On the nature of cavities on protein surfaces: Application to the identification of drug-binding sites

Proteins: Structure, Function and Genetics

Volumn 63, Issue 4, 2006, Pages 892-906

  Nayal, Murad ^a   Honig, Barry ^a,b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b Department of Biochemistry and Molecular Biophysics ^*  (United States)

Author keywords

Molecular recognition; Molecular surface patches; Protein function; Protein surface cavities; Protein drug interactions; Protein drug binding sites

Indexed keywords

ACCURACY; ANALYTICAL ERROR; ARTICLE; CRYSTALLIZATION; DRUG BINDING SITE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN STRUCTURE; SURFACE PROPERTY; TECHNIQUE;

BINDING SITES; DRUG DESIGN; HUMANS; MODELS, MOLECULAR; PHARMACEUTICAL PREPARATIONS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEINS;

EID: 33646757492     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.20897     Document Type: Article

References (89)

1. Sheinerman FB, Honig B. On the role of electrostatic interactions in the design of protein-protein interfaces. J Mol Biol 2002;318:161-177.
2. Laskowski RA, Luscombe NM, Swindells MB, Thornton JM. Protein clefts in molecular recognition and function. Protein Sci 1996;5:2438-2452.
3. Jones S, Thornton JM. Principles of protein-protein interactions. Proc Natl Acad Sci USA 1996;93:13-20.
4. Jones S, Thornton JM. Prediction of protein-protein interaction sites using patch analysis. J Mol Biol 1997;272:133-143.
5. Jones S, Thornton JM. Analysis of protein-protein interaction sites using surface patches. J Mol Biol 1997;272:121-132.
6. Keil M, Exner TE, Brickmann J. Pattern recognition strategies for molecular surfaces: III. Binding site prediction with a neural network. J Comput Chem 2004;25:779-789.
7. Lo Conte L, Chothia C, Janin J. The atomic structure of protein-protein recognition sites. J Mol Biol 1999;285:2177-2198.
8. Lijnzaad P, Berendsen HJ, Argos P. Hydrophobic patches on the surfaces of protein structures. Proteins 1996;25:389-397.
9. Neuvirth H, Raz R, Schreiber G. ProMate: a structure based prediction program to identify the location of protein-protein binding sites. J Mol Biol 2004;338:181-199.
10. Stawiski EW, Gregoret LM, Mandel-Gutfreund Y. Annotating nucleic acid-binding function based on protein structure. J Mol Biol 2003;326:1065-1079.
11. Pettit FK, Bowie JU. Protein surface roughness and small molecular binding sites. J Mol Biol 1999;285:1377-1382.
12. Peters KP, Fauck J, Frommel C. The automatic search for ligand binding sites in proteins of known three-dimensional structure using only geometric criteria. J Mol Biol 1996;256:201-213.
13. Aqvist J, Tapia O. Surface fractality as a guide for studying protein-protein interactions. J Mol Graph. 1987;5:30-34.
14. Ofran Y, Rost B. Analysing six types of protein-protein interfaces. J Mol Biol 2003;325:377-387.
15. Lewis RA. Clefts and binding sites in protein receptors. Methods Enzymol 1991;202:126-156.
16. Liang J, Edelsbrunner H, Woodward C. Anatomy of protein pockets and cavities: measurement of binding site geometry and implications for ligand design. Protein Sci 1998;7:1884-1897.
17. Nicholls A, Sharp KA, Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 1991;11:281-296.
18. Honig B, Nicholls A. Classical electrostatics in biology and chemistry. Science 1995;268:1144-1149.
19. Fernandez-Recio J, Totrov M, Skorodumov C, Abagyan R. Optimal docking area: a new method for predicting protein-protein interaction sites. Proteins 2005;58:134-143.
20. Preissner R, Goede A, Frommel C. Dictionary of interfaces in proteins (DIP): data bank of complementary molecular surface patches. J Mol Biol 1998;280:535-550.
21. Cosgrove DA, Bayada DM, Johnson AP. A novel method of aligning molecules by local surface shape similarity. J Comput Aided Mol Des 2000;14:573-591.
22. Schmitt S, Kuhn D, Klebe G. A new method to detect related function among proteins independent of sequence and fold homology. J Mol Biol 2002;323:387-406.
23. Ferre F, Ausiello G, Zanzoni A, Helmer-Citterich M. SURFACE: a database of protein surface regions for functional annotation. Nucleic Acids Res 2004;32(Database issue):D240-D244.
24. Glaser F, Pupko T, Paz I, Bell RE, Bechor-Shental D, Martz E, Ben-Tal N. ConSurf: identification of functional regions in proteins by surface-mapping of phylogenetic information. Bioinformatics 2003;19:163-164.
25. Pupko T, Bell RE, Mayrose I, Glaser F, Ben-Tal N. Rate4Site: an algorithmic tool for the identification of functional regions in proteins by surface mapping of evolutionary determinants within their homologues. Bioinformatics 2002;18(Suppl 1):S71-S77.
26. Lichtarge O, Bourne HR, Cohen FE. An evolutionary trace method defines binding surfaces common to protein families. J Mol Biol 1996;257:342-358.
27. Nayal M, Hitz BC, Honig B. GRASS: a server for the graphical representation and analysis of structures. Protein Sci 1999;8:676-679.
28. Young L, Jernigan RL, Covell DG. A role for surface hydrophobicity in protein-protein recognition. Protein Sci 1994;3:717-729.
29. Exner TE, Keil M, Brickmann J. Pattern recognition strategies for molecular surfaces: I. Pattern generation using fuzzy set theory. J Comput Chem 2002;23:1176-1187.
30. Stahl M, Taroni C, Schneider G. Mapping of protein surface cavities and prediction of enzyme class by a self-organizing neural network. Protein Eng 2000;13:83-88.
31. Di L, Kerns EH. Profiling drug-like properties in discovery research. Curr Opin Chem Biol 2003;7:402-408.
32. Oprea TI. Current trends in lead discovery: are we looking for the appropriate properties? J Comput Aided Mol Des 2002;16:325-334.
33. Lipinski CA, Lombardo F, Dominy BW, Feeney PJ. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 2001;46:3-26.
34. Voorintholt R, Kosters MT, Vegter G, Vriend G, Hol WG. A very fast program for visualizing protein surfaces, channels and cavities. J Mol Graph 1989;7:243-245.
35. Ho CM, Marshall GR. Cavity search: an algorithm for the isolation and display of cavity-like binding regions. J Comput Aided Mol Des 1990;4:337-354.
36. Levitt DG, Banaszak LJ. POCKET: a computer graphics method for identifying and displaying protein cavities and their surrounding amino acids. J Mol Graph 1992;10:229-234.
37. Hendlich M, Rippmann F, Barnickel G. LIGSITE: automatic and efficient detection of potential small molecule-binding sites in proteins. J Mol Graph Model 1997;15:359-363, 389.
38. Kleywegt GJ, Jones TA. Detection, delineation, measurement and display of cavities in macromolecular structures. Acta Crystallogr D Biol Crystallogr 1994;50:178-185.
39. Delaney JS. Finding and filling protein cavities using cellular logic operations. J Mol Graph 1992;10:174-177, 163.
40. Masuya M, Doi J. Detection and geometric modeling of molecular surfaces and cavities using digital mathematical morphological operations. J Mol Graph 1995;13:331-336.
41. Kuntz I, Blaney J, Oatley S, Langridge R, Ferrin T. A geometric approach to macromolecule-ligand interactions. J Mol Biol 1982;161:269-288.
42. Laskowski RA. SURFNET: a program for visualizing molecular surfaces, cavities, and intermolecular interactions. J Mol Graph 1995;13:323-330, 307-328.
43. Brady GP Jr, Stouten PF. Fast prediction and visualization of protein binding pockets with PASS. J Comput Aided Mol Des 2000;14:383-401.
44. Lewis RA. Determination of clefts in receptor structures. J Comput Aided Mol Des 1989;3:133-147.
45. Connolly ML. Measurement of protein surface shape by solid angles. J Mol Graphics 1986;4:3-6.
46. Lewis M, Rees DC. Fractal surfaces of proteins. Science 1985;230:1163-1165.
47. Wodak SJ, Janin J. Computer analysis of protein-protein interaction. J Mol Biol 1978;124:323-342.
48. Fanning DW, Smith JA, Rose GD. Molecular cartography of globular proteins with application to antigenic sites. Biopolymers 1986;25:863-883.
49. Badel-Chagnon A, Nessi J, Buffat L, Hazout S. "Iso-depth contour map" of a molecular surface. J Mol Graph 1994;12:162-168,193.
50. Voronoi G. New applications of continuous parameters of the theory of quadratic forms. Journal für die Reine und Angewandte Mathematik 1907;133:97-178.
51. Rogers CA. Packing and covering. Cambridge UK: Cambridge University Press; 1964.
52. Edelsbrunner H, Mucke EP. Three dimensional alpha shapes. ACM Trans Graph 1994;13:43-72.
53. Edelsbrunner H. The union of balls and its dual shape. Discrete Comput Geom 1995;13:415-440.
54. Edelsbrunner H, Facello M, Liang J. On the definition and the construction of pockets in macromolecules. Discrete Appl Math 1998;88:83-102.
55. Ruppert J, Welch W, Jain AN. Automatic identification and representation of protein binding sites for molecular docking. Protein Sci 1997;6:524-533.
56. An J, Totrov M, Abagyan R. Pocketome via comprehensive identification and classification of ligand-binding envelopes. Mol Cell Proteomics 2005;4:752-761.
57. Laurie AT, Jackson RM. Q-SiteFinder: an energy-based method for the prediction of protein-ligand binding sites. Bioinformatics 2005;21:1908-1916.
58. Nissink JW, Murray C, Hartshorn M, Verdonk ML, Cole JC, Taylor R. A new test set for validating predictions of protein-ligand interaction. Proteins 2002;49:457-471.
59. Eisenhaber F, Argos P. Hydrophobic regions on protein surfaces: definition based on hydration shell structure and a quick method for their computation. Protein Eng 1996;9:1121-1133.
60. Heiden W, Brickmann J. Segmentation of protein surfaces using fuzzy logic. J Mol Graph 1994;12:106-115.
61. Klapper I, Hagstrom R, Fine R, Sharp K, Honig B. Focussing of electric fields in the active site of CuZn Superoxide dismutase: effects of ionic strength and amino acid modification. Proteins 1986;1:47-59.
62. Bate P, Warwicker J. Enzyme/non-enzyme discrimination and prediction of enzyme active site location using charge-based methods. J Mol Biol 2004;340:263-276.
63. Nayeem A, Krystek S, Jr., Stouch T. An assessment of protein-ligand binding site polarizability. Biopolymers 2003;70:201-211.
64. Alkorta I, Perez JJ, Villar HO. Molecular polarization maps as a tool for studies of intermolecular interactions and chemical reactivity. J Mol Graph 1994;12:3-13.
65. Ondrechen MJ, Clifton JG, Ringe D. THEMATICS: a simple computational predictor of enzyme function from structure. Proc Natl Acad Sci USA 2001;98:12473-12478.
66. Shehadi IA, Yang H, Ondrechen MJ. Future directions in protein function prediction. Mol Biol Rep 2002;29:329-335.
67. Duncan B, Olson A. Approximation and characterization of molecular surfaces. Biopolymers 1993;33:219-229.
68. Liang S, Zhang J, Zhang S, Guo H. Prediction of the interaction site on the surface of an isolated protein structure by analysis of side chain energy scores. Proteins 2004;57:548-557.
69. Elcock AH. Prediction of functionally important residues based solely on the computed energetics of protein structure. J Mol Biol 2001;312:885-896.
70. Korolev S, Nayal M, Barnes WM, Di Cera E, Waksman G. Crystal structure of the large fragment of Thermus aquaticus DNA polymerase I at 2.5-Å resolution: structural basis for thermostability. Proc Natl Acad Sci USA 1995;92:9264-9268.
71. Breiman L. Bagging predictors. Machine Learning 1996;24:123-140.
72. Breiman L. Random Forests. Machine Learning 2001;45:5-32.
73. Perola E, Walters WP, Charifson PS. A detailed comparison of current docking and scoring methods on systems of pharmaceutical relevance. Proteins 2004;56:235-249.
74. Cover TM, Thomas JA. Elements of information theory. New York: Wiley-Interscience; 1991.
75. Iversen LF, Andersen HS, Moller KB, Olsen OH, Peters GH, Branner S, Mortensen SB, Hansen TK, Lau J, Ge Y, Holsworth DD, Newman MJ, Hundahl Moller NP. Steric hindrance as a basis for structure-based design of selective inhibitors of protein-tyrosine phosphatases. Biochemistry 2001;40:14812-14820.
76. Smith GM, Alexander RS, Christianson DW, McKeever BM, Ponticello GS, Springer JP, Randall WC, Baldwin JJ, Habecker CN. Positions of His-64 and a bound water in human carbonic anhydrase II upon binding three structurally related inhibitors. Protein Sci 1994;3:118-125.
77. Maignan S, Guilloteau JP, Pouzieux S, Choi-Sledeski YM, Becker MR, Klein SI, Ewing WR, Pauls HW, Spada AP, Mikol V. Crystal structures of human factor Xa complexed with potent inhibitors. J Med Chem 2000;43:3226-3232.
78. DePristo MA, de Bakker PI, Blundell TL. Heterogeneity and inaccuracy in protein structures solved by X-ray crystallography. Structure (Camb) 2004;12:831-838.
79. Burnham KP, Anderson DR. Model selection and multimodel inference: a practical information-theoretic approach. 2nd ed. New York: Springer-Verlag; 2002.
80. Henry CM. Structure-based drug design. Chem Eng News 2001;79:69-74.
81. Cochran AG. Antagonists of protein-protein interactions. Chem Biol 2000;7:R85-R94.
82. Koenderink JJ, Solid shape. Cambridge, MA: MIT Press; 1990.
83. Diamond R. Real-space refinement of the structure of hen eggwhite lysozyme. J Mol Biol 1974;82:371-391.
84. Eisenberg D, Wesson L. Atomic solvation parameters applied to molecular dynamics of proteins in solution. Protein Sci 1992;1:227-235.
85. Radzicka A, Wolfenden R. Comparing the polarities of the amino acids: Side-chain distribution coefficients between the vapor phase, cyclohexane, 1-octanol, and neutral aqueous solution. Biochemistry 1988;27:1644-1670.
86. Sharp KA, Honig B. Applications of the finite difference Poisson-Boltzmann method to proteins and nucleic acids. In: Sarma RH, Sarma MH, editors. DNA protein complexes and proteins: Vol. 2. Structure and methods. Adenine Press; 1990. p 211.
87. Kabsch W, Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 1983;22:2577-2637.
88. Pickett SD, Sternberg MJ. Empirical scale of side-chain conformational entropy in protein folding. J Mol Biol 1993;231:825-839.
89. Vajda S, Weng Z, Rosenfeld R, DeLisi C. Effect of conformational flexibility and solvation on receptor-ligand binding free energies. Biochemistry 1994;33:13977-13988.