β-tubulin mutations are associated with resistance to 2-methoxyestradiol in MDA-MB-435 cancer cells

Cancer Research

Volumn 65, Issue 20, 2005, Pages 9406-9414

  Gökmen Polar, Yesina ^a,f   Escuin, Daniel ^c,d   Walls, Chad D ^b   Soule, Sharon E ^a   Wang, Yuefang ^c   Sanders, Kerry L ^a   LaVallee, Theresa M ^e   Wang, Mu ^a,b   Guenther, Brian D ^a   Giannakakou, Paraskevi ^c   Sledge Jr , George W ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Indiana Centers for Applied Protein Sciences   (United States)

^c EMORY UNIVERSITY   (United States)

^d HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

^e ENTREMED INC   (United States)

^f INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 METHOXYESTRADIOL; ANTINEOPLASTIC AGENT; ASPARAGINE; ASPARTIC ACID; AVE 8062A; BETA TUBULIN; COLCHICINE; DEMECOLCINE; EPOTHILONE B; LYSINE; NAVELBINE; PACLITAXEL; TYROSINE; UNCLASSIFIED DRUG; VINBLASTINE; VINCA ALKALOID; VINCRISTINE;

ACETYLATION; ARTICLE; CANCER; CANCER CELL CULTURE; CONTROLLED STUDY; CROSS RESISTANCE; CULTURE MEDIUM; DEPOLYMERIZATION; DRUG EFFECT; GENE SEQUENCE; HETEROZYGOSITY; HUMAN; HUMAN CELL; IC 50; MICROTUBULE; POINT MUTATION; PRIORITY JOURNAL; SEQUENCE ANALYSIS; TANDEM MASS SPECTROMETRY;

AMINO ACID SEQUENCE; BREAST NEOPLASMS; CELL LINE, TUMOR; DNA, NEOPLASM; DRUG RESISTANCE, NEOPLASM; ESTRADIOL; HUMANS; MASS SPECTROMETRY; MICROTUBULES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POINT MUTATION; PROTEIN ISOFORMS; STRUCTURE-ACTIVITY RELATIONSHIP; TUBULIN; TUBULIN MODULATORS;

EID: 27144486110     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-05-0088     Document Type: Article

References (44)

1. Pribluda VS, Gubish ER, LaVallee TM, Treston A, Swartz GM, Green SJ. 2-Methoxyestradiol: an endogenous antiangiogenic and antiproliferative drug candidate. Cancer Metastasis Rev 2000;19:173-9.
2. Mooberry SL. New insights into 2-methoxyestradiol, a promising antiangiogenic and antitumor agent. Curr Opin Oncol 2003;15:425-30.
3. Lakhani NJ, Sarkar MA, Venitz J, Figg WD. 2-Methoxyestradiol, a promising anticancer agent Pharmacotherapy 2003;23:165-72.
4. LaVallee TM, Zhan XH, Herbstritt CJ, Rough EC, Green SJ, Pribluda VS. 2-Methoxyestradiol inhibits proliferation and induces apoptosis independently of estrogen receptors α and β. Cancer Res 2002;62:3691-7.
5. D'Amato RJ, Lin CM, Flynn E, Folkman J, Hamel E. 2-Methoxyestradiol, an endogenous mammalian metabolite, inhibits tubulin polymerization by interacting at the colchicine site. Proc Natl Acad Sci U S A 1994;91:3964-8.
6. Cushman M, He HM, Katzenellenbogen JA, Lin CM, Hamel E. Synthesis, antitubulin and antimitotic activity, and cytotoxicity of analogs of 2-methoxyestradiol, an endogenous mammalian metabolite of estradiol that inhibits tubulin polymerization by binding to the colchicine binding site. J Med Chem 1995;38:2041-9.
7. Lottering ML, de Kock M, Viljoen TC, Grobler CJ, Seegers JC. 17β-Estradiol metabolites affect some regulators of the MCF-7 cell cycle. Cancer Lett 1996;110:181-6.
8. Zoubine MN, Weston AP, Johnson DC, Campbell DR, Banerjee SK, 2-Methoxyestradiol-induced growth suppression and lethality in estrogen-responsive MCF-7 cells may be mediated by downregulation of p34cdc2 and cyclin B1 expression. Int J Oncol 1999;15:639-46.
9. Attalla H, Mäkelä TP, Adlercreutz H, Andersson LC. 2-Methoxyestradiol arrests cells in mitosis without depolymerizing tubulin. Biochem Biophys Res Commun 1996;228:467-73.
10. Huang P, Feng L, Oldham EA, Keating MJ, Plunkett W. Superoxide dismutase as a target for the selective killing of cancer cells. Nature 2000;407:390-5.
11. Kachadourian R, Liochev SI, Cabelli DE, Patel MN, Fridovich I, Day BJ. 2-Methoxyestradiol does not inhibit superoxide dismutase. Arch Biochem Biophys 2001;392:349-53.
12. Mukhopadhyay T, Roth JA. Induction of apoptosis in human lung cancer cells after wild-type p53 activation by methoxyestradiol. Oncogene 1997;14:379-84.
13. Seegers JC, Lottering ML, Grobler CJ, et al. The mammalian metabolite, 2-methoxyestradiol, affects p53 levels and apoptosis induction in transformed cells but not in normal cells. J Steroid Biochem Mol Biol 1997;62:253-67.
14. LaVallee TM, Zhan XH, Johnson MS, et al. 2-Methoxyestradiol up-regulates death receptor 5 and induces apoptosis through activation of the extrinsic pathway. Cancer Res 2003;63:468-75.
15. Mabjeesh NJ, Escuin D, LaVallee TM, et al. 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF. Cancer Cell 2003;3:363-75.
16. Jordan MA, Wilson L. Microtubules as a target for anticancer drugs. Nat Rev Cancer 2004;4:253-65.
17. Gigant B, Wang C, Ravelli RB, et al. Structural basis for the regulation of tubulin by vinblastine. Nature 2005;435:519-22.
18. Drukman S, Kavallaris M. Microtubule alterations and resistance to tubulin-binding agents. Int J Oncol 2002;21:621-8.
19. Burkhart CA, Kavallaris M, Band Horwitz S. The role of β-tubulin isotypes in resistance to antimitotic drugs. Biochim Biophys Acta 2001;1471:1-9.
20. Verrills NM, Kavallaris M. Improving the targeting of tubulin-binding agents: lessons from drug resistance studies. Curr Pharm Des 2005;11:1719-33.
21. Giannakakou P, Sackett DL, Kang YK, et al. Paclitaxel-resistant human ovarian cancer cells have mutant β-tubulins that exhibit impaired paclitaxel-driven polymerization. J Biol Chem 1997;272:17118-25.
22. Gonzalez-Garay ML, Chang L, Blade K, Menick DR, Cabral F. A β-tubulin leucine cluster involved in microtubule assembly and paclitaxel resistance. J Biol Chem 1999;274:23875-82.
23. Giannakakou P, Gussio R, Nogales E, et al. A common pharmacophore for epothilone and taxanes: molecular basis for drug resistance conferred by tubulin mutations in human cancer cells. Proc Natl Acad Sci U S A 2000;97:2904-9.
24. He L, Yang CP, Horwitz SB. Mutations in β-tubulin map to domains involved in regulation of microtubule stability in epothilone-resistant cell lines. Mol Cancer Ther 2001;1:3-10.
25. Verrills NM, Flemming CL, Liu M, et al. Microtubule alterations and mutations induced by desoxyepothilone B: implications for drug-target interactions. Chem Biol 2003;10:597-607.
26. Yang CP, Verdier-Pinard P, Wang F, et al. A highly epothilone B-resistant A549 cell line with mutations in tubulin that confer drug dependence. Mol Cancer Ther 2005;4:987-95.
27. Kavallaris M, Tait AS, Walsh BJ, et al. Multiple microtubule alterations are associated with Vinca alkaloid resistance in human leukemia cells. Cancer Res 2001;61:5803-9.
28. Hua XH, Genini D, Gussio R, et al. Biochemical genetic analysis of indanocine resistance in human leukemia. Cancer Res 2001;61:7248-54.
29. Hari M, Wang Y, Veeraraghavan S, Cabral F. Mutations in α- and β- tubulin that stabilize microtubules and confer resistance to colcemid and vinblastine. Mol Cancer Ther 2003;2:597-605.
30. Poruchynsky MS, Kim JH, Nogales E, et al. Tumor cells resistant to a microtubule-depolymerizing hemi-asterlin analogue, HTI-286, have mutations in α-or β-tubulin and increased microtubule stability. Biochemistry 2004;43:13944-54.
31. Don S, Verrills NM, Liaw TY, et al. Neuronal-associated microtubule proteins class III β-tubulin and MAP2c in neuroblastoma: role in resistance to microtubule-targeted drugs. Mol Cancer Ther 2004;3:1137-46.
32. Zhang CC, Yang JM, White E, Murphy M, Levine A, Hait WN. The role of MAP4 expression in the sensitivity to paclitaxel and resistance to Vinca alkaloids in p53 mutant cells. Oncogene 1998;16:1617-24.
33. Vallee RB. A taxol-dependent procedure for the isolation of microtubules and microtubule-associated proteins (MAPs). J Cell Biol 1982;92:435-42.
34. Verdier-Pinard P, Wang F, Martello L, Burd B, Orr GA, Horwitz SB. Analysis of tubulin isotypes and mutations from taxol-resistant cells by combined isoelectrofocusing and mass spectrometry. Biochemistry 2003;42:5349-57.
35. Zhou J, Gupta K, Aggarwal S, et al. Brominated derivatives of noscapine are potent microtubule-interfering agents that perturb mitosis and inhibit cell proliferation. Mol Pharmacol 2003;63:799-807.
36. Krishna R, Mayer LD. Multidrug resistance (MDR) in cancer. Mechanisms, reversal using modulators of MDR and the role of MDR modulators in influencing the pharmacokinetics of anticancer drugs. Eur J Pharm Sci 2000;11:265-83.
37. Nicoletti MI, Valoti G, Giannakakou P, et al. Expression of β-tubulin isotypes in human ovarian carcinoma xenografts and in a sub-panel of human cancer cell lines from the NCI-Anticancer Drug Screen: correlation with sensitivity to microtubule active agents. Clin Cancer Res 2001;7:2912-22.
38. Bai R, Covell DG, Pei XF, et al. Mapping the binding site of colchicinoids on β -tubulin. 2-Chloroacetyl-2-demethylthiocolchicine covalently reacts predominantly with cysteine 239 and secondarily with cysteine 354. J Biol Chem 2000;275:40443-52.
39. Ravelli RB, Gigant B, Curmi PA, et al. Insight into tubulin regulation from a complex with colchicine and a stathmin-like domain. Nature 2004;428:198-202.
40. Westermann S, Weber K. Post-translational modifications regulate microtubule function. Nat Rev Mol Cell Biol 2003;4:938-47.
41. Nogales E, Wolf SG, Downing KH. Structure of the αβ tubulin dimer by electron crystallography. Erratum in: Nature 1998;393:191 Nature 1998;391:199-203.
42. Nettles JH, Li H, Cornett B, Krahn JM, Snyder JP, Downing KH. The binding mode of epothilone A on α,β-tubulin by electron crystallography. Science 2004;305:866-9.
43. 2- tubulin confer altered sensitivity to microtubule inhibitors in Chlamydomonas. Plant Cell 1990;2:1051-7.
44. R15 β-tubulin mutations in Chlamydomonas reinhardtii confer altered sensitivities to microtubule inhibitors and herbicides by enhancing microtubule stability. J Cell Biol 1991;113:605-14.