Proton binding to proteins: A free-energy component analysis using a dielectric continuum model

Biophysical Journal

Volumn 88, Issue 6, 2005, Pages 3888-3904

  Archontis, Georgios ^a   Simonson, Thomas ^b  

^a UNIVERSITY OF CYPRUS   (Cyprus)

^b LABORATOIRE DE BIOCHIMIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; CARBOXYLIC ACID; LYSINE; PROTEIN; PROTON; RIBONUCLEASE A; SOLVENT; THIOREDOXIN;

ANALYTIC METHOD; ARTICLE; AVERAGING; DESOLVATION; DIELECTRIC CONTINUUM MODEL; ELECTRIC POTENTIAL; ELECTRICITY; ELECTROSTATIC POTENTIAL; ENERGY; ERROR; FREE ENERGY COMPONENT ANALYSIS; LINEAR RESPONSE METHOD; MARCUS REORGANIZATION; MATHEMATICAL ANALYSIS; MODEL; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PHYSICAL PHENOMENA; PKA; POISSON BOLTZMANN METHOD; POLARIZATION; PRECIPITATION; PRINCIPAL COMPONENT ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; SIMULATION;

EID: 22244488061     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.055996     Document Type: Article

References (85)

1. B in bacterial photosynthetic reaction centers. Biochemistry. 38:8253-8270.
2. Antosiewicz, J., J. A. McCammon, and M. K. Gilson. 1994. Prediction of pH-dependent properties of proteins. J. Mol. Biol. 238:415-436.
3. as in proteins. Biochemistry, 35:7819-7833.
4. Aqvist, J. 1991. Calculation of absolute binding free energies for charged ligands and effects of long-range electrostatic interactions. J. Comput. Chem. 17:1587-1597.
5. Aqvist, J., V. B. Luzhkov, and B. O. Brandsal. 2002. Ligand binding affinities from MD simulations. Acc. Chem, Res. 35:358-365.
6. Archontis, G., and T. Simonson. 2001. Dielectric relaxation in an enzyme active site: molecular dynamics simulations interpreted with a macroscopic continuum model. J. Am. Chem. Soc. 123:11047-11056.
7. Bader, J. S., and B. Berne. 1995. Solvation energies and electronic spectra in polar, polarizable media: simulation tests of dielectric continuum theory. J. Chem. Phys. 104:1293-1308.
8. Baptista, A. M., P. J. Martel, and S. B. Petersen. 1997. Simulation of protein conformational freedom as a function of pH: constant pH molecular dynamics using implicit titration. Proteins. 27:523-544.
9. Bashford, D. 1997. An object-oriented programming suite for electrostatic effects in biological molecules. In Scientific Computing in Object-Oriented Parallel Environments. Vol. 1343. Lecture Notes in Computer Science. ISCOPE97. Y. Ishikawa, R. R. Oldehoeft, J. V. W. Reynders, and M. Tholburn, editors. Springer, Berlin, Germany.
10. as of ionizable groups in proteins: atomic detail from a continuum electrostatic model. Biochemistry. 29: 10219-10225.
11. Beroza, P., and D. Case. 1996. Including sidechain flexibility in continuum electrostatics calculations of protein titration. J. Phys. Chem. 100:20156-20163.
12. Bone, S., and R. Pethig. 1985. Dielectric studies of protein hydration and hydration-induced flexibility. J. Mol. Biol. 181:323-326.
13. Ceccarelli, M., and M. Marchi. 2003. Simulation and modeling of the Rhodobacter spaeroides bacterial reaction center. J. Phys. Chem. B. 107:1423-1431.
14. Cornell, W., P. Cieplak, C. Bayly, I. Gould, K. Merz, D. Ferguson, D. Spellmeyer, T. Fox, J. Caldwell, and P. Kollman. 1995. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117:5179-5197.
15. Cramer, C., and D. Truhlar. 1999. Implicit solvent models: equilibria, structure, spectra, and dynamics. Chem. Rev. 99:2161-2200.
16. Davis, M. E., and J. A. McCammon. 1990. Electrostatics in biomolecular structure and dynamics. Chem. Rev. 90:509-521.
17. as of ionizable residues in proteins: an explicit solvent calculation for lysozyme. Proteins. 20:85-97.
18. as in the active site of Escherichia coli thioredoxin. Biochemistry. 37:10298-10306.
19. Dlugosz, M., and J. Antosiewicz. 2004. Constant-pH molecular dynamics simulations: a test case of succinic acid. Chem. Phys. 302:161-170.
20. a calculations. Proteins. 54:744-758.
21. Feig, M., and C. L. Brooks III. 2004. Recent advances in the development and application of implicit solvent models in biomolecule simulations. Curr. Opin. Struct. Biol. 14:217-224.
22. Florian, J., M. Goodman, and A. Warshel. 2002. Theoretical investigation of the binding free energies and key substrate-recognition components of the replication fidelity of human DNA polymerase β. J. Phys. Chem. B. 106:5739-5753.
23. Florian, J., M. Goodman, and A. Warshel. 2003. Computer simulation studies of the fidelity of DNA polymerases. Biopolymers. 68:286-299.
24. Flyvbjerg, H., and H. Petersen. 1989. Error estimates on averages of correlated data. J. Chem. Phys. 91:461-466.
25. α values in proteins. Proteins. 48:388-403.
26. Fröhlich, H. 1949. Theory of Dielectrics. Clarendon Press, Oxford, UK.
27. as in proteins. Biophys. J. 83:1731-1748.
28. Gilson, M. K. 1993. Multiple-site titration and molecular modeling: two rapid methods for computing energies and forces for ionizable groups in proteins. Proteins. 15:266-282.
29. Hoefinger, S., and T. Simonson. 2001. Dielectric relaxation in proteins: a continuum electrostatics model- incorporating dielectric heterogeneity of the protein and time-dependent charges. J. Comput. Chem. 22:290-305.
30. Honig, B., and A. Nicholls. 1995. Classical electrostatics in biology and chemistry. Science. 268:1144-1149.
31. Jorgensen, W. L. 2004. The many roles of computation in drug discovery. Science. 303:1813-1818.
32. Jorgensen, W. L., and J. Tirado-Rives. 1988. The OPLS potential function for proteins, energy minimization for crystals of cyclic peptides and crambin. J. Am. Chem. Soc. 110:1657-1666.
33. King, G., F. Lee, and A. Warshel. 1991. Microscopic simulations of macroscopic dielectric constants of solvated proteins. J. Chem. Phys. 95:4366-4377.
34. Krishtalik, L., A. Kuznetsov, and E. Mertz. 1997. Electrostatics of proteins: description in terms of two dielectric constants simultaneously. Proteins. 28:174-182.
35. a of 7.5. Its titration produces a related shift in global stability. Biochemistry. 30:7603-7609.
36. a. Biochemistry. 30:7609-7614.
37. Lee, F., Z. Chu, M. B. Bolger, and A. Warshel. 1992. Calculations of antibody-antigen interactions: microscopic and semi-microscopic evaluation of the free energies of binding of phosphorylcholine analogues to McPC603. Protein Eng. 5:215-228.
38. Lee, F., Z. Chu, and A. Warshel. 1993. Microscopic and semimicroscopic calculations of electrostatic energies in proteins by the Polaris and Enzymix programs. J. Comput. Chem. 14:161-185.
39. Lee, M., F. Salsbury, and C. L. Brooks. 2003. Constant pH molecular dynamics using continuous titration coordinates. Proteins. 56:731-752.
40. Mackerell, A. D., D. Bashford, M. Bellott, R. Dunbrack, J. Evanseck, M. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph, L. Kuchnir, et al. 1998. An all-atom empirical potential for molecular modelling and dynamics study of proteins. J. Phys. Chem. B. 102:3586-3616.
41. 1 and implications for catalysis. J. Mol. Biol. 247:774-807.
42. Madura, J., J. Briggs, R. Wade, M. Davis, B. Luty, A. Hin, J. Antosiewicz, M. Gilson, B. Baheri, L. Scott, and J. McCammon. 1995. Electrostatics and diffusion of molecules in solution: simulations with the University of Houston Brownian dynamics program. Comput. Phys. Commun. 91:57-95.
43. Marcus, R. 1956. Electrostatic free energy and other properties of states having nonequilibrium polarization. J. Chem. Phys. 24:979-989.
44. Marcus, R. 1964. Chemical and electro-chemical electron transfer theory. Annu. Rev. Phys. Chem. 15:155-196.
45. Marcus, R. 1965. On the theory of shifts and broadening of electronic spectra of polar solutes in polar media. J. Chem. Phys. 43:1261-1274.
46. Mehler, E., and F. Guarnieri. 1999. A self-consistent, microenvironment modulated screened potential approximation to calculate pH-dependent electrostatic effects in proteins. Biophys. J. 77:3-22.
47. Mertz, E., and L. Krishtalik. 2000. Low dielectric response in enzyme active site. Proc. Natl. Acad. Sci. USA. 97:2081-2086.
48. Mohan, V., M. Davis, J. A. McCammon, and B. M. Pettitt. 1992. Continuum model calculations of solvation free energies: accurate evaluation of electrostatic contributions. J. Phys. Chem. 96:6428-6431.
49. Morikis, D., A. H. Elcock, P. A. Jennings, and J. A. McCammon. 2001. Native state conformational dynamics of GART: a regulatory pH-dependent coil-helix transition examined by electrostatic calculations. Protein Sci. 10:2363-2378.
50. Muegge, I., P. X. Qi, A. J. Wand, Z. T. Chu, and A. Warshel. 1997. Reorganization energy of cytochrome c revisited. J. Phys. Chem. B. 101: 825-836.
51. Nakamura, H. 1996. Roles of electrostatic interactions in proteins. Q. Rev. Biophys. 29:1-90.
52. a values in enzyme active sites. Protein Sci. 12:1894-1901.
53. Pitera, J., M. Falta, and W. van Gunsteren. 2001. Dielectric properties of proteins from simulations: the effects of solvent, ligands, pH, and temperature. Biophys. J. 80:2546-2555.
54. a calculations for class a β-lactamases: methodological and mechanistic implications. Biophys. J. 73:2416-2426.
55. Roux, B., and T. Simonson. 1999. Implicit solvent models. Biophys. Chem. 78:1-20.
56. Schaefer, M., and M. Karplus. 1997. pH-dependence of protein stability: absolute electrostatic free energy differences between conformations. J. Phys. Chem. B. 101:1663-1683.
57. Schaefer, M., H. v. Vlijmen, and M. Karplus. 1998. Electrostatic contributions to molecular free energies in solution. Adv. Protein Chem. 51:1-57.
58. Schutz, C. N., and A. Warshel. 2001. What are the dielectric constants of proteins and how to validate electrostatic models? Proteins. 44:400-417.
59. as of ionizable residues in proteins: semi-microscopic and microscopic approaches. J. Phys. Chem. B. 101:4458-4472.
60. Sham, Y. Y., I. Muegge, and A. Warshel. 1998. The effect of protein relaxation on charge-charge interactions and dielectric constants of proteins. Biophys. J. 74:1744-1753.
61. Sharp, K. 1998. Calculation of electron transfer reorganization energies using the finite-difference Poisson-Boltzmann model. Biophys. J. 73: 1241-1250.
62. Simonson, T. 2002. Gaussian fluctuations and linear response in an electron transfer protein. Proc. Natl. Acad. Sci. USA. 99:6544-6549.
63. Simonson, T. 2003. Electrostatics and dynamics of proteins. Rep. Prog. Phys. 66:737-787.
64. Simonson, T., G. Archontis, and M. Karplus. 1999. A Poisson-Boltzmann study of charge insertion in an enzyme active site: the effect of dielectric relaxation. J. Phys. Chem. B. 103:6142-6156.
65. Simonson, T., and A. T. Brünger. 1994. Solvation free energies estimated from macroscopic continuum theory: an accuracy assessment. J. Phys. Chem. 98:4683-4694.
66. a calculations with explicit and implicit solvent models. J. Am. Chem. Soc. 126:4167-4180.
67. Simonson, T., and D. Perahia. 1995a. Internal and interfacial dielectric properties of cytochrome c from molecular dynamics simulations in aqueous solution. Proc. Natl. Acad. Sci. USA. 92:1082-1086.
68. Simonson, T., and D. Perahia. 1995b. Microscopic dielectric properties of cytochrome c from molecular dynamics simulations in aqueous solution. J. Am. Chem. Soc. 117:7987-8000.
69. Simonson, T., D. Perahia, and A. T. Brünger. 1991. Microscopic theory of the dielectric properties of proteins. Biophys. J. 59:670-690.
70. Smith, P., R. Brunne, A. Mark, and W. F. van Gunsteren. 1993. The dielectric constant of trypsin inhibitor and lysozyme calculated from molecular dynamics simulations. J. Phys. Chem. 97:2009-2014.
71. Steffen, M., K. Lao, and S. Boxer. 1994. Dielectric asymmetry in the photosynthetic reaction center. Science. 264:810-816.
72. Stern, H., and S. Feller. 2003. Calculation of the dielectric permittivity profile of a nonuniform system: application to a lipid bilayer simulation. J. Chem. Phys. 118:3401-3412.
73. Sternberg, M., F. Hayes, A. Russell, P. Thomas, and A. Fersht. 1987. Prediction of electrostatic effects of engineering of protein charges. Nature. 330:86-88.
74. Swietnicki, W. R., R. Petersen, P. Gambetti, and W. K. Suerwicz. 1997. pH-dependent stability and conformation of the recombinant human prion protein PrP(90-231). J. Biochem. (Tokyo). 272:27517-27520.
75. van Vlijmen, H., S. Curry, M. Schaefer, and M. Karplus. 1998. Titration calculations of foot-and-mouth disease virus and their stabilities as a function of pH. J. Mol. Biol. 275:295-308.
76. Varadarajan, R., T. Zewert, H. Gray, and S. Boxer. 1989. Effects of buried ionizable amino acids on the reduction potential of recombinant hemoglobin. Science. 243:69-72.
77. a, proton transfer reactions, and general acid catalysis reactions in enzymes. Biochemistry. 20:3167-3177.
78. Warshel, A. 1987. What about protein polarity? Nature. 330:15-17.
79. Warshel, A., and S. T. Russell. 1985. Calculations of electrostatic interactions in biological systems and in solutions. Q. Rev. Biophys. 17: 283-422.
80. Warshel, A., S. T. Russell, and A. K. Churg. 1984. Macroscopic models for studies of electrostatic interactions in proteins: limitations and applicability. Proc. Natl. Acad. Sci. USA. 81:4785-4789.
81. a and acid pH-dependent stability estimation in proteins: removing dielectric and counterion boundaries. Protein Sci. 8:418-425.
82. a calculations through flexibility based sampling of a water-dominated interaction scheme. Protein Sci. 13: 2793-2805.
83. Warwicker, J., and H. Watson. 1982. Calculation of the electrostatic potential in the active site cleft due to a helix dipoles. J. Mol. Biol. 157:671-679.
84. Yang, A., and B. Honig. 1993. On the pH dependence of protein stability. J. Mol. Biol. 231:459-474.
85. You, T., and D. Bashford. 1995. Conformation and hydrogen ion titration of proteins: a continuum electrostatic model with conformational flexibility. Biophys. J. 69:1721-1733.