The antihelmintic flubendazole inhibits microtubule function through a mechanism distinct from Vinca alkaloids and displays preclinical activity in leukemia and myeloma

Blood

Volumn 115, Issue 23, 2010, Pages 4824-4833

  Spagnuolo, Paul A ^a   Hu, Jiayi ^a   Hurren, Rose ^a   Wang, Xiaoming ^a   Gronda, Marcela ^a   Sukhai, Mahadeo A ^a   Di Meo, Ashley ^a   Boss, Jonathan ^a   Ashali, Iman ^a   Zavareh, Reza Beheshti ^a   Fine, Noah ^a   Simpson, Craig D ^a   Sharmeen, Sumaiya ^a   Rottapel, Rob ^a   Schimmer, Aaron D ^a  

^a PRINCESS MARGARET HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COLCHICINE; CYTARABINE; DAUNORUBICIN; FLUBENDAZOLE; GLYCOPROTEIN P; MEBENDAZOLE; OXIBENDAZOLE; TIABENDAZOLE; TUBULIN; VINBLASTINE; VINCRISTINE; ANTINEMATODAL AGENT; ANTINEOPLASTIC AGENT; DRUG DERIVATIVE; VINCA ALKALOID;

ACUTE MYELOBLASTIC LEUKEMIA; ANIMAL EXPERIMENT; ANTINEOPLASTIC ACTIVITY; AREA UNDER THE CURVE; ARTICLE; BINDING SITE; CANCER INHIBITION; CANCER RESISTANCE; CELL CYCLE ARREST; CELL VIABILITY; DRUG POTENTIATION; DRUG PROTEIN BINDING; GLUCOSE TRANSPORT; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA; MAXIMUM PLASMA CONCENTRATION; MICROTUBULE ASSEMBLY; MOUSE; MYELOMA; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CELL DEATH; CELL STRAIN U937; CELL SURVIVAL; DOSE RESPONSE; DRUG SCREENING; FEMALE; HELA CELL; MALE; METABOLISM; METHODOLOGY; MICROTUBULE; MULTIPLE MYELOMA;

ANIMALS; ANTINEMATODAL AGENTS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; CELL DEATH; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; FEMALE; HELA CELLS; HUMANS; LEUKEMIA; MALE; MEBENDAZOLE; MICE; MICROTUBULES; MULTIPLE MYELOMA; U937 CELLS; VINBLASTINE; VINCA ALKALOIDS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 77954741282     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-09-243055     Document Type: Article

References (50)

1. Vazquez-Martin A, Oliveras-Ferraros C, del Barco S, Martin-Castillo B, Menendez JA. The antidiabetic drug metformin: a pharmaceutical AMPK activator to overcome breast cancer resistance to HER2 inhibitors while decreasing risk of cardiomyopathy. Ann Oncol. 2009;20(3):592-595.
2. Ben Sahra I, Laurent K, Loubat A, et al. The antidiabetic drug metformin exerts an antitumoral effect in vitro and in vivo through a decrease of cyclin D1 level. Oncogene. 2008;27(25):3576-3586. (Pubitemid 351793803)
3. Li D, Yeung SC, Hassan MM, Konopleva M, Abbruzzese JL. Antidiabetic therapies affect risk of pancreatic cancer. Gastroenterology. 2009;137(2):482-488.
4. Cazzaniga M, Bonanni B, Guerrieri-Gonzaga A, Decensi A. Is it time to test metformin in breast cancer clinical trials? Cancer Epidemiol Biomarkers Prev. 2009;18(3):701-705.
5. Larkin M. Low-dose thalidomide seems to be effective in multiple myeloma. Lancet. 1999;354(9182):925.
6. Richardson PG, Mitsiades CS, Munshi NC, Anderson KC. Can thalidomide improve outcome in patients with multiple myeloma? Nat Clin Pract Oncol. 2006;3(11):590-591.
7. Feldmeier H, Bienzle U, Dohring E, Dietrich M. Flubendazole versus mebendazole in intestinal helminthic infections. Acta Trop. 1982;39(2):185-189. (Pubitemid 12055261)
8. Lassègue A, Estavoyer JM, Minazzi H, et al. Treatment of human alveolar echinococcosis with flubendazole: clinical, morphological and immunological study. Gastroenterol Clin Biol. 1984;8(4):314-320.
9. Téllez-Girón E, Ramos MC, Dufour L, et al. Treatment of neurocysticercosis with flubendazole. Am J Trop Med Hyg. 1984;33(4):627-631.
10. Fuchs R. Flubendazole. Vol 31. Geneva, Switzerland: World Health Organization; 1993.
11. Ceballos L, Elissondo M, Bruni SS, Denegri G, Alvarez L, Lanusse C. Flubendazole in cystic echinococcosis therapy: pharmaco-parasitological evaluation in mice. Parasitol Int. 2009;58(4):354-358.
12. Doudican N, Rodriguez A, Osman I, Orlow SJ. Mebendazole induces apoptosis via Bcl-2 inactivation in chemoresistant melanoma cells. Mol Cancer Res. 2008;6(8):1308-1315.
13. Gupta K, Bishop J, Peck A, Brown J, Wilson L, Panda D. Antimitotic antifungal compound benomyl inhibits brain microtubule polymerization and dynamics and cancer cell proliferation at mitosis, by binding to a novel site in tubulin. Biochemistry. 2004;43(21):6645-6655.
14. Cumino AC, Elissondo MC, Denegri GM. Flubendazole interferes with a wide spectrum of cell homeostatic mechanisms in Echinococcus granulosus protoscoleces. Parasitol Int. 2009;58(3):270-277.
15. Jasra N, Sanyal SN, Khera S. Effect of thiabendazole and fenbendazole on glucose uptake and carbohydrate metabolism in Trichuris globulosa. Vet Parasitol. 1990;35(3):201-209. (Pubitemid 20220214)
16. Lacey E, Watson TR. Activity of benzimidazole carbamates against L1210 mouse leukaemia cells: correlation with in vitro tubulin polymerization assay. Biochem Pharmacol. 1985;34(19):3603-3605.
17. Xu GW, Ali M, Wood TE, et al. The ubiquitin-activating enzyme E1 as a therapeutic target for the treatment of leukemia and multiple myeloma. Blood. 2010;115(11):2251-2259.
18. Mawji IA, Simpson CD, Hurren R, et al. Critical role for Fas-associated death domain-like interleukin-1-converting enzyme-like inhibitory protein in anoikis resistance and distant tumor formation. J Natl Cancer Inst. 2007;99(10):811-822.
19. Santra M, Santra S, Roberts C, Zhang RL, Chopp M. Doublecortin induces mitotic microtubule catastrophe and inhibits glioma cell invasion. J Neurochem. 2009;108(1):231-245.
20. Wood TE, Dalili S, Simpson CD, et al. A novel inhibitor of glucose uptake sensitizes cells to FAS-induced cell death. Mol Cancer Ther. 2008;7(11):3546-3555.
21. Beyer CF, Zhang N, Hernandez R, et al. TTI-237: a novel microtubule-active compound with in vivo antitumor activity. Cancer Res. 2008;68(7):2292-2300. (Pubitemid 351521803)
22. Roychowdhury M, Sarkar N, Manna T, et al. Sulfhydryls of tubulin: a probe to detect conformational changes of tubulin. Eur J Biochem. 2000;267(12):3469-3476.
23. Beheshti Zavareh R, Lau KS, Hurren R, et al. Inhibition of the sodium/potassium ATPase impairs N-glycan expression and function. Cancer Res. 2008;68(16):6688-6697.
24. Mao X, Li X, Sprangers R, et al. Clioquinol inhibits the proteasome and displays preclinical activity in leukemia and myeloma. Leukemia. 2009;23(3):585-590.
25. Grover VS, Sharma A, Singh M. Role of nitric oxide in diabetes-induced attenuation of antinociceptive effect of morphine in mice. Eur J Pharmacol. 2000;399(2):161-164. (Pubitemid 30407036)
26. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul. 1984;22:27-55.
27. Sharmeen S, Skrtic M, Sukhai M, et al. Activation of chloride channels with the anti-parasitic agent ivermectin induces membrane hyperpolarization and cell death in leukemia cells. American Society of Hematology, New Orleans, LA, December 7, 2009.
28. Jordan MA, Wilson L. Microtubules as a target for anticancer drugs. Nat Rev Cancer. 2004;4(4):253-265.
29. Sternlicht H, Ringel I. Colchicine inhibition of microtubule assembly via copolymer formation. J Biol Chem. 1979;254(20):10540-10550. (Pubitemid 10180993)
30. Manfredi JJ, Parness J, Horwitz SB. Taxol binds to cellular microtubules. J Cell Biol. 1982;94(3):688-696.
31. Risinger AL, Giles FJ, Mooberry SL. Microtubule dynamics as a target in oncology. Cancer Treat Rev. 2009;35(3):255-261.
32. Zelnak AB. Clinical pharmacology and use of microtubule-targeting agents in cancer therapy. Methods Mol Med. 2007;137:209-234.
33. Bhattacharyya B, Wolff J. Promotion of fluorescence upon binding of colchicine to tubulin. Proc Natl Acad Sci U S A. 1974;71(7):2627-2631.
34. Gao J, Huo L, Sun X, et al. The tumor suppressor CYLD regulates microtubule dynamics and plays a role in cell migration. J Biol Chem. 2008;283(14):8802-8809.
35. Jordan MA, Kamath K, Manna T, et al. The primary antimitotic mechanism of action of the synthetic halichondrin E7389 is suppression of microtubule growth. Mol Cancer Ther. 2005;4(7):1086-1095.
36. Loganzo F, Hari M, Annable T, et al. Cells resistant to HTI-286 do not overexpress P-glycoprotein but have reduced drug accumulation and a point mutation in alpha-tubulin. Mol Cancer Ther. 2004;3(10):1319-1327.
37. He L, Yang CP, Horwitz SB. Mutations in beta-tubulin map to domains involved in regulation of microtubule stability in epothilone-resistant cell lines. Mol Cancer Ther. 2001;1(1):3-10.
38. Dumontet C, Sikic BI. Mechanisms of action of and resistance to antitubulin agents: microtubule dynamics, drug transport, and cell death. J Clin Oncol. 1999;17(3):1061-1070. (Pubitemid 29109340)
39. Huang TH, Bebawy M, Tran VH, Roufogalis BD. Specific reversal of multidrug resistance to colchicine in CEM/VLB(100) cells by Gynostemma pentaphyllum extract. Phytomedicine. 2007;14(12):830-839.
40. Chou TC. Preclinical versus clinical drug combination studies. Leuk Lymphoma. 2008;49(11):2059-2080.
41. Moreno L, Alvarez L, Mottier L, Virkel G, Bruni SS, Lanusse C. Integrated pharmacological assessment of flubendazole potential for use in sheep: disposition kinetics, liver metabolism and parasite diffusion ability. J Vet Pharmacol Ther. 2004;27(5):299-308.
42. Castro N, Marquez-Caraveo C, Brundage RC, et al. Population pharmacokinetics of albendazole in patients with neurocysticercosis. Int J Clin Pharmacol Ther. 2009;47(11):679-685.
43. Singer CR, Linch DC. Comparison of the sensitivity of normal and leukaemic myeloid progenitors to in-vitro incubation with cytotoxic drugs: a study of pharmacological purging. Leuk Res. 1987;11(11):953-959.
44. Spiro TE, Socquet M, Delforge A, Stryckmans P. Chemotherapeutic sensitivity of normal and leukemic hematopoietic progenitor cells to N-[4-(9-acridinylamino)-3-methoxyphenyl]-methanesulfonamide, a new anticancer agent. J Natl Cancer Inst. 1981;66(4):615-618. (Pubitemid 11101028)
45. Cardinali G, Cardinali G, Enein MA. Studies on the antimitotic activity of leurocristine (Vincristine). Blood. 1963;21(1):102-110.
46. Coltman CA Jr, Bodey GP, Hewlett JS, et al. Chemotherapy of acute leukemia: a comparison of vincristine, cytarabine, and prednisone alone and in combination with cyclophosphamide or daunorubicin. Arch Intern Med. 1978;138(9):1342-1348.
47. Curtis JE, Cowan DH, Bergsagel DE, Hasselback R, McCulloch EA. Acute leukemia in adults: assessment of remission induction with combination chemotherapy by clinical and cell-culture criteria. Can Med Assoc J. 1975;113(4):289-294.
48. Morris DL, Jourdan JL, Pourgholami MH. Pilot study of albendazole in patients with advanced malignancy: effect on serum tumor markers/high incidence of neutropenia. Oncology. 2001;61(1):42-46.
49. Westermann S, Weber K. Post-translational modifications regulate microtubule function. Nat Rev Mol Cell Biol. 2003;4(12):938-947. (Pubitemid 37493642)
50. Ireland CM, Gull K, Gutteridge WE, Pogson CI. The interaction of benzimidazole carbamates with mammalian microtobule protein. Biochem Pharmacol. 1979;28(17):2680-2682. (Pubitemid 10229291)