An overview of microtubule targeting agents for cancer therapy

Karahalil, Bensu; Yardım-Akaydin, Sevgi; Nacak Baytas, Sultan

doi:10.2478/aiht-2019-70-3258

Abstract

The entire world is looking for effective cancer therapies whose benefits would outweigh their toxicity. One way to reduce resistance to chemotherapy and its adverse effects is the so called targeted therapy, which targets specific molecules (“molecular targets”) that play a critical role in cancer growth, progression, and metastasis. One such specific target are microtubules. In this review we address the current knowledge about microtubule-targeting agents or drugs (MTAs/MTDs) used in cancer therapy from their synthesis to toxicities. Synthetic and natural MTAs exhibit antitumor activity, and preclinical and clinical studies have shown that their anticancer effectiveness is higher than that of traditional drug therapies. Furthermore, MTAs involve a lower risk of adverse effects such as neurotoxicity and haemotoxicity. Several new generation MTAs are currently being evaluated for clinical use. This review brings updated information on the benefits of MTAs, therapeutic approaches, advantages, and challenges in their research.

References

1. Chabner BA, Roberts TG Jr. Timeline: Chemotherapy and the war on cancer. Nat Rev Cancer 2005;5:65–72. doi: 10.1038/nrc152910.1038/nrc152915630416
Open DOI Search in Google Scholar Back to article
2. World Health Organization (WHO). Cancer, Fact sheet February 2017 [displayed 9 September 2019]. Available at https://www.who.int/news-room/fact-sheets/detail/cancer
Search in Google Scholar Back to article
3. Kumar S, Ahmad MK, Waseem M, Pandey AK. Drug targets for cancer treatment: an overview. Med Chem 2015;5:115–23. doi: 10.4172/2161-0444.100025210.4172/2161-0444.1000252
Open DOI Search in Google Scholar Back to article
4. Poruchynsky MS, Komlodi-Pasztor E, Trostel S, Wilkerson J, Regairaz M, Pommier Y, Zhang X, Kumar Maity T, Robey R, Burotto M, Sackett D, Guha U, Fojo AT. Microtubule-targeting agents augment the toxicity of DNA-damaging agents by disrupting intracellular trafficking of DNA repair proteins. Proc Natl AcadSci U S A 2015;112:1571–6. doi: 10.1073/pnas.141641811210.1073/pnas.1416418112432124525605897
Open DOI Search in Google Scholar Back to article
5. Giavazzi R, Bonezzi K, Taraboletti G. Microtubule targeting agents and the tumor vasculature. In: Fojo AT, editor. The role of microtubules in cell biology, neurobiology, and oncology. Totowa (NJ). Humana Press; 2008. p. 519–30.10.1007/978-1-59745-336-3_19
Search in Google Scholar Back to article
6. Jordan MA, Wilson L. Microtubules as a target for anticancer drugs. Nat Rev Cancer 2004;4:253–65. doi: 10.1038/nrc13171505728510.1038/nrc131715057285
Open DOI Search in Google Scholar Back to article
7. Dong M, Liu F, Zhou H, Zhai S, Yan B. Novel natural product and privileged scaffold-based tubulin inhibitors targeting the colchicine binding site. Molecules 2016;21:1375. doi: 10.3390/molecules2110137510.3390/2110137527754459
Open DOI Search in Google Scholar Back to article
8. Kavallaris M, Kuo DY, Burkhart CA, Regl DL, Norris MD, Haber M, Horwitz SB. Taxol-resistant epithelial ovarian tumors are associated with altered expression of specific beta-tubulin isotypes. J Clin Invest 1997;100:1282–93. doi: 10.1172/JCI119642927674710.1172/JCI119642
Search in Google Scholar Back to article
9. Forli S. Epothilones: from discovery to clinical trials. Curr Top Med Chem 2014;14:2312–21. doi: 10.2174/156802661466614113009585510.2174/1568026614666141130095855462978825434353
Open DOI Search in Google Scholar Back to article
10. Crimmins MT. Synthetic approaches to the microtubule stabilizing agent (-)-laulimalide. Curr Opin Drug Discov Devel 2002;5:944–59. PMID: 12478725
Search in Google Scholar Back to article
11. Steinmetz MO, Prota AE. Microtubule-targeting agents: strategies to hijack the cytoskeleton. Trends Cell Biol 2018;28:776–92. doi: 10.1016/j.tcb.2018.05.00110.1016/j.tcb.2018.05.00129871823
Open DOI Search in Google Scholar Back to article
12. Sapra S, Bhalla Y, Sharma S, Singh G, Nepali K, Budhiraja A, Dhar KL. Colchicine and its various physicochemical and biological aspects. Med Chem Res 2013;22:531–47. doi: 10.1007/s00044-012-0077-z10.1007/s00044-012-0077-z
Open DOI Search in Google Scholar Back to article
13. Jain S, Vahdat LT. Eribulinmesylate. Clin Cancer Res 2011;17:6615–22. doi: 10.1158/1078-0432.CCR-11-180710.1158/1078-0432.CCR-11-180721859830
Open DOI Search in Google Scholar Back to article
14. Modrianský M, Dvorák Z. Microtubule disruptors and their interaction with biotransformation enzymes. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 2005;149:213–5. doi: 10.5507/bp.2005.02810.5507/bp.2005.028
Open DOI Search in Google Scholar Back to article
15. Dumontet C, Jordan MA. Microtubule-binding agents: a dynamic field of cancer therapeutics. Nat Rev Drug Discov 2010;9:790–803. doi: 10.1038/nrd325310.1038/nrd3253
Open DOI Search in Google Scholar Back to article
16. Prota AE, Bargsten K, Zurwerra D, Field JJ, Díaz JF, Altmann KH, Steinmetz MO. Molecular mechanism of action of microtubule-stabilizing anticancer agents. Science 2013;339:587–90. doi: 10.1126/science.123058210.1126/.1230582
Open DOI Search in Google Scholar Back to article
17. Pryor DE, O’Brate A, Bilcer G, Díaz JF, Wang Y, Wang Y, Kabaki M, Jung MK, Andreu JM, Ghosh AK, 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;41:9109–15. doi: 10.1021/bi020211b10.1021/bi020211b
Open DOI Search in Google Scholar Back to article
18. Prota AE, Bargsten K, Northcote PT, Marsh M, Altmann KH, Miller JH, Díaz JF, Steinmetz MO. Structural basis of microtubule stabilization by laulimalide and peloruside A. Angew Chem Int Ed Engl 2014;53:1621–5. doi: 10.1002/anie.20130774910.1002/anie.201307749
Open DOI Search in Google Scholar Back to article
19. Pellegrini F. Review: Tubulin function, action of antitubulin drugs and new drug development. Cancer Invest 2005;23:264–73. doi: 10.1081/CNV-20005597010.1081/CNV-200055970
Open DOI Search in Google Scholar Back to article
20. Ley CD, Horsman MR, Kristjansen PE. Early effects of combretastatin-A4 disodium phosphate on tumor perfusion and interstitial fluid pressure. Neoplasia 2007;9:108–12. doi: 10.1593/neo.0673310.1593/neo.06733
Open DOI Search in Google Scholar Back to article
21. Gutiérrez ST, Díaz-Oltra S, Falomir E, Murga J, Cardaa M, Marco JA. Synthesis of combretastatin A-4 O-alkyl derivatives and evaluation of their cytotoxic, antiangiogenic and antitelomerase activity. Bioorg Med Chem 2013;21:7267–74. doi: 10.1016/j.bmc.2013.09.06410.1016/j.bmc.2013.09.064
Open DOI Search in Google Scholar Back to article
22. Ohsumi K, Hatanaka T, Fujita K, Nakagawa R, Fukuda Y, Nihei Y, Suga Y, Morinaga Y, Akiyama Y, Tsuji T. Syntheses and antitumor activity of cis-restricted combretastatins, 5-membered heterocyclic analogues. Bioorg Med Chem Lett 1998;8:3153–8. doi: 10.1016/s0960-894x(98)00579-410.1016/S0960-894X(98)00579-4
Search in Google Scholar Back to article
23. Yang T, Wang Y, Li Z, Dai W, Yin J, Liang L, Ying X, Zhou S, Wang J, Zhang X, Zhang Q. Targeted delivery of a combination therapy consisting of combretastatin A4 and low-dose doxorubicin against tumorneovasculature. Nanomedicine 2012;8:81–92. doi: 10.1016/j.nano.2011.05.00310.1016/j.nano.2011.05.00321664295
Search in Google Scholar Back to article
24. Gao M, Zhang D, Jin Q, Jiang C, Wang C, Li J, Peng F, Huang D, Zhang J, Song S. Combretastatin-A4 phosphate improves the distribution and antitumor efficacy of albumin-bound paclitaxel in W256 breast carcinoma model. Oncotarget 2016;7:58133–41. doi: 10.18632/oncotarget.1124910.18632/oncotarget.11249529541827531898
Search in Google Scholar Back to article
25. Abma E, Daminet S, Smets P, Ni Y, de Rooster H. Combretastatin A4-phosphate and its potential in veterinary oncology, a review. Vet Comp Oncol 2017;15:184–93. doi: 10.1111/vco.1215010.1111/vco.1215025988493
Open DOI Search in Google Scholar Back to article
26. Marzo-Mas A, Barbier P, Breuzard G, Allegro D, Falomir E, Murga J, Carda M, Peyrot V, Marco JA. Interactions of long-chain homologues of colchicine with tubulin. Eur J Med Chem 2017;126:526–35. doi: 10.1016/j.ejmech.2016.11.04910.1016/j.ejmech.2016.11.04927915168
Open DOI Search in Google Scholar Back to article
27. Ahmed RI, Osman EE, Awadallah FM, El-Moghazy SM. Design, synthesis and molecular docking of novel diarylcyclohexenone and diarylindazole derivatives as tubulin polymerization inhibitors. J Enzyme Inhib Med Chem 2017;32:176–88. doi: 10.1080/14756366.2016.124453210.1080/14756366.2016.1244532600992527771966
Open DOI Search in Google Scholar Back to article
28. De Martino G, La Regina G, Coluccia A, Edler MC, Barbera MC, Brancale A, Wilcox E, Hamel E, Artico M, Silvestri R. Arylthioindoles, potent inhibitors of tubulin polymerization. J Med Chem 2004;47:6120–3. doi: 10.1021/jm049360d10.1021/jm049360d15566282
Open DOI Search in Google Scholar Back to article
29. Tantak MP, Wang J, Singh RP, Kumar A, Shah K, Kumar D. 2-(3’-Indolyl)-N-arylthiazole-4-carboxamides: Synthesis and evaluation of antibacterial and anticancer activities. Bioorg Med Chem Lett 2015;25:4225–31. doi: 10.1016/j.bmcl.2015.07.10510.1016/j.bmcl.2015.07.105456747626298501
Open DOI Search in Google Scholar Back to article
30. Kamath PR, Sunil D, Ajees AA, Pai KS, Das S. Some new indole-coumarin hybrids; Synthesis, anticancer and Bcl-2 docking studies. Bioorg Chem 2015;63:101–9. doi: 10.1016/j.bioorg.2015.10.00110.1016/j.bioorg.2015.10.00126469742
Open DOI Search in Google Scholar Back to article
31. Das Mukherjee D, Kumar NM, Tantak MP, Das A, Ganguli A, Datta S, Kumar D, Chakrabarti G. Development of novel bis(indolyl)-hydrazide-hydrazone derivatives as potent microtubule-targeting cytotoxic agents against A549 lung cancer cells. Biochemistry 2016;55:3020–35. doi: 10.1021/acs.biochem.5b0112710.1021/acs.biochem.5b0112727110637
Open DOI Search in Google Scholar Back to article
32. Liu Y-M, Chen H-L, Lee H-Y, Liou J-P. Tubulin inhibitors: a patent review. Expert OpinTher Pat 2014;24:69–88. doi: 10.1517/13543776.2014.85924710.1517/13543776.2014.85924724313741
Open DOI Search in Google Scholar Back to article
33. Ramya PVS, Guntuku L, Angapelly S, Digwal CS, Lakshmi UJ, Sigalapalli DK, Babu BN, Naidu VGM, Kamal A. Synthesis and biological evaluation of curcumin inspired indole analogues as tubulin polymerization inhibitors. Eur J Med Chem 2017;127:100–14. doi: 10.1016/j.ejmech.2016.12.04310.1016/j.ejmech.2016.12.04328038323
Open DOI Search in Google Scholar Back to article
34. Zhang YL, Qin YJ, Tang DJ, Yang MR, Li BY, Wang YT, Cai HY, Wang BZ, Zhu HL. Synthesis and biological evaluation of 1-methyl-1H-indole-pyrazoline hybrids as potential tubulin polymerization inhibitors. Chem Med Chem 2016;11:1446–58. doi: 10.1002/cmdc.20160013710.1002/cmdc.20160013727159418
Open DOI Search in Google Scholar Back to article
35. Wang YT, Cai XC, Shi TQ, Zhang YL, Wang ZC, Liu CH, Zhu HL. Synthesis, molecular docking and biological evaluation of 1-phenylsulphonyl-2-(1-methylindol-3-yl)-benzimidazole derivatives as novel potential tubulin assembling inhibitors. Chem Biol Drug Des 2017;90:112–8. doi: 10.1111/cbdd.1293210.1111/cbdd.1293228032450
Search in Google Scholar Back to article
36. Guggilapu SD, Lalita G, Reddy TS, Prajapti SK, Nagarsenkar A, Ramu S, Brahma UR, Lakshmi UJ, Vegi GMN, Bhargava SK, Babu BN. Synthesis of C5-tethered indolyl-3-glyoxylamide derivatives as tubulin polymerization inhibitors. Eur J Med Chem 2017;28:1–12. doi: 10.1016/j.ejmech.2017.01.02610.1016/j.ejmech.2017.01.02628131777
Open DOI Search in Google Scholar Back to article
37. Chennamaneni S, Gan C, Lama R, Zhong B, Su B. Indomethacin derivatives as tubulin stabilizers to inhibit cancer cell proliferation. Bioorg Med Chem 2016;24:277–85. doi: 10.1016/j.bmc.2015.12.01610.1016/j.bmc.2015.12.01626712098
Open DOI Search in Google Scholar Back to article
38. Baytas SN, Inceler N, Yilmaz A, Olgac A, Menevse S, Banoglu E, Hamel E, Bortolozzi R, Viola G. Synthesis, biological evaluation and molecular docking studies of trans-indole-3-acrylamide derivatives, a new class of tubulin polymerization inhibitors. Bioorg Med Chem 2014;22:3096–104. doi: 10.1016/j.bmc.2014.04.02710.1016/j.bmc.2014.04.027409168024816066
Open DOI Search in Google Scholar Back to article
39. Ghinet A, Moise IM, Rigo B, Homerin G, Farce A, Dubois J, Bîcu E. Studies on phenothiazines, new microtubule-interacting compounds with phenothiazine A-ring as potent antineoplastic agents. Bioorg Med Chem 2016;24:2307–17. doi: 10.1016/j.bmc.2016.04.00110.1016/j.bmc.2016.04.00127073050
Open DOI Search in Google Scholar Back to article
40. Ali I, Lone MN, Al-Othman ZA, Al-Warthan A, Sanagi MM. Heterocyclic scaffolds: centrality in anticancer drug development. Curr Drug Targets 2015;16:711–34. doi: 10.2174/138945011666615030911592210.2174/138945011666615030911592225751009
Open DOI Search in Google Scholar Back to article
41. Singh S, Ahmad A, Raghuvanshi DS, Hasanain M, Agarwal K, Dubey V, Fatima K, Alam S, Sarkar J, Luqman S, Khan F, Tandon S, Gupta A. Synthesis of 3,5-dihydroxy-7,8-dimethoxy-2-(4-methoxyphenyl)benzopyran-4-one derivatives as anticancer agents. Bioorg Med Chem Lett 2016;26:5322–7. doi: 10.1016/j.bmcl.2016.09.03610.1016/j.bmcl.2016.09.03627671497
Open DOI Search in Google Scholar Back to article
42. Andújar I, Ríos JL, Giner RM, Recio MC. Pharmacological properties of shikonin - a review of literature since 2002. Planta Med 2013;79:1685–97. doi: 10.1055/s-0033-135093410.1055/s-0033-135093424155261
Open DOI Search in Google Scholar Back to article
43. Andújar I, Ríos JL, Giner RM, Recio MC. Shikonin promotes intestinal wound healing in vitro via induction of TGF-β release in IEC-18 cells. Eur J Pharm Sci 2013;49:637–41. doi: 10.1016/j.ejps.2013.05.01810.1016/j.ejps.2013.05.01823727294
Open DOI Search in Google Scholar Back to article
44. Huang CS, Lin AH, Yang TC, Liu KL, Chen HW, Lii CK. Shikonin inhibits oxidized LDL-induced monocyte adhesion by suppressing NFκB activation via up-regulation of PI3K/Akt/Nrf2-dependent antioxidation in EA.hy926 endothelial cells. Biochem Pharmacol 2015;93:352–61. doi: 10.1016/j.bcp.2014.12.00510.1016/j.bcp.2014.12.00525541286
Open DOI Search in Google Scholar Back to article
45. Skrzypczak A, Przystupa N, Zgadzaj A, Parzonko A, Sykłowska-Baranek K, Paradowska K, Nałęcz-Jawecki G. Antigenotoxic, anti-photogenotoxic and antioxidant activities of natural naphthoquinone shikonin and acetylshikonin and Arnebiaeuchroma callus extracts evaluated by the umu-test and EPR method. Toxicol In Vitro 2015;30:364–72. doi: 10.1016/j.tiv.2015.09.02910.1016/j.tiv.2015.09.02926434532
Open DOI Search in Google Scholar Back to article
46. Liang D, Sun Y, Shen Y, Li F, Song X, Zhou E, Zhao F, Liu Z, Fu Y, Guo M, Zhang N, Yang Z, Cao Y. Shikonin exerts anti-inflammatory effects in a murine model of lipopolysaccharide-induced acute lung injury by inhibiting the nuclear factor-kappa B signaling pathway. IntImmunopharmacol 2013;16:475–80. doi: 10.1016/j.intimp.201310.1016/j.intimp.2013
Open DOI Search in Google Scholar Back to article
47. Liu J, Wang P, Xue YX, Li Z, Qu CB, Liu YH. Enhanced antitumor effect of shikonin by inhibiting Endoplasmic Reticulum Stress via JNK/c-Jun pathway in human glioblastoma stem cells. Biochem Biophys Res Commun 2015;466:103–10. doi: 10.1016/j.bbrc.2015.08.11510.1016/j.bbrc.2015.08.11526321663
Search in Google Scholar Back to article
48. Qiu HY, Wang F, Wang X, Sun WX, Qi JL, Pang YJ, Yang RW, Lu GH, Wang XM, Yang YH. Design, synthesis, and biological evaluation of chalcone-containing shikonin derivatives as inhibitors of tubulin polymerization. Chem Med Chem 2017;12:399–406. doi: 10.1002/cmdc.20170000110.1002/cmdc.20170000128211616
Open DOI Search in Google Scholar Back to article
49. Kamal A, Srikanth YV, Naseer Ahmed Khan M, Ashraf M, Kashi Reddy M, Sultana F, Kaur T, Chashoo G, Suri N, Sehar I, Wani ZA, Saxena A, Sharma PR, Bhushan S, Mondhe DM, Saxena AK. 2-Anilinonicotinyl linked 2-aminobenzothiazoles and [1,2,4]triazolo[1,5-b] [1,2,4]benzothiadiazine conjugates as potential mitochondrial apoptotic inducers. Bioorg Med Chem 2011;19:7136–50. doi: 10.1016/j.bmc.2011.09.06010.1016/j.bmc.2011.09.06022047801
Open DOI Search in Google Scholar Back to article
50. Kamal A, Hussaini SM, Nayak VL, Malik MS, Sucharitha ML, Shaik TB, Ashraf M, Bagul C. Synthesis of 2-anilinopyridine dimers as microtubule targeting and apoptosis inducing agents. Bioorg Med Chem 2014;22:6755–67. doi: 10.1016/j.bmc.2014.11.00110.1016/j.bmc.2014.11.00125468039
Open DOI Search in Google Scholar Back to article
51. Kamal A, Khan MN, Srinivasa Reddy K, Rohini K. Synthesis of a new class of 2-anilino substituted nicotinylarylsulfonylhydrazides as potential anticancer and antibacterial agents. Bioorg Med Chem 2007;15:1004–13. doi: 10.1016/j.bmc.2006.10.02710.1016/j.bmc.2006.10.02717097292
Open DOI Search in Google Scholar Back to article
52. Dorléans A, Gigant B, Ravelli RB, Mailliet P, Mikol V, Knossow M. Variations in the colchicine-binding domain provide insight into the structural switch of tubulin. Proc Natl Acad Sci USA 2009;106:13775–9. doi: 10.1073/pnas.090422310610.1073/pnas.0904223106272897019666559
Open DOI Search in Google Scholar Back to article
53. Elmeligie S, Khalil NA, Ahmed EM, Emam SH. New 3-substituted-2-(4-hydroxyanilino) pyridine derivatives, synthesis, antitumor activity and tubulin polymerization inhibition. Arch Pharm (Weinheim) 2017;350(2):e1600256. doi: 10.1002/ardp.20160025610.1002/ardp.20160025628150327
Search in Google Scholar Back to article
54. Liu YN, Wang JJ, Ji YT, Zhao GD, Tang LQ, Zhang CM, Guo XL, Liu ZP. Design, synthesis and biological evaluation of 1 methyl-1,4-dihydroindeno[1,2-c]pyrazole analogues as potential anticancer agents targeting tubulin colchicine binding site. J Med Chem 2016;59:5341–55. doi: 10.1021/acs.jmedchem.6b0007110.1021/acs.jmedchem.6b0007127172319
Open DOI Search in Google Scholar Back to article
55. Ali I, Haque A, Saleem K, Hsieh MF. Curcumin-I Knoevenagel’s condensates and their Schiff’s bases as anticancer agents: synthesis, pharmacological and simulation studies. Bioorg Med Chem 2013;21:3808–20. doi: 10.1016/j.bmc.2013.04.01810.1016/j.bmc.2013.04.01823643901
Open DOI Search in Google Scholar Back to article
56. Saleem K1, Wani WA, Haque A, Lone MN, Hsieh MF, Jairajpuri MA, Ali I. Synthesis, DNA binding, hemolysis assays and anticancer studies of copper(II), nickel(II) and iron(III) complexes of a pyrazoline-based ligand. Future Med Chem 2013;5:135–46. doi: 10.4155/fmc.12.20110.4155/fmc.12.20123360139
Open DOI Search in Google Scholar Back to article
57. Magalhaes LG, Marques FB, da Fonseca MB, Rogério KR, Graebin CS, Andricopulo AD. Discovery of a series of acridinones as mechanism-based tubulin assembly inhibitors with anticancer activity. Plos One 2016;11(8):e0160842. doi: 10.1371/journal.pone.016084210.1371/journal.pone.0160842498002827508497
Search in Google Scholar Back to article
58. Devambatla RK, Namjoshi OA, Choudhary S, Hamel E, Shaffer CV, Rohena CC, Mooberry SL, Gangjee A. Design, synthesis, and preclinical evaluation of 4 substituted-5-methyl-furo[2,3-d]pyrimidines as microtubule targeting agents that are effective against multidrug resistant cancer cells. J Med Chem 2016;59:5752–65. doi: 10.1021/acs.jmedchem.6b0023710.1021/acs.jmedchem.6b00237559010127213719
Open DOI Search in Google Scholar Back to article
59. Mollinedo F, Gajate C. Microtubules, microtubule-interfering agents and apoptosis. Apoptosis 2003;8:413–50. doi: 10.1023/A:102551310633010.1023/A:1025513106330
Search in Google Scholar Back to article
60. Zhou J, Giannakakou P. Targeting microtubules for cancer chemotherapy. Curr Med Chem Anticancer Agents 2005;5:65–71. doi: 10.2174/156801105335256910.2174/156801105335256915720262
Open DOI Search in Google Scholar Back to article
61. Schiff PB, Fant J, Horwitz SB. Promotion of microtubule assembly in vitro by taxol. Nature 1979;277:665–7. doi: 10.1016/j.ab.2006.10.01410.1016/j.ab.2006.10.014186841017097592
Open DOI Search in Google Scholar Back to article
62. Buey RM, Barasoain I, Jackson E, Meyer A, Giannakakou P, Paterson I, Mooberry S, Andreu JM, Díaz JF. Microtubule interactions with chemically diverse stabilizing agents, thermodynamics of binding to the paclitaxel site predicts cytotoxicity. Chem Biol 2005;12:1269–79. doi: 10.1016/j.chembiol.2005.09.0101635684410.1016/j.chembiol.2005.09.01016356844
Open DOI Search in Google Scholar Back to article
63. Kingston DGI, Jagtap PG, Yuan H, Samala L. The chemistry of taxol and related taxoids. In: Herz W, Falk H, Kirby GW, editors. Progress in the chemistry of organic natural products. Vol. 84. Wien: Springer; 2002. p. 53–225.10.1007/978-3-7091-6160-9_212132389
Search in Google Scholar Back to article
64. Wang Y, Wang J, Wang H, Ye W. Novel taxane derivatives from Taxus wallichiana with high anticancer potency on tumor cells. Chem Biol Drug Des 2016;88:556–61. doi: 10.1111/cbdd.1278210.1111/cbdd.127822715381327153813
Open DOI Search in Google Scholar Back to article
65. Barbier P, Tsvetkov PO, Breuzard G, Devred F. Deciphering the molecular mechanisms of anti-tubulin plant derived drugs. Phytochem Rev 2014;13:157–69. doi: 10.1007/s11101-013-9302-810.1007/s11101-013-9302-8
Open DOI Search in Google Scholar Back to article
66. Verma K, Kannan K, Shanthi V, Sethumadhavan R, Karthick V, Ramanathan K. Exploring β-tubulin inhibitors from plant origin using computational approach. Phytochem Anal 2017;28:230–41. doi: 10.1002/pca.266510.1002/pca.266528008675
Open DOI Search in Google Scholar Back to article
67. Busch T, Kirschning A. Recent advances in the total synthesis of pharmaceutically relevant diterpenes. Nat Prod Rep 2008;25:318–41. doi: 10.1039/b705652b10.1039/b705652b18389140
Open DOI Search in Google Scholar Back to article
68. Pfeffer TJ, Sasse F, Schmidt CF, Lakämper S, Kirschning A, Scholz T. The natural diterpenetonantzitlolone A its synthetic enantiomer inhibits cell proliferation and kinesin-5 function. Eur J Med Chem 2016;112:164–70. doi: 10.1016/j.ejmech.2016.02.02210.1016/j.ejmech.2016.02.02226896705
Open DOI Search in Google Scholar Back to article
69. Lee YJ, Lee YM, Lee CK, Jung JK, Han SB, Hong JT. Therapeutic applications of compounds in the Magnolia family. Pharmacol Ther 2011;130:157–76. doi: 10.1016/j.pharmthera.2011.01.01010.1016/j.pharmthera.2011.01.01021277893
Open DOI Search in Google Scholar Back to article
70. Hwang ES, Park KK. Magnolol suppresses metastasis via inhibition of invasion, migration, and matrix metalloproteinase-2/-9 activities in PC-3 human prostate carcinoma cells. Biosci Biotechnol Biochem 2010;74:961–7. doi: 10.1271/bbb.9078510.1271/bbb.9078520460721
Open DOI Search in Google Scholar Back to article
71. Kang YJ, Park HJ, Chung HJ, Min HY, Park EJ, Lee MA, Shin Y, Lee SK. Wnt/β-catenin signaling mediates the antitumor activity of magnolol in colorectal cancer cells. Mol Pharmacol 2012;82:168–77. doi: 10.1124/mol.112.07853510.1124/mol.112.07853522550094
Open DOI Search in Google Scholar Back to article
72. Li ML, Zhang F, Wang XA, Wu XS, Zhang BT, Zhang N, Wu WG, Wang Z, Weng H, Liu SB, Gao GF, Mu JS, Shu YJ, Bao RF, Cao Y, Lu JH, Gu J, Zhu J, Liu YB. Magnolol inhibits growth of gallbladder cancer cells through the p53 pathway. Cancer Sci 2015;106:1341–50. doi: 10.1111/cas.1276210.1111/cas.12762463801026250568
Open DOI Search in Google Scholar Back to article
73. Shen J, Ma H, Zhang T, Liu H, Yu L, Li G, Li H, Hu M. Magnolol inhibits the growth of non-small cell lung cancer via inhibiting microtubule polymerization. Cell Physiol Biochem 2017;42:1789–801. doi: 10.1159/00047945810.1159/00047945828746938
Open DOI Search in Google Scholar Back to article
74. Wu W-N, Beal JL, Doskotch RW. Alkaloids of thalictrum XXX. Eleven minor alkaloids from Thalictrum rugosum. J Nat Prod 1980;43:143–50. doi: 10.1021/np50007a01410.1021/np50007a014
Open DOI Search in Google Scholar Back to article
75. Levrier C, Rockstroh A, Gabrielli B, Kavallaris M, Lehman M, Davis RA, Sadowski MC, Nelson CC. Discovery of thalicthuberine as a novel antimitotic agent from nature that disrupts microtubule dynamics and induces apoptosis in prostate cancer cells. Cell Cycle 2018;17:652–68. doi: 10.1080/15384101.2017.135651210.1080/15384101.2017.1356512597620628749250
Open DOI Search in Google Scholar Back to article
76. Levrier C, Sadowski MC, Nelson CC, Davis RA. Cytotoxic C₂₀ diterpenoid alkaloids from the Australian endemic rainforest plant Anopterusmacleayanus. J Nat Prod 2015;78:2908–16. doi: 10.1021/acs.jnatprod.5b0050910.1021/acs.jnatprod.5b0050926600001
Open DOI Search in Google Scholar Back to article
77. Levrier C, Sadowski MC, Rockstroh A, Gabrielli B, Kavallaris M, Lehman M, Davis RA, Nelson CC. 6α-acetoxyanopterine, a novel structure class of mitotic inhibitor disrupting microtubule dynamics in prostate cancer cells. Mol Cancer Ther 2017;16:3–15. doi: 10.1158/1535-7163.MCT-16-032510.1158/1535-7163.MCT-16-032527760837
Open DOI Search in Google Scholar Back to article
78. Williams RB, Martin SM, Lawrence JA, Norman VL, O’Neil-Johnson M, Eldridge GR, Starks CM. Isolation and identification of the novel tubulin polymerization inhibitor bifidenone. J Nat Prod 2017;80:616–24. doi: 10.1021/acs.jnatprod.6b0089310.1021/acs.jnatprod.6b0089328335606
Open DOI Search in Google Scholar Back to article
79. Mukhtar E, Mustafa Adhami V, Mukhtar H. Targeting microtubules by natural agents for cancer therapy. Mol Cancer Ther 2014;13:275–84. doi: 10.1158/1535-7163.MCT-13-07912443544510.1158/1535-7163.MCT-13-0791394604824435445
Open DOI Search in Google Scholar Back to article
80. Soto E, Keizer RJ, Trocóniz IF, Huitema AD, Beijnen JH, Schellens JH, Wanders J, Cendrós JM, Obach R, Peraire C, Friberg LE, Karlsson MO. Predictive ability of a semi-mechanistic model for neutropenia in the development of novel anti-cancer agents: two case studies. Invest New Drugs 2011;29:984–95. doi: 10.1007/s10637-010-9437-z10.1007/s10637-010-9437-z316055720449627
Open DOI Search in Google Scholar Back to article
81. Cheng KL, Bradley T, Budman DR. Novel microtubule-targeting agents - the epothilones. Biologics 2008;2:789–811. PMCID: PMC272790010.2147/BTT.S3487272790019707459
Search in Google Scholar Back to article
82. Baas PW, Ahmad FJ. Beyond taxol: microtubule-based treatment of disease and injury of the nervous system. Brain 2013;136:2937–51. doi: 10.1093/brain/awt15310.1093//awt153
Open DOI Search in Google Scholar Back to article
83. Rowinsky EK, Donehower RC. Paclitaxel (taxol). N Engl J Med 1995;332:1004–14. doi: 10.1056/NEJM19950413332150710.1056/NEJM1995041333215077885406
Open DOI Search in Google Scholar Back to article
84. Lee JJ, Swain SM. Peripheral neuropathy induced by microtubule-stabilizing agents. J Clin Oncol 2006;24:1633–42. doi: 10.1200/JCO.2005.04.054310.1200/JCO.2005.04.054316575015
Open DOI Search in Google Scholar Back to article
85. Ying Z, Xin M, Guanhua D. Microtubule-stabilizing agents: New drug discovery and cancer therapy. Pharmacol Therap 2016;162:134–43. doi: 10.1016/j.pharmthera.2015.12.00610.1016/j.pharmthera.2015.12.00626706241
Open DOI Search in Google Scholar Back to article
86. Tarade D, Pandey S, McNulty J. Review of cytotoxic CA4 analogues that do not target microtubules, implications for CA4 development. Mini Rev Med Chem 2017;17:1507–14. doi: 10.2174/138955751566616050912582910.2174/138955751566616050912582927156516
Open DOI Search in Google Scholar Back to article
87. US National Library of Medicine (NLM). ClinicalTrials.gov [displayed 10 September 2019]. Available at https://clinicaltrials.gov/ct2/results?term=tubulin+inhibitors
Search in Google Scholar Back to article
88. de Lemos E, Porée FH, Bourin A, Barbion J, Agouridas E, Lannou MI, Commerçon A, Betzer JF, Pancrazi A, Ardisson J. Total synthesis of discodermolide, optimization of the effective synthetic route. Chemistry 2008;14:11092–112. doi: 10.1002/chem.2008014781897316210.1002/chem.20080147818973162
Open DOI Search in Google Scholar Back to article
89. Wender PA, Hegde SG, Hubbard RD, Zhang L. Total synthesis of (-)-laulimalide. J Am Chem Soc 2002;124:4956–7. doi: 10.1021/ja025842810.1021/ja025842811982349
Open DOI Search in Google Scholar Back to article
90. Moffat JG, Rudolph J, Bailey D. Phenotypic screening in cancer drug discovery - past, present and future. Nat Rev Drug Discov 2014;13:588–602. doi: 10.1038/nrd436610.1038/nrd43662503373625033736
Open DOI Search in Google Scholar Back to article
91. Cortes Cabrera A, Lucena-Agell D, Redondo-Horcajo M, Barasoain I, Díaz JF, Fasching B, Petrone PM. Aggregated compound biological signatures facilitate phenotypic drug discovery and target elucidation. ACS Chem Biol 2016;11:3024–34. doi: 10.1021/acschembio.6b0035810.1021/acschembio.6b0035827564241
Open DOI Search in Google Scholar Back to article

An overview of microtubule targeting agents for cancer therapy

Abstract

Paradigm

My account