Crystal structure of RuvC resolvase in complex with Holliday junction substrate

Nucleic Acids Research

Volumn 41, Issue 21, 2013, Pages 9945-9955

  Górecka, Karolina M ^a   Komorowska, Weronika ^a   Nowotny, Marcin ^a  

^a INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE I; ENDONUCLEASE VII; PHOSPHATE; PROTEIN RUVC; RESOLVASE; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA BINDING; DNA CONFORMATION; DNA CROSS LINKING; ENZYME ACTIVITY; ENZYME BINDING; ENZYME CONFORMATION; ENZYME LOCALIZATION; ENZYME SUBSTRATE COMPLEX; HOLLIDAY JUNCTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN UNFOLDING; THERMUS THERMOPHILUS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; DNA, CRUCIFORM; HOLLIDAY JUNCTION RESOLVASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA;

EID: 84890028597     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt769     Document Type: Article

References (45)

1. West, S.C. (1992) Enzymes and molecular mechanisms of genetic recombination. Annu. Rev. Biochem., 61, 603-640.
2. Holliday, R. (1964) A mechanism for gene conversion in fungi. Genet. Res. Camb., 5, 282-304.
3. Duckett, D.R., Murchie, A.I., Diekmann, S., von Kitzing, E., Kemper, B. and Lilley, D.M. (1988) The structure of the Holliday junction, and its resolution. Cell, 55, 79-89.
4. Lilley, D.M. (2000) Structures of helical junctions in nucleic acids. Q. Rev. Biophys., 33, 109-159.
5. 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.
6. Chang, J.H., Kim, J.J., Choi, J.M., Lee, J.H. and Cho, Y. (2008) Crystal structure of the Mus81-Eme1 complex. Genes Dev., 22, 1093-1106.
7. 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.
8. 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.
9. 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.
10. Dunin-Horkawicz, S., Feder, M. and Bujnicki, J.M. (2006) Phylogenomic analysis of the GIY-YIG nuclease superfamily. BMC Genomics, 7, 98.
11. Nowotny, M. (2009) Retroviral integrase superfamily: the structural perspective. EMBO Rep., 10, 144-151.
12. Connolly, B., Parsons, C.A., Benson, F.E., Dunderdale, H.J., Sharples, G.J., Lloyd, R.G. and West, S.C. (1991) Resolution of Holliday junctions in vitro requires the Escherichia coli ruvC gene product. Proc. Natl Acad. Sci. USA, 88, 6063-6067.
13. 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.
14. Iwasaki, H., Takahagi, M., Shiba, T., Nakata, A. and Shinagawa, H. (1991) Escherichia coli RuvC protein is an endonuclease that resolves the Holliday structure. EMBO J., 10, 4381-4389.
15. Sharples, G.J. (2001) The X philes: structure-specific endonucleases that resolve Holliday junctions. Mol. Microbiol., 39, 823-834.
16. Yamada, K., Miyata, T., Tsuchiya, D., Oyama, T., Fujiwara, Y., Ohnishi, T., Iwasaki, H., Shinagawa, H., Ariyoshi, M., Mayanagi, K. et al. (2002) Crystal structure of the RuvA-RuvB complex: a structural basis for the Holliday junction migrating motor machinery. Mol. Cell, 10, 671-681.
17. Bennett, R.J., Dunderdale, H.J. and West, S.C. (1993) Resolution of Holliday junctions by RuvC resolvase: cleavage specificity and DNA distortion. Cell, 74, 1021-1031.
18. 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.
19. Shida, T., Iwasaki, H., Saito, A., Kyogoku, Y. and Shinagawa, H. (1996) Analysis of substrate specificity of the RuvC Holliday junction resolvase with synthetic Holliday junctions. J. Biol. Chem., 271, 26105-26109.
20. 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.
21. 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.
22. Green, V., Curtis, F.A., Sedelnikova, S., Rafferty, J.B. and Sharples, G.J. (2013) Mutants of phage bIL67 RuvC with enhanced Holliday junction binding selectivity and resolution symmetry. Mol. Microbiol., 89, 1240-1258.
23. 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.
24. Adams, P.D., Afonine, P.V., Bunkó czi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.-W., Kapral, G.J., Grosse-Kunstleve, R.W. et al. (2010) PHENIX: a comprehensive Pythonbased system for macromolecular structure solution. Acta Cryst., D66, 213-221.
25. 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.
26. 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.
27. Fogg, J.M., Schofield, M.J., White, M.F. and Lilley, D.M. (1999) Sequence and functional-group specificity for cleavage of DNA junctions by RuvC of Escherichia coli. Biochemistry, 38, 11349-11358.
28. 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.
29. 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.
30. 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.
31. Ohtani, N., Tomita, M. and Itaya, M. (2010) An extreme thermophile, Thermus thermophilus, is a polyploid bacterium. J. Bacteriol., 192, 5499-5505.
32. Banerjee, A., Santos, W.L. and Verdine, G.L. (2006) Structure of a DNA glycosylase searching for lesions. Science, 311, 1153-1157.
33. Huang, H., Chopra, R., Verdine, G.L. and Harrison, S.C. (1998) Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science, 282, 1669-1675.
34. Biertumpfel, C., Yang, W. and Suck, D. (2007) Crystal structure of T4 endonuclease VII resolving a Holliday junction. Nature, 449, 616-620.
35. Chan, S.N., Vincent, S.D. and Lloyd, R.G. (1998) Recognition and manipulation of branched DNA by the RusA Holliday junction resolvase of Escherichia coli. Nucleic Acids Res., 26, 1560-1566.
36. Giraud-Panis, M.J. and Lilley, D.M. (1998) Structural recognition and distortion by the DNA junction-resolving enzyme RusA. J. Mol. Biol., 278, 117-133.
37. Macmaster, R., Sedelnikova, S., Baker, P.J., Bolt, E.L., Lloyd, R.G. and Rafferty, J.B. (2006) RusA Holliday junction resolvase: DNA complex structure-insights into selectivity and specificity. Nucleic Acids Res., 34, 5577-5584.
38. Fogg, J.M., Kvaratskhelia, M., White, M.F. and Lilley, D.M. (2001) Distortion of DNA junctions imposed by the binding of resolving enzymes: a fluorescence study. J. Mol. Biol., 313, 751-764.
39. Sha, R., Iwasaki, H., Liu, F., Shinagawa, H. and Seeman, N.C. (2000) Cleavage of symmetric immobile DNA junctions by Escherichia coli RuvC. Biochemistry, 39, 11982-11988.
40. Hendrickson, W.A., Horton, J.R. and LeMaster, D.M. (1990) Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three-dimensional structure. EMBO J., 9, 1665-1672.
41. Mueller, U., Darowski, N., Fuchs, M.R., Forster, R., Hellmig, M., Paithankar, K.S., Puhringer, S., Steffien, M., Zocher, G. and Weiss, M.S. (2012) Facilities for macromolecular crystallography at the Helmholtz-Zentrum Berlin. J. Synchrotron Radiat., 19, 442-449.
42. Kabsch, W. (2010) Xds. Acta Crystallogr. D Biol. Crystallogr., 66, 125-132.
43. Terwilliger, T.C. and Berendzen, J. (1999) Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr., 55, 849-861.
44. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132.
45. Brunger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S. et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr., 54, 905-921.