Quantitative analysis of the kinetics of end-dependent disassembly of RecA filaments from ssDNA

Journal of Molecular Biology

Volumn 288, Issue 3, 1999, Pages 391-401

  Arenson, Tanya A ^a   Tsodikov, Oleg V ^a   Cox, Michael M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Assembly; Disassembly; Filament; Kinetic analysis; RecA protein

Indexed keywords

ADENOSINE TRIPHOSPHATE; RECA PROTEIN; SINGLE STRANDED DNA;

ARTICLE; HYDROLYSIS; MOLECULAR MODEL; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN ASSEMBLY;

EID: 0033531964     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.2705     Document Type: Article

References (50)

1. Anderson D. G., Kowalczykowski S. C. The recombination hot spot chi is a regulatory element that switches the polarity of DNA degradation by the RecBCD enzyme. Genes Dev. 11:1997a;571-581.
2. Anderson D. G., Kowalczykowski S. C. The translocating RecBCD enzyme stimulates recombination by directing RecA protein onto ssDNA in a chi-regulated manner. Cell. 90:1997b;77-86.
3. Bedale W. A., Cox M. Evidence for the coupling of ATP hydrolysis to the final (extension) phase of RecA protein-mediated DNA strand exchange. J. Biol. Chem. 271:1996;5725-5732.
4. Brendel V., Brocchieri L., Sandler S. J., Clark A. J., Karlin S. Evolutionary comparisons of RecA-like proteins across all major kingdoms of living organisms. J. Mol. Evol. 44:1997;528-541.
5. Brenner S. L., Mitchell R. S., Morrical S. W., Neuendorf S. K., Schutte B. C., Cox M. M. RecA protein-promoted ATP hydrolysis occurs throughout RecA nucleoprotein filaments. J. Biol. Chem. 262:1987;4011-4016.
6. Brenner S. L., Zlotnick A., Griffith J. D. RecA protein self-assembly. Multiple discrete aggregation states. J. Mol. Biol. 204:1988;959-972.
7. Brenner S. L., Zlotnick A., Stafford W. F. RecA protein self-assembly. 2. analytical equilibrium ultracentrifugation studies of the entropy-driven self-association of RecA. J. Mol. Biol. 216:1990;949-964.
8. Chabbert M., Cazenave C., Helene C. Kinetic studies of RecA protein binding to a fluorescent single-stranded polynucleotide. Biochemistry. 26:1987;2218-2225.
9. Cox M. M. A broadening view of recombinational DNA repair in bacteria. Genes Cells. 3:1998;65-78.
10. Cox M. M., McEntee K., Lehman I. R. A simple and rapid procedure for the large scale purification of the RecA protein of Escherichia coli. J. Biol. Chem. 256:1981;4676-4678.
11. Craig N. L., Roberts J. W. Function of nucleoside triphosphate and polynucleotide in Escherichia coli recA protein-directed cleavage of phage lambda repressor. J. Biol. Chem. 256:1981;8039-8044.
12. Dixon D. A., Kowalczykowski S. C. Homologous pairing in vitro stimulated by the recombination hotspot, Chi. Cell. 66:1991;361-371.
13. Dutreix M., Rao B. J., Radding C. M. The effects on strand exchange of 5′versus 3′ ends of single-stranded DNA in RecA nucleoprotein filaments. J. Mol. Biol. 219:1991;645-654.
14. Griffith J. D., Harris L. D. DNA strand exchanges. CRC Crit. Rev. Biochem. 23:1988;S43-S86.
15. Johnson M. L., Frasier S. G. Nonlinear least squares analysis. Methods Enzymol. 117:1985;301-342.
16. Konforti B. B., Davis R. W. DNA substrate requirements for stable joint molecule formation by the RecA and single-stranded DNA-binding proteins ofEscherichia coli. J. Biol. Chem. 266:1991;10112-10121.
17. Kowalczykowski S. C., Eggleston A. K. Homologous pairing and DNA strand-exchange proteins. Annu. Rev. Biochem. 63:1994;991-1043.
18. Kowalczykowski S. C., Clow J., Somani R., Varghese A. Effects of the Escherichia coli SSB protein on the binding of Escherichia coli RecA protein to single-stranded DNA. Demonstration of competitive binding and the lack of a specific protein-protein interaction. J. Mol. Biol. 193:1987;81-95.
19. Lee J. W., Cox M. M. Inhibition of RecA protein-promoted ATP hydrolysis. I. ATPγS and ADP are antagonistic inhibitors. Biochemistry. 29:1990;7666-7676.
20. Lindsley J. E., Cox M. M. Dissociation pathway for RecA nucleoprotein filaments formed on linear duplex DNA. J. Mol. Biol. 205:1989;695-711.
21. Lindsley J. E., Cox M. M. Assembly and disassembly of RecA protein filaments occurs at opposite filament ends: relationship to DNA strand exchange. J. Biol. Chem. 265:1990;9043-9054.
22. Lohman T. M., Overman L. B. Two binding modes in Escherichia coli single strand binding protein-single stranded DNA complexes. Modulation by NaCl concentration. J. Biol. Chem. 260:1985;3594-3603.
23. Madiraju M. V., Lavery P. E., Kowalczykowski S. C., Clark A. J. Enzymatic properties of the RecA803 protein, a partial suppressor of recF mutations. Biochemistry. 31:1992;10529-10535.
24. Masui R., Mikawa T., Kato R., Kuramitsu S. Characterization of the oligomeric states of RecA protein: monomeric RecA protein can form a nucleoprotein filament. Biochemistry. 37:1998;14788-14797.
25. Menetski J. P., Kowalczykowski S. C. Interaction of RecA protein with single-stranded DNA. Quantitative aspects of binding affinity modulation by nucleotide cofactors. J. Mol. Biol. 181:1985;281-295.
26. Menge K. L., Bryant F. R. ATP-stimulated hydrolysis of GTP by RecA protein: kinetic consequences of cooperative RecA protein-ATP interactions. Biochemistry. 27:1988;2635-2640.
27. Meselson M. S., Radding C. M. A general model for genetic recombination. Proc. Natl Acad. Sci. USA. 72:1975;358-361.
28. Messing J. New M13 vectors for cloning. Methods Enzymol. 101:1983;20-78.
29. Mikawa T., Masui R., Kuramitsu S. RecA protein has extremely high cooperativity for substrate in its ATPase activity. J. Biochem. 123:1998;450-457.
30. Morrical S. W., Cox M. M. Light scattering studies of the recA protein of Escherichia coli: relationship between freerecA filaments and the recA ?ssDNA complex. Biochemistry. 24:1985;760-767.
31. Morrical S. W., Lee J., Cox M. M. Continuous association of Escherichia coli single-stranded DNA binding protein with stable complexes of RecA protein and single-stranded DNA. Biochemistry. 25:1986;1482-1494.
32. Muench K. A., Bryant F. R. Disruption of an ATP-dependent isomerization of the recA protein by mutation of histidine 163. J. Biol. Chem. 266:1991;844-850.
33. Neuendorf S. K., Cox M. M. Exchange of RecA protein between adjacent RecA protein-single-stranded DNA complexes. J. Biol. Chem. 261:1986;8276-8282.
34. Nguyen T. T., Muench K. A., Bryant F. R. Inactivation of the recA protein by mutation of histidine 97 or lysine 248 at the subunit interface. J. Biol. Chem. 268:1993;3107-3113.
35. Pugh B. F., Cox M. M. General mechanism for RecA protein binding to duplex DNA. J. Mol. Biol. 203:1988;479-493.
36. Register J. C. III, Griffith J. The direction of RecA protein assembly onto single strand DNA is the same as the direction of strand assimilation during strand exchange. J. Biol. Chem. 260:1985;12308-12312.
37. Rehrauer W. M., Kowalczykowski S. C. Alteration of the nucleoside triphosphate (NTP) catalytic domain within Escherichia coli recA protein attenuates NTP hydrolysis but not joint molecule formation. J. Biol. Chem. 268:1993;1292-1297.
38. Resnick M. A. The repair of double-strand breaks in DNA; a model involving recombination. J. Theor. Biol. 59:1976;97-106.
39. Roca A. I., Cox M. M. RecA protein: structure, function, and role in recombinational DNA repair. Prog. Nucl. Acid Res. Mol. Biol. 56:1997;129-223.
40. Schutte B. C., Cox M. M. Homology-dependent changes in adenosine 5′-triphosphate hydrolysis during RecA protein promoted DNA strand exchange: evidence for long paranemic complexes. Biochemistry. 26:1987;5616-5625.
41. Shan Q., Cox M. M. RecA protein dynamics in the interior of RecA nucleoprotein filaments. J. Mol. Biol. 257:1996;756-774.
42. Shan Q., Cox M. M. RecA filament dynamics during DNA strand exchange reactions. J. Biol. Chem. 272:1997;11063-11073.
43. Shan Q., Bork J. M., Webb B. L., Inman R. B., Cox M. M. RecA protein filaments: end-dependent dissociation from ssDNA and stabilization by RecO and RecR proteins. J. Mol. Biol. 265:1997;519-540.
44. Smith G. R. Conjugational recombination in E. coli: myths and mechanisms. Cell. 64:1991;19-27.
45. Szostak J. W., Orr W. T. L., Rothstein R. J., Stahl F. W. The double-strand-break repair model for recombination. Cell. 33:1983;25-35.
46. Tracy R. B., Kowalczykowski S. C. In vitro selection of preferred DNA pairing sequences by the Escherichia coli RecA protein. Genes Dev. 10:1996;1890-1903.
47. Umezu K., Kolodner R. D. Protein interactions in genetic recombination in Escherichia coli. Interactions involving RecO and RecR overcome the inhibition of RecA by single-stranded DNA-binding protein. J. Biol. Chem. 269:1994;30005-30013.
48. Webb B. L., Cox M. M., Inman R. B. Recombinational DNA repair-the RecF and RecR proteins limit the extension of RecA filaments beyond single-strand DNA gaps. Cell. 91:1997;347-356.
49. Wegner A. Treadmilling of actin at physiological salt concentrations. An analysis of the critical concentrations of actin filaments. J. Mol. Biol. 161:1982;607-615.
50. Weinstock G. M., McEntee K., Lehman I. R. Hydrolysis of nucleoside triphosphates catalyzed by the recA protein of Escherichia coli. Characterization of ATP hydrolysis. J. Biol. Chem. 256:1981;8829-8834.