Structural comparison of the interaction of tubulin with various ligands affecting microtubule dynamics

Current Cancer Drug Targets

Volumn 12, Issue 6, 2012, Pages 658-666

  Stec Martyna, E ^a   Ponassi, M ^b   Miele, M ^c   Parodi, S ^b   Felli, L ^c   Rosano, C ^b  

^a MEDICAL UNIVERSITY OF LODZ   (Poland)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

Author keywords

Microtubule stabilising agent; Microtubules; Structure based drug design; Structure activity relationship; Tubulin

Indexed keywords

ALPHA TUBULIN; BETA TUBULIN; COLCHICINE; ESTRAMUSTINE; HETERODIMER; LAULIMALIDE; MICROTUBULE ASSOCIATED PROTEIN; MONOMER; PACLITAXEL; SOBLIDOTIN; TUBULIN; VINBLASTINE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING KINETICS; BINDING SITE; INHIBITION KINETICS; LIGAND BINDING; MICROTUBULE; MICROTUBULE ASSEMBLY; MOLECULAR DYNAMICS; PHARMACOPHORE; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN SUBUNIT; REGULATORY MECHANISM; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

ANIMALS; ANTINEOPLASTIC AGENTS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; HUMANS; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; MICROTUBULES; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; TUBULIN; TUBULIN MODULATORS;

EID: 84862632433     PISSN: 15680096     EISSN: 18735576     Source Type: Journal    
DOI: 10.2174/156800912801784893     Document Type: Article

References (103)

1. Nogales, E.; Wolf, S. G.; Downing, K. H. Structure of the α β tubulin dimer by electron crystallography. Nature 1998, 391, 199-203.
2. Sharp, D. J.; Rogers, G. C.; Scholey, J. M. Microtubule motors in mitosis. Nature 2000, 407, 41-47.
3. Hyams, J. S.; Lloyd, C. W. Microtubules. New York: John-Wiley, 1994.
4. Lawler, S. Microtubule dynamics: if you need a shrink try stathmin/Op18. Curr. Biol. 1998, 8, 212-214.
5. Amos, L.; Klug, A. Arrangement of subunits in flagellar microtubules. J. Cell Sci. 1974, 14, 523-549.
6. Allen, C.; Borisy, G. C. Structural polarity and directional growth of microtubules of Chlamydomonas flagella. J. Mol. Biol. 1974, 90, 381-402.
7. Downing, K. H.; Nogales, E. Tubulin structure: insights into microtubule properties and functions. Curr. Opin. Struct. Biol. 1998, 8, 785-791.
8. Amos, L. A. What tubulin drugs tell us about microtubule structure and dynamics. Semin. Cell. Dev. Biol. 2011. [Epub ahead of print].
9. Mitchison, T.; Kirschner, M. Dynamic instability of microtubule growth. Nature 1984, 312, 237-242.
10. Shaw, S. L.; Kamyar, R.; Ehrhardt, D. W. Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 2003, 300, 1715-1718.
11. Chen, W.; Zhang, D. Kinetochore fibre dynamics outside the context of the spindle during anaphase. Nat. Cell Biol. 2004, 6, 227-231
12. Jordan, M. A.; Kamath, K. How do microtubule-targeted drugs work? An overview. Curr. Cancer Drug Targets 2007, 7, 730-742.
13. Nogales, E.; Whittaker, M.; Miligan, R. A.; Downing, K. H. Highresolution model of the microtubule. Cell. 1999, 96, 79-88.
14. Lee, H.; DeRosier, D. J.; Nicholson, W. V.; Nogales, E.; Downing, K. H. Microtubule structure at 8 Å resolution. Structure 2002, 10, 1317-1328.
15. Meurer-Grob, P.; Kasparian, J.; Wade, R. H. Microtubule structure at improved resolution. Biochemistry 2001, 40, 8000-8008.
16. Gigant, B.; Curmi, P. A.; Martin-Barbey, C.; Charbaut, E.; Lachkar, S.; Lebeau, L.; Siavoshian, S.; Sobel, A.; Knossow, M. The 4 Å X-ray structure of a tubulin:stathmin-like domain complex. Cell 2000, 102, 809-816.
17. Gigant, B.; Cormier, A.; Dorléans, A.; Ravelli, R. B. G.; Knossow, M. Microtubule-destabilizing agents: structural and mechanistic insights from the interaction of colchicine and vinblastine with tubulin. Top. Curr. Chem. 2009, 286, 259-278.
18. Nogales, E.; Wang, H. W. Structural intermediates in microtubule assembly and disassembly: how and why? Curr. Opin. Cell Biol. 2006, 18, 179-184.
19. Jordan, M. A.; Wilson, L. The use and action of drugs in analyzing mitosis. Methods Cell Biol. 1999, 61, 267-295.
20. Checchi, P. M.; Nettles, J. H.; Zhou, J.; Snyder, J. P.; Joshi, H. C. Microtubule-interacting drugs for cancer treatment. Trends Pharmacol. Sci. 2003, 24, 361-365.
21. Jordan, M. A.; Wilson, L. Microtubules as a target for anticancer drugs. Nat. Rev. Cancer 2004, 4, 253-265.
22. Jordan, M. A.; Toso, R. J.; Thrower, D.; Wilson, L. Mechanism of mitotic block and inhibition of cell proliferation by taxol at low concentrations. Proc. Nat. Acad. Sci. U.S.A. 1993, 90, 9552-9556.
23. Yvon, A. M.; Wadsworth, P.; Jordan, M. A. Taxol Suppresses Dynamics of Individual Microtubules in Living Human Tumor Cells. Mol. Biol. Cell. 1999, 10, 947-959.
24. Jordan, M. A. Mechanism of action of antitumor drugs that interact with microtubules and tubulin. Curr. Med. Chem. Anti-Cancer Agents 2002, 2, 1-17.
25. Calligaris, D.; Verdier-Pinard, P.; Devred, F.; Villard, C.; Braguer, D.; Lafitte, D. Microtubule targeting agents: from biophysics to proteomics. Cell. Mol. Life Sci. 2010, 67, 1089-104.
26. 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 (29), 9109-9115.
27. Jordan, M. A. Mechanism of action of antitumor drugs that interact with microtubules and tubulin. (2002) Curr. Med. Chem. Anticancer Agents 2002, 2 (1),1-17.
28. Balbi, A.; Anzaldi, M.; Macciò, C.; Aiello, C.; Mazzei, M.; Gangemi, R.; Castagnola, P.; Miele, M.; Rosano, C.; Viale, M. Synthesis and biological evaluation of novel pyrazole derivatives with anticancer activity. Eur. J. Med. Chem. 2011 Aug 31. [Epub ahead of print].
29. Kiselyov, A.; Balakin, K. V.; Tkachenko, S. E.; Savchuk, N.; Ivachtchenko, A. V. Recent progress in discovery and development of antimitotic agents. Anticancer Agents Med. Chem. 2007, 7, 189-208.
30. Jordan, M. A.; Margolis, R. L.; Himes, R. H.; Wilson, L. Identification of a distinct class of vinblastine binding sites on microtubules. J. Mol. Biol. 1986, 187, 61-73.
31. Rai, S. S.; Wolff, J. Localization of the vinblastine-binding site on β-tubulin. J. Biol. Chem. 1996, 271, 14707-14711.
32. Cormier, A.; Knossow, M.; Wang, C.; Gigant, B. The binding of vinca domain agents to tubulin: structural and biochemical studies. Methods Cell Biol. 2010, 95, 373-390.
33. Rao, S.; Krauss, N. E.; Heerding, J. M.; Swindell, C. S.; Ringel, I.; Orr, G. A.; Horwitz, S. B. 3'-(p-azidobenzamido)taxol photolabels the N-terminal 31 amino acids of β-tubulin. J. Biol. Chem. 1994, 269, 3132-3134.
34. Rao, S.; Orr, G. A.; Chaudhary, A. G.; Kingston, D. G.; Horwitz, S. B. Characterization of the taxol binding site on the microtubule. 2-(m-Azidobenzoyl)taxol photolabels a peptide (amino acids 217-231) of β-tubulin. J. Biol. Chem. 1995, 270, 20235-20238.
35. Rao, S.; He, L.; Chakravarty, S.; Ojima, I.; Orr, G. A.; Horwitz, S. B. Characterization of the Taxol binding site on the microtubule. Identification of Arg(282) in β-tubulin as the site of photoincorporation of a 7-benzophenone analogue of Taxol. J. Biol. Chem. 1999, 274, 37990-37994.
36. Snyder, J. P.; Nettles, J. H.; Cornett, B.; Downing, K. H.; Nogales, E. The binding conformation of Taxol in β-tubulin: a model based on electron crystallographic density. Proc. Natl. Acad. Sci. USA 2001, 98, 5312-5316.
37. Uppuluri, S.; Knipling, L.; Sackett, D. L.; Wolff, J. Localization of the colchicine-binding site of tubulin. Proc. Natl. Acad. Sci. USA 1993, 90, 11598-11602.
38. Bai, R.; Pei, X. F.; Boye, O.; Getahun, Z.; Grover, S.; Bekisz, J.; Nguyen, N. Y.; Brossi, A.; Hamel, E. J. Identification of cysteine 354 of beta-tubulin as part of the binding site for the A ring of colchicine. Biol. Chem. 1996, 271, 12639-12645.
39. 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.
40. Pryor, D. E.; O'Brate, A.; Bilcer, G.; Diaz, J. F.; 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.
41. Gaitanos, T. N.; Buey, R. M.; Diaz, J. F.; Northcote, P. T.; Teesdale-Spittle, P.; Andreu, J. M.; Miller, J. H. Peloruside. A does not bind to the taxoid site on beta-tubulin and retains its activity in multidrug-resistant cell lines. Cancer Res. 2004, 64, 5063-5067.
42. Pineda, O.; Farras, J.; Maccari, L.; Manetti, F.; Botta, M.; Vilarrasa, J. Computational comparison of microtubule-stabilising agents laulimalide and peloruside with taxol and colchicine. Bioorg. Med. Chem. Lett. 2004, 14, 4825-4829.
43. Jimenez-Barbero, J.; Canales, A.; Northcote, P. T.; Buey, R. M.; Andreu, J. M.; Diaz, J. F. NMR determination of the bioactive conformation of peloruside A bound to microtubules. J. Am. Chem. Soc. 2006, 128, 8757-8765.
44. 3H]peloruside A. J. Chem. Inf. Model 2010, 50, 2019-2028.
45. Usui, T.; Kondoh, M.; Cui, C. B.; Mayumi, T.; Osada, H. Tryptostatin A, a specific and novel inhibitor of microtubule assembly. Biochem. J. 1998, 333, 543-548.
46. Laing, N.; Dahllöf, B.; Hartley-Asp, B.; Ranganathan, S.; Tew, K. D. Interaction of estramustine with tubulin isotypes. Biochemistry 1997, 36, 871-878.
47. Panda, D.; Miller, H.; Islam, K.; Wilson, L. Stabilization of microtubule dynamics by estramustine by binding to a novel site in tubulin: a possible mechanistic basis for its antitumor action. Proc. Natl. Acad. Sci. USA 1997, 94, 10560-10564.
48. Bai, R.; Pettit, G. R.; Hamel, E. J. Binding of dolastatin 10 to tubulin at a distinct site for peptide antimitotic agents near the exchangeable nucleotide and vinca alkaloid sites. J. Biol. Chem. 1990, 265, 17141-17149.
49. Hamel, E. Natural products which interact with tubulin in the vinca domain: maytansine, rhizoxin, phomopsin A, dolastatins 10 and 15 and halichondrin B. Pharmacol. Ther. 1992, 55, 31-51.
50. Gigant, B.; Wang, C. G.; Ravelli, R. B. G.; Roussi, F.; Steinmetz, M. O.; Curmi, P. A.; Sobel, A.; Knossow, M. Structural basis for the regulation of tubulin by vinblastine. Nature 2005, 435, 519-522.
51. Tonsing, E. M.; Steyn, P. S.; Osborn, M.; Weber, K. Phomopsin A, the causative agent of lupinosis, interacts with microtubules in vivo and in vitro. Eur. J. Cell Biol. 1984, 35, 156-164.
52. Natsume, T.; Watanabe, J.; Ogawa, K.; Yasumura, K.; Kobayashi, M. Tumor-specific antivascular effect of TZT-1027 (Soblidotin) elucidated by magnetic resonance imaging and confocal laser scanning microscopy. Cancer Sci. 2007, 98, 598-604.
53. Menendez, M.; Rivas, G.; Díaz, J. F.; Andreu, J. M. Control of the structural stability of the tubulin dimer by one high affinity bound magnesium ion at nucleotide N-site. J. Biol. Chem. 1998, 273, 167-176.
54. Bai, R.; Covell, D. G.; Pei, X-F.; Ewell, J. B.; Nguyen, N. Y.; Brossi, A.; Hamel, E. Mapping the binding site of colchicinoids on β-tubulin. 2-Chloroacetyl-2-demethylthiocolchicine covalently reacts predominantly with cysteine 239 and secondarily with cysteine 354. J. Biol. Chem. 2000, 275, 40443-40452.
55. Ayad, N. G.; Rankin, S.; Murakami, M.; Jebanathirajah, J.; Gygi, S. Kirschner, M. W. Tome-1, a trigger of mitotic entry, is degraded during G1 via the APC. Cell 2003, 113, 101-113.
56. Dorleans, A.; Gigant, B.; Ravelli, R. B. G.; Mailliet, P.; Mikol, V.; Knossow, M. Variations in the colchicine-binding domain provide insight into the structural switch of tubulin. Proc. Nat. Acad. Sci. USA 2009, 106, 13775-13779.
57. Arai, T. Inhibition of microtubule assembly in vitro by TN-16, a synthetic antitumor drug. FEBS Lett. 1983, 155, 273-276.
58. 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.; Beckman, 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.
59. 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.
60. McGuire, W. P.; Rowinsky, E. K.; Rosenshein, N. B.; Grumbine, F. C.; Ettinger, D. S.; Armstrong, D. K.; Donehower, R. C. Taxol: a unique antineoplastic agent with significant activity in advanced ovarian epithelial neoplasms. Ann. Intern. Med. 1989, 111, 273-279.
61. Slichenmyer, W. J.; Von Hoff, D. D. Taxol: a new and effective anti-cancer drug. Anticancer Drugs 2001, 2, 519-530.
62. Woo, D. D.; Miao, S. Y.; Pelayo, J. C.; Woolf, A. S. Taxol inhibits progression of congenital polycistic kidney disease. Nature 1994, 368, 750-753.
63. Choy, H. Taxanes in combined modality therapy for solid tumors. Crit. Rev. Oncol. Hematol. 2003, 37, 237-247.
64. Holton, R. A.; Biediger, R. J.; Boatman, P. D. Semisynthesis of taxol and taxotere. In: Taxol Science and Applications; Suffness M. CRC Press, Ed.; Boca Raton Florida 1995, 97-121.
65. Hook, I.; Poupat, C.; Ahond, A.; Guernard, D.; Guerritte, F.; Adeline, M. T.; Wang, X. P.; Dempsey, D.; Breuillet, S.; Potier, P. Seasonal variation of neutral and basic taxoid contents in shoots of European Yew (Taxus baccata). Phytochemistry 1999, 52, 1041-1045.
66. Poupat C.; Hook I.; Guerritte F.; Ahond A.; Guernard D.; Adeline M. T.; Wang X. P.; Dempsey D.; Breuillet S.; Potier, P. Neutral and basic taxoid contents in needles of Taxus species. Planta Medica 2000, 66, 580-584.
67. Gueritte-Voegelein, F. Structure of a synthetic taxol precursor: Ntert-butoxycarbonyl-10-deacetyl-N-debenzoyltaxol. Acta Crystallogr. C 1990, 46, 781-784.
68. Gueritte-Voegelein, F.; Gubnard, D.; Lavelle, F.; Le Goff, M. T.; Mangatal, L.; Potier, P. Relationships between the structure of taxol analogues and their antimitotic activity. J. Med. Chem. 1991, 34, 992-998.
69. Schiff, P. B.; Fant, J.; Horwitz, S. B. Promotion of microtubule assembly in vitro by taxol. Nature 1979, 277, 665-667.
70. Derry, W. B.; Wilson, L.; Jordan, M. A. Low potency of taxol at microtubule minus ends: implications for its antimitotic and therapeutic mechanism. Cancer Res. 1998, 58, 1177-1184.
71. Jordan, M. A.; Wendell, K.; Gardiner, S.; Derry, W. B.; Copp, H.; Wilson, L. Mitotic block induced in HeLa cells by low concentrations of paclitaxel (Taxol) results in abnormal mitotic exit and apoptotic cell death. Cancer Res. 1996, 56, 816-825.
72. Horwitz, S. B. Mechanism of action of taxol. Trends Pharmacol. Sci. 1992, 13, 134-136.
73. Derry, W. B.; Wilson, L.; Jordan, M. A. Substoichiometric binding of taxol suppresses microtubule dynamics. Biochemistry 1995, 34, 2203-2211.
74. Amos, L.; Lowe, J. How Taxol stabilises microtubule structure. Chem. Biol. 1999, 6, 65-69.
75. Xiao, H.; Verdier-Pinard, P.; Fernandez-Fuentes, N.; Burd, B.; Angeletti, R.; Fiser, A. Insights into the mechanism of microtubule stabilization by Taxol. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 10166-10173.
76. Elie-Caille, C.; Severin, F.; Helenius, J.; Howard, J.; Muller, D. J.; Hyman, A. A. Straight GDP-tubulin protofilaments form in the presence of taxol. Curr. Biol. 2007, 17, 1765-1770.
77. Lowe, J.; Li, H.; Downing, K. H.; Nogales, E. Refined structure of alpha beta-tubulin at 3.5 Å resolution. J. Mol. Biol. 2001, 313, 1045-1057.
78. 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.
79. Ferrandina, G.; Mariani, M.; Andreoli, M,; Shahabi, S.; Scambia, G.; Ferlini, C. Novel Drugs targeting microtubules: the role of epothilones. Curr. Pharm. Des. 2012 Feb 28. [Epub ahead of print].
80. ter Haar, E.; Kowalski, R. J.; Hamel, E.; Lin, C. M.; Longley, R. E.; Gunasekera, S. P.; Rosenkranz, H. S.; Day, B. W. Discodermolide, a cytotoxic marine agent that stabilizes microtubules more potently than taxol. Biochemistry 1996, 35, 243-250.
81. 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 paclitaxelresistant cells. Mol. Pharmacol. 1997, 52, 613-622.
82. Long, B. H.; Carboni, J. M.; Wasserman, A. J.; Cornell, L. A.; Casazza, A. M.; Jensen, P. R.; Lindel, T.; Fenical, W.; Fairchild, C. R. Eleutherobin, a novel cytotoxic agent that induces tubulin polymerization, is similar to paclitaxel (Taxol). Cancer Res. 1998, 58, 1111-1115.
83. Nicolaou, K. C.; Winssinger, N.; Vourloumis, D.; Ohshima, T.; Kim, S.; Pfefferkorn, J.; Xu, J. Y.; Li, T. Solidand solution phase synthesisand biological evaluation of combinatorial sarcodicty in libraries. J. Am. Chem. Soc. 1998, 120, 10814-10826.
84. Heinz, D. W.; Schubert, W. D.; Höfle, G. Much anticipated-the bioactive conformation of epothilone and its binding to tubulin. Ang. Chem. Int. Ed. 2005, 44, 1298-1301.
85. 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.
86. Nettles, J. H.; Li, H. L.; 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.
87. Carlomagno, T.; Blommers, M. J. J.; Meiler, J.; Jahne, W.; Schupp, T.; Petersen, F.; Schinzer, D.; Altmann, K. H.; Griesinger, C. The high-resolution solution structure of epothilone A bound to tubulin: an understanding of the structure-activity relationships for a powerful class of antitumor agents. Angew. Chem. Int. Ed. Engl. 2003, 42, 2511-2515.
88. Reese, M.; Sanchez-Pedregal, V. M.; Meiler, J.; Blommers, M. J. J.; Griesinger, C.; Carlomagno, T. Structural basis of the activity of the microtubule-stabilizing agent epothilone a studied by NMR spectroscopy in solution. Angew. Chem. Int. Ed. 2007, 46, 1864-1868.
89. Jefford, C. W.; Bernardinelli, G.; Tanaka, J.; Higa, T. Structures and absolute configurations of the marine toxins, latrunculin A and laulimalide. Tetrahedron Lett. 1996, 37, 159-162.
90. Tanaka, J.; Higa, T.; Bernardinelli, G.; Jefford C. W. New Cytotoxic Macrolides from the Sponge Fasciospongia rimosa. Chem. Lett. 1996, 25, 255-256.
91. Naik, P. K.; Santoshi, S.; Rai, A.; Joshi, H. C. Molecular modelling and competition binding study of Br-noscapine and colchicine provide insight into noscapinoid-tubulin binding site. J. Mol. Graph Model 2011, 29, 947-955.
92. Naik, P. K.; Lopus, M.; Aneja, R.; Vangapandu, S. N.; Joshi, H. C. In silico inspired design and synthesis of a novel tubulin-binding anti-cancer drug: folate conjugated noscapine (Targetin). J. Comput. Aided Mol. Des. 2012, 26, 233-247.
93. 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.
94. 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.
95. Sanchez-Pedral, V. M.; Griesinger, C. The tubulin-binding mode of MT stabilizing and destabilizing agents studied by NMR. Top. Curr. Chem. 2009, 286, 151-208.
96. Cleveland, D. W.; Hwo, S. Y.; Kirschner, M.W. Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly. J. Mol. Biol. 1977, 116, 227-247.
97. Lee, D.; Lee, H. W.; Hong, S.; Choi, B. I.; Kim, H. W.; Han, S. B.; Kim, I. H.; Bae, J. Y.; Bae, Y. C.; Rhyu, I. J.; Sun, W.; Kim, H. Inositol 1,4,5 trisphosphate 3-kinase A is a novel microtubuleassociated protein: PKA-dependent phosphoregulation of microtubule binding affinity. J. Biol. Chem. 2012 Mar 2. [Epub ahead of print]
98. Cope, J.; Gilbert, S.; Rayment, I.; Mastronarde, D.; Hoenger, A. Cryo-electron tomography of microtubule-kinesin motor complexes. J. Struct. Biol. 2010, 17, 257-65
99. Bassam, J.; Ozer, R. S.; Safer, D.; Halpain, S.; Milligan, R. A. MAP2 and tau bind longitudinally along the outer ridges of microtubule protofilaments. J. Cell Biol. 2002, 157, 1187-1196.
100. Kar, S.; Fan, J.; Smith, M. J.; Goedert, M.; Amos, L. A. Repeat motifs of tau bind to the insides of microtubules in the absence of taxol. EMBO J. 2003, 22, 70-77.
101. Ackmann, M.; Wiech, H.; Mandelkow, E. Nonsaturable binding indicates clustering of tau on the microtubule surface in a paired helical filament-like conformation. J. Biol. Chem. 2000, 275, 30335-30343.
102. Stamer, K.; Vogel, R.; Thies, E.; Mandelkow, E.; Mandelkow, E.-M. Tau blocks traffic of organelles, neurofilaments and APP vesicles in neurons and enhances oxidative stress. J. Cell Biol. 2002, 156, 1051-1063.
103. Chen, J.; Kanai, Y.; Cowan N. J.; Hirokawa, N. Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons. Nature 1992, 360, 674-676.