Structural and Thermodynamic Basis for Enhanced DNA Binding by a Promiscuous Mutant EcoRI Endonuclease

Structure

Volumn 15, Issue 11, 2007, Pages 1368-1382

  Sapienza, Paul J ^a   Rosenberg, John M ^a   Jen Jacobson, Linda ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

DNA

Indexed keywords

AMINO ACID; ENDONUCLEASE; GLYCYLALANYLALANYLTHREONYLTHREONYLCYSTEINE; HOMODIMER; MACROGOL 400; MUTANT PROTEIN; UNCLASSIFIED DRUG; WATER;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; CRYSTAL; DNA BINDING; DNA FLANKING REGION; HYDROPHILICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN INTERACTION; PROTEIN STRUCTURE; SIMULATION; THERMODYNAMICS; WILD TYPE;

BASE SEQUENCE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DEOXYRIBONUCLEASE ECORI; DNA; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS;

EID: 35748982414     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2007.09.014     Document Type: Article

References (53)

1. Alves J., Ruter T., Geiger R., Fliess A., Maass G., and Pingoud A. Changing the hydrogen-bonding potential in the DNA binding site of EcoRI by site-directed mutagenesis drastically reduces the enzymatic activity, not, however, the preference of this restriction endonuclease for cleavage within the site -GAATTC-. Biochemistry 28 (1989) 2678-2684
2. Berendsen H.J.C., Postma J.P.M., van Gunsteren W.F., Dinola A., and Haak J.R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81 (1984) 3684-3690
3. Bevington P.R. Data Reduction and Error Analysis for the Physical Sciences (1969), McGraw-Hill, New York
4. Brünger A.T. Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355 (1992) 472-475
5. Brünger 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. Crystallography & NMR System: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998) 905-921
6. Cao, D.F. (2002). Co-solute effects as probes of the role of water release in DNA binding and catalysis by three restriction endonucleases. PhD thesis, University of Pittsburgh, Pittsburgh, PA.
7. Case, D.A., Darden, T.A., Cheatham, T.E. III, Simmerling, C.L., Wang, J., Duke, R.E., Luo, R., Merz, K.M., Wang, B., Pearlman, D.A., et al. (2004). AMBER 8 (computer program). University of California, San Francisco.
8. Cheng S.C., Kim R., King K., Kim S.H., and Modrich P. Isolation of gram quantities of EcoRI restriction and modification enzymes from an overproducing strain. J. Biol. Chem. 259 (1984) 11571-11575
9. Clarke E.C.W., and Glew D.N. Evaluation of thermodynamic functions from equilibrium constants. Trans. Faraday Soc. 62 (1966) 539-547
10. Dauter Z. Data-collection strategies. Acta Crystallogr. D Biol. Crystallogr. 55 (1999) 1703-1717
11. Dec S.F., and Gill S.J. Temperature dependence of errors in parameters derived from van't Hoff studies. J. Chem. Educ. 62 (1985) 879-881
12. DeLano W.L. The PyMOL Molecular Graphics System (2002), DeLano Scientific, Palo Alto, CA
13. de Leeuw S.W., Perram J.W., and Smith E.R. Ewald summations and dielectric constants. Proc. R. Soc. Lond. A 373 (1980) 27-56
14. Duan Y., Wu C., Chowdhury S., Lee M.C., Xiong G., Zhang W., Yang R., Cieplak P., Luo R., Lee T., et al. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J. Comput. Chem. 24 (2003) 1999-2012
15. Dunbrack Jr. R.L., and Cohen F.E. Bayesian statistical analysis of protein side-chain rotamer preferences. Protein Sci. 6 (1997) 1661-1681
16. Dunitz J.D. The entropic cost of bound water in crystals and biomolecules. Science 264 (1994) 670
17. Engh R.A., and Huber R. Accurate bond and angle parameters for X-ray structure refinement. Acta Crystallogr. A 47 (1991) 392-400
18. Engler L.E., Welch K.K., and Jen-Jacobson L. Specific binding by EcoRV endonuclease to its DNA recognition site GATATC. J. Mol. Biol. 269 (1997) 82-101
19. Fritz A., Kuster W., and Alves J. Asn141 is essential for DNA recognition by EcoRI restriction endonuclease. FEBS Lett. 438 (1998) 66-70
20. Grigorescu, A. (2003). Structural and energetic determinants of the binding specificity of EcoRI endonuclease. PhD thesis, University of Pittsburgh, Pittsburgh, PA.
21. Grigorescu A., Horvath M., Wilkosz P.A., Chandrasekhar K., and Rosenberg J.M. The integration of recognition and cleavage: X-ray structures of pre-transition state complex, post reactive complex and the DNA-free endonuclease. In: Pingoud A.M. (Ed). Restriction Endonucleases (2004), Springer, Berlin 137-173
22. Heinig M., and Frishman D. STRIDE: a web server for secondary structure assignment from known atomic coordinates of proteins. Nucleic Acids Res. 32 (2004) W500-W502
23. Heitman J., and Model P. Substrate recognition by the EcoRI endonuclease. Proteins 7 (1990) 185-197
24. Heitman J., and Model P. Mutants of the EcoRI endonuclease with promiscuous substrate specificity implicate residues involved in substrate recognition. EMBO J. 9 (1990) 3369-3378
25. Hendsch Z.S., and Tidor B. Electrostatic interactions in the GCN4 leucine zipper: substantial contributions arise from intramolecular interactions enhanced on binding. Protein Sci. 8 (1999) 1381-1392
26. Holbrook J.A., Tsodikov O.V., Saecker R.M., and Record Jr. M.T. Specific and non-specific interactions of integration host factor with DNA: thermodynamic evidence for disruption of multiple IHF surface salt-bridges coupled to DNA binding. J. Mol. Biol. 310 (2001) 379-401
27. Hubbard, S.J., and Thornton, J.M. (1993). NACCESS (computer program). Department of Biochemistry and Molecular Biology, University College London.
28. Ivanenko T., Heitman J., and Kiss A. Mutational analysis of the function of Met137 and Ile197, two amino acids implicated in sequence-specific DNA recognition by the EcoRI endonuclease. Biol. Chem. 379 (1998) 459-465
29. Jen-Jacobson L. Structural-perturbation approaches to thermodynamics of site-specific protein-DNA interactions. Methods Enzymol. 259 (1995) 305-344
30. Jen-Jacobson L. Protein-DNA recognition complexes: conservation of structure and binding energy in the transition state. Biopolymers 44 (1997) 153-180
31. Jen-Jacobson L., Kurpiewski M., Lesser D., Grable J., Boyer H.W., Rosenberg J.M., and Greene P.J. Coordinate ion pair formation between EcoRI endonuclease and DNA. J. Biol. Chem. 258 (1983) 14638-14646
32. Jen-Jacobson L., Engler L.E., Ames J.T., Kurpiewski M.R., and Grigorescu A. Thermodynamic parameters of specific and nonspecific protein-DNA binding. Supramol. Chem. 12 (2000) 143-160
33. Jen-Jacobson L., Engler L.E., and Jacobson L.A. Structural and thermodynamic strategies for site-specific DNA-binding proteins. Structure 8 (2000) 1015-1023
34. Joachimiak A., Haran T.E., and Sigler P.B. Mutagenesis supports water mediated recognition in the trp repressor-operator system. EMBO J. 13 (1994) 367-372
35. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47 (1991) 110-119
36. Kim Y.C., Grable J.C., Love R., Greene P.J., and Rosenberg J.M. Refinement of Eco RI endonuclease crystal structure: a revised protein chain tracing. Science 249 (1990) 1307-1309
37. Kozlov A.G., and Lohman T.M. Calorimetric studies of E. coli SSB protein-single-stranded DNA interactions. Effects of monovalent salts on binding enthalpy. J. Mol. Biol. 278 (1998) 999-1014
38. Kozlov A.G., and Lohman T.M. Large contributions of coupled protonation equilibria to the observed enthalpy and heat capacity changes for ssDNA binding to Escherichia coli SSB protein. Protein Sci. 41 Suppl 4 (2000) 8-22
39. Kumar S., Duan Y., Kollman P.A., and Rosenberg J.M. Molecular dynamics simulations suggest that the Eco RI kink is an example of molecular strain. J. Biomol. Struct. Dyn. 12 (1994) 487-525
40. Kurpiewski M.R., Engler L.E., Wozniak L.A., Kobylanska A., Koziolkiewicz M., Stec W.J., and Jen-Jacobson L. Mechanisms of coupling between DNA recognition specificity and catalysis in EcoRI endonuclease. Structure 12 (2004) 1775-1788
41. Lesser D.R., Kurpiewski M.R., and Jen-Jacobson L. The energetic basis of specificity in the Eco RI endonuclease-DNA interaction. Science 250 (1990) 776-786
42. Lesser D.R., Grajkowski A., Kurpiewski M.R., Koziolkiewicz M., Stec W.J., and Jen-Jacobson L. Stereoselective interaction with chiral phosphorothioates at the central DNA kink of the EcoRI endonuclease-GAATTC complex. J. Biol. Chem. 267 (1992) 24810-24818
43. Lu X.J., and Olson W.K. 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures. Nucleic Acids Res. 31 (2003) 5108-5121
44. Minor W., Tomchick D., and Otwinowski Z. Strategies for macromolecular synchrotron crystallography. Structure 8 (2000) R105-R110
45. Needels M.C., Fried S.R., Love R., Rosenberg J.M., Boyer H.W., and Greene P.J. Determinants of EcoRI endonuclease sequence discrimination. Proc. Natl. Acad. Sci. USA 86 (1989) 3579-3583
46. Osuna J., Flores H., and Soberon X. Combinatorial mutagenesis of three major groove-contacting residues of EcoRI: single and double amino acid replacements retaining methyltransferase-sensitive activities. Gene 106 (1991) 7-12
47. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
48. Parkinson G. New parameters for the refinement of nucleic acid-containing structures. Acta Crystallogr. D Biol. Crystallogr. 52 (1996) 57-64
49. Poon G.M., and Macgregor Jr. R.B. A thermodynamic basis of DNA sequence selectivity by the ETS domain of murine PU.1. J. Mol. Biol. 335 (2004) 113-127
50. Ryckaert J.-P., Ciccotti G., and Berendsen H.J.C. Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 23 (1977) 327-341
51. Sapienza P.J., dela Torre C.A., McCoy III W.H., Jana S.V., and Jen-Jacobson L. Thermodynamic and kinetic basis for the relaxed DNA sequence specificity of "promiscuous" mutant EcoRI endonucleases. J. Mol. Biol. 348 (2005) 307-324
52. Shui X., McFail-Isom L., Hu G.G., and Williams L.D. The B-DNA dodecamer at high resolution reveals a spine of water on sodium. Biochemistry 37 (1998) 8341-8355
53. Wibowo F.R., Rauch C., Trieb M., Wellenzohn B., and Liedl K.R. Water-mediated contacts in the trp-repressor operator complex recognition process. Biopolymers 73 (2004) 668-681