RecA protein filaments: End-dependent dissociation from ssDNA and stabilization by RecO and RecR proteins

Journal of Molecular Biology

Volumn 265, Issue 5, 1997, Pages 519-540

  Shan, Qun ^a   Bork, Julie M ^a   Webb, Brian L ^a   Inman, Ross B ^a   Cox, Michael M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

DNA; Filament; RecA; Recombination; Repair

Indexed keywords

ADENOSINE TRIPHOSPHATE; CIRCULAR DNA; DEOXYADENOSINE TRIPHOSPHATE; DNA BINDING PROTEIN; RECA PROTEIN; SINGLE STRANDED DNA;

ARTICLE; CONTROLLED STUDY; DNA RECOMBINATION; DNA REPAIR; HYDROLYSIS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN STABILITY;

EID: 0031556955     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0748     Document Type: Article

References (76)

1. Bedale W. A., Cox M. 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.
2. Bochner B. R., Ames B. N. Complete analysis of cellular nucleotides by two-dimensional thin layer chromatography. J. Biol. Chem. 257:1982;9759-9769.
3. 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.
4. Brenner S. L., Zlotnick A., Griffith J. D. RecA protein self-assembly. Multiple discrete aggregation states. J. Mol. Biol. 204:1988;959-972.
5. Brenner S. L., Zlotnick A., Stafford W. F. RecA protein self-assembly. II. Analytical equilibrium ultracentrifugation studies of the entropy-driven self-association of RecA. J. Mol. Biol. 216:1990;949-964.
6. Chow S. A., Honigberg S. M., Radding C. M. DNase protection by RecA protein during strand exchange. Asymmetric protection of the Holliday structure. J. Biol. Chem. 263:1988;3335-3347.
7. Clark A. J. Toward a metabolic interpretation of genetic recombination of E. coli and its phages. Annu. Rev. Microbiol. 25:1971;437-464.
8. Clark A. J., Sandler S. J. Homologous genetic recombination: the pieces begin to fall into place. Crit. Rev. Microbiol. 20:1994;125-142.
9. Cox M. M. Why does RecA protein hydrolyze ATP. Trends Biochem Sci. 19:1994;217-222.
10. Cox M. M. Alignment of three (but not four) DNA strands in a RecA protein filament. J. Biol. Chem. 270:1995;26021-26024.
11. Cox M. M., Lehman I. R. RecA protein-promoted DNA strand exchange. Stable complexes of RecA protein and single-stranded DNA formed in the presence of ATP and single-stranded DNA binding protein. J. Biol. Chem. 257:1982;8523-8532.
12. Cox M. M., Soltis D. A., Lehman I. R., DeBrosse C., Benkovic S. J. ADP-mediated dissociation of stable complexes of RecA protein and single-stranded DNA. J. Biol. Chem. 258:1983;2586-2592.
13. 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.
14. Davis R. W., Botstein D., Roth J. R. Advanced Bacterial Genetics. 1980;Cold Spring Harbor, New York.
15. Dixon D. A., Kowalczykowski S. C. Homologous pairing in vitro stimulated by the recombination hotspot, Chi. Cell. 66:1991;361-371.
16. 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.
17. Guyer M. S., Reed R. R., Steitz J. A., Low K. B. Identification of a sex-factor-affinity site in E. coli as gamma delta. Cold Spring Harbor Symp. Quant. Biol. 45:1981;135-140.
18. Honigberg S. M., Gonda D. K., Flory J., Radding C. M. The pairing activity of stable nucleoprotein filaments made from RecA protein, single-stranded DNA, and adenosine 5′-(γ-thio)triphosphate. J. Biol. Chem. 260:1985;11845-11851.
19. Kolodner R., Fishel R. A., Howard M. Genetic recombination of bacterial plasmid DNA: effect of RecF pathway mutations on plasmid recombination in Escherichia coli. J. Bacteriol. 163:1985;1060-1066.
20. Konforti B. B., Davis R. W. The preference for a 3′ homologous end is intrinsic to RecA-promoted strand exchange. J. Biol. Chem. 265:1990;6916-6920.
21. Konforti B. B., Davis R. W. DNA substrate requirements for stable joint molecule formation by the RecA and single-stranded DNA-binding proteins of Escherichia coli. J. Biol. Chem. 266:1991;10112-10121.
22. Konforti B. B., Davis R. W. ATP hydrolysis and the displaced strand are two factors that determine the polarity of RecA-promoted DNA strand exchange. J. Mol. Biol. 227:1992;38-53.
23. Kowalczykowski S. C. In vitro reconstitution of homologous recombination reactions. Experientia. 50:1994;204-215.
24. Kowalczykowski S. C., Eggleston A. K. Homologous pairing and DNA strand-exchange proteins. Annu. Rev. Biochem. 63:1994;991-1043.
25. Kowalczykowski S. C., Krupp R. A. Effects of Escherichia coli SSB protein on the single-stranded DNA-dependent ATPase activity of Escherichia coli RecA protein. Evidence that SSB protein facilitates the binding of RecA protein to regions of secondary structure within single-stranded DNA. J. Mol. Biol. 193:1987;97-113.
26. Kowalczykowski S. C., Dixon D. A., Eggleston A. K., Lauder S. D., Rehrauer W. M. Biochemistry of homologous recombination in Escherichia coli. Microbiol. Rev. 58:1994;401-465.
27. Lee J. W., Cox M. M. Inhibition of RecA protein-promoted ATP hydrolysis. I. ATPγS and ADP are antagonistic inhibitors. Biochemistry. 29:1990a;7666-7676.
28. Lee J. W., Cox M. M. Inhibition of RecA protein-promoted ATP hydrolysis. II. Longitudinal assembly and disassembly of RecA protein filaments mediated by ATP and ADP. Biochemistry. 29:1990b;7677-7683.
29. Lindsley J. E., Cox M. M. Dissociation pathway for RecA nucleoprotein filaments formed on linear duplex DNA. J. Mol. Biol. 205:1989;695-711.
30. 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. 265:1990a;9043-9054.
31. Lindsley J. E., Cox M. M. On RecA protein-mediated homologous alignment of 2 DNA molecules - 3 strands versus 4 strands. J. Biol. Chem. 265:1990b;10164-10171.
32. Lohman T. M., Overman L. B. Two binding modes in Escherichia col i single strand binding protein-single stranded DNA complexes. Modulation by NaCl concentration. J. Biol. Chem. 260:1985;3594-3603.
33. Lcontrol. Biochemistry. 25:1986;21-25.
34. Lohman T. M., Chao K., Green J. M., Sage S., Runyon G. T. Large-scale purification and characterization of the Escherichia coli rep gene product. J. Biol. Chem. 264:1989;10139-10147.
35. Luisi-DeLuca C., Kolodner R. Purification and characterization of the Escherichia coli RecO protein. Renaturation of complementary single-stranded DNA molecules catalyzed by the RecO protein. J. Mol. Biol. 236:1994;124-138.
36. Mahdi A. A., Lloyd R. G. Identification of the recR locus of Escherichia coli K-12 and analysis of its role in recombination and DNA repair. Mol. Gen. Genet. 216:1989a;503-510.
37. Mahdi A. A., Lloyd R. G. The recR locus of Escherichia coli K-12: molecular cloning, DNA sequencing and identification of the gene product. Nulc. Acids Res. 17:1989b;6781-6794.
38. Marrione P. E., Cox M. M. RuvB protein-mediated ATP hydrolysis: functional asymmetry in the RuvB hexamer. Biochemistry. 34:1995;9809-9818.
39. Menetski J. P., Kowalczykowski S. C. Transfer of recA protein from one polynucleotide to another. Effect of ATP and determination of the processivity of ATP hydrolysis during transfer. J. Biol. Chem. 262:1987a;2093-2100.
40. Menetski J. P., Kowalczykowski S. C. Transfer of RecA protein from one polynucleotide to another. Kinetic evidence for a ternary intermediate during the transfer reaction. J. Biol. Chem. 262:1987b;2085-2092.
41. Menetski J. P., Kowalczykowski S. C. Enhancement of Escherichia coli RecA protein enzymatic function by dATP. Biochemistry. 28:1989;5871-5881.
42. Menetski J. P., Varghese A., Kowalczykowski S. C. Properties of the high-affinity single-stranded DNA binding state of the Escherichia coli RecA protein. Biochemistry. 27:(1988;1205-1212.
43. Menetski J. P., Bear D. G., Kowalczykowski S. C. Stable DNA heteroduplex formation catalyzed by the Escherichia coli RecA protein in the absence of ATP hydrolysis. Proc. Natl Acad. Sci. USA, 87:(1990;21-25.
44. Messing J. New M13 vectors for cloning. Methods Enzymol. 101:1983;20-78.
45. 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.
46. Morrison P. T., Lovett S. T., Gilson L. E., Kolodner R. Molecular analysis of the Escherichia coli recO gene. J. Bacteriol. 171:1989;3641-3649.
47. Muniyappa K., Williams K., Chase J. W., Radding C. M. Active nucleoprotein filaments of single-stranded binding protein and RecA protein on single-stranded DNA have a regular repeating structure. Nucl. Acids Res. 18:1990;3967-3973.
48. 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.
49. Ogawa T., Yu X., Shinohara A., Egelman E. H. Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science. 259:1993;1896-1899.
50. Phillips G. J., Prasher D. C., Kushner S. R. Physical and biochemical characterization of cloned sbcB and xonA mutations from Escherichia coli K-12. J. Bacteriol. 170:1988;2089-2094.
51. Pugh B. F., Cox M. M. Stable binding of RecA protein to duplex DNA. Unraveling a paradox. J. Biol. Chem. 262:1987;1326-1336.
52. Pugh B. F., Cox M. M. General mechanism for RecA protein binding to duplex DNA. J. Mol. Biol. 203:1988;479-493.
53. Pugh B. F., Schutte B. C., Cox M. M. Extent of duplex DNA underwinding induced by RecA protein binding in the presence of ATP. J. Mol. Biol. 205:1989;487-492.
54. Razavy H., Szigety S. K., Rosenberg S. M. Evidence for both 3′ and 5′ single-strand DNA ends in intermediates in Chi-stimulated recombination in vivo. Genetics. 142:1996;133-339.
55. 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.
56. Register J. C., III, Griffith J. Direct visualization of RecA protein binding to and unwinding duplex DNA following the D-loop cycle. J. Biol. Chem. 263:1988;11029-11032.
57. 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.
58. Roca A. I., Cox M. M. The RecA protein: structure and function. CRC Crit. Rev. Biochem. Mol Biol. 25:1990;415-456.
59. Roca A. I., Cox M. M. RecA protein: structure, function, and role in recombinational DNA repair. Prog. Nucl. Acids Res. Mol. Biol. 56:1996;in press.
60. Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning: A Laboratory Manual. 1989;Cold Spring Harbor, NY.
61. Shan Q., Cox M. M. RecA protein dynamics in the interior of RecA nucleoprotein filaments. J. Mol. Biol. 257:1996;756-774.
62. 2+requirements. J. Biol. Chem. 271:1996;5712-5724.
63. Shaner S. L., Radding C. M. Translocation of Escherichia coli RecA protein from a single-stranded tail to contiguous duplex DNA. J. Biol. Chem. 262:1987;9211-9219.
64. Shaner S. L., Flory J., Radding C. M. The distribution of Escherichia coli recA protein bound to duplex DNA with single-stranded ends. J. Biol. Chem. 262:1987;9220-9230.
65. Smith G. R. Homologous recombination in E. coli: multiple pathways for multiple reasons. Cell. 58:1989;807-809.
66. Smith G. R. Hotspots of homologous recombination. (A Review). Experientia. 50:1994;234-241.
67. Soltis D. A., Lehman I. R. RecA protein promoted DNA strand exchange. Isolation of recA protein-DNA complexes formed in the presence of single-stranded DNA binding protein. J. Biol. Chem. 258:1983;6073-6077.
68. Stasiak A., Egelman E. H., Howard-Flanders P. Structure of helical RecA-DNA complexes. III. The structural polarity of RecA filaments and functional polarity in the RecA-mediated strand exchange reaction. J. Mol. Biol. 202:(1988;659-662.
69. Sung P. Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science. 265:1994;1241-1243.
70. Thresher R. J., Christiansen G., Griffith J. D. Assembly of presynaptic filaments. Factors affecting the assembly of RecA protein onto single-stranded DNA. J. Mol. Biol. 201:1988;101-113.
71. Ullsperger C. J., Cox M. M. Quantitative RecA protein binding to the hybrid duplex product of DNA strand exchange. Biochemistry. 34:1995;10859-10866.
72. 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.
73. Webb B. L., Cox M. M., Inman R. B. An interaction between the Escherichia coli RecF and RecR proteins dependent on ATP and double-stranded DNA. J. Biol. Chem. 270:1995;31397-31404.
74. Wegner A. Head to tail polymerization of actin. J. Mol. Biol. 108:1976;139-150.
75. West S. C. Enzymes and molecular mechanisms of genetic recombination. Annu. Rev. Biochem. 61:1992;603-640.
76. Zyskind J. W., Svitil A. L., Stine W. B., Biery M. C., Smith D. W. RecA protein of Escherichia coli and chromosome partitioning. Mol. Microbiol. 6:1992;2525-2537.