Development and validation of a genetic algorithm for flexible docking

Journal of Molecular Biology

Volumn 267, Issue 3, 1997, Pages 727-748

  Jones, Gareth ^a   Willett, Peter ^a   Glen, Robert C ^b,e   Leach, Andrew R ^c   Taylor, Robin ^d  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b Wellcome Found Res Laboratories   (United Kingdom)

^c GLAXOSMITHKLINE   (United Kingdom)

^d CAMBRIDGE CRYSTALLOGRAPHIC DATA CENTRE   (United Kingdom)

^e TRIPOS INC   (United States)

Author keywords

Docking problem; Genetic algorithm; Molecular recognition; Protein ligand docking

Indexed keywords

PROTEIN; WATER;

ALGORITHM; ARTICLE; COMPUTER PROGRAM; DATA BASE; DRUG DESIGN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 0031552362     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0897     Document Type: Article

References (87)

1. Allen F. H., Davies J. E., Galloy J. J., Johnson O., Kennard O., Macrae C. F., Mitchell E. M., Mitchell G. F., Smith J. M., Watson D. G. The development of versions 3 and 4 of the Cambridge Structural Database system. J. Chem. Inform. Comput. Sci. 31:1991;187-204.
2. 3substructures: reaction pathway for the protonation of nitrogen. Acta Crystallog. sect. B. 51:1995;1068-1081.
3. Ajay, Murcko M. A. Computational methods to predict binding free energy in ligand-receptor complexes. J. Med. Chem. 38:1995;4953-4968.
4. Badger J., Minor I., Oliveira M. A., Smith T. J., Rossmann M. G. Structural analysis of antiviral agents that interact with the capsid of human rhinoviruses. Proteins: Struct. Funct. Genet. 6:1989;1-19.
5. Bernstein F. C., Koetzle T. F., Williams G. J. B., Meyer F., Bryce M. D., Rogers J. R., Kennard O., Shikanouchi T., Tasumi M. The Protein Data Bank: a computer-based archival file for macromolecular structures. J. Mol. Biol. 112:1977;535-542.
6. Blaney J. M., Dixon J. S. A good ligand is hard to find: automated docking methods. Perspect. Drug Discov. Res. 1:1993;301-319.
7. Böcskei Z., Groom C. R., Flower D. R., Wright C. E., Phillips S. E. V., Cavaggioni A., Findlay J. B. C., North A. C. T. Pheromone binding to two rodent urinary proteins revealed by X-ray crystallography. Nature. 360:1992;186-188.
8. Bolin J. T., Filman D. J., Matthews D. A., Hamlin R. C., Kraut J. Crystal structures of Escherichia coli and Lactobacillus casei dihydrofolate reductase refined at 1.7 Å resolution. J. Biol. Chem. 257:1982;13650-13662.
9. Borah B., Chen C. W., Egan W., Miller M., Wlodawer A., Cohen J. S. Nuclear magnetic resonance and neutron-diffraction studies of the complex of ribonuclease-A with uridine vanadate, a transition-state analog. Biochemistry. 24:1985;2058-2067.
10. Brandsetter H., Turk D., Hoeffken H. E., Grosse D., Sturzebecher J., Martin P. D., Edwards B. F .P., Bode W. Refined 2.3 Angstrom X-ray crystal structure of bovine thrombin complexes formed with the benzamidine and arginine-based thrombin inhibitoes NAPDP 4-TAPAP and MQPA: a starting point for improving antithrombotics. J. Mol. Biol. 226:1992;1085-1099.
11. Brodmeier T., Pretsch E. Application of genetic algorithms in molecular modelling. J. Comput. Chem. 15:1994;588-595.
12. Brünger A. T., Leahy D. J., Hynes T. R., Fox R. O. 2.9 Å Resolution Structure of an anti-dinitrophenyl-spin-label monoclonal antibody fab fragment with bound hapten. J. Mol. Biol. 221:1991;239-256.
13. Bystroff C., Kraut J. Crystal structure of unliganded Escherichia coli dihydrofolate reductase-ligand-induced conformational changes and cooperativity in binding. Biochemistry. 30:1991;2227-2239.
14. Chen C. C. H., Rahil J., Pratt R. F., Herzberg O. Structure of a phosphonate inhibited β-lactamase. An analog of the tetrahedral transition state/intermediate of β-lactam hydrolysis. J. Mol. Biol. 234:1993;165-178.
15. Clark D. E., Jones G., Willett P., Kenny P. W., Glen R. C. Pharmacophoric pattern matching in files of three-dimensional structures: comparison of conformational-searching algorithms for flexible searching. J. Chem. Inform. Comput. Sci. 34:1994;197-206.
16. Clark M., Cramer R. D., Van Opdenbosch N. Validation of the general-purpose TRIPOS 5.2 force field. J. Comput. Chem. 10:1989;982-1012.
17. Connolly M. J. Analytical molecular surface calculation. J. Appl. Crystallog. 16:1983;548-558.
18. Cooper J. B., Quail W., Frazao C., Foundling S. I., Blundell T. L. X-ray crystalographic analysis of inhibition of endothiapepsin by cyclohexyl renin inhibitors. Biochemistry. 31:1992;8142-8150.
19. Dandekar T., Argos P. Identifying the tertiary fold of small proteins with different topologies from sequence and secondary structure using the genetic algorithm and extended criteria specific for strand regions. J. Mol. Biol. 256:1996;645-660.
20. Davis L. D. Handbook of Genetic Algorithms. 1991;Van Nostrand Rheinhold, New York.
21. Delaney J. S. Finding and filling protein cavities using cellular logic operations. J. Mol. Graph. 10:1992;174-177.
22. Diederichs K., Schultz G. E. The refined structure of the complex between adenylate kynase from beef-heart mitochondrial matrix and its substrate AMP at 1.85 Å resolution. J. Mol. Biol. 217:1991;541-549.
23. Dreyer G. B., Lambert D. M., Meek T. D., Carr T. J., Tomaszek T. A., Fernandez A. V., Bartus H., Cacciavillani E., Hassel A. M., Minnich M., Petteway S. R., Metcalf B. W. Hydroxyethylene isostere inhibitors of human immunodeficiency virus-I protease: structure-activity analysis using enzyme kinetics, X-ray crystallography, and infected T-cell assays. Biochemistry. 31:1992;6646-6639.
24. Arg106→Glnwith bound oleate at 1.74 Å resolution. J. Biol. Chem. 268:1993;26375-26385.
25. Edmundson A. B., Harris D. L., Fan Z. C., Guddat L. W., Schley B. T., Hanson B. L., Tribbick G., Geysen H. M. Principles and pitfalls in designing site-directed peptide ligands. Proteins: Struct. Funct. Genet. 16:1993;246-267.
26. Filman D. J., Syed R., Chow M., Macadam A. J., Minor P. D., Hogle J. M. Structural factors that control transitions and serotype specificity in type 3 poliovirus. EMBO J. 8:1989;1567-1579.
27. Fraternali F., van Gunsteren W. F. An efficient mean solvation force model for use in molecular dynamics simulations of proteins in aqueous solution. J. Mol. Biol. 256:1996;939-948.
28. Gehlhaar D. K., Verkhivker G. M., Rejto P. A., Sherman C. J., Fogel D. B., Fogel L. J., Freer S. T. Molecular recognition of the inhibitor AG-1343 by HIV-1 protease: conformationally flexible docking by evolutionary programming. Chem. Biol. 2:1995;317-324.
29. Ghosh D., Erman M., Wawrzak Z., Duax W. L., Pangborn W. Mechanism of inhibition of 3α,20β-hydroxysteroid dehydrogenase by a licorice-derived steroidal inhibitor. Structure. 2:1994;973-980.
30. Glen R. C. A fast empirical method for the calculation of molecular polarizability. J. Comput. Aid. Mol. Des. 8:1994;457-466.
31. Glusker J. P. Structural Aspects of metal liganding to functional groups in proteins. Advan. Protein Chem. 42:1991;1-76.
32. Goldberg D. E. Genetic Algorithms in Search Opimization and Machine Learning. 1989;Addison-Wesley, Reading.
33. Goldberg D. E., Deb K. An investigation of niche and species formation in genetic function optimisation. Proceedings of the Third International Conference on Genetic Algorithms and their Applications. 1989;Morgan Kaufmann, San Mateo.
34. Goodsell D. S., Olson A. J. Automated docking of substrates to proteins by simulated annealing. Proteins: Struct. Funct. Genet. 8:1990;195-202.
35. Goto H., Osawa E. Corner flapping: a simple and fast algorithm for exhaustive generation of ring conformations. J. Am. Chem. Soc. 111:1989;8950-8951.
36. Hamilton J. A., Steinrauf L. K., Braden B. C., Leipnieks J., Benson M. D., Holmgren G., Sandgren O., Steen L. The X-ray crystal structure refinements of normal human transthyretin and the amyloidogenic Val30→Met variant to 1.7 Å resolution. J. Biol. Chem. 268:1993;2416-2424.
37. Harel M., Schalk I., Ehret-Sabattier L., Bouet F., Goeldner M., Hirth C., Axelsen P., Silman I., Sussman J. Quaternary ligand binding to aromatic residues in the active site gorge of acetylcholinesterase. Proc. Natl Acad. Sci., USA. 90:1993;9031-9035.
38. Hayes I. C., Stone A. J. An intermolecular perturbation theory for the region of moderate overlap. Mol. Phys. 53:1984;83-105.
39. Herron J. N., He X. M., Mason M. L., Voss E. W., Edmundson A. B. Three-dimensional structure of a fluorescein FAB complex crystallized in 2-methyl-2,4-pentanediol. Proteins: Struct. Funct. Genet. 5:1989;271-280.
40. Herzberg O. Refined crystal structure of β-lactamase from Staphylococcus aureus PC1 at 2.0 Å resolution. J. Mol. Biol. 217:1991;701-719.
41. Hirschfelder J. O., Curtiss C. F., Bird R. B. Molecular Theory of Gases and Liquids. 1964;John Wiley, New York.
42. Hinze J., Jaffe H. H. Electronegativity. I. Orbital electronegativity of neutral atoms. J. Am. Chem. Soc. 84:1962;540-546.
43. Ho C. M. W., Marshall G. R. Cavity search: an algorithm for the isolation and display of cavity like binding regions. J. Comput. Aid. Mol. Des. 4:1990;337-354.
44. Holland J. H. Adaptation in Natural and Artificial Systems. 1992;MIT Press, Cambridge.
45. Holt D. A., Luengo J. I., Yamashita D. S., Oh H. J., Konialian A. L., Yen H. K., Rozamus L. E., Brandt M., Bossard M. J., Levy M. A., Eggleston D. S., Liang J., Schultz L. W., Stout T. J., Clardy J. Design, synthesis, and kenetic evaluation of high-affinity FKBP ligands and the x-ray crystal structures of their complexes with FKBP12. J. Am. Chem. Soc. 115:1993;9925-9938.
46. James N. M. G., Sielecki A. R., Moult J. Crystallographic analysis of a pepstatin analogue binding to the aspartyl proteinase penicillopepsin at 1.8 Å resolution. Hruby V. J., Rich D. H. Peptides: Structure and Function, Proceedings of the Eighth American Peptide Symposium. 1983;Pierce Chemical Company, Rockford.
47. Jedrzejas M. J., Singh S., Brouillette W. J., Laver W. G., Air G. M., Luo M. Structures of aromatic inhibitors of influenza virus neuraminidase. Biochemistry. 34:1995;3144-3151.
48. Jeffrey P. D., Strong R. K., Sieker L. C., Chang C. Y. Y., Campbell R. L., Petsko G. A., Haber E., Margolies M. N., Sheriff S. 26-10 FAB-digoxin complex: affinity and specificity due to surface complementarity. Proc. Natl Acad. Sci., USA. 90:1993;10310-10314.
49. Jones G., Willett P. Docking small molecule ligands into active sites. Curr. Opin. Biotechnology. 6:1995;652-656.
50. Jones G., Willett P., Glen R. C. Molecular recognition of receptor sites using a genetic algorithm with a description of desolvation. J. Mol. Biol. 254:1995a;43-53.
51. Jones G., Willett P., Glen R. C. A genetic algorithm for flexible molecular overlay and pharmacophore elucidation. J. Comput. Aid. Mol. Des. 9:1995b;532-549.
52. Judson R. S., Jaeger E. P., Treasurywala A. M. A genetic algorithm method for docking flexible molecules. J. Mol. Struct. 308:1994;191-206.
53. Judson R. S., Tan Y. T., Mori E., Melius C., Jaeger E. P., Treasurywala A. M., Mathiowetz A. Docking flexible molecules: a case study of three proteins. J. Comput. Chem. 16:1995;1405-1419.
54. Klebe G. Mapping common molecular fragments in crystal structures to explore conformation and configuration space under the conditions of a molecular environment. J. Mol. Struct. 308:1994;53-89.
55. Kuntz I. D., Blaney J. M., Oatley S. J., Langridge R., Ferrin T. E. A geometric approach to macromolecule-ligand interactions. J. Mol. Biol. 161:1982;269-288.
56. LaLonde J. M., Bernlohr D. A., Banaszak L. J. X-ray crystallographic studies of adipocyte lipid-binding protein complexed with palmitate and hexadecanesulfonic acid. Properties of cavity binding sites. Biochemistry. 33:1994;4885-4895.
57. Landro J. A., Gerlt J. A., Kozarich J. W. The role of lysine 166 in the mechanism of mandelate racemase from Pseudomonas putida: mechanistic and crystallographic evidence for stereospecific alkylation by (R)-α-phenylglycidate. Biochemisty. 33:1994;635-643.
58. Lauble M., Kennedy M. C., Beinert H., Stout C. D. Crystal structures of aconitase with trans-aconitate and nitrocitrate bound. J. Mol. Biol. 237:1994;437-451.
59. Leslie A. G. W. Refined crystal structure of type III chloramphenicol acetyltransferase at 1.75 Å resolution. J. Mol. Biol. 213:1990;167-186.
60. Lisgarten J. N., Gupta V., Maes D., Wyns L., Zegers I., Palmer R. A, Dealwis C. G., Aguilar C. F., Hemmings A. M. Structure of the crystalline complex of cytidylic acid (2′-CMP) with ribonuclease at 1.6 Angstrom resolution-conservation of solvent sites in RNase-A high resolution structures. Acta Crystallog. sect. D. 49:1993;541-547.
61. Lommerse J. P. M., Stone A. J., Taylor R., Allen F. H. The nature and geometry of intermolecular interactions between halogens and oxygen or nitrogen. J. Am. Chem. Soc. 118:1996;3108-3116.
62. Matthews D. A., Bolin J. T., Burridge J. M., Filman D. J., Volz K. W., Kaufman B. T., Beddell C. R., Champness J. N., Stammers D. K., Kraut J. Refined crystal structures of Escherichia coli and chicken liver dihydrofolate reductase containing bound trimethoprim. J. Biol. Chem. 260:1985;381-391.
63. Miller M. D., Kearsley S. K., Underwood D. J., Sheridan R. P. FLOG: a system to select "quasi flexible" ligands complementary to a receptor of known three-dimensional structure. J. Comput. Aided Mol. Des. 8:1994;153-174.
64. Mitchell J. B. O., Price S. L. On the relative strengths of amide.amide and amide.water hydrogens bonds. Chem. Phys. Letters. 180:1991;517-523.
65. Murthy K. H. M., Winborne E. L., Minnich M. D., Culp J. S., Debouck C. The crystal structures at 2.2- Å resolution of hydroxyethylene-based inhibitors bound to human immunodeficiency virus type 1 protease show that the inhibitors are present in two distinct orientations. J. Biol. Chem. 32:1992;22770-22778.
66. Nicklaus M. C., Wang S. M., Driscoll J. S., Milne G. W. A. Conformational changes of small molecules binding to proteins. Bioorg. Med. Chem. 3:1995;411-428.
67. 1homologue) complexed with a guanyly-3′,5′-cytidine analogue. Biochemistry. 32:1993;11825-11837.
68. Oshiro C. M., Kuntz I. D., Dixon J. S. Flexible ligand docking using a genetic algorithm. J. Comput. Aided Mol. Des. 9:1995;113-130.
69. Payne A. W. R., Glen R. C. Molecular recognition using a binary genetic search algorithm. J. Mol. Graph. 11:1993;74-91.
70. Padlan E. A., Cohen G. H., Davies D. R. On the specificity of antibody 3-antigen interactions: phosphocholine binding to MCPC603 and the correlation of three-dimensional structure and sequence data. Ann. Immunol. (Paris). C136:1985;271-276.
71. Perry K. M., Carreras C. W., Chang L. C., Santi D. V., Stroud R. M. Structures of thymidylate synthase with a C-terminal deletion: role of the C-terminus in alignment of 2′-deoxyuridine 5′-monophosphate and 5,10-methylenetetrahydrofolate. Biochemistry. 32:1993;7116-7125.
72. Peters K. P., Fauck J., Frömmel C. The automatic search for ligand binding sites in proteins of known three-dimensional structure using only geometric criteria. J. Mol. Biol. 256:1996;201-213.
73. Rarey M., Kramer B., Lengauer T., Klebe G. Predicting receptor-ligand interactions by an incremental construction algorithm. J. Mol. Biol. 261:1996;470-489.
74. Smith G. D., Dodson G. G. The structure of a rhombohedral R6 insulin hexamer that binds phenol. Biopolymers. 32:1992;441-445.
75. Starkweather T., Whitley D., Mathias K. Optimisation using distributed genetic algorithms. Schwefel H. P., Manner R. Parallel Problem Solving from Nature. 1990;Springer-Verlag, Berlin.
76. Stewart J. J. P. MOPAC User Manual Version 6.0. 1992;Quantum Chemical Program Exchange, Department of Chemistry, University of Indiana, Bloomington.
77. Still W. C., Tempczyk A., Hawley R. C., Hendrickson T. Semianalytical treatment of solvation for molecular mechanics and dynamics. J. Am. Chem. Soc. 112:1990;6127-6129.
78. Stoddard B. L., Bruhnke J., Porter N., Ringe D., Petsko G. A. Structure and activity of two photoreversible cinnamates bound to chymotrypsin. Biochemistry. 29:1990;4871-4879.
79. Sun S. Reduced representation model of protein structure prediction: statistical potential and genetic algorithms. Protein Sci. 2:1993;762-785.
80. Surles M. C., Richardson J. S., Richardson D. C., Brooks F. P. Sculpting proteins interactively: continual energy minimization embedded in a graphical modeling system. Protein Sci. 3:1994;198-210.
81. Tanese R. Distributed genetic algorithms. Schaffer D. Proceedings of the Third International Conference on Genetic Algorithms and their Applications. 1989;Morgan Kaufmann, San Mateo.
82. Teplyakov A., Obolova G., Wilson K. S., Ishii K., Kaji H., Samejima T., Kuranova I. Crystal-structure of inorganic pyrophosphatase from Thermus thermophilus. Protein Sci. 3:1994;1098-1107.
83. Tong L., Pav S., Mui S., Lamarre D., Yoakim C., Beaulieu P., Anderson P. C. Crystal structures of HIV-2 protease in complex with inhibitors containing the hydroxyethylamine dipeptide isostere. Structure. 3:1995;33-40.
84. Van Duyne G. D., Standaert R. F., Karplus P. A., Schreiber S. L., Clardy J. Atomic structures of human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol. 229:1993;105-124.
85. Wang J., Smerdon S. J., Jäger J., Kohlstaedt L. A., Rice P. A., Friedman J. M., Steitz T. A. Structural basis of asymmetry in the human immunodeficiency virus type 1 reverse transcriptase heterodimer. Proc. Natl Acad. Sci. USA. 91:1994;7242-7246.
86. Zhang A., Nanni R. G., Li T., Arnold G. F., Oren D. A., Jacobo-Molina A., Williams R. L., Kamer G., Rubenstein D. A., Li Y., Rozhon E., Cox S., Buontempo P., O'Connell J., Schwartz J., Miller G., Bauer B., Versace R., Pinto P., Ganguly A., Girijavallabhan V., Arnold E. Structure determination of antiviral compound SCH 38057 complexed with human rhinovirus 14. J. Mol. Biol. 230:1993;857-867.
87. Zhou G. W., Gou J., Huang W., Fletterick R. J., Scanlan T. S. Crystal structure of a catalytic antibody with a serine protease active site. Science. 265:1994;1059-1064.