Dissociation kinetics of RecA protein-three-stranded DNA complexes reveals a low fidelity of RecA-assisted recognition of homology

Journal of Molecular Biology

Volumn 278, Issue 2, 1998, Pages 317-330

  Malkov, Vladislav A ^a   Camerini Otero, R Daniel ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Dissociation kinetics; Fidelity; RecA; Three stranded DNA

Indexed keywords

ADENOSINE TRIPHOSPHATE; HETERODUPLEX; OLIGONUCLEOTIDE; RECA PROTEIN; RESTRICTION ENDONUCLEASE; SINGLE STRANDED DNA;

ARTICLE; CONTROLLED STUDY; DISSOCIATION; DNA PROTEIN COMPLEX; DNA STRUCTURE; DNA SUPERCOILING; HYDROLYSIS; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SYNAPSE;

EID: 0032080009     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.1706     Document Type: Article

References (57)

1. Aboul-ela, F., Koh, D. & Tinoco, I. (1985). Base-base mismatches. Thermodynamics of double helix formation for dCAAAXAAAG + dCTTTYTTTC (X, Y = A, C, G, T). Nucl. Acids Res. 13, 4811-4824.
2. Adzuma, K. (1992). Stable synapsis of homologous DNA molecules mediated by the E. coli RecA protein involves local exchange of DNA strands. Genes Dev. 6, 1679-1694.
3. Balatskaya, S. V., Belotserkovskii, B. P. & Johnston, B. H. (1996). Alternate-strand triplex formation: modulation of binding to matched and mismatched duplexes by sequence choice in the Pu-Pu-Py block. Biochemistry, 35, 13328-13337.
4. Baumann, P., Benson, F. E. & West, S. C. (1996). Human RadSl protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell, 87, 757-766.
5. Bazemore, L. R., Folta-Stogniew, E., Takahashi, M. & Radding, C. M. (1997). RecA tests homology at both pairing and strand exchange. Proc. Natl Acad. Sci. USA, 94, 11863-11868.
6. Beal, P. A. & Dervan, P. B. (1992). The influence of single base triplet changes on the stability of a Pu. Pu. Py triple helix determined by affinity cleaving. Nucl. Acids Res. 20, 2773-2776.
7. Belotserkovskii, B. P., Veselkov, A. G., Fillipov, S. A., Dobrynin, V. N., Mirkin, S. M. & Frank-Kamenetskii, M. D. (1990). Formation of intramolecular triplex in homopurine-homopyrimidine mirror repeats with point substitutions. Nucl. Acids Res. 18, 6621-6624.
8. Benson, F. E., Stasiak, A. & West, S. C. (1994). Purification and characterization of the human Rad51 protein, an analogue of E. coli RecA. EMBO J. 13, 5764-5771.
9. Bianchi, M. E. & Radding, C. M. (1983). Insertions, deletions and mismatches in heteroduplex DNA made by RecA protein. Cell, 35, 511-520.
10. Camerini-Otero, R. D. & Hsieh, P. (1993). Parallel DNA triplexes, homologous recombination, and other homology-dependent DNA interactions. Cell, 73, 217-223.
11. Camerini-Otero, R. D. & Hsieh, P. (1995). Homologous recombination proteins in prokaryotes and eukaryotes. Annu. Rev. Genet. 29, 509-552.
12. Cate, J. H., Gooding, A. R., Podell, E., Zhou, K., Golden, B. L., Kundrot, C. E., Cech, T. R. & Doubna, J. A. (1996). Crystal structure of a group I rybozime domain: principles of RNA packing. Science, 273, 1678-1685.
13. Chiu, S. K., Rao, B. J., Story, R. M. & Radding, C. M. (1993). Interactions of three strands in joints made by RecA protein. Biochemistry, 32, 13146-55.
14. Cox, M. M. (1995). Alignment of 3 (but not 4) DNA strands within a RecA protein filament. J. Biol. Chem. 270, 26021-26024.
15. Cox, M. M. & Lehman, I. R. (1981). Directionality and polarity in recA protein-promoted branch migration. Proc. Natl Acad. Sci. USA, 78, 6018-6022.
16. Egelman, E. H. & Stasiak, A. (1986). Structure of helical RecA-DNA complexes. Complexes formed in the presence of ATP-γ-S or ATP. J. Mol. Biol. 191, 677-697.
17. Egelman, E. H. & Yu, X. (1989). The location of DNA in RecA-DNA helical filaments. Science, 245, 404-407.
18. Ellouze, C., Norden, B. & Takahashi, M. (1997). Dissociation of non-complementary second DNA from RecA filament without ATP hydrolysis: mechanism of search for homologous DNA. J. Biochem. 121, 1070-1075.
19. Frank-Kamenetskii, M. D. & Mirkin, S. M. (1995). Triplex DNA Structures. Annu. Rev. Biochem. 64, 65-95.
20. Freund, J. E. (1962). Mathemtatical Statistics, pp. 308-314, Prentice-Hall, Inc., Englewood Cliffs, NJ.
21. Gaffney, B. L. & Jones, R. A. (1989). Thermodynamic comparison of the base pairs formed by the carcinogenic lesion O6-methylguanine with reference both the Watson-Crick pairs and to mismatched pairs. Biochemistry, 28, 5881-5889.
22. Herschlag, D. (1991). Implications of ribozyme kinetics for targeting the cleavage of specific RNA molecules in vivo: more isn't always better. Proc. Natl Acad. Sci. USA, 88, 6921-6925.
23. Howard-Flanders, P., West, S. C. & Stasiak, A. (1984). Role of RecA spiral filaments in genetic recombination. Nature, 309, 215-220.
24. Hsieh, P., Camerini-Otero, C. S. & Camerini-Otero, R. D. (1990). Pairing of homologous DNA sequences by proteins: evidence for three-stranded DNA. Genes Dev. 4, 1951-1963.
25. Hsieh, P., Camerini-Otero, C. S. & Camerini-Otero, R. D. (1992). The synapsis event in the homologous pairing of DNAs: RecA recognizes and pairs less than one helical repeat of DNA. Proc. Natl Acad. Sci. USA, 89, 6492-6496.
26. Jain, S. K., Cox, M. M. & Inman, R. B. (1994). On the role of ATP hydrolysis in RecA protein-mediated DNA strand exchange. III. Unidirectional branch migration and extensive hybrid DNA formation. J. Biol. Chem. 269, 20653-20661.
27. Kahn, R., Cunningham, R. P., DasGupta, C. & Radding, C. M. (1981). Polarity of heteroduplex formation promoted by E. coli recA protein. Proc. Natl Acad. Sci. USA, 78, 4786-4790.
28. Kim, J. I., Cox, M. M. & Inman, R. B. (1992). On the role of ATP hydrolysis in recA protein-mediated DNA strand exchange. I. Bypassing a short heterologous insert in one DNA substrate. J. Biol. Chem. 267, 16438-16443.
29. Kim, M. G., Zhurkin, V. B., Jernigan, R. L. & Camerini-Otero, R. D. (1995). Probing the structure of a putative intermediate in homologous recombination: the third strand in the parallel DNA triplex is in contact with the major groove of the duplex. J. Mol. Biol. 247, 874-889.
30. Kowalczykowski, S. C., Dixon, D. A., Eggleston, A. K., Lauder, S. D. & Rehrauer, W. M. (1994). Biochemistry of homologous recombination in E. coli. Microbiol. Rev. 58, 401-465.
31. Malkov, V. A., Sastry, L. & Camerini-Otero, R. D. (1997). RecA protein assisted selection reveals a low fidelity of recognition of homology in a duplex DNA by an oligonucleotide. J. Mol. Biol. 271, 168-177.
32. Mazin, A. V. & Kowalczykowski, S. C. (1996). The specificity of the secondary DNA binding site of RecA defines its role in DNA strand exchange. Proc. Natl Acad. Sci. USA, 93, 10673-10678.
33. Menetski, J. P., Bear, D. G. & Kowalczykowski, S. C. (1990). Stable DNA heteroduplex formation catalyzed by the E. coli RecA protein in the absence of ATP hydrolysis. Proc. Natl Acad. Sci. USA, 72, 21-25.
34. Nishinaka, T., Ito, Y., Yokoyama, S. & Shibata, T. (1997). An extended DNA structure through deoxyribosebase stacking induced by RecA protein. Proc. Natl Acad. Sci. USA, 24, 6623-6628.
35. Ogawa, T., Yu, X., Shinohara, A. & Egelman, E. H. (1993). Similarity of the yeast Rad51 filament to the bacterial RecA filament. Science, 259, 1896-1899.
36. *(GC) triplets. J. Mol. Biol. 231, 431-444.
37. Rao, B. J. & Radding, C. M. (1994). Formation of base triplets by non-Watson-Crick bonds mediates homologous recognition in RecA recombination filaments. Proc. Natl Acad. Sci. USA, 91, 6161-6165.
38. Rao, B. J. & Radding, C. M. (1995). RecA protein mediates homologous recognition via non-Watson-Crick bonds in base triplets. Phil. Trans. Roy. Soc. London Biol. Sci. 347, 5-12.
39. Roberts, R. W. & Crothers, D. M. (1991). Specificity and stringency in DNA triplex formation. Proc. Natl Acad. Sci. USA, 88, 9397-9401.
40. Roca, A. I. & Cox, M. M. (1997). RecA protein: structure, function, and role in recombinational DNA repair. Prog. Nucl. Acid Res. Mol. Biol. 56, 129-223.
41. Rosselli, W. & Stasiak, A. (1990). Energetics of RecA-mediated recombination reactions: without ATP hydrolysis RecA can mediate polar strand exchange but is unable to recycle. J. Mol. Biol. 216, 335-352.
42. Rosselli, W. & Stasiak, A. (1991). The ATPase activity of RecA is needed to push the DNA strand exchange through heterologous regions. EMBO J. 10, 4391-4396.
43. Rougee, M., Faucon, B., Mergny, J. L., Barcelo, F., Giovannangeli, C., Garestier, T. & Helene, C. (1992). Kinetics and thermodynamics of triple-helix formation: effects of ionic strength and mismatches. Biochemistry, 31, 9269-9278.
44. Spink, N., Nunn, C. M., Vojtechovsky, J., Berman, H. M. & Neidle, S. (1995). Crystal structure of a DNA decamer showing a novel pseudo four-way helix-helix junction. Proc. Natl Acad. Sci. USA, 92, 10767-10771.
45. Sung, P. (1994). Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science, 265, 1241-1243.
46. Sung, P. & Robberson, D. L. (1995). DNA strand exchange mediated by a Rad51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell, 82, 453-461.
47. Tracy, R. B. & Kowalczykowski, S. C. (1996). In vitro selection of preferred DNA pairing sequences by the E. coli RecA protein. Genes Dev. 10, 1890-1903.
48. *G base triplets. Nature, 374, 742-744.
49. 2 triple helix fragments in a crystal structure. Science, 273, 1702-1705.
50. Voloshin, O. N. & Camerini-Otero, R. D. (1997). The duplex DNA is very underwound in the three-stranded RecA protein-mediated synaptic complex. Genes Cells, 2, 303-314.
51. Werntges, H., Steger, G., Riesner, D. & Fritz, H.-J. (1986). Mismatches in DNA double strands: thermodynamic parameters and their correlation to repair efficiencies. Nucl. Acids Res. 14, 3773-3790.
52. West, S. C. (1992). Enzymes and molecular mechanisms of genetic recombination. Annu. Rev. Biochem. 61, 603-640.
53. West, S. C., Cassuto, E. & Howard-Flanders, P. (1981). Heteroduplex formation by RecA protein: polarity of strand exchanges. Proc. Natl Acad. Sci. USA, 78, 6149-6153.
54. Wittung, P., Bazemore, L. R., Takahashi, M., Norden, B. & Radding, C. (1996). Second-site RecA-DNA interactions: lack of identical recognition. Biochemistry, 35, 15349-15355.
55. Yancey-Wrona, J. E. & Camerini-Otero, R. D. (1995). The search for DNA homology does not limit stable homologous pairing promoted by RecA protein. Curr. Biol. 5, 1149-1158.
56. Yu, X. & Egelman, E. H. (1992). Direct visualization of dynamics and co-operative conformational changes within RecA filaments that appear to be associated with the hydrolysis of adenosine 5′-O-(3-thiotriphosphate). J. Mol. Biol. 225, 193-216.
57. Zhurkin, V. B., Raghunathan, G., Ulyanov, N. B., Camerini-Otero, R. D. & Jernigan, R. L. (1994). A parallel DNA triplex as a model for the intermediate in homologous recombination. J. Mol. Biol. 239, 181-200.