Explicit ligand hydration shells improve the correlation between MM-PB/GBSA binding energies and experimental activities

Journal of Chemical Theory and Computation

Volumn 9, Issue 6, 2013, Pages 2706-2717

  Maffucci, Irene ^a   Contini, Alessandro ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84879083130     PISSN: 15499618     EISSN: 15499626     Source Type: Journal    
DOI: 10.1021/ct400045d     Document Type: Article

References (59)

1. Pearlman, D. A.; Charifson, P. S. Are Free Energy Calculations Useful in Practice? A Comparison with Rapid Scoring Functions for the p38 MAP Kinase Protein System J. Med. Chem. 2001, 44 (21) 3417-3423
2. Srivastava, H. K.; Sastry, G. N. Molecular Dynamics Investigation on a Series of HIV Protease Inhibitors: Assessing the Performance of MM-PBSA and MM-GBSA Approaches J. Chem. Inf. Model. 2012, 52 (11) 3088-3098
3. Massova, I.; Kollman, P. Combined molecular mechanical and continuum solvent approach (MM-PBSA/GBSA) to predict ligand binding Perspect. Drug Discov. 2000, 18 (1) 113-135
4. Kollman, P. A.; Massova, I.; Reyes, C.; Kuhn, B.; Huo, S.; Chong, L.; Lee, M.; Lee, T.; Duan, Y.; Wang, W.; Donini, O.; Cieplak, P.; Srinivasan, J.; Case, D. A.; Cheatham, T. E., III. Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models Acc. Chem. Res. 2000, 33 (12) 889-897
5. Åqvist, J.; Luzhkov, V. B.; Brandsdal, B. O. Ligand Binding Affinities from MD Simulations Acc. Chem. Res. 2002, 35 (6) 358-365
6. Price, D.; Jorgensen, W. Improved convergence of binding affinities with free energy perturbation: Application to nonpeptide ligands with pp60src SH2 domain J. Comput.-Aided Mol. Des. 2001, 15 (8) 681-695
7. Xu, D. Autodock2MMGBSA, A multi-level virtual screening rescoring and refinement scheme that combines consensus scoring, simulated annealing and MM-GBSA binding free energy methods, American Chemical Society: Washington, DC, 2012; p NORM-153.
8. Xu, D.; Sawaya, N.; McCammon, J. A.; Li, W. W. In Autodock2MMGBSA, A multi-level virtual screening rescoring and refinement scheme that combines consensus scoring and MM-GBSA binding free energy methods, American Chemical Society: Washington, DC, 2010; p COMP-78.
9. Jackson, J. D. Classical Electrodynamics; Wiley: New York, 1999.
10. Constanciel, R.; Contreras, R. Self consistent field theory of solvent effects representation by continuum models: Introduction of desolvation contribution Theor. Chim. Acta 1984, 65 (1) 1-11
11. Still, W. C.; Tempczyk, A.; Hawley, R. C.; Hendrickson, T. Semianalytical treatment of solvation for molecular mechanics and dynamics J. Am. Chem. Soc. 1990, 112 (16) 6127-6129
12. Hou, T.; Wang, J.; Li, Y.; Wang, W. Assessing the Performance of the MM/PBSA and MM/GBSA Methods. 1. The Accuracy of Binding Free Energy Calculations Based on Molecular Dynamics Simulations J. Chem. Inf. Model. 2011, 51, 69-82
13. Hou, T.-J.; Wang, J.-M.; Li, Y.-Y.; Wang, W. Assessing the performance of the molecular mechanics/Poisson Boltzmann surface area and molecular mechanics/generalized Born surface area methods. II: The accuracy of ranking poses generated from docking J. Comput. Chem. 2011, 32, 866-877
14. Yang, T.; Wu, J. C.; Yan, C.; Wang, Y.; Luo, R.; Gonzales, M. B.; Dalby, K. N.; Ren, P. Virtual screening using molecular simulations Proteins: Struct., Funct., Bioinf. 2011, 79 (6) 1940-1951
15. Genheden, S.; Ryde, U. Comparison of end-point continuum-solvation methods for the calculation of protein-ligand binding free energies Proteins: Struct., Funct., Bioinf. 2012, 80 (5) 1326-1342
16. Wong, S.; Amaro, R. E.; McCammon, J. A. MM-PBSA Captures Key Role of Intercalating Water Molecules at a Protein-Protein Interface J. Chem. Theory Comput. 2009, 5, 422-429
17. Hayes, J. M.; Skamnaki, V. T.; Archontis, G.; Lamprakis, C.; Sarrou, J.; Bischler, N.; Skaltsounis, A.-L.; Zographos, S. E.; Oikonomakos, N. G. Kinetics, in silico docking, molecular dynamics, and MM-GBSA binding studies on prototype indirubins, KT5720, and staurosporine as phosphorylase kinase ATP-binding site inhibitors: The role of water molecules examined Proteins 2011, 79, 703-719
18. Freedman, H.; Huynh, L. P.; Le, L.; Cheatham, I. I. I. T. E.; Tuszynski, J. A.; Truong, T. N. Explicitly Solvated Ligand Contribution to Continuum Solvation Models for Binding Free Energies: Selectivity of Theophylline Binding to an RNA Aptamer J. Phys. Chem. B 2010, 114, 2227-2237
19. Greenidge, P. A.; Kramer, C.; Mozziconacci, J.-C.; Wolf, R. M. MM/GBSA Binding Energy Prediction on the PDBbind Data Set: Successes, Failures, and Directions for Further Improvement J. Chem. Inf. Model. 2012, 53 (1) 201-209
20. Checa, A.; Ortiz, A. R.; de Pascual-Teresa, B.; Gago, F. Assessment of solvation effects on calculated binding affinity differences: Trypsin inhibition by flavonoids as a model system for congeneric series J. Med. Chem. 1997, 40 (25) 4136-4145
21. Wallnoefer, H. G.; Liedl, K. R.; Fox, T. A challenging system: Free energy prediction for factor Xa J. Comput. Chem. 2011, 32 (8) 1743-1752
22. Ferri, N.; Corsini, A.; Bottino, P.; Clerici, F.; Contini, A. Virtual screening approach for the identification of new Rac1 inhibitors J. Med. Chem. 2009, 52 (14) 4087-4090
23. Ferri, N.; Radice, T.; Antonino, M.; Beccalli, E. M.; Tinelli, S.; Zunino, F.; Corsini, A.; Pratesi, G.; Ragg, E. M.; Gelmi, M. L.; Contini, A. Synthesis, structural, and biological evaluation of bis-heteroarylmaleimides and bis-heterofused imides Bioorg. Med. Chem. 2011, 19 (18) 5291-5299
24. Pellegrino, S.; Contini, A.; Clerici, F.; Gori, A.; Nava, D.; Gelmi, M. L. 1H-Azepine-4-amino-4-carboxylic acid: A new alpha,alpha-disubstituted ornithine analogue capable of inducing helix conformations in short Ala-Aib pentapeptides Chem.-Eur. J. 2012, 18 (28) 8705-8715
25. Contini, A.; Cappelletti, G.; Cartelli, D.; Fontana, G.; Gelmi, M. L. Molecular dynamics and tubulin polymerization kinetics study on 1,14-heterofused taxanes: Evidence of stabilization of the tubulin head-to-tail dimer-dimer interaction Mol. BioSyst. 2012, 8 (12) 3254-3261
26. Casoni, A.; Clerici, F.; Contini, A. Molecular dynamic simulation of mGluR5 amino terminal domain: Essential dynamics analysis captures the agonist or antagonist behaviour of ligands J. Mol. Graph. Model. 2013, 41, 72-78
27. Ferri, N.; Beccalli, E. M.; Contini, A.; Corsini, A.; Antonino, M.; Radice, T.; Pratesi, G.; Tinelli, S.; Zunino, F.; Gelmi, M. L. Antiproliferative effects on human tumor cells and rat aortic smooth muscular cells of 2,3-heteroarylmaleimides and heterofused imides Bioorg. Med. Chem. 2008, 16 (4) 1691-1701
28. Pommier, Y.; Leo, E.; Zhang, H.; Marchand, C. DNA Topoisomerases and Their Poisoning by Anticancer and Antibacterial Drugs Chem. Biol. 2010, 17 (5) 421-433
29. Samorì, C.; Guerrini, A.; Varchi, G.; Fontana, G.; Bombardelli, E.; Tinelli, S.; Beretta, G. L.; Basili, S.; Moro, S.; Zunino, F.; Battaglia, A. Semisynthesis, Biological Activity, and Molecular Modeling Studies of C-Ring-Modified Camptothecins J. Med. Chem. 2009, 52 (4) 1029-1039
30. Genheden, S.; Luchko, T.; Gusarov, S.; Kovalenko, A.; Ryde, U. An MM/3D-RISM Approach for Ligand Binding Affinities J. Phys. Chem. B 2010, 114 (25) 8505-8516
31. Genheden, S.; Ryde, U. How to obtain statistically converged MM/GBSA results J. Comput. Chem. 2010, 31 (4) 837-846
32. Staker, B. L.; Hjerrild, K.; Feese, M. D.; Behnke, C. A.; Burgin, A. B.; Stewart, L. The mechanism of topoisomerase I poisoning by a camptothecin analog Proc. Natl. Acad. Sci. 2002, 99 (24) 15387-15392
33. Chhatriwala, H.; Jafri, N.; Salgia, R. A review of topoisomerase inhibition in lung cancer Cancer Biol. Ther. 2006, 5 (12) 1600-1607
34. Dupradeau, F.-Y.; Pigache, A.; Zaffran, T.; Savineau, C.; Lelong, R.; Grivel, N.; Lelong, D.; Rosanski, W.; Cieplak, P. The R.E.D. tools: advances in RESP and ESP charge derivation and force field library building Phys. Chem. Chem. Phys. 2010, 12 (28) 7821-7839
35. Hornak, V. A., 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
36. Case, D. A.; Cheatham, T. E.; Darden, T.; Gohlke, H.; Luo, R.; Merz, K. M.; Onufriev, A.; Simmerling, C.; Wang, B.; Woods, R. J. The Amber biomolecular simulation programs J. Comput. Chem. 2005, 26 (16) 1668-1688
37. as and adding missing hydrogens to macromolecules Nucleic Acids Res. 2005, 33 (Suppl 2) W368-W371
38. MOE, MOE v2010.10; Chemical Computing Group, Inc.: Montreal, Canada, 2010.
39. Chirgadze, N. Y.; Sall, D. J.; Briggs, S. L.; Clawson, D. K.; Zhang, M.; Smith, G. F.; Schevitz, R. W. The crystal structures of human alpha-thrombin complexed with active site-directed diamino benzo[b]thiophene derivatives: A binding mode for a structurally novel class of inhibitors Protein Sci. 2000, 9 (1) 29-36
40. Banner, D. W.; Hadvary, P. Crystallographic analysis at 3.0-Å resolution of the binding to human thrombin of four active site-directed inhibitors J. Biol. Chem. 1991, 266 (30) 20085-20093
41. James, M. N. G.; Sielecki, A. R.; Moult, J. Crystallographic Analysis of a Pepstatin Analogue Binding to the Aspartyl Proteinase Penicillopepsin at 1.8 Angstroms Resolution. In Peptides: Structure and Function, Proceedings of the of the Eighth American Peptide Symposium, 1983; Hruby, V.; Rich, D., Eds.; Pierce Chemical Company: Rockford, IL, 1983; pp 521-530.
42. James, M. N.; Sielecki, A. R.; Hayakawa, K.; Gelb, M. H. Crystallographic analysis of transition state mimics bound to penicillopepsin: Difluorostatine-and difluorostatone-containing peptides Biochemistry 1992, 31 (15) 3872-3886
43. Ding, J.; Fraser, M. E.; Meyer, J. H.; Bartlett, P. A.; James, M. N. G. Macrocyclic Inhibitors of Penicillopepsin. 2. X-ray Crystallographic Analyses of Penicillopepsin Complexed with a P3-P1 Macrocyclic Peptidyl Inhibitor and with Its Two Acyclic Analogues J. Am. Chem. Soc. 1998, 120 (19) 4610-4621
44. Pugliese, L.; Coda, A.; Malcovati, M.; Bolognesi, M. Three-dimensional structure of the tetragonal crystal form of egg-white avidin in its functional complex with biotin at 2.7 A resolution J. Mol. Biol. 1993, 231 (3) 698-710
45. Green, Thermodynamics of the binding of biotin and some analogues by avidin. Biochem. J. 1966, 101 (3), 774-780.
46. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Nakatsuji, H.; Caricato, M.; Li, X.; Hratchian, H. P.; Izmaylov, A. F.; Bloino, J.; Zheng, G.; Sonnenberg, J. L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Montgomery, J. A., Jr.; Peralta, J. E.; Ogliaro, F.; Bearpark, M.; Heyd, J. J.; Brothers, E.; Kudin, K. N.; Staroverov, V. N.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A.; Burant, J. C.; Iyengar, S. S.; Tomasi, J.; Cossi, M.; Rega, N.; Millam, J. M.; Klene, M.; Knox, J. E.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Martin, R. L.; Morokuma, K.; Zakrzewski, V. G.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Dapprich, S.; Daniels, A. D.; Farkas, Ö.; Foresman, J. B.; Ortiz, J. V.; Cioslowski, J.; Fox, D. J. G09, Gaussian 09, Revision A.1; Gaussian, Inc.: Wallingford, CT, 2009.
47. 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 (9) 1157-1174
48. Ryckaert, J.-P.; Ciccotti, G.; Berendsen, H. J. C. Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n -alkanes J. Comput. Phys. 1977, 23 (3) 327-341
49. Kuhn, B.; Kollman, P. A. Binding of a Diverse Set of Ligands to Avidin and Streptavidin: An Accurate Quantitative Prediction of Their Relative Affinities by a Combination of Molecular Mechanics and Continuum Solvent Models J. Med. Chem. 2000, 43 (20) 3786-3791
50. Miller, B. R.; McGee, T. D.; Swails, J. M.; Homeyer, N.; Gohlke, H.; Roitberg, A. E. MMPBSA.py: An Efficient Program for End-State Free Energy Calculations J. Chem. Theory Comput. 2012, 8 (9) 3314-3321
51. Onufriev, A.; Bashford, D.; Case, D. A. Exploring protein native states and large-scale conformational changes with a modified generalized born model Proteins 2004, 55 (2) 383-394
52. Weis, A.; Katebzadeh, K.; Söderhjelm, P.; Nilsson, I.; Ryde, U. Ligand Affinities Predicted with the MM/PBSA Method: Dependence on the Simulation Method and the Force Field J. Med. Chem. 2006, 49 (22) 6596-6606
53. Case, D. A. Normal mode analysis of protein dynamics Curr. Opin. Struct. Biol. 1994, 4 (2) 285-290
54. Humphrey, W.; Dalke, A.; Schulten, K. VMD-Visual Molecular Dynamics J. Mol. Graphics 1996, 14, 33-38
55. Schiffer, C.; Hermans, J. Promise of Advances in Simulation Methods for Protein Crystallography: Implicit Solvent Models, Time-Averaging Refinement, and Quantum Mechanical Modeling. In Methods in Enzymology; Carter, C. W., Jr.; Sweet, R. M., Eds.; Academic Press: New York, 2003; Vol. 374, pp 412-461.
56. Kongsted, J.; Ryde, U. An improved method to predict the entropy term with the MM/PBSA approach J. Comput.-Aided Mol. Des. 2009, 23 (2) 63-71
57. Dewar, M. J. S.; Zoebisch, E. G.; Healy, E. F.; Stewart, J. J. P. Development and use of quantum mechanical molecular models. 76. AM1: A new general purpose quantum mechanical molecular model J. Am. Chem. Soc. 1985, 107 (13) 3902-3909
58. Ferri, N.; Bernini, S. K.; Corsini, A.; Clerici, F.; Erba, E.; Stragliotto, S.; Contini, A. 3-Aryl-N -aminoylsulfonylphenyl-1H-pyrazole-5- carboxamides: A new class of selective Rac inhibitors Med. Chem. Comm. 2013, 4 (3) 537-541
59. Liu, T.; Lin, Y.; Wen, X.; Jorissen, R. N.; Gilson, M. K. BindingDB: A web-accessible database of experimentally determined protein-ligand binding affinities Nucleic Acids Res. 2007, 35 (Database issue) D198-D201