Insights into the mechanisms of homologous recombination from the structure of RuvA

Current Opinion in Structural Biology

Volumn 7, Issue 6, 1997, Pages 798-803

  Rice, David W ^a   Rafferty, John B ^a   Artymiuk, Peter J ^a   Lloyd, Robert G ^b  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DNA; DNA BINDING PROTEIN; TETRAMER;

DNA PROTEIN COMPLEX; ESCHERICHIA COLI; GENETIC RECOMBINATION; HOLLIDAY JUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN TERTIARY STRUCTURE; REVIEW;

EID: 0031456267     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(97)80149-2     Document Type: Article

References (31)

1. Kowalczykowski SC, Dixon DA, Eggleston AK, Lauder SD, Rehrauer WM. Biochemistry of homologous recombination in Escherichia coli. Micro Rev. 58:1994;401-465.
2. Holliday R. A mechanism for gene conversion in fungi. Genet Res Camb. 5:1964;282.
3. West SC. The RuvABC proteins and Holliday junction processing in Escherichia coli. of special interest J Bacteriol. 178:1996;1237-1241 An early mini-review of the field including reference to the biochemical characterisation presented in [17], which outlined the first observation of a tripartite complex of RuvAB bound to DNA and proposed a square planar arrangement for the Holliday junction during branch migration.
4. Benson FE, Illing GT, Sharples GJ, Lloyd RG. Nucleotide sequencing of the ruv region of Escherichia coli K-12 reveals a LexA regulated operon encoding two genes. Nucleic Acid Res. 16:1988;1541-1549.
5. Shinagawa H, Makino K, Amemura M, Kimura S, Iwasaki H, Nakata A. Structure and regulation of the Escherichia coli ruv operon involved in DNA repair and recombination. J Bacteriol. 170:1988;4322-4329.
6. Sharples GJ, Benson FE, Illing GT, Lloyd RG. 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.
7. Takahagi M, Iwasaki H, Nakata A, Shinagawa H. Molecular analysis of the Escherichia coli ruvC gene, which encodes a Holliday junction-specific endonuclease. J Bacteriol. 173:1991;5747-5753.
8. Parsons CA, Tsaneva I, Lloyd RG, West SC. Interaction of E. coli RuvA and RuvB proteins with synthetic Holliday junctions. Proc Natl Acad Sci USA. 89:1992;5452-5456.
9. Iwasaki H, Takahagi M, Nakata A, Shinagawa H. Escherichia coli RuvA and RuvB proteins specifically interact with holliday junctions and promote branch migration. Genes Dev. 6:1992;2214-2220.
10. Shah R, Cosstick R, West SC. The RuvC protein dimer resolves Holliday junction by a dual incision mechanism that involves base-specific contacts. EMBO J. 16:1997;1464-1472.
11. Shah R, Bennett RJ, West SC. Genetic recombination in E. coli RuvC protein cleaves Holliday junctions at resolution hotspots in vitro. Cell. 92:1994;853-864.
12. Tsaneva IR, Illing GT, Lloyd RG, West SC. Purification and physical properties of the RuvA and RuvB proteins of Escherichia coli. Mol Gen Genet. 235:1992;1-10.
13. Whitby MC, Bolt EL, Chan SN, Lloyd RG. Interactions between RuvA and RuvC at Holliday junctions: inhibition of junction cleavage and formation of a RuvA-RuvC-DNA complex. of outstanding interest J Mol Biol. 264:1996;878-890 The first in vitro evidence of the simultaneous binding of RuvA and RuvC to Holliday junction DNA.
14. Rafferty JB, Sedelnikova SE, Hargreaves D, Artymiuk PJ, Baker PJ, Sharples GJ, Mahdi AA, Lloyd RG, Rice DW. Crystal structure of DNA recombination protein RuvA and model for its binding to the Holliday junction. of outstanding interest Science. 274:1996;415-421 The first detailed insight into a component of the machinery of DNA branch migration responsible for binding the four-way branch point, which leads to models for the architecture of protein-Holliday junction complexes and proposals concerning the mechanism of branch migration and junction resolution.
15. Duckett DR, Murchie AIH, Diekmann S, Vonkitzing E, Kemper B, Lilley DMJ. The structure of the Holliday junction and its resolution. Cell. 55:1988;89-89.
16. Clegg RM, Murchie AIH, Zechel A, Lilley DMJ. The solution structure of the four way DNA junction at low-salt conditions-a fluorescence resonance energy transfer analysis. Biophys J. 66:1994;99-109.
17. Parsons CA, Stasiak A, Bennett RJ, West SC. Structure of a multisubunit complex that promotes DNA branch migration. Nature. 374:1995;375-378.
18. Yu X, West SC, Egelman EH. Structure and subunit composition of the RuvAB Holliday junction complex. of outstanding interest J Mol Biol. 266:1997;217-222 Electron microscopic and image analysis study reveals the low-resolution shape of a RuvAB-DNA complex, and in particular the shape of RuvB, which confirms the bipolar orientation of two RuvB hexamers on opposite arms of the Holliday junction. Mass and image analysis of the complex also suggests that two tetramers of RuvA sandwich the DNA under the conditions used.
19. Thayer MM, Ahern H, Xing D, Cunningham RP, Tainer JA. Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure. EMBO J. 14:1995;4108-4120.
20. Doherty AJ, Serpell LC, Ponting CP. The helix-hairpin-helix DNA-binding motif: a structural basis for non-sequence-specific recognition of DNA. of special interest Nucleic Acids Res. 24:1996;2488-2497 A sequence database analysis predicting the presence of a motif termed the helix-hairpin-helix in wide range of DNA-binding proteins including RuvA. The motif was first observed and described for endonuclease III [19] and is proposed to play a role in nonsequence-specific DNA interactions.
21. Stasiak A, Tsaneva IR, West SC, Benson CJB, Yu X, Egelman EH. The E. coli RuvB branch migration protein forms double hexameric rings around DNA. Proc Natl Acad Sci USA. 91:1994;7618-7622.
22. Mitchell AH, West SC. Hexameric rings of Escherichia coli RuvB protein: cooperative assembly, processivity and ATPase activity. J Mol Biol. 243:1994;208-215.
23. Hiom K, West SC. The mechanism of branch migration in homologous recombination: assembly of a RuvAB-Holliday junction complex in vitro. Cell. 80:1995;787-793.
24. Hiom K, Tsaneva IR, West SC. The directionality of RuvAB mediated branch migration in vitro studies with 3-armed junctions. Genes Cells. 1:1996;443-451.
25. Ariyoshi M, Vassylyev DG, 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.
26. Saito A, Iwasaki H, Ariyoshi M, Morikawa K, Shinagawa H. Indentification of four acidic amino acids that constitute the catalytic center of the RuvC Holliday junction resolvase. Proc Natl Acad Sci USA. 92:1995;7470-7474.
27. Mahdi AA, Sharples Mandal TM, Lloyd RG. Holliday junction resolvases encoded by homologous rusA genes in Escherichia coli K-12 and phage 82. J Mol Biol. 257:1996;561-573.
28. Mandal TN, Mahdi AA, Sharples GJ, Lloyd RG. Resolution of Holliday intermediates in recombination and DNA repair: indirect suppression of ruvA, ruvB and ruvC mutations. J Bacteriol. 175:1993;4325-4334.
29. Dunderdale HJ, Benson FE, Parsons CA, Sharples GJ, Lloyd RG, West SC. Formation and resolution and recombination intermediates by E. coli RecA and RuvC proteins. Nature. 354:1991;506-510.
30. Eggleston AK, Mitchell AH, West SC. In vitro reconstitution of the late steps of genetic recombination in Escherichia coli. of outstanding interest Cell. 89:1997;607-617 A seminal paper describing the in vitro reconstitution of recombination mediated by RecA and RuvABC proteins.
31. Guo F, Gopaul DN, Van Duyne GD. Structure of Cre recombinase complexed with DNA in a site-specific recombination synapse. of outstanding interest Nature. 389:1997;40-46 This paper descibes the structure of the P1 bacteriophage Cre recombinase, which catalyses site-specific recombination, bound to its DNA substrate. Four recombinases and two DNA sites from a synapsed structure in which the DNA resembles a cleaved Holliday junction intermediate.