Strategies to calculate water binding free energies in protein-ligand complexes

Journal of Chemical Information and Modeling

Volumn 54, Issue 6, 2014, Pages 1623-1633

  Bodnarchuk, Michael S ^a   Viner, Russell ^b   Michel, Julien ^c   Essex, Jonathan W ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b JEALOTT S HILL INTERNATIONAL RESEARCH CENTRE   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; COMPLEXATION; FREE ENERGY; LIGANDS; LOCATION; MOLECULES; MONTE CARLO METHODS; PROTEINS;

BINDING FREE ENERGY; BOUND WATER MOLECULES; COMPUTATIONAL EFFORT; GRAND CANONICAL MONTE CARLO; HIGH DEGREE OF ACCURACY; PROTEIN-LIGAND COMPLEXES; RATIONAL DRUG DESIGNS; RIGOROUS APPROACH;

BINDING ENERGY;

LIGAND; PROTEIN BINDING; SIALIDASE; WATER;

ALGORITHM; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; ENZYMOLOGY; METABOLISM; MONTE CARLO METHOD; ORTHOMYXOVIRUS; THERMODYNAMICS;

ALGORITHMS; BINDING SITES; COMPUTER SIMULATION; LIGANDS; MODELS, MOLECULAR; MONTE CARLO METHOD; NEURAMINIDASE; ORTHOMYXOVIRIDAE; PROTEIN BINDING; THERMODYNAMICS; WATER;

EID: 84902128861     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci400674k     Document Type: Article

References (62)

1. Cappel, D.; Wahlstrom, R.; Brenk, R.; Sotriffer, C. A. Probing the dynamic nature of water molecules and their influences on ligand binding in a model binding site J. Chem. Inf. Model. 2011, 51, 2581-2594
2. Wallnoefer, H. G.; Liedl, K. R.; Fox, T. A GRID-derived water network stabilizes molecular dynamics computer simulations of a protease J. Chem. Inf. Model. 2011, 51, 2860-2867
3. Li, Y.; Sutch, B. T.; Bui, H.-H.; Gallaher, T. K.; Haworth, I. S. Modeling of the water network at protein-RNA interfaces J. Chem. Inf. Model. 2011, 51, 1347-1352
4. Fadda, E.; Woods, R. J. On the role of water models in quantifying the binding free energy of highly conserved water molecules in proteins: The case of Concanavalin A J. Chem. Theory Comput. 2011, 7, 3391-3398
5. Barillari, C.; Duncan, A. L.; Westwood, I. M.; Blagg, J.; Van Montfort, R. L. M. Analysis of water patterns in protein kinase binding sites Proteins: Struct. Funct. Bioinf. 2011, 79, 2109-2121
6. Poornima, C. S.; Dean, P. M. Hydration in drug design. 1. Multiple hydrogen-bonding features of water molecules in mediating protein-ligand interactions J. Comput.-Aided Mol. Des. 1995, 9, 500-512
7. Poornima, C. S.; Dean, P. M. Hydration in drug design. 2. Influence of local site surface shape on water binding J. Comput.-Aided Mol. Des. 1995, 9, 513-520
8. Poornima, C. S.; Dean, P. M. Hydration in drug design. 3. Conserved water molecules at the ligand-binding sites of homologous proteins J. Comput.-Aided Mol. Des. 1995, 9, 521-531
9. Cheng, T.; Li, Q.; Zhou, Z.; Wang, Y.; Bryant, S. H. Structure-based virtual screening for drug discovery: a problem-centric review Am. Asso. Pharma. Sci. 2012, 14, 131-141
10. Wong, S. E.; Lightstone, F. C. Accounting for water molecules in drug design Exp. Opin. Drug Discov. 2011, 6, 65-74
11. Huggins, D. J.; Tidor, B. Systematic placement of structural water molecules for improved scoring of protein-ligand interactions Prot. Eng. Des. Sel. 2011, 24, 777-789
12. Varghese, J. N.; Epa, V. C.; Colman, P. M. Three-dimensional structure of the complex of 4-guanidino-Neu5Ac2en and influenza virus neuraminidase Protein Sci. 1995, 4, 1081-1087
13. Smith, B. J.; Colman, P. M.; Von Itzstein, M.; Danylec, B.; Varghese, J. N. Analysis of inhibitor binding in influenza virus neuraminidase Protein Sci. 2001, 10, 689-696
14. De Lucca, G. V.; Erickson-Viitanen, S.; Lam, P. Y. S. Cyclic HIV protease inhibitors capable of displacing the active site structural water molecule Drug Discov. Today 1997, 2, 6-18
15. De Beer, S. B. A.; Vermeulen, N. P. E.; Oostenbrink, C. The role of water molecules in computational drug design Curr. Top. Med. Chem. 2010, 10, 55-66
16. Hummer, G. Molecular binding: Under water's influence Nat. Chem. 2010, 2, 906-907
17. Setny, P.; Baron, R.; McCammon, J. A. How can hydrophobic association be enthalpy driven? J. Chem. Theory Comput. 2010, 6, 2866-2871
18. Baron, R.; Setny, P.; McCammon, J. A. Water in cavity-ligand recognition J. Am. Chem. Soc. 2010, 132, 12091-12097
19. Shan, Y.; Kim, E. T.; Eastwood, M. P.; Dror, R. O.; Seeliger, M. A.; Shaw, D. E. How does a drug molecule find its target binding site? J. Am. Chem. Soc. 2011, 133, 9181-9183
20. Bren, U.; Janežič, D. Individual degrees of freedom and the solvation properties of water J. Chem. Phys. 2012, 137, 024108-024119
21. Homans, S. W. Water, water everywhere-except where it matters? Drug Discov. Today 2007, 12, 534-539
22. Englert, L.; Biela, A.; Zayed, M.; Heine, A.; Hangauer, D.; Klebe, G. Displacement of disordered water molecules from hydrophobic pocket creates enthalpic signature: binding of phosphonamidate to the S4-pocket of thermolysin Biochim. Biophys. Acta 2010, 1800, 1192-1202
23. Ball, P. Biophysics: More than a bystander Nature 2011, 478, 467-468
24. Carugo, O.; Bordo, D. How many water molecules can be detected by protein crystallography? Acta Cryst. Sec. D Biol. Cryst. 1999, 55, 479-483
25. Abel, R.; Salam, N. K.; Shelley, J.; Farid, R.; Friesner, R. A.; Sherman, W. Contribution of explicit solvent effects to the binding affinity of small-molecule inhibitors in blood coagulation factor serine proteases Chem. Med. Chem. 2011, 6, 1049-1066
26. Davis, A. M.; Teague, S. J.; Kleywegt, G. J. Application and limitations of X-ray crystallographic data in structure-based ligand and drug design Angew. Chem., Int. Ed. 2003, 42, 2718-2736
27. Adams, D. J. Chemical potential of hard-sphere fluids by Monte-Carlo methods Mol. Phys. 1974, 28, 1241-1252
28. Adams, D. J. Grand canonical ensemble Monte Carlo for a Lennard-Jones fluid Mol. Phys. 1975, 29, 307-311
29. Guarnieri, F.; Mezei, M. Simulated annealing of chemical potential: a general procedure for locating bound waters. Application to the study of the differential hydration propensities of the major and minor grooves of DNA J. Am. Chem. Soc. 1996, 118, 8493-8494
30. Woo, H.-J.; Dinner, A. R.; Roux, B. Grand canonical Monte Carlo simulations of water in protein environments J. Chem. Phys. 2004, 121, 6392-6400
31. Bortolato, A.; Tehan, B.; Bodnarchuk, M. S.; Essex, J. W.; Mason, J. Water network perturbation in ligand binding: Adenosine A(2A) antagonists as a case study J. Chem. Inf. Model. 2013, 53, 1700-1713
32. Mezei, M. A cavity-biased (T,V,mu) Monte-Carlo method for the computer-simulation of fluids Mol. Phys. 1980, 40, 901-906
33. Mezei, M. Grand-canonical ensemble Monte Carlo study of dense liquid Lennard-Jones, soft spheres and water Mol. Phys. 1987, 61, 565-582
34. Shelley, J. C.; Patey, G. N. A configuration bias Monte-Carlo method for water J. Chem. Phys. 1995, 102, 7656-7664
35. Lazaridis, T. Inhomogeneous fluid approach to solvation thermodynamics. 1. Theory J. Phys. Chem. B 1998, 102, 3531-3541
36. Lazaridis, T. Inhomogeneous fluid approach to solvation thermodynamics. 2. Applications to simple fluids J. Phys. Chem. B 1998, 102, 3542-3550
37. Nguyen, C. N.; Young, T. K.; Gilson, M. K. Grid inhomogeneous solvation theory: Hydration structure and thermodynamics of the miniature receptor cucurbit[7]uril J. Chem. Phys. 2012, 137, 044101
38. Prabhu, E. P.; MacKerell, A. D. Rapid estimation of hydration thermodynamics of macromolecular regions J. Chem. Phys. 2013, 139, 055105
39. Young, T.; Abel, R.; Kim, B.; Berne, B. J.; Friesner, R. A. Motifs for molecular recognition exploiting hydrophobic enclosure in protein-ligand binding Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 808-813
40. Abel, R.; Young, T.; Farid, R.; Berne, B. J.; Friesner, R. A. Role of the active-site solvent in the thermodynamics of factor Xa ligand binding J. Am. Chem. Soc. 2008, 130, 2817-2831
41. Michel, J.; Tirado-Rives, J.; Jorgensen, W. L. Prediction of the water content in protein binding sites J. Phys. Chem. B 2009, 113, 13337-13346
42. Robinson, D. D.; Sherman, W.; Farid, R. Understanding kinase selectivity through energetic analysis of binding site waters Chem. Med. Chem. 2010, 5, 618-627
43. Beuming, T.; Farid, R.; Sherman, W. High-energy water sites determine peptide binding affinity and specificity of PDZ domains Protein Sci. 2009, 18, 1609-1619
44. Kong, X.; Brooks, C. L., III Lambda-Dynamics: A new approach to free energy calculations J. Chem. Phys. 1996, 105, 2414-2423
45. Ross, G. A.; Morris, G. M.; Biggin, P. C. Rapid and accurate prediction and scoring of water molecules in protein binding sites PLoS One 2012, 7, e32036
46. Michel, J.; Tirado-Rives, J.; Jorgensen, W. L. Energetics of displacing water molecules from protein binding sites: consequences for ligand optimization J. Am. Chem. Soc. 2009, 131, 15403-15411
47. Luccarelli, J.; Michel, J.; Tirado-Rives, J.; Jorgensen, W. L. Effects of water placement on predictions of binding affinities for p38α MAP kinase inhibitors J. Chem. Theory Comput. 2010, 6, 3850-3856
48. Gilson, M. K.; Given, J. A.; Bush, B. L.; McCammon, J. A. The statistical-thermodynamic basis for computation of binding affinities: a critical review Biophys. J. 1997, 72, 1047-1069
49. Barillari, C.; Taylor, J.; Viner, R.; Essex, J. W. Classification of water molecules in protein binding sites J. Am. Chem. Soc. 2007, 129, 2577-2587
50. Woods, C. J.; Essex, J. W.; King, M. A. Enhanced configurational sampling in binding free-energy calculations J. Phys. Chem. B 2003, 107, 13711-13718
51. Woods, C. J.; Essex, J. W.; King, M. A. The development of replica-exchange-based free-energy methods J. Phys. Chem. B 2003, 107, 13703-13710
52. Vriend, G. WHAT IF: a molecular modeling and drug design program J. Mol. Graph. 1990, 8, 52-56, 29
53. Jakalian, A.; Bush, B. L.; Jack, D. B.; Bayly, C. I. Fast, efficient generation of high-quality atomic charges. AM1-BCC model: I. Method J. Comput. Chem. 2000, 21, 132-146
54. Udommaneethanakit, T.; Rungrotmongkol, T.; Bren, U.; Frecer, V.; Stanislav, M. Dynamic behavior of avian influenza A virus neuraminidase subtype H5N1 in complex with oseltamivir, zanamivir, peramivir, and their phosphonate analogues J. Chem. Inf. Model. 2009, 49, 2323-2332
55. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 1983, 79, 926-935
56. Wang, J.; Cieplak, P.; Kollman, P. A. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem. 2000, 21, 1049-1074
57. Brunsteiner, M.; Boresch, S. Influence of the treatment of electrostatic interactions on the results of free energy calculations of dipolar systems J. Chem. Phys. 2000, 112, 6953-6955
58. Wang, J.; Wolf, R. M.; Caldwell, J. W.; Kollman, P. A.; Case, D. A. Development and testing of a general amber force field J. Comput. Chem. 2004, 25, 1157-1174
59. Woods, C.; Michel, J. ProtoMS2.2.; 2007.
60. Hartshorn, M. J. AstexViewer: a visualisation aid for structure-based drug design J. Comput.-Aided Mol. Des. 2002, 16, 871-881
61. Clark, M.; Meshkat, S.; Wiseman, J. S. Grand canonical free-energy calculations of protein-ligand binding J. Chem. Inf. Model. 2009, 49, 934-943
62. Clark, M.; Guarnieri, F.; Shkurko, I.; Wiseman, J. Grand canonical Monte Carlo simulation of ligand-protein binding J. Chem. Inf. Model. 2006, 46, 231-242