Assessing molecular docking tools for relative biological activity prediction: A case study of triazole HIV-1 NNRTIs

Journal of Chemical Information and Modeling

Volumn 53, Issue 12, 2013, Pages 3326-3342

  Fraì̈czek, Tomasz ^a   Siwek, Agata ^a,b   Paneth, Piotr ^a  

^a LODZ UNIVERSITY OF TECHNOLOGY   (Poland)

^b MEDICAL UNIVERSITY OF LUBLIN   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

FORECASTING; MOLECULAR MODELING;

1 ,2 ,4-TRIAZOLE; COMPARATIVE STUDIES; DIFFERENT PROTOCOLS; DOCKING PROGRAMS; MOLECULAR DOCKING; NON-NUCLEOSIDE REVERSE TRANSCRIPTASE INHIBITORS; RELATED COMPOUNDS; SCORING FUNCTIONS;

BIOACTIVITY;

1,2,4 TRIAZOLE; 1,2,4-TRIAZOLE; LIGAND; RNA DIRECTED DNA POLYMERASE; RNA DIRECTED DNA POLYMERASE INHIBITOR; TRIAZOLE DERIVATIVE;

ARTICLE; CHEMISTRY; COMPUTER PROGRAM; DRUG ANTAGONISM; DRUG DEVELOPMENT; ENZYME ACTIVE SITE; ENZYMOLOGY; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR DOCKING; PROTEIN BINDING; THERMODYNAMICS;

CATALYTIC DOMAIN; DRUG DISCOVERY; HIV REVERSE TRANSCRIPTASE; HIV-1; LIGANDS; MOLECULAR DOCKING SIMULATION; PROTEIN BINDING; REVERSE TRANSCRIPTASE INHIBITORS; SOFTWARE; THERMODYNAMICS; TRIAZOLES;

EID: 84896532392     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci400427a     Document Type: Article

References (72)

1. Baldwin, J. J.; Ponticello, G. S.; Anderson, P. S.; Christy, M. E.; Murcko, M. A.; Randall, W. C.; Schwam, H.; Sugrue, M. F.; Springer, J. P.; Gautheron, P.; Grove, J.; Mallorga, P.; Viader, M. P.; McKeever, B. M.; Navia, M. A. Thienothiopyran-2-sulfonamides: Novel topically active carbonic anhydrase inhibitors for the treatment of glaucoma J. Med. Chem. 1989, 32, 2510-2513
2. Von Itzstein, M.; Wu, W. Y.; Kok, G. B.; Pegg, M. S.; Dyason, J. C.; Jin, B.; Phan, T. V.; Smythe, M. L.; White, H. F.; Oliver, S. W.; Colman, P. M.; Varghese, J. N.; Ryan, D. M.; Woods, J. M.; Bethell, R. C.; Hotham, V. J.; Cameron, J. M.; Penn, C. R. Rational design of potent sialidase-based inhibitors of influenza virus replication Nature 1993, 363, 418-423
3. Schames, J. R.; Henchman, R. H.; Siegel, J. S.; Sotriffer, C. A.; Ni, H.; McCammon, J. A. Discovery of a novel binding trench in HIV integrase J. Med. Chem. 2004, 47, 1879-1881
4. Rahuel, J.; Rasetti, V.; Maibaum, J.; Rüeger, H.; Göschke, R.; Cohen, N. C.; Stutz, S.; Cumin, F.; Fuhrer, W.; Wood, J. M.; Grütter, M. G. Structure-based drug design: The discovery of novel nonpeptide orally active inhibitors of human renin Chem. Biol. 2000, 7, 493-504
5. Burkhard, P.; Hommel, U.; Sanner, M.; Walkinshaw, M. D. The discovery of steroids and other novel FKBP inhibitors using a molecular docking program J. Mol. Biol. 1999, 287, 853-858
6. Perola, E.; Xu, K.; Kollmeyer, T. M.; Kaufmann, S. H.; Prendergast, F. G.; Pang, Y. P. Successful virtual screening of a chemical database for farnesyltransferase inhibitor leads J. Med. Chem. 2000, 43, 401-408
7. Böhm, H. J.; Banner, D. W.; Weber, L. Combinatorial docking and combinatorial chemistry: Design of potent non-peptide thrombin inhibitors J. Comput.-Aided Mol. Des. 1999, 13, 51-56
8. Bressi, J. C.; Verlinde, C. L. M. J.; Aronov, A. M.; Shaw, M. L.; Shin, S. S.; Nguyen, L. N.; Suresh, S.; Buckner, F. S.; Van Voorhis, W. C.; Kuntz, I. D.; Hol, W. G. J.; Gelb, M. H. Adenosine analogues as selective inhibitors of glyceraldehyde-3-phosphate dehydrogenase of trypanosomatidae via structure-based drug design J. Med. Chem. 2001, 44, 2080-2093
9. Iwata, Y.; Arisawa, M.; Hamada, R.; Kita, Y.; Mizutani, M. Y.; Tomioka, N.; Itai, A.; Miyamoto, S. Discovery of Novel Aldose Reductase Inhibitors Using a protein structure-based approach: 3D-database search followed by design and synthesis J. Med. Chem. 2001, 44, 1718-1728
10. Kawada, H.; Ebiike, H.; Tsukazaki, M.; Nakamura, M.; Morikami, K.; Yoshinari, K.; Yoshida, M.; Ogawa, K.; Shimma, N.; Tsukuda, T.; Ohwada, J. Lead optimization of a dihydropyrrolopyrimidine inhibitor against phosphoinositide 3-kinase (PI3K) to improve the phenol glucuronic acid conjugation Bioorg. Med. Chem. Lett. 2013, 23, 673-678
11. 1 receptor Bioorg. Med. Chem. Lett. 2013, 23, 2868-2871
12. Sengupta, S.; Obiorah, I.; Maximov, P. Y.; Curpan, R.; Jordan, V. C. Molecular mechanism of action of bisphenol and bisphenol A mediated by oestrogenreceptor alpha in growth and apoptosis of breast cancer cells Br. J. Pharmacol. 2013, 169, 167-178
13. Filikov, A. V.; Mohan, V.; Vickers, T. A.; Griffey, R. H.; DanCook, P.; Abagyan, R. A.; James, T. L. Identification of ligands for RNA targets via structure-based virtual screening: HIV-1 TAR J. Comput.-Aided Mol. Des. 2000, 14, 593-610
14. Bissantz, C.; Folkers, G.; Rognan, D. Protein-based virtual screening of chemical databases. 1. Evaluation of different docking/scoring combinations J. Med. Chem. 2000, 43, 4759-4767
15. Caporuscio, F.; Rastelli, G.; Imbriano, C.; Del Rio, A. Structure-based design of potent aromatase inhibitors by high-throughput docking J. Med. Chem. 2011, 54, 4006-4017
16. 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
17. Ferrara, P.; Gohlke, H.; Price, D. J.; Klebe, G.; Brooks, C. L., III Assessing scoring functions for protein-ligand interactions J. Med. Chem. 2004, 47, 3032-3047
18. Wang, R.; Lu, Y.; Wang, S. Comparative evaluation of 11 scoring functions for molecular docking J. Med. Chem. 2003, 46, 2287-2303
19. Wang, R.; Lu, Y.; Fang, X.; Wang, S. An extensive test of 14 scoring functions using the PDB bind refined set of 800 protein-ligand complexes J. Chem. Inf. Comput. Sci. 2004, 44, 2114-2125
20. Kellenberger, E.; Rodrigo, J.; Muller, P.; Rognan, D. Comparative evaluation of eight docking tools for docking and virtual screening accuracy Proteins 2004, 57, 225-242
21. Kontoyianni, M.; McClellan, L. M.; Sokol, G. S. Evaluation of docking performance: Comparative data on docking algorithms J. Med. Chem. 2004, 47, 558-565
22. Houston, D. R.; Walkinshaw, M. D. Consensus docking: Improving the reliability of docking in a virtual screening context J. Chem. Inf. Model. 2013, 53, 384-390
23. Charifson, P. S.; Corkery, J. J.; Murcko, M. A.; Walters, W. P. Consensus scoring: A method for obtaining improved hit rates from docking databases of three-dimensional structures into proteins J. Med. Chem. 1999, 42, 5100-5109
24. Clark, R. D.; Strizhev, A.; Leonard, J. M.; Blake, J. F.; Matthew, J. B. Consensus scoring for ligand/protein interactions J. Mol. Graph. Modell. 2002, 20, 281-295
25. 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
26. Vaqué, M.; Ardévol, A.; Bladé, C.; Salvadó, M. J.; Blay, M.; Fernández-Larrea, J.; Arola, L.; Pujadas, G. Protein-ligand docking: A review of recent advances and future perspectives Curr. Pharm. Anal. 2008, 4, 1-19
27. Sivaprakasam, P.; Tosso, P. N.; Doerksen, R. J. Structure-activity relationship and comparative docking studies for cycloguanil analogs as Pf DHFR-TS inhibitors J. Chem. Inf. Model. 2009, 49, 1787-1796
28. Terp, G. E.; Johansen, B. N.; Christensen, I. T.; Jørgensen, F. S. A new concept for multidimensional selection of ligand conformations (multiselect) and multidimensional scoring (multiscore) of protein-ligand binding affinities J. Med. Chem. 2001, 44, 2333-2343
29. Stahl, M.; Rarey, M. Detailed analysis of scoring functions for virtual screening J. Med. Chem. 2001, 44, 1035-1042
30. Kirschberg, T. A.; Balakrishnan, M.; Huang, W.; Hluhanich, R.; Kutty, N.; Liclican, A. C.; McColl, D. J.; Squires, N. H.; Lansdon, E. B. Triazole derivatives as non-nucleoside inhibitors of HIV-1 reverse transcriptase: Structure-activity relationships and crystallographic analysis Bioorg. Med. Chem. Lett. 2008, 18, 1131-1134
31. De La Rosa, M.; Kim, H. W.; Gunic, E.; Jenket, C.; Boyle, U.; Koh, Y.; Korboukh, I.; Allan, M.; Zhang, W.; Chen, H.; Xu, W.; Nilar, S.; Yao, N.; Hamatake, R.; Lang, S. A.; Hong, Z.; Zhang, Z.; Girardet, J. L. Tri-substituted triazoles as potent non-nucleoside inhibitors of the HIV-1 reverse transcriptase Bioorg. Med. Chem. Lett. 2006, 16, 4444-4449
32. Muraglia, E.; Kinzel, O. D.; Laufer, R.; Miller, M. D.; Moyer, G.; Munshi, V.; Orvieto, F.; Palumbi, M. C.; Pescatore, G.; Rowley, M.; Williams, P. D.; Summa, V. Tetrazolethioacetanilides: Potent non-nucleoside inhibitors of WT HIV reverse transcriptase and its K103N mutant Bioorg. Med. Chem. Lett. 2006, 16, 2748-2752
33. Tucker, T. J.; Saggar, S.; Sisko, J. T.; Tynebor, R. M.; Williams, T. M.; Felock, P. J.; Flynn, J. A.; Lai, M. T.; Liang, Y.; McGaughey, G.; Liu, M.; Miller, M.; Moyer, G.; Munshi, V.; Perlow-Poehnelt, R.; Prasad, S.; Sanchez, R.; Torrent, M.; Vacca, J. P.; Wan, B. L.; Yan, Y. The design and synthesis of diaryl ether second generation HIV-1 non-nucleoside reverse transcriptase inhibitors (NNRTIs) with enhanced potency versus key clinical mutations Bioorg. Med. Chem. Lett. 2008, 18, 2959-2966
34. Zhang, Z.; Xu, W.; Koh, Y. H.; Shim, J. H.; Girardet, J. L.; Yeh, L. T.; Hamatake, R. K.; Hong, Z. A novel nonnucleoside analogue that inhibits human immunodeficiency virus type 1 isolates resistant to current nonnucleoside reverse transcriptase inhibitors Antimicrob. Agents Chemother. 2007, 51, 429-437
35. Su, D. S.; Lim, J. J.; Tinney, E.; Wan, B. L.; Young, M. B.; Anderson, K. D.; Rudd, D.; Munshi, V.; Bahnck, C.; Felock, P. J.; Lu, M.; Lai, M. T.; Touch, S.; Moyer, G.; DiStefano, D. J.; Flynn, J. A.; Liang, Y.; Sanchez, R.; Prasad, S.; Yan, Y.; Perlow-Poehnelt, R.; Torrent, M.; Miller, M.; Vacca, J. P.; Williams, T. M.; Anthony, N. J. Substituted tetrahydroquinolines as potent allosteric inhibitors of reverse transcriptase and its key mutants Bioorg. Med. Chem. Lett. 2009, 19, 5119-5123
36. Romines, K. R.; Freeman, G. A.; Schaller, L. T.; Cowan, J. R.; Gonzales, S. S.; Tidwell, J. H.; Andrews, C. W., III; Stammers, D. K.; Hazen, R. J.; Ferris, R. G.; Short, S. A.; Chan, J. H.; Boone, L. R. Structure-activity relationship studies of novel benzophenones leading to the discovery of a potent, next generation hiv nonnucleoside reverse transcriptase inhibitor J. Med. Chem. 2006, 49, 727-739
37. Zhan, P.; Liu, X.; Li, Z.; Fang, Z.; Li, Z.; Wang, D.; Pannecouque, C.; De Clercq, E. Novel 1,2,3-thiadiazole derivatives as HIV-1 NNRTIs with improved potency: Synthesis and preliminary SAR studies Bioorg. Med. Chem. 2009, 17, 5920-5927
38. Zhan, P.; Liu, X.; Cao, Y.; Wang, Y.; Pannecouque, C.; De Clercq, E. 1,2,3-thiadiazole thioacetanilides as a novel class of potent HIV-1 non-nucleoside reverse transcriptase inhibitors Bioorg. Med. Chem. Lett. 2008, 18, 5368-5371
39. Zhan, P.; Liu, X.; Li, Z.; Fang, Z.; Li, Z.; Pannecouque, C.; De Clercq, E. Synthesis and biological evaluation of imidazole thioacetanilides as novel non-nucleoside HIV-1 reverse transcriptase inhibitors Bioorg. Med. Chem. 2009, 17, 5775-5781
40. Glide, version 5.7; Schrödinger, LLC, New York, 2011.
41. 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
42. Halgren, T. A.; Murphy, R. B.; Friesner, R. A.; Beard, H. S.; Frye, L. L.; Pollard, W. T.; Banks, J. L. Glide: A new approach for rapid, accurate docking and scoring. 2. Enrichment factors in database screening J. Med. Chem. 2004, 47, 1750-1759
43. Thomsen, R.; Christensen, M. H. MolDock: A new technique for high-accuracy molecular docking J. Med. Chem. 2006, 49, 3315-3321
44. Rarey, M.; Kramer, B.; Lengauer, T.; Klebe, G. A fast flexible docking method using an incremental construction algorithm J. Mol. Biol. 1996, 261, 470-489
45. Trott, O.; Olson, A. J. AutoDockVina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization and multithreading J. Comput. Chem. 2010, 31, 455-461
46. Reulecke, I.; Lange, G.; Albrecht, J.; Klein, R.; Rarey, M. Towards an integrated description of hydrogen bonding and dehydration: Reducing false positives in virtual screening using the HYDE scoring function Chem. Med. Chem. 2008, 3, 885-897
47. Zhan, P.; Li, X.; Li, Z.; Chen, X.; Tian, Y.; Chen, W.; Liu, X.; Pannecouque, C.; De Clercq, E. Structure-based bioisosterism design, synthesis and biological evaluation of novel 1,2,4-triazin-6-ylthioacetamides as potent HIV-1 NNRTIs Bioorg. Med. Chem. Lett. 2012, 22, 7155-7162
48. Gagnon, A.; Amad, M. H.; Bonneau, P. R.; Coulombe, R.; DeRoy, P. L.; Doyon, L.; Duan, J.; Garneau, M.; Guse, I.; Jakalian, A.; Jolicoeur, E.; Landry, S.; Malenfant, E.; Simoneau, B.; Yoakim, C. Thiotetrazole alkynylacetanilides as potent and bioavailable non-nucleoside inhibitors of the HIV-1 wild type and K103N/Y181C double mutant reverse transcriptases Bioorg. Med. Chem. Lett. 2007, 17, 4437-4441
49. Gagnon, A.; Landry, S.; Coulombe, R.; Jakalian, A.; Guse, I.; Thavonekham, B.; Bonneau, P. R.; Yoakim, C.; Simoneau, B. Investigation on the role of the tetrazole in the binding of thiotetrazolylacetanilides with HIV-1 wild type and K103N/Y181C double mutant reverse transcriptases Bioorg. Med. Chem. Lett. 2009, 19, 1199-1205
50. Wang, Z.; Wu, B.; Kuhen, K. L.; Bursulaya, B.; Nguyen, T. N.; Nguyen, D. G.; He, Y. Synthesis and biological evaluations of sulfanyltriazoles as novel HIV-1 non-nucleoside reverse transcriptase inhibitors Bioorg. Med. Chem. Lett. 2006, 16, 4174-4177
51. Craig, I. R.; Essex, J. W.; Spiegel, K. Ensemble docking into multiple crystallographically derived protein structures: An evaluation based on the statistical analysis of enrichments J. Chem. Inf. Model. 2010, 50, 511-524
52. Rueda, M.; Bottegoni, G.; Abagyan, R. Recipes for the selection of experimental protein conformations for virtual screening J. Chem. Inf. Model. 2010, 50, 186-193
53. Lima, A. N.; Philot, E. A.; Perahia, D.; Braz, A. S. K.; Scott, L. P. B. GANM: A protein-ligand docking approach based on genetic algorithm and normal modes Appl. Math. Comput. 2012, 219, 511-520
54. Ding, F.; Yin, S.; Dokholyan, N. V. Rapid flexible docking using a stochastic rotamer library of ligands J. Chem. Inf. Model. 2010, 50, 1623-1632
55. Borrelli, K. W.; Cossins, B.; Guallar, V. Exploring hierarchical refinement techniques for induced fit docking with protein and ligand flexibility J. Comput. Chem. 2010, 31, 1224-1235
56. Antes, I. DynaDock: A new molecular dynamics-based algorithm for protein-peptide docking including receptor flexibility Proteins 2010, 78, 1084-1104
57. Whalen, K. L.; Chang, K. M.; Spies, M. A. Hybrid steered molecular dynamics-docking: An efficient solution to the problem of ranking inhibitor affinities against a flexible drug target Mol. Inf. 2011, 30, 459-471
58. Floquet, N.; Marechal, J. D.; Badet-Denisot, M. A.; Robert, C. H.; Dauchez, M.; Perahia, D. Using normal modes analysis as a prerequisite for drug design: Application to matrix metalloproteinase inhibitors FEBS Lett. 2006, 580, 5130-5136
59. Cavasotto, C. N.; Orry, A. J. W.; Abagyan, R. A. The challenge of considering receptor flexibility in ligand docking and virtual screening Curr. Comput.-Aided Drug Des. 2005, 1, 423-440
60. Chandrika, B.; Subramanian, J.; Sharma, S. D. Managing protein flexibility in docking and its applications Drug Discovery Today 2009, 14, 394-400
61. Schrödinger Suite 2011 Induced Fit Docking protocol; Glide version 5.7, Schrödinger, LLC, New York, 2011; Prime, version 3.0, Schrödinger, LLC, New York, 2011.
62. Sherman, W.; Day, T.; Jacobson, M. P.; Friesner, R. A.; Farid, R. Novel procedure for modeling ligand/receptor induced fit effects J. Med. Chem. 2006, 49, 534-553
63. Kendall, M. G. Rank Correlation Methods, 4 th ed.; Griffin: London, 1970; pp 29-48.
64. Friesner, R. A.; Murphy, R. B.; Repasky, M. P.; Frye, L. L.; Greenwood, J. R.; Halgren, T. A.; Sanschagrin, P. C.; Mainz, D. T. Extra Precision Glide: Docking and scoring incorporating a model of hydrophobic enclosure for protein ligand complexes J. Med. Chem. 2006, 49, 6177-6196
65. Jorgensen, W. L.; Tirado-Rives, J. The OPLS force field for proteins. Energy minimizations for crystals of cyclic peptides and crambin J. Am. Chem. Soc. 1988, 110, 1657-1666
66. LigPrep, version 2.5; Schrödinger, LLC, New York, 2011.
67. Schrödinger Suite 2011 Protein Preparation Wizard; Epik, version 2.2, Schrödinger, LLC, New York, 2011; Impact, version 5.7, Schrödinger, LLC, New York, 2011; Prime. version 3.0, Schrödinger, LLC, New York, 2011.
68. Sastry, G. M.; Adzhigirey, M.; Day, T.; Annabhimoju, R.; Sherman, W. Protein and ligand preparation: parameters, protocols, and influence on virtual screening enrichments J. Comput.-Aided Mol. Des. 2013, 27, 221-234
69. Monod, J.; Wyman, J.; Changeux, J.-P. On the nature of allosteric transitions: A plausible model J. Mol. Biol. 1965, 12, 88-118
70. Zhan, P.; Wang, L.; Liu, H.; Chen, X.; Li, X.; Jiang, X.; Zhang, Q.; Liu, X.; Pannecouque, C.; Naesens, L.; De Clercq, E.; Liu, A.; Du, G. Arylazolyl(azinyl)thioacetanilide. Part 9: Synthesis and biological investigation of thiazolylthioacetamides derivatives as a novel class of potential antiviral agents Arch. Pharm. Res. 2012, 35, 975-986
71. 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. Design 1997, 11, 425-445
72. LeadIT 2.1.0; BioSolveIT GmbH: St. Augustin, Germany, 2012.