Microtubule-stabilizing agents: New drug discovery and cancer therapy

Pharmacology and Therapeutics

Volumn 162, Issue , 2016, Pages 134-143

  Zhao, Ying ^a   Mu, Xin ^a   Du, Guanhua ^b  

^a INSTITUTE OF MATERIA MEDICA   (China)

^b Professional Committee of Pharmacology on Traditional Chinese Medicine and Natural Medicine   (China)

Author keywords

Cancer therapy; Epothilone; Microtubule stabilizing agent; Natural product; Paclitaxel

Indexed keywords

ANTINEOPLASTIC AGENT; CERATAMINE DERIVATIVE; CYCLOSTREPTIN; DICTYOSTATIN; DISCODERMOLIDE; ELEUTHEROBIN; EPOTHILONE DERIVATIVE; LAULIMALIDE; MICROTUBULE STABILIZING AGENT; PELORUSIDE A; SARCODICTYIN DERIVATIVE; STABILIZING AGENT; TACCALONOLIDE DERIVATIVE; TAXANE DERIVATIVE; TAXOID; UNCLASSIFIED DRUG; ZAMPANOLIDE;

ARTICLE; CANCER CHEMOTHERAPY; CLINICAL PHARMACOLOGY; CLINICAL RESEARCH; DRUG BINDING SITE; MICROTUBULE; NATURAL RESOURCE; PRECLINICAL STUDY; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION; DRUG DEVELOPMENT; DRUG EFFECTS; HUMAN; NEOPLASMS;

ANTINEOPLASTIC AGENTS; DRUG DISCOVERY; HUMANS; MICROTUBULES; NEOPLASMS;

EID: 84954342035     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2015.12.006     Document Type: Review

References (149)

1. K.H. Altmann Epothilone B and its analogs - a new family of anticancer agents Mini Rev Med Chem 3 2003 149 158
2. K.H. Altmann Recent developments in the chemical biology of epothilones Curr Pharm Des 11 2005 1595 1613
3. K.H. Altmann, A. Flörsheimer, T. O'Reilly, and M. Wartmann 4. The natural products epothilones A and B as lead structures for anticancer drug discovery: chemistry, biology, and SAR studies Prog Med Chem 42 2004 171 205
4. K.H. Altmann, F.Z. Gaugaz, and R. Schiess Diversity through semisynthesis: The chemistry and biological activity of semisynthetic epothilone derivatives Mol Divers 15 2011 383 399
5. K.H. Altmann, and K. Memmert Epothilones as lead structures for new anticancer drugs-pharmacology, fermentation, and structure-Activity-relationships Prog Drug Res 66 273 2008 275 334
6. D. Arnold, W. Voigt, P. Kiewe, C. Behrmann, S. Lindemann, S. Reif, and et al. Weekly administration of sagopilone (ZK-EPO), a fully synthetic epothilone, in patients with refractory solid tumours: results of a phase I trial Br J Cancer 101 2009 1241 1247
7. Y. Asami, J.-H. Jang, N.-K. Soung, L. He, D.O. Moon, J.W. Kim, and et al. Protuboxepin A, a marine fungal metabolite, inducing metaphase arrest and chromosomal misalignment in tumor cell Bioorg Med Chem 20 2012 3799 3806
8. R. Bai, C.D. Vanderwal, J.F. Díaz, and E. Hamel Interaction of a cyclostreptin analogue with the microtubule taxoid site: The covalent reaction rapidly follows binding J Nat Prod 71 2008 370 374
9. C. Ballatore, K.R. Brunden, D.M. Huryn, J.Q. Trojanowski, V.M.-Y. Lee, and A.B. Smith III Microtubule stabilizing agents as potential treatment for Alzheimer's disease and related neurodegenerative tauopathies J Med Chem 55 2012 8979 8996
10. G. Battogtokh, and Y.T. Ko Self-Assembled chitosan-ceramide nanoparticle for enhanced oral delivery of paclitaxel Pharm Res 31 2014 3019 3030
11. M.J. Bennett, K. Barakat, J.T. Huzil, J. Tuszynski, and D.C. Schriemer Discovery and characterization of the laulimalide-microtubule binding mode by mass shift perturbation mapping Chem Biol 17 2010 735-734
12. K.M. Bhat, and V. Setaluri Microtubule-Associated proteins as targets in cancer chemotherapy Clin Cancer Res 13 2007 2849 2854
13. D.M. Bollag, P.A. McQueney, J. Zhu, O. Hensens, L. Koupal, J. Liesch, and et al. Epothilones, a new class of microtubule-stabilizing agents with a Taxol-like mechanism of action Cancer Res 55 1995 2325 2333
14. A. Broggini-Tenzer, A. Sharma, K.J. Nytko, S. Bender, V. Vuong, K. Orlowski, and et al. Combined treatment strategies for microtubule stabilizing agent-resistant tumors J Natl Cancer Inst 107 2015 dju504
15. L.E. Bröker, F.Y. de Vos, C.J. van Groeningen, B.C. Kuenen, H.E. Gall, M.H. Woo, and et al. Phase I trial with BMS-275183, a novel oral taxane with promising antitumor activity Clin Cancer Res 12 2006 1760 1767
16. K.R. Brunden, N.M. Gardner, M.J. James, Y. Yao, J.Q. Trojanowski, V.M.-Y. Lee, and et al. MT-stabilizer, dictyostatin, exhibits prolonged brain retention and activity: potential therapeutic implications ACS Med Chem Lett 4 2013 886 889
17. R.M. Buey, I. Barasoain, E. Jackson, A. Meyer, P. Giannakakou, I. Paterson, and et al. Microtubule interactions with chemically diverse stabilizing agents: Thermodynamics of binding to the Taxol site predicts cytotoxicity Chem Biol 12 2005 1269 1279
18. R.M. Buey, E. Calvo, I. Barasoain, O. Pineda, M.C. Edler, R. Matesanz, and et al. Cyclostreptin binds covalently to microtubule pores and lumenal taxoid binding sites Nat Chem Biol 3 2007 117 125
19. P. Cai, P. Lu, F. Sharom, and W.S. Fang A semisynthetic taxane Yg-3-46a effectively evades P-glycoprotein and βIII tubulin mediated tumor drug resistance in vitro Cancer Lett 341 2013 214 223
20. E. Calvo, I. Barasoain, R. Matesanz, B. Pera, E. Camafeita, O. Pineda, and et al. Cyclostreptin derivatives specifically target cellular tubulin and further map the paclitaxel site Biochemistry 51 2012 329 341
21. A. Canales, J. Rodríguez-Salarichs, C. Trigili, L. Nieto, C. Coderch, J.M. Andreu, and et al. 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 Chem Biol 6 2011 789 799
22. N. Chen, C. Brachmann, X. Liu, D.W. Pierce, J. Dey, W.S. Kerwin, and et al. Albumin-bound nanoparticle (nab) paclitaxel exhibits enhanced paclitaxel tissue distribution and tumor penetration Cancer Chemother Pharmacol 76 2015 699 712
23. J.-G.C. Chen, and S.B. Horwitz Differential mitotic responses to microtubule-stabilizing and -destabilizing drugs Cancer Res 14 2002 1935 1938
24. C.-H. Chen, C.-H. Liao, Y.-L. Chang, J.-H. Guh, S.-L. Pan, and C.-M. Teng Protopine, a novel microtubule-stabilizing agent, causes mitotic arrest and apoptotic cell death in human hormone-refractory prostate cancer cell lines Cancer Lett 315 2012 1 11
25. Z.-L. Chen, B.-D. Wang, and M.-Q. Chen Steroidal bitter principles from Tacca plantaginea. Structures of taccalonolide A and B Tetrahedron Lett 28 1987 1673 1678
26. J.-G.C. Chen, H.Y. Yang C-P, M. Cammer, and S.B. Horwitz Gene expression and mitotic exit induced by microtubule-stabilizing drugs Cancer Res 15 2003 7891 7899
27. C.D. Churchill, M. Klobukowski, and J.A. Tuszynski The unique binding mode of laulimalide to two tubulin protofilaments Chem Biol Drug Des 86 2015 190 199
28. C.D. Churchill, M. Klobukowski, and J.A. Tuszynski Analysis of the binding mode of laulimalide to microtubules: establishing a laulimalide-tubulin pharmacophore J Biomol Struct Dyn 31 2015 1 35
29. M. Ciomei, C. Albanese, W. Pastori, M. Grandi, F. Pietra, M. D'Ambrosio, and et al. Sarcodictyins: A new class of marine derivatives with mode of action similar to Taxol [abstract 30] Proc Am Assoc Cancer Res 38 1997 5
30. E.A. Clark, P.M. Hills, B.S. Davidson, P.A. Wender, and S.L. Mooberry Laulimalide and synthetic laulimalide analogues are synergistic with paclitaxel and 2-methoxyestradiol Mol Pharm 3 2006 457 467
31. R.S. Coleman, E.L. Campbell, and D.J. Carper A direct and efficient total synthesis of the tubulin-binding agents ceratamine A and B; use of IBX for a remarkable heterocycle dehydrogenation Org Lett 11 2009 2133 2136
32. N. Colombo, E. Kutarska, M. Dimopoulos, D.S. Bae, I. Rzepka-Gorska, M. Bidzinski, and et al. Randomized, open-label, phase III study comparing patupilone (EPO906) with pegylated liposomal doxorubicin in platinum-refractory or -resistant patients with recurrent epithelial ovarian, primary fallopian tube, or primary peritoneal cancer J Clin Oncol 30 2012 3841 3847
33. D.G. Corley, R. Herb, R.E. Moore, P.J. Scheuer, and V.J. Paul Laulimalides. New potent cytotoxic macrolides from a marine sponge and a nudibranch predator J Org Chem 53 1988 3644 3646
34. J.F. Deeken, J.L. Marshall, M.J. Pishvaian, J. Hwang, C.M. Ahlers, P.L. Clemens, and et al. A phase I study of oral ixabepilone in patients with advanced solid tumors Cancer Chemother Pharmacol 73 2014 1071 1078
35. N. Denduluri, and S. Swain Ixabepilone: clinical role in metastatic breast cancer Clin Breast Cancer 11 2011 139 145
36. N. Desai, V. Trieu, Z. Yao, L. Louie, S. Ci, A. Yang, and et al. Increased antitumor activity, intratumor paclitaxel concentrations, and endothelial cell transport of Cremophor-free, albumin-bound paclitaxel, ABI-007, compared with Cremophor-based paclitaxel Clin Cancer Res 12 2006 1317 1324
37. M.C. Edler, R.M. Buey, R. Gussio, A.I. Marcus, C.D. Vanderwal, E.J. Sorensen, and et al. Cyclostreptin (FR182877), an antitumor tubulin-polymerizing agent deficient in enhancing tubulin assembly despite its high affinity for the taxoid site Biochemistry 44 2005 11525 11528
38. D.R. Feldman, G.V. Kondagunta, M.S. Ginsberg, N. Ishill, S. Patil, J. Cestaro, and et al. Phase II trial of ixabepilone in patients with cisplatin-refractory germ cell tumors Invest New Drugs 25 2007 487 490
39. Q. Feng, L. Tao, and Z. Liu Total synthesis of microtubule-stabilizing agent ceratamine A J Org Chem 78 2013 12814 12818
40. C. Ferlini, G. Raspaglio, S. Mozzetti, L. Cicchillitti, F. Filippetti, D. Gallo, and et al. The seco-taxaneIDN5390 is able to target class III beta-tubulin and to overcome paclitaxel resistance Cancer Res 65 2005 2397 2405
41. F. Feyen, F. Cachoux, J. Gertsch, M. Wartmann, and K.H. Altmann Epothilones as lead structures for the synthesis-based discovery of new chemotypes for microtubule stabilization Acc Chem Res 41 2008 21 31
42. J.J. Field, J.F. Díaz, and J.H. Miller The binding sites of microtubule-stabilizing agents Chem Biol 20 2013 301 315
43. J.J. Field, B. Pera, E. Calvo, A. Canales, D. Zurwerra, C. Trigili, and et al. Zampanolide, a potent new microtubule stabilizing agent, covalently reacts with the taxane luminal site in both tubulin α, β-heterodimers and microtubules Chem Biol 19 2012 686
44. J.J. Field, A.J. Singh, A. Kanakkanthara, T. Halafihi, P.T. Northcote, and J.H. Miller Microtubule-stabilizing activity of zampanolide, a potent macrolide isolated from the Tongan marine sponge Cacospongia mycofijiensis J Med Chem 52 2009 7328
45. D.P. Fitzgerald, D.L. Emerson, Y. Qian, T. Anwar, D.J. Liewehr, S.M. Steinberg, and et al. TPI-287, a new taxane family member, reduces the brain metastatic colonization of breast cancer cells Mol Cancer Ther 11 2012 1959 1967
46. G.J. Florence, N.M. Gardner, and I. Paterson Development of practical syntheses of the marine anticancer agents discodermolide and dictyostatin Nat Prod Rep 25 2008 342 375
47. R.A. Freedman, E. Bullitt, L. Sun, R. Gelman, G. Harris, J.A. Ligibel, and et al. A phase II study of sagopilone (ZK 219477; ZK-EPO) in patients with breast cancer and brain metastases Clin Breast Cancer 11 2011 376 383
48. T.N. Gaitanos, R.M. Buey, J.F. Díaz, P.T. Northcote, P. Teesdale-Spittle, J.M. Andreu, and et al. Peloruside A does not bind to the taxoid site on β-tubulin and retains its activity in multidrug-resistant cell lines Cancer Res 64 2004 5063 5067
49. E.J. Gapud, R. Bai, A.K. Ghosh, and E. Hamel Laulimalide and paclitaxel: A comparison of their effects on tubulin assembly and their synergistic action when present simultaneously Mol Pharmacol 66 2004 113 121
50. J. Gertsch, S. Meier, M. Müller, and K.-H. Altmann Differential effects of natural product microtubule stabilizers on microtubule assembly: single agent and combination studies with Taxol, epothilone B, and discodermolide Chembiochem 10 2009 166 175
51. S.P. Gunasekera, M. Gunasekera, R.E. Longley, and G.K. Schulte Discodermolide: A new bioactive polyhydroxylated lactone from the marine sponge Discodermia dissoluta J Org Chem 55 1990 4912 4915
52. E. Hamel, B.W. Day, J.H. Miller, M.K. Jung, P.T. Northcote, A.K. Ghosh, and et al. Synergistic effects of peloruside A and laulimalide with taxoid site drugs, but not with each other, on tubulin assembly Mol Pharmacol 70 2006 1555 1564
53. E. Hamel, D.L. Sackett, D. Vourloumis, and K.C. Nicolaou 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 38 1999 5490 5498
54. I.H. Hardt, H. Steinmetz, K. Gerth, F. Sasse, H. Reichenbach, and G. Höfle New natural epothilones from Sorangium cellulosum, strains So ce90/B2 and So ce90/D13: isolation, structure elucidation, and SAR studies J Nat Prod 64 2001 847 856
55. Z. He, A. Schulz, X. Wan, J. Seitz, H. Bludau, D.Y. Alakhova, and et al. Poly(2-oxazoline) based micelles with high capacity for 3rd generation taxoids: preparation, in vitro and in vivo evaluation J Control Release 28 2015 67 75
56. E.I. Heath, P. Lorusso, S.S. Ramalingam, A. Awada, M.J. Egorin, T. Besse-Hamer, and et al. A phase 1 study of BMS-275183, a novel oral analogue of paclitaxel given on a daily schedule to patients with advanced malignancies Invest New Drugs 29 2011 1426 1431
57. J. Hoffman, I. Fichtmer, M. Lemm, P. Lienau, H. Hess-Stumpp, A. Rotgeri, and et al. Sagopilone crosses the blood-brain barrier in vivo to inhibit brain tumor growth and metastases Neuro Oncol 11 2009 158 166
58. S. Honore, K. Kamath, D. Braguer, S.B. Horwitz, L. Wilson, C. Briand, and et al. Synergistic suppression of microtubule dynamics by discodermolide and paclitaxel in non-small cell lung carcinoma cells Cancer Res 64 2004 4957 4964
59. K.A. Hood, L.M. West, B. Rouwé, P.T. Northcote, M.V. Berridge, S.J. Wakefield, and et al. Peloruside A, a novel antimitotic agent with paclitaxel-like microtubule-stabilizing activity Cancer Res 62 2002 3356 3360
60. D.T. Hung, J. Chen, and S.L. Schreiber (+)-Discodermolide binds to microtubules in stoichiometric ratio to tubulin dimers, blocks taxol binding and results in mitotic arrest Chem Biol 3 1996 287 293
61. J.T. Huzil, J.K. Chik, G.W. Slysz, H. Freedman, J. Tuszynski, R.E. Taylor, and et al. A unique mode of microtubule stabilization induced by peloruside A J Mol Biol 378 2008 1016 1030
62. N.K. Ibrahim, N. Desai, S. Legha, P. Soon-Shiong, R.L. Theriault, E. Rivera, and et al. Phase I and pharmacokinetic study of ABI-007, a Cremophor-free, protein-stabilized, nanoparticle formulation of paclitaxel Clin Cancer Res 8 2002 1038 1044
63. R.A. Isbrucker, J. Cummins, S.A. Pomponi, R.E. Longley, and A.E. Wright Tubulin polymerizing activity of dictyostatin-1, a polyketide of marine sponge origin Biochem Pharmacol 66 2003 75 82
64. Y. Jing, W. Zhou, W. Li, L. Zhao, and Y. Wang The synthesis of novel taxoids for oral administration Bioorg Med Chem 22 2014 194 203
65. M.A. Jordan, I. Ojima, F. Rosas, M. Distefano, L. Wilson, G. Scambia, and et al. Effects of novel taxanes SB-T-1213 and IDN5109 on tubulin polymerization and mitosis Chem Biol 9 2002 93 101
66. M.A. Jordan, and L. Wilson Microtubule as a target for anticancer drugs Nat Rev Cancer 4 2004 253 265
67. G. Karjala, Q. Chan, E. Manzo, R.J. Andersen, and M. Roberge Ceratamines, structurally simple microtubule-stabilizing antimitotic agents with unusual cellular effects Cancer Res 65 2005 3040 3043
68. M. Khrapunovich-Baine, V. Menon, P. Verdier-Pinard, A.B. Smith III, R.H. Angeletti, A. Fiser, and et al. Distinct pose of discodermolide in Taxol binding pocket drives a complementary mode of microtubule stabilization Biochemistry 48 2009 11664 11677
69. M. Khrapunovich-Baine, V. Menon, C.P. Yang, P.T. Northcote, J.H. Miller, R.H. Angeletti, and et al. Hallmarks of molecular action of microtubule stabilizing agents: effects of epothilone B, ixabepilone, peloruside A, and laulimalide on microtubule conformation J Biol Chem 286 2011 11765 11778
70. T.Y. Kim, D.W. Kim, J.Y. Chung, S.G. Shin, S.C. Kim, and et al. Phase I and pharmacokinetic study of Genexol-PM, a Cremophor-free, polymeric micelle-formulated paclitaxel, in patients with advanced malignancies Clin Cancer Res 10 2004 3708 3716
71. J. Konner, R.N. Grisham, J. Park, O.A. O'Connor, G. Cropp, R. Johnson, and et al. Phase I clinical, pharmacokinetic, and pharmacodynamic study of KOS-862 (epothilone D) in patients with advanced solid tumors and lymphoma Invest New Drugs 30 2012 2294 2302
72. R.J. Kowalski, P. Giannakakou, S.P. Gunasekera, R.E. Longley, B.W. Day, and E. Hamel 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 cell Mol Pharmacol 52 1997 613 622
73. M.N. Kundranda, and J. Niu Albumin-bound paclitaxel in solid tumors: clinical development and future directions Drug Des Devel Ther 9 2015 3767 3777
74. E.T. Lam, S. Goel, L.J. Schaaf, G.F. Cropp, A.L. Hannah, Y. Zhou, and et al. Phase I dose escalation study of KOS-1584, a novel epothilone, in patients with advanced solid tumors Cancer Chemother Pharmacol 69 2012 523 531
75. J. Li, A.L. Risinger, and S.L. Mooberry Taccalonolide microtubule stabilizers Bioorg Med Chem 22 2014 5091 5096
76. S.Y. Liao, G.Q. Mo, J.C. Chen, and K.C. Zheng Exploration of the binding mode between (-)-zampanolide and tubulin using docking and molecular dynamics simulation J Mol Model 20 2014 2070 2078
77. T. Lindel, P.R. Jensen, W. Fenical, B.H. Long, A.M. Casazza, J. Carboni, and et al. Eleutherobin, a new cytotoxin class that mimics paclitaxel (Taxol) by stabilizing microtubules J Am Chem Soc 119 1997 8744 8745
78. J. Liu, M.J. Towle, H. Cheng, P. Saxton, C. Reardon, J. Wu, and et al. In vitro and in vivo anticancer activities of synthetic (-)-laulimalide, a marine natural product microtubule stabilizing agent Anticancer Res 27 2007 1509 1518
79. A.C. Lockhart, R. Bukowski, M.L. Rothenberg, K.K. Wang, W. Cooper, J. Grover, and et al. Phase I trial of oral MAC-321 in subjects with advanced malignant solid tumors Cancer Chemother Pharmacol 60 2007 203 209
80. ®) Cancer Res 58 1998 1111 1115
81. R.E. Longley, D. Caddigan, D. Harmody, M. Gunasekera, and S.P. Gunasekera Discodermolide - a new, marine derived immunosuppressive compound. II. In vivo studies Transplantation 52 1991 656 661
82. C. Madiraju, M.C. Edler, E. Hamel, and et al. Tubulin assembly, taxoid site binding, and cellular effects of the microtubule-stabilizing agent dictyostatin Biochemistry 44 2005 15053 15063
83. E. Manzo, R. van Soest, L. Matainaho, M. Roberge, and R.J. Andersen Ceratamines A and B, antimitotic heterocyclic alkaloids isolated from the marine sponge Pseudoceratina sp. collected in Papua New Guinea Org Lett 5 2003 4591 4594
84. L.A. Martello, H.M. McDaid, D.L. Regl, C.P. Yang, D. Meng, T.R. Pettus, and et al. Taxol and discodermolide represent a synergistic drug combination in human carcinoma cell lines Clin Cancer Res 6 2000 1978 1987
85. S. McMeekin, D. Dizon, J. Barter, G. Scambia, L. Manzyuk, A. Lisyanskaya, and et al. Phase III randomized trial of second-line ixabepilone versus paclitaxel or doxorubicin in women with advanced endometrial cancer Gynecol Oncol 138 2015 18 23
86. O. Metzger-Filho, C. Moulin, E. de Azambuja, and A. Ahmad Larotaxel: broadening the road with new taxanes Expert Opin Investig Drugs 18 2009 1183 1189
87. C.J. Meyer, M. Krauth, M.J. Wick, J.W. Shay, G. Gellert, J.K. De Brabander, and et al. Peloruside A inhibits growth of human lung and breast tumor xenografts in an athymic nu/nu mouse model Mol Cancer Ther 14 2015 1816 1823
88. A. Mita, A. Lockhart, T.L. Chen, K. Bochinske, J. Curtright, W. Cooper, and et al. A phase I pharmacokinetic (PK) trial of XAA296A (discodermolide) administered every 3 wks to adult patients with advance solid malignancies J Clin Oncol 22 S14 2004 2025
89. A.C. Mita, A.J. Olszanski, R.C. Walovitch, R.P. Perez, K. MacKay, and et al. Phase I and pharmacokinetic study of AI-850, a novel microparticle hydrophobic drug delivery system for paclitaxel Clin Cancer Res 13 2007 3293 3301
90. D. Mitchell, G. Bergendahl, W. Ferguson, W. Roberts, T. Higgins, T. Ashikaga, and et al. A phase 1 trial of TPI 287 as a single agent and in combination with temozolomide in patients with refractory or recurrent neuroblastoma or medulloblastoma Pediatr Blood Cancer 2015 10.1002/pbc.25687
91. S.L. Mooberry, G. Tien, A.H. Hernandez, A. Plubrukarn, and B.S. Davidson Laulimalide and isolaulimalide, new paclitaxel-like microtubule-stabilizing agents Cancer Res 59 1999 653 660
92. E. Mukhtar, V.M. Adhami, M. Sechi, and H. Mukhtar Dietary flavonoid fisetin binds to β-tubulin and disrupts microtubule dynamics in prostate cancer cells Cancer Lett 367 2015 173 183
93. L. Nayak, L.M. DeAngelis, H.I. Robins, R. Govindan, S. Gadgeel, K. Kelly, and et al. Multicenter phase 2 study of patupilone for recurrent or progressive brain metastases from non-small cell lung cancer Cancer 2015 10.1002/cncr.29636
94. J.H. Nettles, H. Li, B. Cornett, J.M. Krahn, J.P. Snyder, and K.H. Downing The binding mode of epothilone A on α-, β-tubulin by electron crystallography Science 305 2004 866 869
95. M.I. Nicoletti, T. Colombo, C. Rossi, C. Monardo, S. Stura, M. Zucchetti, and et al. IDN5109, a taxane with oral bioavailability and potent antitumor activity Cancer Res 60 2000 842 846
96. G. Nightingale, and J. Ryum Cabazitaxel (jevtana): A novel agent for metastatic castration-resistant prostate cancer. P T 37 440-442 2012 445 448
97. M. Nodwell, J.L. Riffell, M. Roberge, and R.J. Andersen Synthesis of antimitotic analogs of the microtubule stabilizing sponge alkaloid ceratamine A Org Lett 10 2008 1051 1054
98. M. Nodwell, C. Zimmerman, M. Roberge, and R.J. Andersen Synthetic analogues of the microtubule-stabilizing sponge alkaloid ceratamine A are more active than the natural product J Med Chem 53 2010 7843 7851
99. T. O'Reilly, M. Wartmann, J. Brueggen, P.R. Allegrini, A. Floersheimer, M. Maira, and et al. Pharmacokinetic profile of the microtubule stabilizer patupilone in tumor-bearing rodents and comparison of anti-cancer activity with other MTS in vitro and in vivo Cancer Chemother Pharmacol 62 2008 1045 1054
100. I. Ojima, J. Chen, L. Sun, C.P. Borella, T. Wang, M.L. Miller, and et al. Design, synthesis and biological evaluation of new generation taxoids J Med Chem 51 2008 3203 3221
101. I. Ojima, and M. Das Recent advances in the chemistry and biology of new generation taxoids J Nat Prod 72 2009 554 565
102. I. Ojima, K. Kumar, D. Awasthi, and J.G. Vineberg Drug discovery targeting cell division proteins, microtubules and FtsZ Bioorg Med Chem 22 2014 5060 5077
103. B. Otová, I. Ojima, R. Václavíková, J. Hrdý, M. Ehrlichová, P. Souček, and et al. Second-generation taxanes effectively suppress subcutaneous rat lymphoma: role of disposition, transport, metabolism, in vitro potency and expression of angiogenesis genes Invest New Drugs 30 2012 991 1002
104. D.M. Peereboom, C. Murphy, M.S. Ahluwalia, A. Conlin, A. Eichler, C. Van Poznak, and et al. Phase II trial of patupilone in patients with brain metastases from breast cancer Neuro Oncol 16 2014 579 583
105. J. Peng, A.L. Risinger, G.A. Fest, E.M. Jackson, G. Helms, L.A. Polin, and et al. Identification and biological activities of new taccalonolide microtubule stabilizers J Med Chem 54 2011 6117 6124
106. A. Pepe, L. Sun, I. Zanardi, X. Wu, C. Ferlini, G. Fontana, and et al. Novel C-seco-taxoids possessing high potency against paclitaxel-resistant cancer cell lines overexpressing class III beta-tubulin Bioorg Med Chem Lett 19 2009 3300 3304
107. B. Pera, M. Razzak, C. Trigili, O. Pineda, A. Canales, R.M. Buey, and et al. Molecular recognition of peloruside A by microtubules. The C24 primary alcohol is essential for biological activity Chembiochem 11 2010 1669 1678
108. B. Pera, M.N. Calvo-Vidal, S. Ambati, M. Jordi, A. Kahn, J.F. Díaz, and et al. High affinity and covalent-binding microtubule stabilizing agents show activity in chemotherapy-resistant acute myeloid leukemia cells Cancer Lett 368 2015 97 104
109. E.A. Perez, G. Lerzo, X. Pivot, E. Thomas, L. Vahdat, L. Bosserman, and et al. Efficacy and safety of ixabepilone (BMS-247550) in a phase II study of patients with advanced breast cancer resistant to an anthracycline, a taxane, and capecitabine J Clin Oncol 25 2007 3407 3414
110. G.R. Pettit, Z.A. Cichacz, F. Gao, M.R. Boyd, and J.M. Schmidt Isolation and structure of the cancer cell growth inhibitor dictyostatin 1 J Chem Soc Chem Commun 9 1994 1111 1112
111. B. Pfeiffer, K. Hauenstein, P. Merz, J. Gertsch, and K.H. Altmann Synthesis and SAR of C12-C13-oxazoline derivatives of epothilone A Bioorg Med Chem Lett 19 2009 3760 3763
112. O. Pineda, J. Farras, L. Maccari, F. Manetti, M. Botta, and J. Vilarrasa Computational comparison of microtubule-stabilising agents laulimalide and peloruside with Taxol and colchicine Bioorg Med Chem Lett 14 2004 4825 4829
113. A.E. Prota, K. Bargsten, P.T. Northcote, M. Marsh, K.-H. Altmann, J.H. Miller, and et al. Structural basis of microtubule stabilization by laulimalide and pelorusideA Angew Chem Int Ed 53 2014 1621 1625
114. A.E. Prota, K. Bargsten, D. Zurwerra, J.J. Field, J.F. Díaz, K.H. Altmann, and et al. Molecular mechanism of action of microtubule-stabilizing anticancer agents 339 2013 587 590
115. A.J. Prussia, Y. Yang, M.T. Geballe, and J.P. Snyder Cyclostreptin and microtubules: is a low-Affinity binding site required? Chembiochem 11 2010 101 109
116. D.E. Pryor, A. O'Brate, G. Bilcer, J.F. Díaz, Y. Wang, Y. Wang, and et al. 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 41 2002 9109 9115
117. R.K. Ramanathan, J. Picus, H. Raftopoulos, S. Bernard, A.C. Lockhart, and G. Frenette A phase II study of milataxel: A novel taxane analogue in previously treated patients with advanced colorectal cancer Cancer Chemother Phamacol 61 2008 453 458
118. A. Regueiro-Ren, K. Leavitt, S.H. Kim, G. Höfle, M. Kiffe, J.Z. Gougoutas, and et al. SAR and pH stability of cyano-substituted epothilones Org Lett 4 2002 3815 3818
119. A.L. Risinger, E.M. Jackson, L.A. Polin, G.L. Helms, D.A. LeBoeuf, P.A. Joe, and et al. The taccalonolides: microtubule stabilizers that circumvent clinically relevant taxane resistance mechanisms Cancer Res 68 2008 8881 8888
120. A.L. Risinger, J. Li, M.J. Bennett, C.C. Rohena, J. Peng, D.C. Schriemer, and et al. Taccalonolide binding to tubulin imparts microtubule stability and potent in vivo activity Cancer Res 73 2013 6780 6792
121. A.L. Risinger, and S.L. Mooberry Cellular studies reveal mechanistic differences between taccalonolide A and paclitaxel Cell Cycle 10 2011 2162 2171
122. A.L. Risinger, S.M. Riffle, M. Lopus, M.A. Jordan, L. Wilson, and S.L. Mooberry The taccalonolides and paclitaxel cause distinct effects on microtubule dynamics and aster formation Mol Cancer 13 2014 41
123. W.C. Rose, B.H. Long, C.R. Fairchild, F.Y. Lee, and J.F. Kadow Preclinical pharmacology of BMS-275183, an orally active taxane Clin Cancer Res 7 2001 2016 2021
124. H.S. Rugo, W.T. Barry, A. Moreno-Aspitia, A.P. Lyss, C. Cirrincione, E. Leung, and et al. Randomized phase III trial of paclitaxel once per week compared with nanoparticle albumin-bound nab-paclitaxel once per week or ixabepilone with bevacizumab as first-line chemotherapy for locally recurrent or metastatic breast cancer: CALGB 40502/NCCTG N063H (alliance) J Clin Oncol 33 2015 2361 2369
125. M.W. Saif, J. Sarantopoulos, A. Patnaik, A.W. Tolcher, C. Takimoto, and M. Beeram Tesetaxel, a new oral taxane, in combination with capecitabine: A phase I, dose-escalation study in patients with advanced solid tumors Cancer Chemother Pharmacol 68 2011 1565 1573
126. D. Sampath, C.M. Discafani, F. Loganzo, C. Beyer, H. Liu, X. Tan, and et al. MAC-321, a novel taxane with greater efficacy than paclitaxel and docetaxel in vitro and in vivo Mol Cancer Ther 2 2003 873 884
127. D. Sampath, L.M. Greenberger, C. Beyer, M. Hari, H. Liu, M. Baxter, and et al. Preclinical pharmacologic evaluation of MST-997, an orally active taxane with superior in vitro and in vivo efficacy in paclitaxel- and docetaxel-resistant tumor models Clin Cancer Res 12 2006 3459 3469
128. B. Sato, H. Muramatsu, M. Miyauchi, Y. Hori, S. Takase, M. Hino, and et al. A new antimitotic substance, FR182877: I. Taxonomy, fermentation, isolation, physico-chemical properties and biological activities J Antibiot (Tokyo) 53 2000 123 130
129. B. Sato, H. Nakajima, Y. Hori, M. Hino, S. Hashimoto, and H. Terano A new antimitotic substance, FR182877: II. The mechanism of action J Antibiot (Tokyo) 53 2000 204 206
130. C. Sessa, A. Perotti, A. Lladò, S. Cresta, G. Capri, M. Voi, and et al. Phase I clinical study of the novel epothilone B analogue BMS-310705 given on a weekly schedule Ann Oncol 18 2007 1548 1553
131. P.B. Schiff, J. Fant, and S.B. Horwitz Promotion of microtubule assembly in vitro by taxol Nature 277 1979 665 667
132. M. Shah, V. Shah, A. Ghosh, Z. Zhang, and T. Minko Molecular inclusion complexes of β-cyclodextrin derivatives enhance aqueous solubility and cellular internalization of paclitaxel: preformulation and in vitro assessments J Pharm Pharmacol (Los Angel) 2 2015 8
133. M. Shionoya, T. Jimbo, M. Kitagawa, T. Soga, and A. Tohgo DJ-927, a novel oral taxane, overcomes P-glycoprotein-mediated multidrug resistance in vitro and in vivo Cancer Sci 94 2003 459 466
134. R. Singh, M. Sharma, P. Joshi, and D. Rawat Clinical status of anti-cancer agents derived from marine sources Anti Cancer Agents Med Chem 8 2008 603 617
135. A.B. Smith, I.G. Safanov, and R.M. Gorbett Total synthesis of (+)-zampanolide J Am Chem Soc 123 2001 12426
136. A.B. Smith, I.G. Safanov, and R.M. Gorbett Total synthesis of (+)-zampanolide and (+)-dactylolide exploiting a unified strategy J Am Chem Soc 124 2002 11102
137. J. Tanaka, and T. Higa Zampanolide, a new cytotoxic macrolide from a marine sponge Tetrahedron Lett 37 1996 5535
138. E. Ter Haar, R.J. Kowalski, E. Hamel, C.M. Lin, R.E. Longley, S.P. Gunasekera, and et al. Discodermolide, a cytotoxic marine agent that stabilizes microtubules more potently than Taxol Biochemistry 35 1996 243 250
139. T.L. Tinley, D.A. Randall-Hlubek, R.M. Leal, E.M. Jackson, J.W. Cessac, J.C. Quada Jr., and et al. Taccalonolides E and A: plant-derived steroids with microtubule-stabilizing activity Cancer Res 63 2003 3211 3220
140. K. Tonkin, H. Herbert, C. Lathia, and et al. A phase I and pharmacokinetic study of a novel oral taxane BAY 59-8862 in solid tumors Proc Am Soc Clin Oncol 22 2003 (Abstract 965)
141. J. Uenishi, T. Iwamoto, and J. Tanaka Total synthesis of (-)-zampanolide and questionable existence of (-)-dactylolide as the elusive biosynthetic precursor of (-)-zampanolide in an Okinawan sponge Org Lett 11 2009 3262
142. L.L. Vollmer, M. Jiménez, D.P. Camarco, W. Zhu, H.N. Daghestani, R. Balachandran, and et al. A simplified synthesis of novel dictyostatin analogs with in vitro activity against epothilone B resistant cells and antiangiogenic activity in zebrafish embryos Mol Cancer Ther 10 2011 994 1006
143. P. Vrignaud, D. Sémiond, P. Lejeune, H. Bouchard, L. Calvet, C. Combeau, and et al. Preclinical antitumor activity of cabazitaxel, a semisynthetic taxane active in taxane-resistant tumors Clin Cancer Res 19 2013 2973 2983
144. Y.J. Wang, L.J. Chen, L.W. Tan, Q. Zhao, F. Luo, Y.Q. Wei, and et al. PEG-PCL based micelle hydrogels as oral docetaxel delivery systems for breast cancer therapy Biomaterials 35 2014 6972 6985
145. L.M. West, P.T. Northcote, and C.N. Battershill Peloruside A: A potent cytotoxic macrolide isolated from the New Zealand marine sponge Mycale sp. J Org Chem 65 2000 445 449
146. A. Wilmes, D. O'Sullivan, A. Chan, C. Chandrahasen, I. Paterson, P.T. Northcote, and et al. Synergistic interactions between peloruside A and other microtubule-stabilizing and destabilizing agents in cultured human ovarian carcinoma cells and murine T cells Cancer Chemother Pharmacol 68 2011 117 126
147. D.A. Yardley Nab-paclitaxel mechanisms of action and delivery J Control Release 170 2013 365 372
148. J.A. Zhang, G. Anyarambhatla, L. Ma, S. Ugwu, T. Xuan, and et al. Development and characterization of a novel Cremophor EL free liposome-based paclitaxel (LEP-ETU) formulation Eur J Pharm Biopharm 59 2005 177 187
149. Y. Zhao, W.S. Fang, and K. Pors Microtubule stabilising agents for cancer chemotherapy Expert Opin Ther Pat 19 2009 607 622