Predicting protein stability changes upon mutation using database-derived potentials: Solvent accessibility determines the importance of local versus non-local interactions along the sequence

Journal of Molecular Biology

Volumn 272, Issue 2, 1997, Pages 276-290

  Gilis, Dimitri ^a   Rooman, Marianne ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Folding free energies; Mean force potentials; Protein stability; Single site mutations

Indexed keywords

MUTANT PROTEIN;

ACCURACY; AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; DATA BASE; HYDROPHOBICITY; PREDICTION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; SOLVATION; THERMODYNAMICS; THERMOSTABILITY; TORSION;

EID: 0030777760     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1237     Document Type: Article

References (57)

1. Alard, P. 1991, Calculs de surface et d'énergie dans le domaine des macromolécules, PhD thesis, Université Libre de Bruxelles.
2. Alber T., Daopin S., Wilson K., Wozniak J. A., Cook S. P., Matthews B. W. Contributions of hydrogen bonds of Thr157 to the thermodynamic stability of phage T4 lysozyme. Nature. 330:1987;41-46.
3. Basch P. A., Singh U. C., Landridge R., Kollman P. A. Free energy calculations by computer simulation. Science. 236:1987;564-568.
4. Bernstein F. C., Koetzle T. F., Williams G. J. B., Meywe E. F. Jr, Brice M. D., Rodgers J. R., Kennard O., Shimanoushi T., Tasumi M. The Protein Data Bank: a computer-based archival file for macromolecular structures. J. Mol. Biol. 112:1977;535-542.
5. Bryant S. H., Lawrence C. E. An empirical energy function for threading protein sequence through the folding motif. Proteins: Struct. Funct. Genet. 16:1993;92-112.
6. Casari G., Sippl M. Structure-derived hydrophobic potential. Hydrophobic potential derived from X-ray structures of globular proteins is able to identify native folds. J. Mol. Biol. 224:1992;725-732.
7. Daopin S., Baase W. A., Matthews B. W. A mutant T4 lysozyme (Val 131→Ala) designed to increase thermostability by the reduction of strain within an α-helix. Proteins: Struct. Funct. Genet. 7:1990;198-204.
8. Daopin S., Alber T., Baase W. A., Wozniak J. A., Matthews B. W. Structural and thermodynamic analysis of the packing of two α-helices in bacteriophage T4 lysozyme. J. Mol. Biol. 221:1991;647-667.
9. Eriksson A. E., Baase W. A., Zhang X.-J., Heinz D. W., Blaber M., Baldwin E. P., Matthews B. W. Response of a protein structure to cavity-creating mutations and its relation to the hydrophobic effect. Science. 255:1992;178-183.
10. Fersht A. R. Optimization of rates of protein folding: the nucleation-condensation mechanism and its implications. Proc. Natl Acad. Sci. USA. 92:1995;1086-10873.
11. Fersht A. R., Matouschek A., Serrano L. The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathways of protein folding. J. Mol. Biol. 224:1992;771-782.
12. Fisher R. A. Statistical Methods for Research Workers. 1958;Oliver and Boyd Ltd, Edinburgh.
13. Gilis D., Rooman M. Stability changes upon mutation of solvent-accessible residues in proteins evaluated by database-derived potentials. J. Mol. Biol. 257:1996;1112-1126.
14. Gō N., Taketomi H. Respective roles of short- and long-range interactions in protein folding. Proc. Natl Acad. Sci. USA. 75:1978;559-563.
15. Govindarajan S., Goldstein R. Optimal local propensities for model proteins. Proteins: Struct. Funct. Genet. 22:1995;413-418.
16. Itzhaki L. S., Otzen D. E., Fersht A. R. The structure of the transition state for folding of chymotrypsin inhibitor 2 analysed by protein engineering methods: evidence for a nucleation-condensation mechanism for protein folding. J. Mol. Biol. 254:1995;260-288.
17. Jackson S. E., Fersht A. R. contribution of residues in the reactive site loop of chymotrypsin inhibitor 2 to protein stability and activity. Biochemistry. 33:1994;13880-13887.
18. Jackson S. E., Moracci M., elMasry N., Johnson C. M., Fersht A. R. Effect of cavity-creating mutations in the hydrophobic core of chymotrypsin inhinbitor 2. Biochemistry. 32:1993;11259-11269.
19. Kabsch W., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 22:1983;2577-2637.
20. Kay M. S., Baldwin R. L. Packing interactions in the apomyoglobin folding intermediate. Nature Struct. Biol. 3:1996;439-445.
21. Kellis J. T. Jr, Nyberg K., Sali D., Fersht A. R. Contribution of hydrophobic interactions to protein stability. Nature. 333:1988;784-786.
22. Kellis J. T., Nyberg K., Fersht A. R. Energetics of complementary side-chain packing in a protein hydrophobic core. Biochemistry. 28:1989;4914-4922.
23. Kocher J.-P. A., Rooman M. J., Wodak S. J. Factors influencing the ability of knowledge-based potentials to identify native sequence-structure matches. J. Mol. Biol. 235:1994;1598-1613.
24. Kocher J.-P., Prévost M., Wodak S. J., Lee B. Properties of the protein matrix revealed by the free energy of cavity formation. Structure. 4:1996;1517-1529.
25. Koehl P., Delarue M. Polar and nonpolar atomic environments in the protein core: implications for folding and binding. Proteins: Struct. Funct. Genet. 20:1994;264-278.
26. Lee C. Predicting protein mutant energetics by self-consistent ensemble optimization. J. Mol. Biol. 236:1994;918-939.
27. Lee C., Levitt M. Accurate prediction of the stability and activity effects on site-directed mutagenesis on a protein core. Nature. 352:1991;448-451.
28. Levitt M. A simplified representation of protein conformations for rapid simulation of protein folding. J. Mol. Biol. 104:1976;59-107.
29. Matouschek A., Kellis J. T. Jr, Serrano L., Fersht A. R. Mapping the transition state and pathway of protein folding by protein engineering. Nature. 340:1989;122-126.
30. Matsumura M., Becktel W. J., Matthews B. W. Hydrophobic stabilization in T4 lysozyme determined directly by multiple substitutions of Ile 3. Nature. 334:1988;406-410.
31. Matthews B. W., Nicholson H., Becktel W. J. Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding. Proc. Natl Acad. Sci. USA. 84:1987;6663-6667.
32. 13C NMR study of the effects of mutation on the tryptophan dynamics in chymotrypsin inhibitor 2: correlations with structure and stability. Biochemistry. 32:1993;657-662.
33. Miyazawa S., Jernigan R. L. Protein stability for single substitution mutants and the extent of local compactness in the denatured state. Protein Eng. 7:1994;1209-1220.
34. Muñoz V., Serrano L. Intrinsic secondary structure propensities of the amino-acids, using statistical φ-ψ matrices: comparison with experimental data. Proteins: Struct. Funct. Genet. 20:1994;301-311.
35. Muñoz V., Serrano L. Local versus nonlocal interactions in protein folding and stability - an experimentalist's point of view. Folding Design. 1:1996;R71-R77.
36. Otzen D. E., Fersht A. R. Side-chain determinants of β-sheet stability. Biochemistry. 34:1995;5718-5724.
37. Pohl F. M. Empirical protein energy maps. Nature. 237:1971;277-279.
38. Ramachandran G., Sasisekharan V. Conformation of peptides and proteins. Advan. Protein Chem. 23:1968;283-437.
39. Rooman M. J., Wodak S. J. Are database-derived potentials valid for scoring both forward and inverted protein folding? Protein Eng. 8:1995;849-858.
40. Rooman M. J., Kocher J.-P. A., Wodak S. J. Prediction of protein backbone conformation based on 7 structure assignments: influence of local interactions. J. Mol. Biol. 221:1991;961-979.
41. Rooman M. J., Kocher J.-P. A., Wodak S. J. Extracting information on folding from the amino acid sequence: accurate predictions for protein regions with stable conformation in absence of tertiary interactions. Biochemistry. 31:1992;10226-10238.
42. Rose G. D., Geselowitz A. R., Lesser G. J., Lee R. H., Zehfus M. H. Hydrophobicity of amino acid residues in globular proteins. Science. 29:1985;834-838.
43. Serrano L., Fersht A. R. Capping and α-helix stability. Nature. 342:1989;296-299.
44. Serrano L., Kellis J. T. Jr, Cann P., Matouschek A., Fersht A. R. The folding of an enzyme. II. Substructure of barnase and the contribution of different interactions to protein stability. J. Mol. Biol. 224:1992a;783-804.
45. Serrano L., Sancho J., Hirshberg M., Fersht A. R. α-Helix stability in proteins. I. Empirical correlations concerning substitution of side-chains at the N and C-cap and the replacement of alanine by glycine or serine at solvent-exposed surfaces. J. Mol. Biol. 227:1992b;544-559.
46. Shakhnovich E., Abkevich V., Ptitsyn O. Conserved residues and the mechanism of protein folding. Nature. 379:1996;96-98.
47. Shih P., Kirsch J. F. Design and structural analysis of an engineered thermostable chicken lysozyme. Protein Sci. 4:1995;2063-2072.
48. Shih P., Holland D. B., Kirsch J. F. Thermal stability determinants of chicken egg-white lysozyme core mutants: hydrophobicity, packing volume, and conserved buried water molecules. Protein Sci. 4:1995;2050-2062.
49. Shoichet B. K., Baase W. A., Kuroki R., Matthews B. W. A relationship between protein stability and protein function. Proc. Natl Acad. Sci. USA. 92:1995;452-456.
50. Sippl M. J. Knowledge-based potentials for proteins. Curr. Opin. Struct. Biol. 5:1995;229-235.
51. Takano K., Ogasahara K., Kaneda H., Yamagata Y., Fujii S., Kanaya E., Kikuchi M., Oobatake M., Yutani K. Contribution of hydrophobic residues to the stability of human lysozyme: calorimetric studies and X-ray structural analysis of the five isoleucine to valine mutants. J. Mol. Biol. 254:1995;62-76.
52. Tidor B., Karplus M. Simulation analysis of the stability mutant R96H of T4 lysozyme. Biochemistry. 30:1991;3217-3228.
53. Unger R., Moult J. Local interactions dominate folding in a simple protein model. J. Mol. Biol. 259:1996;988-994.
54. Wintjens R. T., Rooman M. J., Wodak S. J. Automatic classification and analysis of αα-turn motifs in proteins. J. Mol. Biol. 255:1996;235-253.
55. Yutani K., Ogasahara K., Tsujita T., Sugino Y. Dependence of conformational stability on hydrophobicity of the amino acid residue in a series of variant proteins substituted at a unique position of tryptophan synthase α subunit. Proc. Natl Acad. Sci. USA. 84:1987;4441-4444.
56. Zhang X.-J., Baase W. A., Matthews B. W. Multiple alanine replacements within α-helix 126-134 of T4 lysozyme have independent, additive effects on both structure and stability. Protein Sci. 1:1992;761-776.
57. Zhang X.-J., Baase W. A., Shoichet B. K., Wilson K. P., Matthews B. W. Enhancement of protein stability by the combination of point mutations in T4 lysozyme is additive. Protein Eng. 8:1995;1017-1022.