Does a more precise chemical description of protein-ligand complexes lead to more accurate prediction of binding affinity?

Journal of Chemical Information and Modeling

Volumn 54, Issue 3, 2014, Pages 944-955

  Ballester, Pedro J ^a   Schreyer, Adrian ^b   Blundell, Tom L ^b  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; COMPLEXATION; COMPUTATION THEORY; FORECASTING; LIGANDS; PROTEINS; REGRESSION ANALYSIS;

ACCURATE PREDICTION; COMPUTATIONAL PREDICTIONS; CONFORMATIONAL HETEROGENEITY; INTERMOLECULAR INTERACTIONS; MACROMOLECULAR TARGETS; NUMERICAL EXPERIMENTS; PROTEIN-LIGAND COMPLEXES; STRUCTURE BASED DRUG DESIGNS;

DESCRIBING FUNCTIONS;

LIGAND; PROTEIN; PROTEIN BINDING;

ARTIFICIAL INTELLIGENCE; BIOLOGICAL MODEL; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN CONFORMATION; PROTEIN DATABASE;

ARTIFICIAL INTELLIGENCE; COMPUTATIONAL BIOLOGY; DATABASES, PROTEIN; LIGANDS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEINS;

EID: 84897010735     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci500091r     Document Type: Article

References (59)

1. Song, L.; Kalyanaraman, C.; Fedorov, A. A.; Fedorov, E. V.; Glasner, M. E.; Brown, S.; Imker, H. J.; Babbitt, P. C.; Almo, S. C.; Jacobson, M. P.; Gerlt, J. A. Prediction and Assignment of Function for a Divergent N-Succinyl Amino Acid Racemase Nat. Chem. Biol. 2007, 3, 486-491
2. Hermann, J. C.; Marti-Arbona, R.; Fedorov, A. A.; Fedorov, E.; Almo, S. C.; Shoichet, B. K.; Raushel, F. M. Structure-Based Activity Prediction for an Enzyme of Unknown Function Nature 2007, 448, 775-779
3. Jorgensen, W. L. Efficient Drug Lead Discovery and Optimization Acc. Chem. Res. 2009, 42, 724-733
4. Schneider, G.; Böhm, H.-J. Virtual Screening and Fast Automated Docking Methods Drug Discovery Today 2002, 7, 64-70
5. Leach, A. R.; Shoichet, B. K.; Peishoff, C. E. Prediction of Protein-Ligand Interactions. Docking and Scoring: Successes and Gaps J. Med. Chem. 2006, 49, 5851-5855
6. Moitessier, N.; Englebienne, P.; Lee, D.; Lawandi, J.; Corbeil, C. R. Towards the Development of Universal, Fast and Highly Accurate Docking/scoring Methods: A Long Way to Go Br. J. Pharmacol. 2008, 153 (Suppl) S7-26
7. Novikov, F. N.; Zeifman, A. A.; Stroganov, O. V.; Stroylov, V. S.; Kulkov, V.; Chilov, G. G. CSAR Scoring Challenge Reveals the Need for New Concepts in Estimating Protein-Ligand Binding Affinity J. Chem. Inf. Model. 2011, 51, 2090-2096
8. Huang, N.; Kalyanaraman, C.; Bernacki, K.; Jacobson, M. P. Molecular Mechanics Methods for Predicting Protein-Ligand Binding Phys. Chem. Chem. Phys. 2006, 8, 5166-5177
9. Ewing, T. J.; Makino, S.; Skillman, A. G.; Kuntz, I. D. DOCK 4.0: Search Strategies for Automated Molecular Docking of Flexible Molecule Databases J. Comput. Mol. Des. 2001, 15, 411-428
10. 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
11. Gehlhaar, D. K.; Verkhivker, G. M.; Rejto, P. A.; Sherman, C. J.; Fogel, D. B.; Fogel, L. J.; Freer, S. T. Molecular Recognition of the Inhibitor AG-1343 by HIV-1 Protease: Conformationally Flexible Docking by Evolutionary Programming Chem. Biol. 1995, 2, 317-324
12. 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
13. Mooij, W. T. M.; Verdonk, M. L. General and Targeted Statistical Potentials for Protein-Ligand Interactions Proteins 2005, 61, 272-287
14. Gohlke, H.; Hendlich, M.; Klebe, G. Knowledge-Based Scoring Function to Predict Protein-Ligand Interactions J. Mol. Biol. 2000, 295, 337-356
15. 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. Mol. Des. 1994, 8, 243-256
16. Eldridge, M. D.; Murray, C. W.; Auton, T. R.; Paolini, G. V.; Mee, R. P. Empirical Scoring Functions: I. The Development of a Fast Empirical Scoring Function to Estimate the Binding Affinity of Ligands in Receptor Complexes J. Comput.-Aided Mol. Des. 1997, 11, 425-445
17. Wang, R.; Lai, L.; Wang, S. Further Development and Validation of Empirical Scoring Functions for Structure-Based Binding Affinity Prediction J. Comput. Mol. Des. 2002, 16, 11-26
18. 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
19. Krammer, A.; Kirchhoff, P. D.; Jiang, X.; Venkatachalam, C. M.; Waldman, M. LigScore: A Novel Scoring Function for Predicting Binding Affinities J. Mol. Graphics Model. 2005, 23, 395-407
20. Michel, J.; Essex, J. W. Prediction of Protein-ligand Binding Affinity by Free Energy Simulations: Assumptions, Pitfalls and Expectations J. Comput.-Aided Mol. Des. 2010, 24, 639-658
21. Mobley, D. L. Lets Get Honest about Sampling J. Comput. Mol. Des. 2012, 26, 93-95
22. Guvench, O.; MacKerell, A. D. Computational Evaluation of Protein-Small Molecule Binding Curr. Opin. Struct. Biol. 2009, 19, 56-61
23. Ballester, P. J.; Mitchell, J. B. O. A Machine Learning Approach to Predicting Protein-Ligand Binding Affinity with Applications to Molecular Docking Bioinformatics 2010, 26, 1169-1175
24. Baum, B.; Muley, L.; Smolinski, M.; Heine, A.; Hangauer, D.; Klebe, G. Non-Additivity of Functional Group Contributions in Protein-Ligand Binding: A Comprehensive Study by Crystallography and Isothermal Titration Calorimetry J. Mol. Biol. 2010, 397, 1042-1054
25. Arunan, E.; Desiraju, G. R.; Klein, R. A.; Sadlej, J.; Scheiner, S.; Alkorta, I.; Clary, D. C.; Crabtree, R. H.; Dannenberg, J. J.; Hobza, P.; Kjaergaard, H. G.; Legon, A. C.; Mennucci, B.; Nesbitt, D. J. Definition of the Hydrogen Bond (IUPAC Recommendations 2011) Pure Appl. Chem. 2011, 83, 1637-1641
26. Snyder, P. W.; Mecinović, J.; Moustakas, D. T.; Thomas, S. W.; Harder, M.; Mack, E. T.; Lockett, M. R.; Héroux, A.; Sherman, W.; Whitesides, G. M. Mechanism of the Hydrophobic Effect in the Biomolecular Recognition of Arylsulfonamides by Carbonic Anhydrase Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 17889-17894
27. Li, L.; Li, J.; Khanna, M.; Jo, I.; Baird, J. P.; Meroueh, S. O. Docking to Erlotinib Off-Targets Leads to Inhibitors of Lung Cancer Cell Proliferation with Suitable in Vitro Pharmacokinetics ACS Med. Chem. Lett. 2010, 1, 229-233
28. Durrant, J. D.; McCammon, J. A. NNScore: A Neural-Network-Based Scoring Function for the Characterization of Protein-Ligand Complexes J. Chem. Inf. Model. 2010, 50, 1865-1871
29. Ballester, P. J.; Mitchell, J. B. O. Comments on "Leave-Cluster-out Cross-Validation Is Appropriate for Scoring Functions Derived from Diverse Protein Data Sets": Significance for the Validation of Scoring Functions J. Chem. Inf. Model. 2011, 51, 1739-1741
30. Kinnings, S. L.; Liu, N.; Tonge, P. J.; Jackson, R. M.; Xie, L.; Bourne, P. E. A Machine Learning-Based Method To Improve Docking Scoring Functions and Its Application to Drug Repurposing J. Chem. Inf. Model. 2011, 51, 408-419
31. Cheng, T.; Li, Q.; Zhou, Z.; Wang, Y.; Bryant, S. H. Structure-Based Virtual Screening for Drug Discovery: A Problem-Centric Review AAPS J. 2012, 14, 133-41
32. Lahti, J. L.; Tang, G. W.; Capriotti, E.; Liu, T.; Altman, R. B. Bioinformatics and Variability in Drug Response: A Protein Structural Perspective J. R. Soc. Interface 2012, 9, 1409-37
33. Sotriffer, C. Scoring Functions for Protein-Ligand Interactions; Gohlke, H., Ed.; Wiley-VCH Verlag GmbH & Co. KGaA: Weinheim, Germany, 2012; pp 237-263.
34. Das, S.; Krein, M. P.; Breneman, C. M. Binding Affinity Prediction with Property-Encoded Shape Distribution Signatures J. Chem. Inf. Model. 2010, 50, 298-308
35. Li, L.; Wang, B.; Meroueh, S. O. Support Vector Regression Scoring of Receptor-Ligand Complexes for Rank-Ordering and Virtual Screening of Chemical Libraries J. Chem. Inf. Model. 2011, 51, 2132-2138
36. Durrant, J. D.; McCammon, J. A. NNScore 2.0: A Neural-Network Receptor-Ligand Scoring Function J. Chem. Inf. Model. 2011, 51, 2897-2903
37. Ballester, P. J.; Mangold, M.; Howard, N. I.; Robinson, R. L. M. L.; Abell, C.; Blumberger, J.; Mitchell, J. B. O. Hierarchical Virtual Screening for the Discovery of New Molecular Scaffolds in Antibacterial Hit Identification J. R. Soc., Interface 2012, 9, 3196-3207
38. Deng, Z.; Chuaqui, C.; Singh, J. Structural Interaction Fingerprint (SIFt): A Novel Method for Analyzing Three-Dimensional Protein-Ligand Binding Interactions J. Med. Chem. 2004, 47, 337-344
39. Schreyer, A.; Blundell, T. CREDO: A Protein-Ligand Interaction Database for Drug Discovery Chem. Biol. Drug Des. 2009, 73, 157-167
40. Allen, F. H.; Baalham, C. A.; Lommerse, J. P. M.; Raithby, P. R. Carbonyl-Carbonyl Interactions Can Be Competitive with Hydrogen Bonds Acta Crystallogr., Sect. B: Struct. Sci. 1998, 54, 320-329
41. OBoyle, N. M.; Morley, C.; Hutchison, G. R. Pybel: A Python Wrapper for the OpenBabel Cheminformatics Toolkit Chem. Cent. J. 2008, 2, 1-7
42. Jones, E.; Oliphant, T.; Peterson, P.; SciPy: Open source scientific tools for Python. http://www.scipy.org/.
43. Breiman, L. Random Forests Mach. Learn. 2001, 45, 5-32
44. Cheng, T.; Li, X.; Li, Y.; Liu, Z.; Wang, R. Comparative Assessment of Scoring Functions on a Diverse Test Set J. Chem. Inf. Model. 2009, 49, 1079-1093
45. 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
46. Rognan, D.; Lauemoller, S. L.; Holm, A.; Buus, S.; Tschinke, V. Predicting Binding Affinities of Protein Ligands from Three-Dimensional Models: Application to Peptide Binding to Class I Major Histocompatibility Proteins J. Med. Chem. 1999, 42, 4650-4658
47. Fan, H.; Schneidman-Duhovny, D.; Irwin, J. J.; Dong, G.; Shoichet, B. K.; Sali, A. Statistical Potential for Modeling and Ranking of Protein-Ligand Interactions J. Chem. Inf. Model. 2011, 51, 3078-3092
48. Smith, R. D.; Dunbar, J. B.; Ung, P. M.-U.; Esposito, E. X.; Yang, C.-Y.; Wang, S.; Carlson, H. A. CSAR Benchmark Exercise of 2010: Combined Evaluation Across All Submitted Scoring Functions J. Chem. Inf. Model. 2011, 51, 2115-2131
49. Hayik, S. A.; Dunbrack, R.; Merz, K. M. A Mixed QM/MM Scoring Function to Predict Protein-Ligand Binding Affinity J. Chem. Theory Comput. 2010, 6, 3079-3091
50. Caravella, J. A.; Carbeck, J. D.; Duffy, D. C.; Whitesides, G. M.; Tidor, B. Long-Range Electrostatic Contributions to Protein-Ligand Binding Estimated Using Protein Charge Ladders, Affinity Capillary Electrophoresis, and Continuum Electrostatic Theory J. Am. Chem. Soc. 1999, 121, 4340-4347
51. Piana, S.; Lindorff-Larsen, K.; Dirks, R. M.; Salmon, J. K.; Dror, R. O.; Shaw, D. E. Evaluating the Effects of Cutoffs and Treatment of Long-Range Electrostatics in Protein Folding Simulations PLoS One 2012, 7, e39918
52. Norberg, J.; Nilsson, L. On the Truncation of Long-Range Electrostatic Interactions in DNA Biophys. J. 2000, 79, 1537-1553
53. Sotriffer, C. A.; Sanschagrin, P.; Matter, H.; Klebe, G. SFCscore: Scoring Functions for Affinity Prediction of Protein-Ligand Complexes Proteins 2008, 73, 395-419
54. Zilian, D.; Sotriffer, C. A. SFCscore(RF): A Random Forest-Based Scoring Function for Improved Affinity Prediction of Protein-Ligand Complexes J. Chem. Inf. Model. 2013, 53, 1923-1933
55. Li, G.-B.; Yang, L.-L.; Wang, W.-J.; Li, L.-L.; Yang, S.-Y. ID-Score: A New Empirical Scoring Function Based on a Comprehensive Set of Descriptors Related to Protein-Ligand Interactions J. Chem. Inf. Model. 2013, 53, 592-600
56. Sukumar, N.; Das, S. Current Trends in Virtual High Throughput Screening Using Ligand-Based and Structure-Based Methods Comb. Chem. High Throughput Screening 2011, 14, 872-888
57. Furnham, N.; Blundell, T. L.; DePristo, M. A.; Terwilliger, T. C. Is One Solution Good Enough? Nat. Struct. Mol. Biol. 2006, 13, 184-185
58. Li, H.; Leung, K.-S.; Ballester, P. J.; Wong, M.-H. Istar: A Web Platform for Large-Scale Protein-Ligand Docking PLoS One 2014, 9, e85678
59. Irwin, J. J.; Sterling, T.; Mysinger, M. M.; Bolstad, E. S.; Coleman, R. G. ZINC: A Free Tool to Discover Chemistry for Biology J. Chem. Inf. Model. 2012, 52, 1757-1768