NMR studies of restriction enzyme-DNA interactions: Role of conformation in sequence specificity

Biochemistry

Volumn 44, Issue 13, 2005, Pages 5065-5074

  Dupureur, Cynthia M ^a  

^a UNIVERSITY OF MISSOURI ST LOUIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CONFORMATIONS; CRYSTALLOGRAPHY; DNA; NUCLEAR MAGNETIC RESONANCE; PROTEINS;

ENDONUCLEASE; ENZYME-DNA INTERACTIONS; SUBSTRATE AFFINITY; SUBSTRATE BINDING;

ENZYMES;

CALCIUM; DNA; MAGNESIUM; METAL ION; NUCLEIC ACID; RESTRICTION ENDONUCLEASE; RESTRICTION ENDONUCLEASE PVU II; TYPE II SITE SPECIFIC DEOXYRIBONUCLEASE; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM BINDING; CHEMICAL ANALYSIS; COMPLEX FORMATION; CRYSTALLOGRAPHY; ENZYME CONFORMATION; ENZYME SUBSTRATE; MOLECULAR RECOGNITION; NITROGEN NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE;

BASE SEQUENCE; CALCIUM; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DNA; MACROMOLECULAR SUBSTANCES; MAGNESIUM; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

EID: 16344380433     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0473758     Document Type: Article

References (64)

1. Pingoud, A., and Jeltsch, A. (2001) Structure and function of type II restriction endonucleases, Nucleic Acids Res. 29, 3705-3727.
2. Pabo, C., and Sauer, R. T. (1992) Transcription factors: Structural families and principles of DNA recognition, Annu. Rev. Biochem. 61, 1053-1095.
3. von Hippel, P. H., and Berg, O. G. (1989) Facilitated target location in biological systems, J. Biol. Chem. 264, 675-678.
4. von Hippel, P. H. (1994) Protein-DNA recognition: New perspectives and underlying themes, Science 263, 769-770.
5. Spolar, R. S., and Record, M. T. (1994) Coupling of local folding to site-specific binding of proteins to DNA, Science 263, 777-784.
6. Nadassy, K., Wodak, S., and Janin, J. (1999) Structural features of protein-nucleic acid recognition sites, Biochemistry 38, 1999-2017.
7. Halford, S. E., and Johnson, N. P. (1983) Single turnovers of the EcoRI restriction endonuclease, Biochem. J. 211, 405-415.
8. Jen-Jacobson, L., Engler, L., Ames, J., Kurpiewski, M., and Grigorescu, A. (2000) Thermodynamic parameters of specific and nonspecific protein-DNA binding, Supramol. Chem. 12, 143-160.
9. Baldwin, G. S., Vipond, I. B., and Halford, S. E. (1995) Rapid reaction analysis of the catalytic site of the EcoRV restriction endonuclease, Biochemistry 34, 705-714.
10. Jen-Jacobson, L. (1995) Structural-perturbation approaches to thermodynamics of site-specific protein-DNA interactions, Methods Enzymol. 259, 305-344.
11. Pingoud, A. (2004) Restriction Endonucleases, Vol. 14, Springer, Berlin.
12. Winkler, F. K., Banner, D. W., Oefner, C., Tsernoglou, D., Brown, R. S., Heathman, S. P., Bryan, R. K., Martin, P. D., Petratos, K., and Wilson, K. S. (1993) The crystal structure of EcoRV endonuclease and of its complexes with cognate and noncognate DNA fragments, EMBO J. 12, 1781-1795.
13. Viadiu, H., and Aggarwal, A. (2000) Structure of BamHI bound to nonspecific DNA: A model for DNA sliding, Mol. Cell 5, 889-895.
14. Kalodimos, C., Boelens, R., and Kaptein, R. (2004) Toward an integrated model of protein-DNA recognition as inferred from NMR studies on the lac repressor system, Chem. Rev. 104, 3567-3586.
15. Cavanagh, J., Fairbrother, W., Palmer, A., and Skelton, N. (1996) Protein NMR Spectroscopy: Principles and Practice, Academic Press, New York.
16. Wuthrich, K. (1998) The second decade: Into the third millenium, Nat. Struct. Biol. (NMR Suppl.), 492-495.
17. Kalodimos, C., Biris, N., Bonvin, A., Levandoski, M., Geuenneugues, M., Boelens, R., and Kaptein, R. (2004) Structure and flexibility adaptation in nonspecific and specific protein-DNA complexes, Science 305, 386-389.
18. Gingeras, T. R., Greenough, L., Schildkraut, I., and Roberts, R. J. (1981) Two new restriction endonucleases from Proteus vulgaris, Nucleic Acids Res. 9, 4525-4536.
19. Conlan, L. H., and Dupureur, C. M. (2002) Dissecting the metal ion dependence of DNA binding by PvuII endonuclease, Biochemistry 41, 1335-1342.
20. Cheng, X., Balendiran, K., Schildkraut, I., and Anderson, J. E. (1994) Structure of PvuII endonuclease with cognate DNA, EMBO J. 13, 3927-3935.
21. Athanasiadis, A., Vlassi, M., Kotsifaki, D., Tucker, P. A., Wilson, K. S., and Kokkinidis, M. (1994) Crystal structure of PvuII endonuclease reveals extensive structural homologies to EcoRV, Struct. Biol. 1, 469-475.
22. Dupureur, C. M., and Hallman, L. M. (1999) Effects of divalent metal ions on the activity and conformation of native and 3-fluorotyrosine-PvuII endonucleases, Eur. J. Biochem. 261, 261-268.
23. Dupureur, C. M., and Dominguez, M. A., Jr. (2001) The PD.... (D/E)XK motif in restriction enzymes: A link between structure and conformation, Biochemistry 40, 387-394.
24. Holmquist, B. (1988) Elimination of Adventitious Metals, Methods Enzymol. 158, 6-12.
25. Balendiran, K., Bonventre, J., Knott, R., Jack, W., Benner, J., Schildkraut, I., and Anderson, J. E. (1994) Expression, purification, and crystallization of restriction endonuclease PvuII with DNA containing its recognition site, Proteins: Struct., Funct., Genet. 19, 77-79.
26. Wagner, F. W. (1988) Preparation of metal-free enzymes, Methods Enzymol. 158, 21-32.
27. Jen-Jacobson, L., Kurpiewski, M., Lesser, D., Grable, D., Boyer, H. W., Rosenberg, J. M., and Greene, P. J. (1983) Coordinate ion pair formation between EcoRI endonuclease and DNA, J. Biol. Chem.258, 14638-14646.
28. José, T. J., Conlan, L. H., and Dupureur, C. M. (1999) Quantitative evaluation of metal ion binding to PvuII restriction endonuclease, J. Biol. Inorg. Chem. 4, 814-823.
29. Roberts, G. C. K. (1993) NMR of Macromolecules, IRL, New York.
30. 2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anistropy indicates an avenue to NMR structures of very large biological macromolecules in solution, Proc. Natl. Acad. Sci. U.S.A. 94, 12366-12371.
31. Jeltsch, A., Alves, J., Maass, G., and Pingoud, A. (1992) On the catalytic mechanism of EcoRI and EcoRV, FEBS Lett. 304, 4-8.
32. Dupureur, C. M., and Conlan, L. H. (2000) A catalytically deficient active site variant of PvuII endonuclease binds Mg(II) ions, Biochemistry 39, 10921-10927.
33. 2+ binding site near Tyr94 in the restriction enzyme PvuII, J. Mol. Biol. 331, 395-406.
34. Conlan, L. H., and Dupureur, C. M. (2002) Multiple metal ions drive DNA association by PvuII endonuclease, Biochemistry 41, 14848-14855.
35. King, J., Bowen, L., and Dupureur, C. M. (2004) Binding and conformational analysis of phosphoramidate-restriction enzyme interactions, Biochemistry 43, 8551-8559.
36. Zhong, X., Patel, S. S., Werneburg, B. G., and Tsai, M. D. (1997) DNA polymerase β: Multiple conformational changes in the mechanism of catalysis, Biochemistry 36, 11891-11900.
37. Ahn, J., Kraynov, V. S., Zhong, X., Werneburg, B. G., and Tsai, M. D. (1998) DNA polymerase β: Effects of gapped DNA substrates on dNTP specificity, fidelity, processivity and conformational changes, Biochem. J. 331, 79-87.
38. Jen-Jacobson, L., Engler, L. E., Lesser, D. R., Kurpiewski, M. R., Yee, C., and McVerry, B. (1996) Structural adaptations in the interaction of EcoRI endonuclease with methylated GAATTC sites, EMBO J. 15, 2870-2882.
39. Becker, M., Lesser, D., Kurpiewski, M., Baranger, A., and Jen-Jacobson, L. (1988) "Ultraviolet Footprinting" accurately maps sequence-specific contacts and DNA kinking in the EcoRI endonuclease-DNA complex, Proc. Natl. Acad. Sci. U.S.A. 85, 6247-6251.
40. Lesser, D. R., Kurpiewski, M. R., and Jacobson, L. J. (1990) The energetic basis of specificity in the EcoRI endonuclease-DNA interaction, Science 250, 776-784.
41. Rosenberg, J. M. (1991) Structure and function of restriction endonucleases, Curr. Opin. Struct. Biol. 1, 104-113.
42. 2+ binding to the active site of EcoRV endonuclease: A crystallographic study of complexes with substrate and product DNA at 2 Å resolution, Biochemistry 34, 683-696.
43. Lagunavicius, A., Grazulis, S., Balciunaite, E., Vainius, D., and Siksnys, V. (1997) DNA binding specificity of MunI restriction endonuclease is controlled by pH and calcium ions: Involvement of active site carboxylate residues, Biochemistry 36, 11093-11099.
44. Vipond, I. B., and Halford, S. E. (1995) Specific DNA recognition by EcoRV restriction endonuclease induced by calcium ions, Biochemistry 34, 1113-1119.
45. Newman, M., Strzelecka, T., Dorner, L. F., Schildkraut, I., and Aggarwal, A. K. (1995) Structure of BamHI endonuclease bound to DNA: Partial folding and unfolding on DNA binding, Science 269, 656-663.
46. Horton, J. R., and Cheng, X. (2000) PvuII endonuclease contains two calcium ions in active sites, J. Mol. Biol. 300, 1049-1056.
47. Horton, N. C., and Perona, J. J. (2004) DNA Cleavage by EcoRV endonuclease: Two metal ions in three metal ion binding sites, Biochemistry 43, 6841-6857.
48. Perona, J. J., and Martin, A. M. (1997) Conformational Transitions and Structural Deformability of EcoRV Endonuclease Revealed by Crystallographic Analysis, J. Mol. Biol. 273, 207-225.
49. Thomas, M., Brady, R., Halford, S. E., Sessions, R., and Baldwin, G. S. (1999) Structural analysis of a mutational hot spot in the EcoRV restriction endonuclease: A catalytic role for a main chain carbonyl group, Nucleic Acids Res. 27, 3438-3445.
50. Newman, M., Strzelecka, T., Dorner, L. F., Schildkraut, I., and Aggarwal, A. K. (1994) Structure of restriction endonuclease BamHI at 1.95 Å resolution by MAD analysis, Structure 2, 439-452.
51. Jeltsch, A., and Urbanke, C. (2004) Sliding or hopping? How restriction enzymes find their way on DNA, in Nucleic Acids and Molecular Biology (Pingoud, A., Ed.) pp 95-110, Springer-Verlag, Berlin.
52. Clore, G., and Gronenbom, A. (1998) NMR structure determination of proteins and protein complexes larger than 20 kDa. Curr. Opin. Struct. Biol. 2, 564-570.
53. Arrowsmith, C. H., and Wu, Y.-S. (1998) NMR of large (>25 kDa) proteins and protein complexes. Prog. NMR Spectrosc. 32, 277-286.
54. Kelly, M., Ball, L., Krieger, C., Yu, Y., Fischer, M., Schiffman, S., Schmieder, P., Kuhne, R., Bermel, W., Bacher, W., Richter, G., and Oschkinat, H. (2001) The NMR structure of the 47-kD dimeric enzyme 3,4-diydroxy-2-butanone-4- phosphate synthase and ligand binding studies reveal the location of the active site, Proc. Natl. Acad. Sci. U.S.A. 98, 13025-13030.
55. Turgarinov, V., Muhandiram, R., Ayed, A., and Kay, L. (2002) Four-dimensional NMR spectroscopy of a 723-residue protein: Chemical shift assignments and secondary structure of malate synthase G, J. Am. Chem. Soc. 124, 10025-10035.
56. Clore, G. M., and Gronenbom, A. M. (1994) Multidimensional heteronuclear nuclear magnetic resonance of proteins, Methods Enzymol. 239, 349-363.
57. 15N multidimensional NMR to study the structure and dynamics of proteins, Annu. Rev. Biophys. Biomol. Struct. 27, 357-406.
58. Polisky, B., Greene, P., Garfin, D. E., McCarthy, B. J., Goodman, H. M., and Boyer, H. W. (1975) Specificity of substrate recognition by the EcoRI restriction endonuclease, Proc. Natl. Acad. Sci. U.S.A. 72, 3310-3314.
59. Taylor, J. D., and Halford, S. E. (1989) Discrimination between DNA sequences by the EcoRV restriction endonuclease, Biochemistry 28, 6198-6207.
60. Sidorova, N. Y., and Rau, D. C. (1996) Differences in water release for the binding of EcoRI to specific and nonspecific sequences, Proc. Natl. Acad. Sci. U.S.A. 93, 12272-12277.
61. Robinson, C. R., and Sligar, S. G. (1998) Changes in solvation during DNA binding and cleavage are critical to altered specificity of the EcoRI endonuclease, Proc. Natl. Acad. Sci. U.S.A. 95, 2186-2191.
62. Nastri, H. G., Evans, P. D., Walker, I. H., and Riggs, P. D. (1997) Catalytic and DNA binding properties of PvuII restriction endonuclease mutants, J. Biol. Chem. 272, 25761-25767.
63. Jeltsch, A., Alves, J., Oelgeschlager, T., Wolfes, H., Maass, G., and Pingoud, A. (1993) Mutational analysis of the function of Gln115 in the EcoRI restriction endonuclease, a critical amino acid for recognition of the inner thymidine residue in the sequence -GAATTC- and for coupling specific DNA binding to catalysis, J. Mol. Biol. 229, 221-234.
64. Kay, L. (1998) Protein dynamics from NMR, Nat. Struct. Biol. 5 (Suppl.), 513-517.