Mutants of phage bIL67 RuvC with enhanced Holliday junction binding selectivity and resolution symmetry

Molecular Microbiology

Volumn 89, Issue 6, 2013, Pages 1240-1258

  Green, Victoria ^a   Curtis, Fiona A ^b   Sedelnikova, Svetlana ^a   Rafferty, John B ^a   Sharples, Gary J ^b  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b DURHAM UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; CELL PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; RUVC PROTEIN; UNCLASSIFIED DRUG; YDC2 PROTEIN;

ARTICLE; BACTERIOPHAGE; BACTERIOPHAGE BLL67; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA BINDING; DNA PURIFICATION; DNA SEQUENCE; ENZYME SPECIFICITY; HOLLIDAY JUNCTION; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR INTERACTION; MOLECULAR MODEL; MOLECULAR RECOGNITION; MOLECULAR STABILITY; NONHUMAN; NUCLEOTIDE BINDING SITE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DNA BINDING; SITE DIRECTED MUTAGENESIS;

BACTERIA (MICROORGANISMS);

AMINO ACID SUBSTITUTION; BACTERIOPHAGES; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DNA, CRUCIFORM; HOLLIDAY JUNCTION RESOLVASES; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY;

EID: 84884292511     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12343     Document Type: Article

References (53)

1. Ariyoshi, M., Vassylyev, D.G., Iwasaki, H., Nakamura, H., Shinagawa, H., and Morikawa, K. (1994) Atomic structure of the RuvC resolvase: a Holliday junction-specific endonuclease from E. coli. Cell 78: 1063-1072.
2. Atkinson, J., and McGlynn, P. (2009) Replication fork reversal and the maintenance of genome stability. Nucleic Acids Res 37: 3475-3492.
3. Ayora, S., Carrasco, B., Doncel-Perez, E., Lurz, R., and Alonso, J.C. (2004) Bacillus subtilis RecU protein cleaves Holliday junctions and anneals single-stranded DNA. Proc Natl Acad Sci USA 101: 452-457.
4. Bennett, R.J., and West, S.C. (1995) Structural analysis of the RuvC-Holliday junction complex reveals an unfolded junction. J Mol Biol 252: 213-226.
5. Benson, F.E., and West, S.C. (1994) Substrate specificity of the Escherichia coli RuvC protein. Resolution of three- and four-stranded recombination intermediates. J Biol Chem 269: 5195-5201.
6. Bidnenko, E., Ehrlich, S.D., and Chopin, M.C. (1998) Lactococcus lactis phage operon coding for an endonuclease homologous to RuvC. Mol Microbiol 28: 823-834.
7. Biertumpfel, C., Yang, W., and Suck, D. (2007) Crystal structure of T4 endonuclease VII resolving a Holliday junction. Nature 449: 616-620.
8. Bond, C.S., Kvaratskhelia, M., Richard, D., White, M.F., and Hunter, W.N. (2001) Structure of Hjc, a Holliday junction resolvase, from Sulfolobus solfataricus. Proc Natl Acad Sci USA 98: 5509-5514.
9. Center, M.S., Studier, F.W., and Richardson, C.C. (1970) The structural gene for a T7 endonuclease essential for phage DNA synthesis. Proc Natl Acad Sci USA 65: 242-248.
10. Ceschini, S., Keeley, A., McAlister, M.S., Oram, M., Phelan, J., Pearl, L.H., etal. (2001) Crystal structure of the fission yeast mitochondrial Holliday junction resolvase Ydc2. EMBO J 20: 6601-6611.
11. Chen, L., Shi, K., Yin, Z., and Aihara, H. (2013) Structural asymmetry in the Thermus thermophilus RuvC dimer suggests a basis for sequential strand cleavages during Holliday junction resolution. Nucleic Acids Res 41: 648-656.
12. Chen, V.B., Arendall, W.B., 3rd, Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., etal. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D66: 12-21.
13. Churchill, M.E., Tullius, T.D., Kallenbach, N.R., and Seeman, N.C. (1988) A Holliday recombination intermediate is two-fold symmetric. Proc Natl Acad Sci USA 85: 4653-4656.
14. Culyba, M.J., Minkah, N., Hwang, Y., Benhamou, O.M., and Bushman, F.D. (2007) DNA branch nuclease activity of vaccinia A22 resolvase. J Biol Chem 282: 34644-34652.
15. Curtis, F.A., Reed, P., and Sharples, G.J. (2005) Evolution of a phage RuvC endonuclease for resolution of both Holliday and branched DNA junctions. Mol Microbiol 55: 1332-1345.
16. Declais, A.C., and Lilley, D.M. (2008) New insight into the recognition of branched DNA structure by junction-resolving enzymes. Curr Opin Struct Biol 18: 86-95.
17. Dunderdale, H.J., Benson, F.E., Parsons, C.A., Sharples, G.J., Lloyd, R.G., and West, S.C. (1991) Formation and resolution of recombination intermediates by E. coli RecA and RuvC proteins. Nature 354: 506-510.
18. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D60: 2126-2132.
19. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr D62: 72-82.
20. Fogg, J.M., and Lilley, D.M. (2000) Ensuring productive resolution by the junction-resolving enzyme RuvC: large enhancement of the second-strand cleavage rate. Biochemistry 39: 16125-16134.
21. Garcia, A.D., Aravind, L., Koonin, E.V., and Moss, B. (2000) Bacterial-type DNA Holliday junction resolvases in eukaryotic viruses. Proc Natl Acad Sci USA 97: 8926-8931.
22. Giraud-Panis, M.J., Duckett, D.R., and Lilley, D.M. (1995) The modular character of a DNA junction-resolving enzyme: a zinc-binding motif in bacteriophage T4 endonuclease VII. J Mol Biol 252: 596-610.
23. Hadden, J.M., Declais, A.C., Carr, S.B., Lilley, D.M., and Phillips, S.E. (2007) The structural basis of Holliday junction resolution by T7 endonuclease I. Nature 449: 621-624.
24. Hagan, N.F., Vincent, S.D., Ingleston, S.M., Sharples, G.J., Bennett, R.J., West, S.C., and Lloyd, R.G. (1998) Sequence-specificity of Holliday junction resolution: identification of RuvC mutants defective in metal binding and target site recognition. J Mol Biol 281: 17-29.
25. Ichiyanagi, K., Iwasaki, H., Hishida, T., and Shinagawa, H. (1998) Mutational analysis on structure-function relationship of a Holliday junction specific endonuclease RuvC. Genes Cells 3: 575-586.
26. Ip, S.C., Rass, U., Blanco, M.G., Flynn, H.R., Skehel, J.M., and West, S.C. (2008) Identification of Holliday junction resolvases from humans and yeast. Nature 456: 357-361.
27. Kemper, B., and Brown, D.T. (1976) Function of gene 49 of bacteriophage T4. II. Analysis of intracellular development and the structure of very fast-sedimenting DNA. J Virol 18: 1000-1015.
28. Leslie, A.G.W., and Powell, H.R. (2007) Processing diffraction data with MOSFLM. In Evolving Methods for Macromolecular Crystallography. Read, R.J., and Sussmann, J.L. (eds). Berlin: Springer, pp. 41-51.
29. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C., and Read, R.J. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
30. McGregor, N., Ayora, S., Sedelnikova, S., Carrasco, B., Alonso, J.C., Thaw, P., and Rafferty, J. (2005) The structure of Bacillus subtilis RecU Holliday junction resolvase and its role in substrate selection and sequence-specific cleavage. Structure 13: 1341-1351.
31. Marchler-Bauer, A., Lu, S., Anderson, J.B., Chitsaz, F., Derbyshire, M.K., DeWeese-Scott, C., etal. (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39: D225-D229.
32. Middleton, C.L., Parker, J.L., Richard, D.J., White, M.F., and Bond, C.S. (2004) Substrate recognition and catalysis by the Holliday junction resolving enzyme Hje. Nucleic Acids Res 32: 5442-5451.
33. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D53: 240-255.
34. Nishino, T., Komori, K., Tsuchiya, D., Ishino, Y., and Morikawa, K. (2001) Crystal structure of the archaeal Holliday junction resolvase Hjc and implications for DNA recognition. Structure 9: 197-204.
35. Oram, M., Keeley, A., and Tsaneva, I. (1998) Holliday junction resolvase in Schizosaccharomyces pombe has identical endonuclease activity to the CCE1 homologue YDC2. Nucleic Acids Res 26: 594-601.
36. Osman, F., Gaskell, L., and Whitby, M.C. (2009) Efficient second strand cleavage during Holliday junction resolution by RuvC requires both increased junction flexibility and an exposed 5' phosphate. PLoS ONE 4: e5347.
37. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326.
38. Rafferty, J.B., Bolt, E.L., Muranova, T., Sedelnikova, S.E., Leonard, P., Pasquo, A., etal. (2003) The structure of E. coli RusA endonuclease reveals a new Holliday junction DNA-binding fold. Structure 11: 1557-1567.
39. Saito, A., Iwasaki, H., Ariyoshi, M., Morikawa, K., and Shinagawa, H. (1995) Identification of four acidic amino acids that constitute the catalytic center of the RuvC Holliday junction resolvase. Proc Natl Acad Sci USA 92: 7470-7474.
40. Sanchez, H., Kidane, D., Reed, P., Curtis, F.A., Cozar, M.C., Graumann, P.L., etal. (2005) The RuvAB branch migration translocase and RecU Holliday junction resolvase are required for double-stranded DNA break repair in Bacillus subtilis. Genetics 171: 873-883.
41. Schouler, C., Ehrlich, S.D., and Chopin, M.C. (1994) Sequence and organization of the lactococcal prolate-headed bIL67 phage genome. Microbiology 140: 3061-3069.
42. Shah, R., Bennett, R.J., and West, S.C. (1994) Genetic recombination in E. coli: RuvC protein cleaves Holliday junctions at resolution hotspots in vitro. Cell 79: 853-864.
43. Sharples, G.J. (2001) The X philes: structure-specific endonucleases that resolve Holliday junctions. Mol Microbiol 39: 823-834.
44. Sharples, G.J., Benson, F.E., Illing, G.T., and Lloyd, R.G. (1990) 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: 219-226.
45. Sharples, G.J., Ingleston, S.M., and Lloyd, R.G. (1999) Holliday junction processing in bacteria: insights from the evolutionary conservation of RuvABC, RecG, and RusA. J Bacteriol 181: 5543-5550.
46. Sharples, G.J., Curtis, F.A., McGlynn, P., and Bolt, E.L. (2004) Holliday junction binding and resolution by the Rap structure-specific endonuclease of phage lambda. J Mol Biol 340: 739-751.
47. Sheldrick, G.M. (2010) Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr D66: 479-485.
48. Takahagi, M., Iwasaki, H., and Shinagawa, H. (1994) Structural requirements of substrate DNA for binding to and cleavage by RuvC, a Holliday junction resolvase. J Biol Chem 269: 15132-15139.
49. Tsujimoto, Y., and Ogawa, H. (1978) Intermediates in genetic recombination of bacteriophage T7 DNA. Biological activity and the roles of gene 3 and gene 5. J Mol Biol 125: 255-273.
50. Winn, M.D., Ballard, C.C., Cowtan, K.D., Dodson, E.J., Emsley, P., Evans, P.R., etal. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D67: 235-242.
51. Yamada, K., Ariyoshi, M., and Morikawa, K. (2004) Three-dimensional structural views of branch migration and resolution in DNA homologous recombination. Curr Opin Struct Biol 14: 130-137.
52. Yoshikawa, M., Iwasaki, H., Kinoshita, K., and Shinagawa, H. (2000) Two basic residues, Lys-107 and Lys-118, of RuvC resolvase are involved in critical contacts with the Holliday junction for its resolution. Genes Cells 5: 803-813.
53. Yoshikawa, M., Iwasaki, H., and Shinagawa, H. (2001) Evidence that phenylalanine 69 in Escherichia coli RuvC resolvase forms a stacking interaction during binding and destabilization of a Holliday junction DNA substrate. J Biol Chem 276: 10432-10436.