme using a novel helicase assay. Biochemistry. 28:2863-2873.
6. Eggleston, A. K., N. A. Rahim, and S. C. Kowalczykowski. 1996. A helicase assay based on the displacement of fluorescent, nucleic acid-binding ligands. Nucleic Acids Res. 24:1179-1186.
7. Rye, H. S., M. A. Quesada, K. Peck, R. A. Mathies, and A. N. Giazer. 1991. High-sensitivity two-color detection of double-stranded DNA with a confocal fluorescence gel scanner using ethidium homodimer and thiazole orange. Nucleic Acids Res. 19:327-333.
8. Webb, M. R. 2007. Development of fluorescent biosensors for probing the function of motor proteins. Mol. Biosyst. 3:249-256.
9. Dwyer, M. A., and H. W. Hellinga. 2004. Periplasmic binding proteins: a versatile superfamily for protein engineering. Curr. Opin. Struct. Biol. 14:495-504.
10. Moschou, E. A., L. G. Bachas, S. Daunert, and S. K. Deo. 2006. Hinge-motion binding proteins: unraveling their analytical potential. Anal. Chem. 78:6692-6700.
11. Brune, M., J. L. Hunter, S. A. Howell, S. R. Martin, T. L. Hazlett, J. E. T. Corrie, and M. R. Webb. 1998. Mechanism of inorganic phosphate interaction with phosphate binding protein from Escherichia coli. Biochemistry. 37:10370-10380.
12. Tolosa, L., I. Gryczynski, L. R. Eichhorn, J. D. Dattelbaum, F. N. Castellano, G. Rao, and J. R. Lakowicz. 1999. Glucose sensor for low-cost lifetime-based sensing using a genetically engineered protein. Anal. Biochem. 267:114-120.
13. Dattelbaum, J. D., L. L. Looger, D. E. Benson, K. M. Sali, R. B. Thompson, and H. W. Hellinga. 2005. Analysis of allosteric signal transduction mechanisms in an engineered fluorescent maltose biosensor. Protein Sci. 14:284-291.
14. Raghunathan, S., A. G. Kozlov, T. M. Lohman, and G. Waksman. 2000. Structure of the DNA binding domain of E. coli SSB bound to ssDNA. Nat. Struct. Biol. 7:648-652.
15. Raghunathan, S., C. S. Ricard, T. M. Lohman, and G. Waksman. 1997. Crystal structure of the homo-tetrameric DNA binding domain of Escherichia coli single-stranded DNA-binding protein determined by multiwavelength x-ray diffraction on the selenomethionyl protein at 2.9-A resolution. Proc. Natl. Acad. Sci. USA. 94:6652-6657.
16. Lohman, T. M., and M. E. Ferrari. 1994. Escherichia Coli single-stranded DNA-binding protein: multiple DNA-binding modes and cooperativities. Annu. Rev. Biochem. 63:527-570.
17. Kuznetsov, S. V., A. G. Kozlov, T. M. Lohman, and A. Ansari. 2006. Microsecond dynamics of protein-DNA interactions: direct observation of the wrapping/unwrapping kinetics of single-stranded DNA around the E. coli SSB tetramer. J. Mol. Biol. 359:55-65.
18. Molineux, I. J., A. Pauli, and M. L. Gefter. 1975. Physical studies of the interaction between the Escherichia coli DNA binding protein and nucleic acids. Nucleic Acids Res. 2:1821-1837.
19. Liu, J., N. Qian, and S. W. Morrical. 2006. Dynamics of bacteriophage T4 presynaptic filament assembly from extrinsic fluorescence measurements of Gp32-single-stranded DNA interactions. J. Biol. Chem. 281:26308-26319.
20. Yeeles, J. T. P., and M. S. Dillingham. 2007. A dual-nuclease mechanism for DNA break processing by AddAB-type helicase-nucleases. J. Mol. Biol. 371:66-78.
21. Singleton, M. R., M. S. Dillingham, M. Gaudier, S. C. Kowalczykowski, and D. B. Wigley. 2004. Crystal structure of RecBCD enzyme reveals a machine for processing DNA breaks. Nature. 432:187-193.
22. Zhang, W., M. S. Dillingham, C. D. Thomas, S. Allen, C. J. Roberts, and P. Soultanas. 2007. Directional loading and stimulation of PcrA helicase by the replication initiator protein RepD. J. Mol. Biol. 371:336-348.
23. Corrie, J. E. T. 1994. Thiol-reactive fluorescent probes for protein labelling. J. Chem. Soc. [Perkin 1] :2975-2982.
24. Munasinghe, V. R. N., and J. E. T. Corrie. 2006. Optimised synthesis of 6-iodoacetamidotetramethylrhodamine. ARKIVOC. (ii):143-149.
25. Lohman, T. M., J. M. Green, and R. S. Beyer. 1986. Large-scale overproduction and rapid purification of the Escherichia coli ssb gene product. Expression of the ssb gene under lambda PL control. Biochemistry. 25:21-25.
26. Fletcher, A. N., and D. E. Bliss. 1978. Laser dye stability. Part 5. Effect of chemical substituents of bicyclic dyes upon photodegradation parameters. Appl. Phys. 16:289-295.
27. Leatherbarrow, R. J. 2001. Grafit Version 5. Erithacus Software Ltd., Horley, UK.
28. Webb, M. R., and J. E. T. Corrie. 2001. Fluorescent coumarin-labeled nucleotides to measure ADP release from actomyosin. Biophys. J. 81:1562-1569.
29. Thomas, C. D., D. F. Balson, and W. V. Shaw. 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.
30. Soultanas, P., M. S. Dillingham, F. Papadopoulos, S. E. Phillips, C. D. Thomas, and D. B. Wigley. 1999. Plasmid replication initiator protein RepD increases the processivity of PcrA DNA helicase. Nucleic Acids Res. 27:1421-1428.
31. Bianco, P. R., L. R. Brewer, M. Corzett, R. Balhorn, Y. Yeh, S. C. Kowalczykowski, and R. J. Baskin. 2001. Processive translocation and DNA unwinding by individual RecBCD enzyme molecules. Nature. 409:374-377.
32. Dillingham, M. S., M. R. Webb, and S. C. Kowalczykowski. 2005. Bipolar DNA translocation contributes to highly processive DNA unwinding by RecBCD enzyme. J. Biol. Chem. 280:37069-37077.
33. Chedin, F., and S. C. Kowalczykowski. 2002. A novel family of regulated helicases/nucleases from Gram-positive bacteria: insights into the initiation of DNA recombination. Mol. Microbiol. 43:823-834.
34. Kozlov, A. G., and T. M. Lohman. 2002. Stopped-flow studies of the kinetics of single-stranded DNA binding and wrapping around the Escherichia coli SSB tetramer. Biochemistry. 41:6032-6044.
35. Akerman, B., and E. Tuite. 1996. Single- and double-strand photo-cleavage of DNA by YO, YOYO and TOTO. Nucleic Acids Res. 24:1080-1090.
36. OhUigin, C., D. J. McConnell, J. M. Kelly, and W. J. M. van der Putten. 1987. Methylene blue photosensitised strand cleavage of DNA: effects of dye binding and oxygen. Nucleic Acids Res. 15:7411-7427.
37. Carisson, C., M. Johnson, and B. Akerman. 1995. Double bands in DNA gel electrophoresis caused by bis-intercalating dyes. Nucleic Acids Res. 23:2413-2420.
38. Brune, M., J. L. Hunter, J. E. T. Corrie, and M. R. Webb. 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.