Significant enhancement of docking sensitivity using implicit ligand sampling

Journal of Chemical Information and Modeling

Volumn 51, Issue 3, 2011, Pages 693-706

  Xu, Mengang ^a   Lill, Markus A ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BIOINFORMATICS; COMPLEXATION; CONFORMATIONS; MOLECULAR DYNAMICS; PROTEINS;

ACCURATE QUANTIFICATIONS; BINDING AFFINITIES; MOLECULAR DYNAMICS SIMULATIONS; PROTEIN CONFORMATION; PROTEIN FLEXIBILITY; PROTEIN STRUCTURES; PROTEIN-LIGAND COMPLEXES; PROTEIN-LIGAND INTERACTIONS;

LIGANDS;

LIGAND;

ARTICLE; MOLECULAR DYNAMICS;

LIGANDS; MOLECULAR DYNAMICS SIMULATION;

EID: 79953180618     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci100457t     Document Type: Article

References (64)

1. Zwanzig, R. W. High-Temperature Equation of State by A Perturbation Method 0.1. Nonpolar Gases J. Chem. Phys. 1954, 22, 1420-1426
2. Kirkwood, J. G. Statistical mechanics of fluid mixtures J. Chem. Phys. 1935, 3, 300-313
3. Aqvist, J.; Medina, C.; Samuelsson, J. E. A new method for predicting binding affinity in computer-aided drug design Protein Eng. 1994, 7, 385-391 (Pubitemid 24063137)
4. Srinivasan, J.; Miller, J.; Kollman, P. A.; Case, D. A. Continuum solvent studies of the stability of RNA hairpin loops and helices J. Biomol. Struct. Dyn. 1998, 16, 671-682 (Pubitemid 29100322)
5. Cheng, T.; Li, X.; Li, Y.; Liu, Z.; Wang, R. Comparative assessment of scoring functions on a diverse test set J. Chem. Inf. Model. 2009, 49, 1079-1093
6. Teague, S. J. Implications of protein flexibility for drug discovery Nat. Rev. Drug Discovery 2003, 2, 527-541 (Pubitemid 37361745)
7. Carlson, H. A. Protein flexibility and drug design: how to hit a moving target Curr. Opin. Chem. Biol. 2002, 6, 447-452 (Pubitemid 34804766)
8. Zavodszky, M. I.; Lei, M.; Thorpe, M. F.; Day, A. R.; Kuhn, L. A. Modeling correlated main-chain motions in proteins for flexible molecular recognition Proteins 2004, 57, 243-261 (Pubitemid 39223730)
9. Sousa, S. F.; Fernandes, P. A.; Ramos, M. J. Protein-ligand docking: current status and future challenges Proteins 2006, 65, 15-26 (Pubitemid 44320611)
10. Mizutani, M. Y.; Takamatsu, Y.; Ichinose, T.; Nakamura, K.; Itai, A. Effective handling of induced-fit motion in flexible docking Proteins 2006, 63, 878-891 (Pubitemid 43765140)
11. Sherman, W.; Day, T.; Jacobson, M. P.; Friesner, R. A.; Farid, R. Novel procedure for modeling ligand/receptor induced fit effects J. Med. Chem. 2006, 49, 534-553 (Pubitemid 43157487)
12. Corbeil, C. R.; Moitessier, N. Docking ligands into flexible and solvated macromolecules. 3. Impact of input ligand conformation, protein flexibility, and water molecules on the accuracy of docking programs J. Chem. Inf. Model. 2009, 49, 997-1009
13. Englebienne, P.; Moitessier, N. Docking ligands into flexible and solvated macromolecules. 4. Are popular scoring functions accurate for this class of proteins? J. Chem. Inf. Model. 2009, 49, 1568-1580
14. Lin, J. H. Accommodating Protein Flexibility for Structure-Based Drug Design Curr. Top. Med. Chem. 2011, 11, 171-178
15. Rao, C.; Subramanian, J.; Sharma, S. D. Managing protein flexibility in docking and its applications Drug Discovery Today 2009, 14, 394-400
16. Sotriffer, C. A. Accounting for Induced-Fit Effects in Docking: What is Possible and What is Not? Curr. Top. Med. Chem. 2011, 11, 179-191
17. Cozzini, P.; Kellogg, G. E.; Spyrakis, F.; Abraham, D. J.; Costantino, G.; Emerson, A.; Fanelli, F.; Gohlke, H.; Kuhn, L. A.; Morris, G. M.; Orozco, M.; Pertinhez, T. A.; Rizzi, M.; Sotriffer, C. A. Target flexibility: an emerging consideration in drug discovery and design J. Med. Chem. 2008, 51, 6237-6255
18. Ferrari, A. M.; Wei, B. Q.; Costantino, L.; Shoichet, B. K. Soft docking and multiple receptor conformations in virtual screening J. Med. Chem. 2004, 47, 5076-5084 (Pubitemid 39314905)
19. Knegtel, R. M.; Kuntz, I. D.; Oshiro, C. M. Molecular docking to ensembles of protein structures J. Mol. Biol. 1997, 266, 424-440 (Pubitemid 27171024)
20. Leach, A. R. Ligand docking to proteins with discrete side-chain flexibility J. Mol. Biol. 1994, 235, 345-356 (Pubitemid 24049519)
21. Hart, T. N.; Read, R. J. A multiple-start Monte Carlo docking method Proteins 1992, 13, 206-222
22. Lill, M. A.; Dobler, M.; Vedani, A. Prediction of small-molecule binding to cytochrome P450 3A4: flexible docking combined with multidimensional QSAR ChemMedChem. 2006, 1, 73-81 (Pubitemid 44104980)
23. Davis, I. W.; Baker, D. RosettaLigand docking with full ligand and receptor flexibility J. Mol. Biol. 2009, 385, 381-392
24. Carlson, H. A.; Masukawa, K. M.; Rubins, K.; Bushman, F. D.; Jorgensen, W. L.; Lins, R. D.; Briggs, J. M.; McCammon, J. A. Developing a dynamic pharmacophore model for HIV-1 integrase J. Med. Chem. 2000, 43, 2100-2114 (Pubitemid 30354535)
25. Lin, J. H.; Perryman, A. L.; Schames, J. R.; McCammon, J. A. The relaxed complex method: Accommodating receptor flexibility for drug design with an improved scoring scheme Biopolymers 2003, 68, 47-62 (Pubitemid 36098307)
26. Lin, J. H.; Perryman, A. L.; Schames, J. R.; McCammon, J. A. Computational drug design accommodating receptor flexibility: the relaxed complex scheme J. Am. Chem. Soc. 2002, 124, 5632-5633 (Pubitemid 34533490)
27. Kua, J.; Zhang, Y.; McCammon, J. A. Studying enzyme binding specificity in acetylcholinesterase using a combined molecular dynamics and multiple docking approach J. Am. Chem. Soc. 2002, 124, 8260-8267 (Pubitemid 34875385)
28. 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
29. Kar, G.; Keskin, O.; Gursoy, A.; Nussinov, R. Allostery and population shift in drug discovery Curr. Opin. Pharmacol. 2010, 10, 715-722
30. Ozbabacan, S. E.; Gursoy, A.; Keskin, O.; Nussinov, R. Conformational ensembles, signal transduction and residue hot spots: application to drug discovery Curr. Opin. Drug Discovery Dev. 2010, 13, 527-537
31. Nevo, R.; Brumfeld, V.; Elbaum, M.; Hinterdorfer, P.; Reich, Z. Direct discrimination between models of protein activation by single-molecule force measurements Biophys. J. 2004, 87, 2630-2634
32. McGovern, S. L.; Shoichet, B. K. Information decay in molecular docking screens against holo, apo, and modeled conformations of enzymes J. Med. Chem. 2003, 46, 2895-2907 (Pubitemid 36775915)
33. Murray, C. W.; Baxter, C. A.; Frenkel, A. D. The sensitivity of the results of molecular docking to induced fit effects: application to thrombin, thermolysin and neuraminidase J. Comput.-Aided Mol. Des. 1999, 13, 547-562 (Pubitemid 29524912)
34. Hoffmann, D.; Kramer, B.; Washio, T.; Steinmetzer, T.; Rarey, M.; Lengauer, T. Two-stage method for protein-ligand docking J. Med. Chem. 1999, 42, 4422-4433 (Pubitemid 29504146)
35. Obst, U.; Banner, D. W.; Weber, L.; Diederich, F. Molecular recognition at the thrombin active site: Structure-based design and synthesis of potent and selective thrombin inhibitors and the x-ray crystal structures of two thrombin-inhibitor complexes Chem. Biol. 1997, 4, 287-295 (Pubitemid 27235868)
36. Schweizer, E.; Hoffmann-Roder, A.; Olsen, J. A.; Seiler, P.; Obst-Sander, U.; Wagner, B.; Kansy, M.; Banner, D. W.; Diederich, F. Multipolar interactions in the D pocket of thrombin: large differences between tricyclic imide and lactam inhibitors Org. Biomol. Chem. 2006, 4, 2364-2375 (Pubitemid 43882758)
37. Schweizer, E.; Hoffmann-Roder, A.; Scharer, K.; Olsen, J. A.; Fah, C.; Seiler, P.; Obst-Sander, U.; Wagner, B.; Kansy, M.; Diederich, F. A fluorine scan at the catalytic center of thrombin: C-F, C-OH, and C-OMe bioisosterism and fluorine effects on pK(a) and log(D) values ChemMedChem 2006, 1, 611-621 (Pubitemid 44105787)
38. Bowman, A. L.; Lerner, M. G.; Carlson, H. A. Protein flexibility and species specificity in structure-based drug discovery: dihydrofolate reductase as a test system J. Am. Chem. Soc. 2007, 129, 3634-3640 (Pubitemid 46502724)
39. Trott, O.; Olson, A. J. AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading J. Comput. Chem. 2010, 31, 455-461
40. Lill, M. A.; Danielson, M. L. Computer-aided drug design platform using PyMOL J. Comput.-Aided Mol. Des 2011, 25, 13-19
41. Morris, G. M.; Huey, R.; Lindstrom, W.; Sanner, M. F.; Belew, R. K.; Goodsell, D. S.; Olson, A. J. AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility J. Comput. Chem. 2009, 30, 2785-2791
42. Case, D. A.; Cheatham, T. E., III; Darden, T.; Gohlke, H.; Luo, R.; Merz, K. M., Jr.; Onufriev, A.; Simmerling, C.; Wang, B.; Woods, R. J. The Amber biomolecular simulation programs J. Comput. Chem. 2005, 26, 1668-1688 (Pubitemid 43076180)
43. Kutzner, C.; van der, S. D.; Fechner, M.; Lindahl, E.; Schmitt, U. W.; de Groot, B. L.; Grubmuller, H. Speeding up parallel GROMACS on high-latency networks J. Comput. Chem. 2007, 28, 2075-2084 (Pubitemid 47153605)
44. van der, S. D.; Lindahl, E.; Hess, B.; Groenhof, G.; Mark, A. E.; Berendsen, H. J. GROMACS: fast, flexible, and free J. Comput. Chem. 2005, 26, 1701-1718 (Pubitemid 43076182)
45. Kortvelyesi, T.; Dennis, S.; Silberstein, M.; Brown, L., III; Vajda, S. Algorithms for computational solvent mapping of proteins Proteins 2003, 51, 340-351 (Pubitemid 36528820)
46. Eisenhaber, F.; Lijnzaad, P.; Argos, P.; Sander, C.; Scharf, M. The Double Cubic Lattice Method-Efficient Approaches to Numerical-Integration of Surface-Area and Volume and to Dot Surface Contouring of Molecular Assemblies J. Comput. Chem. 1995, 16, 273-284
47. Eisenhaber, F.; Argos, P. Improved Strategy in Analytic Surface Calculation for Molecular-Systems-Handling of Singularities and Computational-Efficiency J. Comput. Chem. 1993, 14, 1272-1280
48. Roitberg, A.; Elber, R. Modeling side chains in peptides and proteins: Application of the locally enhanced sampling technique and the simulated annealing methods to find minimum energy conformations J. Chem. Phys. 1991, 95, 9277-9287
49. The multilinear regression data analysis for this paper was generated using SAS software, Version 9.2 of the SAS system for Windows, Copyright 2002-2008, SAS Institute Inc. SAS and all other SAS Institute Inc. product or service names are registered trademarks or trademarks of SAS Institute Inc., Cary, NC, USA, 2010.
50. Ferrara, P.; Gohlke, H.; Price, D. J.; Klebe, G.; Brooks, C. L., III Assessing scoring functions for protein-ligand interactions J. Med. Chem. 2004, 47, 3032-3047 (Pubitemid 38702700)
51. Kuntz, I. D.; Chen, K.; Sharp, K. A.; Kollman, P. A. The maximal affinity of ligands Proc. Natl. Acad. Sci. U. S. A 1999, 96, 9997-10002 (Pubitemid 29422500)
52. Bahar, I.; Rader, A. J. Coarse-grained normal mode analysis in structural biology Curr. Opin. Struct. Biol. 2005, 15, 586-592 (Pubitemid 41393491)
53. Bahar, I.; Lezon, T. R.; Yang, L. W.; Eyal, E. Global Dynamics of Proteins: Bridging Between Structure and Function Ann. Rev. Biophys. 2010, 39, 23-42
54. Chennubhotla, C.; Rader, A. J.; Yang, L. W.; Bahar, I. Elastic network models for understanding biomolecular machinery: From enzymes to supramolecular assemblies Phys. Biol. 2005, 2, S173-S180
55. Keating, K. S.; Flores, S. C.; Gerstein, M. B.; Kuhn, L. A. StoneHinge: Hinge prediction by network analysis of individual protein structures Protein Sci. 2009, 18, 359-371
56. Kuhn, L. A.; Zavodszky, M. I.; Thorpe, M. F.; Lei, M. Balancing large and small scale flexibility in protein: ligand docking Abstr. Paper Am. Chem. Soc. Natl. Meet. 2003, 225, U743
57. Rader, A. J.; Hespenheide, B. M.; Kuhn, L. A.; Thorpe, M. F. Protein unfolding: rigidity lost Proc. Natl. Acad. Sci. U. S. A 2002, 99, 3540-3545 (Pubitemid 34256390)
58. Thorpe, M. F.; Lei, M.; Rader, A. J.; Jacobs, D. J.; Kuhn, L. A. Protein flexibility and dynamics using constraint theory J. Mol. Graphics Modell. 2001, 19, 60-69 (Pubitemid 32411502)
59. Xiang, Z.; Soto, C. S.; Honig, B. Evaluating conformational free energies: the colony energy and its application to the problem of loop prediction Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 7432-7437 (Pubitemid 34568708)
60. Jacobson, M. P.; Pincus, D. L.; Rapp, C. S.; Day, T. J.; Honig, B.; Shaw, D. E.; Friesner, R. A. A hierarchical approach to all-atom protein loop prediction Proteins 2004, 55, 351-367 (Pubitemid 38437493)
61. Zhang, C.; Liu, S.; Zhou, Y. Accurate and efficient loop selections by the DFIRE-based all-atom statistical potential Protein Sci. 2004, 13, 391-399 (Pubitemid 38124960)
62. Zhu, K.; Pincus, D. L.; Zhao, S.; Friesner, R. A. Long loop prediction using the protein local optimization program Proteins 2006, 65, 438-452 (Pubitemid 44454115)
63. Zhu, K.; Shirts, M. R.; Friesner, R. A. Improved methods for side chain and loop predictions via the protein local optimization program: Variable dielectric model for implicitly improving the treatment of polarization effects J. Chem. Theory Comput. 2007, 3, 2108-2119
64. Danielson, M. L.; Lill, M. A. New computational method for prediction of interacting protein loop regions Proteins 2010, 78, 1748-1759