Evaluating Free Energies of Binding and Conservation of Crystallographic Waters Using SZMAP

Journal of Chemical Information and Modeling

Volumn 55, Issue 8, 2015, Pages 1552-1565

  Bayden, Alexander S ^a,b   Moustakas, Demetri T ^a,c   Joseph McCarthy, Diane ^a,b   Lamb, Michelle L ^a  

^a ASTRAZENECA   (United Kingdom)

^b ASB: CMD Bioscience Inc ^*  (United States)

^c Alkermes   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEXATION; CRYSTAL STRUCTURE; CRYSTALS; ENTROPY; FREE ENERGY; MOLECULES; PROTEINS; WATER CONSERVATION;

BINDING FREE ENERGY; DEGREE OF CORRELATIONS; ENTROPY DIFFERENCES; MEDIATED INTERACTION; PROTEIN-LIGAND COMPLEXES; SCIENTIFIC SOFTWARES; THERMODYNAMIC INTEGRATION; X RAY CRYSTAL STRUCTURES;

BINDING ENERGY;

BACTERIAL PROTEIN; CARRIER PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE; LIGAND; LIPOPROTEIN; OLIGOPEPTIDE-BINDING PROTEIN, BACTERIA; P16 PROTEASE, HUMAN IMMUNODEFICIENCY VIRUS 1; PROTEIN; PROTEIN BINDING; WATER;

BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER PROGRAM; HUMAN IMMUNODEFICIENCY VIRUS 1; PROTEIN DATABASE; SALMONELLA ENTERICA; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

BACTERIAL PROTEINS; BINDING SITES; CARRIER PROTEINS; CRYSTALLOGRAPHY, X-RAY; DATABASES, PROTEIN; HIV PROTEASE; HIV-1; LIGANDS; LIPOPROTEINS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEINS; SALMONELLA ENTERICA; SOFTWARE; THERMODYNAMICS; WATER;

EID: 84940189864     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci500746d     Document Type: Article

References (75)

1. SZMAP, 1.0.0; OpenEye Scientific Software Inc.: Santa Fe, NM, USA, 2011
2. SZMAP, 1.0.0; OpenEye Scientific Software Inc.: Santa Fe, NM, USA, 2011.
3. Fernández, A. Epistructural Tension Promotes Protein Associations Phys. Rev. Lett. 2012, 108, 188102 10.1103/PhysRevLett.108.188102
4. Meiering, E. M.; Wagner, G. Detection of Long-Lived Bound Water Molecules in Complexes of Human Dihydrofolate Reductase with Methotrexate and NADPH J. Mol. Biol. 1995, 247, 294-308 10.1006/jmbi.1994.0140
5. Goodford, P. J. A Computational Procedure for Determining Energetically Favorable Binding Sites on Biologically Important Macromolecules J. Med. Chem. 1985, 28, 849-857 10.1021/jm00145a002
6. Miranker, A.; Karplus, M. Functionality Maps of Binding Sites: A Multiple Copy Simultaneous Search Method Proteins: Struct., Funct., Bioinf. 1991, 11, 29-34 10.1002/prot.340110104
7. Evensen, E.; Joseph-McCarthy, D.; Weiss, G. A.; Schreiber, S. L.; Karplus, M. Ligand Design by a Combinatorial Approach Based on Modeling and Experiment: Application to HLA-DR4 J. Comput.-Aided Mol. Des. 2007, 21, 395-418 10.1007/s10822-007-9119-x
8. Bitetti-Putzer, R.; Joseph-McCarthy, D.; Hogle, J. M.; Karplus, M. Functional Group Placement in Protein Binding Sites: A Comparison of GRID and MCSS J. Comput.-Aided Mol. Des. 2001, 15, 935-960 10.1023/A:1014309222984
9. Joseph-McCarthy, D.; Fedorov, A. A.; Almo, S. C. Comparison of Experimental and Computational Functional Group Mapping of an RNase A Structure: Implications for Computer-Aided Drug Design Protein Eng., Des. Sel. 1996, 9, 773-780 10.1093/protein/9.9.773
10. 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 10.1021/ci200138u
11. Lensink, M. F.; Moal, I. H.; Bates, P. A.; Kastritis, P. L.; Melquiond, A. S. J.; Karaca, E.; Schmitz, C.; van Dijk, M.; Bonvin, A. M. J. J.; Eisenstein, M.; Jiménez-García, B.; Grosdidier, S.; Solernou, A.; Pérez-Cano, L.; Pallara, C.; Fernández-Recio, J.; Xu, J.; Muthu, P.; Praneeth Kilambi, K.; Gray, J. J.; Grudinin, S.; Derevyanko, G.; Mitchell, J. C.; Wieting, J.; Kanamori, E.; Tsuchiya, Y.; Murakami, Y.; Sarmiento, J.; Standley, D. M.; Shirota, M.; Kinoshita, K.; Nakamura, H.; Chavent, M.; Ritchie, D. W.; Park, H.; Ko, J.; Lee, H.; Seok, C.; Shen, Y.; Kozakov, D.; Vajda, S.; Kundrotas, P. J.; Vakser, I. A.; Pierce, B. G.; Hwang, H.; Vreven, T.; Weng, Z.; Buch, I.; Farkash, E.; Wolfson, H. J.; Zacharias, M.; Qin, S.; Zhou, H.; Huang, S.; Zou, X.; Wojdyla, J. A.; Kleanthous, C.; Wodak, S. J. Blind Prediction of Interfacial Water Positions in CAPRI Proteins: Struct., Funct., Bioinf. 2014, 82, 620-632 10.1002/prot.24439
12. Raymer, M. L.; Sanschagrin, P. C.; Punch, W. F.; Venkataraman, S.; Goodman, E. D.; Kuhn, L. A. Predicting Conserved Water-Mediated and Polar Ligand Interactions in Proteins using a K-Nearest-Neighbors Genetic Algorithm J. Mol. Biol. 1997, 265, 445-464 10.1006/jmbi.1996.0746
13. Garcia-Sosa, A. T.; Mancera, R. L.; Dean, P. M. WaterScore: A Novel Method for Distinguishing between Bound and Displaceable Water Molecules in the Crystal Structure of the Binding Site of Protein-Ligand Complexes J. Mol. Model. 2003, 9, 172-182 10.1007/s00894-003-0129-x
14. Rossato, G.; Ernst, B.; Vedani, A.; Smieško, M. AcquaAlta: A Directional Approach to the Solvation of Ligand-Protein Complexes J. Chem. Inf. Model. 2011, 51, 1867-1881 10.1021/ci200150p
15. Allen, F. The Cambridge Structural Database: A Quarter of a Million Crystal Structures and Rising Acta Crystallogr., Sect. B: Struct. Sci. 2002, 58, 380-388 10.1107/S0108768102003890
16. Kellogg, G. E.; Abraham, D. J. Hydrophobicity: Is LogPo/W More than the Sum of its Parts? Eur. J. Med. Chem. 2000, 35, 651-661 10.1016/S0223-5234(00)00167-7
17. Kellogg, G. E.; Chen, D. L. The Importance of being Exhaustive. Optimization of Bridging Structural Water Molecules and Water Networks in Models of Biological Systems Chem. Biodiversity 2004, 1, 98-105 10.1002/cbdv.200490016
18. Amadasi, A.; Spyrakis, F.; Cozzini, P.; Abraham, D. J.; Kellogg, G. E.; Mozzarelli, A. Mapping the Energetics of Water-Protein and Water-Ligand Interactions with the "Natural" HINT Forcefield: Predictive Tools for Characterizing the Roles of Water in Biomolecules J. Mol. Biol. 2006, 358, 289-309 10.1016/j.jmb.2006.01.053
19. Amadasi, A.; Surface, J. A.; Spyrakis, F.; Cozzini, P.; Mozzarelli, A.; Kellogg, G. E. Robust Classification of "Relevant" Water Molecules in Putative Protein Binding Sites J. Med. Chem. 2008, 51, 1063-1067 10.1021/jm701023h
20. Bayden, A.; Fornabaio, M.; Scarsdale, J.; Kellogg, G. Web Application for Studying the Free Energy of Binding and Protonation States of Protein-ligand Complexes Based on HINT J. Comput.-Aided Mol. Des. 2009, 23, 621-632 10.1007/s10822-009-9270-7
21. 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 10.1371/journal.pone.0032036
22. 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 10.1002/jcc.21334
23. Grochowski, P.; Trylska, J. Continuum Molecular Electrostatics, Salt Effects, and Counterion Binding - A Review of the Poisson-Boltzmann Theory and its Modifications Biopolymers 2008, 89, 93-113 10.1002/bip.20877
24. Baker, N. A. Improving Implicit Solvent Simulations: A Poisson-Centric View Curr. Opin. Struct. Biol. 2005, 15, 137-143 10.1016/j.sbi.2005.02.001
25. Kleinjung, J.; Fraternali, F. Design and Application of Implicit Solvent Models in Biomolecular Simulations Curr. Opin. Struct. Biol. 2014, 25, 126-134 10.1016/j.sbi.2014.04.003
26. Friesner, R. A.; Abel, R.; Goldfeld, D. A.; Miller, E. B.; Murrett, C. S. Computational Methods for High Resolution Prediction and Refinement of Protein Structures Curr. Opin. Struct. Biol. 2013, 23, 177-184 10.1016/j.sbi.2013.01.010
27. Chen, J.; Brooks, C. L., III; Khandogin, J. Recent Advances in Implicit Solvent-Based Methods for Biomolecular Simulations Curr. Opin. Struct. Biol. 2008, 18, 140-148 10.1016/j.sbi.2008.01.003
28. Bashford, D.; Case, D. A. Generalized Born Models of Macromolecular Solvation Effects Annu. Rev. Phys. Chem. 2000, 51, 129-152 10.1146/annurev.physchem.51.1.129
29. Beglov, D.; Roux, B. An Integral Equation to Describe the Solvation of Polar Molecules in Liquid Water J. Phys. Chem. B 1997, 101, 7821-7826 10.1021/jp971083h
30. Chandler, D.; McCoy, J. D.; Singer, S. J. Density Functional Theory of Nonuniform Polyatomic Systems. I. General Formulation J. Chem. Phys. 1986, 85, 5971-5976 10.1063/1.451510
31. Sindhikara, D. J.; Hirata, F. Analysis of Biomolecular Solvation Sites by 3D-RISM Theory J. Phys. Chem. B 2013, 117, 6718-6723 10.1021/jp4046116
32. Molecular Operating Environment (MOE); Chemical Computing Group Inc.: Montreal, QC, Canada, 2010.
33. Hornak, V.; Abel, R.; Okur, A.; Strockbine, B.; Roitberg, A.; Simmerling, C. Comparison of Multiple Amber Force Fields and Development of Improved Protein Backbone Parameters Proteins: Struct., Funct., Bioinf. 2006, 65, 712-725 10.1002/prot.21123
34. 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 10.1002/jcc.20035
35. Luchko, T.; Gusarov, S.; Roe, D. R.; Simmerling, C.; Case, D. A.; Tuszynski, J.; Kovalenko, A. Three-Dimensional Molecular Theory of Solvation Coupled with Molecular Dynamics in Amber J. Chem. Theory Comput. 2010, 6, 607-624 10.1021/ct900460m
36. Huggins, D. J. Application of Inhomogeneous Fluid Solvation Theory to Model the Distribution and Thermodynamics of Water Molecules Around Biomolecules Phys. Chem. Chem. Phys. 2012, 14, 15106-15117 10.1039/c2cp42631e
37. Huggins, D. J. Benchmarking the Thermodynamic Analysis of Water Molecules Around a Model Beta Sheet J. Comput. Chem. 2012, 33, 1383-1392 10.1002/jcc.22971
38. Cui, G.; Swails, J. M.; Manas, E. S. SPAM: A Simple Approach for Profiling Bound Water Molecules J. Chem. Theory Comput. 2013, 9, 5539-5549 10.1021/ct400711g
39. 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 p38α MAP Kinase Inhibitors Proteins: Struct., Funct., Bioinf. 2013, 81, 1509-1526 10.1002/prot.24276
40. 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 10.1517/17460441.2013.749853
41. 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 10.1021/ja0771033
42. Beuming, T.; Che, Y.; Abel, R.; Kim, B.; Shanmugasundaram, V.; Sherman, W. Thermodynamic Analysis of Water Molecules at the Surface of Proteins and Applications to Binding Site Prediction and Characterization Proteins: Struct., Funct., Bioinf. 2012, 80, 871-883 10.1002/prot.23244
43. 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 10.1021/ja066980q
44. 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 10.1021/jp9047456
45. Grant, J. A.; Pickup, B. T.; Nicholls, A. A Smooth Permittivity Function for Poisson-Boltzmann Solvation Methods J. Comput. Chem. 2001, 22, 608-640 10.1002/jcc.1032.abs
46. Mason, J. S.; Bortolato, A.; Congreve, M.; Marshall, F. H. New Insights from Structural Biology into the Druggability of G Protein-Coupled Receptors Trends Pharmacol. Sci. 2012, 33, 249-260 10.1016/j.tips.2012.02.005
47. Bortolato, A.; Tehan, B. G.; Bodnarchuk, M. S.; Essex, J. W.; Mason, J. S. Water Network Perturbation in Ligand Binding: Adenosine A2A Antagonists as a Case Study J. Chem. Inf. Model. 2013, 53, 1700-1713 10.1021/ci4001458
48. Efstathiou, A.; Gaboriaud-Kolar, N.; Smirlis, D.; Myrianthopoulos, V.; Vougogiannopoulou, K.; Alexandratos, A.; Kritsanida, M.; Mikros, E.; Soteriadou, K.; Skaltsounis, A. An Inhibitor-Driven Study for Enhancing the Selectivity of Indirubin Derivatives Towards Leishmanial Glycogen Synthase Kinase-3 Over Leishmanial Cdc2-Related Protein Kinase 3 Parasites Vectors 2014, 7, 234 10.1186/1756-3305-7-234
49. Maestro, 9.2; Schrödinger LLC: New York, NY, 2011.
50. Prime, 3.0; Schrödinger LLC: New York, NY, 2011.
51. Jacobson, M. P.; Friesner, R. A.; Xiang, Z.; Honig, B. On the Role of the Crystal Environment in Determining Protein Side-Chain Conformations J. Mol. Biol. 2002, 320, 597-608 10.1016/S0022-2836(02)00470-9
52. Labute, P. Protonate3D: Assignment of Ionization States and Hydrogen Coordinates to Macromolecular Structures Proteins: Struct., Funct., Bioinf. 2009, 75, 187-205 10.1002/prot.22234
53. Zheng, Y.; Bruice, T. C. Role of a Critical Water in Scytalone Dehydratase-Catalyzed Reaction Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 4158-4163 10.1073/pnas.95.8.4158
54. Trylska, J.; Antosiewicz, J.; Geller, M.; Hodge, C. N.; Klabe, R. M.; Head, M. S.; Gilson, M. K. Thermodynamic Linkage between the Binding of Protons and Inhibitors to HIV-1 Protease Protein Sci. 1999, 8, 180-195 10.1110/ps.8.1.180
55. Yamazaki, T.; Nicholson, L. K.; Wingfield, P.; Stahl, S. J.; Kaufman, J. D.; Eyermann, C. J.; Hodge, C. N.; Lam, P. Y. S.; Torchia, D. A. NMR and X-Ray Evidence that the HIV Protease Catalytic Aspartyl Groups are Protonated in the Complex Formed by the Protease and a Non-Peptide Cyclic Urea-Based Inhibitor J. Am. Chem. Soc. 1994, 116, 10791-10792 10.1021/ja00102a057
56. Wittayanarakul, K.; Hannongbua, S.; Feig, M. Accurate Prediction of Protonation State as a Prerequisite for Reliable MM-PB(GB)SA Binding Free Energy Calculations of HIV-1 Protease Inhibitors J. Comput. Chem. 2008, 29, 673-685 10.1002/jcc.20821
57. Jakalian, A.; Jack, D. B.; Bayly, C. I. Fast, Efficient Generation of High-Quality Atomic Charges. AM1-BCC Model: II. Parameterization and Validation J. Comput. Chem. 2002, 23, 1623-1641 10.1002/jcc.10128
58. Wlodawer, A.; Vondrasek, J. Inhibitors of HIV-1 Protease: A Major Success of Structure-Assisted Drug Design Annu. Rev. Biophys. Biomol. Struct. 1998, 27, 249-284 10.1146/annurev.biophys.27.1.249
59. Hamelberg, D.; McCammon, J. A. Standard Free Energy of Releasing a Localized Water Molecule from the Binding Pockets of Proteins: Double-Decoupling Method J. Am. Chem. Soc. 2004, 126, 7683-7689 10.1021/ja0377908
60. Lu, Y.; Yang, C.; Wang, S. Binding Free Energy Contributions of Interfacial Waters in HIV-1 Protease/Inhibitor Complexes J. Am. Chem. Soc. 2006, 128, 11830-11839 10.1021/ja058042g
61. Chen, J. M.; Xu, S. L.; Wawrzak, Z.; Basarab, G. S.; Jordan, D. B. Structure-Based Design of Potent Inhibitors of Scytalone Dehydratase: Displacement of a Water Molecule from the Active Site Biochemistry 1998, 37, 17735-17744 10.1021/bi981848r
62. Wawrzak, Z.; Sandalova, T.; Steffens, J. J.; Basarab, G. S.; Lundqvist, T.; Lindqvist, Y.; Jordan, D. B. High-Resolution Structures of Scytalone Dehydratase-Inhibitor Complexes Crystallized at Physiological pH Proteins: Struct., Funct., Bioinf. 1999, 35, 425-439 10.1002/(SICI)1097-0134(19990601)35:4<425::AID-PROT6>3.0.CO;2-1
63. Jennings, L. D.; Wawrzak, Z.; Amorose, D.; Schwartz, R. S.; Jordan, D. B. A New Potent Inhibitor of Fungal Melanin Biosynthesis Identified through Combinatorial Chemistry Bioorg. Med. Chem. Lett. 1999, 9, 2509-2514 10.1016/S0960-894X(99)00424-2
64. Spearman, C. The Proof and Measurement of Association between Two Things Am. J. Psychol. 1904, 15, 72-101 10.2307/1412159
65. Reprinted. Int. J. Epidemiol. 2010, 39, 1137-1150.10.1093/ije/dyq191
66. Bland, J. M.; Altman, D. Statistical Methods for Assessing Agreement between Two Methods of Clinical Measurement Lancet 1986, 327, 307-310 10.1016/S0140-6736(86)90837-8
67. Halgren, T. A. Merck Molecular Force Field. II. MMFF94 Van Der Waals and Electrostatic Parameters for Intermolecular Interactions J. Comput. Chem. 1996, 17, 520-552 10.1002/(SICI)1096-987X(199604)17:5/6<520::AID-JCC2>3.0.CO;2-W
68. SZYBKI, 1.8.0.2; OpenEye Scientific Software Inc.: Santa Fe, NM, USA, 2015.
69. Biela, A.; Sielaff, F.; Terwesten, F.; Heine, A.; Steinmetzer, T.; Klebe, G. Ligand Binding Stepwise Disrupts Water Network in Thrombin: Enthalpic and Entropic Changes Reveal Classical Hydrophobic Effect J. Med. Chem. 2012, 55, 6094-6110 10.1021/jm300337q
70. Breiten, B.; Lockett, M. R.; Sherman, W.; Fujita, S.; Al-Sayah, M.; Lange, H.; Bowers, C. M.; Heroux, A.; Krilov, G.; Whitesides, G. M. Water Networks Contribute to Enthalpy/Entropy Compensation in Protein-Ligand Binding J. Am. Chem. Soc. 2013, 135, 15579-15584 10.1021/ja4075776
71. Snyder, P. W.; Mecinovic, J.; Moustakas, D. T.; Thomas, S. W.; Harder, M.; Mack, E. T.; Lockett, M. R.; Héroux, A.; Sherman, W.; Whitesides, G. M. Mechanism of the Hydrophobic Effect in the Biomolecular Recognition of Arylsulfonamides by Carbonic Anhydrase Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 17889-17894 10.1073/pnas.1114107108
72. Nittinger, E.; Schneider, N.; Lange, G.; Rarey, M. Evidence of Water Molecules-A Statistical Evaluation of Water Molecules Based on Electron Density J. Chem. Inf. Model. 2015, 55, 771-783 10.1021/ci500662d
73. Karplus, P. A.; Faerman, C. Ordered Water in Macromolecular Structure Curr. Opin. Struct. Biol. 1994, 4, 770-776 10.1016/S0959-440X(94)90178-3
74. Parthasarathy, S.; Murthy, M. R. N. Analysis of Temperature Factor Distribution in High-Resolution Protein Structures Protein Sci. 1997, 6, 2561-2567 10.1002/pro.5560061208
75. Kuriyan, J.; Karplus, M.; Petsko, G. A. Estimation of Uncertainties in X-Ray Refinement Results by use of Perturbed Structures Proteins: Struct., Funct., Bioinf. 1987, 2, 1-12 10.1002/prot.340020102