Molecular simulations with solvent competition quantify water displaceability and provide accurate interaction maps of protein binding sites

Journal of Medicinal Chemistry

Volumn 57, Issue 20, 2014, Pages 8530-8539

  Alvarez Garcia, Daniel ^a   Barril, Xavier ^a,b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACETAMIDE; ALCOHOL; HEAT SHOCK PROTEIN 90; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE; LIGAND; ORGANIC SOLVENT; SOLVENT; WATER; P16 PROTEASE, HUMAN IMMUNODEFICIENCY VIRUS 1; PROTEIN; PROTEIN BINDING;

ARTICLE; BINDING COMPETITION; BINDING SITE; COMPUTER; COMPUTER PROGRAM; HYDROGEN BOND; LIGAND BINDING; MOLECULAR DYNAMICS; PREDICTION; PROTEIN BINDING; PROTEIN INTERACTION; SIMULATION; SOLVATION; WATER TRANSPORT; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN TERTIARY STRUCTURE; REPRODUCIBILITY;

BINDING SITES; HIV PROTEASE; HSP90 HEAT-SHOCK PROTEINS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEINS; REPRODUCIBILITY OF RESULTS; SOFTWARE; SOLVENTS; WATER;

EID: 84908374552     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm5010418     Document Type: Article

References (43)

1. Goodford, P. J. A Computational Procedure for Determining Energetically Favorable Binding Sites on Biologically Important Macromolecules J. Med. Chem. 1985, 28, 849-857
2. Sotriffer, C.; Klebe, G. Identification and Mapping of Small-Molecule Binding Sites in Proteins: Computational Tools for Structure-Based Drug Design Farmaco 2002, 57, 243-251
3. Gohlke, H.; Klebe, G. Approaches to the Description and Prediction of the Binding Affinity of Small-Molecule Ligands to Macromolecular Receptors Angew. Chem., Int. Ed. 2002, 41, 2644-2676
4. Boobbyer, D. N.; Goodford, P. J.; McWhinnie, P. M.; Wade, R. C. New Hydrogen-Bond Potentials for Use in Determining Energetically Favorable Binding Sites on Molecules of Known Structure J. Med. Chem. 1989, 32, 1083-1094
5. 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
6. Bissantz, C.; Kuhn, B.; Stahl, M. A Medicinal Chemist's Guide to Molecular Interactions J. Med. Chem. 2010, 53, 5061-5084
7. Sotriffer, C. A.; Gohlke, H.; Klebe, G. Docking into Knowledge-Based Potential Fields: A Comparative Evaluation of DrugScore J. Med. Chem. 2002, 45, 1967-1970
8. Bashford, D.; Case, D. A. Generalized Born Models of Macromolecular Solvation Effects Annu. Rev. Phys. Chem. 2000, 51, 129-152
9. Li, Z.; Lazaridis, T. Water at Biomolecular Binding Interfaces Phys. Chem. Chem. Phys. 2007, 9, 573-581
10. 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
11. 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
12. Barril, X.; Morley, S. D. Unveiling the Full Potential of Flexible Receptor Docking Using Multiple Crystallographic Structures J. Med. Chem. 2005, 48, 4432-4443
13. Seco, J.; Luque, F. J.; Barril, X. Binding Site Detection and Druggability Index from First Principles J. Med. Chem. 2009, 52, 2363-2371
14. Liepinsh, E.; Otting, G. Organic Solvents Identify Specific Ligand Binding Sites on Protein Surfaces Nat. Biotechnol. 1997, 15, 264-268
15. Mattos, C.; Bellamacina, C. R.; Peisach, E.; Pereira, A.; Vitkup, D.; Petsko, G. A.; Ringe, D. Multiple Solvent Crystal Structures: Probing Binding Sites, Plasticity and Hydration J. Mol. Biol. 2006, 357, 1471-1482
16. Guvench, O.; MacKerell, A. D. Computational Fragment-Based Binding Site Identification by Ligand Competitive Saturation PLoS Comput. Biol. 2009, 5, e1000435
17. Raman, E. P.; Yu, W.; Lakkaraju, S. K.; Mackerell, A. D. Inclusion of Multiple Fragment Types in the Site Identi Fi Cation by Ligand Competitive Saturation (SILCS) Approach J. Chem. Inf. Model. 2013, 53, 3384-3398
18. Lexa, K. W.; Carlson, H. A. Full Protein Flexibility Is Essential for Proper Hot-Spot Mapping J. Am. Chem. Soc. 2011, 133, 200-202
19. Lexa, K.; Carlson, H. Improving Protocols for Protein Mapping through Proper Comparison to Crystallography Data J. Chem. Inf. 2013, 53, 391-402
20. Lazaridis, T. Inhomogeneous Fluid Approach to Solvation Thermodynamics. 1. Theory J. Phys. Chem. B 1998, 102, 3531-3541
21. 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
22. Stebbins, C. E.; Russo, A. A.; Schneider, C.; Rosen, N.; Hartl, F. U.; Pavletich, N. P. Crystal Structure of an Hsp90-Geldanamycin Complex: Targeting of a Protein Chaperone by an Antitumor Agent Cell 1997, 89, 239-250
23. Ringhofer, S.; Kallen, J.; Dutzler, R.; Billich, A.; Visser, A. J.; Scholz, D.; Steinhauser, O.; Schreiber, H.; Auer, M.; Kungl, A. J. X-Ray Structure and Conformational Dynamics of the HIV-1 Protease in Complex with the Inhibitor SDZ283-910: Agreement of Time-Resolved Spectroscopy and Molecular Dynamics Simulations J. Mol. Biol. 1999, 286, 1147-1159
24. Alvarez-garcia, D.; Barril, X. Relationship between Protein Flexibility and Binding: Lessons for Structure-Based Drug Design J. Chem. Theory Comput. 2014, 10, 2608-2614
25. Molecular Operating Environment (MOE), version 2013.8; Chemical Computing Group Inc.: Montreal, Canada, 2013.
26. Wright, L.; Barril, X.; Dymock, B.; Sheridan, L.; Surgenor, A.; Beswick, M.; Drysdale, M.; Collier, A.; Massey, A.; Davies, N.; Fink, A.; Fromont, C.; Aherne, W.; Boxall, K.; Sharp, S.; Workman, P.; Hubbard, R. E. Structure-Activity Relationships in Purine-Based Inhibitor Binding to HSP90 Isoforms Chem. Biol. 2004, 11, 775-785
27. Sangster, J. Octanol-Water Partition Coefficients of Simple Organic Compounds J. Phys. Chem. Ref. Data 1989, 18, 1111-1229
28. Hann, M. M. Molecular Obesity, Potency and Other Addictions in Drug Discovery Med. Chem. Commun. 2011, 2, 349-355
29. Kaldor, S. W.; Kalish, V. J.; Davies, J. F.; Shetty, B. V.; Fritz, J. E.; Appelt, K.; Burgess, J. A.; Campanale, K. M.; Chirgadze, N. Y.; Clawson, D. K.; Dressman, B. A.; Hatch, S. D.; Khalil, D. A.; Kosa, M. B.; Lubbehusen, P. P.; Muesing, M. A.; Patick, A. K.; Reich, S. H.; Su, K. S.; Tatlock, J. H. Viracept (nelfinavir Mesylate, AG1343): A Potent, Orally Bioavailable Inhibitor of HIV-1 Protease J. Med. Chem. 1997, 40, 3979-3985
30. Dymock, B. W.; Barril, X.; Brough, P. A.; Cansfield, J. E.; Massey, A.; McDonald, E.; Hubbard, R. E.; Surgenor, A.; Roughley, S. D.; Webb, P.; Workman, P.; Wright, L.; Drysdale, M. J. Novel, Potent Small-Molecule Inhibitors of the Molecular Chaperone Hsp90 Discovered through Structure-Based Design J. Med. Chem. 2005, 48, 4212-4215
31. Kung, P. P.; Sinnema, P. J.; Richardson, P.; Hickey, M. J.; Gajiwala, K. S.; Wang, F.; Huang, B.; McClellan, G.; Wang, J.; Maegley, K.; Bergqvist, S.; Mehta, P. P.; Kania, R. Design Strategies to Target Crystallographic Waters Applied to the Hsp90 Molecular Chaperone Bioorg. Med. Chem. Lett. 2011, 21, 3557-3562
32. Davies, N. G. M.; Browne, H.; Davis, B.; Drysdale, M. J.; Foloppe, N.; Geoffrey, S.; Gibbons, B.; Hart, T.; Hubbard, R.; Jensen, M. R.; Mansell, H.; Massey, A.; Matassova, N.; Moore, J. D.; Murray, J.; Pratt, R.; Ray, S.; Robertson, A.; Roughley, S. D.; Schoepfer, J.; Scriven, K.; Simmonite, H.; Stokes, S.; Surgenor, A.; Webb, P.; Wood, M.; Wright, L.; Brough, P. Targeting Conserved Water Molecules: Design of 4-Aryl-5-cyanopyrrolo[2,3-D] Pyrimidine Hsp90 Inhibitors Using Fragment-Based Screening and Structure-Based Optimization Bioorg. Med. Chem. 2012, 20, 6770-6789
33. Fradera, X.; Mestres, J. Guided Docking Approaches to Structure-Based Design and Screening Curr. Top. Med. Chem. 2004, 4, 687-700
34. Yang, Y.; Lightstone, F. C.; Wong, S. E. Approaches to Efficiently Estimate Solvation and Explicit Water Energetics in Ligand Binding: The Use of WaterMap Expert Opin. Drug Discovery 2013, 8, 277-287
35. Pearlstein, R. A.; Sherman, W.; Abel, R. Contributions of Water Transfer Energy to Protein-Ligand Association and Dissociation Barriers: Watermap Analysis of a Series of p38 MAP Kinase Inhibitors Proteins: Struct., Funct., Bioinf. 2013, 81, 1509-1526
36. Pearlstein, R. A.; Hu, Q.-Y.; Zhou, J.; Yowe, D.; Levell, J.; Dale, B.; Kaushik, V. K.; Daniels, D.; Hanrahan, S.; Sherman, W.; Abel, R. New Hypotheses about the Structure-Function of Proprotein Convertase Subtilisin/kexin Type 9: Analysis of the Epidermal Growth Factor-like Repeat A Docking Site Using WaterMap Proteins 2010, 78, 2571-2586
37. Tran, Q. T.; Williams, S.; Farid, R.; Erdemli, G.; Pearlstein, R. The Translocation Kinetics of Antibiotics through Porin OmpC: Insights from Structure-Based Solvation Mapping Using WaterMap Proteins: Struct., Funct., Bioinf. 2013, 81, 291-299
38. Haider, K.; Huggins, D. J. Combining Solvent Thermodynamic Profiles with Functionality Maps of the hsp90 Binding Site to Predict the Displacement of Water Molecules J. Chem. Inf. Model. 2013, 53, 2571-2586
39. Miranker, A.; Karplus, M. Functionality Maps of Binding Sites: A Multiple Copy Simultaneous Search Method Proteins 1991, 11, 29-34
40. Ladbury, J. E.; Klebe, G.; Freire, E. Adding Calorimetric Data to Decision Making in Lead Discovery: A Hot Tip Nat. Rev. Drug Discovery 2010, 9, 23-27
41. 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
42. Hann, M. M.; Keserü, G. M. Finding the Sweet Spot: The Role of Nature and Nurture in Medicinal Chemistry Nat. Rev. Drug Discovery 2012, 11, 355-365
43. Lakkaraju, S.; Raman, E.; Yu, W., Jr A. D. M. Sampling of Organic Solutes in Aqueous and Heterogeneous Environments Using Oscillating Excess Chemical Potentials in Grand Canonical-Like Monte Carlo-Molecular Dynamics Simulations J. Chem. Theory Comput. 2014, 10, 2281-2290