Scoring and lessons learned with the CSAR benchmark using an improved iterative knowledge-based scoring function

Journal of Chemical Information and Modeling

Volumn 51, Issue 9, 2011, Pages 2097-2106

  Huang, Sheng You ^a   Zou, Xiaoqin ^a  

^a UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; COMPLEXATION; CORRELATION METHODS; CRYSTAL ATOMIC STRUCTURE; KNOWLEDGE BASED SYSTEMS; LIGANDS; PROTEINS; STATISTICAL MECHANICS; VAN DER WAALS FORCES;

BINDING AFFINITIES; COMMUNITY STRUCTURES; COMPARATIVE ANALYSIS; PEARSON CORRELATION; PROTEIN-LIGAND COMPLEXES; PROTEIN-LIGAND INTERACTIONS; SCORING FUNCTIONS; SCORING PERFORMANCE;

ITERATIVE METHODS;

LIGAND; PROTEIN;

ARTICLE; CHEMISTRY; CRYSTALLIZATION; PROTEIN BINDING; STRUCTURE ACTIVITY RELATION;

CRYSTALLIZATION; LIGANDS; PROTEIN BINDING; PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 80053297657     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci2000727     Document Type: Article

References (81)

1. Brooijmans, N.; Kuntz, I. D. Molecular recognition and docking algorithms Annu. Rev. Biophys. Biomol. Struct. 2003, 32, 335-373 (Pubitemid 37056233)
2. Shoichet, B. K. Virtual screening of chemical libraries Nature 2004, 432, 862-865 (Pubitemid 40037142)
3. Gilson, M. K.; Zhou, H.-X. Calculation of protein-ligand binding affinities Annu. Rev. Biophys. Biomol. Struct. 2007, 36, 21-42 (Pubitemid 46998108)
4. Rajamani, R.; Good, A. C. Ranking poses in structure-based lead discovery and optimization: Current trends in scoring function development Curr. Opin. Drug Discovery Dev. 2007, 10, 308-315 (Pubitemid 46804927)
5. Huang, N.; Jacobson, M. P. Physics-based methods for studying protein-ligand interactions Curr. Opin. Drug Discovery Dev. 2007, 30, 325-331 (Pubitemid 46800226)
6. Huang, S.-Y.; Zou, X. Advances and challenges in protein-ligand docking Int. J. Mol. Sci. 2010, 11, 3016-3034
7. Huang, S.-Y.; Grinter, S. Z.; Zou, X. Scoring functions and their evaluation methods for protein-ligand docking: recent advances and future directions Phys. Chem. Chem. Phys. 2010, 12, 12899-12908
8. Case, D. A.; Cheatham, T. E., III; 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)
9. Brooks, B. R.; Brooks, C. L., III; 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
10. Christen, M.; Hunenberger, P. H.; Bakowies, D.; Baron, R.; Burgi, R.; Geerke, D. P.; Heinz, T. N.; Kastenholz, M. A.; Krautler, V.; Oostenbrink, C.; Peter, C.; Trzesniak, D.; van Gunsteren, W. F. The GROMOS software for biomolecular simulation: GROMOS05 J. Comput. Chem. 2005, 26, 1719-1751 (Pubitemid 43076183)
11. Jorgensen, W. L.; Maxwell, D. S.; Tirado-Rives, J. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids J. Am. Chem. Soc. 1996, 118, 11225-11236 (Pubitemid 26399746)
12. Wang, W.; Donini, O.; Reyes, C. M.; Kollman, P. A. Biomolecular simulations: Recent developments in force fields, simulations of enzyme catalysis, protein-ligand, protein-protein, and protein-nucleic acid noncovalent interactions Annu. Rev. Biophys. Biomol. Struct. 2001, 30, 211-243 (Pubitemid 32566163)
13. 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 (Pubitemid 34063137)
14. Grant, J. A.; Pickup, B. T.; Nicholls, A. A smooth permittivity function for Poisson-Boltzmann solvation methods J. Comput. Chem. 2001, 22, 608-640 (Pubitemid 32382607)
15. 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. U.S.A. 2001, 98, 10037-10041 (Pubitemid 32802969)
16. Wei, B. Q.; Baase, W. A.; Weaver, L. H.; Matthews, B. W.; Shoichet, B. K. A model binding site for testing scoring functions in molecular docking J. Mol. Biol. 2002, 322, 339-355
17. Wang, J.; 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 MM-PBSA J. Am. Chem. Soc. 2001, 123, 5221-5230 (Pubitemid 32910665)
18. Naim, M.; Bhat, S.; Rankin, K. N.; Dennis, S.; Chowdhury, S. F.; Siddiqi, I.; Drabik, P.; Sulea, T.; Bayly, C. I.; Jakalian, A.; Purisima, E. O. Solvated Interaction Energy (SIE) for Scoring Protein-Ligand Binding Affinities. 1. Exploring the Parameter Space J. Chem. Inf. Model. 2007, 47, 122-133 (Pubitemid 46225568)
19. Thompson, D. C.; Humblet, C.; Joseph-McCarthy, D. Investigation of MM-PBSA rescoring of docking poses J. Chem. Inf. Model. 2008, 48, 1081-1091
20. 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
21. Hawkins, G. D.; Cramer, C. J.; Truhlar, D. G. Chem. Phys. Lett. 1995, 246, 122-129
22. Lee, M. S.; Feig, M.; Salsbury, F. R., Jr.; Brooks, C. L., III. New analytic approximation to the standard molecular volume definition and its application to generalized Born calculations J. Comput. Chem. 2003, 24, 1348-1356
23. 6: A parameterization-free, accurate, analytical generalized Born method J. Phys. Chem. B 2007, 111, 3055-3061 (Pubitemid 46543295)
24. Zou, X.; Sun, Y.; Kuntz, I. D. Inclusion of solvation in ligand binding free energy calculations using the generalized-Born model J. Am. Chem. Soc. 1999, 121, 8033-8043
25. Liu, H.-Y.; Kuntz, I. D.; Zou, X. Pairwise GB/SA scoring function for structure-based drug design J. Phys. Chem. B 2004, 108, 5453-5462
26. Liu, H.-Y.; Zou, X. Electrostatics of ligand binding: Parametrization of the generalized born model and comparison with the Poisson-Boltzmann approach J. Phys. Chem. B 2006, 110, 9304-9313 (Pubitemid 43829028)
27. Liu, H.-Y.; Grinter, S. Z.; Zou, X. Multiscale generalized born modeling of ligand binding energies for virtual database screening J. Phys. Chem. B 2009, 113, 11793-11799
28. Majeux, N.; Scarsi, M.; Apostolakis, J.; Ehrhardt, C.; Caflisch, A. Exhaustive docking of molecular fragments with electrostatic solvation Proteins 1999, 37, 88-105 (Pubitemid 29408922)
29. Ghosh, A.; Rapp, C. S.; Friesner, R. A. Generalized Born model based on a surface integral formulation J. Phys. Chem. B 1998, 102, 10983-10990 (Pubitemid 128716615)
30. Huang, N.; Kalyanaraman, C.; Irwin, J. J.; Jacobson, M. P. Physics-based scoring of protein-ligand complexes: Enrichment of known inhibitors in large-scale virtual screening J. Chem. Inf. Model. 2006, 46, 243-253 (Pubitemid 43282119)
31. Lyne, P. D.; Lamb, M. L.; Saeh, J. C. Accurate prediction of the relative potencies of members of a series of kinase inhibitors using molecular docking and MM-GBSA scoring J. Med. Chem. 2006, 49, 4805-4808 (Pubitemid 44201037)
32. 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
33. Meng, E. C.; Shoichet, B. K.; Kuntz, I. D. Automated docking with grid-based energy approach to macromolecule-ligand interactions J. Comput. Chem. 1992, 13, 505-524
34. Morris, G. M.; Goodsell, D. S.; Halliday, R. S.; Huey, R.; Hart, W. E.; Belew, R. K.; Olson, A. J. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function J. Comput. Chem. 1998, 19, 1639-1662 (Pubitemid 128590223)
35. Aqvist, J.; Medina, C; Samuelsson, J. E. A new method for predicting binding affinity in computer-aided drug design Protein Eng. 1994, 7, 385-391 (Pubitemid 24063137)
36. Böhm, H. J. The development of a simple empirical scoring function to estimate the binding constant for a protein-ligand complex of known three-dimensional structure J. Comput.-Aided Mol. Des. 1994, 8, 243-256
37. Head, R. D.; Smythe, M. L.; Oprea, T. I.; Waller, C. L.; Green, S. M.; Marshall, G. R. Validate a new method for the receptor-based prediction of binding affinities of novel ligands J. Am. Chem. Soc. 1996, 118, 3959-3969 (Pubitemid 26168541)
38. Wang, R.; Lai, L.; Wang, S. Further development and validation of empirical scoring functions for structure-based binding affinity prediction J. Comput.-Aided Mol. Des. 2002, 16, 11-26 (Pubitemid 34855041)
39. Zhang, S.; Golbraikh, A.; Oloff, S.; Kohn, H.; Tropsha, A. A novel automated lazy learning QSAR (ALL-QSAR) approach: method development, applications, and virtual screening of chemical databases using validated ALL-QSAR models J. Chem. Inf. Model. 2006, 46, 1984-1995 (Pubitemid 44625970)
40. Jain, A. N. Surflex-Dock 2.1: Robust performance from ligand energetic modeling, ring flexibility, and knowledge-based search J. Comput.-Aided Mol. Des. 2007, 21, 281-306 (Pubitemid 46630055)
41. Zsoldos, Z.; Reid, D.; Simon, A.; Sadjad, S. B.; Johnson, A. P. eHiTS: A new fast, exhaustive flexible ligand docking system J. Mol. Graphics Modell. 2007, 26, 198-212 (Pubitemid 46977244)
42. Huang, S.-Y.; Zou, X. Mean-force scoring functions for protein-ligand binding Annu. Rep. Comput. Chem. 2010, 6, 280-296
43. Verkhivker, G.; Appelt, K.; Freer, S. T.; Villafranca, J. E. Empirical free energy calculations of ligand-protein crystallographic complexes. I. Knowledge-based ligand-protein interaction potentials applied to the prediction of human immunodeficiency virus 1 protease binding affinity Protein Eng. 1995, 8, 677-691
44. Wallqvist, A.; Jernigan, R. L.; Covell, D. G. A preference-based free-energy parameterization of enzyme-inhibitor binding. Applications to HIV-1-protease inhibitor design Protein Sci. 1995, 4, 1881-1903
45. DeWitte, R. S.; Shakhnovich, E. I. SMoG: de Novo design method based on simple, fast, and accutate free energy estimate. 1. Methodology and supporting evidence J. Am. Chem. Soc. 1996, 118, 11733-11744 (Pubitemid 26417462)
46. Muegge, I.; Martin, Y. C. A general and fast scoring function for protein-ligand interactions: A simplified potential approach J. Med. Chem. 1999, 42, 791-804 (Pubitemid 29136170)
47. Muegge, I. PMF scoring revisited J. Med. Chem. 2006, 49, 5895-5902 (Pubitemid 44484936)
48. Gohlke, H.; Hendlich, M.; Klebe, G. Knowledge-based scoring function to predict protein-ligand interactions J. Mol. Biol. 2000, 295, 337-356 (Pubitemid 30045364)
49. CSD - Knowledge-based scoring function derived from small molecule crystal data with superior recognition rate of near-native ligand poses and better affinity prediction J. Med. Chem. 2005, 48, 6296-6303 (Pubitemid 41428984)
50. Mitchell, J. B. O.; Laskowski, R. A.; Alex, A.; Thornton, J. M. BLEEP - Potential of mean force describing protein-ligand interactions: I. Generating potential J. Comput. Chem. 1999, 20, 1165-1176 (Pubitemid 129651749)
51. Ishchenko, A. V.; Shakhnovich, E. I. Small molecule growth 2001 (SMoG2001): An improved knowledge-based scoring function for protein-ligand interactions J. Med. Chem. 2002, 45, 2770-2780 (Pubitemid 34627647)
52. Ozrin, V. D.; Subbotin, M. V.; Nikitin, S. M. PLASS: protein-ligand affinity statistical score - A knowledge-based force-field model of interaction derived from the PDB J. Comput.-Aided Mol. Des. 2004, 18, 261-270
53. Zhang, C.; Liu, S.; Zhu, Q.; Zhou, Y. A knowledge-based energy function for protein-ligand, protein-protein, and protein-DNA complexes J. Med. Chem. 2005, 48, 2325-2335 (Pubitemid 40516427)
54. Mooij, W. T. M.; Verdonk, M. L. General and targeted statistical potentials for protein-ligand interactions Proteins 2005, 61, 272-287 (Pubitemid 41429135)
55. Yang, C. Y.; Wang, R. X.; Wang, S. M. M-score: a knowledge-based potential scoring function accounting for protein atom mobility J. Med. Chem. 2006, 49, 5903-5911
56. Huang, S.-Y.; Zou, X. An iterative knowledge-based scoring function to predict protein-ligand interactions: I. Derivation of interaction potentials J. Comput. Chem. 2006, 27, 1866-1875 (Pubitemid 44672568)
57. Huang, S.-Y.; Zou, X. An iterative knowledge-based scoring function to predict protein-ligand interactions: II. Validation of the scoring function J. Comput. Chem. 2006, 27, 1876-1882 (Pubitemid 44672569)
58. Huang, S.-Y.; Zou, X. Inclusion of solvation and entropy in the knowledge-based scoring function for protein-ligand interactions J. Chem. Inf. Model. 2010, 50, 262-273
59. Tanaka, S.; Scheraga, H. A. Medium- and long-range interaction parameters between amino acids for predicting three-dimensional structures of proteins Macromolecules 1976, 9, 945-950
60. Miyazawa, S.; Jernigan, R. L. Estimation of effective interresidue contact energies from protein crystal structures: quasi-chemical approximation Macromolecules 1985, 18, 534-552
61. Sippl, M. J. Calculation of conformational ensembles from potentials of mean force J. Mol. Biol. 1990, 213, 859-883
62. Thomas, P. D.; Dill, K. A. An iterative method for extracting energy-like quantities from protein structures Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 11628-11633 (Pubitemid 26347173)
63. Thomas, P. D.; Dill, K. A. Statistical potentials extracted from protein structures: How accurate are they? J. Mol. Biol. 1996, 257, 457-469 (Pubitemid 26114046)
64. Koppensteiner, W. A.; Sippl, M. J. Knowledge-based potentials - Back to the roots Biochem. (Moscow) 1998, 63, 247-252 (Pubitemid 128588262)
65. McQuarrie, D. A. Statistical Mechanics; Harper Collins Publishers: New York, 1976.
66. Ewing, T. J. A.; Kuntz, I. D. Critical evaluation of search algorithms for automated molecular docking and database screening J. Comput. Chem. 1997, 18, 1175-1189 (Pubitemid 127650573)
67. Huang, S.-Y.; Zou, X. A statistical mechanics-based method to extract atomic distance-dependent potentials from protein structures. Proteins 2011, DOI: 10.1002/prot.23086, (in press).
68. Wang, R.; Fang, X.; Lu, Y.; Yang, C.-Y.; Wang, S. The PDBbind database: Methodologies and updates J. Med. Chem. 2005, 48, 4111-4119 (Pubitemid 40800619)
69. Wang, R.; Fang, X.; Lu, Y.; Wang, S. The PDBbind database: Collection of binding affinities for protein-ligand complexes with known three-dimensional structures J. Med. Chem. 2004, 47, 2977-2980 (Pubitemid 38702694)
70. Huang, S.-Y.; Zou, X. An iterative knowledge-based scoring function for protein-protein recognition Proteins 2008, 72, 557-579 (Pubitemid 351928512)
71. Jakalian, A.; Bush, B. L.; Jack, D. B.; Bayly, C. I. Fast, efficient generation of high-quality atomic charges. AM1-BCC model: I. Method J. Comput. Chem. 2000, 21, 132-146
72. 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 (Pubitemid 35330860)
73. Pettersen, E. F.; Goddard, T. D.; Huang, C. C.; Couch, G. S.; Greenblatt, D. M.; Meng, E. C.; Ferrin, T. E. UCSF Chimera - A visualization system for exploratory research and analysis J. Comput. Chem. 2004, 25, 1605-1612
74. Huang, S.-Y.; Zou, X. Ensemble docking of multiple protein structures: considering protein structural variations in molecular docking Proteins 2007, 66, 399-421 (Pubitemid 46053470)
75. Huang, S.-Y.; Zou, X. Efficient molecular docking of NMR structures: Application to HIV-1 protease Protein Sci. 2007, 16, 43-51 (Pubitemid 46036497)
76. Mesters, J. R.; Henning, K.; Hilgenfeld, R. Human glutamate carboxypeptidase II inhibition: structures of GCPII in complex with two potent inhibitors, quisqualate and 2-PMPA Acta Crystallogr., Sect. D: Biol. Crystallogr. 2007, 63, 508-513 (Pubitemid 46465946)
77. Zhang, D. W.; Xiang, Y.; Zhang, J. Z. H. New advance in computational chemistry: full quantum mechanical ab initio computation of streptavidin-biotin interaction energy J. Phys. Chem. B 2003, 107, 12039-12041
78. Δ-(N′-sulfodiaminophosphinyl)-l-ornithine, a true transition state analogue? Crystal structure and implications for catalytic mechanism J. Biol. Chem. 2000, 275, 20012-20019 (Pubitemid 30441609)
79. Ali, A.; Reddy, G. S.; Cao, H.; Anjum, S. G.; Nalam, M. N.; Schiffer, C. A.; Rana, T. M. Discovery of HIV-1 protease inhibitors with picomolar affinities incorporating N-aryl-oxazolidinone-5-carboxamides as novel P2 ligands J. Med. Chem. 2006, 49, 7342-7356 (Pubitemid 44913395)
80. Wang, R.; Lu, Y.; Wang, S. Comparative evaluation of 11 scoring functions for molecular docking J. Med. Chem. 2003, 46, 2287-2303 (Pubitemid 36637914)
81. Berman, H. M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T. N.; Weissig, H.; Shindyalov, I. N.; Bourne, P. E. The Protein Data Bank Nucleic Acids Res. 2000, 8, 235-242 (Pubitemid 30047768)