Taxol-resistant epithelial ovarian tumors are associated with altered expression of specific β-tubulin isotypes

Journal of Clinical Investigation

Volumn 100, Issue 5, 1997, Pages 1282-1293

  Kavallaris, Maria ^a   Kuo, Dennis Y S ^a   Burkhart, Catherine A ^a   Regl, Donna Lee ^a   Norris, Murray D ^b   Haber, Michelle ^b   Horwitz, Susan Band ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b SYDNEY CHILDREN'S HOSPITAL   (Australia)

Author keywords

Carcinoma; Drug resistance; Lung; Microtubules; Polymerase chain reaction

Indexed keywords

BETA TUBULIN; PACLITAXEL;

ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; DRUG RESISTANCE; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG CANCER; OVARY CARCINOMA; OVARY TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 0030931827     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119642     Document Type: Article

References (60)

1. Parker, S.L., T. Tong, S. Bolden, and P.A. Wingo. 1996. Cancer Statistics, 1996. CA Cancer J. Clin. 46:5-27.
2. Cannistra, S.A. 1993. Cancer of the ovary. N. Engl. J. Med. 329:1550-1559.
3. Johnson, S.W., R.E. Ozols, and T.C. Hamilton. 1993. Mechanisms of drug resistance in ovarian cancer. Cancer. 71:644-649.
4. McGuire, W.P., W.J. Hoskins, M.F. Brady, P.R. Kucera, E.E. Partridge, K.Y. Look, D.L. Clarke-Pearson, and M. Davidson. 1996. Cyclophosphamide and cisplatin compared with paclitaxel and cisplatin in patients with stage III and stage IV ovarian cancer. N. Engl. J. Med. 334:1-6.
5. Holmes, F.A., R.S. Walters, R.L. Theriault, A.D. Forman, L.K. Newton, M.N. Raber, A.U. Buzdar, O.K. Frye, and G.N. Hortobagyi. 1991. Phase II trial of taxol, an active drug in the treatment of metastatic breast cancer. J. Natl. Cancer Inst. 83:1797-1805.
6. Murphy, W.K., F.V. Fossella, R.J. Winn, D.M. Shin, H.E. Hynes, H.M. Gross, E. Davilla, J. Leimert, H. Dhingra, M.N. Raber, et al. 1993. Phase II trial of taxol in patients with untreated advanced non-small-cell lung cancer. J. Natl. Cancer Inst. 85:384-387.
7. Horwitz, S.B., D. Cohen, S. Rao, I. Ringel, H.J. Shen, and C.P. Yang. 1993. Taxol: mechanisms of action and resistance. J. Natl. Cancer Inst. Monogr. 15:55-61.
8. Wani, M.C., H.L. Taylor, M.E. Wall, P. Coggon, and AT. McPhail. 1971. Plant antitumor agents VI. The isolation and structure of taxol, a novel antileukemic and antitumor agent from taxus brevifolia. J. Am. Chem. Soc. 93:2325-2327.
9. Schiff, P.B., and S.B. Horwitz. 1980. Taxol stabilizes microtubules in mouse fibroblast cells. Proc. Natl. Acad. Sci. USA. 77:1561-1565.
10. Rao, S., G.A. Orr, A.C. Chaudhary, D.G.I. Kingston, and S.B. Horwitz. 1995. Characterization of the taxol binding site on the microtubule. J. Biol. Chem. 270:20235-20238.
11. Cowan, N.J., and L. Dudley. 1983. Tubulin isotypes and the multigene tubulin families. Int. Rev. Cytol. 85:147-173.
12. Lewis, S.A., and N.J. Cowan. 1990. Tubulin genes: structure, expression, and regulation. In Microtubule Proteins. J. Avila, editor. CRC Press, Inc., Boca Raton, FL. 37-66.
13. Sullivan, K.F., and D.W. Cleveland. 1986. Identification of conserved isotype-defining variable region sequences for four vertebrate β tubulin polypeptide classes. Proc. Natl. Acad. Sci. USA. 83:4327-4331.
14. Sullivan, K.F. 1988. Structure and utilization of tubulin isotypes. Annu. Rev. Cell Biol. 4:687-716.
15. Burgoyne, R.D., M.A. Cambray Deakin, S.A. Lewis, S. Sarkar, and N.J. Cowan. 1988. Differential distribution of β-tubulin isotypes in cerebellum. EMBO (Eur. Mol. Biol. Organ.) J. 7:2311-2319.
16. Cowan, N.J., S.A. Lewis, S. Sarkar, and W. Gu. 1987. Functional versatility of mammalian β-tubulin isotypes. In The Cytoskeleton in Cell Differentiation and Development. R. Maccioni and J. Arechaya, editors. ICSU Press, Miami, FL. 157-166.
17. Wang, D., A. Villasante, S.A. Lewis, and N.J. Cowan. 1986. The mammalian β-tubulin repertoire: hematopoietic expression of a novel heterologous β-tubulin isotype. J. Cell Biol. 103:1903-1910.
18. Panda, D., H.P. Miller, A. Banerjee, R.F. Luduena, and L. Wilson. 1994. Microtubule dynamics in vitro are regulated by the tubulin isotype composition. Proc. Natl. Acad. Sci. USA. 91:11358-11362.
19. Derry, W.B., L. Wilson, and M.A. Jordan. 1995. Substoichiometric binding of taxol suppresses microtubule dynamics. Biochemistry. 34:2203-2211.
20. Jordan, M.A., R.J. Toso, D. Thrower, and L. Wilson. 1993. Mechanism of mitotic block and inhibition of cell proliferation by taxol at low concentrations. Proc. Natl. Acad. Sci. USA. 90:9552-9556.
21. III isotype enhances taxol induced microtubule assembly. Cell Struct. Funct. 18:173-182.
22. Haber, M., C.A. Burkhart, D.L. Regl, J. Madafiglio, M.D. Norris, and S.B. Horwitz. 1995. Altered expression of Mβ2, the class II β-tubulin isotype, in a murine J744.2 cell line with a high level of taxol resistance. J. Biol. Chem. 270: 31269-31275.
23. Roy, S.N., and S.B. Horwitz. 1985. A phosphoglycoprotein associated with taxol resistance in J774.2 cells. Cancer Res. 45:3856-3863.
24. Greenberger, L.M., L. Lothestein, S.S. Williams, and S.B.H. Horwitz. 1988. Distinct P-glycoprotein precursors are overproduced in independently isolated drug-resistant cell lines. Proc. Natl. Acad. Sci. USA. 85:3762-3766.
25. Towbin, H., T. Staehelm, and J. Gordon. 1979. Electrophoretic transfer of proteins from nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA. 76:4350-4354.
26. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
27. Kuo, D.Y.-S., S. Mallick, H.-J. Shen, C. DeVictoria, J. Jones, A.L. Fields, G.L. Goldberg, C.D. Runowicz, and S.B. Horwitz. 1996. Analysis of MDR1 expression in normal and malignant endometrium by reverse transcription-polymerase chain reaction and immunohistochemistry. J. Clin. Cancer Res. 2:1981-1992.
28. Chomczynski, P. 1993. TRI Reagent: RNA, DNA, Protein Isolation Reagent. Manufacturer Protocol, Molecular Research Center, Inc., Cincinnati, OH.
29. Noonan, K.E., C. Beck, T.A. Holzmayer, J.E. Chin, J.S. Wunder, I.L. Andrulis, A.F. Gazdar, C.L. Willman, B. Grifith, D.D. Von Hof, and I.B. Roninson. 1990. Quantitative analysis of MDR1 (multidrug resistant) gene expression in human tumors by polymerase chain reaction. Proc. Natl. Acad. Sci. USA. 87:7160-7164.
30. Gilbert, J., M.D. Norris, M. Haber, M. Kavallaris, G.M. Marshall, and B.W. Stewart. 1993. Determination of N-myc gene amplification in neuroblastoma by differential polymerase chain reaction. Mol. Cell. Probes. 7:227-234.
31. Jaffrezou, J.-P., C. Dumontet, W.B. Derry, G. Duran, G. Chen, E. Tsuchiya, L. Wilson, M.A. Jordan, and B.L. Sikic. 1995. Novel mechanism of resistance to Paclitaxel (Taxol) in human K562 leukemia cells by combined selection with PSC 833. Oncol. Res. 7:517-527.
32. Bordow, S.B., M. Haber, J. Madafiglio, B. Cheung, G.M. Marshall, and M.D. Norris. 1994. Expression of the multidrug resistance-associated protein (MRP) gene correlates with amplification and overexpression of the N-myc oncogene in childhood neuroblastoma. Cancer Res. 54:5036-5040.
33. Chomczynski, P., and P.K. Qasba. 1984. Alkaline transfer of DNA to plastic membrane. Biochem. Biophys. Res. Commun. 122:340-344.
34. Khandjian, E.W., and C. Meric. 1986. A procedure for northern blot analysis of native RNA. Anal. Biochem. 159:227-232.
35. Cabral, F., and S.B. Barlow. 1989. Mechanisms by which mammalian cells acquire resistance to drugs that affect microtubule assembly. FASEB (Fed. Am. Soc. Exp. Biol.) J. 3:1593-1599.
36. Cabral, F.R., R.C. Brady, and M.J. Schibler. 1986. A mechanism of cellular resistance to drugs that interfere with microtubule assembly. Ann. NY Acad. Sci. 466:745-756.
37. Ohta, S., K. Nishio, N. Kubota, T. Ohmori, Y. Funayama, T. Ohira, H. Nakajima, M. Adachi, and N. Saijo. 1994. Characterisation of a taxol-resistant human small-cell lung cancer cell line. Jpn. J. Cancer Res. 85:290-297.
38. Laferriere, N.B., and D.L. Brown. 1995. Effects of taxol on the polymerization and posttranslational modification of class III β-tubulin in P19 embryonal carcinoma cells. Biochem. Cell Biol. 73:687-694.
39. Minotti, A.M., S.B. Barlow, and F. Cabral. 1991. Resistance to antimitotic drugs in Chinese hamster ovary cells correlates with changes in the level of polymerized tubulin. J. Biol. Chem. 266:3987-3994.
40. Weinstein, B., and F. Solomon. 1990. Phenotypic consequences of tubulin overproduction in Saccharomyces cerevisiae: differences between alpha-tubulin and beta-tubulin. Mol. Cell. Biol. 10:5295-5304.
41. Burke, D., P. Gasdaska, and L. Hartwell. 1989. Dominant effects of tubulin overexpression in Saccharomyces cerevisiae. Mol. Cell. Biol. 9:1049-1059.
42. IVa-tubulin in human prostate carcinoma cells as a result of estramustine resistance. Cancer Res. 56:2584-2589.
43. Murdoch, W.J. 1996. Ovarian surface epithelium, ovulation and carcinogenesis. Biol. Rev. 71:529-543.
44. Lewis, S.A., M.E. Gilmartin, J.L. Hall, and N.J. Cowan. 1985. Three expressed sequences within the human β-tubulin multigene family each define a distinct isotype. J. Mol. Biol. 182:11-20.
45. Lewis, S.A., W. Gu, and N.J. Cowan. 1987. Free intermingling of mammalian β-tubulin isotypes among functionally distinct microtubules. Cell. 49: 539-548.
46. Lewis, S.A., M. Gwo-Shu Lee, and N.J. Cowan. 1985. Five mouse tubulin isotypes and their regulated expression during development. J. Cell Biol. 101:852-861.
47. Luduena, R.F. 1993. Are tubulin isotypes functionally significant? Mol. Biol. Cell. 4:445-157.
48. Alexander, J.E., D.F. Hunt, M.K. Lee, J. Shabanowitz, H. Michel, S.C. Berlin, T.L. Macdonald, R.J. Sunberg, L.I. Rebhun, and A. Frankfurter. 1991. Characterization of posttranslational modifications in neuron-specific class III β-tubulin by mass spectrometry. Proc. Natl Acad. Sci. USA. 88:4685-1689.
49. Mary, J., V. Redeker, J.-P. Le Caer, J.-G. Prome, and J. Rossier. 1994. Class I and IVa β-tubulin isotypes expressed in adult mouse brain are glutamylated. FEBS (Fed. Eur. Biochem. Soc.) Lett. 353:89-94.
50. Rudiger, M., U. Plessman, K.-D. Kloppel, J. Wehland, and K. Weber. 1992. Class II tubulin, the major brain β tubulin isotype is polyglutamylated on glutamic acid residue 435. FEBS (Fed. Eur. Biochem. Soc.) Lett. 308:101-105.
51. III-tubulin. Biochemistry. 35:3704-3711.
52. Holzmayer, T.A., S. Hilsenbeck, D.D. Don Hoff, and I.B. Roninson. 1992. Clinical correlates of MDR1 (P-glycoprotein) gene expression in ovarian and small-cell lung carcinomas. J. Natl. Cancer Inst. 84:1486-1491.
53. Kavallaris, M., J.A. Leary, J.A. Barrett, and M.L. Friedlander. 1996. MDR1 and multidrug resistance-associated protein (MRP) gene expression in epithelial ovarian tumors. Cancer Lett. 102:7-16.
54. Bourhis, J., L.J. Goldstein, G. Riou, I. Pastan, M.M. Gottesman, and J. Benard. 1989. Expression of a human multidrug resistance gene in ovarian carcinomas. Cancer Res. 49:5062-5065.
55. Bell, D.R., J.H. Gerlach, N. Kartner, R.N. Buick, and V. Ling. 1985. Detection of P-glycoprotein in ovarian cancer: a molecular marker associated with multidrug resistance. J. Clin. Oncol. 3:311-315.
56. McGuire, W.P., E.K. Rowinsky, N.B. Rosenshein, F.C. Grumbine, D.S. Ettinger, D.K. Armstrong, and R.C. Donehower. 1989. Taxol: a unique antineoplastic agent with significant activity in advanced ovarian epithelial neoplasms. Ann. Intern. Med. 111:273-279.
57. Zaman, G.J.R., M.J. Flens, M.R. van Leusden, M. de Haas, H.S. Mulder, J. Lankelma, H.M. Pinedo, R.J. Scheper, F. Baas, H.J. Broxterman, and P. Borst. 1994. The human multidrug-resistance-associated protein MRP is a plasma membrane drug-efflux pump. Proc. Natl Acad. Sci. USA. 91:8822-8826.
58. Cole, S.P.C., K.E. Sparkes, K. Fraser, D.W. Loe, C.E. Grant, G.M. Wilson, and R.G. Deeley. 1994. Pharmacological characterisation of multidrug resistant MRP-transfected human tumor cells. Cancer Res. 54:5902-5910.
59. Van Der Zee, A.G.J., H.H. Hollema, H.W.A. De Bruijn, P.H.B. Willemse, H. Boonstra, N.H. Mulder, J.G. Aalders, and E.G.E. De Vries. 1995. Cell biological markers of drug resistance in ovarian carcinoma. Gynecol. Oncol. 58:165-178.
60. Derry, W.B., S. Wilson, I.A. Khan, R.F. Luduena, and M.A. Jordan. 1997. Taxol differentially modulates the dynamics of microtubules assembled from unfractionated and purified β-tubulin isotypes. Biochemistry. 36:3554-3562.