Atomistic models for free energy evaluation of drug binding to membrane proteins

Current Medicinal Chemistry

Volumn 18, Issue 17, 2011, Pages 2601-2611

  Durdagi, S ^a   Zhao, C ^a   Cuervo, J E ^a   Noskov, S Y ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Free energy computation; Free energy perturbation; Lead optimization; Ligand binding; Membrane protein; MM PBSA; Molecular docking; Molecular simulation; Rational drug design; Scoring function

Indexed keywords

CALCIUM CHANNEL; CHLORIDE CHANNEL; MEMBRANE PROTEIN; POTASSIUM CHANNEL; PROTEOME; SODIUM CHANNEL;

ACCURACY; ARTICLE; BINDING AFFINITY; CHANNEL GATING; DECOMPOSITION; DRUG PROTEIN BINDING; ENERGY; EVALUATION; INTERMETHOD COMPARISON; LIGAND BINDING; MATHEMATICAL COMPUTING; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR MODEL; PRINCIPAL COMPONENT ANALYSIS; SIMULATION;

CHANNELOPATHIES; DRUG DESIGN; ENTROPY; ETHER-A-GO-GO POTASSIUM CHANNELS; FULLERENES; HIV PROTEASE; ION CHANNELS; LIGANDS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PHENETHYLAMINES; PROTEIN BINDING; SULFONAMIDES;

EID: 79957958970     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/092986711795933641     Document Type: Article

References (88)

1. Anson, L., Membrane Protein Biophysics, Nature, 2009, 459, (7245), 343-343.
2. Arinaminpathy, Y.; Khurana, E.; Engelman, D.M.; Gerstein, M.B., Computational analysis of membrane proteins: the largest class of drug targets, Drug Discov Today, 2009, 14, (23-24), 1130-1135.
3. Rudnick, G., Serotonin transporters - Structure and function, Journal of Membrane Biology, 2006, 213, (2), 101-110. (Pubitemid 46626129)
4. Schafer, W.R., How do antidepressants work? Prospects for genetic analysis of drug mechanisms, Cell, 1999, 98, (5), 551-554. (Pubitemid 29418946)
5. Subbotina, J.; Yarov-Yarovoy, V.; Lees-Miller, J.; Durdagi, S.; Guo, J.Q.; Duff, H.J.; Noskov, S.Y., Structural refinement of the hERG1 pore and voltage-sensing domains with ROSETTAmembrane and molecular dynamics simulations, Proteins, 2010, 78, (14), 2922-2934.
6. Durdagi, S.; Subbotina, J.; Lees-Miller, J.; Guo, J.; Duff, H.J.; Noskov, S.Y., Insights into the Molecular Mechanism of hERG1 Channel Activation and Blockade by Drugs, Curr Med Chem, 2010, 17, (30), 3514-3532.
7. Gilson, M.K.; Zhou, H.X., Calculation of protein-ligand binding affinities, Annual Review of Biophysics and Biomolecular Structure, 2007, 36, 21-42. (Pubitemid 46998108)
8. Cramer, C.J. Essentials of Computational Chemistry: Theories and Models. John Wiley & Sons Ltd. , 2002.
9. Leach, A.R. Molecular Modelling: Principles and Application. Pearson Educ. Ltd.: England, 2001.
10. Levine, I.N. Quantum Chemistry. Prentice Hall, 2000.
11. May, A.; Sieker, F.; Zacharias, M., How to efficiently include receptor flexibility during computational docking, Curr Comput-Aid Drug, 2008, 4, (2), 143-153.
12. Kontoyianni, M.; McClellan, L.M.; Sokol, G.S., Evaluation of docking performance: Comparative data on docking algorithms, J Med Chem, 2004, 47, (3), 558-565. (Pubitemid 38129714)
13. Jones, G.; Willett, P.; Glen, R.C.; Leach, A.R.; Taylor, R., Development and validation of a genetic algorithm for flexible docking, J Mol Biol, 1997, 267, (3), 727-748. (Pubitemid 27170693)
14. Bohm, H.J., The Development of a Simple Empirical Scoring Function to Estimate the Binding Constant for a Protein Ligand Complex of Known 3- Dimensional Structure, J Comput Aid Mol Des, 1994, 8, (3), 243-256.
15. Ajay; Murcko, M.A., Computational methods to predict binding free energy in ligand-receptor complexes, J Med Chem, 1995, 38, (26), 4953-4967. (Pubitemid 26012256)
16. Taylor, R.D.; Jewsbury, P.J.; Essex, J.W., A review of protein-small molecule docking methods, J Comput Aid Mol Des, 2002, 16, (3), 151-166.
17. Friesner, R.A.; Banks, J.L.; Murphy, R.B.; Halgren, T.A.; Klicic, J.J.; Mainz, D.T.; Repasky, M.P.; Knoll, E.H.; Shelley, M.; Perry, J.K.; Shaw, D.E.; Francis, P.; Shenkin, P.S., Glide: A new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy, J Med Chem, 2004, 47, (7), 1739-1749. (Pubitemid 38380917)
18. Verdonk, M.L.; Chessari, G.; Cole, J.C.; Hartshorn, M.J.; Murray, C.W.; Nissink, J.W.M.; Taylor, R.D.; Taylor-, R., Modeling water molecules in protein-ligand docking using GOLD, J Med Chem, 2005, 48, (20), 6504-6515. (Pubitemid 41429002)
19. Holger, J.S.; Minnigan, H.J.; Lamon, R.P.; Gornick, C.C., The utility of ultrasound to determine ventricular capture in external cardiac pacing, Am J Emerg Med, 2001, 19, (2), 134-136. (Pubitemid 32205274)
20. Sherman, W.; Day, T.; Jacobson, M.P.; Friesner, R.A.; Farid, R., Novel procedure for modeling ligand/receptor induced fit effects, J Med Chem, 2006, 49, (2), 534-553. (Pubitemid 43157487)
21. Hille, B. Ion Channels of Exitable Membranes. Sinauer Associates Sunderland, 2001.
22. Ashcroft, F.M. Ion Channels and disease: Channelopathies. Academic Press: San Diego, 2000. 24
23. Lehmann-Horn, F.; Jurkat-Rott, K., Voltage-gated ion channels and hereditary disease, Physiol Rev, 1999, 79, (4), 1317-1372. (Pubitemid 29473318)
24. Sanguinetti, M.C.; Jiang, C.G.; Curran, M.E.; Keating, M.T., A Mechanistic Link between an Inherited and an Acquired Cardiac-Arrhythmia - Herg Encodes the I-Kr Potassium Channel, Cell, 1995, 81, (2), 299-307.
25. Curran, M.E.; Splawski, I.; Timothy, K.W.; Vincent, G.M.; Green, E.D.; Keating, M.T., A Molecular-Basis for Cardiac-Arrhythmia - Herg Mutations Cause Long Qt Syndrome, Cell, 1995, 80, (5), 795-803.
26. Fehrst, A. Structure and Mechanism in Protein Science. Freeman: New York, 1999.
27. Elcock, A.H.; Sept, D.; McCammon, J.A., Computer simulation of proteinprotein interactions, J Phys Chem B, 2001, 105, (8), 1504-1518.
28. Friesner, R.A.; Murphy, R.B.; Repasky, M.P.; Frye, L.L.; Greenwood, J.R.; Halgren, T.A.; Sanschagrin, P.C.; Mainz, D.T., Extra precision glide: Docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes, J Med Chem, 2006, 49, (21), 6177-6196. (Pubitemid 44595196)
29. Lees-Miller, J.P.; Subbotina, J.O.; Guo, J.Q.; Yarov-Yarovoy, V.; Noskov, S.Y.; Duff, H.J., Interactions of H562 in the S5 Helix with T618 and S621 in the Pore Helix Are Important Determinants of hERG1 Potassium Channel Structure and Function, Biophys J, 2009, 96, (9), 3600-3610.
30. Wolber, G.; Langer, T., LigandScout: 3-d pharmacophores derived from protein-bound Ligands and their use as virtual screening filters, J Chem Inf Model, 2005, 45, (1), 160-169. (Pubitemid 40736968)
31. Zhou, H.X.; Gilson, M.K., Theory of Free Energy and Entropy in Noncovalent Binding, Chemical Reviews, 2009, 109, (9), 4092-4107.
32. Deng, Y.Q.; Roux, B., Computations of Standard Binding Free Energies with Molecular Dynamics Simulations, Journal of Physical Chemistry B, 2009, 113, (8), 2234-2246.
33. Simonson, T.; Archontis, G.; Karplus, M., Free energy simulations come of age: Protein-ligand recognition, Accounts of Chemical Research, 2002, 35, (6), 430-437.
34. Gilson, M.K.; Given, J.A.; Bush, B.L.; McCammon, J.A., The statisticalthermodynamic basis for computation of binding affinities: A critical review, Biophysical Journal, 1997, 72, (3), 1047-1069. (Pubitemid 27113632)
35. Kollman, P., Free-Energy Calculations - Applications to Chemical and Biochemical Phenomena, Chemical Reviews, 1993, 93, (7), 2395-2417.
36. Tobias, D.J.; Brooks, C.L., The Thermodynamics of Solvophobic Effects - a Molecular-Dynamics Study of Normal-Butane in Carbon-Tetrachloride and Water, Journal of Chemical Physics, 1990, 92, (4), 2582-2592.
37. Jorgensen, W.L.; Severance, D.L., Aromatic Aromatic Interactions - Free- Energy Profiles for the Benzene Dimer in Water, Chloroform, and Liquid Benzene, Journal of the American Chemical Society, 1990, 112, (12), 4768-4774.
38. Sneddon, S.F.; Tobias, D.J.; Brooks, C.L., Thermodynamics of Amide Hydrogen-Bond Formation in Polar and Apolar Solvents, Journal of Molecular Biology, 1989, 209, (4), 817-820. (Pubitemid 20046134)
39. Jorgensen, W.L., Free-Energy Calculations - a Breakthrough for Modeling Organic-Chemistry in Solution, Accounts of Chemical Research, 1989, 22, (5), 184-189.
40. Beveridge, D.L.; Dicapua, F.M., Free-Energy Via Molecular Simulation - Applications to Chemical and Biomolecular Systems, Annual Review of Biophysics and Biophysical Chemistry, 1989, 18, 431-492.
41. Guvench, O.; MacKerell, A.D., Computational evaluation of protein-small molecule binding, Current Opinion in Structural Biology, 2009, 19, (1), 56-61. 25
42. Villoutreix, B.O.; Bastard, K.; Sperandio, O.; Fahraeus, R.; Poyet, J.L.; Calvo, F.; Deprez, B.; Miteva, M.A., In silico-in vitro screening of proteinprotein interactions: Towards the next generation of therapeutics, Current Pharmaceutical Biotechnology, 2008, 9, (2), 103-122. (Pubitemid 351513489)
43. Gane, P.J.; Dean, P.M., Recent advances in structure-based rational drug design, Current Opinion in Structural Biology, 2000, 10, (4), 401-404. (Pubitemid 30496791)
44. Wang, J.M.; Morin, P.; Wang, W.; Kollman, P.A., Use of MM-PBSA in reproducing the binding free energies to HIV-1 RT of TIBO derivatives and predicting the binding mode to HIV-1 RT of efavirenz by docking and MMPBSA, Journal of the American Chemical Society, 2001, 123, (22), 5221-5230. (Pubitemid 32910665)
45. Bashford, D.; Case, D.A., Generalized born models of macromolecular solvation effects, Annu. Rev. Phys. Chem., 2000, 51, 129-152.
46. Swanson, J.M.J.; McCammon, J.A., Applying the statistical mechanics behind ligand-receptor binding affinities., Biophys J, 2003, 84, (2), 341A- 341A.
47. Minh, D.D.L.; Bui, J.M.; Chang, C.E.; Jain, T.; Swanson, J.M.J.; McCammon, J.A., The entropic cost of protein-protein association: A case study on acetylcholinesterase binding to fasciculin-2, Biophys J, 2005, 89, (4), L25-L27. (Pubitemid 41401009)
48. Wright, J.D.; Noskov, S.Y.; Lim, C., Factors governing loss and rescue of DNA binding upon single and double mutations in the p53 core domain, Nucleic Acids Research, 2002, 30, (7), 1563-1574. (Pubitemid 34679731)
49. Noskov, S.Y.; Lim, C., Free energy decomposition of protein-protein interactions, Biophys J, 2001, 81, (2), 737-750. (Pubitemid 32721449)
50. Roux, B., The Membrane Potential and its Representation by a Constant Electric Field in Computer Simulations, Biophys J, 2008, 95, (9), 4205-4216.
51. Roux, B., Influence of the membrane potential on the free energy of an intrinsic protein, Biophys J, 1997, 73, (6), 2980-2989. (Pubitemid 27525765)
52. Kutluay, E.; Roux, B.; Heginbotham, L., Rapid intracellular TEA block of the KcsA potassium channel, Biophys J, 2005, 88, (2), 1018-1029. (Pubitemid 40975935)
53. Onufriev, A.; Case, D.A.; Bashford, D., Effective Born radii in the generalized Born approximation: The importance of being perfect, Journal of Computational Chemistry, 2002, 23(14), 1297-1304. (Pubitemid 35186231)
54. Strockbine, B.; Rizzo, R.C., Binding of antifusion peptides with HIVgp41 from molecular dynamics simulations: Quantitative correlation with experiment, Proteins, 2007, 67, (3), 630-642. (Pubitemid 46625579)
55. McGillick, B.E.; Balius, T.E.; Mukherjee, S.; Rizzo, R.C., Origins of Resistance to the HIVgp41 Viral Entry Inhibitor T20, Biochemistry-Us, 2010, 49, (17), 3575-3592.
56. Wu, Y.L.; Cao, Z.J.; Yi, H.; Jiang, D.H.; Mao, X.; Liu, H.; Li, W.X., Simulation of the interaction between ScyTx and small conductance calciumactivated potassium channel by docking and MM-PBSA, Biophys J, 2004, 87, (1), 105-112. (Pubitemid 38880069)
57. Zhou, Z.; Bates, M.; Madura, J.D., Structure modeling, ligand binding, and binding affinity calculation (LR-MM-PBSA) of human heparanase for inhibition and drug design, Proteins, 2006, 65, (3), 580-592. (Pubitemid 44583209)
58. Deng, Y.Q.; Roux, B., Calculation of standard binding free energies: Aromatic molecules in the T4 lysozyme L99A mutant, Journal of Chemical Theory and Computation, 2006, 2, (5), 1255-1273.
59. Brandsdal, B.O.; Osterberg, F.; Almlof, M.; Feierberg, I.; Luzhkov, V.B.; Aqvist, J., Free energy calculations and ligand binding, Protein Simulations, 2003, 66, 123-+.
60. Nervall, M.; Hanspers, P.; Carlsson, J.; Boukharta, L.; Aqvist, J., Predicting binding modes from free energy calculations, J Med Chem, 2008, 51, (9), 2657-2667. (Pubitemid 351620787)
61. Kumar, S.; Bouzida, D.; Swendsen, R.H.; Kollman, P.A.; Rosenberg, J.M., The Weighted Histogram Analysis Method for Free-Energy Calculations on Biomolecules .1. The Method, Journal of Computational Chemistry, 1992, 13, (8), 1011-1021.
62. Oostenbrink, C.; van Gunsteren, W.F., Free energies of ligand binding for structurally diverse compounds, P Natl Acad Sci USA, 2005, 102, (19), 6750-6754. (Pubitemid 40675387)
63. Straatsma, T.P.; Mccammon, J.A., Multiconfiguration Thermodynamic Integration, Journal of Chemical Physics, 1991, 95, (2), 1175-1188.
64. Archontis, G.; Watson, K.A.; Xie, Q.; Andreou, G.; Chrysina, E.D.; Zographos, S.E.; Oikonomakos, N.G.; Karplus, M., Glycogen phosphorylase inhibitors: A free energy perturbation analysis of glucopyranose spirohydantoin analogues, Proteins, 2005, 61, (4), 984-998. (Pubitemid 41753167)
65. Hermans, J.; Shankar, S., The Free-Energy of Xenon Binding to Myoglobin from Molecular-Dynamics Simulation, Israel J Chem, 1986, 27, (2), 225-227.
66. Boresch, S.; Tettinger, F.; Leitgeb, M.; Karplus, M., Absolute binding free energies: A quantitative approach for their calculation, J Phys Chem B, 2003, 107, (35), 9535-9551.
67. Jorgensen, W.L.; Buckner, J.K.; Boudon, S.; Tiradorives, J., Efficient Computation of Absolute Free-Energies of Binding by Computer- Simulations - Application to the Methane Dimer in Water, Journal of Chemical Physics, 1988, 89, (6), 3742-3746.
68. Wang, J.Y.; Deng, Y.Q.; Roux, B., Absolute binding free energy calculations using molecular dynamics simulations with restraining potentials, Biophys J, 2006, 91, (8), 2798-2814. (Pubitemid 44526470)
69. Im, W.; Berneche, S.; Roux, B., Generalized solvent boundary potential for computer simulations, Journal of Chemical Physics, 2001, 114, (7), 2924-2937. (Pubitemid 32253408)
70. Noskov, S.Y., Molecular mechanism of substrate specificity in the bacterial neutral amino acid transporter LeuT, Proteins, 2008, 73, (4), 851-863.
71. Zhao, C.F.; Caplan, D.A.; Noskov, S.Y., Evaluations of the Absolute and Relative Free Energies for Antidepressant Binding to the Amino Acid Membrane Transporter LeuT with Free Energy Simulations, Journal of Chemical Theory and Computation, 2010, 6, (6), 1900-1914.
72. Singh, S.K.; Piscitelli, C.L.; Yamashita, A.; Gouaux, E., A Competitive Inhibitor Traps LeuT in an Open-to-Out Conformation, Science, 2008, 322, (5908), 1655-1661.
73. Yamashita, A.; Singh, S.K.; Kawate, T.; Jin, Y.; Gouaux, E., Crystal structure of a bacterial homologue of Na+/Cl-dependent neurotransmitter transporters, Nature, 2005, 437, (7056), 215-223. (Pubitemid 41294479)
74. Lee, M.S.; Olson, M.A., Calculation of absolute protein-ligand binding affinity using path and endpoint approaches, Biophys J, 2006, 90, (3), 864-877.
75. Woo, H.J.; Roux, B., Calculation of absolute protein-ligand binding free energy from computer simulations, P Natl Acad Sci USA, 2005, 102, (19), 6825-6830. (Pubitemid 40675400)
76. Roux, B., The Calculation of the Potential of Mean Force Using Computer- Simulations, Computer Physics Communications, 1995, 91, (1-3), 275-282.
77. Torrie, G.M.; Valleau, J.P., Non-Physical Sampling Distributions in Monte- Carlo Free-Energy Estimation - Umbrella Sampling, J Comput Phys, 1977, 23, (2), 187-199.
78. Zhang, D.Q.; Gullingsrud, J.; McCammon, J.A., Potentials of mean force for acetylcholine unbinding from the alpha7 nicotinic acetylcholine receptor ligand-binding domain (vol 128, pg 3019, 2006), Journal of the American Chemical Society, 2006, 128, (13), 4493-4493.
79. Jensen, M.O.; Park, S.; Tajkhorshid, E.; Schulten, K., Energetics of glycerol conduction through aquaglyceroporin GlpF, P Natl Acad Sci USA, 2002, 99, (10), 6731-6736. (Pubitemid 34527148)
80. Jarzynski, C., Nonequilibrium equality for free energy differences, Physical Review Letters, 1997, 78, (14), 2690-2693. (Pubitemid 127655287)
81. Hornak, V.; Okur, A.; Rizzo, R.C.; Simmerling, C., HIV-1 protease flaps spontaneously close to the correct structure in simulations following manual placement of an inhibitor into the open state, Journal of the American Chemical Society, 2006, 128, (9), 2812-2813.
82. Friedman, S.H.; Ganapathi, P.S.; Rubin, Y.; Kenyon, G.L., Optimizing the binding of fullerene inhibitors of the HIV-1 protease through predicted increases in hydrophobic desolvation, J Med Chem, 1998, 41, (13), 2424-2429. (Pubitemid 28285743)
83. Sijbesma, R.; Srdanov, G.; Wudl, F.; Castoro, J.A.; Wilkins, C.; Friedman, S.H.; Decamp, D.L.; Kenyon, G.L., Synthesis of a Fullerene Derivative for the Inhibition of Hiv Enzymes, Journal of the American Chemical Society, 1993, 115, (15), 6510-6512. (Pubitemid 23276369)
84. Durdagi, S.; Mavromoustakos, T.; Chronakis, N.; Papadopoulos, M.G., Computational design of novel fullerene analogues as potential HIV-1 PR inhibitors: Analysis of the binding interactions between fullerene inhibitors and HIV-1 PR residues using 3D QSAR, molecular docking and molecular dynamics simulations, Bioorgan Med Chem, 2008, 16, (23), 9957-9974.
85. Zoumpoulakis, P.; Daliani, I.; Zervou, M.; Kyrikou, I., Siapi, E.; Lamprinidis, G.; Mikros, E.; Mavromoustakos, T., Losartan's molecular basis of interaction with membranes and AT1 receptor. Chem. Phys. Lipids 2003, (125), 13-25. (Pubitemid 37414802)
86. Fotakis, C.; Christodouleas, D.; Chatzigeorgiou, P.; Zervou, M.; Benetis, N. P.; Viras, K.; Mavromoustakos, T., Application of a novel CP-31P NMR methodology to study the possible interdigitation effect of losartan in phospholipids bilayers. Comparison with Raman spectroscopy data Biophys. J. 2009, (96), 2227-2236.
87. Fotakis, C.; Gega, S.; Siapi, E.; Potamitis, C.; Viras, K.; Moutevelis- Minakakis, P.; Kokotos, G.; Durdagi, S.; Grdadolnik, S.; Sartori, B.; Rappolt, M.; Mavromoustakos, T., Drug interactions at the bilayer interface and receptor site induced by the novel synthetic pyrrolidinone analog MMK3. Biochim. Biophys. Acta 2010, (1798) (3) 422-432.
88. Durdagi, S.; Duff, H. J.; Noskov, S. Yu. Combined Receptor and Ligand- Based Approach to the Universal Pharmacophore Model Development for Studies of Drug Blockade to the hERG1 Pore Domain. J. Chem. Inf. Model. 2011, (51), 463-474.