Insights into the interaction of discodermolide and docetaxel with tubulin. Mapping the binding sites of microtubule-stabilizing agents by using an integrated NMR and computational approach

ACS Chemical Biology

Volumn 6, Issue 8, 2011, Pages 789-799

  Canales, Angeles ^a,b   Rodríguez Salarichs, Javier ^a,c   Trigili, Chiara ^a   Nieto, Lidia ^a   Coderch, Claire ^d   Andreu, José Manuel ^a   Paterson, Ian ^e   Jiménez Barbero, Jesús ^a   Díaz, J Fernando ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c Centro de Estudios Avanzados de Cuba   (Cuba)

^d UNIVERSITY OF ALCALÁ   (Spain)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; BETA TUBULIN; DISCODERMOLIDE; DOCETAXEL; HETERODIMER; PACLITAXEL;

ARTICLE; CONTROLLED STUDY; CRYSTALLOGRAPHY; DRUG BINDING SITE; DRUG CONFORMATION; DRUG PROTEIN BINDING; MICROTUBULE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS;

ALKANES; ANTINEOPLASTIC AGENTS; BINDING SITES; CARBAMATES; COMPUTER SIMULATION; HUMANS; LACTONES; MICROTUBULES; MODELS, MOLECULAR; MOLECULAR CONFORMATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PACLITAXEL; PROTEIN MULTIMERIZATION; PYRONES; TAXOIDS; TUBULIN; TUBULIN MODULATORS;

EID: 80051985188     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb200099u     Document Type: Article

References (50)

1. Cragg, G. M., Kingston, D. G., and Newman, D. J. (2005) Anticancer Agents from Natural Products, Taylor & Francis, Boca Raton.
2. Paterson, I. and Anderson, E. A. (2005) Chemistry. The renaissance of natural products as drug candidates Science 310, 451-453 (Pubitemid 41507948)
3. Cragg, G. M., Grothaus, P. G., and Newman, D. J. (2009) Impact of natural products on developing new anti-cancer agents Chem. Rev. 109, 3012-3043
4. Buey, R. M., Barasoain, I., Jackson, E., Meyer, A., Giannakakou, P., Paterson, I., Mooberry, S., Andreu, J. M., and Díaz, J. F. (2005) Microtubule interactions with chemically diverse stabilizing agents: Thermodynamics of binding to the paclitaxel site predicts cytotoxicity Chem. Biol. 12, 1269-1279 (Pubitemid 41779467)
5. Díaz, J. F., Barasoain, I., Souto, A. A., Amat-Guerri, F., and Andreu, J. M. (2005) Macromolecular accessibility of fluorescent taxoids bound at a paclitaxel binding site in the microtubule surface J. Biol. Chem. 280, 3928-3937 (Pubitemid 40223862)
6. Barasoain, I., Garcia-Carril, A. M., Matesanz, R., Maccari, G., Trigili, M., Mori, M., Shi, J. Z., Fang, W. S., Andreu, J. M., Botta, M., and Díaz, J. F. (2010) Probing the pore drug binding site of microtubules with fluorescent taxanes: Evidence of two binding poses Chem. Biol. 17, 243-253
7. Buey, R. M., Calvo, E., Barasoain, I., Pineda, O., Edler, M. C., Matesanz, R., Cerezo, G., Vanderwal, C. D., Day, B. W., Sorensen, E. J., Lopez, J. A., Andreu, J. M., Hamel, E., and Díaz, J. F. (2007) Cyclostreptin binds covalently to microtubule pores and lumenal taxoid binding sites Nat. Chem. Biol. 3, 117-125 (Pubitemid 46134999)
8. Díaz, J. F. and Andreu, J. M. (1993) Assembly of purified GDP-tubulin into microtubules induced by taxol and taxotere: reversibility, ligand stoichiometry, and competition Biochemistry 32, 2747-2755 (Pubitemid 23102795)
9. Buey, R. M., Diaz, J. F., Andreu, J. M., O'Brate, A., Giannakakou, P., Nicolaou, K. C., Sasmal, P. K., Ritzen, A., and Namoto, K. (2004) Interaction of epothilone analogs with the paclitaxel binding site; relationship between binding affinity, microtubule stabilization, and cytotoxicity Chem. Biol. 11, 225-236 (Pubitemid 38300292)
10. Canales, A., Matesanz, R., Gardner, N. M., Andreu, J. M., Paterson, I., Diaz, J. F., and Jimenez-Barbero, J. (2008) The bound conformation of microtubule-stabilizing agents: NMR insights into the bioactive 3D structure of discodermolide and dictyostatin Chem.-Eur. J. 14, 7557-7569
11. Gaitanos, T. N., Buey, R. M., Díaz, J. F., Northcote, P. T., Teesdale-Spittle, P., Andreu, J. M., and Miller, J. H. (2004) Peloruside A does not bind to the taxoid site on beta-tubulin and retains its activity in multidrug-resistant cell lines Cancer Res. 64, 5063-5067 (Pubitemid 39006519)
12. Jiménez-Barbero, J., Canales, A., Northcote, P. T., Buey, R. M., Andreu, J. M., and Díaz, J. F. (2006) NMR determination of the bioactive conformation of peloruside a bound to microtubules J. Am. Chem. Soc. 128, 8757-8765 (Pubitemid 44061534)
13. Gigant, B., Curmi, P. A., Martin-Barbey, C., Charbaut, E., Lachkar, S., Lebeau, L., Siavoshian, S., Sobel, A., and Knossow, M. (2000) The 4 A X-ray structure of a tubulin:stathmin-like domain complex Cell 102, 809-816
14. Ravelli, R. B., Gigant, B., Curmi, P. A., Jourdain, I., Lachkar, S., Sobel, A., and Knossow, M. (2004) Insight into tubulin regulation from a complex with colchicine and a stathmin-like domain Nature 428, 198-202 (Pubitemid 38374318)
15. Gigant, B., Wang, C., Ravelli, R. B., Roussi, F., Steinmetz, M. O., Curmi, P. A., Sobel, A., and Knossow, M. (2005) Structural basis for the regulation of tubulin by vinblastine Nature 435, 519-522 (Pubitemid 40734250)
16. Nogales, E., Whittaker, M., Milligan, R. A., and Downing, K. H. (1999) High-resolution model of the microtubule Cell 96, 79-88 (Pubitemid 29044155)
17. Snyder, J. P., Nettles, J. H., Cornett, B., Downing, K. H., and Nogales, E. (2001) The binding conformation of Taxol in beta-tubulin: A model based on electron crystallographic density Proc. Natl. Acad. Sci. U.S.A. 98, 5312-5316 (Pubitemid 32397125)
18. Nettles, J. H., Li, H., Cornett, B., Krahn, J. M., Snyder, J. P., and Downing, K. H. (2004) The binding mode of epothilone A on alpha,beta-tubulin by electron crystallography Science 305, 866-869 (Pubitemid 39038421)
19. Díaz, J. F., Menéndez, M., and Andreu, J. M. (1993) Thermodynamics of ligand-induced assembly of tubulin Biochemistry 32, 10067-10077 (Pubitemid 23312433)
20. Díaz, J. F., Barasoain, I., and Andreu, J. M. (2003) Fast kinetics of Taxol binding to microtubules. Effects of solution variables and microtubule-associated proteins J. Biol. Chem. 278, 8407-8419 (Pubitemid 36800591)
21. Sanchez-Pedregal, V. M. and Griesinger, C. (2009) The Tubulin Binding Mode of MT Stabilizing and Destabilizing, In Tubulin-Binding Agents. Synthetic, Structural and Mecanistic Insights (Carlomagno, T., Ed.), pp 151-208, Springer, Heidelberg.
22. Andreu, J. M., De Ancos, J. G., Starling, D., Hodgkinson, J. L., and Bordas, J. (1989) A synchrotron x-ray-scattering characterization of purified tubulin and of its expansion induced by mild detergent binding Biochemistry 28, 4036-4040 (Pubitemid 19125458)
23. Chakrabarti, G., Kim, S., Gupta, M. L., Jr., Barton, J. S., and Himes, R. H. (1999) Stabilization of tubulin by deuterium oxide Biochemistry 38, 3067-3072
24. Panda, D., Chakrabarti, G., Hudson, J., Pigg, K., Miller, H. P., Wilson, L., and Himes, R. H. (2000) Suppression of microtubule dynamic instability and treadmilling by deuterium oxide Biochemistry 39, 5075-5081 (Pubitemid 30241628)
25. Matesanz, R., Barasoain, I., Yang, C., Wang, L., Li, X., De Ines, C., Coderch, C., Gago, F., Jiménez-Barbero, J., Andreu, J. M., Fang, W., and JF, D. (2008) Optimization of taxane binding to microtubules. Binding affinity decomposition and incremental construction of a high-affinity analogue of paclitaxel Chem. Biol. 15, 573-585 (Pubitemid 351815058)
26. Geney, R., Sun, L., Pera, P., Bernacki, R. J., Xia, S. J., Horwitz, S. B., Simmerling, C. L., and Ojima, I. (2005) Use of the tubulin bound paclitaxel conformation for structure-based rational drug design Chem. Biol. 12, 339-348 (Pubitemid 40406281)
27. Nogales, E., Wolf, S. G., and Downing, K. H. (1998) Structure of the alpha beta tubulin dimer by electron crystallography Nature 391, 199-203 (Pubitemid 28092482)
28. Magnani, M., Maccari, G., Andreu, J. M., Diaz, J. F., and Botta, M. (2009) Possible binding site for paclitaxel at microtubule pores FEBS J. 276, 2701-2712
29. Freedman, H., Huzil, J. T., Luchko, T., Luduena, R. F., and Tuszynski, J. A. (2009) Identification and characterization of an intermediate taxol binding site within microtubule nanopores and a mechanism for tubulin isotype binding selectivity J. Chem. Inf. Model. 49, 424-436
30. Xiao, H., Verdier-Pinard, P., Fernandez-Fuentes, N., Burd, B., Angeletti, R., Fiser, A., Horwitz, S. B., and Orr, G. A. (2006) Insights into the mechanism of microtubule stabilization by Taxol Proc. Natl. Acad. Sci. U.S.A. 103, 10166-10173 (Pubitemid 44051138)
31. Lowe, J., Li, H., Downing, K. H., and Nogales, E. (2001) Refined structure of alpha beta-tubulin at 3.5 A resolution J. Mol. Biol. 313, 1045-1057 (Pubitemid 33081900)
32. Díaz, J. F., Strobe, R., Engelborghs, Y., Souto, A. A., and Andreu, J. M. (2000) Molecular recognition of taxol by microtubules. Kinetics and thermodynamics of binding of fluorescent taxol derivatives to an exposed site J. Biol. Chem. 275, 26265-26276
33. Evangelio, J. A., Abal, M., Barasoain, I., Souto, A. A., Lillo, M. P., Acuna, A. U., Amat-Guerri, F., and Andreu, J. M. (1998) Fluorescent taxoids as probes of the microtubule cytoskeleton Cell Motil. Cytoskeleton 39, 73-90 (Pubitemid 28042460)
34. Odde, D. (1998) Diffusion inside microtubules Eur. Biophys. J. 27, 514-520 (Pubitemid 28414891)
35. Díaz, J. F., Valpuesta, J. M., Chacón, P., Diakun, G., and Andreu, J. M. (1998) Changes in microtubule protofilament number induced by Taxol binding to an easily accessible site. Internal microtubule dynamics J. Biol. Chem. 273, 33803-33810
36. Andreu, J. M. (2007) Tubulin Purification, in Methods Mol. Med. (Zhou, J., Ed.), pp 17-28, Humana Press Inc., Totowa, NJ.
37. Paterson, I. and Lyothier, I. (2004) Total synthesis of (+)-discodermolide: an improved endgame exploiting a Still-Gennari-type olefination with a C1-C8 beta-ketophosphonate fragment Org. Lett. 6, 4933-4936 (Pubitemid 40125845)
38. 2O J. Inorg. Biochem. 98, 161-166 (Pubitemid 37495021)
39. Andreu, J. M., Gorbunoff, M. J., Lee, J. C., and Timasheff, S. N. (1984) Interaction of tubulin with bifunctional colchicine analogues: an equilibrium study Biochemistry 23, 1742-1752 (Pubitemid 14139815)
40. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling Biophys. J. 78, 1606-1619 (Pubitemid 30141584)
41. Schuck, P., Perugini, M. A., Gonzales, N. R., Howlett, G. J., and Schubert, D. (2002) Size-distribution analysis of proteins by analytical ultracentrifugation: strategies and application to model systems Biophys. J. 82, 1096-1111 (Pubitemid 34111246)
42. Laue, T. M., Shah, B. D., Ridgeway, T. M., and Pelletier, S. L. (1992) Computer-aided interpretation of analytical sedimentation data for proteins, in Analytical Ultracentrifugation in Biochemistry and Polymer Science (Harding, S. E., Rowe, A. J., and Horton, J. C., Eds.) pp 90-125, Royal Society of Chemistry, Cambridge.
43. Macura, S. and Ernst, R. R. (1980) Elucidation of cross relaxation in liquids by two-dimensional NMR-spectroscopy Mol. Phys. 41, 95-117
44. Bernardi, A., Potenza, D., Capelli, A. M., García-Herrero, A., Cañada, F. J., and Jiménez-Barbero, J. (2002) Second-generation mimics of ganglioside GM1 oligosaccharide: A three-dimensional view of their interactions with bacterial enterotoxins by NMR and computational methods Chem.-Eur. J. 8, 4598-4612
45. Moseley, H. N. B., Curto, E. V., and Krishna, N. R. (1995) Complete relaxation and conformational exchange matrix (CORCEMA) analysis of NOESY spectra of interacting systems-2-dimensional transferred NOESY J. Magn. Reson. Ser. B 108, 243-261
46. Garcia de la Torre, J., Huertas, M. L., and Carrasco, B. (2000) Calculation of hydrodynamic properties of globular proteins from their atomic-level structure Biophys. J. 78, 719-730 (Pubitemid 30211830)
47. Mohamadi, F., Richards, N. G. J., Guida, W. C., Liskamp, R., Lipton, M., Caufield, C., Chang, G., Hendrickson, T., and Still, W. C. (1990) MacroModel an integrated software system for modeling organic and bioorganic molecules using molecular mechanics J. Comput. Chem. 11, 440-467
48. Still, W. C., Tempczyk, A., Hawley, R. C., and Hendrickson, T. (1990) Semianalytical treatment of solvation for molecular mechanics and dynamics J. Am. Chem. Soc. 112, 6127-6129
49. Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K., and Olson, A. J. (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function J. Comput. Chem. 19, 1639-1662 (Pubitemid 128590223)
50. Jayalakshmi, V. and Krishna, N. R. (2002) Complete relaxation and conformational exchange matrix (CORCEMA) analysis of intermolecular saturation transfer effects in reversibly forming ligand-receptor complexes J. Magn. Reson. 155, 106-118