Role of desolvation in thermodynamics and kinetics of ligand binding to a kinase

Journal of Chemical Theory and Computation

Volumn 10, Issue 12, 2014, Pages 5696-5705

  Mondal, Jagannath ^a   Friesner, Richard A ^a   Berne, B J ^a  

^a Department of Chemistry Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84916623121     PISSN: 15499618     EISSN: 15499626     Source Type: Journal    
DOI: 10.1021/ct500584n     Document Type: Article

References (48)

1. Shaw, D. E. et al. J. Am. Chem. Soc. 2011, 133, 9181 - 9183
2. Massova, I.; Kollman, P. A. Combined Molecular Mechanical and Continuum Solvent Approach (MM-PBSA/GBSA) to Predict Ligand Binding Perspect. Drug Discovery Des. 2000, 18, 113-135
3. Moble, D.; Dill, K. A. Binding of Small-molecule Ligands to Proteins: "What You See" is Not Always "What you Get" Structure 2009, 17, 489-498
4. Gilson, M. K.; Zhou, H. X. Calculation of Protein-Ligand Binding Affinities Annu. Rev. Biophys. Biomol. Struct. 2007, 36, 21-42
5. Guvench, O.; MacKerell, A. D. J. Computational Evaluation of Protein-small molecule Binding Curr. Opin. Struct. Biol. 2009, 19, 56-61
6. Copeland, R. A.; Pompliano, D. L.; Meek, T. A. Drug-target Residence Time and its Implications for Lead Optimization Nat. Rev. Drug Discovery 2006, 5, 730-739
7. 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
8. 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
9. Baron, R.; Setny, P.; McCammon, J. A. Water in Cavity-Ligand Recognition J. Am. Chem. Soc. 2010, 132, 12091-12097
10. Wang, L.; Berne, B. J.; Friesner, R. A. Ligand Binding to Protein-binding Pockets with Wet and Dry Regions Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 1326-1330
11. Mondal, J.; Morrone, J. A.; Berne, B. J. How Hydrophobic Drying Forces Impact the Kinetics of Molecular Recognition Proc. Nat. Acad. Sci. U.S.A. 2013, 110, 13277-13282
12. Setny, P.; Baron, R.; Kekenes-Huskey, P. M.; McCammon, J. A.; Dzubiella, J. Solvent Fluctuations in Hydrophobic Cavity-ligand Binding Kinetics Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 1197-1202
13. Dror, R. O.; Pan, A. C.; Arlow, D. H.; Borhani, D. W.; Maragakis, P.; Shan, Y. Pathway and Mechanism of Drug Binding to G-protein-coupled Receptors Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 13118-13123
14. 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
15. Zhang, J.; Yang, P.; Ullrich, A. Targeting Cancer with Small Molecule Kinase Inhibitors Nat. Rev. Cancer 2009, 9, 28-39
16. Gschwind, A.; Fisher, O.; Gray, N. The Discovery of Receptor Tyrosine Kinases: Targets for Cancer Therapy Nat. Rev. Cancer 2004, 4, 361-370
17. Getlik, M.; Grütter, C.; Simard, J. R.; Klüter, S.; Rabiller, M.; Rode, H. B.; Robubi, A.; Rauh, D. Hybrid Compound Design to Overcome The Gatekeeper T338M Mutation in cSrc J. Med. Chem. 2009, 52, 3915-3926
18. Cohen, P. Protein kinases-The Major drug Targets of the Twenty-first Century? Nature Rev. 2002, 1, 309-315
19. Wang, L.; Wu, Y.; Deng, Y.; Kim, B.; Pierce, L.; Krilov, G.; Lupyan, D.; Robinson, S.; Dahlgren, M.; Greenwood, J.; Romero, D. L.; Masse, C.; Knight, J. L.; Steinbrecher, T.; Damm, W.; Harder, E.; Sherman, W.; Brewer, M.; Wester, R.; Murcko, M.; Frye, L.; Farid, R.; Lin, T.; Mobley, D.; Jorgensen, W. L.; Berne, B. J.; Friesner, R. A.; Abel, R. Accurate and Reliable Prediction of Relative Protein-Ligand Binding Affinities via Free Energy Calculations: Validation in Prospective Drug Discovery. 2014; Manuscript In Preparation.
20. 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: Struct., Funct., Bioinf. 2010, 78, 2571-2586
21. 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
22. 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 aMAP Kinase Inhibitors Proteins: Struct., Funct., Bioinf. 2013, 81, 1509-1526
23. Madhavi Sastry, G.; Adzhigirey, M.; Day, T.; Annabhimoju, R.; Sherman, W. Protein and Ligand Preparation: Parameters, Protocols, and Influence on Virtual Screening Enrichments J. Comput.-Aided Mol. Des. 2013, 27, 221-234
24. Schrödinger suite 2012 Protein Preparation Wizard; Schrödinger: New York. http://www.schrodinger.com (accessed 2012, -09-30).
25. Kaminski, G.; Friesner, R.; Tirado-Rives, J.; Jorgensen, W. Evaluation and Reparametrization of the OPLS-AA Force Field for Proteins via Comparison with Accurate Quantum Chemical Calculations on Peptides J. Phys. Chem. B 2001, 105, 6474-6487
26. Jorgensen, W.; Chandrasekhar, J.; Madura, J.; Impey, R.; Klein, M. Comparison of Simple Potential Functions for Simulating Liquid Water J. Chem. Phys. 1983, 79, 926-935
27. Nosé, S. A Molecular Dynamics Method for Simulations in The Canonical Ensemble Mol. Phys. 1984, 52, 255-268
28. Hoover, W. Canonical Dynamics: Equilibrium Phase-Space Distributions Phys. Rev. A 1985, 31, 1695-1697
29. Parrinello, M.; Rahman, A. Polymorphic Transitions in Single Crystals: A New Molecular Dynamics Method J. Appl. Phys. 1981, 52, 7182-7190
30. Darden, T.; York, D.; Pederson, L. G. Particle mesh Ewald: An Nlog(N) Method for Ewald Sums in Large System J. Chem. Phys. 1993, 98, 10089-10092
31. Essman, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pederson, L. G. A Smooth Particle Mesh Ewald Potential J. Chem. Phys. 1995, 103, 8577-8592
32. Miyamoto, S.; Kollman, P. Settle: An Analytical Version of the SHAKE and RATTLE Algorithm for Rigid Water Models J. Comput. Chem. 1992, 13, 952-962
33. Hess, B.; Bekker, H.; Berendsen, H.; Fraaije, J. G. E. LINCS: A Linear Constraint Solver for Molecular Simulations J. Comput. Chem. 1997, 18, 1463-1472
34. Hess, B.; Kutzner, C.; Van der Spoel, D.; Lindahl, E. GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation J. Chem. Theory Comput. 2008, 4, 435-447
35. Qiu, D.; Shenkin, P. S.; Hollinger, F. P.; Still, W. C. The GB/SA Continuum Model for Solvation. A Fast Analytical Method for the Calculation of Approximate Born Radii J. Phys. Chem. A 1997, 101, 3005-3014
36. Larsson, P.; Lindahl, E. A High-Performance Parallel-Generalized Born Implementation Enabled by Tabulated Interaction Rescaling J. Comput. Chem. 2010, 31, 2593-2600
37. Onufriev, A.; Bashford, D.; Case, D. Exploring Protein Native States and Large-scale Conformational Changes with a Modified Generalized Born Model Proteins: Struct., Funct., Genet. 2004, 55, 383-394
38. Schaefer, M.; Bartels, C.; Karplus, M. Solution Conformations and Thermodynamics of Structured Peptides: Molecular Dynamics Simulation with an Implicit Solvation Model J. Mol. Biol. 1998, 284, 835-848
39. Kumar, S.; Bouzida, D.; Swendsen, R. H.; Kollman, P. A.; Rosenberg, J. M. The Weighted Histogram Analysis Method for Free-energy Calculations on Biomolecules. I. The method J. Comput. Chem. 1992, 13, 1011-1021
40. Patel, A. J.; Varilly, P.; Chandler, D. Fluctuations of Water Near Extended Hydrophobic and Hydrophilic Surfaces J. Phys. Chem. B 2010, 114, 1632-1637
41. Andreev, S.; Reichman, D.; Hummer, G. Effect of Flexibility on Hydrophobic Behavior of Nanotube Water Channels J. Chem. Phys. 2005, 123, 194502
42. Zhu, F.; Hummer, G. Drying Transition in the Hydrophobic Gate of the GLIC Channel Blocks Ion Conduction Biophys. J. 2012, 103, 219-227
43. Tribello, G. A.; Bonomi, M.; Branduardi, D.; Camilloni, C.; Bussi, G. PLUMED 2: New Feathers For an Old Bird Comput. Phys. Commun. 2014, 185, 604-613
44. Lazaridis, T. Inhomogeneous Fluid Approach to Solvation Thermodynamics. 1. Theory J. Phys. Chem. B 1998, 102, 3531-3541
45. Gallicchio, E.; Kubo, M. M.; Levy, R. M. Enthalpy, Entropy and Cavity Decomposition of Alkane Hydration Free Energies: Numerical Results and Implications for Theories of Hydrophobic Solvation J. Phys. Chem. B 2000, 104, 6271-6285
46. Zhu, F.; Hummer, G. Pore Opening and Closing of a Pentameric Ligand-gated Ion Channel Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 19814-19819
47. Mondal, J.; Zhou, X.; Cui, Q.; Yethiraj, A. Self-Assembly of b-Peptides: Insight from the Pair and Many-Body Free Energy of Association J. Phys. Chem. B 2010, 114, 13551-13556
48. Zhou, R.; Berne, B. J. Can a Continuum Solvent Model Reproduce The Free Energy Landscape of a b-hairpin Folding in Water? Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 12777-12782