Free Energy Analysis of Protein-DNA Binding: The EcoRI Endonuclease-DNA Complex

Journal of Computational Physics

Volumn 151, Issue 1, 1999, Pages 333-357

  Jayaram, B ^a   McConnell, K J ^b   Dixit, Surjit B ^a   Beveridge, D L ^b  

^a WESLEYAN UNIVERSITY   (United States)

^b INDIAN INSTITUTE OF TECHNOLOGY DELHI   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; COMPLEXATION; DEGREES OF FREEDOM (MECHANICS); ELECTROSTATICS; ENTROPY; FREE ENERGY; HYDROPHOBICITY; IONS; PROTEINS; SOLVATION; STATISTICAL MECHANICS; VAN DER WAALS FORCES;

COMPLEX FORMATIONS; DNA COMPLEX; ECORI ENDONUCLEASE; ELECTROSTATIC SCREENING; FREE ENERGY ANALYSIS; PROTEIN-DNA BINDING; STRUCTURAL ADAPTATION; THERMODYNAMIC CYCLE; VAN DER WAAL; VAN DER WAALS INTERACTIONS;

DNA;

EID: 0001101548     PISSN: 00219991     EISSN: None     Source Type: Journal    
DOI: 10.1006/jcph.1998.6173     Document Type: Article

References (84)

1. Hehre W. J., Radom L., Schleyer P. V. R. Ab Initio Molecular Orbital Theory. 1986.
2. Beveridge D. L., DiCapua F. M. Free energy via molecular simulation applications to chemical and biomolecular systems. Ann. Rev. Biophys. Biophys. Chem. 18:1989;431.
3. Jorgensen W. L. Free energy calculations: A breakthrough for modeling organic chemistry in solution. Acc. Chem. Res. 22:1989;184.
4. McCammon J. A. Free energy from simulations. Curr. Opinion Struct. Biol. 1:1991;196.
5. Kollman P. A. Free energy calculations: Applications to chemical and biochemical phenomena. Chem. Rev. 93:1993;2395.
6. van Gunsteren W. F., Berendsen H. J. C. Computer simulation of molecular dynamics: Methodology, applications and perspectives in chemistry. Angew. Chem. Int. Ed. Engl. 29:1990;992.
7. E. J. Simon, Harvard University, 1996.
8. Misra V. K., Hecht J. L., Sharp K. A. Salt effects on protein-DNA interactions. The lambda cI repressor and EcoRI endonuclease. J. Mol. Biol. 238:1994;264.
9. Misra V. K., Sharp K. A., Friedman R. A. Salt effects on ligand-DNA binding: Minor groove binding antibiotics. J. Mol. Biol. 238:1994;245.
10. Gilson M. K., Given J. A., Bush B. L. The statistical thermodynamic basis for computation of binding affinities: A critical review. Biophys. J. 72:1997;1047.
11. Cornell W. D., Cieplak P., Bayly C. I. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117:1995;5179.
12. Pearlman D. A., Case D. A., Caldwell J. W. AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comput. Phys. Commun. 91:1995;1.
13. Still W. C., Tempczyk A., Hawley R. C. Semianalytical treatment of solvation for molecular mechanics and dynamics. J. Am. Chem. Soc. 112:1990;6127.
14. Hawkins G. D., Cramer C. J., Truhlar D. G. Parametrized models of aqueous free energies of solvation based on pairwise descreening of solute atomic charges from a dielectric medium. J. Phys. Chem. 100:1996;19824.
15. Hawkins G. D., Cramer C. J., Truhlar D. G. Pairwise solute descreening of solute charges from a dielectric medium. Chem. Phys. Lett. 246:1995;122.
16. Jayaram B., Liu Y., Beveridge D. L. A modification of the generalized Born theory for improved estimates of solvation energies and pKa shifts. J. Phys. Chem. 109:1998;1465.
17. Jayaram B., Sprous D., Beveridge D. L. Solvation free energy of biomacromolecules: Parameters for a modified generalized Born model consistent with the AMBER force field. J. Phys. Chem. B. 102:1998;9571.
18. Reddy M. R., Erion M. D., Agarwal A. Solvation free energies calculated using the GB/SA model. J. Comput. Chem. 19:1998;769.
19. Travers A. DNA-Protein Interactions. 1993.
20. McClarin J. A., Frederick C. A., Wang B.-C. Structure of the DNA-Eco RI endonuclease recognition complex at 3 Å resolution. Science. 234:1986;1526.
21. Kim Y., Grable J. C., Love R. Refinement of the Eco RI endonuclease crystal structure: A revised protein chain tracing. Science. 249:1990;1307.
22. Drew H. R., Wing R. M., Takano T. Structure of a B DNA dodecamer. I. Conformation and dynamics. Proc. Nat./Acad. Sci. USA. 78:1981;2179.
23. Jen-Jacobson L. Protein-DNA recognition complexes: Conservation of structure and binding energy in the transition state. Biopolymers. 44:1997;153.
24. Lesser D. R., Kurpiewski M. R., Jen-Jacobson L. The energetic basis of specificity in the EcoRI endonuclease-DNA interaction. Science. 250:1990;776.
25. Beveridge D. L., Young M. A., Sprous D. Modeling of DNA via molecular dynamics simulation: Structure, bending, and conformational transitions. Molecular Modeling of Nucleic Acids. 1:1998;260.
26. R. E. Dickerson, Oxford Handbook of Nucleic Acid Structure, S. Neidle, Oxford Univ. Press, Oxford, UK, 1998.
27. Steitz T. A. Structural studies of protein-Nucleic acid interactions: The sources of sequence-specific binding. Quart. Rev. Biophys. 23:1990;205.
28. Seeman N. C., Rosenberg J. M., Rich A. Sequence-specific recognition of double helical nucleic acids by proteins. Proc. Natl. Acad. Sci. USA. 73:1976;804.
29. Wharton R. P., Brown E. L., Ptashne M. Substituting an alpha-helix switches the sequence-specific DNA interactions of a repressor. Cell. 38:1984;361.
30. Wharton R. P., Ptashne M. Changing the binding specificity of a repressor by redesigning an alpha-helix. Nature. 316:1985;601.
31. Otwinowski Z., Schevitz R. W., Zhang R. G. Crystal structure of trp repressor/operator complex at atomic resolution. Nature. 335:1988;321.
32. Koudelka G. B., Harrison S. C., Ptashne M. Effect of non-contacted bases on the affinity of 434 operator for 434 repressor and Cro. Nature. 326:1987;886.
33. Matthews B. W. Protein-DNA interaction, No code for recognition [news]. Nature. 335:1988;294.
34. Dickerson R. E. The DNA helix and how it is read. Sci. Am. 249:1983;94.
35. Rice P. A., Yang S., Mizuuchi K. Crystal structure of an IHF-DNA complex: A protein-induced DNA U-turn. Cell. 87:1996;1295.
36. Parkinson G., Wilson C., Gunasekera A. Structure of the CAP-DNA complex at 2.5 angstroms resolution: A complete picture of the protein-DNA interface. J. Mol. Biol. 260:1996;395.
37. Schultz S. C., Shields G. C., Steitz T. A. Crystal structure of a CAP-DNA complex: The DNA is bent by 90 degrees. Science. 253:1991;1001.
38. Record M. T. Jr., Anderson C. F., Mills P. Ions as regulators of protein-nucleic acid interactions in vitro and in vivo. Adv. Biophys. 20:1985;109.
39. Manning G. S. The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides. Quart. Rev. Biophys. 11:1978;179.
40. Record M. T. Jr., Anderson C. F., Lohman T. M. Thermodynamics analysis of ion effects on the binding and conformational equilibria of proteins and nucleic acids: The role of ion association and release, screening, and ion effects on water activity. Quart. Rev. Biophys. 11:1978;103.
41. Spolar R. S., Record M. T. Jr. Coupling of local folding to site-specific binding of proteins to DNA [see comments]. Science. 263:1994;777.
42. Schwabe J. W. The role of water in protein-DNA interactions. Curr. Opinion Struct. Biol. 7:1997;126.
43. Lundback T., Hansson H., Knapp S. Thermodynamic characterization of non-sequence-specific DNA-binding by the Sso7d protein from Sulfolobus solfataricus. J. Mol. Biol. 276:1998;775.
44. Chan H. S., Dill K. A. Solvation: How to obtain microscopic energies from partitioning and solvation experiments. Annu. Rev. Biophys. Biomol. Struct. 26:1997;425.
45. Beveridge D. L., McConnell K. J., Nirmala R. Molecular dynamics simulations of DNA and protein-DNA complexes including solvent: Recent progress. ACS Symp. Seri. 568:1994;381.
46. Eriksson M., Haerd T., Nilsson L. Molecular dynamics simulation of a DNA binding protein free and in complex with DNA. NATO ASI Ser. C. 426:1994;441.
47. Harris L. F., Sullivan M. R., Popken-Harris P. D. Molecular dynamics simulations in solvent of the glucocorticoid receptor protein in complex with a glucocorticoid response element DNA sequence. J. Biomol. Struct. Dyn. 12:1994;249.
48. Harris L. F., Sullivan M. R., Popken-Harris P. D. Molecular dynamics simulation in solvent of the estrogen receptor protein DNA binding domain in complex with a non-consensus estrogen response element DNA sequence. J. Biomol. Struct. Dyn. 15:1997;407.
49. M. G. Cooney, K. Miaskiewicz, M. Shibata, et al., Biomacromol: 3-D Appl, Hanford Symp. Health Environ, 34th, R. L. Ornstein, Battelle Press, Columbus, OH, 1997, 145.
50. Roxstroem G., Velazquez I., Paulino M. Molecular dynamics simulation of a Zif268-DNA complex in water: Spatial patterns and fluctuations sensed from a nanosecond trajectory. J. Phys. Chem. B. 102:1998;1828.
51. Thomasson K. A., Ouporov I. V., Baumgartner T. Free energy of nonspecific binding of Cro repressor protein to DNA. J. Phys. Chem. B. 101:1998;9127.
52. Duan Y., Wilkosz P., Rosenberg J. M. Dynamic contributions to the DNA binding entropy of the EcoRI and EcoRV restriction endonucleases. J. Mol. Biol. 264:1996;546.
53. Jayaram B., DiCapua F. M., Beveridge D. L. A theoretical study of polyelecrolyte effects in protein-DNA interactions: Monte Carlo free energy simulations on the ion atmosphere contribution to the thermodynamics of lambda repressor-operator complex formation. J. Am. Chem. Soc. 113:1991;5211.
54. Jayaram B., Swaminathan S., Beveridge D. L. Monte-Carlo simulation studies of the structure of the counteranion atmosphere of B-DNA: Variations on the primitive dielectric model. Macromolecules. 23:1990;3156.
55. Zacharias M., Luty B. A., Davis M. E. Poisson-Boltzmann analysis of the lambda repressor-operator interaction. Biophys. J. 63:1992;1280.
56. Jen-Jacobson L. Structural-perturbation approaches to thermodynamics of site-specific protein-DNA interactions. Methods Enzymol. 259:1995;305.
57. Chothia C. Structural invariants in protein folding. Nature. 254:1975;304.
58. Berman H. M., Olson W. K., Beveridge D. L. The nucleic acid database: A comprehensive relational database of three-dimensional structures of nucleic acids. Biophys. J. 63:1992;751.
59. Jayaram B., Sprous D., Young M. A. Free energy analysis of the conformational preferences of A and B forms of DNA in solution. J. Am. Chem. Soc. 120:1998;10629.
60. Lazaridis T., Archontis G., Karplus M. Enthalpic contribution to protein stability: Insights from atom-based calculations and statistical mechanics. Adv. Protein Chem. 47:1995;231.
61. Janin J. Elusive affinities. Proteins. 21:1995;30.
62. Janin J. Protein-protein recognition. Prog. Biophys. Mol. Biol. 64:1995;145.
63. Novotny J., Bruccoleri R. E., Davis M. Empirical free energy calculations: A blind test and further improvements to the method. J. Mol. Biol. 268:1997;401.
64. Proloff N., Windemuth A., Honig B. On the calculation of binding free energies using continuum methods: Application to MHC class I protein-Peptide interactions. Protein Sci. 6:1997;1293.
65. B. Jayaram, K. McConnell, S. B. Dixit, et al., Analysis of the binding free energy of protein-DNA complexes based on 40 X-ray crystal structures.
66. Dill K. A. Additivity principles in biochemistry. J. Biol. Chem. 272:1997;701.
67. Holtzer A. The "Cratic Correction" and related fallacies. Biopolymers. 35:1994;595.
68. Young M. A., Jayaram B., Beveridge D. L. Intrusion of counterions into the spine of hydration in the minor groove of B-DNA: Fractional occupancy of electronegative pockets. J. Am. Chem. Soc. 119:1997;59.
69. Young M. A., Ravishanker G., Beveridge D. L. A 5-nanosecond molecular dynamics trajectory for B-DNA: Analysis of structure, motions and solvation. Biophys. J. 73:1997;2313.
70. Olmsted M. C., Anderson C. F., Record M. T. Jr. Importance of oligoelectrolyte end effects for the thermodynamics of conformational transitions of nucleic acid oligomers: A grand canonical Monte Carlo analysis. Biopolymers. 31:1991;1593.
71. Krestov G. A. Thermodynamics of Solvation. 1991.
72. H. L. Friedman, C. V. Krishnan, Water: A Comprehensive Treatise, F. Franks, Plenum, New York, 1973, 3.
73. Atkins P. W. Physical Chemistry. 1990.
74. Finkelstein A. V., Janin J. The price of lost freedom: Entropy of biomolecular complex formation. Protein Eng. 3:1989;1.
75. Sharp K., Fine R., Honig B. Computer simulations of the diffusion of a substrate to an active site of an enzyme. Science. 236:1987;1460.
76. Sharp K. A., Nicholls A., Fine R. F. Reconciling the magnitude of the microscopic and macroscopic hydrophobic effects. Science. 252:1991;106.
77. Ohtaki H., Fukushima N. A structural study of saturated aqueous solutions of some alkali halides by X-ray diffraction. J. Sol. Chem. 21:1992;23.
78. Karplus P. A. Hydrophobicity regained. Protein Sci. 6:1997;1302.
79. Drew H. R., Samson S., Dickerson R. E. Structure of a B-DNA dodecamer at 16 K. Proc. Natl. Acad. Sci. USA. 79:1982;4040.
80. Lee B. K., Richards F. M. The interpretation of protein structures: Estimation of static accessibility. J. Mol. Biol. 55:1971;379.
81. Forsyth W. R., Gilson M. K., Antosiewicz J. Theoretical and experimental analysis of ionization equilibria in ovomucoid third domain. Biochemistry. 37:1998;8643.
82. Karplus M., Kushick J. N. Method for estimating the configurational entropy of macromolecules. Macromolecules. 14:1981;325.
83. Luscombe N. M., Laskowski R. A., Thornton J. M. NUCPLOT: A program to generate schematic diagrams of protein-nucleic acid interactions. Nucleic Acids Res. 25:1997;4940.
84. Laskowski R. A., MacArthur M. W., Moss D. S. PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:1993;283.