Low potency of Taxol at microtubule minus ends: Implications for its antimitotic and therapeutic mechanism

Cancer Research

Volumn 58, Issue 6, 1998, Pages 1177-1184

  Derry, W Brent ^a   Wilson, Leslie ^a   Jordan, Mary Ann ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PACLITAXEL;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CATTLE; CONCENTRATION RESPONSE; DRUG MECHANISM; DRUG POTENCY; MICROTUBULE ASSEMBLY; MITOSIS INHIBITION; MITOSIS SPINDLE; NONHUMAN; PHASE TRANSITION; PRIORITY JOURNAL; STOICHIOMETRY;

ANIMALS; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; CATTLE; KINETICS; MALE; MICROTUBULES; MITOSIS; PACLITAXEL; PROTEIN BINDING; SEA URCHINS; SPERM TAIL; TUBULIN;

EID: 0032520944     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (62)

1. Arbuck, S. G., Dorr, A., and Friedman, M. A. Paclitaxel (Taxol) in breast cancer. Breast Cancer, 8: 121-140, 1994.
2. von Pawel, J., Wagner, H., Niederle, N., Heider, A., Koschel, G., Gromotka, E., and Hanske, M. Paclitaxel and cisplatin in patients with non-small cell lung cancer: results of a Phase II trial. Semin. Oncol., 23 (Suppl. 12): 7-9, 1996.
3. Holmes, F. A. Paclitaxel combination therapy in the treatment of metastatic breast cancer. Semin. Oncol., 23 (Suppl. 12): 29-39, 1996.
4. Younes, A., Ayoub, J., Sarris, A., North, L., Pate, O., McLaughlin, P., Rodriguez, M., Romaguera, J., Hagemeister, F., and Bachier, C. Paclitaxel (Taxol) for the treatment of lymphoma. Ann. Oncol., 8 (Suppl. 1): 129-131, 1997.
5. Hortobagyi, G., Holmes, F., Ibrahim, N., Champlin, R., and Buzdar, A. The University of Texas M. D. Anderson Cancer Center experience with paclitaxel in breast cancer. Semin. Oncol., 24 (Suppl. 3): S30-S33, 1997.
6. Rieder, C., Schultz, A., Cole, R., and Sluder, G. Anaphase onset in vertebrate somatic cells is controlled by a checkpoint that monitors sister kinetochore attachment to the spindle. J. Cell Biol., 127: 1301-1310, 1994.
7. Waters, J. C., Mitchison, T. J., Rieder, C. L., and Salmon, E. D. The kinetochore microtubule minus-end disassembly associated with poleward flux produces a force that can do work. Mol. Biol. Cell. 7: 1547-1558, 1996.
8. Liao, G., Nagasaki, T., and Gundersen, G. G. Low concentrations of nocodazole interfere with fibroblast locomotion without significantly affecting microtubule level: implications for the role of dynamic microtubules in cell locomotion. J. Cell Sci, 108: 3473-3483, 1995.
9. Challacombe, J. F., Snow, D. M., and Letourneau, P. C. Dynamic microtubule ends are required for growth cone turning to avoid an inhibitory guidance cue. J. Neurosci., 17: 3085-3095, 1997.
10. Jordan, M. A., and Wilson, L. The use of drugs to study the role of microtubule assembly dynamics in living cells. In: R. Vallee (ed.), Methods in Enzymology. In press, 1998.
11. Wilson, P. J., and Forer, A. Effects of nanomolar Taxol on crane-fly spermatocyte spindles indicate that acetylation of kinetochore microtubules can be used as a marker of poleward tubulin flux. Cell Motil. Cytoskeleton, 37: 20-32, 1997.
12. Fuchs, D. A., and Johnson, R. K. Cytologic evidence that Taxol, an antineoplastic agent, from Taxus brevifolia, acts as a mitotic spindle poison. Cancer Treat. Rep., 62: 1219-1222, 1978.
13. Schiff, P. B., and Horwitz, S. B. Taxol stabilizes microtubules in mouse fibroblast cells. Proc. Natl. Acad. Sci. USA, 77: 1561-1565, 1980.
14. Jordan, M. A., Toso, R. J., Thrower, D., and Wilson, L. Mechanism of mitotic block and inhibition of cell proliferation by Taxol at low concentrations. Proc. Natl. Acad. Sci. USA, 90: 9552-9556, 1993.
15. Wilson, L., and Jordan, M. A. Microtubule dynamics: taking aim at a moving target. Chem. Biol., 2: 569-573, 1995.
16. Jordan, M. A., and Wilson, L. Microtubules and actin filaments: dynamic targets for cancer chemotherapy. Curr. Opin. Cell Biol., 10: 123-130, 1998.
17. Dustin, P. Microtubules, Ed. 2, pp. 19-93. Berlin: Springer-Verlag, 1984.
18. Amos, L. A., and Klug, A. Arrangement of subunits in flagellar microtubules. J. Cell Sci., 14: 523-549, 1974.
19. Mitchison, T. J., and Kirschner, M. Microtubule assembly nucleated by isolated centrosomes. Nature (Lond.), 312: 232-237, 1984.
20. Mitchison, T. J., and Kirschner, M. Dynamic instability of microtubule growth. Nature (Lond.), 312: 237-242, 1984.
21. Horio, T., and Hotani, H. Visualization of the dynamic instability of individual microtubules by dark-field microscopy. Nature (Lond.), 321: 605-607, 1986.
22. Walker, R. A., O'Brien, E. T., Pryer, N. K., Soboeiro, M. F., Voter, W. A., Erickson, H., and Salmon, E. D. Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies. J. Cell Biol., 107: 1437-1448, 1988.
23. Margolis, R. L., and Wilson, L. Opposite end assembly and disassembly of microtubules at steady state in vitro. Cell, 13: 1-8, 1978.
24. Parness, J., and Horwitz, S. B. Taxol binds to polymerized tubulin in vitro. J. Cell Biol., 91: 479-487, 1981.
25. Diaz, J. F., Menendez, M., and Andreu, J. M. Thermodynamics of ligand-induced assembly of tubulin. Biochemistry, 32: 10067-10077, 1993.
26. Caplow, M., Shanks, J., and Ruhlen, R. How Taxol modulates microtubule disassembly. Biochemistry, 269: 23399-23402, 1994.
27. Derry, W., B., Wilson, L., and Jordan, M. A. Substoichiometric binding of Taxol suppresses microtubule dynamics. Biochemistry, 34: 2203-2211, 1995.
28. DeBrabander, M., Geuens, G., Nuydens, R., Willebrords, R., and De Mey, J. Taxol induces the assembly of free microtubules in living cells and blocks the organizing capacity of the centrosomes and kinetochores. Proc. Natl. Acad. Sci USA, 78: 5608-5612, 1981.
29. Kallajoki, M., Weber, K., and Osborn, M. Ability to organize microtubules in Taxol-treated mitotic PtK2 cells goes with the SPN antigen and not with the centrosome. J. Cell Sci., 102: 91-102, 1992.
30. Snyder, J. A., and Mullins, J. M. Analysis of spindle microtubule organization in untreated and Taxol-treated PtK1 cells. Cell Biol. Int., 17: 1075-1084, 1993.
31. McNally, F. J., and Vale, R. D. Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell, 75: 419-429, 1993.
32. Endow, S. A., Kang, S. K., Satterwhite, L. L., Rose, M. D., Skeen, V. P., and Salmon, E. D. Yeast Kar3 is a minus-end microtubule motor protein that destabilizes microtubules preferentially at the minus ends. EMBO J., 13: 2708-2713, 1994.
33. Jordan, M. A., Wendell, K. L., Gardiner, S., Derry, W. B., Copp, H., and Wilson, L. Mitotic block induced in HeLa cells by low concentrations of paclitaxel (Taxol) results in abnormal mitotic exit and apoptotic cell death. Cancer Res., 56: 816-825, 1996.
34. Farrell, K. W., and Wilson, L. The differential kinetic stabilization of opposite microtubule ends by tubulin-colchicine complexes. Biochemistry, 23: 3741-3748, 1984.
35. Toso, R. J., Jordan, M. A., Farrell, K. W., Matsumoto, B., and Wilson, L. Kinetic stabilization of microtubule dynamic instability in vitro by vinblastine. Biochemistry, 32: 1285-1293, 1993.
36. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72: 248-254, 1976.
37. Derry, W. B., Wilson, L., Khan, I. A., Luduena, R. F., and Jordan, M. A. Taxol differentially modulates the dynamics of microtubules assembled from unfractionated and purified β-tubulin isotypes. Biochemistry, 36: 3554-3562, 1997.
38. Panda, D., Jordan, M. A., Chin, K., and Wilson, L. Differential effects of vinblastine on polymerization and dynamics at opposite microtubule ends. J. Biol. Chem., 271: 29807-29812, 1996.
39. Kowalski, R. J., and Williams, R. C., Jr. Unambiguous classification of microtubule-ends in vitro: dynamic properties of the plus- and minus-ends. Cell Motil. Cytoskeleton. 26: 282-290, 1993.
40. Gildersleeve, R. F., Cross, A. R., Cullen, K. E., Fagan, L. P., and Williams, J., R. C. Microtubules grow and shorten at intrinsically variable rates. J. Biol. Chem., 267: 7995-8006, 1992.
41. O'Brien, E. T., Salmon, E. D., Walker, R. A., and Erickson, H. P. Biochemistry, 29: 6648-6656, 1990.
42. Diaz, J. F., and Andreu, J. M. Assembly of purified GDP-tubulin into microtubules induced by Taxol and taxotere: reversibility, ligand stoichiometry, and competition. Biochemistry, 32: 2747-2755, 1993.
43. Caplow, M., and Zeeberg, B. Dynamic properties of microtubules at steady state in the presence of Taxol. Eur. J. Biochem., 127: 319-324, 1982.
44. Wilson, L., Miller, H. P., Farrell, K. W., Snyder, K. B., Thompson, W. C., and Purich, D. L. Taxol stabilization of microtubules in vitro: dynamics of tubulin addition and loss at opposite microtubule ends. Biochemistry, 24: 5254-5262, 1985.
45. Mandelkow, E., Mandelkow, E., and Milligan, R. Microtubule dynamics and microtubule caps: a time-resolved cryo-electron microscopy study. J. Cell Biol., 114: 977-991, 1991.
46. Tran, P., Joshi, P., and Salmon, E. How tubulin subunits are lost from the shortening ends of microtubules. J. Struct. Biol., 118: 107-118, 1997.
47. Hyman, A. A., Chretien, D., Arnal, I., and Wade, R. H. Structural changes accompanying GTP hydrolysis in microtubules: information from a slowly hydrolyzable analogue guanylyl-(α, β) methylene-diphosphonate. J. Cell. Biol., 128: 117-125, 1995.
48. Arnal, I., and Wade, R. H. How does Taxol stabilize microtubules? Curr. Biol., 5: 900-908, 1995.
49. Andreu, J. M., Bordas, J., Diaz, J. F., Garcia de Ancos, J., Gil, R., Medrano, F. J., Nogales, E., Pantos, E., and Towns-Andrews, E. Low resolution structure of microtubules in solution. Synchrotron x-ray scattering and electron microscopy of Taxol-induced microtubules assembled from purified tubulin in comparison with glycerol and MAP-induced microtubules. J. Mol. Biol., 226: 169-184, 1992.
50. Nogales, E., Wolf, S. G., Khan, I. A., Luduena, R. F., and Downing, K. A. Structure of tubulin at 6.5A and location of the Taxol-binding site. Nature (Lond.), 375: 424-427, 1995.
51. Mogenson, M. M., and Tucker, J. B. Taxol influences control of protofilament number at microtubule-nucleating sites in Drosophila. J. Cell Sci., 97: 101-107, 1990.
52. Jordan, M. A., and Wilson, L. Kinetic analysis of tubulin exchange at microtubule ends at low vinblastine concentrations. Biochemistry, 29: 2730-2739, 1990.
53. Photiou, A., Shah, P., Leong, L., Moss, J., and Retsas, S. In vitro synergy of paclitaxel (Taxol) and vinorelbine (navelbine) against human melanoma cell lines. Eur. J. Cancer, 33: 463-470, 1997.
54. Thrower, D. A. Activity and localization of a CENP-E-associated minus end-directed microtubule motor in Hela cells (Thesis). Santa Barbara, CA: University of California Santa Barbara, 1995.
55. Li, X., and Nicklas, R. B. Mitotic forces control a cell-cycle checkpoint. Nature (Lond.), 373: 630-632, 1995.
56. Glantz, M. J., Choy, H., Kearns, C. M., Mills, P. C., Wahlberg, L. U., Zuhowski, E. G., Calabresi, P., and Egorin, M. J. Paclitaxel disposition in plasma and central nervous systems of humans and rats with brain tumors. J. Natl. Cancer Inst. (Bethesda). 87: 1077-1081, 1995.
57. Walle, T., Walle, U., Kumar, G., and Bhalla, K. Taxol metabolism and disposition in cancer patients. Drug Metab. Dispos., 23: 506-512, 1995.
58. Huizing, M. T., Giaccone, G., van Warmerdam, L. J., Rosing, H., Bakker, P. J., Vermorken, J. B., Postmus, P. E., van Zandwijk, N., Koolen, M. G. J., Huinink, W. W. T. B., van der Vijgh, W. J. F., Bierhorst, F. J., Lai, A., Dalesio, O., Pinedo, H. M., Veenhof, C. H. N., and Beijnen, J. H. Pharmacokinetics of paclitaxel and carboplatin in a dose-escalating and dose-sequencing study in patients with non-small-cell lung cancer. J. Clin. Oncol., 15: 317-329, 1997.
59. Huizing, M., Vermorken, J., Rosing, H., ten Bokkel Huinink, W., Mandjes, I., Pinedo, H., and Beijnen, J. Pharmacokinetics of paclitaxel and three major metabolites in patients with advanced breast carcinoma refractory to anthracycline therapy treated with a 3-hour paclitaxel infusion: a European Cancer Centre (ECC) trial. Ann. Oncol., 6: 699-704, 1995.
60. Vermorken, J., ten Bokkel Huinink, W., Mandjes, I., Postma, T., Huizing, M., Heimans, J., Beijnen, J., Bierhorst, F., Winograd, B., and Pinedo, H. High-dose paclitaxel with granulocyte colony-stimulating factor in patients with advanced breast cancer refractory to anthracycline therapy: a European Cancer Center trial. Semin. Oncol., 22: 16-22.
61. Kumar, G., Walle, U., Bhalla, K., and Walle, T. Binding of Taxol to human plasma, albumin and α-1-acid glycoprotein. Res. Commun. Chem. Pathol. Pharmacol., 80: 337-344, 1993.
62. Guy, R., Scott, Z., Sloboda, R., and Nicolaou, K. Fluorescent taxoids. Chem. Biol., 3: 1021-1031, 1996.