Computational protein design is a challenge for implicit solvation models

Biophysical Journal

Volumn 88, Issue 1, 2005, Pages 156-171

  Jaramillo, Alfonso ^a,b   Wodak, Shoshana J ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b LABORATOIRE DE BIOCHIMIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; SOLVENT;

AMINO ACID TRANSPORT; ARTICLE; CRYSTAL STRUCTURE; POISSON DISTRIBUTION; PROTEIN DESIGN; PROTEIN FOLDING; PROTEIN STRUCTURE; SOLVATION; SURFACE PROPERTY; VALIDATION PROCESS;

EID: 11244318120     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.042044     Document Type: Article

References (69)

1. Bashford, D., and D. A. Case. 2000. Generalized bom models of macromolecular solvation effects. Annu. Rev. Phys. Chem. 51:129-152.
2. Bashford, D., and M. Karplus. 1990. pKa's of ionizable groups in proteins: atomic detail from a continuum electrostatic model. Biochemistry. 29: 10219-10225.
3. Bateman, A., E. Birney, L. Cerruti, R. Durbin, L. Etwiller, S. R. Eddy, S. Griffiths-Jones, K. L. Howe, M. Marshall, and E. L. Sonnhammer. 2002. The PFAM protein families database. Nucleic Acids Res. 30:276-280.
4. Ben Naim, A., and Y. Marcus. 1984. Solvation thermodynamics of non-ionic solutes. J. Chem. Phys. 81:2016.
5. Berman, H. M., J. Westbrook, Z. Feng, G. Gilliland, T. N. Bhat, H. Weissig, I. N. Shindyalov, and P. E. Bourne. 2000. The Protein Data Bank. Nucleic Acids Res. 28:235-242.
6. Brooks, B., R. Bruccoleri, B. Olafson, D. States, S. Swaminathan, and M. Karplus. 1983. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4:187-217.
7. Colonna-Cesari, F., and C. Sander. 1990. Excluded volume approximation to protein-solvent interaction The solvent contact model. Biophys. J. 57: 1103-1107.
8. Dahiyat, B. I., C. A. Sarisky, and S. L. Mayo. 1997. De novo protein design: towards fully automated sequence selection. J. Mol. Biol. 273: 789-796.
9. Desjarlais, J. R., and T. M. Handel. 1999. Side-chain and backbone flexibility in protein core design. J. Mol. Biol. 290:305-318.
10. Drexler, K. E. 1981. Proc. Nail. Acad. Sci. USA. 78:5275-5278.
11. Dominy, B. N., and C. L. Brooks. 1999. Development of a generalized Born model parametrization for proteins and nucleic acids. J. Phys. Chem. B. 103:3765-3773.
12. Dunbrack, R. L., Jr., and M. Karplus. 1993. Backbone-dependent rotamer library for proteins. Application to side-chain prediction. J. Mol. Biol. 230:543-574.
13. Edinger, S., C. Cortis, P. Shenkin, and R. Freisner. 1997. Solvation free energies of peptides: comparison of approximate continuum solvation models with accurate solution of the Poisson-Boltzmann equation. J. Phys. Chem. 101:1190-1197.
14. Eisenberg, D., and A. D. McLachlan. 1986. Solvation energy in protein folding and binding. Nature. 319:199-203.
15. Elcock, A. H. 1999. Realistic modeling of the denatured states of proteins allows accurate calculations of the pH dependence of protein stability. J. Mol. Biol. 294:1051-1062.
16. Engelman, D. M., and T. A. Steitz. 1981. The spontaneous insertion of proteins into and across membranes: the helical hairpin hypothesis. Cell. 23:411-422.
17. Feig, M., W. Im, and C. L. Boorks 3rd. 2004. Implicit solvation based on generalized Bom theory in different dielectric environments. J. Chem. Phys. 120:903-911.
18. Feig, M., and C. L. Brooks 3rd. 2004. Advances in the development and application of implicit solvent models in biomolecule simulations. Curr. Opin. Struct. Biol. 14:217-224.
19. Gibson, K. D., and H. A. Scheraga. 1967. Minimization of polypeptide energy. II. Preliminary structures of oxytocin, vasopressin, and an octapeptide from ribonuclease. Proc. Natl. Acad. Sci. USA. 58:1317-1323.
20. Gilson, M. K., M. E. Davis, B. A. Luty, and J. A. McCammon. 1993. Computation of electrostatic forces on solvated molecules using the Poisson-Boltzmann equation. J. Phys. Chem. 97:3591-3600.
21. Goldstein, R. A., Z. A. Luthey-Schulten, and P. G. Wolynes. 1992. Protein tertiary structure recognition using optimized Hamiltonians with local interactions. Proc. Natl. Acad. Sci. USA. 89:9029-9033.
22. Gordon, D. B., S. A. Marshall, and S. L. Mayo. 1999. Energy functions for protein design. Curr. Opin. Struct. Biol. 9:509-513.
23. Henrick, K., and J. M. Thornton. 1998. PQS: a protein quaternary structure file server. Trends Biochem. Sci. 23:358-361.
24. Honig. B., and A. Nicholls. 1995. Classical electrostatics in biology and chemistry. Science. 268:1144-1149.
25. Jaramillo, A., L. Wemisch, S. Hery, and S. J. Wodak. 2001. Automatic procedures for protein design. Comb. Chem. High Throughput Screen. 4:643-659.
26. Jaramillo, A., L. Wernisch, S. Hery, and S. J. Wodak. 2002. Native protein sequences are near optimal for their structures in the protein core but not on the surface. Proc. Natl. Acad. Sci. USA. 99:13554-13559.
27. Jayaram, B., Y. Liu, D. Beveridge. 1998. A modification of the generalized Born theory for improved estimates of solvation energies and pKa shifts. J. Chem. Phys. 109:1465-1471.
28. Kang, Y. K., K. D. Gibson, G. Nemethy, and H. A. Scheraga. 1988. Free energies of hydration of solute molecules 4. Revised treatment of the hydration shell model. J. Phys. Chem. 92:4739-4742.
29. Khechinashvili, N. N., J. Janin, and F. Kodier. 1995. Thermodynamics of the temperature-induced unfolding of globular proteins. Protein Sci. 4:1315-1324.
30. Kirkwood, J. G., and F. H. Westheimer. 1938. J. Chem. Phys. 6:506-517.
31. Koehl, P., and M. Levitt. 1999a. De novo protein design. I. In search of stability and specificity. J. Mol. Biol. 293:1161-1181.
32. Koehl, P., and M. Levitt. 1999b. De novo protein design. II. Plasticity in sequence space. J. Mol. Biol. 293:1183-1193.
33. Kraemer-Pecore, C. M., A. M. Wollacott, and J. R. Desjarlais. 2001. Computational protein design. Curr. Opin. Chem. Biol. 5:690-695.
34. Kuhlman, B., and D. Baker. 2000. Native protein sequences are close to optimal for their structures. Proc Natl Acad Sci USA. 97:10383-10388. Erratum in Proc. Natl. Acad. Sci. USA. 97:13460.
35. Kuhlman, B., and D. Baker. 2000. Native protein sequences are close to optimal for their structures. Proc Natl Acad Sci USA. 97:10383-10388. Erratum in Proc. Natl. Acad. Sci. USA. 97:13460.
36. Lazar, G. A., S. A. Marshall, J. J. Plecs, S. L. Mayo, and J. R. Desjarlais. 2003. Designing proteins for therapeutic applications. Curr. Opin. Struct. Biol. 13:513-518.
37. Lazaridis, T., and M. Karplus. 1997. "New view" of protein folding reconciled with the old through multiple unfolding simulations. Science. 278:1928-1931.
38. Lazaridis, T., and M. Karplus. 1999a. Effective energy function for proteins in solution. Proteins. 35:133-152.
39. Lazaridis, T., and M. Karplus. 1999b. Discrimination of the native from misfolded protein models with an energy function including implicit solvation. J. Mol. Biol. 288:477-487.
40. Lee, M. S., F. R. Salsbury, and C. L. Brooks. 2002. Novel generalized Born methods. J. Chem. Phys. 116:10606-10614.
41. Luo, R., L. David, and M. K. Gilson. 2002. Accelerated Poisson-Boltzmann calculations for static and dynamic systems. J. Comput. Chem. 23:1244-1253.
42. MacKerell, A. D., Jr., D. Bashford, M. Bellott, R. L. Dunbrack, Jr., J. D. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph-McCarthy, L. Kuchnir, K. Kuczera, F. T. K. Lau, C. Mattos, S. Michnick, T. Ngo, D. T. Nguyen, B. Prodhom, W. E. Reiher III, B. Roux, M. Schlenkrich, J. C. Smith, R. Stole, J. Straub, M. Watanabe, J. Wiorkiewicz-Kuczera, D. Yin. and M. Karplus. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102:3586-3616.
43. Makhatadze, G. I., and P. L. Privalov. 1993. Contribution of hydration to protein folding thermodynamics. II., The entropy and Gibbs energy of hydration. J. Mol. Biol. 232:660-679.
44. Nina, M., W. Im, and B. Roux. 1999. Optimized radii for protein solvation forces based on continuum, electrostatics. Biophys. Chem. 78:89-96.
45. Novotny, J., A. A. Rashin, and R. E. Bruccoleri. 1988. Criteria that discriminate between native proteins and incorrectly folded models. Proteins. 4:19-30.
46. Onufriev, A., D. A. Case, and D. Bashford. 2002. Effective Bom radii in the generalized Born approximation: the importance of being perfect. J. Comput. Chem. 23:1297-1304.
47. Ooi, T., M. Oobatake, G. Nemethy, and H. A. Scheraga. 1987. Accessible surface areas as a measure of the thermodynamic parameters of hydration of peptides. Proc. Natl. Acad. Sci. USA. 84:3086-3090.
48. Privalov, P. L., and G. I. Makhatadze. 1993. Contribution of hydration to protein folding thermodynamics I. The enthalpy of hydration J. Mol. Biol. 232:639-659.
49. Raha, K., A. M. Wollacott, M. J. Italia, and J. R. Desjarlais, 2000. Prediction of amino acid sequence from structure. Protein Sci. 9:1106-1119.
50. Roux, B., and T. Simonson. 1999. Implicit solvent models. Biophys. Chem. 78:1-20.
51. Sagui, C., and T. A. Darden. 1999. Molecular dynamics simulations of biomolecules: long-range electrostatic effects. Anna. Rev. Biophys. Biomol. Struct. 28:155-179.
52. Sali, A., E. Shakhnovich, and M. Karplus. 1994. How does a protein fold? Nature. 369:248-251.
53. Samudrala, R., E. S. Huang, P. Koehl, and M. Levitt. 2000. Constructing side chains on near-native main chains for ab initio protein structure prediction. Protein Eng. 13:453-457.
54. Schaefer, M., C. Bartels, and M. Karplus. 1998. Solution conformations and thermodynamics of structured peptides: molecular dynamics simulation with an implicit solvation model. J. Mol. Biol. 284:835-848.
55. Schaefer, M., and M. Karplus. 1996. A comprehensive analytical treatment of continuum electrostatics. J. Phys. Chem. 100:1578-1599.
56. Schiffer, C. A., J. W. Caldwell, R. M. Striud, and P. A. Kollman. 1992. Inclusion of solvation free energy with molecular mechanics energy: alanyl dipeptide as a test case. Protein Sci. 1:396-400.
57. Simonson. T. 2001. Macromolecular electrostatics: continuum models and their growing pains. Curr. Opin. Struct. Biol. 11:243-252.
58. Sitkoff, D., D. J. Lockhart, K. A. Sharp, and B. Honig. 1996. Calculation of electrostatic effects at the amino terminus of an alpha helix. Biophys. J. 67:2251-2260.
59. Sitkoff D., K. A. Sharp, B. Honig. 1994. Correlating solvation free energies and surface tensions of hydrocarbon solutes. Biophys. Chem. 51:397-403; discussion, Biophys. Chem. 51:404-409.
60. Sitkoff D., K. A. Sharp, B. Honig. 1994. Correlating solvation free energies and surface tensions of hydrocarbon solutes. Biophys. Chem. 51:397-403; discussion, Biophys. Chem. 51:404-409.
61. Street, A. G., and S. L. Mayo. 1998. Pairwise calculation of protein solvent accessible surface area. Fold. Des. 3:253-258.
62. Tsui, V., and D. A. Case. 2000. Theory and applications of the generalized Bom solvation model in macromolecular simulations. Biopolymers. 56: 275-291.
63. Wagner, F., and T. Simonson. 1999. Implicit solvent models: combining an analytical formulation of continuum electrostatics with simple models of the hydrophobic effect. J. Comput. Chem. 20:322-335.
64. Wang, G., and R. L. Dunbrack, Jr. 2003. PISCES: a protein sequence culling server. Bioinformatics. 19:1589-1591.
65. Wernisch, L., S. Hery, and S. J. Wodak. 2000. Automatic protein design with all atom force-fields by exact and heuristic optimization. J. Mol. Biol. 301:713-736.
66. Wesson, L., and D. Eisenberg. 1992. Atomic solvation parameters applied to molecular dynamics of proteins in solution. Protein Sci. 1: 227-235.
67. Williams, D., and H. Hall. 1999. Unrestrained simulations of the UUCG tetraloop using an implicit solvation model. Biophys. J. 76:3192-3205.
68. Wodak, S. J., and M. J. Rooman. 1993. Generating and testing protein folds. Curr. Opin. Struct. Biol. 3:247-259.
69. Zou, X., Y. Sun, and I. D. Kuntz. 1999. Inclusion of solvation in ligand binding free energy calculations using the generalized-Bom model. J. Am. Chem. Soc. 121:8033-8043.