Application of binding free energy calculations to prediction of binding modes and affinities of MDM2 and MDMX inhibitors

Journal of Chemical Information and Modeling

Volumn 52, Issue 7, 2012, Pages 1821-1832

  Lee, Hui Sun ^a   Jo, Sunhwan ^a   Lim, Hyun Suk ^b   Im, Wonpil ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDERS; FORECASTING; FREE ENERGY; LIGANDS; MOLECULAR DYNAMICS; MOLECULES; PROTEINS;

BINDING AFFINITIES; BINDING FREE ENERGY; FREE ENERGY PERTURBATION; INTEGRATED APPROACH; LIGAND CONFORMATIONS; PROTEIN-LIGAND INTERACTIONS; SENSITIVITY AND SPECIFICITY; STRUCTURAL FLEXIBILITIES;

BINDING ENERGY;

LIGAND; MDM2 PROTEIN, HUMAN; MDM4 PROTEIN, HUMAN; NUCLEAR PROTEIN; ONCOPROTEIN; PROTEIN MDM2; PROTEIN BINDING;

ARTICLE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG ANTAGONISM; DRUG STABILITY; FORECASTING; HUMAN; MOLECULAR DYNAMICS; PROTEIN BINDING; THERMODYNAMICS; ANTAGONISTS AND INHIBITORS; MEDICINAL CHEMISTRY;

BINDING SITES; CHEMISTRY, PHARMACEUTICAL; DRUG STABILITY; FORECASTING; HUMANS; LIGANDS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; NUCLEAR PROTEINS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MDM2; THERMODYNAMICS;

EID: 84864192298     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci3000997     Document Type: Article

References (54)

1. Kitchen, D. B.; Decornez, H.; Furr, J. R.; Bajorath, J. Docking and scoring in virtual screening for drug discovery: Methods and applications Nat. Rev. Drug Discovery 2004, 3, 935-949 (Pubitemid 39529931)
2. Yuriev, E.; Agostino, M.; Ramsland, P. A. Challenges and advances in computational docking: 2009 in review J. Mol. Recognit. 2011, 24, 149-164
3. Morris, G. M.; Huey, R.; Lindstrom, W.; Sanner, M. F.; Belew, R. K.; Goodsell, D. S.; Olson, A. J. AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility J. Comput. Chem. 2009, 30, 2785-2791
4. Trott, O.; Olson, A. J. AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading J. Comput. Chem. 2010, 31, 455-461
5. Lang, P. T.; Brozell, S. R.; Mukherjee, S.; Pettersen, E. F.; Meng, E. C.; Thomas, V.; Rizzo, R. C.; Case, D. A.; James, T. L.; Kuntz, I. D. DOCK 6: Combining techniques to model RNA-small molecule complexes RNA 2009, 15, 1219-1230
6. Kramer, B.; Rarey, M.; Lengauer, T. Evaluation of the FLEXX incremental construction algorithm for protein-ligand docking Proteins 1999, 37, 228-241 (Pubitemid 29503004)
7. 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, 1739-1749 (Pubitemid 38380917)
8. Verdonk, M. L.; Cole, J. C.; Hartshorn, M. J.; Murray, C. W.; Taylor, R. D. Improved protei-ligand docking using GOLD Proteins 2003, 52, 609-623 (Pubitemid 37034158)
9. Totrov, M.; Abagyan, R. Flexible protein-ligand docking by global energy optimization in internal coordinates Proteins 1997, Suppl 1) 215-220 (Pubitemid 28090502)
10. Jain, A. N. Surflex: Fully automatic flexible molecular docking using a molecular similarity-based search engine J. Med. Chem. 2003, 46, 499-511 (Pubitemid 36182752)
11. Cross, J. B.; Thompson, D. C.; Rai, B. K.; Baber, J. C.; Fan, K. Y.; Hu, Y.; Humblet, C. Comparison of several molecular docking programs: Pose prediction and virtual screening accuracy J. Chem. Inf. Model. 2009, 49, 1455-1474
12. Jain, A. N. Effects of protein conformation in docking: Improved pose prediction through protein pocket adaptation J. Comput.-Aided Mol. Des. 2009, 23, 355-374
13. Deng, Y.; Roux, B. Computations of standard binding free energies with molecular dynamics simulations J. Phys. Chem. B 2009, 113, 2234-2246
14. Carlson, H. A.; Masukawa, K. M.; Rubins, K.; Bushman, F. D.; Jorgensen, W. L.; Lins, R. D.; Briggs, J. M.; McCammon, J. A. Developing a dynamic pharmacophore model for HIV-1 integrase J. Med. Chem. 2000, 43, 2100-2114 (Pubitemid 30354535)
15. Beglov, D.; Roux, B. Finite representation of an infinite bulk system: Solvent boundary potential for computer simulations J. Chem. Phys. 1994, 100, 9050-9063
16. Im, W.; Berneche, S.; Roux, B. Generalized solvent boundary potential for computer simulations J. Chem. Phys. 2000, 114, 2924-2937 (Pubitemid 32253408)
17. Deng, Y.; Roux, B. Calculation of standard binding free energies: Aromatic molecules in the T4 Lysozyme L99A mutant J. Chem. Theory. Comput. 2006, 2, 1255-1273
18. Wang, J.; Deng, Y.; Roux, B. Absolute binding free energy calculations using molecular dynamics simulations with restraining potentials Biophys. J. 2006, 91, 2798-2814 (Pubitemid 44526470)
19. Ge, X.; Roux, B. Absolute binding free energy calculations of sparsomycin analogs to the bacterial ribosome J. Phys. Chem. B 2010, 114, 9525-9539
20. Berg, T. Small-molecule inhibitors of protein-protein interactions Curr. Opin. Drug Discovery Devel. 2008, 11, 666-674
21. Arkin, M. R.; Whitty, A. The road less traveled: Modulating signal transduction enzymes by inhibiting their protein-protein interactions Curr. Opin. Chem. Biol. 2009, 13, 284-290
22. Matthews, M. M.; Weber, D. J.; Shapiro, P. S.; Coop, A.; Mackerell, A. D., Jr. Inhibition of protein-protein interactions with low molecular weight compounds Curr. Trends Med. Chem. 2008, 5, 21-32
23. Joerger, A. C.; Fersht, A. R. Structural biology of the tumor suppressor p53 Annu. Rev. Biochem. 2008, 77, 557-582
24. Haupt, Y.; Maya, R.; Kazaz, A.; Oren, M. Mdm2 promotes the rapid degradation of p53 Nature 1997, 387, 296-299 (Pubitemid 27220766)
25. Huang, L.; Yan, Z.; Liao, X.; Li, Y.; Yang, J.; Wang, Z. G.; Zuo, Y.; Kawai, H.; Shadfan, M.; Ganapathy, S.; Yuan, Z. M. The p53 inhibitors MDM2/MDMX complex is required for control of p53 activity in vivo Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 12001-12006
26. Kussie, P. H.; Gorina, S.; Marechal, V.; Elenbaas, B.; Moreau, J.; Levine, A. J.; Pavletich, N. P. Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain Science 1996, 274, 948-953 (Pubitemid 26398409)
27. Popowicz, G. M.; Czarna, A.; Holak, T. A. Structure of the human Mdmx protein bound to the p53 tumor suppressor transactivation domain Cell Cycle 2008, 7, 2441-2443
28. Vassilev, L. T.; Vu, B. T.; Graves, B.; Carvajal, D.; Podlaski, F.; Filipovic, Z.; Kong, N.; Kammlott, U.; Lukacs, C.; Klein, C.; Fotouhi, N.; Liu, E. A. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2 Science 2004, 303, 844-848 (Pubitemid 38174664)
29. Grasberger, B. L.; Lu, T.; Schubert, C.; Parks, D. J.; Carver, T. E.; Koblish, H. K.; Cummings, M. D.; LaFrance, L. V.; Milkiewicz, K. L.; Calvo, R. R.; Maguire, D.; Lattanze, J.; Franks, C. F.; Zhao, S.; Ramachandren, K.; Bylebyl, G. R.; Zhang, M.; Manthey, C. L.; Petrella, E. C.; Pantoliano, M. W.; Deckman, I. C.; Spurlino, J. C.; Maroney, A. C.; Tomczuk, B. E.; Molloy, C. J.; Bone, R. F. Discovery and cocrystal structure of benzodiazepinedione HDM2 antagonists that activate p53 in cells J. Med. Chem. 2005, 48, 909-912 (Pubitemid 40270436)
30. Allen, J. G.; Bourbeau, M. P.; Wohlhieter, G. E.; Bartberger, M. D.; Michelsen, K.; Hungate, R.; Gadwood, R. C.; Gaston, R. D.; Evans, B.; Mann, L. W.; Matison, M. E.; Schneider, S.; Huang, X.; Yu, D.; Andrews, P. S.; Reichelt, A.; Long, A. M.; Yakowec, P.; Yang, E. Y.; Lee, T. A.; Oliner, J. D. Discovery and optimization of chromenotriazolopyrimidines as potent inhibitors of the mouse double minute 2-tumor protein 53 protein-protein interaction J. Med. Chem. 2009, 52, 7044-7053
31. Popowicz, G. M.; Czarna, A.; Wolf, S.; Wang, K.; Wang, W.; Domling, A.; Holak, T. A. Structures of low molecular weight inhibitors bound to MDMX and MDM2 reveal new approaches for p53-MDMX/MDM2 antagonist drug discovery Cell Cycle 2010, 9, 1104-1111
32. Maestro v9.0; Schrödinger, LLC: Portland, OR.
33. Forli, S. Raccoon|Autodock VS: An automated tool for preparing AutoDock virtual screenings, 2011. http://autodock.scripps.edu/resources/raccoon.
34. 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, 1545-1614
35. Jo, S.; Kim, T.; Iyer, V. G.; Im, W. CHARMM-GUI: A web-based graphical user interface for CHARMM J. Comput. Chem. 2008, 29, 1859-1865
36. MacKerell, A. D., Jr.; Bashford, D.; Bellott, M.; Dunbrack, R. L., Jr.; Evanseck, J.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S.; Joseph, D.; Kuchnir, L.; Kuczera, K.; Lau, F. T. K.; Mattos, C.; Michnick, S.; Ngo, T.; Nguyen, D. T.; Prodhom, B.; Reiher, I., W. E.; Roux, B.; Schlenkrich, M.; Smith, J.; Stote, R.; Straub, J.; Watanabe, M.; Wiorkiewicz-Kuczera, J.; Yin, D.; Karplus, M. All-atom empirical potential for molecular modeling and dynamics studies of protein J. Phys. Chem. B 1998, 102, 3586-3616 (Pubitemid 128576688)
37. Buck, M.; Bouguet-Bonnet, S.; Pastor, R. W.; MacKerell, A. D., Jr. Importance of the CMAP correction to the CHARMM22 protein force field: Dynamics of hen lysozyme Biophys. J. 2006, 90, L36-L38
38. Vanommeslaeghe, K.; Hatcher, E.; Acharya, C.; Kundu, S.; Zhong, S.; Shim, J.; Darian, E.; Guvench, O.; Lopes, P.; Vorobyov, I.; Mackerell, A. D., Jr. CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields J. Comput. Chem. 2010, 31, 671-690
39. 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 -alkans J. Comput. Phys. 1977, 23, 327-341
40. 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
41. Feller, S. E.; Zhang, Y.; Paster, R. W.; Brooks, B. R. Constant pressure molecular dynamics simulations: The Langevin piston method J. Chem. Phys. 1995, 103, 4613-4621
42. Hoover, W. G. Canonical dynamics: Equilibrium phase-space distributions Phys. Rev. A 1985, 31, 1695-1697
43. Kozakov, D.; Clodfelter, K. H.; Vajda, S.; Camacho, C. J. Optimal clustering for detecting near-native conformations in protein docking Biophys. J. 2005, 89, 867-875 (Pubitemid 41098973)
44. Malmstrom, R. D.; Watowich, S. J. Using free energy of binding calculations to improve the accuracy of virtual screening predictions J. Chem. Inf. Model. 2011, 51, 1648-1655
45. Lee, H. S.; Lee, C. S.; Kim, J. S.; Kim, D. H.; Choe, H. Improving virtual screening performance against conformational variations of receptors by shape matching with ligand binding pocket J. Chem. Inf. Model. 2009, 49, 2419-2428
46. Lee, H. S.; Zhang, Y. BSP-SLIM: A blind low-resolution ligand-protein docking approach using predicted protein structures Proteins 2012, 80, 93-110
47. C, B. R.; Subramanian, J.; Sharma, S. D. Managing protein flexibility in docking and its applications Drug Discovery Today 2009, 14, 394-400
48. Uhrinova, S.; Uhrin, D.; Powers, H.; Watt, K.; Zheleva, D.; Fischer, P.; McInnes, C.; Barlow, P. N. Structure of free MDM2 N-terminal domain reveals conformational adjustments that accompany p53-binding J. Mol. Biol. 2005, 350, 587-598 (Pubitemid 40828916)
49. Deng, Y.; Roux, B. Computation of binding free energy with molecular dynamics and grand canonical Monte Carlo simulations J. Chem. Phys. 2008, 128, 115103
50. Sinko, W.; de Oliveira, C. A.; Pierce, L. C.; McCammon, J. A. Protecting high energy barriers: A new equation to regulate boost energy in accelerated molecular dynamics simulations J. Chem. Theory Comput. 2012, 8, 17-23
51. Joseph, T. L.; Madhumalar, A.; Brown, C. J.; Lane, D. P.; Verma, C. S. Differential binding of p53 and nutlin to MDM2 and MDMX: Computational studies Cell Cycle 2010, 9, 1167-1181
52. Czarna, A.; Popowicz, G. M.; Pecak, A.; Wolf, S.; Dubin, G.; Holak, T. A. High affinity interaction of the p53 peptide-analogue with human MDM2 and MDMX Cell Cycle 2009, 8, 1176-1184
53. Boresch, S.; Archontis, G.; Karplus, M. Free energy simulations: The meaning of the individual contributions from a component analysis Proteins 1994, 20, 25-33 (Pubitemid 24308147)
54. Jiang, W.; Hodoscek, M.; Roux, B. Computation of absolute hydration and binding free energy with free energy perturbation distributed replica-exchange molecular dynamics (FEP/REMD) J. Chem. Theory Comput. 2009, 5, 2583-2588