Effects of salt bridges on protein structure and design

Protein Science

Volumn 7, Issue 9, 1998, Pages 1898-1914

  Sindelar, Charles V ^a   Hendsch, Zachary S ^a   Tidor, Bruce ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Electrostatics; Ion pairs; Lattice models; Protein design; Protein electrostatics; Protein stability; Salt bridge; Specificity

Indexed keywords

SODIUM CHLORIDE;

ARTICLE; CHEMICAL BOND; ELECTRICITY; ENERGY; HYDROPHOBICITY; MUTATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE;

EID: 0031659672     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1002/pro.5560070906     Document Type: Article

References (69)

1. Abola EE, Bernstein FC, Bryant SH, Koetzle TF, Weng J. 1987. Protein Data Bank. In: Allen FH, Bergerhoff G, Sievers R, eds. Crystallographic data-bases: Information content, software systems, scientific applications. Bonn, Germany: Data Commission of the International Union of Crystallography. pp 107-132.
2. Anderson DE, Becktel WJ, Dahlquist FW. 1990. pH-induced denaturation of proteins: A single salt bridge contributes 3-5 kcal/mol to the free energy of folding of T4 lysozyme. Biochemistry 29:2403-2408.
3. Baker EN, Hubbard RE. 1984. Hydrogen bonding in globular proteins. Progr Biophys Mol Biol 44:91-179.
4. Bernstein FC, Koetzle TF, Williams GJB, Meyer EF Jr, Brice MD, Rodgers JR, Kennard O, Shimanouchi T, Tasumi M. 1977. The Protein Data Bank: A computer-based archival file for macromolecular structures. J Mol Biol 112:535-542.
5. Chan HS, Dill KA. 1990. The effects of internal constraints on the configurations of chain molecules. J Chem Phys 92:3118-3135.
6. Chan HS, Dill KA. 1996. Comparing folding codes for proteins and polymers. Proteins Struct Funct Genet 24:335-344.
7. Clarage JB, Romo T, Andrews BK, Pettitt BM, Phillips GN Jr. 1995. A sampling problem in molecular dynamics simulations of macromolecules. Proc Natl Acad Sci USA 92:3288-3292.
8. Dahiyat BI, Mayo SL. 1997. De novo protein design: Fully automated sequence selection. Science 278:82-87.
9. Dao-pin S, Sauer U, Nicholson H, Matthews BW. 1991. Contributions of engineered surface salt bridges to the stability of T4 lysozyme determined by directed mutagenesis. Biochemistry 30:7142-7153.
10. Dill KA, Bromberg S, Yue K, Fiebig KM, Yee DP, Thomas PD, Chan HS. 1995. Principles of protein folding: A perspective from simple exact models. Protein Sci 4:561-602.
11. - group on helix stability. Proteins Struct Funct Genet 5:1-7.
12. Fersht AR. 1971. Conformational equilibria and the salt bridge in chymotrypsin. Cold Spring Harbor Symp Quant Biol 36:71-73.
13. Fersht AR. 1972. Conformational equilibria in α-and δ-chymotrypsin. The energetics and importance of the salt bridge. J Mol Biol 64:497-509.
14. Fersht AR, Shi J-P, Knill-Jones J, Lowe DM, Wilkinson AJ, Blow DM, Brick P, Carter P, Waye MMY, Winter G. 1985. Hydrogen bonding and biological specificity analysed by protein engineering. Nature (London) 314:235-238.
15. Finkelstein AV, Janin J. 1989. The price of lost freedom: Entropy of bimolecular complex formation. Protein Eng 3:1-3.
16. Gilson MK, Given JA, Bush BL, McCammon JA. 1997. The statisticalthermodynamic basis for computation of binding affinities: A critical review. Biophys J 72:1047-1069.
17. Harbury PB, Zhang T, Kim PS, Alber T. 1993. A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 262:1401-1407.
18. Hendsch ZS, Tidor B. 1994. Do salt bridges stabilize proteins? A continuum electrostatic analysis. Protein Sci 3:211-226.
19. Hinds DA, Levitt M. 1992. A lattice model for protein structure prediction at low resolution. Proc Natl Acad Sci USA 89:2536-2540.
20. Hol WGJ. 1985. The role of the α-helix dipole in protein function and structure. Prog Biophys Molec Biol 45:149-195.
21. Hol WGJ, van Duijnen PT, Berendsen HJC. 1978. The α-helix dipole and the properties of proteins. Nature (London) 273:443-446.
22. Honig B, Cohen FE. 1996. Adding backbone to protein folding: Why proteins are polypeptides. Fold Design 1:R17-R20.
23. Horovitz A, Serrano L, Avron B, Bycroft M, Fersht AR. 1990. Strength and co-operativity of contributions of surface salt bridges to protein stability. J Mol Biol 216:1031-1044.
24. Huyghues-Despointes BMP, Scholtz JM, Baldwin RL. 1993. Helical peptides with three pairs of Asp-Arg and Glu-Arg residues in different orientations and spacings. Protein Sci 2:80-85.
25. Irikura KK, Tidor B, Brooks BR, Karplus M. 1985. Transition from B to Z DNA: Contribution of internal fluctuations to the configurational entropy difference. Science 229:571-572.
26. Kametekar S, Schiffer JM, Xiong H, Babik JM, Hecht MH. 1993. Protein design by binary patterning of polar and nonpolar amino acids. Science 262:1680-1685.
27. Karplus M, Shakhnovich E. 1992. Protein folding: Theoretical studies of thermodynamics and dynamics. In: Creighton T, ed. Protein folding. New York: Freeman, pp 127-195.
28. Kauzmann W. 1959. Some factors in the interpretation of protein denaturation. Adv Protein Chem 14:1-63.
29. Kellis JT Jr, Nyberg K, Šali D, Fersht AR. 1988. Contribution of hydrophobic interactions to protein stability. Nature (London) 333:784-786.
30. Kirkpatrick S, Gelatt CD Jr, Vecchi MP. 1983. Optimization by simulated annealing. Science 220:671-680.
31. Lattman EE, Rose GD. 1993. Protein folding: What's the question? Proc Natl Acad Sci USA 90:439-441.
32. Li H, Helling R, Tang C, Wingreen N. 1996. Emergence of preferred structures in a simple model of protein folding. Science 273:666-669.
33. Lumb KJ, Kim PS. 1995. A buried polar interaction imparts structural uniqueness in a designed heterodimeric coiled coil. Biochemistry 34:8642-8648.
34. Lyu PC, Gans PJ, Kallenbach NR. 1992. Energetic contribution of solvent-exposed ion pairs to alpha-helix structure. J Mol Biol 223:343-350.
35. Lyu PC, Wemmer DE, Zhou HX, Pinker RJ, Kallenbach NR. 1993. Capping interactions in isolated α helices: Position-dependent substitution effects and structure of a serine-capped peptide helix. Biochemistry 32:421-425.
36. + salt bridges in short peptides of de novo design. Proc Natl Acad Sci USA 84:8898-8902.
37. Matsumura M, Becktel WJ, Matthews BW. 1988. Hydrophobic stabilization in T4 lysozyme determined directly by multiple substitutions of Ile 3. Nature (London) 334:406-410.
38. Matthews BW, Nicholson H, Becktel WJ. 1987. Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding. Proc Natl Acad Sci USA 84:6663-6667.
39. Merutka G, Stellwagen E. 1991. Effect of amino acid ion pairs on peptide helicity. Biochemistry 30:1591-1594.
40. Miyazawa S, Jemigan RL. 1985. Estimation of effective interresidue contact energies from protein crystal structures: Quasi-chemical approximation. Macromolecules 18:534-552.
41. Munson M, O'Brien R, Sturtevant JM, Regan L. 1994. Redesigning the hydrophobic core of a four-helix-bundle protein. Protein Sci 3:2015-2022.
42. Nicholls A, Sharp KA, Honig B. 1991. Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins Struct Funct Genet 11:281-296.
43. Nicholson H, Anderson DE, Dao-pin S, Matthews BW. 1991. Analysis of the interaction between charged side chains and the α-helix dipole using designed thermostable mutants of phage T4 lysozyme. Biochemistry 30:9816-9828.
44. Nicholson H, Becktel WJ, Matthews BW. 1988. Enhanced protein thermostability from designed mutations that interact with α-helix dipoles. Nature (London) 336:651-656.
45. Pace CN. 1992. Contribution of the hydrophobic effect to globular protein stability. J Mol Biol 226:29-35.
46. Page MI, Jencks WP. 1971. Entropic contributions to rate accelerations in enzymic and intramolecular reactions and the chelate effect. Proc Natl Acad Sci USA 68:1678-1683.
47. Paul CH. 1982. Building models of globular protein molecules from their amino acid sequences. I. Theory. J Mol Biol 155:53-62.
48. Pickett SD, Sternberg MJE. 1993. Empirical scale of side chain conformational entropy in protein folding. J Mol Biol 237:825-839.
49. Presta LG, Rose GD. 1988. Helix signals in proteins. Science 240:1632-1641.
50. a of His 18 in barnase. J Mol Biol 260:99-110.
51. Richardson JS, Richardson DC. 1988. Amino acid preferences for specific locations at the ends of α helices. Science 240:1648-1652.
52. Šali D, Bycroft M, Fersht AR. 1988. Stabilization of protein structure by interaction of α-helix dipole with a charged side chain. Nature (London) 335:740-743.
53. Serrano L, Fersht AR. 1989. Capping and α-helix stability. Nature (London) 342:296-299.
54. Serrano L, Horovitz A, Avron B, Bycroft M, Fersht AR. 1990. Estimating the contribution of engineered surface electrostatic interactions to protein stability by using double-mutant cycles. Biochemistry 29:9343-9352.
55. Sheridan RP, Levy RM, Salemme FR. 1982. α-Helix dipole model and electrostatic stabilization of 4-α-helical proteins. Proc Natl Acad Sci USA 79:4545-4549.
56. Shoemaker KR, Kim PS, York EJ, Stewart JM, Baldwin RL. 1987. Tests of the helix dipole model for stabilization of α-helices. Nature (London) 326:563-567.
57. Skolnick J, Kolinski A. 1989. Computer simulations of globular protein folding and tertiary structure. Annu Rev Phys Chem 40:207-235.
58. Straatsma TP, McCammon JA. 1989. Treatment of rotational isomers in free energy evaluations. Analysis of the evaluation of free energy differences by molecular dynamics simulations of systems with rotational isomeric states. J Chem Phys 90:3300-3304.
59. Tanford C, De PK, Taggart VG. 1960. The role of the α-helix in the structure of proteins. Optical rotatory dispersion of β-lactoglobulin. J Am Chem Soc 82:6028-6034.
60. Tidor B. 1994. Helix-capping interaction in λ Cro protein: A free energy simulation analysis. Proteins Struct Funct Genet 19:310-323.
61. Tidor B, Karplus M. 1993. The contribution of cross-links to protein stability: A normal mode analysis of the configurational entropy of the native state. Proteins Struct Fund Genet 15:71-79.
62. Tidor B, Karplus M. 1994. The contribution of vibrational entropy to molecular association. The dimerization of insulin. J Mol Biol 238:405-414.
63. Tobias DJ, Brooks CL III, Fleischman SH. 1989. Conformational flexibility in free energy simulations. Chem Phys Lett 156:256-260.
64. Unger R, Moult J. 1993. Genetic algorithms for protein folding simulations. J Mol Biol 231:75-81.
65. Waldburger CD, Schildbach JF, Sauer RT. 1995. Are buried salt bridges important for protein stability and conformational specificity? Nature Struct Biol 2:122-128.
66. Wang L, O'Connell T, Tropsha A, Hermans J. 1996. Energetic decomposition of the α-helix-coil equilibrium of a dynamic model system. Biopolymers 39:479-489.
67. Wimey WC, Gawrisch K, Creamer TP, White SH. 1996. Direct measurement of salt bridge solvation energies using a peptide model system: Implications for protein stability. Proc Natl Acad Sci USA 93:2985-2990.
68. Yang A-S, Honig B. 1995. Free energy determinants of secondary structure formation: I. α-Helices. J Mol Biol 252:351-365.
69. Yang A-S, Sharp KA, Honig B. 1992. Analysis of the heat capacity dependence of protein folding. J Mol Biol 227:889-900.