Inhibitors of microtubule polymerization- new natural compounds as potential anti-cancer drugs

COMMENTARY ON THE LAW

Inhibitors of microtubule polymerization- new natural compounds as potential anti-cancer drugs

Aneta Rogalska 1 , Klaudia Miśkiewicz 1 , Agnieszka Marczak 1

1. Katedra Termobiologii, Instytut Biofizyki, Wydział Biologii i Ochrony Środowiska, Uniwersytet Łódzki

Published: 2015-05-04
GICID: 01.3001.0009.6532
Available language versions: en pl
Issue: Postepy Hig Med Dosw 2015; 69 : 571-585

 

Abstract

Inhibitors of microtubule polymerization are compounds which, by binding to the tubulin dimer, prevent the normal course of cell division and lead to cell death. They cause inhibition of mitosis, affect the cytoskeleton and disrupt the process of angiogenesis. Inhibitors of microtubule polymerization include natural substances, synthetic and semi-synthetic analogs. They contain a group of compounds having the ability to bind to the vinca alkaloid and colchicine domain of β-tubulin. Among them are vinca alkaloids, dolastatins and halichondrins, which connect to the vinca alkaloids domain, and combretastatins binding the colchicine site of protein. Tumor cells have greater capacity for cell proliferation and are also more susceptible to damage by microtubule inhibitors. Their action has been widely used in cancer therapy.

References

  • 1. Akashi Y., Okamoto I., Suzuki M., Tamura K., Iwasa T., Hisada S.,Satoh T., Nakagawa K., Ono K., Fukuoka M.: The novel microtubule–interfering agent TZT-1027 enhances the anticancer effect of radiationin vitro and in vivo. Br. J. Cancer, 2007; 96: 1532-1539
    Google Scholar
  • 2. Bachner M., De Santis M.: Vinflunine in the treatment of bladdercancer. Ther. Clin. Risk Manag., 2008; 4: 1243-1253
    Google Scholar
  • 3. Bai R., Edler M.C., Bonate P.L., Copeland T.D., Pettit G.R., LudueñaR.F., Hamel E.: Intracellular activation and deactivation of tasidotin,an analog of dolastatin 15: correlation with cytotoxicity. Mol. Pharmacol,2009; 75: 218-226
    Google Scholar
  • 4. Bai R., Nguyen T.L., Burnett J.C., Atasoylu O., Munro M.H., PettitG.R., Smith A.B.III, Gussio R., Hamel E.: Interactions of halichondrinB and eribulin with tubulin. J. Chem. Inf. Model., 2011; 51: 1393-1404
    Google Scholar
  • 5. Bhattacharyya B., Panda D., Gupta S., Banerjee M.: Anti-mitoticactivity of colchicine and the structural basis for its interaction withtubulin. Med. Res. Rev., 2008; 28: 155-183
    Google Scholar
  • 6. Cai S.X.: Small molecule vascular disrupting agents: potentialnew drugs for cancer treatment. Recent Pat. Anticancer Drug Discov.,2007; 2: 79-101
    Google Scholar
  • 7. Carr M., Greene L.M., Knox A.J., Lloyd D.G., Zisterer D.M., MeeganM.J.: Lead identification of conformationally restricted β-lactam typecombretastatin analogues: synthesis, antiproliferative activity andtubulin targeting effects. Eur. J. Med. Chem., 2010; 45: 5752-5766
    Google Scholar
  • 8. Chaplin D.J., Jelinek C., Pettit G.R., Edvardsen K., Pinney K.G.:The Discovery and Development of the Combretastatins. CRC Press,LLC 2005
    Google Scholar
  • 9. Checchi P.M., Nettles J.H., Zhou J., Snyder J.P., Joshi H.C.: Microtubule-interactingdrugs for cancer treatment. Trends Pharmacol.Sci., 2003; 24: 361-365
    Google Scholar
  • 10. Ciulla T.A.: Opening new fronts in the battle against AMD. Nutritionand pharmacology are two key areas of study in the evolving effortto beat age-related macular degeneration. http://www.reviewofophthalmology.com/content/d/retinal_insider/i/1293/c/24902/
    Google Scholar
  • 11. Cunningham C., Appleman L.J., Kirvan-Visovatti M., Ryan D.P.,Regan E., Vukelja S., Bonate P.L., Ruvuna F., Fram R.J., Jekunen A.,Weitman S., Hammond L.A., Eder J.P. Jr.: Phase I and pharmacokineticstudy of the dolastatin-15 analogue tasidotin (ILX651) administeredintravenously on days 1, 3, and 5 every 3 weeks in patientswith advanced solid tumors. Clin. Cancer Res., 2005; 11: 7825-7833
    Google Scholar
  • 12. Dark G.G., Hill S.A., Prise V.E., Tozer G.M., Pettit G.R., ChaplinD.J.: Combretastatin A-4, an agent that displays potent and selectivetoxicity toward tumor vasculature. Cancer Res., 1997; 57: 1829-1834
    Google Scholar
  • 13. Dorleans A., Gigant B., Ravelli R.B., Mailliet P., Mikol V., KnossowM.: Variations in the colchicine-binding domain provide insightinto the structural switch of tubulin. Proc. Natl. Acad. Sci. USA,2009; 106: 13775-13779
    Google Scholar
  • 14. Downing K.H., Nogales E.: Crystallographic structure of tubulin:implications for dynamics and drug binding. Cell Struct. Funct.,1999; 24: 269-275
    Google Scholar
  • 15. English D.P., Roque D.M., Santin A.D.: Class III b-tubulin overexpressionin gynecologic tumors: implications for the choice ofmicrotubule targeted agents? Expert Rev. Anticancer Ther., 2013;13: 63-74
    Google Scholar
  • 16. Fahy J., Hellier P., Breillout F., Bailly C.: Vinflunine: discoveryand synthesis of a novel microtubule inhibitor. Semin. Oncol.,2008; 35: S3-S5
    Google Scholar
  • 17. Faller B.A., Pandit T.N.: Safety and efficacy of vinorelbine in thetreatment of non-small cell lung cancer. Clin. Med. Insights Oncol.,2011; 5: 131-144
    Google Scholar
  • 18. Farnsworth N.R.: Screening plants for new medicines. Biodiversity,1988; 9: 83-97
    Google Scholar
  • 19. Galano G., Caputo M., Tecce M.F., Capasso A.: Efficacy and tolerabilityof vinorelbine in the cancer therapy. Curr. Drug Saf., 2011; 6: 185-193
    Google Scholar
  • 20. Giraud A., Provot O., Hamzé A., Brion J.D., Alami M.: One-pothydrosilylation–protodesilylation of functionalized diarylalkynes:a highly selective access to Z-stilbenes. Application to the synthesisof combretastatin A-4. Tetrahedron Lett., 2008; 49: 1107-1110
    Google Scholar
  • 21. González Pérez P., Serrano-Pozo A., Franco-Macías E., Montes–Latorre E., Gómez-Aranda F., Campos T.: Vincristine-induced acuteneurotoxicity versus Guillain-Barré syndrome: a diagnostic dilemma.Eur. J. Neurol., 2007; 14: 826-828
    Google Scholar
  • 22. Greene L.M., Nathwani S.M., Bright S.A., Fayne D., Croke A., GagliardiM., McElligott A.M., O’Connor L., Carr M., Keely N.O., O’BoyleN.M., Carroll P., Sarkadi B., Conneally E., Lloyd D.G., Lawler M., MeeganM.J., Zisterer D.M.: The vascular targeting agent combretastatin-A4and a novel cis-restricted β-lactam analogue, CA-432, induceapoptosis in human chronic myeloid leukemia cells and ex vivopatient samples including those displaying multidrug resistance. J.Pharmacol. Exp. Ther., 2010; 335: 302-313
    Google Scholar
  • 23. Greystoke A., Blagden S., Thomas A.L., Scott E., Attard G., MolifeR., Vidal L., Pacey S., Sarkar D., Jenner A., De-Bono J.S., StewardW.: A phase I study of intravenous TZT-1027 administered on day 1and day 8 of a three-weekly cycle in combination with carboplatingiven on day 1 alone in patients with advanced solid tumours. Ann.Oncol., 2006; 17: 1313-1319
    Google Scholar
  • 24. Hayashi Y., Yamazaki-Nakamura Y., Yakushiji F.: Medicinal chemistryand chemical biology of diketopiperazine-type antimicrotubuleand vascular-disrupting agents. Chem. Pharm. Bull., 2013; 61: 889-901
    Google Scholar
  • 25. Hori K., Saito S.: Induction of tumour blood flow stasis and necrosis:a new function for epinephrine similar to that of combretastatinA-4 derivative AVE8062 (AC7700). Br. J. Cancer, 2004; 90: 549-553
    Google Scholar
  • 26. Hu Y., Lu X., Chen K., Yan R., Li Q.S., Zhu H.L.: Design, synthesis,biological evaluation and molecular modeling of 1,3,4-oxadiazolineanalogs of combretastatin-A4 as novel antitubulin agents. Bioorg.Med. Chem., 2012; 20: 903-909
    Google Scholar
  • 27. Ishikawa H., Colby D.A., Seto S., Va P., Tam A., Kakei H., Rayl T.J.,Hwang I., Boger D.L.: Total synthesis of vinblastine, vincristine, relatednatural products, and key structural analogues. J. Am. Chem.Soc., 2009; 131: 4904-4916
    Google Scholar
  • 28. Jacquesy J.C., Jouannetaud M.P.: La vinflunine, nouvel agentanticancéreux fluoré dérivé des alcaloïdes de Vinca. Ann. Pharm.Fr., 2005; 63: 28-34
    Google Scholar
  • 29. Jagetia G.C., Krishnamurthy H., Jyothi P.: Evaluation of cytotoxiceffects of different doses of vinblastine on mouse spermatogenesisby flow cytometry. Toxicology, 1996; 112: 227-236
    Google Scholar
  • 30. Jain S., Cigler T.: Eribulin mesylate in the treatment of metastaticbreast cancer. Biologics, 2012; 6: 21-29
    Google Scholar
  • 31. Johnson P.D., Sohn J.H., Rawal V.H.: Synthesis of C-15 vindolineanalogues by palladium-catalyzed cross-coupling reactions.J. Org. Chem., 2006; 71: 7899-7902
    Google Scholar
  • 32. Jurczyszyn A., Wolska-Smoleń T., Skotnicki A.B.: Znaczenieangiogenezy w prawidłowej i nowotworowej hematopoezie. Adv.Clin. Exp. Med., 2003; 12: 489-496
    Google Scholar
  • 33. Kambhampati S., Rajewski R.A., Tanol M., Haque I., Das A.,Banerjee S., Jha S., Burns D., Borrego-Diaz E., Van Veldhuizen P.J.,Banerjee S.K.: A second-generation 2-Methoxyestradiol prodrugis effective against Barrett’s adenocarcinoma in a mouse xenograftmodel. Mol. Cancer Ther., 2013; 12: 255-263
    Google Scholar
  • 34. Kanakkanthara A., Teesdale-Spittle P.H., Miller J.H.: Cytoskeletalalterations that confer resistance to anti-tubulin chemotherapeutics.Anticancer Agents Med. Chem., 2013; 13: 147-158
    Google Scholar
  • 35. Kelly E.B., Tuszynski J.A., Klobukowski M.: QM and QM/MD simulationsof the Vinca alkaloids docked to tubulin. J. Mol. Graph.Model, 2011; 30: 54-66
    Google Scholar
  • 36. Kim T.J., Ravoori M., Landen C.N., Kamat A.A., Han L.Y., LuC., Lin Y.G., Merritt W.M., Jennings N., Spannuth W.A., Langley R.,Gershenson D.M., Coleman R.L., Kundra V., Sood A.K.: Antitumorand antivascular effects of AVE8062 in ovarian carcinoma. CancerRes., 2007; 67: 9337-9345
    Google Scholar
  • 37. Kingston D.G.: Tubulin-interactive natural products as anticanceragents. J. Nat. Prod., 2009; 72: 507-515
    Google Scholar
  • 38. Kuboyama T., Yokoshima S., Tokuyama H., Fukuyama T.: Stereocontrolledtotal synthesis of (+)-vincristine. Proc. Natl. Acad.Sci. USA, 2004; 101: 11966-11970
    Google Scholar
  • 39. Lim K.H., Hiraku O., Komiyama K., Kam T.S.: Jerantinines A-G,cytotoxic aspidosperma alkaloids from Tabernaemontana corymbosa.J. Nat. Prod., 2008; 71: 1591-1594
    Google Scholar
  • 40. Lu Y., Chen J., Xiao M., Li W, Miller D.D.: An overview of tubulininhibitors that interact with the colchicine binding site.Pharm. Res., 2012; 29: 2943-2971
    Google Scholar
  • 41. Madlambayan G.J., Meacham A.M., Hosaka K., Mir S., JorgensenM., Scott E.W., Siemann D.W., Cogle C.R.: Leukemia regressionby vascular disruption and antiangiogenic therapy. Blood, 2010;116: 1539-1547
    Google Scholar
  • 42. Mollinedo F., Gajate C.: Microtubules, microtubule-interferingagents and apoptosis. Apoptosis, 2003; 8: 413-450
    Google Scholar
  • 43. Moudi M., Go R., Yien C.Y., Nazre M.: Vinca alkaloids. Int. J.Prev. Med., 2013; 4: 1231-1235
    Google Scholar
  • 44. Mutschler E., Geisslinger G., Kroemer H.K., Ruth P., Schaefer-KortingM.: Farmakologia i toksykologia. Med. Pharm., 2009
    Google Scholar
  • 45. Nabha S.M., Mohammad R.M., Dandashi M.H., Coupaye-GerardB., Aboukameel A., Pettit G.R., Al-Katib A.M.: Combretastatin-A4prodrug induces mitotic catastrophe in chronic lymphocytic leukemiacell line independent of caspase activation and poly(ADP–ribose) polymerase cleavage. Clin. Cancer Res., 2002; 8: 2735-2741
    Google Scholar
  • 46. Ngan V.K., Bellman K., Panda D., Hill B.T., Jordan M.A., WilsonL.: Novel actions of the antitumor drugs vinflunine and vinorelbineon microtubules. Cancer Res., 2000; 60: 5045-5051
    Google Scholar
  • 47. Nowak A.K., Brown C., Millward M.J., Creaney J., Byrne M.J.,Hughes B., Kremmidiotis G., Bibby D.C., Leske A.F., Mitchell P.L.,Pavlakis N., Boyer M., Stockler M.R.: A phase II clinical trial of thevascular disrupting agent BNC105P as second line chemotherapyfor advanced Malignant Pleural Mesothelioma. Lung Cancer,2013; 81: 422-427
    Google Scholar
  • 48. Oostendorp R.L., Witteveen P.O., Schwartz B., Vainchtein L.D.,Schot M., Nol A., Rosing H., Beijnen J.H., Voest E.E., Schellens J.H.:Dose-finding and pharmacokinetic study of orally administeredindibulin (D-24851) to patients with advanced solid tumors. Invest.New Drugs, 2010; 28: 163-170
    Google Scholar
  • 49. Pan L., Chai H., Kinghorn A.D.: The continuing search for antitumoragents from higher plants. Phytochem. Lett., 2010; 3: 1-8
    Google Scholar
  • 50. Pérez-Melero C., Maya A.B., del Rey B., Peláez R., Caballero E.,Medarde M.: A new family of quinoline and quinoxaline analoguesof combretastatins. Bioorg. Med. Chem. Lett., 2004; 14: 3771-3774
    Google Scholar
  • 51. Pettit G.R., Rhodes M.R., Herald D.L., Hamel E., Schmidt J.M.,Pettit R.K.: Antineoplastic agents. 445. Synthesis and evaluationof structural modifications of (Z)- and (E)-Combretastatin A-4. J.Med. Chem., 2005; 48: 4087-4099
    Google Scholar
  • 52. Raja V.J., Lim K.H., Leong C.O., Kam T.S., Bradshaw T.D.: Novelantitumour indole alkaloid, Jerantinine A, evokes potent G2/Mcell cycle arrest targeting microtubules. Invest. New Drugs. 2014;32: 838-850
    Google Scholar
  • 53. Ramnath N., Schwartz G.N., Smith P., Bong D., Kanter P.,Berdzik J., Creaven P.J.: Phase I and pharmacokinetic study ofanhydrovinblastine every 3 weeks in patients with refractorysolid tumors. Cancer Chemother. Pharmacol., 2003; 51: 227-230
    Google Scholar
  • 54. Ray A., Okouneva T., Manna T., Miller H.P., Schmid S., ArthaudL., Luduena R., Jordan M.A., Wilson L.: Mechanism of action ofthe microtubule-targeted antimitotic depsipeptide tasidotin (formerlyILX651) and its major metabolite tasidotin C-carboxylate.Cancer Res., 2007; 8: 3767-3776
    Google Scholar
  • 55. Rice L., Pampo C., Lepler S., Rojiani A.M., Siemann D.W.: Supportof a free radical mechanism for enhanced antitumor efficacyof the microtubule disruptor OXi4503. Microvasc Res., 2011;81: 44-51
    Google Scholar
  • 56. Rischin D., Bibby D.C., Chong G., Kremmidiotis G., Leske A.F.,Matthews C.A., Wong S.S., Rosen M.A., Desai J.: Clinical, pharmacodynamic,and pharmacokinetic evaluation of BNC105P: a phaseI trial of a novel vascular disrupting agent and inhibitor of cancercell proliferation. Clin. Cancer Res. 2011; 17: 5152-5160
    Google Scholar
  • 57. Risinger A.L., Giles F.J., Mooberry S.L.: Microtubule dynamicsas a target in oncology. Cancer Treat. Rev., 2009; 35: 255-261
    Google Scholar
  • 58. Robinson R.: Zybrestat could help thyroid cancer patients tolive longer. Belle News, Science-tech, 2011
    Google Scholar
  • 59. Roepke J., Salim V., Wu M., Thamm A.M., Murata J., Ploss K.,Boland W., De Luca V.: Vinca drug components accumulate exclusivelyin leaf exudates of Madagascar periwinkle. Proc. Natl.Acad. Sci. USA, 2010; 107: 15287-15292
    Google Scholar
  • 60. Rogalska A., Szula E., Marczak A.: Novel agents stabilizingmicrotubule (MSA) from marine organisms – the future of chemotherapy.Probl. Ter. Monitorowanej, 2011; 22: 63-76
    Google Scholar
  • 61. Roubille F., Kritikou E., Busseuil D., Barrere-Lemaire S., TardifJ.C.: Colchicine: an old wine in a new bottle? Antiinflamm.Antiallergy Agents Med. Chem., 2013; 12: 14-23
    Google Scholar
  • 62. Sato M., Sagawa M., Nakazato T., Ikeda Y., Kizaki M.: A naturalpeptide, dolastatin 15, induces G2/M cell cycle arrest andapoptosis of human multiple myeloma cells. Int. J. Oncol., 2007;30: 1453-1459
    Google Scholar
  • 63. Ścibior-Bentkowska D., Czeczot H.: Komórki nowotworowea stres oksydacyjny. Postępy Hig. Med. Dośw., 2009; 63: 58-72
    Google Scholar
  • 64. Seve P., Dumontet C.: Is class III β-tubulin a predictive factorin patients receiving tubulin binding agents? Lancet Oncol.,2008; 9: 168-175
    Google Scholar
  • 65. Shen C.H., Shee J.J., Wu J.Y., Lin Y.W., Wu J.D., Liu Y.W.: CombretastatinA-4 inhibits cell growth and metastasis in bladdercancer cells and retards tumour growth in a murine orthotopicbladder tumour model. Br. J. Pharmacol., 2010; 160: 2008-2027
    Google Scholar
  • 66. Siemann D.W., Mercer E., Lepler S., Rojiani A.M.: Vasculartargeting agents enhance chemotherapeutic agent activities insolid tumor therapy. Int. J. Cancer, 2002; 99: 1-6
    Google Scholar
  • 67. Simmons T.L., Andrianasolo E., McPhail K., Flatt P., GerwickW.H.: Marine natural products as anticancer drugs. Mol. CancerTher., 2005; 4: 333-342
    Google Scholar
  • 68. Smith N.F., Mani S., Schuetz E.G., Yasuda K., Sissung T.M.,Bates S.E., Figg W.D., Sparreboom A.: Induction of CYP3A4 by vinblastine:role of the nuclear receptor NR1I2. Ann. Pharmacother.,2010; 44: 1709-1717
    Google Scholar
  • 69. Stanton R.A., Gernert K.M., Nettles J.H., Aneja R.: Drugs thattarget dynamic microtubules: a new molecular perspective. Med.Res. Rev., 2011; 31: 443-481
    Google Scholar
  • 70. Stengel C., Newman S.P., Leese M.P., Potter B.V., Reed M.J.,Purohit A.: Class III β-tubulin expression and in vitro resistanceto microtubule targeting agents. Br. J. Cancer, 2010; 102: 316-324
    Google Scholar
  • 71. Szczepański M., Grzanka A., Izdebska M.: Mikrotubule – celterapii przeciwnowotworowej. J. Oncol., 2007; 57: 579-585
    Google Scholar
  • 72. Tarlaci S.: Vincristine-induced fatal neuropathy in non-Hodgkin’slymphoma. Neurotoxicology, 2008; 29: 748-749
    Google Scholar
  • 73. Thorpe P.E.: Vascular targeting agents as cancer therapeutics.Clin. Cancer Res., 2004; 10: 415-427
    Google Scholar
  • 74. Toso R.J, Jordan M.A., Farrell K.W., Matsumoto B., Wilson L.:Kinetic stabilization of microtubule dynamic instability in vitroby vinblastine. Biochemistry, 1993; 32: 1285-1293
    Google Scholar
  • 75. Towle M.J., Salvato K.A., Budrow J., Wels B.F., Kuznetsov G.,Aalfs K.K., Welsh S., Zheng W., Seletsky B.M., Palme M.H., HabgoodG.J., Singer L.A., Dipietro L.V., Wang Y., Chen J.J. i wsp.: In vitroand in vivo anticancer activities of synthetic macrocyclic ketoneanalogues of halichondrin B. Cancer Res., 2001; 61: 1013-1021
    Google Scholar
  • 76. Vaishampayan U., Glode M., Du W., Kraft A., Hudes G., WrightJ., Hussain M.: Phase II study of dolastatin-10 in patients withhormone-refractory metastatic prostate adenocarcinoma. Clin.Cancer Res., 2000; 6: 4205-4208
    Google Scholar
  • 77. Vici P., Colucci G., Giotta F., Sergi D., Filippelli G., Perri P.,Botti C., Vizza E., Carpino A., Pizzuti L., Latorre A., GiannarelliD., Lopez M., Di Lauro L.: A multicenter prospective phase II randomizedtrial of epirubicin/vinorelbine versus pegylated liposomaldoxorubicin/vinorelbine as first-line treatment in advancedbreast cancer. A GOIM study. J. Exp. Clin. Cancer Res., 2011; 30: 39
    Google Scholar
  • 78. Voss M.E., Ralph J.M., Xie D., Manning D.D., Chen X., FrankA.J., Leyhane A.J., Liu L., Stevens J.M., Budde C., Surman M.D.,Friedrich T., Peace D., Scott I.L., Wolf M., Johnson R.: Synthesisand SAR of vinca alkaloid analogues. Bioorg. Med. Chem. Lett.,2009; 19: 1245-1249
    Google Scholar
  • 79. Wen X., Wu J., Wang F., Liu B., Huang C., Wei Y.: Deconvolutingthe role of reactive oxygen species and autophagy in humandiseases. Free Radic. Biol. Med., 2013; 65: 402-410
    Google Scholar
  • 80. Woyke T., Pettit G.R., Winkelmann G., Pettit R.K.: In vitroactivities and postantifungal effects of the potent dolastatin 10derivative auristatin PHE. Antimicrob. Agents Chemother., 2001;45: 3580-3584
    Google Scholar
  • 81. Yamamoto N., Andoh M., Kawahara M., Fukuoka M., NiitaniH.: Phase I study of TZT-1027, a novel synthetic dolastatin 10derivative and inhibitor of tubulin polymerization, given weeklyto advanced solid tumor patients for 3 weeks. Cancer Sci., 2009;100: 316-321
    Google Scholar

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