Discovery of novel tubulin inhibitors via structure-based hierarchical virtual screening

Journal of Chemical Information and Modeling

Volumn 52, Issue 10, 2012, Pages 2730-2740

  Cao, Ran ^a,b   Liu, Minyu ^c,d   Yin, Min ^c   Liu, Quanhai ^d   Wang, Yanli ^b   Huang, Niu ^b  

^a TIANJIN UNIVERSITY   (China)

^b NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^c SHANGHAI JIAO TONG UNIVERSITY   (China)

^d SHANGHAI INSTITUTE OF PHARMACEUTICAL INDUSTRY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

SCAFFOLDS;

BINDING CHARACTERISTICS; EXPERIMENTAL VALIDATIONS; HIERARCHICAL STRATEGIES; INHIBITION ACTIVITY; STRUCTURAL INFORMATION; STRUCTURAL MODIFICATIONS; STRUCTURE ACTIVITY RELATIONSHIPS; TUBULIN POLYMERIZATION;

BINDERS;

2 (2 FLUOROBENZAMIDO) 3 CARBOXAMIDE 4,5 DIMETHYLTHIOPHENE; 2-(2-FLUOROBENZAMIDO)-3-CARBOXAMIDE-4,5-DIMETHYLTHIOPHENE; BENZAMIDE DERIVATIVE; COLCHICINE; LIGAND; THIOPHENE DERIVATIVE; TUBULIN; TUBULIN MODULATOR;

ALGORITHM; ARTICLE; BINDING SITE; CHEMISTRY; COMPUTER INTERFACE; DRUG DEVELOPMENT; HIGH THROUGHPUT SCREENING; HUMAN; MOLECULAR DOCKING; MOLECULAR LIBRARY; POLYMERIZATION; PROTEIN BINDING; STRUCTURE ACTIVITY RELATION; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

ALGORITHMS; BENZAMIDES; BINDING SITES; COLCHICINE; CRYSTALLOGRAPHY, X-RAY; DRUG DISCOVERY; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; LIGANDS; MOLECULAR DOCKING SIMULATION; POLYMERIZATION; PROTEIN BINDING; SMALL MOLECULE LIBRARIES; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS; THIOPHENES; TUBULIN; TUBULIN MODULATORS; USER-COMPUTER INTERFACE;

EID: 84867757394     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci300302c     Document Type: Article

References (66)

1. Jordan, M. A.; Wilson, L. Microtubules as a target for anticancer drugs Nat. Rev. Cancer 2004, 4, 253-265
2. Barbier, P.; Dorleans, A.; Devred, F.; Sanz, L.; Allegro, D.; Alfonso, C.; Knossow, M.; Peyrot, V.; Andreu, J. M. Stathmin and interfacial microtubule inhibitors recognize a naturally curved conformation of tubulin dimers J. Biol. Chem. 2010, 285, 31672-31681
3. Schmidt, M.; Bastians, H. Mitotic drug targets and the development of novel anti-mitotic anticancer drugs Drug Resist. Updates 2007, 10, 162-181
4. Massarotti, A.; Coluccia, A.; Silvestri, R.; Sorba, G.; Brancale, A. The tubulin colchicine domain: a molecular modeling perspective ChemMedChem 2012, 7, 33-42
5. Singh, P.; Rathinasamy, K.; Mohan, R.; Panda, D. Microtubule assembly dynamics: an attractive target for anticancer drugs IUBMB Life 2008, 60, 368-375
6. Kavallaris, M. Microtubules and resistance to tubulin-binding agents Nat. Rev. Cancer 2010, 10, 194-204
7. Risinger, A. L.; Giles, F. J.; Mooberry, S. L. Microtubule dynamics as a target in oncology Cancer Treat. Rev. 2009, 35, 255-261
8. Yoshimatsu, K.; Yamaguchi, A.; Yoshino, H.; Koyanagi, N.; Kitoh, K. Mechanism of action of E7010, an orally active sulfonamide antitumor agent: inhibition of mitosis by binding to the colchicine site of tubulin Cancer Res. 1997, 57, 3208-3213
9. Bacher, G.; Nickel, B.; Emig, P.; Vanhoefer, U.; Seeber, S.; Shandra, A.; Klenner, T.; Beckers, T. D-24851, a novel synthetic microtubule inhibitor, exerts curative antitumoral activity in vivo, shows efficacy toward multidrug-resistant tumor cells, and lacks neurotoxicity Cancer Res. 2001, 61, 392-399
10. Wienecke, A.; Bacher, G. Indibulin, a novel microtubule inhibitor, discriminates between mature neuronal and nonneuronal tubulin Cancer Res. 2009, 69, 171-177
11. Tozer, G. M.; Kanthou, C.; Baguley, B. C. Disrupting tumour blood vessels Nat. Rev. Cancer 2005, 5, 423-435
12. Kanthou, C.; Tozer, G. M. Microtubule depolymerizing vascular disrupting agents: novel therapeutic agents for oncology and other pathologies Int. J. Exp. Pathol. 2009, 90, 284-294
13. D'Amato, R. J.; Lin, C. M.; Flynn, E.; Folkman, J.; Hamel, E. 2-Methoxyestradiol, an endogenous mammalian metabolite, inhibits tubulin polymerization by interacting at the colchicine site Proc. Natl. Acad. Sci. U.S.A. 1994, 91, 3964-3968
14. Dumontet, C.; Jordan, M. A. Microtubule-binding agents: a dynamic field of cancer therapeutics Nat. Rev. Drug Discovery 2010, 9, 790-803
15. Chen, J.; Liu, T.; Dong, X.; Hu, Y. Recent development and SAR analysis of colchicine binding site inhibitors Mini-Rev. Med. Chem. 2009, 9, 1174-1190
16. Hsieh, H. P.; Liou, J. P.; Mahindroo, N. Pharmaceutical design of antimitotic agents based on combretastatins Curr. Pharm. Des. 2005, 11, 1655-1677
17. Tron, G. C.; Pirali, T.; Sorba, G.; Pagliai, F.; Busacca, S.; Genazzani, A. A. Medicinal chemistry of combretastatin A4: present and future directions J. Med. Chem. 2006, 49, 3033-3044
18. Chaudhary, A.; Pandeya, S. N.; Kumar, P.; Sharma, P. P.; Gupta, S.; Soni, N.; Verma, K. K.; Bhardwaj, G. Combretastatin a-4 analogs as anticancer agents Mini-Rev. Med. Chem. 2007, 7, 1186-1205
19. Shoichet, B. K. Virtual screening of chemical libraries Nature 2004, 432, 862-865
20. Schneider, G. Virtual screening: an endless staircase? Nat. Rev. Drug Discovery 2010, 9, 273-276
21. Chiang, Y. K.; Kuo, C. C.; Wu, Y. S.; Chen, C. T.; Coumar, M. S.; Wu, J. S.; Hsieh, H. P.; Chang, C. Y.; Jseng, H. Y.; Wu, M. H.; Leou, J. S.; Song, J. S.; Chang, J. Y.; Lyu, P. C.; Chao, Y. S.; Wu, S. Y. Generation of ligand-based pharmacophore model and virtual screening for identification of novel tubulin inhibitors with potent anticancer activity J. Med. Chem. 2009, 52, 4221-4233
22. Kim, N. D.; Park, E. S.; Kim, Y. H.; Moon, S. K.; Lee, S. S.; Ahn, S. K.; Yu, D. Y.; No, K. T.; Kim, K. H. Structure-based virtual screening of novel tubulin inhibitors and their characterization as anti-mitotic agents Bioorg. Med. Chem. 2010, 18, 7092-7100
23. Nguyen, T. L.; McGrath, C.; Hermone, A. R.; Burnett, J. C.; Zaharevitz, D. W.; Day, B. W.; Wipf, P.; Hamel, E.; Gussio, R. A common pharmacophore for a diverse set of colchicine site inhibitors using a structure-based approach J. Med. Chem. 2005, 48, 6107-6116
24. Massarotti, A.; Theeramunkong, S.; Mesenzani, O.; Caldarelli, A.; Genazzani, A. A.; Tron, G. C. Identification of novel antitubulin agents by using a virtual screening approach based on a 7-point pharmacophore model of the tubulin colchi-site Chem. Biol. Drug Des. 2011, 78, 913-922
25. Dorleans, A.; Gigant, B.; Ravelli, R. B.; Mailliet, P.; Mikol, V.; Knossow, M. Variations in the colchicine-binding domain provide insight into the structural switch of tubulin Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 13775-13779
26. Leynadier, D.; Peyrot, V.; Sarrazin, M.; Briand, C.; Andreu, J. M.; Rener, G. A.; Temple, C., Jr. Tubulin binding of two 1-deaza-7,8- dihydropteridines with different biological properties: enantiomers NSC 613862 (S)-(-) and NSC 613863 (R)-(+) Biochemistry 1993, 32, 10675-10682
27. Bowdon, B. J.; Waud, W. R.; Wheeler, G. P.; Hain, R.; Dansby, L.; Temple, C., Jr. Comparison of 1,2-dihydropyrido[3,4-b]pyrazines (1-deaza-7,8- dihydropteridines) with several other inhibitors of mitosis Cancer Res. 1987, 47, 1621-1626
28. de Ines, C.; Leynadier, D.; Barasoain, I.; Peyrot, V.; Garcia, P.; Briand, C.; Rener, G. A.; Temple, C., Jr. Inhibition of microtubules and cell cycle arrest by a new 1-deaza-7,8-dihydropteridine antitumor drug, CI 980, and by its chiral isomer, NSC 613863 Cancer Res. 1994, 54, 75-84
29. Kim, D. Y.; Kim, K.-H.; Kim, N. D.; Lee, K. Y.; Han, C. K.; Yoon, J. H.; Moon, S. K.; Lee, S. S.; Seong, B. L. Design and biological evaluation of novel tubulin inhibitors as antimitotic agents using a pharmacophore binding model with tubulin J. Med. Chem. 2006, 49, 5664-5670
30. Ravelli, R. B.; Gigant, B.; Curmi, P. A.; Jourdain, I.; Lachkar, S.; Sobel, A.; Knossow, M. Insight into tubulin regulation from a complex with colchicine and a stathmin-like domain Nature 2004, 428, 198-202
31. Meng, E. C.; Shoichet, B. K.; Kuntz, I. D. Automated docking with grid-based energy evaluation J. Comput. Chem. 1992, 13, 505-524
32. Lorber, D. M.; Shoichet, B. K. Hierarchical docking of databases of multiple ligand conformations Curr. Top. Med. Chem. 2005, 5, 739-749
33. 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
34. Jacobson, M. P.; Kaminski, G. A.; Friesner, R. A.; Rapp, C. S. Force field validation using protein side chain prediction J. Phys. Chem. B 2002, 106, 11673-11680
35. Jacobson, M. P.; Pincus, D. L.; Rapp, C. S.; Day, T. J.; Honig, B.; Shaw, D. E.; Friesner, R. A. A hierarchical approach to all-atom protein loop prediction Proteins 2004, 55, 351-367
36. Li, X.; Jacobson, M. P.; Friesner, R. A. High-resolution prediction of protein helix positions and orientations Proteins 2004, 55, 368-382
37. 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
38. Srinivasan, J.; Miller, J.; Kollman, P. A.; Case, D. A. Continuum solvent studies of the stability of RNA hairpin loops and helices J. Biomol. Struct. Dyn. 1998, 16, 671-682
39. Flynn, B. L.; Flynn, G. P.; Hamel, E.; Jung, M. K. The synthesis and tubulin binding activity of thiophene-based analogues of combretastatin A-4 Bioorg. Med. Chem. Lett. 2001, 11, 2341-2343
40. Romagnoli, R.; Baraldi, P. G.; Cruz-Lopez, O.; Tolomeo, M.; Di Cristina, A.; Pipitone, R. M.; Grimaudo, S.; Balzarini, J.; Brancale, A.; Hamel, E. Synthesis of novel antimitotic agents based on 2-amino-3-aroyl-5-(hetero) arylethynyl thiophene derivatives Bioorg. Med. Chem. Lett. 2011, 21, 2746-2751
41. Romagnoli, R.; Baraldi, P. G.; Cara, C. L.; Hamel, E.; Basso, G.; Bortolozzi, R.; Viola, G. Synthesis and biological evaluation of 2-(3′,4′,5′-trimethoxybenzoyl)-3-aryl/arylaminobenzo[b] thiophene derivatives as a novel class of antiproliferative agents Eur. J. Med. Chem. 2010, 45, 5781-5791
42. Romagnoli, R.; Baraldi, P. G.; Pavani, M. G.; Cruz-Lopez, O.; Hamel, E.; Balzarini, J.; Brognara, E.; Zuccato, C.; Gambari, R. Synthesis and cellular pharmacology studies of a series of 2-amino-3-aroyl-4-substituted thiophene derivatives Med. Chem. 2010, 6, 329-343
43. Liao, S. Y.; Chen, T. J.; Miao, T. F.; Qian, L.; Zheng, K. C. Binding orientations, QSAR, and molecular design of thiophene derivative inhibitors Chem. Biol. Drug Des. 2009, 74, 289-296
44. McGovern, S. L.; Helfand, B. T.; Feng, B.; Shoichet, B. K. A specific mechanism of nonspecific inhibition J. Med. Chem. 2003, 46, 4265-4272
45. Hsieh, J. H.; Yin, S.; Liu, S.; Sedykh, A.; Dokholyan, N. V.; Tropsha, A. Combined application of cheminformatics- and physical force field-based scoring functions improves binding affinity prediction for CSAR data sets J. Chem. Inf. Model. 2011, 51, 2027-2035
46. Hsieh, J. H.; Yin, S.; Wang, X. S.; Liu, S.; Dokholyan, N. V.; Tropsha, A. Cheminformatics meets molecular mechanics: a combined application of knowledge-based pose scoring and physical force field-based hit scoring functions improves the accuracy of structure-based virtual screening J. Chem. Inf. Model. 2012, 52, 16-28
47. Ducki, S. The development of chalcones as promising anticancer agents IDrugs 2007, 10, 42-46
48. Kuntz, I. D.; Chen, K.; Sharp, K. A.; Kollman, P. A. The maximal affinity of ligands Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 9997-10002
49. Hopkins, A. L.; Groom, C. R.; Alex, A. Ligand efficiency: a useful metric for lead selection Drug Discovery Today 2004, 9, 430-431
50. Irwin, J. J.; Shoichet, B. K. ZINC - a free database of commercially available compounds for virtual screening J. Chem. Inf. Model. 2005, 45, 177-182
51. Connolly, M. L. Solvent-accessible surfaces of proteins and nucleic acids Science 1983, 221, 709-713
52. Ferrin, T. E.; Huang, C. C.; Jarvis, L. E.; Langridge, R. The MIDAS display system J. Mol. Graphics Modell. 1988, 6, 13-27
53. Kuntz, I. D.; Blaney, J. M.; Oatley, S. J.; Langridge, R.; Ferrin, T. E. A geometric approach to macromolecule-ligand interactions J. Mol. Biol. 1982, 161, 269-288
54. Nicholls, A.; Honig, B. A rapid finite difference algorithm, utilizing successive over-relaxation to solve the Poisson-Boltzmann equation J. Comput. Chem. 1991, 12, 435-445
55. Mysinger, M. M.; Shoichet, B. K. Rapid context-dependent ligand desolvation in molecular docking J. Chem. Inf. Model. 2010, 50, 1561-1573
56. 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
57. Huang, N.; Jacobson, M. P. Binding-site assessment by virtual fragment screening PLoS One 2010, 5, e10109
58. 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
59. Kaminski, G. A.; Friesner, R. A.; Tirado-Rives, J.; Jorgensen, W. L. Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides? J. Phys. Chem. B 2001, 105, 6474-6487
60. Case, D. A.; Darden, T. A.; Cheatham, I. T. E.; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Crowley, M.; Walker, R. C.; Zhang, W.; Merz, K. M.; Wang, B.; Hayik, S.; Roitberg, A.; Seabra, G.; Kolossváry, I.; Wong, K. F.; Paesani, F.; Vanicek, J.; Wu, X.; Brozell, S. R.; Steinbrecher, T.; Gohlke, H. AMBER 10; University of California: San Francisco, CA, 2008.
61. Wang, J.; Cieplak, P.; Kollman, P. A. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem. 2000, 21, 1049-1074
62. 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
63. Luo, R.; David, L.; Gilson, M. K. Accelerated Poisson-Boltzmann calculations for static and dynamic systems J. Comput. Chem. 2002, 23, 1244-1253
64. Sitkoff, D.; Sharp, K. A.; Honig, B. Accurate calculation of hydration free energies using macroscopic solvent models J. Phys. Chem. 1994, 98, 1978-1988
65. Castoldi, M.; Popov, A. V. Purification of brain tubulin through two cycles of polymerization-depolymerization in a high-molarity buffer Protein Expression Purif. 2003, 32, 83-88
66. Shan, B.; Medina, J. C.; Santha, E.; Frankmoelle, W. P.; Chou, T. C.; Learned, R. M.; Narbut, M. R.; Stott, D.; Wu, P.; Jaen, J. C.; Rosen, T.; Timmermans, P. B.; Beckmann, H. Selective, covalent modification of beta-tubulin residue Cys-239 by T138067, an antitumor agent with in vivo efficacy against multidrug-resistant tumors Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 5686-5691