The crystal structure of the gene targeting homing endonuclease I-SceI reveals the origins of its target site specificity

Journal of Molecular Biology

Volumn 334, Issue 4, 2003, Pages 685-695

  Moure, Carmen M ^a   Gimble, Frederick S ^b   Quiocho, Florante A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

Asymmetry; Homing endonuclease; Metal binding; Protein DNA interactions; Structure

Indexed keywords

CALCIUM; DEOXYRIBONUCLEASE I; DNA; ENDONUCLEASE 1 SCE1; ENZYME; ESTER DERIVATIVE; PHOSPHODIESTER; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; DNA STRUCTURE; ENZYME SPECIFICITY; ENZYME SUBUNIT; GENE TARGETING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

EID: 0242636378     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.09.068     Document Type: Article

References (52)

1. Capecchi M.R. The new mouse genetics: altering the genome by gene targeting. Trends Genet. 5:1989;70-76.
2. Sedivy J.M., Sharp P.A. Positive genetic selection for gene disruption in mammalian cells by homologous recombination. Proc. Natl Acad. Sci. USA. 86:1989;227-231.
3. Rouet P., Smih F., Jasin M. Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol. Cell. Biol. 14:1994;8096-8106.
4. Smih F., Rouet P., Romanienko P.J., Jasin M. Double-strand breaks at the target locus stimulate gene targeting in embryonic stem cells. Nucl. Acids Res. 23:1995;5012-5019.
5. Choulika A., Perrin A., Dujon B., Nicolas J.-F. Induction of homologous recombination in mammalian chromosomes by using the I-SceI system of Saccharomyces cerevisiae. Mol. Cell. Biol. 15:1995;1968-1973.
6. Donoho G., Jasin M., Berg P. Analysis of gene targeting and intrachromosomal homologous recombination stimulated by genomic double-strand breaks in mouse embryonic stem cells. Mol. Cell. Biol. 18:1998;4070-4078.
7. Bellaiche Y., Mogila V., Perrimon N. I-SceI endonuclease, a new tool for studying DNA double-strand break repair mechanisms in Drosophila. Genetics. 152:1999;1037-1044.
8. Lin Y., Waldman A.S. Capture of DNA sequences at double-strand breaks in mammalian chromosomes. Genetics. 158:2001;1665-1674.
9. Ricchetti M., Fairhead C., Dujon B. Mitochondrial DNA repairs double-strand breaks in yeast chromosomes. Nature. 402:1999;96-100.
10. Puchta H. Use of I-SceI to induce DNA double-strand breaks in Nicotiana. Methods Mol. Biol. 113:1999;447-451.
11. Thermes V., Grabher C., Ristoratore F., Bourrat F., Choulika A., Wittbrodt J., Joly J. I-SceI meganuclease mediates highly efficient transgenesis in fish. Mech. Dev. 118:2002;91-98.
12. Cohen-Tannoudji M., Robine S., Choulika A., Pinto D., El Marjou F., Babinet C., et al. I-SceI-induced gene replacement at a natural locus in embryonic stem cells. Mol. Cell. Biol. 18:1998;1444-1448.
13. Jacquier A., Dujon B. An intron-encoded protein is active in a gene conversion process that spreads an intron into a mitochondrial gene. Cell. 41:1985;383-394.
14. Colleaux L., D'Auriol L., Betermier M., Cottarel G., Jacquier A., Galibert F., Dujon B. Universal code equivalent of a yeast mitochondrial intron reading frame is expressed into E. coli as a specific double strand endonuclease. Cell. 44:1986;521-533.
15. Belfort M., Roberts R.J. Homing endonucleases: keeping the house in order. Nucl. Acids Res. 25:1997;3379-3388.
16. Chevalier B.S., Stoddard B.L. Homing endonucleases: structural and functional insight into the catalysts of intron/intein mobility. Nucl. Acids Res. 29:2001;3757-3774.
17. Gimble F.S. Invasion of a multitude of genetic niches by homing endonuclease genes. FEMS Microbiol. Letters. 185:2000;99-107.
18. Thierry A., Perrin A., Boyer J., Fairhead C., Dujon B., Frey B., Schmitz G. Cleavage of yeast and bacteriophage T7 genomes at a single site using the rare cutter endonuclease I-SceI. Nucl. Acids Res. 19:1991;189-190.
19. Colleaux L., D'Auriol L., Galibert F., Dujon B. Recognition and cleavage site of the intron-encoded omega transposase. Proc. Natl Acad. Sci. USA. 85:1988;6022-6026.
20. Chevalier B.S., Monnat R.J. Jr, Stoddard B.L. The homing endonuclease I-CreI uses three metals, one of which is shared between the two active-sites. Nature Struct. Biol. 8:2001;312-316.
21. Heath P.J., Stephens K.M., Monnat R.J. Jr, Stoddard B.L. The structure of I-CreI, a group I intron-encoded homing endonuclease. Nature Struct. Biol. 4:1997;468-476.
22. Silva G.H., Dalgaard J.Z., Belfort M., Van Roey P. Crystal structure of the thermostable archaeal intron-encoded endonuclease I-DmoI. J. Mol. Biol. 286:1999;1123-1136.
23. Duan X., Gimble F.S., Quiocho F.A. Crystal structure of PI-SceI, a homing endonuclease with protein splicing activity. Cell. 89:1997;555-564.
24. Ichiyanagi K., Ishino Y., Ariyoshi M., Komori K., Morikawa K. Crystal structure of an archaeal intein-encoded homing endonuclease PI-PfuI. J. Mol. Biol. 300:2000;889-901.
25. Jurica M.S., Monnat R.J. Jr, Stoddard B.L. DNA recognition and cleavage by the LAGLIDADG homing endonuclease I-CreI. Mol. Cell. 2:1998;469-476.
26. Chevalier B., Turmel M., Lemieux C., Monnat R.J., Stoddard B.L. Flexible DNA target site recognition by divergent homing endonuclease isoschizomers I-CreI and I-MsoI. J. Mol. Biol. 329:2003;253-269.
27. Moure C.M., Gimble F.S., Quiocho F.A. Crystal structure of the intein homing endonuclease PI-SceI bound to its recognition sequence. Nature Struct. Biol. 9:2002;764-770.
28. Perrin A., Buckle M., Dujon B. Asymmetrical recognition and activity of the I-SceI endonuclease on its site and on intron-exon junctions. EMBO J. 12:1993;2939-2947.
29. Beylot B., Spassky A. Chemical probing shows that the intron-encoded endonuclease I-SceI distorts DNA through binding in monomeric form to its homing site. J. Biol. Chem. 276:2001;25243-25253.
30. Lavery R., Sklenar H. The definition of generalised helicoidal parameters and of axis curvature for irregular nucleic acids. J. Biomol. Struct. Dynam. 6:1988;63-91.
31. Schapira M., Desdouets C., Jacq C., Perea J. I-SceIII an intron-encoded DNA endonuclease from yeast mitochondria. Asymmetrical DNA binding properties and cleavage reaction. Nucl. Acids Res. 21:1993;3683-3689.
32. Luscombe N.M., Laskowski R.A., Thornton J.M. Amino acid-base interactions: a three-dimensional analysis of protein-DNA interactions at an atomic level. Nucl. Acids Res. 29:2001;2860-2874.
33. Kovall R.A., Matthews B.W. Type II restriction endonucleases: structural, functional and evolutionary relationships. Curr. Opin. Chem. Biol. 3:1999;578-583.
34. Gimble F.S., Stephens B.W. Substitutions in conserved dodecapeptide motifs that uncouple the DNA binding and DNA cleavage activities of PI-SceI endonuclease. J. Biol. Chem. 270:1995;5849-5856.
35. 2+ binding ligands of the homing endonuclease PI-SceI. Biochemistry. 39:2000;15895-15900.
36. Galburt E.A., Stoddard B.L. Catalytic mechanisms of restriction and homing endonucleases. Biochemistry. 41:2002;13851-13860.
37. Seligman L.M., Stephens K.M., Savage J.H., Monnat R.J. Jr. Genetic analysis of the Chlamydomonas reinhardtii I-CreI mobile intron homing system in Escherichia coli. Genetics. 147:1997;1653-1664.
38. Gimble F.S., Hu D., Duan X., Quiocho F.A. Identification of Lys403 in the PI-SceI homing endonuclease as part of a symmetric catalytic center. J. Biol. Chem. 273:1998;30524-30529.
39. Christ F., Schoettler S., Wende W., Steuer S., Pingoud A., Pingoud V. The monomeric homing endonuclease PI-SceI has two catalytic centres for cleavage of the two strands of its DNA substrate. EMBO J. 18:1999;6908-6916.
40. Bibikova M., Beumer K., Trautman J.K., Carroll D. Enhancing gene targeting with designed zinc finger nucleases. Science. 300:2003;764.
41. Porteus M.H., Baltimore D. Chimeric nucleases stimulate gene targeting in human cells. Science. 300:2003;763.
42. Chevalier B.S., Kortemme T., Chadsey M.S., Baker D., Monnat R.J., Stoddard B.L. Design, activity, and structure of a highly specific artificial endonuclease. Mol. Cell. 10:2002;895-905.
43. Epinat J.C., Arnould S., Chames P., Rochaix P., Desfontaines D., Puzin C., et al. A novel engineered meganuclease induces homologous recombination in yeast and mammalian cells. Nucl. Acids Res. 31:2003;2952-2962.
44. Monteilhet C., Perrin A., Thierry A., Colleaux L., Dujon B. Purification and characterization of the in vitro activity of I-SceI, a novel and highly specific endonuclease encoded by a group I intron. Nucl. Acids Res. 18:1990;1407-1413.
45. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
46. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921.
47. de La Fortelle E., Bricogne G. SHARP: Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276:1997;472-494.
48. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
49. Kraulis P. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
50. Esnouf R. An extensively modified version of MolScript that includes greatly enhanced coloring capabilities. J. Mol. Graph. Model. 15:1997;132-134.
51. Merrit E., Murphy M. Raster3D Version 2.0. A program for photorealistic molecular graphics. Acta Crystallog. sect. D. 50:1994;869-873.
52. Nicholls A., Bharadwaj R., Honig B. GRASP: graphical representation and analysis of surface properties. Biophys. J. 64:1993;166-170.