Structural and Functional Characterisation of a Conserved Archaeal RadA Paralog with Antirecombinase Activity

Journal of Molecular Biology

Volumn 389, Issue 4, 2009, Pages 661-673

  McRobbie, Anne Marie ^a   Carter, Lester G ^a   Kerou, Melina ^a   Liu, Huanting ^a   McMahon, Stephen A ^a   Johnson, Kenneth A ^a   Oke, Muse ^a   Naismith, James H ^a   White, Malcolm F ^a  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

archaea; homologous recombination; RadA; recombinase; strand exchange

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; DNA DEPENDENT PROTEIN KINASE; RADA PROTEIN; RECA PROTEIN; RECOMBINASE; SINGLE STRANDED DNA; SSO2452 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME INHIBITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN STRUCTURE; SULFOLOBUS SOLFATARICUS; ULTRAVIOLET RADIATION;

ARCHAEA; EUKARYOTA; SULFOLOBUS SOLFATARICUS;

EID: 65849188791     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.04.060     Document Type: Article

References (63)

1. Cox M.M. The bacterial RecA protein as a motor protein. Annu. Rev. Microbiol. 57 (2003) 551-577
2. Kowalczykowski S.C., and Eggleston A.K. Homologous pairing and DNA strand-exchange proteins. Annu. Rev. Biochem. 63 (1994) 991-1043
3. Sonoda E., Sasaki M.S., Buerstedde J.M., Bezzubova O., Shinohara A., Ogawa H., et al. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 17 (1998) 598-608
4. McGlynn P., and Lloyd R.G. Recombinational repair and restart of damaged replication forks. Nat. Rev. Mol. Cell Biol. 3 (2002) 859-870
5. Sung P., Krejci L., Van Komen S., and Sehorn M.G. Rad51 recombinase and recombination mediators. J. Biol. Chem. 278 (2003) 42729-42732
6. Masson J.Y., Tarsounas M.C., Stasiak A.Z., Stasiak A., Shah R., McIlwraith M.J., et al. Identification and purification of two distinct complexes containing the five RAD51 paralogs. Genes Dev. 15 (2001) 3296-3307
7. Liu N., Schild D., Thelen M.P., and Thompson L.H. Involvement of Rad51C in two distinct protein complexes of Rad51 paralogs in human cells. Nucleic Acids Res. 30 (2002) 1009-1015
8. Thacker J. The RAD51 gene family, genetic instability and cancer. Cancer Lett. 219 (2005) 125-135
9. Liu Y., Tarsounas M., O'Regan P., and West S.C. Role of RAD51C and XRCC3 in genetic recombination and DNA repair. J. Biol. Chem. 282 (2007) 1973-1979
10. Sung P. Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad51 recombinase. Genes Dev. 11 (1997) 1111-1121
11. Kelman Z., and White M.F. Archaeal DNA replication and repair. Curr. Opin. Microbiol. 8 (2005) 669-676
12. Bell S.D., Magill C.P., and Jackson S.P. Basal and regulated transcription in Archaea. Biochem. Soc. Trans. 29 (2001) 392-395
13. Bell S.D., and Jackson S.P. Transcription and translation in Archaea: a mosaic of eukaryal and bacterial features. Trends Microbiol. 6 (1998) 222-228
14. Hopfner K.P., Karcher A., Craig L., Woo T.T., Carney J.P., and Tainer J.A. Structural biochemistry and interaction architecture of the DNA double-strand break repair Mre11 nuclease and Rad50-ATPase. Cell 105 (2001) 473-485
15. Shin D.S., Chahwan C., Huffman J.L., and Tainer J.A. Structure and function of the double-strand break repair machinery. DNA Repair (Amst.) 3 (2004) 863-873
16. Lin Z., Kong H., Nei M., and Ma H. Origins and evolution of the recA/RAD51 gene family: evidence for ancient gene duplication and endosymbiotic gene transfer. Proc. Natl Acad. Sci. USA 103 (2006) 10328-10333
17. Akiba T., Ishii N., Rashid N., Morikawa M., Imanaka T., and Harata K. Structure of RadB recombinase from a hyperthermophilic archaeon, Thermococcus kodakaraensis KOD1: an implication for the formation of a near-7-fold helical assembly. Nucleic Acids Res. 33 (2005) 3412-3423
18. Komori K., Miyata T., DiRuggiero J., Holley-Shanks R., Hayashi I., Cann K., et al. Both RadA and RadB are involved in homologous recombination in Pyrococcus furiosus. J. Biol. Chem. 275 (2000) 33782-33790
19. Guy C.P., Haldenby S., Brindley A., Walsh D.A., Briggs G.S., Warren M.J., et al. Interactions of RadB, a DNA repair protein in archaea, with DNA and ATP. J. Mol. Biol. 358 (2006) 46-56
20. Waters E., Hohn M.J., Ahel I., Graham D.E., Adams M.D., Barnstead M., et al. The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism. Proc. Natl Acad. Sci. USA 100 (2003) 12984-12988
21. Haldenby S., White M.F., and Allers T. RecA family proteins in archaea: RadA and its cousins. Biochem. Soc. Trans. 37 (2009) 102-107
22. Wang J. Recent cyanobacterial Kai protein structures suggest a rotary clock. Structure 13 (2005) 735-741
23. Sheng D., Zhu S., Wei T., Ni J., and Shen Y. The in vitro activity of a Rad55 homologue from Sulfolobus tokodaii, a candidate mediator in RadA-catalyzed homologous recombination. Extremophiles 12 (2008) 147-157
24. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29 (2001) e45
25. Götz D., Paytubi S., Munro S., Lundgren M., Bernander R., and White M.F. Responses of hyperthermophilic crenarchaea to UV irradiation. Genome Biol. 8 (2007) R220
26. Salerno V., Napoli A., White M.F., Rossi M., and Ciaramella M. Transcriptional response to DNA damage in the archaeon Sulfolobus solfataricus. Nucleic Acids Res. 31 (2003) 6127-6138
27. Cubeddu L., and White M.F. DNA damage detection by an archaeal single-stranded DNA-binding protein. J. Mol. Biol. 353 (2005) 507-516
28. Fröls S., Gordon P.M., Panlilio M.A., Duggin G., Bell S.D., Sensen C.W., and Schleper C. Response of the hyperthermophilic archaeon Sulfolobus solfataricus to UV damage. J. Bacteriol. 189 (2007) 8708-8718
29. Abella M., Rodriquez S., Paytubi S., Campoy S., White M.F., and Barbe J. The Sulfolobus solfataricus radA paralogue sso0777 is DNA damage inducible and positively regulated by the Sta1 protein. Nucleic Acids Res. 35 (2007) 6788-6797
30. Seitz E.M., Brockman J.P., Sandler S.J., Clark A.J., and Kowalczykowski S.C. RadA protein is an archaeal RecA protein homolog that catalyzes DNA strand exchange. Genes Dev. 12 (1998) 1248-1253
31. Jain S.K., Cox M.M., and Inman R.B. On the role of ATP hydrolysis in RecA protein-mediated DNA strand exchange: III. Unidirectional branch migration and extensive hybrid DNA formation. J. Biol. Chem. 269 (1994) 20653-20661
32. 2+ activates human homologous recombination protein Rad51 by modulating its ATPase activity. Proc. Natl Acad. Sci. USA 101 (2004) 9988-9993
33. Jelinska C., Conroy M.J., Craven C.J., Hounslow A.M., Bullough P.A., Waltho J.P., et al. Obligate heterodimerization of the archaeal Alba2 protein with Alba1 provides a mechanism for control of DNA packaging. Structure 13 (2005) 963-971
34. Morrical S.W., and Cox M.M. Stabilization of recA protein-ssDNA complexes by the single-stranded DNA binding protein of Escherichia coli. Biochemistry 29 (1990) 837-843
35. Sigurdsson S., Van Komen S., Bussen W., Schild D., Albala J.S., and Sung P. Mediator function of the human Rad51B-Rad51C complex in Rad51/RPA-catalyzed DNA strand exchange. Genes Dev. 15 (2001) 3308-3318
36. Lusetti S.L., and Cox M.M. The bacterial RecA protein and the recombinational DNA repair of stalled replication forks. Annu. Rev. Biochem. 71 (2002) 71-100
37. Krissinel E., and Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2256-2268
38. Logan K.M., Forget A.L., Verderese J.P., and Knight K.L. ATP-mediated changes in cross-subunit interactions in the RecA protein. Biochemistry 40 (2001) 11382-11389
39. Aihara H., Ito Y., Kurumizaka H., Yokoyama S., and Shibata T. 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 (1999) 495-504
40. Kinebuchi T., Kagawa W., Kurumizaka H., and Yokoyama S. Role of the N-terminal domain of the human DMC1 protein in octamer formation and DNA binding. J. Biol. Chem. 280 (2005) 28382-28387
41. Shin D.S., Pellegrini L., Daniels D.S., Yelent B., Craig L., Bates D., et al. Full-length archaeal Rad51 structure and mutants: mechanisms for RAD51 assembly and control by BRCA2. EMBO J. 22 (2003) 4566-4576
42. Chen Z., Yang H., and Pavletich N.P. Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453 (2008) 489-494
43. Chen L.T., Ko T.P., Chang Y.W., Lin K.A., Wang A.H., and Wang T.F. Structural and functional analyses of five conserved positively charged residues in the L1 and N-terminal DNA binding motifs of archaeal RADA protein. PLoS ONE 2 (2007) e858
44. Wang T.F., Chen L.T., and Wang A.H. Right or left turn? RecA family protein filaments promote homologous recombination through clockwise axial rotation. BioEssays 30 (2008) 48-56
45. Krejci L., Van Komen S., Li Y., Villemain J., Reddy M.S., Klein H., et al. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423 (2003) 305-309
46. Bohr A. Rising from the RecQ-age: the role of human RecQ helicases in genome maintenance. Trends Biochem. Sci. 33 (2008) 609-620
47. Ariza A., Richard D.J., White M.F., and Bond C.S. Conformational flexibility revealed by the crystal structure of a crenarchaeal RadA. Nucleic Acids Res. 33 (2005) 1465-1473
48. Wadsworth R.I., and White M.F. Identification and properties of the crenarchaeal single-stranded DNA binding protein from Sulfolobus solfataricus. Nucleic Acids Res. 29 (2001) 914-920
49. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26 (1993) 795-800
50. Matthews B.W. Solvent content of protein crystals. J. Mol. Biol. 33 (1968) 491-497
51. Storoni L.C., McCoy A.J., and Read R.J. Likelihood-enhanced fast rotation functions. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 432-438
52. McCoy A.J., Grosse-Kunstleve R.W., Storoni L.C., and Read R.J. Likelihood-enhanced fast translation functions. Acta Crystallogr., Sect. D: Biol. Crystallogr. 61 (2005) 458-464
53. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 (1994) 760-763
54. Morris R.J., Perrakis A., and Lamzin V.S. ARP/wARP's model-building algorithms: I. The main chain. Acta Crystallogr., Sect. D: Biol. Crystallogr. 58 (2002) 968-975
55. Perrakis A., Morris R., and Lamzin V.S. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6 (1999) 458-463
56. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr., Sect. D: Biol. Crystallogr. 53 (1997) 240-255
57. Murshudov G.N., Vagin A.A., Lebedev A., Wilson K.S., and Dodson E.J. Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallogr., Sect. D: Biol. Crystallogr. 55 (1999) 247-255
58. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2126-2132
59. Winn M.D., Murshudov G.N., and Papiz M.Z. Macromolecular TLS refinement in REFMAC at moderate resolutions. Macromol. Crystallogr., Part D 374 (2003) 300-321
60. Winn M.D., Isupov M.N., and Murshudov G.N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr., Sect. D: Biol. Crystallogr. 57 (2001) 122-133
61. Davis W., Murray L.W., Richardson J.S., and Richardson D.C. MolProbity: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res. 32 (2004) W615-W619
62. Dorazi R., Götz D., Munro S., Bernander R., and White M.F. Equal rates of repair of DNA photoproducts in transcribed and non-transcribed strands in Sulfolobus solfataricus. Mol. Microbiol. 63 (2007) 521-529
63. Reid S.L., Parry D., Liu H.H., and Connolly B.A. Binding and recognition of GATATC target sequences by the EcoRV restriction endonuclease: a study using fluorescent oligonucleotides and fluorescence polarization. Biochemistry 40 (2001) 2484-2494