Neural-Network Scoring Functions Identify Structurally Novel Estrogen-Receptor Ligands

Journal of Chemical Information and Modeling

Volumn 55, Issue 9, 2015, Pages 1953-1961

  Durrant, Jacob D ^a   Carlson, Kathryn E ^b   Martin, Teresa A ^b   Offutt, Tavina L ^a   Mayne, Christopher G ^b   Katzenellenbogen, John A ^b   Amaro, Rommie E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIAGNOSIS; DRUG PRODUCTS; LIGANDS; MOLECULES;

DRUG DISCOVERY PROCESS; ESTROGEN RECEPTOR; EXPERIMENTAL TESTING; LEAD IDENTIFICATION; RESEARCH AND DEVELOPMENT; SCORING FUNCTIONS; SMALL MOLECULES; VIRTUAL SCREENING;

NEURAL NETWORKS;

ESTRADIOL; ESTROGEN RECEPTOR; LIGAND; PROTEIN BINDING;

ANTAGONISTS AND INHIBITORS; ARTIFICIAL NEURAL NETWORK; BIOLOGICAL MODEL; CHEMISTRY; COMPUTER SIMULATION; CONFORMATION; DRUG DEVELOPMENT; FACTUAL DATABASE; HUMAN;

COMPUTER SIMULATION; DATABASES, FACTUAL; DRUG DISCOVERY; ESTRADIOL; HUMANS; LIGANDS; MODELS, BIOLOGICAL; MOLECULAR CONFORMATION; NEURAL NETWORKS (COMPUTER); PROTEIN BINDING; RECEPTORS, ESTROGEN;

EID: 84942543577     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/acs.jcim.5b00241     Document Type: Article

References (54)

1. Eiler, S.; Gangloff, M.; Duclaud, S.; Moras, D.; Ruff, M. Overexpression, Purification, and Crystal Structure of Native Er Alpha Lbd Protein Expression Purif. 2001, 22, 165-173 10.1006/prep.2001.1409
2. Shiau, A. K.; Barstad, D.; Loria, P. M.; Cheng, L.; Kushner, P. J.; Agard, D. A.; Greene, G. L. The Structural Basis of Estrogen Receptor/Coactivator Recognition and the Antagonism of This Interaction by Tamoxifen Cell 1998, 95, 927-937 10.1016/S0092-8674(00)81717-1
3. Shiau, A. K.; Barstad, D.; Radek, J. T.; Meyers, M. J.; Nettles, K. W.; Katzenellenbogen, B. S.; Katzenellenbogen, J. A.; Agard, D. A.; Greene, G. L. Structural Characterization of a Subtype-Selective Ligand Reveals a Novel Mode of Estrogen Receptor Antagonism Nat. Struct. Biol. 2002, 9, 359-364 10.1038/nsb787
4. Stierand, K.; Maass, P. C.; Rarey, M. Molecular Complexes at a Glance: Automated Generation of Two-Dimensional Complex Diagrams Bioinformatics 2006, 22, 1710-1716 10.1093/bioinformatics/btl150
5. Rosenblatt, F. The Perceptron-a Probabilistic Model for Information-Storage and Organization in the Brain Psychol. Rev. 1958, 65, 386-408 10.1037/h0042519
6. Agrafiotis, D. K.; Cedeno, W.; Lobanov, V. S. On the Use of Neural Network Ensembles in Qsar and Qspr J. Chem. Inf. Model. 2002, 42, 903-911 10.1021/ci0203702
7. 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 10.1021/jm030580l
8. Wang, R.; Fang, X.; Lu, Y.; Yang, C. Y.; Wang, S. The Pdbbind Database: Methodologies and Updates J. Med. Chem. 2005, 48, 4111-4119 10.1021/jm048957q
9. Hu, L.; Benson, M. L.; Smith, R. D.; Lerner, M. G.; Carlson, H. A. Binding Moad (Mother of All Databases) Proteins: Struct., Funct., Genet. 2005, 60, 333-340 10.1002/prot.20512
10. Huang, S. Y.; Grinter, S. Z.; Zou, X. Q. Scoring Functions and Their Evaluation Methods for Protein-Ligand Docking: Recent Advances and Future Directions Phys. Chem. Chem. Phys. 2010, 12, 12899-12908 10.1039/c0cp00151a
11. Smith, R. D.; Dunbar, J. B.; Ung, P. M. U.; Esposito, E. X.; Yang, C. Y.; Wang, S. M.; Carlson, H. A. Csar Benchmark Exercise of 2010: Combined Evaluation across All Submitted Scoring Functions J. Chem. Inf. Model. 2011, 51, 2115-2131 10.1021/ci200269q
12. Plewczynski, D.; Lazniewski, M.; Augustyniak, R.; Ginalski, K. Can We Trust Docking Results? Evaluation of Seven Commonly Used Programs on Pdbbind Database J. Comput. Chem. 2011, 32, 742-755 10.1002/jcc.21643
13. Wang, J. C.; Lin, J. H. Scoring Functions for Prediction of Protein-Ligand Interactions Curr. Pharm. Des. 2013, 19, 2174-2182 10.2174/1381612811319120005
14. Cheng, T. J.; Li, Q. L.; Zhou, Z. G.; Wang, Y. L.; Bryant, S. H. Structure-Based Virtual Screening for Drug Discovery: A Problem-Centric Review AAPS J. 2012, 14, 133-141 10.1208/s12248-012-9322-0
15. Yuriev, E.; Agostino, M.; Ramsland, P. A. Challenges and Advances in Computational Docking: 2009 in Review J. Mol. Recognit. 2011, 24, 149-164 10.1002/jmr.1077
16. Meng, X. Y.; Zhang, H. X.; Mezei, M.; Cui, M. Molecular Docking: A Powerful Approach for Structure-Based Drug Discovery Curr. Comput.-Aided Drug Des. 2011, 7, 146-157 10.2174/157340911795677602
17. Durrant, J. D.; Friedman, A. J.; Rogers, K. E.; McCammon, J. A. Comparing Neural-Network Scoring Functions and the State of the Art: Applications to Common Library Screening J. Chem. Inf. Model. 2013, 53, 1726-1735 10.1021/ci400042y
18. 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 10.1021/ci100244v
19. Durrant, J. D.; McCammon, J. A. Nnscore 2.0: A Neural-Network Receptor-Ligand Scoring Function J. Chem. Inf. Model. 2011, 51, 2897-2903 10.1021/ci2003889
20. 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 10.1093/bioinformatics/btq112
21. Lindert, S.; Zhu, W.; Liu, Y. L.; Pang, R.; Oldfield, E.; McCammon, J. A. Farnesyl Diphosphate Synthase Inhibitors from in Silico Screening Chem. Biol. Drug Des. 2013, 81, 742-748 10.1111/cbdd.12121
22. Zhu, W.; Zhang, Y.; Sinko, W.; Hensler, M. E.; Olson, J.; Molohon, K. J.; Lindert, S.; Cao, R.; Li, K.; Wang, K.; Wang, Y.; Liu, Y. L.; Sankovsky, A.; de Oliveira, C. A.; Mitchell, D. A.; Nizet, V.; McCammon, J. A.; Oldfield, E. Antibacterial Drug Leads Targeting Isoprenoid Biosynthesis Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 123-128 10.1073/pnas.1219899110
23. Ballester, P. J.; Mangold, M.; Howard, N. I.; Robinson, R. L. M.; 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 10.1098/rsif.2012.0569
24. Barrett-Connor, E.; Mosca, L.; Collins, P.; Geiger, M. J.; Grady, D.; Kornitzer, M.; McNabb, M. A.; Wenger, N. K. Effects of Raloxifene on Cardiovascular Events and Breast Cancer in Postmenopausal Women N. Engl. J. Med. 2006, 355, 125-137 10.1056/NEJMoa062462
25. Jordan, V. C. Fourteenth Gaddum Memorial Lecture-University of Cambridge-January 1993-a Current View of Tamoxifen for the Treatment and Prevention of Breast Cancer Br. J. Pharmacol. 2000, 131, 221-231
26. Pfeifer, S.; Fritz, M.; Lobo, R.; McClure, R. D.; Goldberg, J.; Thomas, M.; Pisarska, M.; Widra, E.; Schattman, G.; Licht, M.; Sandlow, J.; Collins, J.; Cedars, M.; Rosen, M.; Vernon, M.; Racowsky, C.; Davis, O.; Dumesic, D.; Odem, R.; Barnhart, K.; Gracia, C.; Catherino, W.; Rebar, R.; La Barbera, A.; Med, A. S. R. Use of Clomiphene Citrate in Infertile Women: A Committee Opinion Fertil. Steril. 2013, 100, 341-348 10.1016/j.fertnstert.2013.05.033
27. Unkila, M.; Kari, S.; Yatkin, E.; Lammintausta, R. Vaginal Effects of Ospemifene in the Ovariectomized Rat Preclinical Model of Menopause J. Steroid Biochem. Mol. Biol. 2013, 138, 107-115 10.1016/j.jsbmb.2013.04.004
28. Shabsigh, A.; Kang, Y.; Shabsign, R.; Gonzalez, M.; Liberson, G.; Fisch, H.; Goluboff, E. Clomiphene Citrate Effects on Testosterone/Estrogen Ratio in Male Hypogonadism J. Sex. Med. 2005, 2, 716-721 10.1111/j.1743-6109.2005.00075.x
29. Durrant, J. D.; McCammon, J. A. Binana: A Novel Algorithm for Ligand-Binding Characterization J. Mol. Graphics Modell. 2011, 29, 888-893 10.1016/j.jmgm.2011.01.004
30. 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. 2009, 31, 455-461 10.1002/jcc.21334
31. Manas, E. S.; Xu, Z. B.; Unwalla, R. J.; Somers, W. S. Understanding the Selectivity of Genistein for Human Estrogen Receptor-Beta Using X-Ray Crystallography and Computational Methods Structure 2004, 12, 2197-2207
32. Dahlman-Wright, K.; Cavailles, V.; Fuqua, S. A.; Jordan, V. C.; Katzenellenbogen, J. A.; Korach, K. S.; Maggi, A.; Muramatsu, M.; Parker, M. G.; Gustafsson, J. A. International Union of Pharmacology. Lxiv. Estrogen Receptors Pharmacol. Rev. 2006, 58, 773-781 10.1124/pr.58.4.8
33. Paterni, I.; Bertini, S.; Granchi, C.; Macchia, M.; Minutolo, F. Estrogen Receptor Ligands: A Patent Review Update Expert Opin. Ther. Pat. 2013, 23, 1247-1271 10.1517/13543776.2013.805206
34. Minutolo, F.; Macchia, M.; Katzenellenbogen, B. S.; Katzenellenbogen, J. A. Estrogen Receptor Beta Ligands: Recent Advances and Biomedical Applications Med. Res. Rev. 2011, 31, 364-442 10.1002/med.20186
35. Katzenellenbogen, B. S.; Katzenellenbogen, J. A. Biomedicine-Defining the "S" in Serms Science 2002, 295, 2380-2381 10.1126/science.1070442
36. Huang, N.; Shoichet, B. K.; Irwin, J. J. Benchmarking Sets for Molecular Docking J. Med. Chem. 2006, 49, 6789-6801 10.1021/jm0608356
37. 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 10.1021/jm0306430
38. Gee, A. C.; Katzenellenbogen, J. A. Probing Conformational Changes in the Estrogen Receptor: Evidence for a Partially Unfolded Intermediate Facilitating Ligand Binding and Release Mol. Endocrinol. 2001, 15, 421-428 10.1210/mend.15.3.0602
39. Katzenellenbogen, J. A. The 2010 Philip S. Portoghese Medicinal Chemistry Lectureship: Addressing the "Core Issue" in the Design of Estrogen Receptor Ligands J. Med. Chem. 2011, 54, 5271-5282 10.1021/jm200801h
40. Nettles, K. W.; Bruning, J. B.; Gil, G.; O'Neill, E. E.; Nowak, J.; Hughs, A.; Kim, Y.; DeSombre, E. R.; Dilis, R.; Hanson, R. N.; Joachimiak, A.; Greene, G. L. Structural Plasticity in the Oestrogen Receptor Ligand-Binding Domain EMBO Rep. 2007, 8, 563-568 10.1038/sj.embor.7400963
41. Durrant, J. D.; McCammon, J. A. Computer-Aided Drug-Discovery Techniques That Account for Receptor Flexibility Curr. Opin. Pharmacol. 2010, 10, 770-774 10.1016/j.coph.2010.09.001
42. Carlson, K. E.; Choi, I.; Gee, A.; Katzenellenbogen, B. S.; Katzenellenbogen, J. A. Altered Ligand Binding Properties and Enhanced Stability of a Constitutively Active Estrogen Receptor: Evidence That an Open Pocket Conformation Is Required for Ligand Interaction Biochemistry 1997, 36, 14897-14905 10.1021/bi971746l
43. Chen, Z.; Tian, G. H.; Wang, Z.; Jiang, H. L.; Shen, J. S.; Zhu, W. L. Multiple Pharmacophore Models Combined with Molecular Docking: A Reliable Way for Efficiently Identifying Novel Pde4 Inhibitors with High Structural Diversity J. Chem. Inf. Model. 2010, 50, 615-625 10.1021/ci9004173
44. Warren, G. L.; Andrews, C. W.; Capelli, A. M.; Clarke, B.; LaLonde, J.; Lambert, M. H.; Lindvall, M.; Nevins, N.; Semus, S. F.; Senger, S.; Tedesco, G.; Wall, I. D.; Woolven, J. M.; Peishoff, C. E.; Head, M. S. A Critical Assessment of Docking Programs and Scoring Functions J. Med. Chem. 2006, 49, 5912-5931 10.1021/jm050362n
45. Langdon, S. R.; Blagg, J.; Brown, N. Scaffold Diversity in Medicinal Chemistry Space. In Scaffold Hopping in Medicinal Chemistry; Wiley-VCH Verlag GmbH & Co. KGaA, 2013; pp 39-60.
46. Hu, Y.; Stumpfe, D.; Bajorath, J. Lessons Learned from Molecular Scaffold Analysis J. Chem. Inf. Model. 2011, 51, 1742-1753 10.1021/ci200179y
47. Langdon, S. R.; Brown, N.; Blagg, J. Scaffold Diversity of Exemplified Medicinal Chemistry Space J. Chem. Inf. Model. 2011, 51, 2174-2185 10.1021/ci2001428
48. Bemis, G. W.; Murcko, M. A. The Properties of Known Drugs 0.1. Molecular Frameworks J. Med. Chem. 1996, 39, 2887-2893 10.1021/jm9602928
49. Krier, M.; Bret, G.; Rognan, D. Assessing the Scaffold Diversity of Screening Libraries J. Chem. Inf. Model. 2006, 46, 512-524 10.1021/ci050352v
50. Brzozowski, A. M.; Pike, A. C. W.; Dauter, Z.; Hubbard, R. E.; Bonn, T.; Engstrom, O.; Ohman, L.; Greene, G. L.; Gustafsson, J. A.; Carlquist, M. Molecular Basis of Agonism and Antagonism in the Oestrogen Receptor Nature 1997, 389, 753-758 10.1038/39645
51. Durrant, J. D.; Amaro, R. E. Machine-Learning Techniques Applied to Antibacterial Drug Discovery Chem. Biol. Drug Des. 2015, 85, 14-21 10.1111/cbdd.12423
52. Katzenellenbogen, J. A.; Johnson, H. J.; Myers, H. N. Photoaffinity Labels for Estrogen Binding Proteins of Rat Uterus Biochemistry 1973, 12, 4085-4092 10.1021/bi00745a010
53. De Angelis, M.; Stossi, F.; Carlson, K. A.; Katzenellenbogen, B. S.; Katzenellenbogen, J. A. Indazole Estrogens: Highly Selective Ligands for the Estrogen Receptor Beta J. Med. Chem. 2005, 48, 1132-1144 10.1021/jm049223g
54. Rdkit: Open-Source Cheminformatics. http://www.rdkit.org/.