A GRID-derived water network stabilizes molecular dynamics computer simulations of a protease

Journal of Chemical Information and Modeling

Volumn 51, Issue 11, 2011, Pages 2860-2867

  Wallnoefer, Hannes G ^a,b   Liedl, Klaus R ^b   Fox, Thomas ^a  

^a BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

^b UNIVERSITY OF INNSBRUCK   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

MOLECULAR DYNAMICS; MOLECULES; PROTEINS;

BLOOD COAGULATION; CLUSTERING APPROACH; EFFECT OF WATER; MOLECULAR DYNAMICS COMPUTER SIMULATIONS; MOLECULAR INTERACTION FIELDS; PROTEIN STRUCTURES; STRUCTURAL DISTORTIONS; STRUCTURAL WATER;

X RAYS;

BLOOD CLOTTING FACTOR 10A; WATER;

ALGORITHM; ARTICLE; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER PROGRAM; HUMAN; METABOLISM; METHODOLOGY; MOLECULAR DYNAMICS; PROTEIN BINDING; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

ALGORITHMS; COMPUTATIONAL BIOLOGY; CRYSTALLOGRAPHY, X-RAY; FACTOR XA; HUMANS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; SOFTWARE; THERMODYNAMICS; WATER;

EID: 82355160789     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci200138u     Document Type: Article

References (94)

1. Wallnoefer, H. G.; Fox, T.; Liedl, K. R. Challenges for Computer Simulations in Drug Design. In Challenges and Advances in Computational Chemistry and Physics; Kinetics and Dynamics; Springer: New York, 2010; Vol. 12, pp 431-463.
2. Jacobs, D. J. Ensemble-based methods for describing protein dynamics Curr. Opin. Pharmacol. 2010, 10, 760-769
3. McGeagh, J. D.; Ranaghan, K. E.; Mulholland, A. J. Protein dynamics and enzyme catalysis: Insights from simulations Biochim. Biophys. Acta, Proteins Proteomics 2011, 1814, 1077-1092
4. Gallicchio, E.; Levy, R. M. Advances in all atom sampling methods for modeling protein-ligand binding affinities Curr. Opin. Struct. Biol. 2011, 21, 161-166
5. Lin, J.-H. Accommodating protein flexibility for structure-based drug design Curr. Top. Med. Chem. 2011, 11, 171-178
6. Grienke, U.; Schmidtke, M.; Kirchmair, J.; Pfarr, K.; Wutzler, P.; Dürrwald, R.; Wolber, G.; Liedl, K. R.; Stuppner, H.; Rollinger, J. M. Antiviral Potential and Molecular Insight into Neuraminidase Inhibiting Diarylheptanoids from Alpinia katsumadai J. Med. Chem. 2010, 53, 778-786
7. Wallnoefer, H. G.; Lingott, T.; Gutiérrez, J. M.; Merfort, I.; Liedl, K. R. Backbone Flexibility Controls the Activity and Specificity of a Protein-Protein Interface: Specificity in Snake Venom Metalloproteases J. Am. Chem. Soc. 2010, 132, 10330-10337
8. Reboul, C. F.; Andrews, D. A.; Nahar, M. F.; Buckle, A. M.; Roujeinikova, A. Crystallographic and molecular dynamics analysis of loop motions unmasking the peptidoglycan-binding site in stator protein MotB of flagellar motor PLoS ONE 2011, 6, e18981
9. Schmidt, R. K.; Gready, J. E. Molecular Dynamics Simulations of L-Lactate Dehydrogenase: Conformation of a Mobile Loop and Influence of the Tetrameric Protein Environment J. Mol. Model. 1999, 5, 153-168 (Pubitemid 129699254)
10. Kamerlin, S. C. L.; Rucker, R.; Boresch, S. A targeted molecular dynamics study of WPD loop movement in PTP1B Biochem. Biophys. Res. Commun. 2006, 345, 1161-1166 (Pubitemid 43776499)
11. Hu, C.; Fang, J.; Borchardt, R. T.; Schowen, R. L.; Kuczera, K. Molecular dynamics simulations of domain motions of substrate-free S-adenosyl- L-homocysteine hydrolase in solution Proteins 2008, 71, 131-143 (Pubitemid 351358597)
12. Kleinekathöfer, U.; Isralewitz, B.; Dittrich, M.; Schulten, K. Domain Motion of Individual F1-ATPase β-Subunits during Unbiased Molecular Dynamics Simulations J. Phys. Chem. A 2011, 115, 7267-7274
13. Wallnoefer, H. G.; Fox, T.; Liedl, K. R.; Tautermann, C. S. Dispersion dominated halogen-π interactions: energies and locations of minima Phys. Chem. Chem. Phys. 2010, 12, 14941
14. Wallnoefer, H. G.; Handschuh, S.; Liedl, K. R.; Fox, T. Stabilizing of a Globular Protein by a Highly Complex Water Network: A Molecular Dynamics Simulation Study on Factor Xa J. Phys. Chem. B 2010, 114, 7405-7412
15. Pikkemaat, M. G.; Linssen, A. B. M.; Berendsen, H. J. C.; Janssen, D. B. Molecular dynamics simulations as a tool for improving protein stability Protein Eng. 2002, 15, 185-192 (Pubitemid 34429229)
16. Palma, R.; Curmi, P. M. Computational studies on mutant protein stability: The correlation between surface thermal expansion and protein stability Protein Sci. 1999, 8, 913-920 (Pubitemid 29165422)
17. Winger, M.; Van Gunsteren, W. F. Use of Molecular-Dynamics Simulation for Optimizing Protein Stability: Consensus-Designed Ankyrin Repeat Proteins Helv. Chim. Acta 2008, 91, 1605-1613
18. Wallnoefer, H. G.; Liedl, K. R.; Fox, T. A challenging system: Free energy prediction for factor Xa J. Comput. Chem. 2011, 32, 1743-1752
19. Kollman, P. Free energy calculations: Applications to chemical and biochemical phenomena Chem. Rev. 1993, 93, 2395-2417
20. Lee, M. S.; Olson, M. A. Calculation of Absolute Protein-Ligand Binding Affinity Using Path and Endpoint Approaches Biophys. J. 2006, 90, 864-877
21. Huang, N.; Jacobson, M. P. Physics-based methods for studying protein-ligand interactions Curr. Opin. Drug Discovery Dev. 2007, 10, 325-331 (Pubitemid 46800226)
22. Gilson, M. K.; Zhou, H. X. Calculation of Protein-Ligand Binding Affinities Annu. Rev. Biophys. Biomol. Struct. 2007, 36, 21
23. Foloppe, N.; Hubbard, R. E. Towards predictive ligand design with free-energy based computational methods Curr. Med. Chem. 2006, 13, 3583-3608 (Pubitemid 44873749)
24. Sreenivasan, U.; Axelsen, P. H. Buried water in homologous serine proteases Biochemistry 1992, 31, 12785-12791 (Pubitemid 23027058)
25. Guvench, O.; Price, D. J.; Brooks, C. L., III Receptor rigidity and ligand mobility in trypsin-ligand complexes Proteins 2005, 58, 407-417 (Pubitemid 40076054)
26. Lesk, A. M.; Fordham, W. D. Conservation and Variability in the Structures of Serine Proteinases of the Chymotrypsin Family J. Mol. Biol. 1996, 258, 501-537 (Pubitemid 26145896)
27. Sanschagrin, P. C.; Kuhn, L. A. Cluster analysis of consensus water sites in thrombin and trypsin shows conservation between serine proteases and contributions to ligand specificity Protein Sci. 1998, 7, 2054-2064 (Pubitemid 28495792)
28. Zhang, X. J.; Matthews, B. W. Conservation of solvent-binding sites in 10 crystal forms of T4 lysozyme Protein Sci. 1994, 3, 1031-1039 (Pubitemid 24209895)
29. Reichmann, D.; Phillip, Y.; Carmi, A.; Schreiber, G. On the Contribution of Water-Mediated Interactions to Protein-Complex Stability Biochemistry 2008, 47, 1051-1060
30. Nilsson, M.; Hämäläinen, M.; Ivarsson, M.; Gottfries, J.; Xue, Y.; Hansson, S.; Isaksson, R.; Fex, T. Compounds binding to the S2-S3 pockets of thrombin J. Med. Chem. 2009, 52, 2708-2715
31. Edsall, J. T.; McKenzie, H. A. Water and proteins. II. The location and dynamics of water in protein systems and its relation to their stability and properties Adv. Biophys. 1983, 16, 53-183
32. Cruz, A.; Ramirez, E.; Santana, A.; Barletta, G.; López, G. E. Molecular dynamic study of subtilisin Carlsberg in aqueous and nonaqueous solvents Mol. Simul. 2009, 35, 205-212
33. Maxwell, M. K.; Enrico, D. C. Conserved water molecules in the specificity pocket of serine proteases and the molecular mechanism of Na+ binding Proteins 1998, 30, 34-42
34. Meyer, E.; Cole, G.; Radhakrishman, R.; Epp, O. Structure of native porcine pancreatic elastase at 1.65 angstrom resolution Acta Cryst., Sect. B 1988, 44, 26-38
35. Silva, J.; Antunes, O. A. C.; de Alencastro, R. B.; De Simone, S. G. The Na+ binding channel of human coagulation proteases: Novel insights on the structure and allosteric modulation revealed by molecular surface analysis Biophys. Chem. 2006, 119, 282-294 (Pubitemid 43204504)
36. Caldwell, R. A.; Boucher, R. C.; Stutts, M. J. Serine protease activation of near-silent epithelial Na+ channels Am. J. Physiol. Cell. Physiol. 2004, 286, C190-C194
37. Carugo, O.; Bordo, D. How many water molecules can be detected by protein crystallography? Acta Cryst., Sect. D 1999, 55, 479-483 (Pubitemid 29083721)
38. Rao, M. S.; Olson, A. J. Modelling of Factor Xa-inhibitor complexes: A computational flexible docking approach Proteins 1999, 34, 173-183 (Pubitemid 29028803)
39. Verdonk, M. L.; Chessari, G.; Cole, J. C.; Hartshorn, M. J.; Murray, C. W.; Nissink, J. W.; Taylor, R. D.; Taylor, R. Modeling Water Molecules in Protein-Ligand Docking Using GOLD J. Med. Chem. 2005, 48, 6504-6515 (Pubitemid 41429002)
40. Doan, B. T.; Fraternali, F.; Do, Q. T.; Atkinson, R. A.; Palmas, P.; Sklenar, V.; Wildgoose, P.; Strop, P.; Saudek, V. A NMR and MD study of the active site of factor Xa by selective inhibitors J. Chim. Phys. Phys.-Chim. Biol. 1998, 95, 443-446 (Pubitemid 29133632)
41. Fraternali, F.; Do, Q. T.; Doan, B. T.; Atkinson, R. A.; Palmas, P.; Sklenar, V.; Safar, P.; Wildgoose, P.; Strop, P.; Saudek, V. Mapping the active site of factor Xa by selective inhibitors: An NMR and MD study Proteins 1998, 30, 264-274 (Pubitemid 28106861)
42. Shokhen, M.; Khazanov, N.; Albeck, A. Screening of the active site from water by the incoming ligand triggers catalysis and inhibition in serine proteases Proteins 2008, 70, 1578-1587 (Pubitemid 351304114)
43. Borensztajn, K.; Peppelenbosch, M. P.; Spek, C. A. Factor Xa: at the crossroads between coagulation and signaling in physiology and disease Trends Mol. Med. 2008, 14, 429-440
44. Bounameaux, H. The novel anticoagulants: Entering a new era Swiss Med. Wkly. 2009, 139, 60-64
45. Ieko, M.; Tarumi, T.; Nakabayashi, T.; Yoshida, M.; Naito, S.; Koike, T. Factor Xa inhibitors: New anti-thrombotic agents and their characteristics Front. Biosci. 2006, 11, 232-248 (Pubitemid 43253489)
46. McVey, J. H. Tissue factor pathway Bailliere's Clin. Haem. 1994, 7, 469-484 (Pubitemid 24296875)
47. Broze, J. Tissue factor pathway inhibitor and the current concept of blood coagulation Blood Coagulation Fibrinolysis 1995, 6, S1
48. Davie, E. W.; Fujikawa, K.; Kisiel, W. The coagulation cascade: initiation, maintenance, and regulation Biochemistry 1991, 30, 10363-10370
49. Hauptmann, J.; Markwardt, F.; Walsmann, P. Synthetic inhibitors of serine proteinases. XIV. Influence of 3- and 4-amidinobenzyl derivatives on the formation and action of thrombin Thromb. Res. 1978, 12, 735-744 (Pubitemid 8378097)
50. Hertzberg, M. Biochemistry of factor X Blood Rev. 1994, 8, 56-62
51. Stubbs, M. T.; Bode, W. Coagulation factors and their inhibitors Curr. Opin. Struct. Biol. 1994, 4, 823-832
52. Tidwell, R. R.; Webster, W. P.; Shaver, S. R.; Geratz, J. D. Strategies for anticoagulation with synthetic protease inhibitors. Xa inhibitors versus thrombin inhibitors Thromb. Res. 1980, 19, 339-349 (Pubitemid 10029564)
53. Warshel, A.; Naray-Szabo, G.; Sussman, F.; Hwang, J. K. How do serine proteases really work? Biochemistry 2011, 28, 3629-3637
54. Hedstrom, L. How do serine proteases really work? Chem. Rev. 2002, 102, 4501-4524
55. Kaiser, B. DX-9065a, a direct inhibitor of factor Xa Cardiovasc. Drug Rev. 2003, 21, 91-104 (Pubitemid 36935488)
56. Nazaré, M.; Will, D. W.; Matter, H.; Schreuder, H.; Ritter, K.; Urmann, M.; Essrich, M.; Bauer, A.; Wagner, M.; Czech, J.; Lorenz, M.; Laux, V.; Wehner, V. Probing the Subpockets of Factor Xa Reveals Two Binding Modes for Inhibitors Based on a 2-Carboxyindole Scaffold: A Study Combining Structure-Activity Relationship and X-ray Crystallography J. Med. Chem. 2005, 48, 4511-4525 (Pubitemid 40993413)
57. 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 (Pubitemid 351416242)
58. Daura, X.; Haaksma, E.; van Gunsteren, W. F. Factor Xa: simulation studies with an eye to inhibitor design J. Comput.-Aided Mol. Des. 2000, 14, 507-529 (Pubitemid 30445056)
59. Ostrovsky, D.; Udier-Blagovic, M.; Jorgensen, W. L. Analyses of Activity for Factor Xa Inhibitors Based on Monte Carlo Simulations J. Med. Chem. 2003, 46, 5691-5699 (Pubitemid 37543319)
60. Singh, N.; Briggs, J. M. Molecular Dynamics Simulations of Factor Xa: Insights into Conformational Transition of Its Binding Subsites Biopolymers 2008, 89, 1104-1113
61. Venkateswarlu, D.; Perera, L.; Darden, T.; Pedersen, L. G. Structure and dynamics of zymogen human blood coagulation factor X Biophys. J. 2002, 82, 1190-1206 (Pubitemid 34204743)
62. Berman, H. M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T. N.; Weissig, H.; Shindyalov, I. N.; Bourne, P. E. The Protein Data Bank Nucleic Acids Res. 2000, 28, 235-242 (Pubitemid 30047768)
63. Golbraikh, A.; Tropsha, A. Predictive QSAR modeling based on diversity sampling of experimental datasets for the training and test set selection J. Comput.-Aided Mol. Des. 2002, 16, 357-369 (Pubitemid 35414668)
64. Goodford, P. J. A computational procedure for determining energetically favorable binding sites on biologically important macromolecules J. Med. Chem. 1985, 28, 849-857 (Pubitemid 15012490)
65. Carosati, E.; Sciabola, S.; Cruciani, G. Hydrogen Bonding Interactions of Covalently Bonded Fluorine Atoms: From Crystallographic Data to a New Angular Function in the GRID Force Field J. Med. Chem. 2004, 47, 5114-5125 (Pubitemid 39314909)
66. Helms, V.; Wade, R. C. Thermodynamics of a Water Mediating Protein-Ligand Interactions in Cytochrome P450cam: A Molecular Dynamics Study Biophys. J. 1995, 69, 810-824
67. Wade, R. C. Solvation of the active site of cytochrome P450-cam J. Comput.-Aided Mol. Des. 1990, 4, 199-204
68. Henchman, R. H.; McCammon, J. A. Structural and Dynamic Properties of Water around Acetylcholinesterase Protein Sci. 2002, 11, 2080-2090 (Pubitemid 34919612)
69. Olkhova, E.; Hutter, M. C.; Lill, M. A.; Helms, V.; Michel, H. Dynamic Water Networks in Cytochrome c Oxidase from Paracoccus denitrificans Investigated by Molecular Dynamics Simulations Biophys. J. 2004, 86, 1873-1889 (Pubitemid 38524385)
70. Schymkowitz, J. W. H.; Rousseau, F.; Martins, I. C.; Ferkinghoff-Borg, J.; Stricher, F.; Serrano, L. Prediction of water and metal binding sites and their affinities by using the Fold-X force field Proc. Natl. Acad. Soc. U.S.A. 2005, 102, 10147-10152 (Pubitemid 41023340)
71. Schymkowitz, J.; Borg, J.; Stricher, F.; Nys, R.; Rousseau, F.; Serrano, L. The FoldX web server: an online force field Nucleic Acids Res. 2005, 33, W382-388
72. Verdonk, M. L.; Cole, J. C.; Watson, P.; Gillet, V.; Willett, P. SuperStar: Improved knowledge-based interaction fields for protein binding sites J. Mol. Biol. 2001, 307, 841-859 (Pubitemid 33027663)
73. Verdonk, M. L.; Cole, J. C.; Taylor, R. SuperStar: A Knowledge-based Approach for Identifying Interaction Sites in Proteins J. Mol. Biol. 1999, 289, 1093-1108 (Pubitemid 29306672)
74. Henchman, R. H.; Tai, K. S.; Shen, T. Y.; McCammon, J. A. Properties of water molecules in the active site gorge of acetylcholinesterase from computer simulation Biophys. J. 2002, 82, 2671-2682 (Pubitemid 34441305)
75. Lounnas, V.; Pettitt, B. M. A connected cluster of hydration around Myoglobin-correlation between molecular dynamics simulations and experiment Proteins 1994, 18, 133-147 (Pubitemid 24055076)
76. Henchman, R. H.; McCammon, J. A. Extracting hydration sites around proteins from explicit water simulations J. Comput. Chem. 2002, 23, 861-869 (Pubitemid 34630529)
77. Li, Z.; Lazaridis, T. Thermodynamics of buried water clusters at a protein-ligand binding interface J. Phys. Chem. B 2006, 110, 1464-1475
78. Li, Z.; Lazaridis, T. Water at biomolecular binding interfaces Phys. Chem. Chem. Phys. 2007, 9, 573-581
79. Li, Z.; Lazaridis, T. Thermodynamic Contributions of the Ordered Water Molecule in HIV-1 Protease J. Am. Chem. Soc. 2003, 125, 6636-6637 (Pubitemid 36667440)
80. Li, Z.; Lazaridis, T. The Effect of Water Displacement on Binding Thermodynamics: Concanavalin A J. Phys. Chem. B 2004, 109, 662-670 (Pubitemid 40121013)
81. Guimarães, C. R. W.; Mathiowetz, A. M. Addressing Limitations with the MM-GB/SA Scoring Procedure using the WaterMap Method and Free Energy Perturbation Calculations J. Chem. Inf. Model. 2011, 50, 547-559
82. 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 ChemMedChem 2011, 6, 1049-1066
83. 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
84. Zwanzig, R. W. High-Temperature Equation of State by a Perturbation Method. I. Nonpolar Gases J. Chem. Phys. 1954, 22, 1420-1426
85. 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. Theor. Comput. 2011, 6, 3850-3856
86. Bui, H. H.; Schiewe, A. J.; Haworth, I. S. WATGEN: An algorithm for modeling water networks at protein-protein interfaces J. Comput. Chem. 2007, 28, 2241-2251 (Pubitemid 47389138)
87. 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
88. Underwood, M. C.; Zhong, D.; Mathur, A.; Heyduk, T.; Bajaj, S. P. Thermodynamic Linkage between the S1 Site, the Na+ Site, and the Ca2+ Site in the Protease Domain of Human Coagulation Factor Xa J. Biol. Chem. 2000, 275, 36876-36884
89. Griffon, N.; Di Stasio, E. Thermodynamics of Na+ binding to coagulation serine proteases Biophys. Chem. 2001, 90, 89-96 (Pubitemid 32178113)
90. Labute, P. Protonate3D: Assignment of ionization states and hydrogen coordinates to macromolecular structures Proteins 2009, 75, 187-205
91. Case, D. A.; Darden, T. E.; Cheatham, T. E.; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Crowley, M.; Walker, R. C.; Zhang, W.; Merz, K. M.; Wang, B.; Hayik, S.; Roitberg, A.; Seabra, G.; Kolossvary, I.; Wong, K. F.; Paesani, F.; Vanicek, J.; Wu, X.; Brozell, S. R.; Steinbrecher, T.; Gohlke, H.; Yang, L.; Mongan, J.; Hornak, G.; Cui, G.; Mathews, D. H.; Seetin, M. G.; Sagui, C.; Babin, V.; Kollman, P. A. AMBER 10; University of California: San Francisco, CA, 2008.
92. Bradbook, G. M.; Gleichmann, T.; Harrop, S. J.; Habash, J.; Raftery, J.; Kalb, J.; Yariv, J.; Hillier, I. H.; Helliwell, J. R. X-Ray and molecular dynamics studies of concanavalin-A glucoside and mannoside complexes relating structure to thermodynamics of binding J. Chem. Soc. Faraday Trans. 1998, 94, 1603-1611 (Pubitemid 128760331)
93. 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
94. 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 2006, 65, 712-725 (Pubitemid 44583220)