Are homology models sufficiently good for free-energy simulations?

Journal of Chemical Information and Modeling

Volumn 52, Issue 11, 2012, Pages 3013-3021

  Genheden, Samuel ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CRYSTAL STRUCTURE; FREE ENERGY; PROTEINS;

BINDING AFFINITIES; DIHYDROFOLATE REDUCTASE; FREE ENERGY SIMULATIONS; HOMOLOGY MODELS; PLASMODIUM FALCIPARUM; PROTEIN HOMOLOGY MODELS; RELATIVE FREE ENERGY; THERMODYNAMIC INTEGRATION;

LIGANDS;

BLOOD CLOTTING FACTOR 10A; DIHYDROFOLATE REDUCTASE; LIGAND; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PROTOZOAL PROTEIN;

ARTICLE; CHEMISTRY; HUMAN; MOLECULAR DYNAMICS; PLASMODIUM FALCIPARUM; STRUCTURAL HOMOLOGY; THERMODYNAMICS;

FACTOR XA; HUMANS; LIGANDS; MOLECULAR DYNAMICS SIMULATION; NADP; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; STRUCTURAL HOMOLOGY, PROTEIN; TETRAHYDROFOLATE DEHYDROGENASE; THERMODYNAMICS;

EID: 84870021560     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci300349s     Document Type: Article

References (59)

1. Adcock, S. A.; McCammon, J. A. Molecular dynamics: Survey of methods for simulating the activity of proteins Chem. Rev. 2006, 106, 1589-1615 (Pubitemid 43792773)
2. van Gunsteren, W. F.; Bakowies, D.; Baron, R.; Chandrasekhar, I.; Christen, M.; Daura, X.; Gee, P.; Geerke, D. P.; Glättlie, A.; Hünenberger, P. H.; Kastenholz, M. A.; Oostenbrink, C.; Schenk, M.; Trzesniak, D.; van der Vegt, N. F. A.; Yu, H. B. Biomolecular modeling: Goals, problems, perspectives Ang. Chem. Int. Ed. 2006, 45, 4064-4092 (Pubitemid 44105659)
3. Michel, J.; Essex, J. Prediction of protein-ligand binding affinity by free energy simulations: assumptions, pitfalls and expectations J. Comput. Aided Mol. Des. 2010, 24, 639-658
4. Shirts, M. R.; Mobley, D. L.; Chodera, J. D. Alchemical free energy calculations: ready for prime time? Ann. Rep. Comput. Chem. 2007, 3, 41-59
5. Senn, H. M.; Thiel, W. Atomistic approaches in modern biology: from quantum chemistry to molecular simulations Top. Curr. Chem. 2007, 268, 173-290
6. Floudas, C. A.; Fung, H. K.; McAllister, S. R.; Mönnigmann, M.; Rajgaria, R. Advances in protein structure prediction and de novo protein design: a review Chem. Eng. Sci. 2006, 61, 966-988 (Pubitemid 41655853)
7. Zhang, Y. Progress and challenges in protein structure prediction Curr. Opin. Struct. Biol. 2008, 18, 342-348
8. Moult, J.; Fidelis, K.; Kryshtafovych, A.; Tramonanto, A. Critical assessment of methods of protein structure prediction (CASP) - round IX Proteins 2011, 79, 1-5
9. Cavasotto, C. N.; Phatak, S. S. Homology modeling in drug discovery: current trends and applications Drug Discov. Today 2009, 14, 676-683
10. Fan, H.; Irwin, J. J.; Webb, B. M.; Klebe, G.; Shoichet, B. K.; Sali, A. Molecular docking screens using comparative models of proteins J. Chem. Inf. Model. 2009, 49, 2512-2527
11. Oshiro, C.; Bradley, E. K.; Eksterowicz, J.; Evensen, E.; Lamb, M. L.; Lanctot, J. K.; Putta, S.; Stanton, R.; Grootenhuis, P. D. J. Performance of 3D-database molecular docking studies into homology models J. Med. Chem. 2004, 47, 764-767 (Pubitemid 38129734)
12. Fernandes, M. X.; Kairys, V.; Gilson, M. K. Comparing ligand interactions with multiple receptors via serial docking J. Chem. Inf. Comput. Sci. 2004, 44, 1961-1970
13. Kairys, V.; Fernandes, M. X.; Gilson, M. K. Screening drug-like compounds by docking to homology models: A systematic study J. Chem. Inf. Model. 2006, 46, 365-379 (Pubitemid 43282128)
14. McGovern, S. L.; Shoichet, B. K. Information decay in molecular docking screen against holo, apo, and modeled conformations of enzymes J. Med. Chem. 2003, 46, 365-379
15. Gohlke, H.; Klebe, G. Approaches to the description and prediction of the binding affinity of small-molecule ligands to macromolecular receptors Ang. Chem. Int. Ed. 2002, 41, 2644-2676
16. Srinivasan, J.; Cheatham, T. E., III; 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 (Pubitemid 28452628)
17. Hansson, T.; Marelius, J.; Åqvist, J. Ligand binding affinity prediction by linear interaction energy methods J. Comput. Aided Mol. Des. 1998, 12, 27-35 (Pubitemid 128513811)
18. Sham, Y. Y.; Chu, Z. T.; Tao, H.; Warshel, A. Examining methods for calculations of binding free energies: LRA, LIE. PDLD-LRA, and PDLS/S-LRA calculations of ligands binding to an HIV protease Proteins: Struct. Funct. Genet. 2000, 39, 393-407 (Pubitemid 30414177)
19. Genheden, S.; Nilsson, I.; Ryde, U. Binding Affinities of Factor Xa Inhibitors Estimated by Thermodynamic Integration and MM/GBSA J. Chem. Inf. Model. 2011, 51, 947-958
20. Mikulskis, P.; Genheden, S.; Rydberg, P.; Sandberg, L.; Olsen, L.; Ryde, U. Binding affinities in the SAMPL3 trypsin and host-guest blind tests estimated with the MM/PBSA and LIE methods J. Comput. Aided Mol. Des. 2012, 26, 527-541
21. Adler, M.; Davey, D. D.; Phillips, G. B.; Kim, S. H.; Jancarik, J.; Rumenik, G.; Light, D. R. Whitlow, M. Preparation, characterization, and the crystal structure of the inhibitor ZK-807834 (CI-1031) complexed with factor Xa Biochem 2000, 39, 12534-12542
22. Yuvaniyama, J.; Chitnumsub, P.; Kamchonwongpaisan, S.; Vanichtanankul, J.; Sirawaraporn, W.; Taylor, P.; Walkinshaw, M. D.; Yuthavong, Y. Insights into antifolate resistance from malarial DHFR-TS structures Nat. Struct. Biol. 2003, 10, 357-365 (Pubitemid 36523270)
23. Genheden, S.; Ryde, U. Improving efficiency of protein-ligand binding free-energy calculations by system truncation J. Chem. Theory Comput. 2012, 8, 1449-1458
24. Kongsted, J.; Ryde, U. An improved method to predict the entropy term with the MM/PBSA approach J. Comput. Aided Mol. Des. 2009, 23, 63-71
25. 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: Struct. Funct. Bioinform. 2006, 65, 712-725 (Pubitemid 44583220)
26. 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
27. Phillips, G.; Davey, D. D.; Eagen, K. A.; Koovakkat, S. K.; Liang, A.; Ng, H. P.; Pinkerton, M.; Trinh, L. Whitlow, M.; Beatty, A. M.; Morrissey, M. M. Design, synthesis, and activity of 2,6-diphenoxypyridine-derived factor Xa inhibitors J. Med. Chem. 1999, 42, 1749-1756 (Pubitemid 29244968)
28. Tarnchompoo, B.; Sirichaiwat, C.; Phupong, W.; Intaraudom, C.; Sirawaraporn, W.; Kamchonwongpaisan, S.; Vanichtanakul, J.; Thebtaranonth, Y.; Yuthavong, Y. Development of 2,4-diaminopyrimidines as antimalarials based on inhibition of the S108N and C59R+S108N mutants of dihydrofolate reductase from pyrimethamine-resistant Plasmodium falciparum J. Med. Chem. 2002, 45, 1244-1252 (Pubitemid 34263561)
29. Guimaraes, C. R. W.; Cardozo, M. MM-GB/SA rescoring of docking poses in structure-based lead optimization J. Chem. Inf. Model. 2008, 48, 958-970
30. Rastelli, G.; del Rio, A.; Degliesposti, G.; Sgobba, M. Fast and accurate predicitions of binding free energies using MM-PBSA and MM-GBSA J. Comput. Chem. 2010, 31, 797-810
31. Dewar, M. J. S.; Zoebisch, E. G.; Healy, E. F.; Stewart, J. J. P. Development and use of quantum mechanical molecular models. AM1: A new general purpose quantum mechanical molecular model J. Am. Chem. Soc. 1985, 107, 3902-3909
32. Besler, B. H.; Merz, K. M.; Kollman, P. A. Atomic charges derived from semiempirical methods J. Comput. Chem. 1990, 11, 431-439
33. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Montgomery, J. A., Jr.; Vreven, T.; Kudin, K. N.; Burant, J. C.; Millam, J. M.; Iyengar, S. S.; Tomasi, J.; Barone, V.; Mennucci, B.; Cossi, M.; Scalmani, G.; Rega, N.; Petersson, G. A.; Nakatsuji, H.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Klene, M.; Li, X.; Knox, J. E.; Hratchian, H, P.; 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.; Ayala, P. Y.; Morokuma, K.; Voth, G, A.; Salvador, P.; Dannenberg, J. J.; Zakrzewski, V. G.; Dapprich, S.; Daniels, A. D.; Strain, M. C.; Farkas, O.; Malick, D. K.; Rabuck, A. D.; Raghavachari, K.; Foresman, J. B.; Ortiz, J. V.; Cui, Q.; Baboul, A. G.; Cliffordmgrt, S.; Cioslowski, J.; Stefanov, B. B.; Liu, G.; Liashenko, A.; Piskorz, P.; Komaromi, I.; Martin, R. L.; Fox, D. J.; Keith, T.; Al-Laham, M. A.; Peng, C. Y.; Nanayakkara, A.; Challacombe, M.; Gill, P. M. W.; Johnson, B.; Chen, W.; Wong, M. W.; Gonzalez, C.; Pople, J. A. Gaussian 03, Gaussian, Inc.: Wallingford, CT, 2004.
34. Bayly, C. I.; Cieplak, P.; Cornell, W. D.; Kollman, P. A. A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: The RESP model J. Phys. Chem. 1993, 97, 10269-10280
35. 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
36. Hopfner, K. P.; Lang, A.; Karcher, A.; Sichler, K.; Kopetzki, E.; Brandstetter, H.; Huber, R.; Bode, W.; Engh, R. A. Coagulation factor IXa: the relaxed conformation of Tyr99 blocks substrate binding Struct. Fold. Des. 1999, 7, 989-996 (Pubitemid 29372520)
37. Mather, T.; Oganessyan, V.; Hof, P.; Huber, R. Foundling, S.; Esmon, C.; Bode, W. The 2.8 A crystal structure of Gla-domainless activated protein C EMBO J. 1996, 15, 6822-6831
38. Lipman, D. J.; Pearson, W. R. Rapid and sensitive protein similarity searches Science 1984, 227, 1435-1441
39. Kongsaeree, P.; Khongsuk, P.; Leartsakulpanich, U.; Chitnumsub, P.; Tarnchompoo, B.; Walkinshaw, M. D.; Yuthavong, Y. Crystal structure of dihydrofolate reductase from Plasmodium vivax: pyrimethamine displacement linked with mutation-induced resistance Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 13046-13051 (Pubitemid 41324976)
40. Li, L.; Du, W.; Ismagilov, R. F. Multiparameter screening on SlipChip used for nanoliter protein crystallization combining free interface diffusion and microbatch methods J. Am. Chem. Soc. 2010, 132, 112-119
41. Doan, L. T.; Martucci, W. E.; Vargo, M. A.; Atreya, C. E.; Anderson, K. S. Nonconserved residues Ala287 and Ser290 of the Cryptosporidium hominis thymidylate synthase domain facilitate its rapid rate of catalysis Biochemistry 2007, 46, 8370-8391
42. Sali, A.; Blundell, T. L. Comparative protein modelling by satisfaction of spatial restraints J. Mol. Biol. 1993, 234, 779-815 (Pubitemid 24007801)
43. Shen, M. Y.; Sali, A. Statistical potential for assessment and prediction of protein structures Protein Sci. 2006, 15, 2507-2524 (Pubitemid 44771688)
44. Martin, A. C. R. http://www.bioinf.org.uk/software/profit/ (accessed November 1, 2012).
45. Kirkwood, J. G. Statistical mechanics of fluid mixtures J. Chem. Phys. 1935, 3, 300-313
46. Steinbrecher, T.; Mobley, D. L.; Case, D. A. Nonlinear scaling schemes for Lennard-Jones interactions in free energy calculations J. Chem. Phys. 2007, 127, 214108
47. Steinbrecher, T.; Joung, I.; Case, D. A. Soft-core potentials in thermodynamic integration: Comparing one- and two-step transformations J. Comput. Chem. 2011, 32, 3253-3263
48. Case, D. A.; Cheatham, T.; Darden, T.; Gohlke, H.; Luo, R.; Merz, K. M., Jr.; Onufriev, A.; Simmerling, C.; Wang, B.; Woods, R. The Amber biomolecular simulation programs J. Comput. Chem. 2005, 26, 1668-1688 (Pubitemid 43076180)
49. Ryckaert, J. P.; Cicotti, 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, 327-341
50. 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
51. Wu., X.; Brooks, B. R. Self-guided Langevin dynamics simulation method Chem. Phys. Lett. 2003, 381, 512-518
52. Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; Dinola, A.; Haak, J. R. Molecular-dynamics with coupling to an external bath J. Chem. Phys. 1984, 81, 3684-3690
53. Genheden, S.; Ryde, U. How to obtain statistically converged MM/GBSA results J. Comput. Chem. 2010, 31, 837-846
54. Genheden, S.; Ryde, U. Comparison of different initialisation protocols to generate independent molecular dynamics simulations J. Comput. Chem. 2012, 32, 187-195
55. Mark, A. E.; van Gunsteren, W. F. Decomposition of the free energy of a system in terms of specific interactions J. Mol. Biol. 1994, 240, 167-176
56. Brady, G. P.; Szabo, A.; Sharp, K. A. On the decomposition of free energies J. Mol. Biol. 1996, 263, 123-125 (Pubitemid 26363076)
57. Bren, M; Florian, J.; Mavri, J.; Bren, U. Do all pieces make a whole? Thiele cumulants and the free energy decomposition Theor. Chem. Acc. 2007, 117, 535-540
58. Ambrish, R.; Alper, K.; Yang, Z. I-TASSER: a unified platform for automated protein structure and function prediction Nat. Prot. 2010, 5, 725-738
59. Bren, U.; Oostenbrink, C. Cytochrome P450 3A4 Inhibition by Ketoconazole: Tackling the Problem of Ligand Cooperativity Using Molecular Dynamics Simulations and Free-Energy Calculations J. Chem. Inf. Model. 2012, 52, 1573-1582