Receptor flexibility in small-molecule docking calculations

Wiley Interdisciplinary Reviews: Computational Molecular Science

Volumn 1, Issue 2, 2011, Pages 298-314

  Kokh, Daria B ^a   Wade, Rebecca C ^a   Wenzel, Wolfgang ^b  

^a HEIDELBERG INSTITUTE FOR THEORETICAL STUDIES   (Germany)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONAL CHANGE; CONFORMATIONAL SPACE; DOCKING CALCULATIONS; PROTEIN CONFORMATIONAL CHANGES; RECEPTOR FLEXIBILITY; RECEPTOR-LIGAND BINDING; REORGANIZATION ENERGIES; STRUCTURAL FLEXIBILITIES;

PROTEINS;

CONFORMATIONS;

EID: 80054807339     PISSN: 17590876     EISSN: 17590884     Source Type: Journal    
DOI: 10.1002/wcms.29     Document Type: Review

References (111)

1. Böhm H-J, Schneider G, eds. Virtual Screening or Bioactive Molecules. Weinheim, Germany: John Wiley & Sons; 2000.
2. Warren GL, Andrews CW, Capelli AM, Clarke B, LaLonde J, Lambert MH, Lindvall M, Semus SF, Senger S, Tedesco G, et al. A critical assessment of docking programs and scoring functions. J Med Chem 2006, 49:5912-5931.
3. Fischer E. Einfluss der konfiguration auf die wirkung der enzyme. Ber Dtsch Chem Ges 1894, 27:2985-2993.
4. Cozzini P, Kellogg GE, Spyrakis F, Abraham DJ, Costantino G, Emerson A, Fanelli F, Gohlke H, Kuhn LA, Morris GM, et al. Target flexibility: an emerging consideration in drug discovery and design. J Med Chem 2008, 51:6237-6255.
5. Totrov M, Abagyan R. Flexible ligand docking to multiple receptor conformations: a practical alternative. Curr Opin Struct Biol 2008, 18:178-184.
6. Mohan V, Gibbs AC, Cummings MD, Jaeger EP, DesJarlais R. Docking: successes and challenges. Curr Pharm Des 2005, 11:323-333.
7. Larsson P, Hess B, Lindahl E. Algorithm improvements for molecular dynamics simulations. WIREs Comput Mol Sci 2011, Accepted.
8. Alonso H, Bliznyuk AA, Gready JE. Combining docking and molecular dynamic simulations in drug design. Med Res Rev 2006, 26:531-568.
9. Verkhivker GM, Bouzada D, Gehlhaar DK, Rejto PA, Freer ST, Rose PW. Complexity and simplicity of ligand-macromolecule interactions: the energy landscape perspective. Curr Opin Struct Biol 2002, 12:197-203.
10. Hammes GG, Chang YC, Oas TG. Conformational selection or induced fit: a flux description of reaction mechanism. Proc Natl Acad Sci U S A 2009, 106:13737-13741.
11. Best B, Lindorff-Larsen K, DePristo MA, Vendruscolo M. Relation between native ensembles and experimental structures in proteins. Proc Natl Acad Sci U S A 2006, 103:10901-10906.
12. Boehr DD, Nussinov R, Wright PP. The role of dynamic conformational ensembles in biomolecular recognition. Nat Chem Biol 2009, 5:789-796.
13. Henzler-Wildman KA, Thai V, Lei M, Ott M, Wolf-Watz M, Fenn T, Pozharski E, Wilson M, Petsko G, Karplus M, et al. Intrinsic motions along an enzymatic reaction trajectory. Nature 2007, 450:838-844.
14. Zhang Q, Stelzer AC, Fisher CK, Al-Hashimi HM. Visualizing spatially correlated dynamics that directs RNA conformational transitions. Nature 2007, 450:1263-1267.
15. Schotte F, Lim M, Jackson TA, Smirnov AV, Soman J, Olson JS, Phillips GN Jr, Wulff M, Anfinrud PhA. Watching a protein as it functions with 150-ps time-resolved X-ray crystallography. Science 2003, 300:1944-1947.
16. Csermely P, Palotai R, Nussinov R. Induced fit, conformational selection and independent dynamic segments: an extended view of binding events. Trends Biochem Sci 2010, 35:539-546.
17. James LC, Tawfic DS. Structure and kinetics of a transient antibody binding intermediate reveal a kinetic discrimination mechanism in antigen recognition. Proc Natl Acad Sci U S A 2005, 102:12730-12735.
18. Boehr D, McElheny D, Dyson HJ, Wright PE. Millisecond timescale fluctuations in dihydrofolate reductase are exquisitely sensitive to the bound ligand. Proc Natl Acad Sci U S A 2010, 107:1373-1378.
19. Weikl TR, von Deuster C. Selected-fit versus induced-fit protein binding: kinetic differences and mutational analysis. Proteins 2009, 75:104-110.
20. James LC, Tawfic DS. Structure and kinetics of a transient antibody binding intermediate reveal a kinetic discrimination mechanism in antigen recognition. Proc Natl Acad Sci U S A 2005, 102:12730-12735.
21. Damm KL, Carlson HA. Exploring experimental sources of multiple protein conformations in structure-based drug design. J Am Chem Soc 2007, 129:8225-8235.
22. Sobolev V, Wade RC, Vrend G, Edelman M. Molecular docking using surface complementarity. Proteins 1996, 25:120-129.
23. Taylor RD, Jewsbury PJ, Essex JW. Flexible ligand and receptor docking with a continuum solvent model and soft-core energy function. J Comp Chem 2003, 24:1637-1656.
24. Ferrari AM, Wei BO, Costantion L, Shoichet BK. Soft docking and multiple receptor conformations in virtual screening. J Med Chem 2004, 47:5076-5084.
25. Mizutani MY, Takamatsu Y, Ichinose T, Nakamura K, Itai A. Effective handling of induced-fit motion in flexible docking. Proteins 2006, 63:878-891.
26. Kokh DB, Wenzel W. Flexible side chain models improve enrichment rates in in silico screening. J Med Chem 2008, 51:5919-5931.
27. Lorber DM, Shoichet BK. Flexible ligand docking using conformational ensembles. Protein Sci 1998, 7:938-950.
28. Sherman W, Day T, Jacobson MP, Friesner RA, Farid R. Novel procedure for modeling ligand/receptor induced fit effects. J Med Chem 2006, 49:534-553.
29. AutoDock 4.0, The Scripps Research Institute, La Jolla, CA; 2006.
30. Van Aalten DMF, De Groot BL, Findlay JBC, Berendsen HJC, Amadei A. A comparison of techniques for calculating protein essential dynamics. J Comput Chem 1997, 18:170-181.
31. Zacharias M. Rapid protein-ligand docking using soft modes from molecular dynamic simulations to account for protein deformability: binding of FK506 to FKBP. Proteins 2004, 54:759-767.
32. Brunne RM, Berndt KD, Guntert P, Wuthrich K, van Gunsteren WF. Structure and internal dynamics of the bovine pancreatic trypsin inhibitor in aqueous solution from long-time molecular dynamics simulations. Proteins 1995, 23:49-62.
33. Eyrisch S, Helms V. Transient pocket on protein surface involved in protein-protein interaction. J Med Chem 2007, 50:3457-3464.
34. Rueda M, Ferrer-Costa C, Meyer T, Perez A, Camps J, Hospital A, Gelpi JL, Orozco M. A consensus view of protein dynamics. Proc Natl Acad Sci U S A 2007, 104:796-801.
35. Miranker A, Karplus M. Functionality maps of binding sites: a multiple copy simultaneous search method. Proteins 1991, 11:29-34.
36. Sugita Y, Okamoto Y. Replica-exchange molecular dynamics method for protein folding. Chem Phys Lett 1999, 314:141-151.
37. Mangoni M, Roccatano D, Di Nola A. Docking of flexible ligands to flexible receptors in solution by molecular dynamics simulation. Proteins 1999, 35:153-162.
38. Nobuyuki O, Agard DA. Binding mode prediction for flexible ligand in a flexible pocket using multi-conformation simulated annealing pseudo crystallographic refinement. J Mol Biol 2001, 314:607-617.
39. Maragakis P, Lindorff-Larsen K, Eastwood MP, Dror RO, Klepeis JL, Arkin IT, Jensen MØ, Xu H, Trbovic N, Friesner RA, et al. Microsecond molecular dynamics simulations show effect of slow loop dynamics on backbone amide order parameters of proteins. J Phys Chem B 2008, 112:6155-6158.
40. Shaw DE, Maragakis P, Lindorff-Larsen K, Pian S, Dror RO, Eastwood MP, Ban JA, Jumpe JM, Salmon JK, Shan Y, et al. Atomic-level characterization of the structural dynamics of proteins. Science 2010, 330:341-346.
41. Freddolino P, Schulten K. Power play. Nature 2008, 45:240-243.
42. Floquet N, Marechal J-D, Badet-Denisot M, Robert CH, Dauchez M, Perahia D. Normal mode analysis as a prerequisite for drug design: application to matrix metalloproteinases inhibitors. FEBS Lett 2006, 580:5130-5136.
43. Cavasotto CN, Kovacs JA, Abagyan RA. Representing receptor flexibility in ligand docking through relevant normal modes. J Am Chem Soc 2005, 127:9632-9640.
44. May A, Zacharias M. Protein-ligand docking accounting for receptor side chain and global flexibility in normal modes; evaluation on kinase inhibitor cross docking. J Med Chem 2008, 51:3499-3506.
45. Lindahl E, Delarue M. Refinement of docking protein-ligand and protein-DNA structures using low frequency normal mode amplitude optimization. Nucleic Acids Res 2005, 33:4496-4506.
46. Seeliger D, Haas J, de Groot BL. Geometry-based sampling of conformational transitions in proteins. Structure 2007, 15:1482-1492.
47. de Groot BL, van Aalten DMF, Scheek RM, Amadei A, Vriend G, Berendsen HJC. Prediction of protein conformational freedom from distance constrains. Proteins 1997, 29:240-251.
48. Seeliger D, de Groot BL. Conformational transitions upon ligand binding: holo-structure prediction from apo conformations. PLoS Comput Biol 2010, 6:e1000634.
49. Meiler J, Baker D. ROSETTALIGAND: protein-small molecule docking with full side-chain flexibility. Proteins 2006, 65:538-548.
50. Cerqueira NMFSA, Bras NF, Fernandes PA, Ramos MJ. MADAMM: a multistaged docking with an automated molecular modeling protocol. Proteins 2009, 74:192-206.
51. Jacobson MP, Pincus DL, Rapp CS, Day TJF, Honig B, Shaw DE, Friesner RA. A hierarchical approach to all-atom protein loop prediction. Proteins 2004, 55:351-367.
52. Zhu K, Pincus DL, Zhao S, Friesner RA. Long loop prediction using the protein local optimization program. Proteins 2006, 65:438-452.
53. Dunbrack RL, Cohen FE. Bayesian statistical analysis of protein side-chain rotamer preferences. Protein Sci 1997, 6:1661-1681.
54. Wong S, Jacobson MP. Conformational selection in silico: loop latching motion and ligand binding in enzymes. Proteins 2008, 71:153-164.
55. Olson MA, Feig M, Brooks CL III. Prediction of protein loop conformations using multiscale modeling methods with physical energy scoring function. J Comput Chem 2008, 29:820-831.
56. Fan H, Irwin JJ, Webb BM, Klebe G, Shoichet BK, Sali A. Molecular docking screens using comparative models of proteins. J Chem Inf Model 2009, 49:2512-2527.
57. Novoa EM, de Pouplana LR, Barril X, Orozco M. Ensemble docking from homology models. J Chem Theory Comput 2010, 6:2547-2557.
58. Paulsen JL, Anderson AC. Scoring ensembles of docking protein: ligand interactions for virtual lead optimization. J Chem Inf Model 2009, 49:2813-2819.
59. Huang SY, Zou X. Ensemble docking of multiple protein structures: considering protein structural variations in molecular docking. Proteins 2007, 66:399-421.
60. Erickson JA, Jalaie M, Robertson DH, Lewis RA, Vieth M. Lessons in molecular recognition: the effects of ligand and protein flexibility on molecular docking accuracy. J Med Chem 2004, 47:45-55.
61. Bowman AL, Lerner MG, Carlson HA. Protein flexibility and species specificity in structure-based drug discovery: dihydrofolate reductase as a test system. J Am Chem Soc 2007, 129:3634-3640.
62. Corbeil CR, Englebienne P, Moitessier N. Docking ligands into flexible and solvated macromolecules. 1. Development and validation of FITTED 1.0. J Chem Inf Model 2007, 47:435-449.
63. Corbeil CR, Englebienne P, Yannopoulos CG, Chan L, Das SK, Bilimoria D, L'Heureux L, Moitessier N. Docking ligands into flexible and solvated macromolecules. 2. Development and application of FITTED 1.5 to the virtual screening of protein HCV polymerase inhibitors. J Chem Inf Model 2008, 48:902-909.
64. Claussen H, Buning C, Rarey M, Lengauer T. FlexE: efficient molecular docking considering protein structure variations. J Mol Biol 2001, 308:377-395.
65. Wei BQ, Weaver LH, Ferrari AM, Matthews BW, Shoichet BK. Testing a flexible-receptor docking algorithm in a model binding site. J Mol Biol 2004, 337:1161-1182.
66. Österberg F, Morris G, Sanner M, Olson A, Goodsell D. Automated docking to multiple targets structures: incorporation of protein mobility and structural water heterogeneity in AutoDock. Proteins 2002, 46:34-40.
67. Knegtel RMA, Kuntz ID, Oshiro CM. Molecular docking to ensemble of protein structures. J Mol Biol 1997, 266:424-440.
68. Broughton HB. A method for including protein flexibility in protein-ligand docking: improving tools for database mining and virtual screening. J Mol Graph Model 2000, 18:247-257.
69. Bolstad ES, Anderson AC. In pursuit of virtual lead optimization: pruning ensembles of receptor structures for increased efficiency and accuracy during docking. Proteins 2009, 75:62-74.
70. Bolstad ES, Anderson AC. In pursuit of virtual lead optimization: the role of the receptor structure and ensembles in accurate docking. Proteins 2008, 73:566-580.
71. Barril X, Morley SD. Unveiling the full potential of flexible receptor docking using multiple crystallographic structures. J Med Chem 2005, 48:4432-4443.
72. Rueda M, Bottegoni G, Abagyan R. Recipes for the selection of experimental protein conformations for virtual screening. J Chem Inf Model 2010, 50:186-193.
73. Hooft RW, Sander C, Vriend G. Positioning hydrogen atoms by optimizing hydrogen-bond networks in protein structures. Proteins 1996, 26:534-553.
74. Schnecke V, Kuhn LA. Virtual screening with solvation and ligand-induced complementarity. Persp Drug Discov Des 2000, 20:171-190.
75. Anderson AC, O'Neil RH, Surti TS, Stroud RM. Approaches to solving the rigid receptor problem by identifying a minimal set of flexible residues during ligand docking. Chem Biol 2001, 8:445-457.
76. Zavodszky MI, Kuhn LA. Side-chain flexibility in protein-ligand binding: the minimal rotation hypothesis. Protein Sci 2005, 14:1104-1114.
77. Najmanovich R, Kuttner J, Sobolev V, Edelman M. Side-chain flexibility in proteins upon ligand binding. Proteins 2000, 39:261-268.
78. Murray CW, Baxter CA, Frenkel AD. The sensitivity of the results of molecular docking to induced fit effects: application to thrombin, thermolysin and neuraminidas. J Comput Aid Mol Des 1999, 13:547-562.
79. Anderson AC, O'Neil RH, Suritu TS, Stroud RM. Approaches to solving the rigid receptor problem by identifying a minimal set of flexible residues during ligand docking. Chem Biol 2001, 8:445-457.
80. Fischer B, Merlitz H, Wenzel W. Increasing Diversity in in-silico screening with target flexibility. Lect Notes Comput Sci 2005, 695:186-197.
81. Lill MA, Vedani A, Dobler M. Raptor: combining dual-shell representation, induced-fit simulation, and hydrophobicity scoring in receptor modeling: application toward the simulation of structurally diverse ligand sets. J Med Chem 2004, 47:6174-6186.
82. Nabuurs SB, Wagener M, de Vlieg J. A flexible approach to induced fit docking. J Med Chem 2007, 50:6507-6518.
83. Garzon JI, Kovacs J, Abagyan R, Chacon P. DFprot: a webtool for predicting local chain deformability. Bioinformatics 2007, 23:901-902.
84. Glaser F, Rosenberg Y, Kessel A, Pupko T, Ben-Tal N. The ConSurf-HSSP database: the mapping of evolutionary conservation among homologs onto PDB structures. Proteins 2005, 58:610-617.
85. Gunasekaran K, Nussinov R. How different are structurally flexible and rigid protein sites? Sequences and structural features discriminate proteins that do and do not undergo conformational change upon ligand binding. J Mol Biol 2007, 365:257-273.
86. Zhao Y, Sanner MF. FLIPDock: docking flexible ligands into flexible receptors. Proteins 2007, 68:726-737.
87. Jones G, Willett P, Glen RC, Leach AR, Taylor R. Development and validation of a genetic algorithm for flexible docking. J Mol Biol 1997, 267:727-748.
88. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, Olson AJ. AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J Comput Chem 2009, 30:785-2791.
89. Leach AR. Ligand docking to proteins with discrete side-chain flexibility. J Mol Biol 1994, 235:345-356.
90. Desmet J, Wilson IA, Joniau M, De Maeyer M, Lasters I. Computation of the binding of fully flexible peptides to proteins with flexible side chains. FASEB J 1997, 11:164-172.
91. Frimurer TM, Peters GH, Iversen LF, Andersen HS, Moller NP, Olsen OH. Ligand-induced conformational changes: improved predictions of ligand binding conformations and affinities. Biophys J 2003, 84:2273-2281.
92. Heringa J, Argos P. Strain in protein structures as viewed through nonrotameric side chains: effect upon ligand binding. Proteins 1999, 37:44-55.
93. Wang C, Schueler-Furman O, Baker D. Improved side-chain modeling for protein-protein docking. Protein Sci 2005, 14:1328-1339.
94. Sousa SF, Fernandes PA, Ramos MJ. Protein-ligand docking: current status and future challenges. Proteins 2006, 65:15-26.
95. Kellenberger E, Rodrigo J, Muller D, Rognan D. Comparative evaluation of eight docking tools for docking and virtual screening accuracy. Proteins 2004, 57:225-242.
96. Totrov MM, Abagyan RA. Flexible protein-ligand docking by global energy optimization in internal coordinates. Proteins 1997, 1:215-220.
97. Bottegoni G, Kufareva I, Totrov M, Abagyan R. A new method for ligand docking to flexible receptors by dual alanine scanning and refinement (SCARE). J Comput Aided Mol Des 2008, 22:311-326.
98. Cavasotto CN, Abagyan RA. Protein flexibility in ligand docking and virtual screening to protein kinases. J Mol Biol 2004, 337:209-225.
99. Zhao Y, Stoffler D, Sanner M. Hierarchical and multi-resolution representation of protein flexibility. Bioinformatics 2006, 22:2768-2774.
100. Sutherland JJ, Nadigam RK, Erickson JA, Vieth M. Lessons in molecular recognition. 2. Assessing and improving cross-docking accuracy. J Chem Inf Model 2007, 47:2293-2302.
101. Polgar T, Keserü GM. Ensemble docking into flexible active sites. Critical evaluation of FlexE against JNK-3 and β-secretase. J Chem Inf Model 2006, 46:1795-1805.
102. Davis AM, Teague SJ, Kleywegt GJ. Application and limitations of X-ray crystallographic data in structure-based ligand and drug design. Angew Chem Int Ed Engl 2003, 42:2718-2736.
103. Park MS, Dessal AL, Smarcka AV, Stern HA. Evaluating docking methods for prediction of binding affinities of small molecules to the G protein beta gamma subunits. J Chem Inf Model 2009, 49:437-443.
104. Friesner RA, Murphy RB, Repasky MP, Frye LL, Greenwood JR, Halgren TA, Sanschagrin PC, Mainz DT. Extra precision glide: docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes. J Med Chem 2006, 49:6177-6196.
105. Kim J, Park JG, Chong Y. FlexE ensemble docking approach to virtual screening for CDK2 inhibitors. Mol Simul 2007, 33:667-676.
106. Molecular Movements Database. Protein structures showing different types of conformational change. Available at: http://www.molmovdb.org/cgi-bin/browse.cgi. (Accessed February 4, 2011).
107. Moitessier N, Englebienne P, Lee D, Lawandi J, Corbeil CR. Towards the development of universal, fast and highly accurate docking/scoring methods: a long way to go. Br J Pharmacol 2008, 153:S7-S26.
108. Gilson MK, Zhou HX. Calculation of protein-ligand binding affinity. Annu Rev Biophys Biomol Struct 2007, 36:21-42.
109. Cozzini P, Kellogg GE, Spyrakis F, Abraham DJ, Costantino G, Emerson A, Fanelli F, Gohlke H, Kuhn LA, Morris GM, et al. Target flexibility: an emerging consideration in drug discovery. J Med Chem 2008, 51:6237-6255.
110. Kuznetsov IB. Simplified computational methods for the analysis of protein flexibility. Curr Protein Pept Sci 2009, 10:607-613.
111. Huang N, Schoichet BK, Irwing JJ. Benchmarking sets for molecular docking. J Med Chem 2006, 49:6789-6801.