A molecular model for RecA-promoted strand exchange via parallel triple- stranded helices

Biophysical Journal

Volumn 77, Issue 3, 1999, Pages 1562-1576

  Bertucat, Guillaume ^a   Lavery, Richard ^a   Prévost, Chantal ^a  

^a INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; DNA DETERMINATION; DNA STRUCTURE; MOLECULAR MODEL; RECA GENE; STRUCTURE ANALYSIS;

EID: 0032865485     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(99)77004-9     Document Type: Article

References (87)

1. Adzuma, K. 1992. Stable synapsis of homologous DNA molecules mediated by the Escherichia coli RecA protein involves local exchange of DNA strands. Genes Dev. 6:1679-1694.
2. Adzuma, K. 1998. No sliding during homology search by RecA protein. J. Biol. Chem. 273:31565-31573.
3. Amos, L. A., and R. A. Cross. 1997. Structure and dynamics of molecular motors. Curr. Opin. Struct. Biol. 7:239-246.
4. Baliga, R., J. W. Singleton, and P. B. Dervan. 1995. RecA.oligonucleotide filaments bind in the minor groove of double-stranded DNA. Proc. Natl. Acad. Sci. USA. 92:10393-10397.
5. Baumann, P., and S. C. West. 1998. Role of the human RAD51 protein in homologous recombination and double-stranded-break repair. Trends Biochem. Sci. 23:247-251.
6. Bazemore, L. R., E. Folta-Stogniew, M. Takahashi, and C. M. Radding. 1997a. RecA tests homology at both pairing and strand exchange. Proc. Natl. Acad. Sci. USA. 94:11863-11868.
7. Bazemore, L. R., M. Takahashi, and C. M. Radding. 1997b. Kinetic analysis of pairing and strand exchange catalyzed by RecA. Detection by fluorescence energy transfer. J. Biol. Chem. 272:14672-14682.
8. Bedale, W. A., and M. Cox. 1996. Evidence for the coupling of ATP hydrolysis to the final (extension) phase of RecA protein-mediated DNA strand exchange. J. Biol. Chem. 271:5725-5732.
9. Bernet, J., K. Zakrzewska, and R. Lavery. 1997. Modelling base pair opening: the role of helical twist. J. Mol. Struct. Theochem. 398-399: 473-482.
10. Bertucat, G., R. Lavery, and C. Prévost. 1998. A model for parallel triple helix formation by RecA: single-strand association with a homologous duplex via the minor groove. J. Biomol. Struct. Dyn. 16:535-546.
11. Bianchi, M. E., and C. M. Radding. 1983. Insertions, deletions and mismatches in heteroduplex DNA made by RecA protein. Cell. 35:511-520.
12. Brown, T., and W. N. Hunter. 1997. Non-Watson-Crick base associations in DNA and RNA revealed by single crystal x-ray diffraction methods: mismatches, modified bases and non-duplex DNA. Biopolymers. 44: 91-103.
13. Burnett, B., B. J. Rao, B. Jwang, G. Reddy, and C. M. Radding. 1994. Resolution of the three-stranded recombination intermediate made by RecA protein. An essential role of ATP hydrolysis. J. Mol. Biol. 238: 540-554.
14. Camerini-Otero, D., and P. Hsieh. 1993. Parallel DNA triplexes, homologous recombination and other homology-dependent DNA interactions. Cell. 73:217-223.
15. Chiu, S. K., B. J. Rao, R. M. Story, and C. M. Radding. 1993. Interactions of three strands in joints made by RecA protein. Biochemistry. 32: 13146-13155.
16. Cluzel, P., A. Lebrun, C. Heller, R. Lavery, J.-L. Viovy, D. Chatenay, and F. Caron. 1996. DNA: an extensible molecule. Science. 271:792-795.
17. Cox, M. M. 1994. Why does RecA protein hydrolyse ATP? Trends Biochem. Sci. 19:217-222.
18. Dagneaux, C., H. Porumb, J. Liquier, M. Takahashi, and E. Taillandier. 1995a. Conformations of three-stranded DNA structures formed in presence and in absence of the RecA protein. J. Biomol. Struct. Dyn. 13:465-470.
19. Dagneaux, C., A. K. Shchyolkina, J. Liquier, V. L. Florentiev, and E. Taillandier. 1995b. A triple helix obtained by specific recognition of all 4 bases in duplex DNA can adopt a collapsed or an extended form. C. R. Acad. Sci. III. 318:559-562.
20. DasGupta, C., and C. M. Radding. 1982a. Polar branch migration promoted by RecA protein: effect of mismatched base pairs. Proc. Natl. Acad. Sci. USA. 79:762-766
21. DasGupta, C., and C. M. Radding. 1982b. Lower fidelity of RecA protein catalysed homologous pairing with a superhelical substrate. Nature. 295:71-73.
22. DiCapua, E., and B. Muller. 1987. The accessibility of DNA to dimethylsulfate in complexes with RecA protein. EMBO J. 6:2493-2498.
23. DiCapua, E., M. Schnarr, R. W. Ruigrok, P. Lindner, and P. A. Timmins. 1990. Complexes of RecA protein in solution. A study by small angle neutron scattering. J. Mol. Biol. 214:557-570.
24. Ellouze, C., M. Takahashi, P. Wittung, K. Mortensen, M. Schnarr, and B. Nordén. 1995. Evidence for elongation of the helical pitch of the RecA filament upon ATP and ADP binding using small-angle neutron scattering. Eur. J. Biochem. 233:579-583.
25. Ellouze, C., H.-K. Kim, K. Maeshima, E. Tuite, K. Morimatsu, T. Horii, K. Mortensen, B. Nordén, and M. Takahashi. 1997a. Nucleotide cofactor-dependent structural change of Xenopus laevis Rad51 protein filament detected by small-angle neutron scattering measurements in solution. Biochemistry. 36:13524-13529.
26. Ellouze, C., B. Nordén, and M. Takahashi. 1997b. Dissociation of non-complementary second DNA from RecA filament without ATP hydrolysis: mechanism of search for homologous DNA. J. Biochem. (Tokyo). 121:1070-1075.
27. Flory, J., S. S. Tsang, and K. Muniyappa. 1984. Isolation and visualization of active presynaptic filaments of RecA protein and single-stranded DNA. Proc. Natl. Acad. Sci. USA. 81:7026-7030.
28. Gumbs, O. H., and S. L. Shaner. 1998. Three mechanistic steps detected by FRET after presynaptic filament formation in homologous recombination. ATP hydrolysis required for release of oligonucleotide heteroduplex product from RecA. Biochemistry. 37:11692-11706.
29. Heuser, J., and J. Griffith. 1989. Visualization of RecA protein and its complexes with DNA by quick-freeze/deep-etch electron microscopy. J. Mol. Biol. 210:473-484.
30. Hingerty, B. E., R. H. Richtie, T. L. Ferrell, and J. E. Turner. 1985. Dielectric effects in biopolymers: the theory of ionic saturation revisited. Biopolymers. 24:427-439.
31. Howard-Flanders, P., S. C. West, and A. Stasiak. 1984. Role of RecA protein spiral filaments in genetic recombination. Nature. 309:215-219.
32. Hsieh, P., C. S. Camerini-Otero, and R. D. Camerini-Otero. 1990. Pairing of homologous DNA sequences by proteins: evidence for three-stranded DNA. Genes Dev. 4:1951-1963.
33. Jain, S. K., M. M. Cox, and R. B. Inman. 1995. Occurrence of three-stranded DNA within a RecA protein filament. J. Biol. Chem. 270: 4943-4949.
34. Kiianitsa, K., and A. Stasiak. 1997. Helical repeat of DNA in the region of homologous pairing. Proc. Natl. Acad. Sci. USA. 94:7837-7840.
35. Kim, S. K., M. Takahashi, and B. Nordén. 1995. Binding of RecA to anti-parallel poly(dA)·2poly(dT) triple helix DNA. Biochem. Biophys. Acta. 1264:129-133.
36. Kowalczykowski, S. C. 1991. Biochemistry of genetic recombination: energetics and mechanism of DNA strand exchange. Annu. Rev. Biophys. Chem. 20:539-575.
37. Kowalczykowski, S. C., D. A. Dixon, A. K. Eggleston, S. D. Lauder, and W. M. Rehrauer. 1994. Biochemistry of homologous recombination in Escherichia coli. Microbiol. Rev. 58:401-465.
38. Kowalczykowski, S. C., and A. K. Eggleston. 1994. Homologous pairing and DNA strand-exchange proteins. Annu. Rev. Biochem. 63:991-1043.
39. Kowalczykowski, S. C., and R. A. Krupp. 1995. DNA-strand exchange promoted by RecA protein in the absence of ATP: implications for the mechanism of energy transduction in protein-promoted nucleic acid transactions. Proc. Natl. Acad. Sci. USA. 92:3478-3482.
40. Kubista, M., M. Takahashi, and B. Nordén. 1990. Stoichiometry, base orientation, and nuclease accessibility of RecA complexes seen by polarized light in flow-oriented solution. Implications for the mechanism of genetic recombination. J. Biol. Chem. 265:18891-18897.
41. Kumar, K. A., and K. Muniyappa. 1992. Use of structure-directed DNA ligands to probe the binding of RecA protein to narrow and wide grooves of DNA and on its ability to promote homologous pairing. J. Biol. Chem. 267:24824-24832.
42. Kurumizaka, H., and T. Shibata. 1996. Homologous recognition by RecA protein using non-equivalent three DNA-strand-binding sites. J. Biochem. 119:216-223.
43. Lavery, R. 1988. Junctions and bends in nucleic acids: a new theoretical modeling approach. In Structure and Expression, Vol 3: DNA Bending and Curvature. W. K. Olson, R. H. Sarma, M. H. Sarma, and M. Sundaralingam, editors. Adenine Press, Schenectady, NY. 191-211.
44. Lavery, R. 1995. Modelling the DNA double helix: techniques and results. In Non-Linear Excitation in Biomolecules. M. Peyrard, editor. Springer-Verlag, Editions de Physique, Berlin and New York. 57-82.
45. Lavery, R., and H. Sklenar. 1988. The definition of generalized helicoidal parameters and of axis curvature for irregular nucleic acids. J. Biomol. Struct. Dyn. 6:63-91.
46. Lavery, R., and H. Sklenar. 1989. Defining the structure of irregular nucleic acids: conventions and principles. J. Biomol. Struct. Dyn. 6:655-667.
47. Lavery, R., H. Sklenar, K. Zakrzewska, and B. Pullman. 1986. The flexibility of the nucleic acids. II. The calculation of internal energy and applications to mononucleotide repeat DNA. J. Biomol. Struct. Dyn. 3:989-1014.
48. Lavery, R., K. Zakrzewska, and H. Sklenar. 1995. JUMNA (junction minimisation of nucleic acids). Comput. Phys. Commun. 91:135-158.
49. Lebrun, A., and R. Lavery. 1995. Modelling a strand exchange tetraplex conformation. J. Biomol. Struct. Dyn. 13:459-464.
50. Lebrun, A., and R. Lavery. 1996. Modelling extreme stretching of DNA. Nucleic Acids Res. 24:2260-2267.
51. Léger, J. F., J. Robert, L. Bourdieu, D. Chatenay, and J. F. Marko. 1998. RecA binding to a single double-stranded DNA molecule: a possible role of DNA conformational fluctuations. Proc. Natl. Acad. Sci. USA. 95: 12295-12299.
52. Leonard, G. A., S. Zhang, M. R. Peterson, S. J. Harrop, J. R. Helliwell, W. B. Cruse, B. Langlois d'Estaintot, O. Kennard, T. Brown, and W. N. Hunter. 1995. Self-association of a DNA loop creates a quadruplex: crystal structure of d(GCATGCT) at 1.8 Å resolution. Structure. 3:335-340.
53. Little, J. W., S. H. Edmiston, L. Z. Pacelli, and D. W. Mount. 1980. Cleavage of the Escherichia coli lexA protein by the recA protease. Proc. Natl. Acad. Sci. USA. 77:3225-3229.
54. Malkov, A. M., and R. D. Camerini-Otero. 1998. Dissociation kinetics of RecA protein-three-stranded DNA complexes reveals a low fidelity of RecA-assisted recognition of homology. J. Mol. Biol. 278:317-330.
55. Mazin, A. V., and S. C. Kowalczykowski. 1996. The specificity of the secondary DNA binding site of RecA protein defines its role in DNA strand exchange. Proc. Natl. Acad. Sci. USA. 93:10673-10678.
56. Mazin, A. V., and S. C. Kowalczykowski. 1998. The function of the secondary DNA-binding site of RecA protein during DNA strand exchange. EMBO J. 17:1161-1168.
57. McGavin, S. 1971. Models of specifically paired like (homologous) nucleic acid structures. J. Mol. Biol. 55:293-298.
58. McGavin, S. 1973. Chromosome pairing. Nature. 242:330.
59. Muller, B., I. Burdett, and S. C. West. 1992. Unusual stability of recombination intermediates made by Escherichia coli RecA protein. EMBO J. 11:2685-2693.
60. Nishinaka, T., Y. Ito, S. Yokoyama, and T. Shibata. 1997. An extended DNA structure through deoxyribose-base stacking induced by RecA protein. Proc. Natl. Acad. Sci. USA. 94:6623-6628.
61. Nishinaka, T., A. Shinohara, Y. Ito, S. Yokoyama, and T. Shibata. 1998. Base pair switching by interconversion of sugar puckers in DNA extended by proteins of RecA-family: a model for homology search in homologous genetic recombination. Proc. Natl. Acad. Sci. USA. 95: 11071-11076.
62. Nordén, B., C. Elvingson, M. Kubista, P. Sjöberg, H. Ryberg, M. Ryberg, K. Mortensen, and M. Takahashi. 1992. Structure of RecA-DNA complexes studied by combination of linear dichroism and small-angle neutron scattering measurements on flow-oriented samples. J. Mol. Biol. 226:1175-1191.
63. Nordén, B., P. Wittung-Stafshede, C. Ellouze, H. K. Kim, K. Mortensen, and M. Takahashi. 1998. Base orientation of second DNA in RecA.DNA filaments. Analysis by combination of linear dichroism and small angle neutron scattering in flow-oriented solution. J. Biol. Chem. 273: 15682-15686.
64. Podyminogin, M. A., R. B. Meyer, Jr., and H. B. Gamper. 1996. RecA-catalyzed, sequence-specific alkylation of DNA by cross-linking oligonucleotides. Effects of length and non-homologous base substitutions. Biochemistry. 35:7267-7274.
65. Pugh, B. F., and M. Cox. 1988. High salt activation of RecA protein ATPase in the absence of DNA. J. Biol. Chem. 263:76-83.
66. Rao, B. J., S. K. Chiu, L. R. Bazemore, G. Reddy, and C. M. Radding. 1995. How specific is the first recognition step of homologous recombination? Trends Biochem. Sci. 20:109-113.
67. Rao, B. J., S. K. Chiu, and C. M. Radding. 1993. Homologous recognition and triplex formation promoted by RecA protein between duplex oligonucleotides and single-stranded DNA. J. Mol. Biol. 229:328-343.
68. Rao, B. J., M. Dutreix, and C. M. Radding. 1991. Stable three-stranded DNA made by RecA protein. Proc. Natl. Acad. Sci. USA. 88: 2984-2988.
69. Reddy, G., B. Burnett, and C. M. Radding. 1995. Uptake and processing of duplex DNA by RecA nucleoprotein filaments: insights provided by a mixed population of dynamic and static intermediates. Biochemistry. 34:10194-10204.
70. Roberts, J. W., C. W. Roberts, and N. L. Craig. 1978. Escherichia coli recA gene product inactivates phage lambda repressor. Proc. Natl. Acad. Sci. USA. 75:4714-4718.
71. Rosselli, W., and A. Stasiak. 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.
72. Rosselli, W., and A. Stasiak. 1991. The ATPase activity of RecA is needed to push the DNA strand through heterologous regions. EMBO J. 10: 4391-4396.
73. Stasiak, A., and E. DiCapua. 1982. The helicity of DNA in complexes with RecA protein. Nature. 299:185-186.
74. Stasiak, A., E. DiCapua, and T. Koller. 1981. Elongation of duplex DNA by recA protein. J. Mol. Biol. 151:557-564.
75. Story, R. M., I. T. Weber, and T. A. Steitz. 1992. The structure of the E. coli RecA protein monomer and polymer. Nature. 355:318-325.
76. Takahashi, M., M. Kubista, and B. Nordén. 1991. Co-ordination of multiple DNA molecules in RecA fiber evidenced by linear dichroism spectroscopy. Biochimie (Paris). 73:219-226.
77. Takahashi, M., and B. Nordén. 1994. Structure of RecA-DNA complex and mechanism of DNA strand exchange reaction in homologous recombination. Adv. Biophys. 30:1-35.
78. Tuite, E., U. Sehlstedt, P. Hagmar, B. Nordén, and M. Takahashi. 1997. Effects of minor and major groove-binding drugs and intercalators on the DNA association of minor groove-binding proteins RecA and deoxyribonuclease I detected by flow linear dichroism. Eur. J. Biochem. 243:482-492.
79. Watt, V. M., C. J. Ingles, M. S. Urdea, and W. J. Rutter. 1985. Homology requirements for recombination in Escherichia coli. Proc. Natl. Acad. Sci. USA. 82:4768-4772.
80. Wilson, J. H. 1979. Nick-free formation of reciprocal heteroduplexes: a simple solution to the topological problem. Proc. Natl. Acad. Sci. USA. 76:3641-3645.
81. Wittung, P., L. R. Bazemore, M. Takahashi, B. Nordén, and C. Radding. 1996. Second-site RecA-DNA interactions: lack of identical recognition. Biochemistry. 35:15349-15355.
82. Wittung, P., B. Nordén, and M. Takahashi. 1994. Spectroscopic observation of renaturation between polynucleotides interacting with RecA in the presence of ATP hydrolysis. Eur. J. Biochem. 224:39-45.
83. Wong, B. C., S.-K. Chiu, and S. A. Chow. 1998. The role of negative superhelicity and length of homology in the formation of paranemic joints promoted by RecA protein. J. Biol. Chem. 273:12120-12127.
84. Yu, X., and E. H. Egelman. 1990. Image analysis reveals that Escherichia coli RecA protein consists of two domains. Biophys. J. 57:555-566.
85. Yu, X., and E. H. Egelman. 1992. Structural data suggest that the active and inactive forms of the RecA filament are not simply interconvertible. J. Mol. Biol. 227:334-346.
86. Zhou, X., and K. Adzuma. 1997. DNA strand exchange mediated by the Escherichia coli RecA protein initiates in the minor groove of double-stranded DNA. Biochemistry. 36:4650-4661.
87. Zhurkin, V. B., G. Raghunathan, N. B. Ulyanov, R. D. Camerini-Otero, and R. L. Jernigan. 1994. A parallel DNA triplex as a model for the intermediate in homologous recombination. J. Mol. Biol. 239:181-200.