The assembly-inducing laulimalide/peloruside a binding site on tubulin: Molecular modeling and biochemical studies with [3H]Peloruside A

Journal of Chemical Information and Modeling

Volumn 50, Issue 11, 2010, Pages 2019-2028

  Nguyen, Tam Luong ^a   Xu, Xiaoming ^b   Gussio, Rick ^c   Ghosh, Arun K ^b   Hamel, Ernest ^c  

^a SAIC FREDERICK INC   (United States)

^b PURDUE UNIVERSITY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIGANDS; PROTEINS;

BINDING MODELS; BIOCHEMICAL STUDIES; DESOLVATION; DISCODERMOLIDE; PROTEIN ARCHITECTURES; PROTEIN-LIGAND INTERACTIONS; STRUCTURAL BASIS; STRUCTURE ACTIVITY RELATIONSHIPS;

BINDING SITES;

FUSED HETEROCYCLIC RINGS; LACTONE; LAULIMALIDE; MACROLIDE; PELORUSIDE A; TRITIUM; TUBULIN;

ANIMAL; ARTICLE; BINDING SITE; CATTLE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECT; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; STEREOISOMERISM;

ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; BINDING SITES; CATTLE; LACTONES; MACROLIDES; MODELS, MOLECULAR; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; STEREOISOMERISM; TRITIUM; TUBULIN;

EID: 78649522219     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci1002894     Document Type: Article

References (42)

1. Schiff, P. B.; Fant, J.; Horwitz, S. B. Promotion of microtubule assembly in vitro by taxol Nature (London) 1979, 277, 665-667
2. Schiff, P. B.; Horwitz, S. B. Taxol stabilizes microtubules in mouse fibroblast cells Proc. Natl. Acad. Sci. U.S.A. 1980, 77, 1561-1565
3. Bollag, D. M.; McQueney, P. A.; Zhu, J.; Hensens, O.; Koupal, L.; Liesch, J.; Goetz, M.; Lazarides, E.; Woods, C. M. Epothilones, a new class of microtubule-stabilizing agents with a taxol-like mechanism of action Cancer Res. 1995, 55, 2325-2333
4. Mooberry, S. L.; Tien, G.; Hernandez, A. H.; Plubrukarn, A.; Davidson, B. S. Laulimalide and isolaulimalide, new paclitaxel-like microtubule-stabilizing agents Cancer Res. 1999, 59, 653-660
5. Kowalski, R. J.; Giannakakou, P.; Hamel, E. Activities of the microtubule-stabilizing agents epothilones A and B with purified tubulin and in cells resistant to paclitaxel (TaxolÂ) J. Biol. Chem. 1997, 272, 2534-2541
6. Kowalski, R. J.; Giannakakou, P.; Gunasekera, S. P.; Longley, R. E.; Day, B. W.; Hamel, E. The microtubule-stabilizing agent discodermolide competitively inhibits the binding of paclitaxel (Taxol) to tubulin polymers, enhances tubulin nucleation reactions more potently than paclitaxel, and inhibits the growth of paclitaxel-resistant cells Mol. Pharmacol. 1997, 52, 613-622
7. Hamel, E.; Sackett, D. L.; Vourloumis, D.; Nicolaou, K. C. The coral-derived natural products eleutherobin and sarcodictyins A and B: effects on the assembly of purified tubulin with and without microtubule-associated proteins and binding at the polymer taxoid site Biochemistry 1999, 38, 5490-5498
8. Buey, R. M.; Díaz, J. F.; Andreu, J. M.; O'Brate, A.; Giannakakou, P.; Nicolaou, K. C.; Sasmal, P. K.; Ritzén, A.; Namoto, K. Interaction of epothilone analogs with the paclitaxel binding site: relationship between binding affinity, microtubule stabilization, and cytotoxicity Chem. Biol. 2004, 11, 225-236
9. Edler, M. C.; Buey, R. M.; Gussio, R.; Marcus, A. I.; Vanderwal, C. D.; Sorensen, E. J.; Díaz, J. F.; Giannakakou, P.; Hamel, E. Cyclostreptin (FR182877), an antitumor tubulin polymerizing agent deficient in enhancing tubulin assembly despite high affinity for the taxoid site Biochemistry 2005, 44, 11525-11538
10. Pryor, D. E.; O'Brate, A.; Bilcer, G.; Díaz, J. F.; Wang, Y.; Wang, Y.; Kabaki, M.; Jung, M. K.; Andreu, J. M.; Ghosh, A. K.; Giannakakou, P.; Hamel, E. The microtubule stabilizing agent laulimalide does not bind in the taxoid site, kills cells resistant to paclitaxel and epothilones, and may not require its epoxide moiety for activity Biochemistry 2002, 41, 9109-9115
11. Gaitanos, T. N.; Buey, R. M.; Díaz, J. F.; Northcote, P. T.; Teesdale-Spittle, P.; Andreu, J. M.; Miller, J. H. Peloruside A does not bind to the taxoid site on β-tubulin and retains its activity in multidrug-resistant cell lines Cancer Res. 2004, 64, 5063-5067
12. Hood, K. A.; West, L. M.; Rouwé, B.; Northcote, P. T.; Berridge, M. V.; Wakefield, S. J.; Miller, J. H. Peloruside A, a novel antimitotic agent with paclitaxel-like microtubule-stabilizing activity Cancer Res. 2002, 62, 3356-3360
13. Gapud, E. J.; Bai, R.; Ghosh, A. K.; Hamel, E. Laulimalide and paclitaxel: a comparison of their effects on tubulin assembly and their synergistic action when present simultaneously Mol. Pharmacol. 2004, 66, 113-121
14. Hamel, E.; Day, B. W.; Miller, J. H.; Jung, M. K.; Northcote, P. T.; Ghosh, A. K.; Curran, D. P.; Cushman, M.; Nicolaou, K. C.; Paterson, I.; Sorensen, E. J. Synergistic effects of peloruside A and laulimalide with taxoid site drugs, but not with each other, on tubulin assembly Mol. Pharmacol. 2006, 70, 1555-1564
15. Ghosh, A. K.; Xu, X.; Kim, J. H.; Xu, C. X. Enantioselective total synthesis of peloruside A: a potent microtubule stabilizer Org. Lett. 2008, 10, 1001-1004
16. Huzil, J. T.; Chik, J. K.; Slysz, G. W.; Freedman, H.; Tuszynski, J.; Taylor, R. E.; Sackett, D. L.; Schriemer, D. C. A unique mode of microtubule stabilization induced by peloruside A J. Mol. Biol. 2008, 378, 1016-1030
17. Ghosh, A. K.; Wang, Y.; Kim, J. T. Total synthesis of microtubule-stabilizing agent (-)-laulimalide J. Org. Chem. 2001, 66, 8973-8982
18. Hamel, E.; Lin, C. M. Separation of active tubulin and microtubule-associated proteins by ultracentrifugation and isolation of a component causing the formation of microtubule bundles Biochemistry 1984, 23, 4173-4184
19. Grover, S.; Hamel, E. The magnesium-GTP interaction in microtubule assembly Eur. J. Biochem. 1994, 222, 163-172
20. Löwe, J.; Downing, K. H.; Nogales, E. Refined structure of αβ-tubulin at 3.5 Å resolution J. Mol. Biol. 2001, 313, 1045-1057
21. Nettles, J. H.; Li, H.; Cornett, B.; Krahn, J. M.; Snyder, J. P.; Downing, K. H. The binding mode of epothilone A on α,β- tubulin by electron crystallography Science 2004, 305, 866-869
22. Nguyen, T. L.; Gussio, R.; Smith, J. A.; Lannigan, D. A.; Hecht, S. M.; Scudiero, D. A.; Shoemaker, R. H.; Zaharevitz, D. W. Homology model of RSK2 N-terminal kinase domain, structure-based identification of novel RSK2 inhibitors, and preliminary common pharmacophore Bioorg. Med. Chem. 2006, 14, 6097-6105
23. Jiménez-Barbero, J.; Canales, A.; Northcote, P. T.; Buey, R. M.; Andreu, J. M.; Díaz, J. F. NMR determination of the bioactive conformation of peloruside A bound to microtubules J. Am. Chem. Soc. 2006, 128, 8757-8765
24. Kellogg, G. E.; Semus, S. F.; Abraham, D. J. HINT: a new method of empirical hydrophobic field calculation for CoMFA J. Comput.-Aided Mol. Des. 1991, 5, 545-552
25. 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
26. Hamel, E.; Lustbader, J.; Lin, C. M. Deoxyguanosine nucleotide analogues: potent stimulators of microtubule nucleation with reduced affinity for the exchangeable nucleotide site of tubulin Biochemistry 1984, 23, 5314-5325
27. Pera, B.; Razzak, M.; Trigili, C.; Pineda, O.; Canales, A.; Buey, R. M.; Jiménez-Barbero, J.; Northcote, P.; Paterson, I.; Barasoain, I.; Díaz, J. F. Molecular recognition of peloruside A by microtubules: the C24 primary alcohol is essential for biological activity ChemBioChem 2010, 11, 1669-1678
28. 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.; López, J. A.; Andreu, J. M.; Hamel, E.; Díaz, J. F. Cyclostreptin binds covalently to microtubule pores and lumenal taxoid binding sites Nat. Chem. Biol. 2007, 3, 117-125
29. Dixon, M.; Webb, E. C.; Thorne, C. J. R.; Tipton, K. F. Enzymes, 3rd ed.; Academic Press: New York, 1979; pp 332 - 354.
30. Sturtevant, J. M. Heat capacity and entropy changes in processes involving proteins Proc. Natl. Acad. Sci. U.S.A. 1977, 74, 2236-2240
31. Hasegawa, S.; Miyoshi, Y.; Egawa, C.; Ishitobi, M.; Tamaki, Y.; Monden, M.; Noguchi, S. Mutational analysis of the class I β-tubulin gene in human breast cancer Int. J. Cancer 2002, 101, 46-51
32. Singh, A. J.; Xu, C.-X.; Xu, X.; West, L. M.; Wilmes, A.; Chan, A.; Hamel, E.; Miller, J. H.; Northcote, P. T.; Ghosh, A. K. Peloruside, B, a potent antitumor macrolide from the New Zealand marine sponge Mycale hentscheli: isolation, structure, total synthesis, and bioactivity J. Org. Chem. 2010, 75, 2-10
33. Ahmed, A.; Hoegenauer, E. K.;; Enev, V. A. S.; Hanbauer, M.; Kaehlig, H.; Öhler, E.; Mulzer, J. Total synthesis of the microtubule stabilizing antitumor agent laulimalide and some nonnatural analogues: the power of Sharpless' asymmetric epoxidation J. Org. Chem. 2003, 68, 3026-3042
34. Wender, P. A.; Hegde, S. G.; Hubbard, R. D.; Zhang, L.; Mooberry, S. L. Synthesis and biological evaluation of (-)-laulimalide analogues Org. Lett. 2003, 5, 3507-3509
35. Gallagher, J. B. M.; Fang, F. G.; Johannes, C. W.; Pesant, M.; Tremblay, M. R.; Zhao, H.; Akasaka, K.; Li, X.; Liu, J.; Littlefield, B. A. Synthesis and biological evaluation of (-)-laulimalide analogues Bioorg. Med. Chem. Lett. 2004, 14, 575-579
36. Mooberry, S. L.; Randall-Hlubek, D. A.; Leal, R. M.; Hegde, S. G.; Hubbard, R. D.; Zhang, L.; Wender, P. A. Microtubule-stabilizing agents based on designed laulimalide analogues Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 8803-8808
37. Paterson, I.; Menche, D.; HÃkansson, A. E.; Longstaff, A.; Wong, D.; Barasoain, I.; Buey, R. M.; Díaz, J. F. Design, synthesis and biological evaluation of novel, simplified analogues of laulimalide: modification of the side chain Bioorg. Med. Chem. Lett. 2005, 15, 2243-2247
38. Wender, P. A.; Hilinski, M. K.; Soldermann, N.; Mooberry, S. L. Total synthesis and biological evaluation of 11-desmethyllaulimalide, a highly potent simplified laulimalide analogue Org. Lett. 2006, 8, 1507-1510
39. Trost, B. M.; Amans, D.; Seganish, W. M.; Chung, C. K. Evaluating transition-metal-catalyzed transformations for the synthesis of laulimalide J. Am. Chem. Soc. 2009, 131, 17087-17089
40. Mooberry, S. L.; Hilinski, M. K.; Clark, E. A.; Wender, P. A. Function-oriented synthesis: biological evaluation of laulimalide analogues derived from a last step cross metathesis diversification strategy Mol. Pharmaceut. 2008, 5, 829-838
41. Gollner, A.; Altmann, K.-H.; Gertsch, J.; Mulzer, J. The laulimalide family: total synthesis and biological evaluation of neolaulimalide, isolaulimalide and a nonnatural analogue Chem.î - ̧Eur. J. 2009, 15, 5979-5997
42. Bennett, M. J.; Barakat, K.; Huzil, J. T.; Tuszynski, J.; Schreimer, D. C. Discovery and characterization of the laulimalide-microtubule binding mode by mass shift perturbation mapping Chem. Biol. 2010, 17, 725-734