ATP half-sites in RadA and RAD51 recombinases bind nucleotides

FEBS Open Bio

Volumn 6, Issue 5, 2016, Pages 372-385

  Marsh, May E ^a,b   Scott, Duncan E ^a   Ehebauer, Matthias T ^a,c   Abell, Chris ^a   Blundell, Tom L ^a   Hyvönen, Marko ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b PAUL SCHERRER INSTITUTE   (Switzerland)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

ATPase; Homologous recombination; Nucleotide binding site; RAD51; RadA; Specificity

Indexed keywords

ADENOSINE TRIPHOSPHATE; MONOMER; RAD51 PROTEIN; RADA RECOMBINASE; RECOMBINASE; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; HOMOLOGOUS RECOMBINATION; HUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN STRUCTURE; PYROCOCCUS FURIOSUS;

EID: 84962826132     PISSN: 22115463     EISSN: None     Source Type: Journal    
DOI: 10.1002/2211-5463.12052     Document Type: Article

References (67)

1. Courcelle J, Ganesan AK and Hanawalt PC (2001) Therefore, what are recombination proteins there for? BioEssays 23, 463-470.
2. Cox M (1998) A broadening view of recombinational DNA repair in bacteria. Genes Cells 3, 65-78.
3. Kowalczykowski SC (2000) Initiation of genetic recombination and recombination-dependent replication. Trends Biochem Sci 25, 156-165.
4. Lusetti SL and Cox MM (2002) The bacterial RecA protein and the recombinational DNA repair of stalled replication forks. Annu Rev Biochem 71, 71-100.
5. Clark AJ and Margulies AD (1965) Isolation and Characterization of recombination-deficient mutants of Escherichia coli K12. Proc Natl Acad Sci USA 53, 451-459.
6. Sandler SJ, Satin LH, Samra HS and Clark AJ (1996) recA-like genes from three archaean species with putative protein products similar to Rad51 and Dmc1 proteins of the yeast Saccharomyces cerevisiae. Nucleic Acids Res 24, 2125-2132.
7. Shinohara A, Ogawa H and Ogawa T (1992) Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69, 457-470.
8. Dillingham M, Spies M and Kowalczykowski S (2003) RecBCD enzyme is a bipolar DNA helicase. Nature 423, 893-897.
9. Taylor AF and Smith GR (2003) RecBCD enzyme is a DNA helicase with fast and slow motors of opposite polarity. Nature 423, 889-893.
10. Bianco PR, Tracy RB and Kowalczykowski SC (1998) DNA strand exchange proteins: a biochemical and physical comparison. Front Biosci 3, D570-D603.
11. Aihara H, Ito Y, Kurumizaka H, Terada T, Yokoyama S and Shibata T (1997) An interaction between a specified surface of the C-terminal domain of RecA protein and double-stranded DNA for homologous pairing. J Mol Biol 274, 213-221.
12. Aihara H, Ito Y, Kurumizaka H, Yokoyama S and Shibata T (1999) The N-terminal domain of the human Rad51 protein binds DNA: structure and a DNA binding surface as revealed by NMR. J Mol Biol 290, 495-504.
13. Egelman E and Yu X (1989) The location of DNA in RecA-DNA helical filaments. Science 245, 404.
14. Ogawa T, Yu X, Shinohara A and Egelman EH (1993) Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science 259, 1896-1899.
15. Yu X, Jacobs SA, West SC, Ogawa T and Egelman EH (2001) Domain structure and dynamics in the helical filaments formed by RecA and Rad51 on DNA. Proc Natl Acad Sci USA 98, 8419-8424.
16. Benson F, Stasiak A and West S (1994) Purification and characterization of the human Rad51 protein, an analogue of E. coli RecA. EMBO J 13, 5764-5771.
17. Gupta RC, Bazemore LR, Golub EI and Radding CM (1997) Activities of human recombination protein Rad51. Proc Natl Acad Sci USA 94, 463-468.
18. Namsaraev E and Berg P (1997) Characterization of strand exchange activity of yeast Rad51 protein. Mol Cell Biol 17, 5359-5368.
19. Sung P and Robberson DL (1995) DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell 82, 453-461.
20. Chen Z, Yang H and Pavletich NP (2008) Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453, 489-494.
21. Shin DS, Pellegrini L, Daniels DS, Yelent B, Craig L, Bates D, Yu DS, Shivji MK, Hitomi C, Arvai AS et al. (2003) Full-length archaeal Rad51 structure and mutants: mechanisms for RAD51 assembly and control by BRCA2. EMBO J 22, 4566-4576.
22. Yang S, Yu X, Seitz EM, Kowalczykowski SC and Egelman EH (2001) Archaeal RadA protein binds DNA as both helical filaments and octameric rings. J Mol Biol 314, 1077-1085.
23. Yu X and Egelman EH (1997) The RecA hexamer is a structural homologue of ring helicases. Nat Struct Biol 4, 101-104.
24. Datta S, Krishna R, Ganesh N, Chandra N, Muniyappa K and Vijayan M (2003) Crystal structures of Mycobacterium smegmatis RecA and its nucleotide complexes. J Bacteriol 185, 4280-4284.
25. Rajan R and Bell CE (2004) Crystal structure of RecA from Deinococcus radiodurans: insights into the structural basis of extreme radioresistance. J Mol Biol 344, 951-963.
26. Sheridan SD, Yu X, Roth R, Heuser JE, Sehorn MG, Sung P, Egelman EH and Bishop DK (2008) A comparative analysis of Dmc1 and Rad51 nucleoprotein filaments. Nucleic Acids Res 36, 4057-4066.
27. Story R, Weber I and Steitz T (1992) The structure of the E. coli RecA protein monomer and polymer. Nature 355, 318-325.
28. Wyman C, Ristic D and Kanaar R (2004) Homologous recombination-mediated double-strand break repair. DNA Repair (Amst) 3, 827-833.
29. Kelley De Zutter J, Forget AL, Logan KM and Knight KL (2001) Phe217 regulates the transfer of allosteric information across the subunit interface of the RecA protein filament. Structure 9, 47-55.
30. McGrew DA and Knight KL (2003) Molecular design and functional organization of the RecA protein. Crit Rev Biochem Mol Biol 38, 385-432.
31. Skiba MC and Knight KL (1994) Functionally important residues at a subunit interface site in the RecA protein from Escherichia coli. J Biol Chem 269, 3823-3828.
32. VanLoock MS, Yu X, Yang S, Lai A, Low C, Campbell MJ and Engleman EH (2003) ATP-mediated conformational changes in the RecA filament. Structure 11, 187-196.
33. Conway AB, Lynch TW, Zhang Y, Fortin GS, Fung CW, Symington LS and Rice PA (2004) Crystal structure of a Rad51 filament. Nat Struct Mol Biol 11, 791-796.
34. Li Y, He Y and Luo Y (2009) Crystal structure of an archaeal Rad51 homologue in complex with a metatungstate inhibitor. Biochemistry 48, 6805-6810.
35. Wu Y, He Y, Moya IA, Qian X and Luo Y (2004) Crystal structure of archaeal recombinase RADA: a snapshot of its extended conformation. Mol Cell 15, 423-435.
36. Datta S, Prabu MM, Vaze MB, Ganesh N, Chandra NR, Muniyappa K and Vijayan M (2000) Crystal structures of Mycobacterium tuberculosis RecA and its complex with ADP-AlF(4): implications for decreased ATPase activity and molecular aggregation. Nucleic Acids Res 28, 4964-4973.
37. Qian X, Wu Y, He Y and Luo Y (2005) Crystal structure of Methanococcus voltae RadA in complex with ADP: hydrolysis-induced conformational change. Biochemistry 44, 13753-13761.
38. Wu Y, Qian X, He Y, Moya IA and Luo Y (2005) Crystal structure of an ATPase-active form of Rad51 homolog from Methanococcus voltae. Insights into potassium dependence. J Biol Chem 280, 722-728.
39. Grigorescu AA, Vissers JHA, Ristic D, Pigli YZ, Lynch TW, Wyman C and Rice PA (2009) Inter-subunit interactions that coordinate Rad51's activities. Nucleic Acids Res 37, 557-567.
40. Chen J, Villanueva N, Rould MA and Morrical SW (2010) Insights into the mechanism of Rad51 recombinase from the structure and properties of a filament interface mutant. Nucleic Acids Res 38, 4889-4906.
41. Erzberger JP and Berger JM (2006) Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu Rev Biophys Biomol Struct 35, 93-114.
42. Li Y, He Y and Luo Y (2009) Conservation of a conformational switch in RadA recombinase from Methanococcus maripaludis. Acta Crystallogr D Biol Crystallogr 65, 602-610.
43. Baumann P, Benson FE and West SC (1996) Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell 87, 757-766.
44. Chi P, Van Komen S, Sehorn MG, Sigurdsson S and Sung P (2006) Roles of ATP binding and ATP hydrolysis in human Rad51 recombinase function. DNA Repair (Amst) 5, 381-391.
45. Morrison C, Shinohara A, Sonoda E, Yamaguchi-Iwai Y, Takata M, Weichselbaum RR and Takeda S (1999) The essential functions of human Rad51 are independent of ATP hydrolysis. Mol Cell Biol 19, 6891-6897.
46. Rehrauer WM and Kowalczykowski SC (1993) Alteration of the nucleoside triphosphate (NTP) catalytic domain within Escherichia coli recA protein attenuates NTP hydrolysis but not joint molecule formation. J Biol Chem 268, 1292-1297.
47. Sung P (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265, 1241-1243.
48. Sung P and Stratton S (1996) Yeast Rad51 recombinase mediates polar DNA strand exchange in the absence of ATP hydrolysis. J Biol Chem 271, 27983-27986.
49. Stark JM, Hu P, Pierce AJ, Moynahan ME, Ellis N and Jasin M (2002) ATP hydrolysis by mammalian RAD51 has a key role during homology-directed DNA repair. J Biol Chem 277, 20185-20194.
50. Cox MM (2003) The bacterial RecA protein as a motor protein. Annu Rev Microbiol 57, 551-577.
51. Ristic D, Modesti M, van der Heijden T, van Noort J, Dekker C, Kanaar R and Wyman C (2005) Human Rad51 filaments on double- and single-stranded DNA: correlating regular and irregular forms with recombination function. Nucleic Acids Res 33, 3292-3302.
52. Niesen FH, Berglund H and Vedadi M (2007) The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat Protoc 2, 2212-2221.
53. Pellegrini L, Yu DS, Lo T, Anand S, Lee M, Blundell TL and Venkitaraman AR (2002) Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature 420, 287-293.
54. Saraste M, Sibbald P and Wittinghofer A (1990) The P-loop-a common motif in ATP-and GTP-binding proteins. Trends Biochem Sci 15, 30-34.
55. Logan K and Knight K (1993) Mutagenesis of the P-loop motif in the ATP binding site of the RecA protein from Escherichia coli. J Mol Biol 232, 1048-1059.
56. Konola J, Logan K and Knight K (1994) Functional characterization of residues in the P-loop motif of the RecA protein ATP binding site. J Mol Biol 237, 20-34.
57. Kelley JA and Knight KL (1997) Allosteric regulation of RecA protein function is mediated by Gln194. J Biol Chem 272, 25778-25782.
58. Voloshin ON, Wang L and Camerini-Otero RD (2000) The homologous pairing domain of RecA also mediates the allosteric regulation of DNA binding and ATP hydrolysis: a remarkable concentration of functional residues. J Mol Biol 303, 709-720.
59. Galkin VE, Wu Y, Zhang X-P, Qian X, He Y, Yu X, Heyer W-D, Luo Y and Egelman EH (2006) The Rad51/RadA N-terminal domain activates nucleoprotein filament ATPase activity. Structure 14, 983-992.
60. Fiala G and Stetter KO (1986) Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100 C. Arch Microbiol 145, 56-61.
61. Peränen J, Rikkonen M, Hyvönen M and Kääriäinen L (1996) T7 vectors with modified T7lac promoter for expression of proteins in Escherichia coli. Anal Biochem 236, 371.
62. Brinkmann U, Mattes R and Buckel P (1989) High-level expression of recombinant genes in Escherichia coli is dependent on the availability of the dnaY gene product. Gene 85, 109-114.
63. Kabsch W (2010) XDS. Acta Crystallogr D Biol Crystallogr 66, 125-132.
64. Trapani S and Navaza J (2008) AMoRe: classical and modern. Acta Crystallogr D Biol Crystallogr 64, 11-16.
65. Murshudov GN, Skubák P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F and Vagin AA (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr 67, 355-367.
66. Emsley P and Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126-2132.
67. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung L-W, Kapral GJ, Grosse-Kunstleve RW et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66, 213-221.