Conformational sampling of peptides in cellular environments

Biophysical Journal

Volumn 94, Issue 3, 2008, Pages 747-759

  Tanizaki, Seiichiro ^a   Clifford, Jacob ^b   Connelly, Brian D ^c   Feig, Michael ^a,b,c  

^a Michigan State University   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c Michigan State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE DERIVATIVE; MELITTIN; POLYALANINE; SOLVENT; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; COMPUTER SIMULATION; CONFORMATION; DIELECTRIC CONSTANT; ENVIRONMENT; METHODOLOGY; PREDICTION; SAMPLING;

EID: 38549152231     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.107.116236     Document Type: Article

References (133)

1. Alberts, B., A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter. 2002. Molecular Biology of the Cell. Garland Science, New York.
2. Zimmerman, S. B., and A. P. Minton. 1993. Macromolecular crowding - biochemical, biophysical, and physiological consequences. Annu. Rev. Biophys. Biomol. Struct. 22:27-65.
3. Fulton, A. B. 1982. How crowded is the cytoplasm. Cell. 30:345-347.
4. Ladbury, J. E., and M. A. Williams. 2004. The extended interface: measuring non-local effects in biomolecular interactions. Curr. Opin. Struct. Biol. 14:562-569.
5. Onuchic, J. N., and P. G. Wolynes. 2004. Theory of protein folding. Curr. Opin. Struct. Biol. 14:70-75.
6. Dill, K. A. 1985. Theory for the folding and stability of globular proteins. Biochemistry. 24:1501-1509.
7. Drew, H. R., and R. E. Dickerson. 1981. Structure of a B-DNA dodecamer. III. Geometry of hydration. J. Mol. Biol. 151:535-556.
8. Makarov, V., B. M. Pettitt, and M. Feig. 2002. Solvation and hydration of proteins and nucleic acids: a theoretical view of simulation and experiment. Acc. Chem. Res. 35:376-384.
9. Rosgen, J., B. M. Pettitt, and D. W. Bolen. 2005. Protein folding, stability, and solvation structure in osmolyte solutions. Biophys. J. 89:2988-2997.
10. Street, T. O., D. W. Bolen, and G. D. Rose. 2006. A molecular mechanism for osmolyte-induced protein stability. Proc. Natl. Acad. Sci. USA. 103:13997-14002.
11. Yancey, P. H., M. E. Clark, S. C. Hand, R. D. Bowlus, and G. N. Somero. 1982. Living with water stress: evolution of osmolyte systems. Science. 217:1214-1222.
12. Hartl, F. U., and M. Hayer-Hartl. 2002. Protein folding - molecular chaperones in the cytosol: from nascent chain to folded protein. Science. 295:1852-1858.
13. Takagi, F., N. Koga, and S. Takada. 2003. How protein thermodynamics and folding mechanisms are altered by the chaperonin cage: molecular simulations. Proc. Natl. Acad. Sci. USA. 100:11367-11372.
14. Bishop, G. R., J. S. Ren, B. C. Polander, B. D. Jeanfreau, J. O. Trent, and J. B. Chaires. 2007. Energetic basis of molecular recognition in a DNA aptamer. Biophys. Chem. 126:165-175.
15. Carlson, H. A. 2002. Protein flexibility is an important component of structure-based drug discovery. Curr. Pharm. Des. 8:1571-1578.
16. Bernado, P., J. G. de la Torre, and M. Pons. 2004. Macromolecular crowding in biological systems: hydrodynamics and NMR methods. J. Mol. Recognit. 17:397-407.
17. Ping, G., J.-M. Yuan, Z. Sun, and Y. Wei. 2004. Studies of effects of macromolecular crowding and confinement on protein folding and protein stability. J. Mol. Recognit. 17:433-440.
18. Ellis, R. J. 2001. Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr. Opin. Struct. Biol. 11:114-119.
19. Zhou, H. X. 2004. Protein folding and binding in confined spaces and in crowded solutions. J. Mol. Recognit. 17:368-375.
20. Minton, A. P. 2006. How can biochemical reactions within cells differ from those in test tubes? J. Cell Sci. 119:2863-2869.
21. Friedel, M., D. J. Sheeler, and J. E. Shea. 2003. Effects of confinement and crowding on the thermodynamics and kinetics of folding of a minimalist β-barrel protein. J. Chem. Phys. 118:8106-8113.
22. Brinker, A., G. Pfeifer, M. J. Kerner, D. J. Naylor, F. U. Hartl, and M. Hayer-Hartl. 2001. Dual function of protein confinement in chaperonin-assisted protein folding. Cell. 107:223-233.
23. Davis-Searles, P. R., A. J. Saunders, D. A. Erie, D. J. Winzor, and G. J. Pielak. 2001. Interpreting the effects of small uncharged solutes on protein-folding equilibria. Annu. Rev. Biophys. Biomol. Struct. 30:271-306.
24. Stern, H. A., and S. E. Feller. 2003. Calculation of the dielectric permittivity profile for a nonuniform system: application to a lipid bilayer simulation. J. Chem. Phys. 118:3401-3412.
25. Akhadov, Y. Y. 1981. Dielectric Properties of Binary Solutions. Pergamon Press, Oxford, UK.
26. Gilson, M. K., and B. H. Honig. 1986. The dielectric-constant of a folded protein. Biopolymers. 25:2097-2119.
27. Antosiewicz, J., J. A. McCammon, and M. K. Gilson. 1996. The determinants of pK(a)s in proteins. Biochemistry. 35:7819-7833.
28. Schutz, C. N., and A. Warshel. 2001. What are the dielectric "constants" of proteins and how to validate electrostatic models? Proteins. 44:400-417.
29. Despa, F., A. Fernandez, and R. S. Berry. 2004. Dielectric modulation of biological water. Phys. Rev. Lett. 93:228104.
30. Elcock, A. H., and J. A. McCammon. 1996. The low dielectric interior of proteins is sufficient to cause major structural changes in DNA on association. J. Am. Chem. Soc. 118:3787-3788.
31. Jaaskelainen, S., C. S. Verma, R. E. Hubbard, and L. S. D. Caves. 1999. Identifying key electrostatic interactions in Rhizomucor miehei lipase: the influence of solvent dielectric. Theor. Chem. Acc. 101:175-179.
32. Buck, M. 1998. Trifluoroethanol and colleagues: cosolvents come of age. Recent studies with peptides and proteins. Q. Rev. Biophys. 31:297-355.
33. Dwyer, D. S. 1999. Molecular simulation of the effects of alcohols on peptide structure. Biopolymers. 49:635-645.
34. Roccatano, D., G. Colombo, M. Fioroni, and A. E. Mark. 2002. Mechanism by which 2,2,2-trifluoroethanol/water mixtures stabilize secondary-structure formation in peptides: a molecular dynamics study. Proc. Natl. Acad. Sci. USA. 99:12179-12184.
35. Liu, H. L., and C. M. Hsu. 2003. The effects of various alcohols on the stability of melittin: a molecular dynamics study. J. Chin. Chem. Soc. 50:1235-1240.
36. Nguyen, H. D., A. J. Marchut, and C. K. Hall. 2004. Solvent effects on the conformational transition of a model polyalanine peptide. Protein Sci. 13:2909-2924.
37. Hirota, N., K. Mizuno, and Y. Goto. 1998. Group additive contributions to the alcohol-induced α-helix formation of melittin: implication for the mechanism of the alcohol effects on proteins. J. Mol. Biol. 275:365-378.
38. Hong, D., M. Hoshino, R. Kuboi, and Y. Goto. 1999. Clustering of fluorine-substituted alcohols as a factor responsible for their marked effects on proteins and peptides. J. Am. Chem. Soc. 121:8427-8433.
39. Bhattacharjya, S., J. Venkatraman, P. Balaram, and A. Kumar. 1999. Fluoroalcohols as structure modifiers in peptides and proteins: hexafluoroacetone hydrate stabilizes a helical conformation of melittin at low pH. J. Pept. Res. 54:100-111.
40. Shibata, A., M. Yamamoto, T. Yamashita, J. S. Chiou, H. Kamaya, and I. Ueda. 1992. Biphasic effects of alcohols on the phase transition of poly(L-lysine) between α-helix and β-sheet conformations. Biochemistry. 31:5728-5733.
41. Searle, M. S., R. Zerella, D. H. Williams, and L. C. Packman. 1996. Native-like β-hairpin structure in an isolated fragment from ferredoxin: NMR and CD studies of solvent effects on the N-terminal 20 residues. Protein Eng. 9:559-565.
42. Kovacs, H., A. E. Mark, J. Johansson, and W. F. van Gunsteren. 1995. The effect of environment on the stability of an integral membrane helix: molecular dynamics simulations of surfactant protein C in chloroform, methanol and water. J. Mol. Biol. 247:808-822.
43. Hartsough, D. S., and K. M. Merz. 1992. Protein flexibility in aqueous and nonaqueous solutions. J. Am. Chem. Soc. 114:10113-10116.
44. Affleck, R., C. A. Haynes, and D. S. Clark. 1992. Solvent dielectric effects on protein dynamics. Proc. Natl. Acad. Sci. USA. 89:5167-5170.
45. Clark, D. S. 2004. Characteristics of nearly dry enzymes in organic solvents: implications for biocatalysis in the absence of water. Philos. Trans. R. Soc. B. 359:1299-1328.
46. Vila, J. A., D. R. Ripoll, and H. A. Scheraga. 2000. Physical reasons for the unusual α-helix stabilization afforded by charged or neutral polar residues in alanine-rich peptides. Proc. Natl. Acad. Sci. USA. 97:13075-13079.
47. Sharp, K. A., and B. Honig. 1990. Electrostatic interactions in macromolecules - theory and applications. Annu. Rev. Biophys. Biophys. Chem. 19:301-332.
48. Feig, M., and S. Tanizaki. 2006. Development of a heterogeneous dielectric generalized Born model for the implicit modeling of membrane environments In Modelling Molecular Structure and Reactivity in Biological Systems. K. Naidoo, editor. Royal Society of Chemistry. Cambridge, UK. 141-150.
49. Lin, J.-H., N. A. Baker, and J. A. McCammon. 2002. Bridging implicit and explicit solvent approaches for membrane electrostatics. Biophys. J. 83:1374-1379.
50. Roux, B. 1997. Influence of the membrane potential on the free energy of an intrinsic protein. Biophys. J. 73:2980-2989.
51. Gilson, M. K., K. A. Sharp, and B. H. Honig. 1987. Calculating the electrostatic potential of molecules in solution: method and error assessment. J. Comput. Chem. 9:327-335.
52. Baker, N. A. 2005. Improving implicit solvent simulations: a Poisson-centric view. Curr. Opin. Struct. Biol. 15:137-143.
53. Feig, M., and C. L. Brooks 3rd. 2004. Recent advances in the development and application of implicit solvent models in biomolecule simulations. Curr. Opin. Struct. Biol. 14:217-224.
54. Feig, M., W. Im, and C. L. Brooks 3rd. 2004. Implicit solvation based on generalized Born theory in different dielectric environments. J. Chem. Phys. 120:903-911.
55. Sigalov, G., P. Scheffel, and A. Onufriev. 2005. Incorporating variable dielectric environments into the generalized Born model. J. Chem. Phys. 122:094511
56. Hassan, S. A., and E. L. Mehler. 2002. A critical analysis of continuum electrostatics: the screened Coulomb potential-implicit solvent model and the study of the alanine dipeptide and discrimination of misfolded structures of proteins. Proteins. 47:45-61.
57. Smith, P. E. 1999. The alanine dipeptide free energy surface in solution. J. Chem. Phys. 111:5568-5579.
58. Wan, S. Z., C. X. Wang, Z. X. Xiang, and Y. Y. Shi. 1997. Stochastic dynamics simulation of alanine dipeptide: including solvation interaction determined by boundary element method. J. Comput. Chem. 18:1440-1449.
59. Chekmarev, D. S., T. Ishida, and R. M. Levy. 2004. Long-time conformational transitions of alanine dipeptide in aqueous solution: continuous and discrete-state kinetic models. J. Phys. Chem. B. 108:19487-19495.
60. Swope, W. C., J. W. Pitera, F. Suits, M. Pitman, M. Eleftheriou, B. G. Fitch, R. S. Germain, A. Rayshubski, T. J. C. Ward, Y. Zhestkov, and R. Zhou. 2004. Describing protein folding kinetics by molecular dynamics simulations. 2. Example applications to alanine dipeptide and β-hairpin peptide. J. Phys. Chem. B. 108:6582-6594.
61. Feig, M. 2007. Kinetics from implicit solvent simulations of biomolecules as a function of viscosity. J. Chem. Theory Comput. 3:1734-1748.
62. Drozdov, A. N., A. Grossfield, and R. V. Pappu. 2004. Role of solvent in determining conformational preferences of alanine dipeptide in water. J. Am. Chem. Soc. 126:2574-2581.
63. Hu, H., M. Elstner, and J. Hermans. 2003. Comparison of a QM/MM force field and molecular mechanics force fields in simulations of alanine and glycine "dipeptides" (Ace-Ala-Nme and Ace-Gly-Nme) in water in relation to the problem of modeling the unfolded peptide backbone in solution. Proteins. 50:451-463.
64. MacKerell, A. D. Jr., M. Feig, and C. L. Brooks 3rd. 2004. Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J. Comput. Chem. 25:1400-1415.
65. Reference deleted in proof.
66. Brooks, C. L., and D. A. Case. 1993. Simulations of peptide conformational dynamics and thermodynamics. Chem. Rev. 93:2487-2502.
67. Kaminski, G. A., R. A. Friesner, J. Tirado-Rives, and W. L. Jorgensen. 2001. Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides. J. Phys. Chem. B. 105:6474-6487.
68. Shi, Z. S., C. A. Olson, G. D. Rose, R. L. Baldwin, and N. R. Kallenbach. 2002. Polyproline II structure in a sequence of seven alanine residues. Proc. Natl. Acad. Sci. USA. 99:9190-9195.
69. Makowska, J., S. Rodziewicz-Motowidlo, K. Baginska, J. A. Vila, A. Liwo, L. Chmurzynski, and H. A. Scheraga. 2006. Polyproline II conformation is one of many local conformational states and is not an overall conformation of unfolded peptides and proteins. Proc. Natl. Acad. Sci. USA. 103:1744-1749.
70. Kim, Y. S., J. P. Wang, and R. M. Hochstrasser. 2005. Two-dimensional infrared spectroscopy of the alanine dipeptide in aqueous solution. J. Phys. Chem. B. 109:7511-7521.
71. Ooi, T., and M. Oobatake. 1991. Prediction of the thermodynamics of protein unfolding: the helix-coil transition of poly (L-alanine). Proc. Natl. Acad. Sci. USA. 88:2859-2863.
72. Takano, M., T. Yamato, J. Higo, A. Suyama, and K. Nagayama. 1999. Molecular dynamics of a 15-residue poly(L-alanine) in water. Helix formation and energetics. J. Am. Chem. Soc. 121:605-612.
73. Ohkubo, Y. Z., and C. L. Brooks 3rd. 2003. Exploring Flory's isolated-pair hypothesis: statistical mechanics of helix-coil transitions in polyalanine and the C peptide for Rnase A. Proc. Natl. Acad. Sci. USA. 100:13916-13921.
74. Daggett, V., P. A. Kollman, and I. D. Kuntz. 1991. A molecular dynamics simulation of polyalanine: an analysis of equilibrium motions and helix-coil transitions. Biopolymers. 31:1115-1134.
75. Miller, J. S., R. J. Kennedy, and D. S. Kemp. 2002. Solubilized, spaced polyalanines: a context-free system for determining amino acid α-helix propensities. J. Am. Chem. Soc. 124:945-962.
76. Levy, Y., J. Jortner, and O. M. Becker. 2001. Solvent effects on the energy landscapes and folding kinetics of polyalanine. Proc. Natl. Acad. Sci. USA. 98:2188-2193.
77. Ingwall, R. T., H. A. Scheraga, N. Lotan, A. Berger, and E. Katchals. 1968. Conformational studies of poly-L-alanine in water. Biopolymers. 6:331-368.
78. Garcia, A. E., and K. Y. Sanbonmatsu. 2002. α-Helical stabilization by side chain shielding of backbone hydrogen bonds. Proc. Natl. Acad. Sci. USA. 99:2782-2787.
79. Cammers-Goodwin, A., T. J. Allen, S. L. Oslick, K. F. McClure, J. H. Lee, and D. S. Kemp. 1996. Mechanism of stabilization of helical conformations of polypeptides by water containing trifluoroethanol. J. Am. Chem. Soc. 118:3082-3090.
80. Olivella, M., X. Deupi, C. Govaerts, and L. Pardo. 2002. Influence of the environment in the conformation of α-helices studied by protein database search and molecular dynamics simulations. Biophys. J. 82:3207-3213.
81. Spek, E. J., C. A. Olson, Z. Shi, and N. R. Kallenbach. 1999. Alanine is an intrinsic α-helix stabilizing amino acid. J. Am. Chem. Soc. 121:5571-5572.
82. Roe, D. R., A. Okur, L. Wickstrom, V. Hornak, and C. Simmerling. 2007. Secondary structure bias in generalized Born solvent models: comparison of conformational ensembles and free energy of solvent polarization from explicit and implicit solvation. J. Phys. Chem. B. 111:1846-1857.
83. Miller, J. S., R. J. Kennedy, and D. S. Kemp. 2001. Short, solubilized polyalanines are conformational chameleons: exceptionally helical if N- and C-capped with helix stabilizers, weakly to moderately helical if capped with rigid spacers. Biochemistry. 40:305-309.
84. Kennedy, R. J., K.-Y. Tsang, and D. S. Kemp. 2002. Consistent helicities from CD and template t/c data for N-templated polyalanines: progress toward resolution of the alanine helicity problem. J. Am. Chem. Soc. 124:934-944.
85. Dempsey, C. E. 1990. The actions of melittin on membranes. Biochim. Biophys. Acta. 1031:143-161.
86. John, E., and F. Jahnig. 1991. Aggregation state of melittin in lipid vesicle membranes. Biophys. J. 60:319-328.
87. Dempsey, C. E., and G. S. Butler. 1992. Helical structure and orientation of melittin in dispersed phospholipid membranes from amide exchange analysis in situ. Biochemistry. 31:11973-11977.
88. Sessions, R. B., N. Gibbs, and C. E. Dempsey. 1998. Hydrogen bonding in helical polypeptides from molecular dynamics simulations and amide hydrogen exchange analysis: alamethicin and melittin in methanol. Biophys. J. 74:138-152.
89. Berneche, S., M. Nina, and B. Roux. 1998. Molecular dynamics simulation of melittin in a dimyristoylphosphatidylcholine bilayer membrane. Biophys. J. 75:1603-1618.
90. Im, W., M. Feig, and C. L. Brooks 3rd. 2003. An implicit membrane generalized Born theory for the study of structure, stability, and interactions of membrane proteins. Biophys. J. 85:2900-2918.
91. Terwilliger, T. C., and D. Eisenberg. 1982. The structure of melittin. I. Structure determination and partial refinement. J. Biol. Chem. 257:6010-6015.
92. Terwilliger, T. C., and D. Eisenberg. 1982. The structure of melittin. II. Interpretation of the structure. J. Biol. Chem. 257:6016-6022.
93. 1H-NMR studies of monomeric melittin in aqueous solution. Biochim. Biophys. Acta. 622:219-230.
94. Gerig, J. T. 2004. Structure and solvation of melittin in 1,1,1,3,3,3-hexafluoro-2-propanol/water. Biophys. J. 86:3166-3175.
95. Gerig, J. T. 2004. Structure and solvation of melittin in hexafluoroacetone/ water. Biopolymers. 74:240-247.
96. 1H-NMR study in methanol. Eur. J. Biochem. 173:139-146.
97. Inagaki, F., I. Shimada, K. Kawaguchi, M. Hirano, I. Terasawa, T. Ikura, and N. Go. 1989. Structure of melittin bound to perdeuterated dodecylphosphocholine micelles as studied by two-dimensional NMR and distance geometry calculations. Biochemistry. 28:5985-5991.
98. Roccatano, D., M. Fioroni, M. Zacharias, and G. Colombo. 2005. Effect of hexafluoroisopropanol alcohol on the structure of melittin: a molecular dynamics simulation study. Protein Sci. 14:2582-2589.
99. Glättli, A., I. Chandrasekhar, and W. F. van Gunsteren. 2006. A molecular dynamics study of the bee venom melittin in aqueous solution, in methanol, and inserted in a phospholipid bilayer. Eur. Biophys. J. 35:255-267.
100. Still, W. C., A. Tempczyk, R. C. Hawley, and T. Hendrickson. 1990. Semianalytical treatment of solvation for molecular mechanics and dynamics. J. Am. Chem. Soc. 112:6127-6129.
101. Lee, M. S., M. Feig, F. R. Salsbury Jr., and C. L. Brooks 3rd. 2003. New analytical approximation to the standard molecular volume definition and its application to generalized Born calculations. J. Comput. Chem. 24:1348-1356.
102. Lee, M. S., F. R. Salsbury Jr., and C. L. Brooks 3rd. 2002. Novel generalized Born methods. J. Chem. Phys. 116:10606-10614.
103. Feig, M., A. Onufriev, M. S. Lee, W. Im, D. A. Case, and C. L. Brooks 3rd. 2004. Performance comparison of generalized Born and Poisson methods in the calculation of electrostatic solvation energies for protein structures. J. Comput. Chem. 25:265-284.
104. Chocholousova, J., and M. Feig. 2006. Balancing an accurate representation of the molecular surface in generalized Born formalisms with integrator stability in molecular dynamics simulations. J. Comput. Chem. 27:719-729.
105. Sitkoff, D., K. A. Sharp, and B. Honig. 1994. Accurate calculation of hydration free-energies using macroscopic solvent models. J. Phys. Chem. 98:1978-1988.
106. Hansmann, U. H. E., and Y. Okamoto. 1999. New Monte Carlo algorithms for protein folding. Curr. Opin. Struct. Biol. 9:177-183.
107. Sugita, Y., and Y. Okamoto. 1999. Replica-exchange molecular dynamics method for protein folding. Chem. Phys. Lett. 314:141-151.
108. Brooks, B. R., R. E. Bruccoleri, B. D. Olafson, D. J. States, S. Swaminathan, and M. Karplus. 1983. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4:187-217.
109. Feig, M., J. Karanicolas, and C. L. Brooks 3rd. 2004. MMTSB tool set: enhanced sampling and multiscale modeling methods for applications in structural biology. J. Mol. Graph. Model. 22:377-395.
110. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:33-38.
111. MacKerell, A. D. Jr., D. Bashford, M. Bellott, J. D. Dunbrack, M. J. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph-McCarthy, L. Kuchnir, et al. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102:3586-3616.
112. MacKerell, A. D. Jr., M. Feig, and C. L. Brooks 3rd. 2004. Improved treatment of the protein backbone in empirical force fields. J. Am. Chem. Soc. 126:698-699.
113. Feig, M., A. D. MacKerell, and C. L. Brooks. 2003. Force field influence on the observation of pi-helical protein structures in molecular dynamics simulations. J. Phys. Chem. B. 107:2831-2836.
114. Ryckaert, J. P., G. Ciccotti, and H. J. C. Berendsen. 1977. Numerical-integration of Cartesian equations of motion of a system with constraints - molecular-dynamics of N-alkanes. J. Comput. Phys. 23:327-341.
115. Brooks, C. L., M. Berkowitz, and S. A. Adelman. 1980. Generalized Langevin theory for many-body problems in chemical-dynamics - gas-surface collisions, vibrational-energy relaxation in solids, and recombination reactions in liquids. J. Chem. Phys. 73:4353-4364.
116. Kumar, S., D. Bouzida, R. H. Swendsen, P. A. Kollman, and J. M. Rosenberg. 1992. The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. J. Comput. Chem. 13:1011-1021.
117. Kumar, S., J. M. Rosenberg, D. Bouzida, R. H. Swendsen, and P. A. Kollman. 1995. Multidimensional free-energy calculations using the weighted histogram analysis method. J. Comput. Chem. 16:1339-1350.
118. Chen, J. H., W. P. Im, and C. L. Brooks. 2006. Balancing solvation and intramolecular interactions: toward a consistent generalized Born force field. J. Am. Chem. Soc. 128:3728-3736.
119. Mackerell, A. D. 2004. Empirical force fields for biological macromolecules: overview and issues. J. Comput. Chem. 25:1584-1604.
120. Zhu, J., L. Xie, and B. Honig. 2006. Structural refinement of protein segments containing secondary structure elements: local sampling, knowledge-based potentials, and clustering. Proteins. 65:463-479.
121. Blondelle, S. E., L. R. Simpkins, E. Perezpaya, and R. A. Houghten. 1993. Influence of tryptophan residues on melittins hemolytic activity. Biochim. Biophys. Acta. 1202:331-336.
122. Cheung, M. S., and D. Thirumalai. 2007. Effects of crowding and confinement on the structure of the transition state ensemble in proteins. J. Phys. Chem. B. 111:8250-8257.
123. Cheung, M. S., and D. Thirumalai. 2006. Nanopore-protein interactions dramatically alter stability and yield of the native state in restricted spaces. J. Mol. Biol. 357:632-643.
124. Cheung, M. S., D. Klimov, and D. Thirumalai. 2005. Molecular crowding enhances native state stability and refolding rates of globular proteins. Proc. Natl. Acad. Sci. USA. 102:4753-4758.
125. Chocholousova, J., and M. Feig. 2006. Implicit solvent simulations of DNA and DNA-protein complexes: agreement with explicit solvent vs experiment. J. Phys. Chem. B. 110:17240-17251.
126. Feig, M., and B. M. Pettitt. 1999. Modeling high-resolution hydration patterns in correlation with DNA sequence and conformation. J. Mol. Biol. 286:1075-1095.
127. Geney, R., M. Layten, R. Gomperts, V. Hornak, and C. Simmerling. 2006. Investigation of salt bridge stability in a generalized born solvent model. J. Chem. Theory Comput. 2:115-127.
128. Petsko, G. A., and D. Ringe. 2003. Protein Structure and Function. New Science Press, London, UK.
129. Marqusee, S., V. H. Robbins, and R. L. Baldwin. 1989. Unusually stable helix formation in short alanine-based peptides. Proc. Natl. Acad. Sci. USA. 86:5286-5290.
130. Yang, S., and M. Cho. 2007. Thermal denaturation of polyalanine peptide in water by molecular dynamics simulations and theoretical prediction of infrared spectra: helix-coil transition kinetics. J. Phys. Chem. B. 111:605-617.
131. Wilcox, W., and D. Eisenberg. 1992. Thermodynamics of melittin tetramerization determined by circular dichroism and implications for protein folding. Protein Sci. 1:641-653.
132. van Gunsteren, W. F., S. R. Billeter, A. A. Eising, P. H. Huenenberger, P. Krueger, A. E. Mark, W. R. P. Scott, and I. G. Tirono. 1996. Biomolecular Simulation: The GROMOS96 Manual and User Guide. Vdf Hochschulverlage AG an der ETH Zürich, Zurich, Switzerland.
133. Yoda, T., Y. Sugita, and Y. Okamoto. 2004. Secondary-structure preferences of force fields for proteins evaluated by generalized ensemble simulations. Chem. Phys. 307:269-283.