Metal-dependent DNA cleavage mechanism of the I-CreI LAGLIDADG homing endonuclease

Biochemistry

Volumn 43, Issue 44, 2004, Pages 14015-14026

  Chevalier, Brett ^a   Sussman, Django ^a   Otis, Christian ^a   Noël, Ann Josée ^a   Turmel, Monique ^a   Lemieux, Claude ^a   Stephens, Kathy ^b   Monnat Jr , Raymond J ^b   Stoddard, Barry L ^a,c  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITÉ LAVAL   (Canada)

^c Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; DIMERS; ENZYME KINETICS; ENZYMES; MONOMERS; MUTAGENESIS;

BINDING AFFINITY; CLEAVAGE REACTIONS; ENDONUCLEASE;

DNA;

CALCIUM; ENDONUCLEASE; LEUCYLALANYLGLYCYLLEUCYLISOLEUCYLASPARTYLALANYLASPARTYLGLYCINE ENDONUCLEASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CALCIUM BINDING; CRYSTAL STRUCTURE; DNA BINDING MOTIF; DNA CLEAVAGE; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; FOURIER ANALYSIS; KINETICS; METAL BINDING; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS;

AMINO ACID MOTIFS; ANIMALS; BINDING SITES; CATALYSIS; CATIONS, DIVALENT; CHLAMYDOMONAS REINHARDTII; CRYSTALLOGRAPHY, X-RAY; DNA RESTRICTION ENZYMES; DNA, ALGAL; DNA, CHLOROPLAST; DNA-BINDING PROTEINS; HYDROLYSIS; KINETICS; LYSINE; METALS; POINT MUTATION; PROTEIN BINDING; SUBSTRATE SPECIFICITY;

EID: 8344256614     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048970c     Document Type: Article

References (43)

1. Dujon, B. (1989) Group I introns as mobile genetic elements: facts and mechanistic speculations - a review, Gene 82, 91-114.
2. Lambowitz, A. M., and Belfort, M. (1993) Introns as mobile genetic elements, Annu. Rev. Biochem. 62, 587-622.
3. Belfort, M., and Perlman, P. S. (1995) Mechanisms of intron mobility, J. Biol. Chem. 270, 30237-30240.
4. Belfort, M., and Roberts, R. J. (1997) Homing endonucleases: keeping the house in order, Nucleic Acids Res. 25, 3379-3388.
5. Chevalier, B. S., and Stoddard, B. L. (2001) Homing endonucleases: structural and functional insight into the catalysts of intron/intein mobility, Nucleic Acids Res. 29, 3757-3774.
6. Jacquier, A., and Dujon, B. (1985) An intron-encoded protein is active in a gene conversion process that spreads an intron into a mitochondrial gene, Cell 41, 383-394.
7. Turmel, M., Cote, V., Otis, C., Mercier, J. P., Gray, M. W., Lonergan, K. M., and Lemieux, C. (1995) Evolutionary transfer of ORF-containing group I introns between different subcellular compartments (chloroplast and mitochondrion), Mol. Biol. Evol. 12, 533-545.
8. Cho, Y., Qiu, Y.-L., Kuhlman, P., and Palmer, J. D. (1998) Explosive invasion of plant mitochondria by a group I intron, Proc. Natl. Acad. Sci. U.S.A. 95, 14244-14249.
9. Dalgaard, J. Z., Klar, A. J., Moser, M. J., Holley, W. R., Chatterjee, A., and Mian, I. S. (1997) Statistical modeling and analysis of the LAGLIDADG family of site-specific endonucleases and identification of an intein that encodes a site-specific endonuclease of the HNH family, Nucleic Acids Res. 25, 4626-4638.
10. Heath, P. J., Stephens, K. M., Monnat, R. J., and Stoddard, B. L. (1997) The structure of I-CreI, a group I intron-encoded homing endonuclease, Nat. Struct. Biol. 4, 468-476.
11. Duan, X., Gimble, F. S., and Quiocho, F. A. (1997) Crystal structure of PI-SceI, a homing endonuclease with protein splicing activity, Cell 89, 555-564.
12. Chevalier, B., Turmel, M., Lemieux, C., Monnat, R. J., and Stoddard, B. L. (2003) Flexible DNA target site recognition by divergent homing endonuclease isoschizomers I-CreI and I-MsoI, J. Mol. Biol. 329, 253-269.
13. Chevalier, B. S., Monnat, R. J., Jr., and Stoddard, B. L. (2001) The homing endonuclease I-CreI uses three metals, one of which is shared between the two active sites, Nat. Struct. Biol. 8, 312-316.
14. Bolduc, J. M., Spiegel, P. C., Chatterjee, P., Brady, K. L., Downing, M. E., Caprara, M. G., Waring, R. B., and Stoddard, B. L. (2003) Structural and biochemical analyses of DNA and RNA binding by a bifunctional homing endonuclease and group I intron splicing cofator, Genes Dev. 17, 2875-2888.
15. Moure, C. M., Gimble, F. S., and Quiocho, F. A. (2003) The crystal structure of the gene targeting homing endonuclease I-SceI reveals the origins of its target site specificity, J. Mol. Biol. 334, 685-696.
16. Chevalier, B. S., Kortemme, T., Chadsey, M. S., Baker, D., Monnat, R. J., Jr., and Stoddard, B. L. (2002) Design, activity and structure of a highly specific artificial endonuclease, Mol. Cell 10, 895-905.
17. Moure, C. M., Gimble, F. S., and Quiocho, F. A. (2002) Crystal structure of the intein homing endonuclease PI-SceI bound to its recognition sequence, Nat. Struct. Biol. 9, 764-770.
18. Chevalier, B. S., and Stoddard, B. L. (2001) Homing endonucleases: structural and functional insight into the catalysts of intron/intein mobility, Nucleic Acids Res. 29, 3757-3774.
19. Lucas, P., Otis, C., Mercier, J. P., Turmel, M., and Lemieux, C. (2001) Rapid evolution of the DNA-binding site in LAGLIDADG homing endonucleases, Nucleic Acids Res. 29, 960-969.
20. Galburt, E. A., Chevalier, B., Tang, W., Jurica, M. S., Flick, K. E., Monnat, R. J., and Stoddard, B. L. (1999) A novel endonuclease mechanism directly visualized for I-PpoI, Nat. Struct. Biol. 6, 1096-1099.
21. Durrenberger, F., and Rochaix, J.-D. (1993) Characterization of the cleavage site and the recognition sequence of the I-CreI DNA endonuclease encoded by the chloroplast ribosomal intron of Chlamydomonas reinhardtii, Mol. Gen. Genet. 236, 409-414.
22. Thompson, A. J., Yuan, X., Kudlicki, W., and Herrin, D. L. (1992) Cleavage and recognition pattern of a double-strand-specific endonuclease (I-CreI) encoded by the chloroplast 23S rRNA intron of Chlamydomonas reinhardtii, Gene 119, 247-251.
23. Wang, J., Kim, H.-H., Yuan, X., and Herrin, D. L. (1997) Purification, biochemical characterization and protein-DNA interactions of the I-CreI endonuclease produced in Escherichia coli, Nucleic Acids Res. 25, 3767-3776.
24. Halford, S. E., Johnson, N. P., and Grinsted, J. (1980) The EcoRI restriction endonuclease with bacteriophage λ DNA, Biochem. J. 191, 581-592.
25. Fersht, A. (1985) in Enzyme structure and mechanism, pp 475, W. H. Freeman and Co., New York.
26. Drouin, M., Lucas, P., Otis, C., Lemieux, C., and Turmel, M. (2000) Biochemical characterization of I-CmoeI reveals that this H-N-H homing endonuclease shares functional similarities with H-N-H colicins, Nucleic Acids Res. 28, 4566-4572.
27. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-326.
28. Kissinger, C. R., and Gehlhaar, D. K. (1997) EPMR, Agouron Pharmaceuticals, La Jolla, CA.
29. McRee, D. E. (1999) A Versatile Program for Manipulating Atomic Coordinates and Electron Density, J. Struct. Biol. 125, 156-165.
30. Jones, T. A., Zou, J.-Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models, Acta Crystallogr. A47, 110-119.
31. 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., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr. D54, 905-921.
32. Brunger, A. (1993) Assessment of phase accuracy by cross validation: the free R value. Methods and Applications, Acta Crystallogr. D49, 24-36.
33. Laskowski, R. J., Macarthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures, J. Appl. Crystallogr. 26, 283-291.
34. Westheimer, F. H. (1987) Why nature chose phosphates, Science 235, 1173-1178.
35. Galburt, E., and Stoddard, B. L. (2002) Catalytic mechanisms of restriction and homing endonucleases, Biochemistry 41, 13851-13860.
36. Pingoud, A., and Jeltsch, A. (2001) Structure and function of type II restriction endonucleases, Nucleic Acids Res. 29, 3705-3727.
37. Turmel, M., Otis, C., Cote, V., and Lemieux, C. (1997) Evolutionarily conserved and functionally important residues in the I-CeuI homing endonuclease, Nucleic Acids Res. 25, 2610-2619.
38. Lagunavicius, A., and Siksnys, V. (1997) Site-directed mutagenesis of putative active site residues of MunI restriction endonuclease: replacement of catalytically essential carboxylate residues triggers DNA binding specificity, Biochemistry 36, 11086-11092.
39. Skirgaila, R., Grazulis, S., Bozic, D., Huber, R., and Siksnys, V. (1998) Structure-Based Redesign of the Catalytic/Metal Binding Site of Cfr10I Restriction Endonuclease Reveals the Importance of Spatial Rather Than Sequence Conservation of Active Centre Residues, J. Mol. Biol. 279, 473-481.
40. Horton, N. C., Otey, C., Lusetti, S., Sam, M. D., Kohn, J., Martin, A. M., Ananthnarayan, V., and Perona, J. J. (2002) Electrostatic contributions to site specific DNA cleavage by EcoRV endonuclease, Biochemistry 41, 10754-10763.
41. Sam, M. D., and Perona, J. J. (1999) Catalytic roles of divalent metal ions in phosphoryl transfer by EcoRV endonuclease, Biochemistry 38, 6576-6586.
42. Thomas, M. P., Brady, R. L., Halford, S. E., Sessions, R. B., and Baldwin, G. S. (1999) Structural analysis of a mutational hotspot in the EcoRV restriction endonuclease: a catalytic role for a main chain carbonyl group, Nucleic Acids Res. 27, 3438-3445.
43. Vipond, I. B., and Halford, S. E. (1996) Random mutagenesis targeted to the active site of the EcoRV restriction endonuclease, Biochemistry 35, 1701-1711.