G-mmpbsa -A GROMACS tool for high-throughput MM-PBSA calculations

Journal of Chemical Information and Modeling

Volumn 54, Issue 7, 2014, Pages 1951-1962

  Kumari, Rashmi ^a   Kumar, Rajendra ^a   Lynn, Andrew ^a  

^a JAWAHARLAL NEHRU UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEXATION; FREE ENERGY; MOLECULAR DYNAMICS; SOLVENTS;

BIOMOLECULAR INTERACTIONS; DIELECTRIC BOUNDARY; HIV-1 PROTEASE INHIBITORS; INTERACTION ENERGIES; INTERACTION FREE ENERGIES; MOLECULAR DYNAMICS SIMULATIONS; POISSON BOLTZMANN SURFACE AREAS (PBSA); SOLVENT ACCESSIBLE SURFACE AREAS;

BINDING ENERGY;

HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE INHIBITOR; P16 PROTEASE, HUMAN IMMUNODEFICIENCY VIRUS 1; SOLVENT;

CHEMISTRY; DRUG DEVELOPMENT; METABOLISM; MOLECULAR DYNAMICS; PROCEDURES; THERMODYNAMICS;

DRUG DISCOVERY; HIV PROTEASE; HIV PROTEASE INHIBITORS; MOLECULAR DYNAMICS SIMULATION; SOLVENTS; THERMODYNAMICS;

EID: 84904964377     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci500020m     Document Type: Article

References (102)

1. Parenti, M. D.; Rastelli, G. Advances and applications of binding affinity prediction methods in drug discovery Biotechnol. Adv. 2012, 30, 244-250
2. Meirovitch, H. Recent developments in methodologies for calculating the entropy and free energy of biological systems by computer simulation Curr. Opin. Struct. Biol. 2007, 17, 181-186
3. Kollman, P. Free energy calculations: Applications to chemical and biochemical phenomena Chem. Rev. 1993, 93, 2395-2417
4. Ytreberg, F. M.; Swendsen, R. H.; Zuckerman, D. M. Comparison of free energy methods for molecular systems J. Chem. Phys. 2006, 125, 184114
5. Foloppe, N.; Hubbard, R. Towards predictive ligand design with free-energy based computational methods? Curr. Med. Chem. 2006, 13, 3583-3608
6. Homeyer, N.; Gohlke, H. Free Energy Calculations by the Molecular Mechanics Poisson-Boltzmann Surface Area Method Mol. Inform. 2012, 31, 114-122
7. Gohlke, H.; Kiel, C.; Case, D. A. Insights into protein-protein binding by binding free energy calculation and free energy decomposition for the Ras-Raf and Ras-RalGDS complexes J. Mol. Biol. 2003, 330, 891-913
8. 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., 3rd Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models Acc. Chem. Res. 2000, 33, 889-897
9. Gilson, M. K.; Honig, B. Calculation of the total electrostatic energy of a macromolecular system: solvation energies, binding energies, and conformational analysis Proteins 1988, 4, 7-18
10. Rizzo, R. C.; Aynechi, T.; Case, D. A.; Kuntz, I. D. Estimation of absolute free energies of hydration using continuum methods: Accuracy of partial, charge models and optimization of nonpolar contributions J. Chem. Theory. Comput. 2006, 2, 128-139
11. Sitkoff, D.; Sharp, K. A.; Honig, B. Accurate Calculation of Hydration Free-Energies Using Macroscopic Solvent Models J. Phys. Chem. 1994, 98, 1978-1988
12. 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, 6127-6129
13. Ferrari, A. M.; Degliesposti, G.; Sgobba, M.; Rastelli, G. Validation of an automated procedure for the prediction of relative free energies of binding on a set of aldose reductase inhibitors Bioorg. Med. Chem. 2007, 15, 7865-7877
14. 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, 3786-3791
15. Rastelli, G.; Del Rio, A.; Degliesposti, G.; Sgobba, M. Fast and accurate predictions of binding free energies using MM-PBSA and MM-GBSA J. Comput. Chem. 2010, 31, 797-810
16. Wang, W.; Kollman, P. A. Free energy calculations on dimer stability of the HIV protease using molecular dynamics and a continuum solvent model J. Mol. Biol. 2000, 303, 567-582
17. Brice, A. R.; Dominy, B. N. Analyzing the robustness of the MM/PBSA free energy calculation method: application to DNA conformational transitions J. Comput. Chem. 2011, 32, 1431-1440
18. Brown, S. P.; Muchmore, S. W. Large-scale application of high-throughput molecular mechanics with Poisson-Boltzmann surface area for routine physics-based scoring of protein-ligand complexes J. Med. Chem. 2009, 52, 3159-3165
19. Weis, A.; Katebzadeh, K.; Soderhjelm, 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, 6596-6606
20. Kumar, R.; Shinde, R. N.; Ajay, D.; Sobhia, M. E. Probing interaction requirements in PTP1B inhibitors: a comparative molecular dynamics study J. Chem. Inf. Model. 2010, 50, 1147-1158
21. Wang, W.; Kollman, P. A. Computational study of protein specificity: the molecular basis of HIV-1 protease drug resistance Proc. Natl. Acad. Sci. USA 2001, 98, 14937-14942
22. Venken, T.; Krnavek, D.; Munch, J.; Kirchhoff, F.; Henklein, P.; De Maeyer, M.; Voet, A. An optimized MM/PBSA virtual screening approach applied to an HIV-1 gp41 fusion peptide inhibitor Proteins 2011, 79, 3221-3235
23. Meliciani, I.; Klenin, K.; Strunk, T.; Schmitz, K.; Wenzel, W. Probing hot spots on protein-protein interfaces with all-atom free-energy simulation J. Chem. Phys. 2009, 131, 034114
24. Zoete, V.; Meuwly, M.; Karplus, M. Study of the insulin dimerization: binding free energy calculations and per-residue free energy decomposition Proteins 2005, 61, 79-93
25. Degliesposti, G.; Portioli, C.; Parenti, M. D.; Rastelli, G. BEAR, a novel virtual screening methodology for drug discovery J. Biomol. Screen. 2011, 16, 129-133
26. Lindström, A.; Edvinsson, L.; Johansson, A.; Andersson, C. D.; Andersson, I. E.; Raubacher, F.; Linusson, A. Postprocessing of Docked Protein-Ligand Complexes Using Implicit Solvation Models J. Chem. Inf. Model. 2011, 51, 267-282
27. Rastelli, G.; Degliesposti, G.; Del Rio, A.; Sgobba, M. Binding estimation after refinement, a new automated procedure for the refinement and rescoring of docked ligands in virtual screening Chem. Biol. Drug. Des. 2009, 73, 283-286
28. Barakat, K. H.; Jordheim, L. P.; Perez-Pineiro, R.; Wishart, D.; Dumontet, C.; Tuszynski, J. A. Virtual screening and biological evaluation of inhibitors targeting the XPA-ERCC1 interaction PLoS One 2012, 7, e51329
29. 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 2011, 79, 1940-1951
30. Kasam, V.; Salzemann, J.; Botha, M.; Dacosta, A.; Degliesposti, G.; Isea, R.; Kim, D.; Maass, A.; Kenyon, C.; Rastelli, G.; Hofmann-Apitius, M.; Breton, V. WISDOM-II: Screening against multiple targets implicated in malaria using computational grid infrastructures Malar. J. 2009, 8, 88
31. 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, 1668-1688
32. Pronk, S.; Pall, S.; Schulz, R.; Larsson, P.; Bjelkmar, P.; Apostolov, R.; Shirts, M. R.; Smith, J. C.; Kasson, P. M.; van der Spoel, D.; Hess, B.; Lindahl, E. GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit Bioinformatics 2013, 29, 845-854
33. Li, L.; Li, C.; Sarkar, S.; Zhang, J.; Witham, S.; Zhang, Z.; Wang, L.; Smith, N.; Petukh, M.; Alexov, E. DelPhi: a comprehensive suite for DelPhi software and associated resources BMC Biophys 2012, 5, 9
34. Baker, N. A.; Sept, D.; Joseph, S.; Holst, M. J.; McCammon, J. A. Electrostatics of nanosystems: application to microtubules and the ribosome Proc. Natl. Acad. Sci. USA 2001, 98, 10037-10041
35. Chiang, H. L.; Ngo, S. T.; Chen, C. J.; Hu, C. K.; Li, M. S. Oligomerization of Peptides LVEALYL and RGFFYT and Their Binding Affinity to Insulin PLoS One 2013, 8, e65358
36. Ganoth, A.; Friedman, R.; Nachliel, E.; Gutman, M. A molecular dynamics study and free energy analysis of complexes between the Mlc1p protein and two IQ motif peptides Biophys. J. 2006, 91, 2436-50
37. Spiliotopoulos, D.; Spitaleri, A.; Musco, G. Exploring PHD fingers and H3K4me0 interactions with molecular dynamics simulations and binding free energy calculations: AIRE-PHD1, a comparative study PLoS One 2012, 7, e46902
38. Levy, R. M.; Zhang, L. Y.; Gallicchio, E.; Felts, A. K. On the nonpolar hydration free energy of proteins: surface area and continuum solvent models for the solute-solvent interaction energy J. Am. Chem. Soc. 2003, 125, 9523-9530
39. Tan, C.; Tan, Y. H.; Luo, R. Implicit nonpolar solvent models J. Phys. Chem. B 2007, 111, 12263-12274
40. Wagoner, J. A.; Baker, N. A. Assessing implicit models for nonpolar mean solvation forces: the importance of dispersion and volume terms Proc. Natl. Acad. Sci. USA 2006, 103, 8331-8336
41. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. Scalable molecular dynamics with NAMD J. Comput. Chem. 2005, 26, 1781-802
42. 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, 3417-23
43. Hou, T.; McLaughlin, W. A.; Wang, W. Evaluating the potency of HIV-1 protease drugs to combat resistance Proteins 2008, 71, 1163-1174
44. Hou, T.; Yu, R. Molecular dynamics and free energy studies on the wild-type and double mutant HIV-1 protease complexed with amprenavir and two amprenavir-related inhibitors: mechanism for binding and drug resistance J. Med. Chem. 2007, 50, 1177-1188
45. Kar, P.; Knecht, V. Origin of decrease in potency of darunavir and two related antiviral inhibitors against HIV-2 compared to HIV-1 protease J. Phys. Chem. B 2012, 116, 2605-2614
46. Srinivasan, J.; Cheatham, T. E.; Cieplak, P.; Kollman, P. A.; Case, D. A. Continuum solvent studies of the stability of DNA, RNA, and phosphoramidate-DNA helices J. Am. Chem. Soc. 1998, 120, 9401-9409
47. Lee, M. R.; Duan, Y.; Kollman, P. A. Use of MM-PB/SA in estimating the free energies of proteins: Application to native, intermediates, and unfolded villin headpiece Proteins 2000, 39, 309-316
48. 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
49. Lindorff-Larsen, K.; Piana, S.; Palmo, K.; Maragakis, P.; Klepeis, J. L.; Dror, R. O.; Shaw, D. E. Improved side-chain torsion potentials for the Amber ff99SB protein force field Proteins 2010, 78, 1950-1958
50. 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
51. Honig, B.; Nicholls, A. Classical Electrostatics in Biology and Chemistry Science 1995, 268, 1144-1149
52. Hunenberger, P. H.; Helms, V.; Narayana, N.; Taylor, S. S.; McCammon, J. A. Determinants of ligand binding to cAMP-dependent protein kinase Biochemistry 1999, 38, 2358-2366
53. Dzubiella, J.; Swanson, J. M. J.; McCammon, J. A. Coupling nonpolar and polar solvation free energies in implicit solvent models J. Chem. Phys. 2006, 124, 084905
54. Hummer, G. Hydrophobic force field as a molecular alternative to surface-area models J. Am. Chem. Soc. 1999, 121, 6299-6305
55. Kang, Y. K.; Nemethy, G.; Scheraga, H. A. Free-Energies of Hydration of Solute Molecules 0.1. Improvement of the Hydration Shell-Model by Exact Computations of Overlapping Volumes J. Phys. Chem. 1987, 91, 4105-4109
56. Smith, R.; Tanford, C. Hydrophobicity of Long-Chain Alkyl Carboxylic-Acids, as Measured by Their Distribution between Heptane and Aqueous-Solutions Proc. Natl. Acad. Sci. USA 1973, 70, 289-293
57. Lum, K.; Chandler, D.; Weeks, J. D. Hydrophobicity at small and large length scales J. Phys. Chem. B 1999, 103, 4570-4577
58. Pierotti, R. A. Scaled Particle Theory of Aqueous and Non-Aqueous Solutions Chem. Rev. 1976, 76, 717-726
59. Weeks, J. D.; Chandler, D.; Andersen, H. C. Role of Repulsive Forces in Determining Equilibrium Structure of Simple Liquids J. Chem. Phys. 1971, 54, 5237-5247
60. Konecny, R.; Baker, N. A.; McCammon, J. A. iAPBS: a programming interface to Adaptive Poisson-Boltzmann Solver (APBS) Comput. Sci. Discov. 2012, 5
61. Brooks, B. R.; Brooks, C. L., 3rd; Mackerell, A. D., Jr.; Nilsson, L.; Petrella, R. J.; Roux, B.; Won, Y.; Archontis, G.; Bartels, C.; Boresch, S.; Caflisch, A.; Caves, L.; Cui, Q.; Dinner, A. R.; Feig, M.; Fischer, S.; Gao, J.; Hodoscek, M.; Im, W.; Kuczera, K.; Lazaridis, T.; Ma, J.; Ovchinnikov, V.; Paci, E.; Pastor, R. W.; Post, C. B.; Pu, J. Z.; Schaefer, M.; Tidor, B.; Venable, R. M.; Woodcock, H. L.; Wu, X.; Yang, W.; York, D. M.; Karplus, M. CHARMM: the biomolecular simulation program J. Comput. Chem. 2009, 30, 1545-614
62. Case, D. A.; Darden, T.; Cheatham, T. E., III; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Walker, R. C.; Zhang, W.; Merz, K. M.; Roberts, B.; Hayik, S.; Roitberg, A.; Seabra, G.; Swails, J.; Goetz, A. W.; Kolossváry, I.; Wong, K. F.; Paesani, F.; Vanicek, J.; Wolf, R. M.; Liu, J.; Wu, X.; Brozell, S. R.; Steinbrecher, T.; Gohlke, H.; Cai, Q.; Ye, X.; Wang, J.; Hsieh, M.-J.; Cui, G.; Roe, D. R.; Mathews, D. H.; Seetin, M. G.; Salomon-Ferrer, R.; Sagui, C.; Babin, V.; Luchko, T.; Gusarov, S.; Kovalenko, A.;; Kollman, P. A. AMBER 12, University of California: San Francisco, 2012.
63. Tsui, V.; Case, D. A. Theory and applications of the generalized Born solvation model in macromolecular Simulations Biopolymers 2001, 56, 275-291
64. Tsui, V.; Case, D. A. Molecular dynamics simulations of nucleic acids with a generalized born solvation model J. Am. Chem. Soc. 2000, 122, 2489-2498
65. Bondi, A. van der Waals Volumes and Radii J. Phys. Chem. 1964, 68, 441-451
66. Eisenhaber, F.; Lijnzaad, P.; Argos, P.; Sander, C.; Scharf, M. The Double Cubic Lattice Method-Efficient Approaches to Numerical-Integration of Surface-Area and Volume and to Dot Surface Contouring of Molecular Assemblies J. Comput. Chem. 1995, 16, 273-284
67. OBoyle, N. M.; Banck, M.; James, C. A.; Morley, C.; Vandermeersch, T.; Hutchison, G. R. Open Babel: An open chemical toolbox J. Cheminform. 2011, 3, 33
68. 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
69. Wang, J.; Wang, W.; Kollman, P. A.; Case, D. A. Automatic atom type and bond type perception in molecular mechanical calculations J. Mol. Graph. Model. 2006, 25, 247-260
70. Sousa da Silva, A. W.; Vranken, W. F. ACPYPE-AnteChamber PYthon Parser interfacE BMC Res. Notes 2012, 5, 367
71. Sondergaard, C. R.; Olsson, M. H. M.; Rostkowski, M.; Jensen, J. H. Improved Treatment of Ligands and Coupling Effects in Empirical Calculation and Rationalization of pK(a) Values J. Chem. Theory. Comput. 2011, 7, 2284-2295
72. 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, 926-935
73. Berendsen, H. J. C.; Postma, J. P. M.; Vangunsteren, W. F.; Dinola, A.; Haak, J. R. Molecular-Dynamics with Coupling to an External Bath J. Chem. Phys. 1984, 81, 3684-3690
74. Bussi, G.; Donadio, D.; Parrinello, M. Canonical sampling through velocity rescaling J. Chem. Phys. 2007, 126, 014101
75. Nose, S.; Klein, M. L. Constant Pressure Molecular-Dynamics for Molecular-Systems Mol. Phys. 1983, 50, 1055-1076
76. Darden, T.; York, D.; Pedersen, L. Particle Mesh Ewald-an N.Log(N) Method for Ewald Sums in Large Systems J. Chem. Phys. 1993, 98, 10089-10092
77. Hess, B. P-LINCS: A parallel linear constraint solver for molecular simulation J. Chem. Theory. Comput. 2008, 4, 116-122
78. Hess, B.; Bekker, H.; Berendsen, H. J. C.; Fraaije, J. G. E. M. LINCS: A linear constraint solver for molecular simulations J. Comput. Chem. 1997, 18, 1463-1472
79. Cheng, Y.; Prusoff, W. H. Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50% inhibition (I50) of an enzymatic reaction Biochem. Pharmacol. 1973, 22, 3099-108
80. Hou, T.; Wang, J.; Li, 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
81. 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
82. Levitt, M.; Sander, C.; Stern, P. S. Protein Normal-Mode Dynamics-Trypsin-Inhibitor, Crambin, Ribonuclease and Lysozyme J. Mol. Biol. 1985, 181, 423-447
83. Hagler, A. T.; Stern, P. S.; Sharon, R.; Becker, J. M.; Naider, F. Computer-Simulation of the Conformational Properties of Oligopeptides-Comparison of Theoretical Methods and Analysis of Experimental Results J. Am. Chem. Soc. 1979, 101, 6842-6852
84. Kopitz, H.; Cashman, D. A.; Pfeiffer-Marek, S.; Gohlke, H. Influence of the Solvent Representation on Vibrational Entropy Calculations: Generalized Born Versus Distance-Dependent Dielectric Model J. Comput. Chem. 2012, 33, 1004-1013
85. Hensen, U.; Lange, O. F.; Grubmuller, H. Estimating Absolute Configurational Entropies of Macromolecules: The Minimally Coupled Subspace Approach PLoS One 2010, 5, e9179
86. Chang, C. E. A.; Chen, W.; Gilson, M. K. Ligand configurational entropy and protein binding Proc. Natl. Acad. Sci. USA 2007, 104, 1534-1539
87. Andricioaei, I.; Karplus, M. On the calculation of entropy from covariance matrices of the atomic fluctuations J. Chem. Phys. 2001, 115, 6289-6292
88. Tidor, B.; Karplus, M. The Contribution of Vibrational Entropy to Molecular Association-the Dimerization of Insulin J. Mol. Biol. 1994, 238, 405-414
89. Schlitter, J. Estimation of Absolute and Relative Entropies of Macromolecules Using the Covariance-Matrix Chem. Phys. Lett. 1993, 215, 617-621
90. 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, 3088-3098
91. Kongsted, J.; Soderhjelm, P.; Ryde, U. How accurate are continuum solvation models for drug-like molecules? J. Comput. Aided. Mol. Des. 2009, 23, 395-409
92. Tan, C.; Yang, L.; Luo, R. How well does Poisson-Boltzmann implicit solvent agree with explicit solvent? A quantitative analysis J. Phys. Chem. B 2006, 110, 18680-18687
93. Harris, R. C.; Boschitsch, A. H.; Fenley, M. O. Influence of Grid Spacing in Poisson-Boltzmann Equation Binding Energy Estimation J. Chem. Theory. Comput. 2013, 9, 3677-3685
94. Simonson, T.; Brooks, C. L. Charge screening and the dielectric constant of proteins: Insights from molecular dynamics J. Am. Chem. Soc. 1996, 118, 8452-8458
95. Wang, J.; Cai, Q.; Xiang, Y.; Luo, R. Reducing grid-dependence in finite-difference Poisson-Boltzmann calculations J. Chem. Theory. Comput. 2012, 8, 2741-2751
96. Rocchia, W.; Sridharan, S.; Nicholls, A.; Alexov, E.; Chiabrera, A.; Honig, B. Rapid grid-based construction of the molecular surface and the use of induced surface charge to calculate reaction field energies: Applications to the molecular systems and geometric objects J. Comput. Chem. 2002, 23, 128-137
97. Gilson, M. K.; Sharp, K. A.; Honig, B. H. Calculating the electrostatic potential of molecules in solution: Method and error assessment J. Comput. Chem. 1988, 9, 327-335
98. Bruccoleri, R. E.; Novotny, J.; Davis, M. E.; Sharp, K. A. Finite difference Poisson-Boltzmann electrostatic calculations: Increased accuracy achieved by harmonic dielectric smoothing and charge antialiasing J. Comput. Chem. 1997, 18, 268-276
99. Im, W.; Beglov, D.; Roux, B. Continuum solvation model: Computation of electrostatic forces from numerical solutions to the Poisson-Boltzmann equation Comput. Phys. Commun. 1998, 111, 59-75
100. Nina, M.; Im, W.; Roux, B. Optimized atomic radii for protein continuum electrostatics solvation forces Biophys. Chem. 1999, 78, 89-96
101. Oehme, D. P.; Brownlee, R. T.; Wilson, D. J. Effect of atomic charge, solvation, entropy, and ligand protonation state on MM-PB(GB)SA binding energies of HIV protease J. Comput. Chem. 2012, 33, 2566-2580
102. Thompson, D. C.; Humblet, C.; Joseph-McCarthy, D. Investigation of MM-PBSA rescoring of docking poses J. Chem. Inf. Model. 2008, 48, 1081-1091