Ring-shaped architecture of RecR: Implications for its role in homologous recombinational DNA repair

EMBO Journal

Volumn 23, Issue 10, 2004, Pages 2029-2038

  Lee II, Byung ^a   Kim, Kyoung Hoon ^a   Park, Soo Jeong ^b   Eom, Soo Hyun ^b   Song, Hyun Kyu ^c   Suh, Se Won ^a  

^a Seoul National University   (South Korea)

^b Gwangju Institute of Science and Technology (GIST)   (South Korea)

^c National Cancer Center   (South Korea)

Author keywords

DNA clamp; DNA repair; Homologous recombination; RecF pathway; RecR

Indexed keywords

DNA BINDING PROTEIN; RECR PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; DEINOCOCCUS RADIODURANS; DNA REPAIR; GENETIC STABILITY; HOMOLOGOUS RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; DEINOCOCCUS; DNA; DNA REPAIR; DNA-BINDING PROTEINS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; RECOMBINATION, GENETIC; SEQUENCE ALIGNMENT;

DEINOCOCCUS; DEINOCOCCUS RADIODURANS; PROKARYOTA;

EID: 2942563756     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600222     Document Type: Article

References (68)

1. Alley SC, Shier VK, Abel-Santos E, Sexton DJ, Soumillion P, Benkovic SJ (1999) Sliding clamp of the bacteriophage T4 polymerase has open and closed subunit interfaces in solution. Biochemistry 38: 7696-7709
2. Alonso JC, Stiege AC, Dobrinski B, Lurz R (1993) Purification and properties of the RecR protein from Bacillus subtilis 168. J Biol Chem 268: 1424-1429
3. Amundsen SK, Smith GR (2003) Interchangeable parts of the Escherichia coli recombination machinery. Cell 112: 741-744
4. Aono S, Hartsch T, Schulze-Gahmen U (2003) Crystallization of a member of the recFOR DNA repair pathway, RecO, with and without bound oligonucleotide. Acta Crystallogr D 59: 576-579
5. Aravind L, Leipe DD, Koonin EV (1998) Toprim-a conserved catalytic domain in type IA and II topoisomerase, DnaG-type primases, OLD family nuclease and RecR proteins. Nucleic Acids Res 26: 4205-4213
6. Aravind L, Walker DR, Koonin EV (1999) Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic Acids Res 27: 1223-1242
7. Ayora S, Alonso JC (1997) Purification and characterization of the RecF protein from Bacillus subtilis 168. Nucleic Acids Res 25: 2766-2772
8. Ayora S, Stiege AC, Lurz R, Alonso JC (1997) Bacillus subtilis 168 RecR protein-DNA complexes visualized as looped structures. Mol Gen Genet 254: 54-62
9. Beernink HT, Morrical SW (1999) RMPs: recombination/replication mediator proteins. Trends Biochem Sci 24: 385-389
10. Berger JM, Gamblin SJ, Harrison SC, Wang JC (1996) Structure and mechanism of DNA topoisomerases II. Nature 379: 225-232
11. Bork JM, Cox MM, Inman RB (2001) The RecOR proteins modulate RecA protein function at 5′ ends of single-stranded DNA. EMBO J 20: 7313-7322
12. Brünger AT (1992) The free R-value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355: 472-474
13. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang J-S, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D 54: 905-921
14. Christmann M, Tomicic MT, Roos WP, Kaina B (2003) Mechanisms of human DNA repair: an update. Toxicology 193: 3-34
15. Clark AJ (1991) Rec genes and homologous recombination proteins in Escherichia coli. Biochimie 73: 523-532
16. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D 50: 760-763
17. Courcelle J, Carswell-Crumpton C, Hanawalt PC (1997) recF and recR are required for the resumption of replication at DNA replication forks in Escherichia coli. Proc Natl Acad Sci USA 94: 3714-3719
18. Courcelle J, Ganesan AK, Hanawalt PC (2001) Therefore, what are recombination proteins there for? BioEssays 23: 463-470
19. Cox MM (1999) Recombinational DNA repair in bacteria and the RecA protein. Prog Nucleic Acid Res Mol Biol 63: 311-366
20. Cox MM (2001a) Historical overview: searching for replication help in all of the rec places. Proc Natl Acad Sci USA 98: 8173-8180
21. Cox MM (2001b) Recombinational DNA repair of damaged replication forks in Escherichia coli: questions. Annu Rev Genet 35: 53-82
22. Cox MM, Goodman MF, Kreuzer KN, Sherratt DJ, Shndler SJ, Marians KJ (2000) The importance of repairing stalled replication forks. Nature 404: 37-41
23. Doherty AJ, Serpell LC, Ponting CP (1996) The helix-hairpin-helix DNA-binding motif: a structural basis for non-specific-specific recognition of DNA. Nucleic Acids Res 24: 2488-2497
24. Griffin IV TJ, Kolodner RD (1990) Purification and preliminary characterization of the Escherichia coli K-12 recF protein. J Bacteriol 172: 6291-6299
25. Guan Y, Manuel RC, Arvai AS, Parikh SS, Mol CD, Miller JH, Lloyd S, Tainer JA (1998) MutY catalytic core, mutant and bound adenine structures define specificity for DNA repair enzyme superfamily. Nat Struct Biol 5: 1058-1064
26. WAF1/C1P1 complexed with human PCNA. Cell 87: 297-306
27. Hegde SP, Qin M-H, Li X-H, Atkinson MA, Clark AJ, Rajagopalan M, Madiraju MV (1996) Interactions of RecF protein with RecO, RecR, and single-stranded DNA binding proteins reveal roles for the RecF-RecO-RecR complex in DNA repair and recombination. Proc Natl Acad Sci USA 93: 14468-14473
28. Hingorani MM, O'Donnell M (2000) A tale of toroids in DNA metabolism. Nat Rev Mol Cell Biol 1: 22-30
29. Holm L, Sander C (1995) Dali: a network tool for protein structure comparison. Trends Biochem Sci 20: 478-480
30. Ikegami T, Kuraoka I, Saijo M, Kodo N, Kyogoku Y, Morikawa K, Tanaka K, Shirakawa M (1998) Solution structure of the DNA- and RPA-binding domain of the human repair factor XPA. Nat Struct Biol 5: 701-706
31. Jeruzalmi D, Yurieva O, Zhao Y, Young M, Stewart J, Hingorani M, O'Donnell M, Kuriyan J (2001) Mechanism of processivity clamp opening by the delta subunit wrench of the clamp loader complex of E. coli DNA polymerase III. Cell 106: 417-428
32. Jones TA, Zou J-Y, Cowan SW, Kjeldgaard M (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47: 110-119
33. Kantake N, Madiraju MV, Sugiyama T, Kowalczykowski SC (2002) Escherichia coli RecO protein anneals ssDNA complexed with its cognate ssDNA-binding protein: a common step in genetic recombination. Proc Natl Acad Sci USA 99: 15327-15332
34. Kato M, Ito T, Wagner G, Richardson CC, Ellenberger T (2003) Modular architecture of the bacteriophage T7 primase couples RNA primer synthesis to DNA synthesis. Mol Cell 11: 1349-1360
35. Keck JL, Roche DD, Lynch AS, Berger JM (2000) Structure of the RNA polymerase domain of E. coli primase. Science 287: 2482-2486
36. Kitayama S, Narumi I, Kikuchi M, Watanabe H (2000) Mutation in recR gene of Deinococcus radiodurans and possible involvement of its product in the repair of DNA interstrand cross-links. Mutat Res 461: 179-187
37. Klug A, Schwabe JW (1995) Protein motifs 5. Zinc fingers. FASEB J 9: 597-604
38. Kong XP, Onrust R, O'Donnell M, Kuriyan J (1992) Three-dimensional structure of the β subunit of E. coli DNA polymerase III holoenzyme: a sliding DNA clamp. Cell 69: 425-437
39. Kovall R, Matthews BW (1997) Toroidal structure of λ-exonuclease. Science 277: 1824-1827
40. Kreuzer KN (2000) Recombination-dependent DNA replication in phage T4. Trends Biochem Sci 25: 165-173
41. Krishna TS, Kong XP, Gary S, Burgers PM, Kuriyan J (1994) Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell 79: 1233-1243
42. Kuzminov A (1999) Recombinational repair of DNA damage in Escherichia coli and bacteriophage λ. Microbiol Mol Biol Rev 63: 751-813
43. Labahn J, Scharer OD, Long A, Ezaz-Nikpay K, Verdine GL, Ellenberger TE (1996) Structural basis for the excision repair of alkylation-damaged DNA. Cell 86: 321-329
44. Lee BI, Kim KH, Shim SM, Ha KS, Yang JK, Yoon H-J, Ha JY, Suh SW (2004) Crystallization and preliminary X-ray crystallographic analysis of the RecR protein from Deinococcus radiodurans, a member of the RecFOR DNA-repair pathway. Acta Crystallogr D 60: 379-381
45. +-dependent DNA ligase: molecular architecture and functional implications. EMBO J 19: 1119-1129
46. Lima CD, Wang JC, Mondragon A (1994) Three-dimensional structure of the 67K N-terminal fragment of E. coli DNA topoisomerase I. Nature 367: 138-146
47. Luisi-DeLuca C (1995) Homologous pairing of single-stranded DNA and superhelical double-stranded DNA by RecO protein from Escherichia coli. J Bacteriol 177: 566-572
48. Luisi-DeLuca C, Kolodner R (1994) Purification and characterization of the Escherichia coli RecO protein. Renaturation of complementary single-stranded DNA molecules catalyzed by the RecO protein. J Mol Biol 236: 124-138
49. Lusetti SL, Shaw JJ, Cox MM (2003) Magnesium ion-dependent activation of the RecA protein involves the C terminus. J Biol Chem 278: 16381-16388
50. Mackay JP, Crossley M (1998) Zinc fingers are sticking together. Trends Biochem Sci 23: 1-4
51. Madiraju MV, Clark AJ (1992) Evidence for ATP binding and double-stranded DNA binding by Escherichia coli RecF protein. J Bacteriol 174: 7705-7710
52. Marians KJ (2000) PriA-directed replication fork restart in Escherichia coli. Trends Biochem Sci 25: 185-189
53. Moarefi I, Jeruzalmi D, Turner J, O'Donnell M, Kuriyan J (2000) Crystal structure of the DNA polymerase processivity factor of T4 bacteriophage. J Mol Biol 296: 1215-1223
54. Morimatsu K, Kowalczykowski SC (2003) RecFOR proteins load RecA protein onto gapped DNA to accelerate DNA strand exchange: a universal step of recombinational repair. Mol Cell 11: 1337-1347
55. Mullen GP, Wilson SH (1997) DNA polymerase β in abasic site repair: a structurally conserved helix-hairpin-helix motif in lesion detection by base excision repair enzymes. Biochemistry 36: 4713-4717
56. Nichols MD, DeAngelis K, Keck JL, Berger JM (1999) Structure and function of an archaeal topoisomerase IV subunit with homology to the meiotic recombination factor Spo11. EMBO J 18: 6177-6188
57. Peláez AI, Ribas-Aparicio RM, Gómez A, Rodicio MR (2001) Structural and functional characterization of the recR gene of Streptomyces. Mol Genet Genomics 265: 663-672
58. Podobnik M, Mclnerney P, O'Donnell M, Kuriyan J (2000) A Toprim domain in the crystal structure of the catalytic core of Escherichia coli primase confirms a structural link to DNA topoisomerases. J Mol Biol 300: 353-362
59. Schmiedeskamp M, Klevit RE (1994) Zinc finger diversity. Curr Opin Struct Biol 4: 28-35
60. Shan Q, Bork JM, Webb BL, Inman RB, Cox MM (1997) RecA protein filaments: end-dependent dissociation from ssDNA and stabilization by RecO and RecR proteins. J Mol Biol 265: 519-540
61. Terwilliger TC, Berendzen J (1999) Automated MAD and MIR structure solution. Acta Crystallogr D 55: 849-861
62. Thayer MM, Ahern H, Xing D, Cunningham RP, Tainer JA (1995) Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure. EMBO J 14: 4108-4120
63. Umezu K, Kolodner RD (1994) Protein interactions in genetic recombination in Escherichia coli. Interactions involving RecO and RecR overcome the inhibition of RecA by single-stranded DNA-binding protein. J Biol Chem 269: 30005-30013
64. Walker JE, Saraste M, Runswick MJ, Gay NJ (1982) Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1: 945-951
65. Webb BL, Cox MM, Inman RB (1995) An interaction between the Escherichia coli RecF and RecR proteins dependent on ATP and double-stranded DNA. J Biol Chem 270: 31397-31404
66. Webb BL, Cox MM, Inman RB (1997) Recombinational DNA repair: the RecF and RecR proteins limit the extension of RecA filaments beyond single-strand DNA gaps. Cell 91: 347-356
67. Webb BL, Cox MM, Inman RB (1999) ATP hydrolysis and DNA binding by the Escherichia coli RecF protein. J Biol Chem 274: 15367-15374
68. West SC (2003) Molecular views of recombination proteins and their control. Nat Rev Mol Cell Biol 4: 435-445