Weak Interactions in Protein Folding: Hydrophobic Free Energy, van der Waals Interactions, Peptide Hydrogen Bonds, and Peptide Solvation

Protein Folding Handbook

Volumn 1, Issue , 2008, Pages 127-162

  Baldwin, Robert L ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Definition; Hydrocarbon; Hydrogen; Prediction; Solvation

Indexed keywords

EID: 84889817479     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527619498.ch6     Document Type: Chapter

References (128)

1. Kauzmann, W. (1959). Factors in interpretation of protein denaturation. Adv. Protein Chem. 14, 1-63.
2. Dill, K. A. (1990). Dominant forces in protein folding. Biochemistry 29, 7133-7155.
3. Privalov, P. L. & Gill, S. J. (1988). Stability of protein structure and hydrophobic interaction. Adv. Protein Chem. 39, 191-234.
4. Privalov, P. L. & Gill, S. J. (1989). The hydrophobic effect: a reappraisal. Pure Appl. Chem. 61, 1097-1104.
5. Dill, K. A. (1990). The meaning of hydrophobicity. Science 250, 297-298.
6. Schellman, J. A. (1955). The stability of hydrogen-bonded peptide structures in aqueous solution. C.R. Trav. Lab. Carlsberg Sér Chim. 29, 230-259.
7. Stickle, D. F., Presta, L. G., Dill, K. A., & Rose, G. D. (1992). Hydrogen bonding in globular proteins. J. Mol. Biol. 226, 1143-1159.
8. Kendrew, J. C., Dickerson, R. E., Strandberg, B. E. et al. (1960). Structure of myoglobin. A threedimensional Fourier synthesis at 2A° resolution. Nature 185, 422-427.
9. Pauling, L., Corey, R. B. & Branson, H. R. (1951). The structure of proteins: two hydrogen-bonded helical configurations of the polypeptide chain. Proc. Natl Acad. Sci. USA 37, 205-211.
10. Tanford, C. (1980). The Hydrophobic Effect, 2nd edn. John Wiley & Sons, New York.
11. Tanford, C. (1997). How protein chemists learned about the hydrophobic factor. Protein Sci. 6, 1358-1366.
12. Southall, N. T., Dill, K. A., & Haymet, A. D. J. (2002). A view of the hydrophobic effect. J. Phys Chem. B 106, 521-533.
13. Nozaki, Y. & Tanford, C. (1971). The solubility of amino acids and two glycine peptides in aqueous ethanol and dioxane solutions. J. Biol. Chem. 246, 2211-2217.
14. Fauchére, J.-L. & Pliska, V. (1983). Hydrophobic parameters p of aminoacid side chains from partitioning of N-acetyl-amino-acid amides. Eur. J. Med. Chem. 18, 369-375.
15. Wimley, W. C., Creamer, T. P., & White, S. H. (1996). Solvation energies of amino acid side chains and backbone in a family of host-guest pentapeptides. Biochemistry 35, 5109-5124.
16. Radzicka, A. & Wolfenden, R. (1988). Comparing the polarities of the amino acids: side-chain distribution coefficients between the vapor phase, cyclohexane, 1-octanol and neutral aqueous solution. Biochemistry 27, 1644-1670.
17. Hermann, R. B. (1972). Theory of hydrophobic bonding. II. The correlation of hydrocarbon solubility in water with solvent cavity surface area. J. Phys. Chem. 76, 2754-2759.
18. Chothia, C. (1974). Hydrophobic bonding and accessible surface area in proteins. Nature 248, 338-339.
19. Reynolds, J. A., Gilbert, D. B., & Tanford, C. (1974). Empirical correlation between hydrophobic free energy and aqueous cavity surface area. Proc. Natl Acad. Sci. USA 71, 2925-2927.
20. Lee, B. & Richards, F. M. (1971). The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55, 379-400.
21. Sharp, K. A., Nicholls, A., Friedman, R., & Honig, B. (1991). Extracting hydrophobic free energies from experimental data: relationship to protein folding and theoretical models. Biochemistry 30, 9686-9697.
22. Hermann, R. B. (1977). Use of solvent cavity area and number of packed molecules around a solute in regard to hydrocarbon solubilities and hydrophobic interactions. Proc. Natl Acad. Sci. USA 74, 4144-4145.
23. Ben-Naim, A. & Marcus, Y. (1984). Solvation thermodynamics of nonionic solutes. J. Chem. Phys. 81, 2016-2027.
24. Lee, B. (1991). Solvent reorganization contribution to the transfer thermodynamics of small nonpolar molecules. Biopolymers 31, 993-1008.
25. Lee, B. (1995). Analyzing solvent reorganization and hydrophobicity. Methods Enzymol. 259, 555-576.
26. Widom, B. (1982). Potentialdistribution theory and the statistical mechanics of fluids. J. Phys. Chem. 86, 869-872.
27. Jorgensen, W. L., Gao, J., & Ravimohan, C. (1985). Monte Carlo simulations of alkanes in water. Hydration numbers and the hydrophobic effect. J. Phys. Chem. 89, 3470-3473.
28. Pratt, L. R. & Chandler, D. (1977). Theory of the hydrophobic effect. J. Chem. Phys. 67, 3683-3704.
29. Gallichio, E., Kubo, M. M., & Levy, R. M. (2000). Enthalpy-entropy and cavity decomposition of alkane hydration free energies: Numerical results and implications for theories of hydrophobic solvation. J. Phys. Chem. B 104, 6271-6285.
30. Lee, B. (1985). The physical origin of the low solubility of nonpolar solutes in water. Biopolymers 24, 813-823.
31. Rank, J. A. & Baker, D. (1998). Contributions of solvent-solvent hydrogen bonding and van der Waals interaction to the attraction between methane molecules in water. Biophys. Chem. 71, 199-204.
32. Tanford, C. (1979). Interfacial free energy and the hydrophobic effect. Proc. Natl Acad. Sci. USA 76, 4175-4176.
33. Postma, J. P. M., Berendsen, H. J. C., & Haak, J. R. (1982). Thermodynamics of cavity formation in water: a molecular dynamics study. Faraday Symp. Chem. Soc. 17, 55-67.
34. Hummer, G., Garde, S., García, A., Pohorille, A., & Pratt, L. R. (1996). An information theory model of hydrophobic interactions. Proc. Natl Acad. Sci. USA 93, 8951-8955.
35. DeYoung, L. R. & Dill, K. A. (1990). Partitioning of nonpolar solutes into bilayers and amorphous n-alkanes. J. Phys. Chem. 94, 801-809.
36. Chan, H. S. & Dill, K. A. (1997). Solvation: how to obtain microscopic energies from partitioning and solvation experiments. Annu. Rev. Biophys. Biomol. Struct. 26, 425-459.
37. Chandler, D. (2004). Hydrophobicity: two faces of water. Nature (London) 417, 491-493.
38. Lum, K., Chandler, D., & Weeks, J. D. (1999). Hydrophobicity at small and large length scales. J. Phys. Chem. B 103, 4570-4577.
39. Lee, B. (1994). Relation between volume correction and the standard state. Biophys. Chem. 51, 263-269.
40. Huang, D. M. & Chandler, D. (2000). Temperature and length scale dependence of hydrophobic effects and their possible implications for protein folding. Proc. Natl Acad. Sci. USA 97, 8324-8327.
41. Southall, N. T. & Dill, K. A. (2000). The mechanism of hydrophobic solvation depends on solute radius. J. Phys. Chem. B 104, 1326-1331.
42. Pohorille, A. & Pratt, L. R. (1990). Cavities in molecular liquids and the theory of hydrophobic solubility. J. Am. Chem. Soc. 112, 5066-5074.
43. Baldwin, R. L. (1986). Temperature dependence of the hydrophobic interaction in protein folding. Proc. Natl Acad. Sci. USA 83, 8069-8072.
44. Gill, S. J., Dec, S. F., Olofsson, G., & Wadsö, I. (1985). Anomalous heat capacity of hydrophobic solvation. J. Phys. Chem. 89, 3758-3761.
45. Pauling, L. (1960). The Nature of the Chemical Bond, 3rd edn, pp. 468-472. Cornell University Press, Ithaca, NY.
46. Lazaridis, T. (2001). Solvent size versus cohesive energy as the origin of hydrophobicity. Acc. Chem. Res. 34, 931-937.
47. Stellner, K. L., Tucker, E. E., & Christian, S. D. (1983). Thermodynamic properties of the benzenephenol dimer in dilute aqueous solution. J. Sol. Chem. 12, 307-313.
48. Raschke, T. M., Tsai, J., & Levitt, M. (2001). Quantification of the hydrophobic interaction by simulations of the aggregation of small hydrophobic solutes in water. Proc. Natl Acad. Sci. USA 98, 5965-5969.
49. Rank, J. A. & Baker, D. (1997). A desolvation barrier to cluster formation may contribute to the ratelimiting step in protein folding. Protein Sci. 6, 347-354.
50. Richards, F. M. (1977). Areas, volumes. packing and protein structure. Annu. Rev. Biophys. Bioeng. 6, 151-176.
51. Gill, S. J., Nichols, N. F., & Wadsö, I. (1976). Calorimetric determination of enthalpies of solution of slightly soluble liquids. II. Enthalpy of solution of some hydrocarbons in water and their use in establishing the temperature dependence of their solubilities. J. Chem. Thermodynam. 8, 445-452.
52. Edsall, J. T. (1935). Apparent molal heat capacities of amino acids and other organic compounds. J. Am. Chem. Soc. 57, 1506-1507.
53. Garde, S., Hummer, G., García, A., Paulaitis, M. E., & Pratt, L. R. (1996). Origin of entropy convergence in hydrophobic hydration and protein folding. Phys. Rev. Lett. 77, 4966-4968.
54. Graziano, G. & Lee, B.-K. (2003). Entropy convergence in hydrophobic hydration: a scaled particle theory analysis. Biophys. Chem. 105, 241-250.
55. Privalov, P. L. (1979). Stability of proteins: small globular proteins. Adv. Protein Chem. 33, 167-241.
56. Robertson, A. D. & Murphy, K. P. (1997). Protein structure and the energetics of protein stability. Chem. Rev. 97, 1251-1267.
57. Schellman, J. A. (1997). Temperature, stability and the hydrophobic interaction. Biophys. J. 73, 2960-2964.
58. Pace, C. N. (1992). Contribution of the hydrophobic effect to globular protein stability. J. Mol. Biol. 226, 29-35.
59. Eriksson, A. E., Baase, W. A., Zhang, X.-J. et al. (1992). Response of a protein structure to cavity-creating mutations and its relation to the hydrophobic effect. Science 255, 178-183.
60. Livingstone, J. R., Spolar, R. S., & Record, M. T. (1991). Contribution to the thermodynamics of protein folding from the reduction in water-accessible nonpolar surface area. Biochemistry 30, 4237-4244.
61. Makhatadze, G. I. & Privalov, P. L. (1993). Contribution of hydration to protein folding. I. The enthalpy of hydration. J. Mol. Biol. 232, 639-659.
62. Gómez, J., Hilser, V. J., Xie, Dong, & Freire, E. (1995). The heat capacity of proteins. Proteins Struct. Funct. Genet. 22, 404-412.
63. Richardson, J. M. & Makhatadze, G. I. (2003). Temperature dependence of the thermodynamics of the helixcoil transition. J. Mol. Biol., 335, 1029-1037.
64. Kauzmann, W. (1987). Thermodynamics of unfolding. Nature (London) 325, 763-764.
65. Hummer, G., Garde, S., García, A., Paulaitis, M. E., & Pratt, L. R. (1998). The pressure dependence of hydrophobic interactions is consistent with the observed pressure denaturation of proteins. Proc. Natl Acad. Sci. USA 95, 1552-1555.
66. Akasaka, K. (2003). Highly fluctuating protein structures revealed by variablepressure nuclear magnetic resonance. Biochemistry 42, 10875-10885.
67. Ooi, T. & Oobatake, M. (1988). Effects of hydrated water on protein unfolding. J. Biochem. (Tokyo) 103, 114-120.
68. Oobatake, M. & Ooi, T. (1992). Hydration and heat stability effects on protein unfolding. Prog. Biophys. Mol. Biol. 59, 237-284.
69. Simonson, T. & Brünger, A. T. (1994). Solvation free energies estimated from macroscopic continuum theory: an accuracy assessment. J. Phys. Chem. 98, 4683-4694.
70. Chen, J., Lu, Z., Sakon, J., & Stites, W. E. (2000). Increasing the thermostability of staphylococcal nuclease: implications for the origin of protein thermostability. J. Mol. Biol. 303, 125-130.
71. Havranek, J. J. & Harbury, P. B. (2003). Automated design of specificity in molecular recognition. Nature Struct. Biol. 10, 45-52.
72. Nicholls, A., Sharp, K. A., & Honig, B. (1991). Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins Struct. Funct. Genet. 11, 281-296.
73. Klapper, M. H. (1971). On the nature of the protein interior. Biochim. Biophys. Acta 229, 557-566.
74. Harpaz, Y., Gerstein, M., & Chothia, C. (1994). Volume changes on protein folding. Structure 2, 641-659.
75. Chen, J. & Stites, W. E. (2001). Packing is a key selection factor in the evolution of protein hydrophobic cores. Biochemistry 40, 15280-15289.
76. Varadarajan, R., Connelly, P. R., Sturtevant, J. M., & Richards, F. M. (1992). Heat capacity changes for protein-peptide interactions in the ribonuclease S system. Biochemistry 31, 1421-1426.
77. Ratnaparkhi, G. S. & Varadarajan, R. (2000). Thermodynamic and structural studies of cavity formation in proteins suggest that loss of packing interactions rather than the hydrophobic effect dominates the observed energetics. Biochemistry 39, 12365-12374.
78. Zhou, H. & Zhou, Y. (2002). Stability scale and atomic solvation parameters extracted from 1023 mutation experiments. Proteins Struct. Funct. Genet. 49, 483-492.
79. Zhou, H. & Zhou, Y. (2003). Quantifying the effect of burial of amino acid residues on protein stability. Proteins Struct. Funct. Genet. 54, 315-322.
80. Schellman, J. A. (1955). The thermodynamics of urea solutions and the heat of formation of the peptide hydrogen bond. C.R. Trav. Lab. Carlsberg, Sér. Chim. 29, 223-229.
81. Klotz, I. M. & Franzen, J. S. (1962). Hydrogen bonds between model peptide groups in solution. J. Am. Chem. Soc. 84, 3461-3466.
82. Susi, H., Timasheff, S. N., & Ard, J. S. (1964). Near infrared investigation of interamide hydrogen bonding in aqueous solution. J. Biol. Chem. 239, 3051-3054.
83. Epand, R. M. & Scheraga, H. A. (1968). The influence of long-range interactions on the structure of myoglobin. Biochemistry 7, 2864-2872.
84. Taniuchi, H. & Anfinsen, C. B. (1969). An experimental approach to the study of the folding of staphylococcal nuclease. J. Biol. Chem. 244, 3864-3875.
85. Klee, W. A. (1968). Studies on the conformation of ribonuclease Speptide. Biochemistry 7, 2731-2736.
86. Brown, J. E. & Klee, W. A. (1971). Helix-coil transition of the isolated amino-terminus of ribonuclease. Biochemistry 10, 470-476.
87. Bierzynski, A., Kim, P. S., & Baldwin, R. L. (1982). A salt bridge stabilizes the helix formed by the isolated C-peptide of RNase A. Proc. Natl Acad. Sci. USA 79, 2470-2474.
88. Baldwin, R. L. (1995). a-Helix formation by peptides of defined sequence. Biophys. Chem. 55, 127-135.
89. Muñoz, V. & Serrano, L. (1994). Elucidating the folding problem of helical peptides using emprical parameters. Nature Struct. Biol. 1, 399-409.
90. Aurora, R. & Rose, G. D. (1998). Helix capping. Protein Sci. 7, 21-38.
91. Marqusee, M., Robbins, V. H., & Baldwin, R. L. (1989). Unusually stable helix formation in short alanine-based peptides. Proc. Natl Acad. Sci. USA 86, 5286-5290.
92. Rohl, C. A., Chakrabartty, A., & Baldwin, R. L. (1996). Helix propagation and N-cap propensities of the amino acids measured in alaninebased peptides in 40 volume percent trifluoroethanol. Protein Sci. 5, 2623-2637.
93. Dyson, H. J., Cross, K. J., Houghten, R. A., Wilson, I. A., Wright, P. E., & Lerner, R. A. (1985). The immunodominant site of a synthetic immunogen has a conformational preference in water for a type-II reverse turn. Nature (London) 318, 480-483.
94. Dyson, H. J., Rance, M., Houghten, R. A., Lerner, R. A., & Wright, P. E. (1988). Folding of immunogenic peptide fragments of proteins in water solution. I. Sequence requirements for the formation of a reverse turn. J. Mol. Biol. 201, 161-200.
95. Blanco, F. J., Rivas, G., & Serrano, L. (1995). A short linear peptide that folds into a stable native b-hairpin in aqueous solution. Nature Struct. Biol. 1, 584-590.
96. Lifson, S., Hagler, A. T., & Dauber, P. (1979). Consistent force field studies of hydrogen-bonded crystals. 1. Carboxylic acids, amides, and the CbO• • •Ha hydrogen bonds. J. Am. Chem. Soc. 101, 5111-5121.
97. Wolfenden, R. (1978). Interaction of the peptide bond with solvent water: a vapor phase analysis. Biochemistry 17, 201-204.
98. Wolfenden, R., Andersson, L., Cullis, P. M., & Southgate, C. C. B. (1981). Affinities of amino acid side chains for solvent water. Biochemistry 20, 849-855.
99. Sitkoff, D., Sharp, K. A., & Honig, B. (1994). Accurate calculation of hydration free energies using macroscopic solvent models. J. Phys. Chem. 98, 1978-1988.
100. Avbelj, F., Luo, P., & Baldwin, R. L. (2000). Energetics of the interaction between water and the helical peptide group and its role in determining helix propensities. Proc. Natl Acad. Sci. USA 97, 10786-10791.
101. Eisenberg, D. & McLachlan, A. D. (1986). Solvation energy in protein folding and binding. Nature (London) 319, 199-203.
102. Dunitz, J. D. (1994). The entropic cost of bound water in crystals and biomolecules. Science 264, 670.
103. Rashin, A. A. & Honig, B. (1985). Reevaluation of the Born model of ion hydration. J. Phys. Chem. 89, 5588-5593.
104. Fersht, A. R., Shi, J.-P., Knill-Jones, J. et al. (1985). Hydrogen bonding and biological specificity analysed by protein engineering. Nature (London) 314, 235-238.
105. Fersht, A. R. (1987). The hydrogen bond in molecular recognition. Trends Biochem. Sci. 12, 301-304.
106. Baldwin, R. L. (2003). In search of the energetic role of peptide H-bonds. J. Biol. Chem. 278, 17581-17588.
107. Mitchell, J. B. O. & Price, S. L. (1991). On the relative strengths of amide• • •amide and amide• • •water hydrogen bonds. Chem. Phys. Lett. 180, 517-523.
108. Galison, P. (1997). Image and Logic, p. 68, University of Chicago Press, Chicago.
109. Born, M. (1920). Volumen und Hydrationswärme der Ionen. Z. Physik 1, 45-48.
110. Grossfield, A., Ren, P., & Ponder, J. W. (2003). Ion solvation thermodynamics from simulation with a polarizable force field. J. Am. Chem. Soc. 125, 15671-15682.
111. Kirkwood, J. G. & Westheimer, F. H. (1938). The electrostatic influence of substituents on the dissociation constants of organic acids. J. Chem. Phys. 6, 506-512.
112. Rajasekaran, E., Jayaram, B., & Honig, B. (1994). Electrostatic interactions in aliphatic dicarboxylic acids: a computational route to the determination of pK shifts. J. Am. Chem. Soc. 116, 8238-8240.
113. Florian, J. & Warshel, A. (1997). Langevin dipoles model for ab initio calculations of chemical processes in solution: parameterization and application to hydration free energies of neutral and ionic solutes and conformational analysis in aqueous solution. J. Phys. Chem. B 101, 5583-5595.
114. Brant, D. A. & Flory, P. J. (1965). The configuration of random polypeptide chains. II. Theory. J. Am. Chem. Soc. 87, 2791-2800.
115. Brant, D. A. & Flory, P. J. (1965). The role of dipole interactions in determining polypeptide configurations. J. Am. Chem. Soc. 87, 663-664.
116. Avbelj, F. & Moult, J. (1995). Role of electrostatic screening in determining protein main chain conformational preferences. Biochemistry 34, 755-764.
117. Avbelj, F. & Fele, L. (1998). Role of main-chain electrostatics, hydrophobic effect and side-chain conformational entropy in determining the secondary structure of proteins. J. Mol. Biol. 279, 665-684.
118. Avbelj, F. (2000). Amino acid conformational preferences and solvation of polar backbone atoms in peptides and proteins. J. Mol. Biol. 300, 1335-1359.
119. Creamer, T. P. & Rose, G. D. (1994). a-Helix-forming propensities in peptides and proteins. Proteins Struct. Funct. Genet. 19, 85-97.
120. Luo, P. & Baldwin, R. L. (1999). Interaction between water and polar groups of the helix backbone: an important determinant of helix propensities. Proc. Natl Acad. Sci. USA 96, 4930-4935.
121. Avbelj, F. & Baldwin, R. L. (2002). Role of backbone solvation in determining thermodynamic b propensities of the amino acids. Proc. Natl Acad. Sci. USA 99, 1309-1313.
122. Ben-Tal, N., Sitkoff, D., Topol, I. A., Yang, A.-S., Burt, S. K., & Honig, B. (1997). Free energy of amide hydrogen bond formation in vacuum, in water, and in liquid alkane solution. J. Phys. Chem. B 101, 450-457.
123. Lopez, M. M., Chin, D.-H., Baldwin, R. L., & Makhatadze, G. I. (2002). The enthalpy of the alanine peptide helix measured by isothermal titration calorimetry using metal-binding to induce helix formation. Proc. Natl Acad. Sci. USA 99, 1298-1302.
124. Goch, G., Maciejczyk, Oleszczuk, M., Stachowiak, D., Malicka, J., & Bierzynski, A. (2003). Experimental investigation of initial steps of helix propagation in model peptides. Biochemistry 42, 6840-6847.
125. Myers, J. K. & Pace, C. N. (1996). Hydrogen bonding stabilizes globular proteins. Biophys. J. 71, 2033-2039.
126. Jayasinghe, S., Hristova, K., & White, S. H. (2001). Energetics, stability and prediction of transmembrane helices. J. Mol. Biol. 312, 927-934.
127. Loladze, V. V., Ermolenko, D. N., & Makhatadze, G. I. (2002). Thermodynamic consequences of burial of polar and nonpolar amino acid residues in the protein interior. J. Mol. Biol. 320, 343-357.
128. Loladze, V. V., Ermolenko, D. N., & Makhatadze, G. I. (2001). Heat capacity changes upon burial of polar and nonpolar groups in proteins. Protein Sci. 10, 1343-1352.