Effect of DNA topology on Holliday junction resolution by Escherichia coli RuvC and bacteriophage T7 endonuclease I

Journal of Molecular Biology

Volumn 270, Issue 5, 1997, Pages 663-673

  Zerbib, Didier ^a,b   Colloms, Sean D ^c   Sherratt, David J ^c   West, Stephen C ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b Université Toulouse III Paul Sabatier   (France)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

DNA repair; Endonuclease; Genetic recombination; Resolvase; Site specific recombination

Indexed keywords

DNA; ENDONUCLEASE; RESOLVASE;

ARTICLE; BACTERIOPHAGE T7; CONTROLLED STUDY; DNA RECOMBINATION; DNA REPAIR; DNA STRUCTURE; DNA SUPERCOILING; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; HOLLIDAY JUNCTION; PRIORITY JOURNAL; PROTEIN DNA INTERACTION;

ESCHERICHIA COLI;

EID: 0031213848     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1157     Document Type: Article

References (49)

1. Arciszewska L. K., Sherratt D. J. Xer site-specific recombination in vitro. EMBO J. 14:1995;2112-2120.
2. Ariyoshi M., Vassylyev D. G., Iwasaki H., Nakamura H., Shinagawa H., Morikawa K. Atomic structure of the RuvC resolvase: a Holliday junction-specific endonuclease from E. coli. Cell. 78:1994;1063-1072.
3. Benbow R. M., Zuccarelli A. J., Sinsheimer R. L. Recombinant DNA molecules of φX174. Proc. Natl Acad. Sci. USA. 72:1975;235-239.
4. Bennett R. J., West S. C. RuvC protein resolves Holliday junctions via cleavage of the continuous (non-crossover) strands. Proc. Natl Acad. Sci. USA. 92:1995a;5635-5639.
5. Bennett R. J., West S. C. Structural analysis of the RuvC-Holliday junction complex reveals an unfolded junction. J. Mol. Biol. 252:1995b;213-226.
6. Bennett R. J., West S. C. Resolution of Holliday junctions in genetic recombination: RuvC protein nicks DNA at the point of strand exchange. Proc. Natl Acad. Sci. USA. 93:1996;12217-12222.
7. Bennett R. J., Dunderdale H. J., West S. C. Resolution of Holliday junctions by RuvC resolvase: cleavage specificity and DNA distortion. Cell. 74:1993;1021-1031.
8. Benson F. E., West S. C. Substrate specificity of the Escherichia coli RuvC protein: resolution of 3- and 4-stranded recombination intermediates. J. Biol. Chem. 269:1994;5195-5201.
9. Bhattacharyya A., Murchie A. I. H., von Kitzing E., Diekmann S., Kemper B., Lilley D. M. J. A model for the interaction of DNA junctions and resolving enzymes. J. Mol. Biol. 221:1991;1191-1207.
10. Blakely G., May G., McCulloch R., Arciszewska L. K., Burke M., Lovett S. T., Sherratt D. J. Two related recombinases are required for site-specific recombination at dif and cer inEscherichia coli K12. Cell. 75:1993;351-361.
11. Churchill M. E. A., Tullius T. D., Kallenbach N. R., Seeman N. C. A Holliday recombination intermediate is two-fold symmetric. Proc. Natl Acad. Sci. USA. 85:1988;4653-4656.
12. Clegg R. M., Murchie A., Zechel A., Carlberg C., Diekmann S., Lilley D. M. J. Fluorescence resonance energy-transfer analysis of the structure of the 4-way DNA junction. Biochemistry. 31:1992;4846-4856.
13. Colloms S. D., Sykora P., Szatmari G., Sherratt D. J. Recombination at ColE1 cer requires the Escherichia coli xerC gene product, a member of the lambda integrase family of site-specific recombinases. J. Bacteriol. 172:1990;6973-6980.
14. Colloms S. D., McCulloch R., Grant K., Neilson L., Sherratt D. J. Xer-mediated site-specific recombination in vitro. EMBO J. 15:1996;1172-1181.
15. Colloms S. D., Bath J., Sherratt D. J. Topology of Xer mediated site-specific recombination at psi and cer. Cell. 88:1997;855-864.
16. Cooper J. P., Hagerman P. J. Gel electrophoretic analysis of the geometry of a DNA four-way junction. J. Mol. Biol. 198:1987;711-719.
17. Cooper J. P., Hagerman P. J. Geometry of a branched DNA structure in solution. Proc. Natl Acad. Sci. USA. 86:1989;7336-7340.
18. Duckett D. R., Murchie A. I. H., Diekmann S., von Kitzing E., Kemper B., Lilley D. M. J. The structure of the Holliday junction and its resolution. Cell. 55:1988;79-89.
19. Duckett D. R., Giraud-Panis M. J. E., Lilley D. M. J. Binding of the junction-resolving enzyme T7 endonuclease I to DNA; separation of binding and catalysis by mutation. J. Mol. Biol. 246:1995;95-107.
20. Dunderdale H. J., Benson F. E., Parsons C. A., Sharples G. J., Lloyd R. G., West S. C. Formation and resolution of recombination intermediates by E. coli RecA and RuvC proteins. Nature. 354:1991;506-510.
21. Dunderdale H. J., Sharples G. J., Lloyd R. G., West S. C. Cloning, over-expression, purification and characterization of the Escherichia coli RuvC Holliday junction resolvase. J. Biol. Chem. 269:1994;5187-5194.
22. Eggleston A. K., Mitchell A. H., West S. C. In vitro reconstitution of the late steps of genetic recombination in E. coli. Cell. 89:1997;607-617.
23. Fu T. J., Tsedinh Y. C., Seeman N. C. Holliday junction crossover topology. J. Mol. Biol. 236:1994;91-105.
24. Holliday R. A mechanism for gene conversion in fungi. Genet. Res. Camb. 5:1964;282-304.
25. Iwasaki H., Takahagi M., Shiba T., Nakata A., Shinagawa H. Escherichia coli RuvC protein is an endonuclease that resolves the Holliday structure. EMBO J. 10:1991;4381-4389.
26. Lilley D. M. J., Clegg R. M. The structure of the four-way junction in DNA. Annu. Rev. Biophys. Biomol. Struct. 22:1993;299-328.
27. Lu M., Guo Q., Seeman N. C., Kallenbach N. R. Parallel and antiparallel Holliday junctions differ in structure and stability. J. Mol. Biol. 221:1991;1419-1432.
28. Mahdi A. A., Sharples G. J., Mandal T. N., Lloyd R. G. Holliday junction resolvases encoded by homologous rusA genes in Escherichia coli K-12 and phage-82. J. Mol. Biol. 257:1996;561-573.
29. Mandal T. N., Mahdi A. A., Sharples G. J., Lloyd R. G. Resolution of Holliday intermediates in recombination and DNA repair: indirect suppression of ruvA, ruvB, andruvC mutations. J. Bacteriol. 175:1993;4325-4334.
30. McCulloch R., Coggins L. W., Colloms S. D., Sherratt D. J. Xer-mediated site-specific recombination at cer generates Holliday junctions in vivo. EMBO J. 13:1994;1844-1855.
31. Meselson M. M., Radding C. M. A general model for genetic recombination. Proc. Natl Acad. Sci. USA. 72:1975;358-361.
32. Müller B., Jones C., Kemper B., West S. C. Enzymatic formation and resolution of Holliday junctions in vitro. Cell. 60:1990;329-336.
33. Murchie A. I. H., Clegg R. M., von Kitzing E., Duckett D. R., Diekmann S., Lilley D. M. J. Fluorescence energy transfer shows that the four-way DNA junction is a right-handed cross of antiparallel molecules. Nature. 341:1989;763-766.
34. Parsons C. A., West S. C. Specificity of binding to four-way junctions in DNA by bacteriophage T7 endonuclease I. Nucl. Acids Res. 18:1990;4377-4384.
35. Petes T. D., Malone R. E., Symington L. S. Recombination in yeast. The Molecular and Cellular Biology of the Yeast Saccharomyces: Genome Dynamics, Protein Synthesis and Energetics. 1991;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
36. Rafferty J. B., Sedelnikova S. E., Hargreaves D., Artymiuk P. J., Baker P. J., Sharples G. J., Mahdi A. A., Lloyd R. G., Rice D. W. Crystal structure of the DNA recombination protein RuvA and a model for its binding to the Holliday junction. Science. 274:1996;415-421.
37. Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning: A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
38. Shah R., Bennett R. J., West S. C. Genetic recombination in E. coli: RuvC protein cleaves Holliday junctions at resolution hotspots in vitro. Cell. 79:1994;853-864.
39. Shah R., Cosstick R., West S. C. The RuvC dimer resolves Holliday junctions by a dual incision mechanism that involves base-specific contacts. EMBO J. 16:1997;1464-1472.
40. Sharples G. J., Benson F. E., Illing G. T., Lloyd R. G. 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. 221:1990;219-226.
41. Sharples G. J., Chan S. N., Mahdi A. A., Whitby M. C., Lloyd R. G. Processing of intermediates in recombination and DNA repair: identification of a new endonuclease that specifically cleaves Holliday junctions. EMBO J. 13:1994;6133-6142.
42. Shida T., Iwasaki H., Saito A., Kyogoku Y., Shinagawa H. Analysis of substrate specificity of the RuvC Holliday junction resolvase with synthetic Holliday junctions. J. Biol. Chem. 271:1996;26105-26109.
43. Strathern J. N. Control and execution of homothallic switching in Saccharomyces cerevisiae. Genetic Recombination. 1988;Am. Soc. Microbiol. Washington.
44. Szostak J. W., Orr-Weaver T. L., Rothstein R. J., Stahl F. W. The double-strand break repair model for recombination. Cell. 33:1983;25-35.
45. Takahagi M., Iwasaki H., Shinagawa H. Structural requirements of substrate DNA for binding to and cleavage by RuvC, a Holliday junction resolvase. J. Biol. Chem. 269:1994;15132-15139.
46. Thompson B. J., Escarmis C., Parker B., Slater W. C., Doniger J., Tessman I., Warner R. C. Figure-8 configuration of dimers of S13 and φX174 replicative form DNA. J. Mol. Biol. 91:1975;409-419.
47. West S. C. The nucleases of genetic recombination. Linn S. M., Lloyd R. S., Roberts R. J. Nucleases. 1993;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
48. West S. C. The RuvABC proteins and Holliday junction processing in Escherichia coli. J. Bacteriol. 178:1996;1237-1241.
49. Whitby M. C., Bolt E. L., Chan S. N., Lloyd R. G. Interactions between RuvA and RuvC at Holliday junctions: inhibition of junction cleavage and formation of a RuvA-RuvC-DNA complex. J. Mol. Biol. 264:1996;878-890.