Assembly of the Escherichia coli RuvABC resolvasome directs the orientation of Holliday junction resolution

Genes and Development

Volumn 13, Issue 14, 1999, Pages 1861-1870

  Van Gool, Alain J ^a,c   Hajibagheri, Nasser M A ^a   Stasiak, Andrzej ^a,b   West, Stephen C ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c NV ORGANON   (Netherlands)

Author keywords

Branch migration; Crossover; DNA repair; Nuclease; Recombination

Indexed keywords

BACTERIAL PROTEIN; PROTEIN RUVABC; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CROSSING OVER; DNA FLANKING REGION; ESCHERICHIA COLI; GENETIC RECOMBINATION; HOLLIDAY JUNCTION; ISOMERISM; NONHUMAN; OPTICAL RESOLUTION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PROKARYOTA;

EID: 0033565930     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.13.14.1861     Document Type: Article

References (73)

1. Adams, D.E. and S.C. West. 1996. Bypass of DNA heterologies during RuvAB-mediated three-and four-strand branch migration. J. Mol. Biol. 263: 582-596.
2. Altona, C. 1996. Classification of nucleic acid junctions. J. Mol. Biol. 263: 568-581.
3. Baumann, P. and S.C. West. 1998. Role of the human Rad51 protein in homologous recombination and double-stranded break repair. Trends Biol. Sci. 23: 247-251.
4. Bennett, R.J., H.J. Dunderdale, and S.C. West. 1993. Resolution of Holliday junctions by RuvC resolvase: Cleavage specificity and DNA distortion. Cell 74: 1021-1031.
5. Bennett, R.J. and S.C. West. 1995. Structural analysis of the RuvC-Holliday junction complex reveals an unfolded junction. J. Mol. Biol. 252: 213-226.
6. Benson, F.E., S. Collier, and R.G. Lloyd. 1991. Evidence of abortive recombination in ruv mutants of Escherichia coli K-12. Mol. Gen. Genet. 225:266-272.
7. Chan, S.N., S.D. Vincent, and R.G. Lloyd. 1998. Recognition and manipulation of branched DNA by the RusA Holliday junction resolvase of Escherichia coli. Nucleic Acids Res. 26: 1560-1566.
8. Chen, S.M. and W.J. Chazin. 1994. 2-dimensional H1-NMR studies of immobile Holliday junctions: Nonlabile proton assignments and identification of crossover isomers. Biochemistry 33: 11453-11459.
9. Connolly, B., C.A. Parsons, F.E. Benson, H.J. Dunderdale, G.J. Sharples, R.G. Lloyd, and S.C. West. 1991. Resolution of Holliday junctions in vitro requires the Escherichia coli ruvC gene product. Proc. Natl. Acad. Sci. 88: 6063-6067.
10. Davies, A.A. and S.C. West. 1998. Formation of RuvABC-Holliday junction complexes in vitro. Curr. Biol. 8: 725-727.
11. Dressler, D. and H. Potter. 1982. Molecular mechanisms in genetic recombination. Ann. Rev. Biochem. 51: 727-762.
12. Duckett, D.R., M.J.E. Giraud-Panis, and D.M.J. Lilley. 1995. Binding of the junction-resolving enzyme T7 endonuclease I to DNA; Separation of binding and catalysis by mutation. J. Mol. Biol. 246: 95-107.
13. Dunderdale, H.J., F.E. Benson, C.A. Parsons, G.J. Sharples, R.G. Lloyd, and S.C. West. 1991. Formation and resolution of recombination intermediates by E. coli RecA and RuvC proteins. Nature 354: 506-510.
14. Dunderdale, H.J., G.J. Sharples, R.G. Lloyd, and S.C. West. 1994. Cloning, over-expression, purification and characterization of the Escherichia coli RuvC Holliday junction resolvase. J. Biol. Chem. 269: 5187-5194.
15. Eggleston, A.K., A.H. Mitchell, and S.C. West. 1997. In vitro reconstitution of the late steps of genetic recombination in E. coli. Cell 89: 607-617.
16. Elborough, K.M. and S.C. West. 1990. Resolution of synthetic Holliday junctions in DNA by an endonuclease activity from calf thymus. EMBO J. 9: 2931-2936.
17. Giraud-Panis, M.J.E. and D.M.J. Lilley. 1998. Structural recognition and distortion by the DNA junction-resolving enzyme RusA. J. Mol. Biol. 278: 117-133.
18. Hagan, N.F.P., S.D. Vincent, S.M. Ingleston, G.J. Sharples, R.J. Bennett, S.C. West, and R.G. Lloyd. 1998. Sequence-specificity of Holliday junction resolution: Identification of RuvC mutants defective in metal binding and target site recognition. J. Mol. Biol. 281: 17-29.
19. Hargreaves, D., D.W. Rice, S.E. Sedelnikova, P.J. Artymiuk, R.G. Lloyd, and J.B. Rafferty. 1998. Crystal structure of E. coli RuvA with bound DNA Holliday junction at 6 Å resolution. Nat. Struct. Biol. 5: 441-446.
20. Hiom, K., I.R. Tsaneva, and S.C. West. 1996. The directionality of RuvAB-mediated branch migration: In vitro studies with three-armed junctions. Genes Cells 1: 443-451.
21. Hiom, K. and S.C. West. 1995. The mechanism of branch migration in homologous recombination: Assembly of a RuvAB-Holliday junction complex in vitro. Cell 80: 787-793.
22. Holliday, R. 1964. A mechanism for gene conversion in fungi. Genet. Res. Camb. 5: 282-304.
23. Holmes, A.M. and J.E. Haber. 1999. Double-strand break repair in yeast requires both leading and lagging strand DNA polymerases. Cell 96: 415-424.
24. Hyde, H., A.A. Davies, F.E. Benson, and S.C. West. 1994. Resolution of recombination intermediates by a mammalian endonuclease activity functionally analogous to Escherichia coli RuvC resolvase. J. Biol. Chem. 269: 5202-5209.
25. Iwasaki, H., M. Takahagi, T. Shiba, A. Nakata, and H. Shinagawa. 1991. Escherichia coli RuvC protein is an endonuclease that resolves the Holliday structure. EMBO J. 10: 4381-4389.
26. Iwasaki, H., M. Takahagi, A. Nakata, and H. Shinagawa. 1992. Escherichia coli RuvA and RuvB proteins specifically interact with Holliday junctions and promote branch migration. Genes & Dev. 6: 2214-2220.
27. Kanaar, R., J.H.J. Hoeijmakers, and D.C. van Gent. 1998. Molecular mechanisms of DNA double-strand break repair. Trends Cell Biol. 8: 483-489.
28. Kemper, B. 1998. Branched DNA resolving enzymes (X-solvases). In DNA damage and repair (ed. J.A. Nicoloff and M.F. Hoekstra), pp. 179-204. Humana Press Inc, Totowa, NJ.
29. Lilley, D.M.J. and R.M. Clegg. 1993. The structure of the four-way junction in DNA. Annu. Rev. Biophys. Biomol. Struct. 22: 299-328.
30. Mandal, T.N., A.A. Mahdi, G.J. Sharples, and R.G. Lloyd. 1993. Resolution of Holliday intermediates in recombination and DNA repair: Indirect suppression of ruvA, ruvB, and ruvC mutations. J. Bacteriol. 175: 4325-4334.
31. Maxam, A.M. and W. Gilbert. 1980. Sequencing end-labeled DNA with base specific chemical cleavages. Methods Enzymol. 65: 499-560.
32. McCulloch, R., L.W. Coggins, S.D. Colloms, and D.J. Sherratt. 1994. Xer-mediated site-specific recombination at cer generates Holliday junctions in vivo. EMBO J. 13: 1844-1855.
33. McGill, C., B. Shafer, and J. Strathern. 1989. Coconversion of flanking sequences with homothallic switching. Cell 57: 459-467.
34. Meselson, M.M. and C.M. Radding. 1975. A general model for genetic recombination. Proc. Natl. Acad. Sci. 72: 358-361.
35. Miick, S.M., R.S. Fee, D.P. Millar, and W.J. Chazin. 1997. Cross-over isomer bias is the primary sequence-dependent property of immobilized Holliday junctions. Proc. Natl. Acad. Sci. 94: 9080-9084.
36. Morel, P., A. Stasiak, S.D. Ehrlich, and E. Cassuto. 1994. Effect of length and location of heterologous sequences on RecA-mediated strand exchange. J. Biol. Chem. 269: 19830-19835.
37. Murchie, A.I.H., J. Portugal, and D.M.J. Lilley. 1991. Cleavage of a 4-way DNA junction by a restriction enzyme spanning the point of strand exchange. EMBO J. 10: 713-718.
38. Parsons, C.A. and S.C. West. 1990. Specificity of binding to four-way junctions in DNA by bacteriophage T7 endonuclease I. Nucleic Acids Res. 18: 4377-4384.
39. _. 1993. Formation of a RuvAB-Holliday junction complex in vitro. J. Mol. Biol. 232: 397-405.
40. Parsons, C.A., I. Tsaneva, R.G. Lloyd, and S.C. West. 1992. Interaction of Escherichia coli RuvA and RuvB proteins with synthetic Holliday junctions. Proc. Natl. Acad. Sci. 89: 5452-5456.
41. Parsons, C.A., A. Stasiak, R.J. Bennett, and S.C. West. 1995. Structure of a multisubunit complex that promotes DNA branch migration. Nature 374: 375-378.
42. Pöhler, J.R.G., M.J.E. Giraud-Panis, and D.M.J. Lilley. 1996. T4 endonuclease VII selects and alters the structure of the four-way junction; binding of a resolution-defective mutant enzyme. J. Mol. Biol. 260: 687-696.
43. Pöhler, J.R.G., D.G. Norman, J. Bramham, M.E. Bianchi, and D.M.J. Lilley. 1998. HMG box proteins bind to 4-way DNA junctions in their open conformation. EMBO J. 17: 817-826.
44. Rafferty, J.B., S.E. Sedelnikova, D. Hargreaves, P.J. Artymiuk, P.J. Baker, G.J. Sharples, A.A. Mahdi, R.G. Lloyd, and D.W. Rice. 1996. Crystal structure of the DNA recombination protein RuvA and a model for its binding to the Holliday junction. Science 274: 415-421.
45. Roe, S.M., T. Barlow, T. Brown, M. Oram, A. Keeley, I.R. Tsaneva, and L.H. Pearl. 1998. Crystal structure of an octameric RuvA-Holliday junction complex. Mol. Cell 2: 361-372.
46. Shah, R., R.J. Bennett, and S.C. West. 1994. Genetic recombination in E. coli: RuvC protein cleaves Holliday junctions at resolution hotspots in vitro. Cell 79: 853-864.
47. Shah, R., R. Cosstick, and S.C. West. 1997. The RuvC dimer resolves Holliday junctions by a dual incision mechanism that involves base-specific contacts. EMBO J. 16: 1464-1472.
48. Sharples, G.J., F.E. Benson, G.T. Illing, and R.G. Lloyd. 1990. Molecular and functional analysis of the ruv region of Escherichia coli K-12 reveals three genes involved in DNA repair and recombination. Mol. Gen. Genet. 221: 219-226.
49. Shiba, T., H. Iwasaki, A. Nakata, and H. Shinagawa. 1991. SOS-inducible DNA repair proteins, RuvA and RuvB, of Escherichia coli: Functional interactions between RuvA and RuvB for ATP hydrolysis and renaturation of the cruciform structure in supercoiled DNA. Proc. Natl. Acad. Sci. 88: 8445-8449.
50. Shida, T., H. Iwasaki, A. Saito, Y. Kyogoku, and H. Shinagawa. 1996. Analysis of substrate specificity of the RuvC Holliday junction resolvase with synthetic Holliday junctions. J. Biol. Chem. 271: 26105-26109.
51. Shinagawa, H., K. Makino, M. Amemura, S. Kimura, H. Iwasaki, and A. Nakata. 1988. Structure and regulation of the Escherichia coli ruv operon involved in DNA repair and recombination. J. Bacteriol. 170: 4322-4329.
52. Shinohara, A. and T. Ogawa. 1995. Homologous recombination and the roles of double-strand breaks. Trends Biochem. Sci. 20: 387-391.
53. Shurvinton, C.E. and R.G. Lloyd. 1982. Damage to DNA induces expression of the ruv gene of Escherichia coli. Mol. Gen. Genet. 185: 352-355.
54. Sogo, J., A. Stasiak, W. De Bernadin, R. Losa, and Koller, T. 1987. Binding of protein to nucleic acids. In Electron microscopy in molecular biology (ed. J. Sommerville and U. Scheer), pp. 61-79. IRL Press, Oxford, UK.
55. Sonoda, E., M.S. Sasaki, J.M. Buerstedde, O. Bezzubova, A. Shinohara, H. Ogawa, M. Takata, Y. Yamaguchi-Iwai, and S. Takeda. 1998. Rad51 deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 17: 598-608.
56. Stasiak, A., I.R. Tsaneva, S.C. West, C.J.B. Benson, X. Yu, and E.H. Egelman. 1994. The Escherichia coli RuvB branch migration protein forms double hexameric rings around DNA. Proc. Natl. Acad. Sci. 91: 7618-7622.
57. Szostak, J.W., T.L. Orr-Weaver, R.J. Rothstein, and F.W. Stahl. 1983. The double-strand break repair model for recombination. Cell 33: 25-35.
58. Takahagi, M., H. Iwasaki, and H. Shinagawa. 1994. Structural requirements of substrate DNA for binding to and cleavage by RuvC, a Holliday junction resolvase. J. Biol. Chem. 269: 15132-15139.
59. Tsaneva, I.R., G.T. Illing, R.G. Lloyd, and S.C. West. 1992a. Purification and properties of the RuvA and RuvB proteins of Escherichia coli. Mol. Gen. Genet. 235: 1-10.
60. Tsaneva, I.R., B. Müller, and S.C. West. 1992b. ATP-dependent branch migration of Holliday junctions promoted by the RuvA and RuvB proteins of E. coli. Cell 69: 1171-1180.
61. Tsaneva, I.R., B. Müller, and S.C. West. 1993. The RuvA and RuvB proteins of Escherichia coli exhibit DNA helicase activity in vitro. Proc. Natl. Acad. Sci. 90: 1315-1319.
62. Umezu, K., N.W. Chi, and R.D. Kolodner. 1993. Biochemical interaction of the Escherichia coli RecF, RecO, and RecR proteins with RecA protein and single-stranded-DNA binding-protein. Proc. Natl. Acad. Sci. 90: 3875-3879.
63. van Gool, A.J., R. Shah, C. Mézard, and S.C. West. 1998. Functional interactions between the Holliday junction resolvase and the branch migration motor of Escherichia coli. EMBO J. 17: 1838-1845.
64. Webb, B.L., M.M. Cox, and R.B. Inman. 1997. Recombinational DNA repair: The RecF and RecR proteins limit the extension of RecA filaments beyond single-strand DNA gaps. Cell 91: 347-356.
65. West, S.C. 1993. The nucleases of genetic recombination. In Nucleases 2nd ed., (ed. S.M. Linn, R.S. Lloyd, and R.J. Roberts), pp. 145-169. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
66. _. 1996. The RuvABC Proteins and Holliday junction processing in Escherichia coli. J. Bacteriol. 178: 1237-1241.
67. _. 1998. RuvA gets X-rayed on Holliday. Cell 94: 699-701.
68. Whitby, M.C., E.L. Bolt, S.N. Chan, and R.G. Lloyd. 1996. Interactions between RuvA and RuvC at Holliday junctions: Inhibition of junction cleavage and formation of a RuvA-RuvC-DNA complex. J. Mol. Biol. 264: 878-890.
69. White, M.F. and D.M.J. Lilley. 1997. The resolving enzyme Ccel of yeast opens the structure of the 4-way DNA junction. J. Mol. Biol. 266: 122-134.
70. White, M.F. and D.M.J. Lilley. 1998. Interaction of the resolving enzyme YDC2 with the four-way DNA junction. Nucleic Acids Res. 26: 5609-5616.
71. Yu, X., S.C. West, and E.H. Egelman. 1997. Structure and subunit composition of the RuvAB-Holliday junction complex. J. Mol. Biol. 266: 217-222.
72. Zerbib, D., S.D. Colloms, D.J. Sherratt, and S.C. West. 1997. Effect of DNA topology on Holliday junction resolution by Escherichia coli RuvC and bacteriophage T7 endonuclease I. J. Mol. Biol. 270: 663-673.
73. Zerbib, D., C. Mézard, H. George, and S.C. West. 1998. Coordinated actions of RuvABC in Holliday junction processing. J. Mol. Biol. 281: 621-630.