Journal of Protein Chemistry

, Volume 15, Issue 4, pp 377–388 | Cite as

Influence of microtubule-associated proteins on the differential effects of paclitaxel and docetaxel

  • Yves Fromes
  • P. Gounon
  • R. Veitia
  • M. C. Bissery
  • A. Fellous
Article
Received:

Abstract

Microtubules are complex structures arising in part from the polymerization of tubulin dimers. Tubulin binds to a wide range of drugs which have been used as probes for tubulin conformation and assembly properties. There is some evidence that taxol and taxotere have differing effects on tubulin conformation. Previous work has shown that MAP2 and Tau, although they both induce microtubule assembly, have qualitatively different effects on tubulin's behavior. Since most microtubulesin vivo are likely to be associated with MAPs, we decided to characterize the differential effects of MAP2, Tau, taxol, and taxotere on tubulin polymerization with the aim of understanding the mechanisms through which these agents stimulate microtubule assembly. Furthermore, the inhibitive effect of calcium has been used to elucidate the ability of the two drugs to force tubulin assembly. These observations suggest that docetaxel, in addition to its greater efficiency in tubulin assembly, may have the capacity to differently alter certain classes of microtubules. Tau and MAP2 accessory proteins may represent important cofactors modulating the effects of taxoids.

Key words

Microtubule-associated proteins MAP2 Tau paclitaxel docetaxel 
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References

  1. Albertini, D. F. (1984).In vivo andin vitro studies on the role of HMW-MAPs in taxol-induced microtubule bundling,Eur. J. Cell Biol. 33, 134–143.PubMedGoogle Scholar
  2. Andreu, J. M., Diaz, J. F., Gil, R., de Pereda, J. M., de Lacoba, M. G., Peyrot, V., Briand, C., Towns-Andrews, E., and Bordas, J. (1994). Solution structure of Taxotere-induced microtubules,J. Biol. Chem. 269, 31785–31792.PubMedGoogle Scholar
  3. Bissery, M. C., Guénard, D., Guéritte-Voegelein, F., and Lavelle, F. (1991). Experimental antitumor activity of taxotere (RP 56976, NSC 628503), a taxol analogue,Cancer Res. 51, 4845–4852.PubMedGoogle Scholar
  4. Bissery, M. C., Nohynek, G., Sanderink, G., and Lavelle, F. (1995). Docetaxel (Taxotere®), a review of preclinical and clinical experience. Part I: Preclinical experience,Anticancer Drugs 6, 1–17.PubMedGoogle Scholar
  5. Chang, A. Y., Kim, K., Glick, J.,et al. (1993). Phase II study of taxol, membarone, and piroxantrone in stage IV non-small-cell lung cancer: The Eastern Cooperative Oncology Group results,J. Natl. Cancer Inst. 85, 388.PubMedGoogle Scholar
  6. De la Torre, J., Carrascosa, J. L., and Avila, J. (1986). The localization of tau proteins on the microtubule surface,Eur. J. Cell Biol. 40, 233–237.PubMedGoogle Scholar
  7. Denis, J.-N., Correa, A., and Greene, A. E. (1990). An improved synthesis of the taxol side chain and of RP 56976,J. Org. Chem. 55, 1957–1959.Google Scholar
  8. Diaz, J. F., and Andreu, J. M. (1993). Assembly of purified GDP-tubulin into microtubules induced by Taxol and Taxotere: Reversibility, ligand stoichiometry and competition,Biochemistry 32(11), 2747–2755.PubMedGoogle Scholar
  9. Dye, R. B., Fink, S. P., and Williams, R. C., Jr. (1993). Taxol-induced flexibility of microtubules and its reversal by MAP-2 and Tau,J. Biol. Chem. 268(10), 6847–6850.PubMedGoogle Scholar
  10. Einzig, A. I., Wiernik, P. H., Sasloff, J.,et al. (1992). Phase II study and long-term follow-up of patients treated with Taxol for advanced ovarian adenocarcinoma,J. Clin. Oncol. 10, 1748.PubMedGoogle Scholar
  11. Fellous, A., Francon, J.,et al. (1977). Microtubule assemblyin vitro. Puruflcation of assembly promoting factors,Eur. J. Biochem. 78, 167–174.PubMedGoogle Scholar
  12. Fellous, A., Luduena, R. F., Prasad, V., Jordan, M. A., Anderson, W., Ohayon, R. and Smith, P. T. (1985). Effects of Tau and MAP2 on the interaction of maytansine with tubulin: Inhibitory effect of maytansine on vinblastine induced aggregation of tubilin,Cancer Res. 45, 5004–5010.PubMedGoogle Scholar
  13. Fellous, A., Ohayon, R., Vacassin, S., Binet, S., Lataste, H., Krikorian, A., Couziner, J. P., and Meininger, V. (1989). Biochemical effects of navelbine on tubulin and associated proteins,Semin. Oncol. 16, 9–14.Google Scholar
  14. Foisner, R., and Wiche, G. (1985). Promotion of MAP/MAP interaction by taxol,J. Ultrastruct. Res. 93, 33–41.PubMedGoogle Scholar
  15. Fromes, Y., Gounon, P., Tapiero, H., and Fellous, A. (1993). Differential effects of anthracyclines on in vitro microtubule assembly,Cell. Parmacol. 1, 589–592.Google Scholar
  16. Garcia, P., Braguer, D., Carles, G., El Khyari, S., Barra, Y., de Ines, C., Barasoain, I., Briand, C. (1994). Comparative effects of taxol and Taxotere on two different human carcinoma cell lines,Cancer Chemother. Pharmacol. 34(4), 335–343.PubMedGoogle Scholar
  17. Guéritte-Voegelein, F., Guénard, D., Lavelle, F., Le Goff, M. T., Mangatal, L., and Potier, P. (1991). Relationships between the structure of taxol analogues and their antimitotic activity,J. Med. Chem. 34, 992–998.PubMedGoogle Scholar
  18. Hamel, E. Campo, A. A. D.,et al. (1981). Interactions of taxol, microtubule-associated proteins and guanine nucleotides in tubulin polymerization,J. Biol. Chem. 256, 11887–11894.PubMedGoogle Scholar
  19. Holmes, F. A., Walters, R. S., Theriault, R. L.,et al. (1991). Phase II trial of taxol, an active drug in the treatment of metastatic breast cancer,J. Natl. Cancer Inst. 83, 1797.PubMedGoogle Scholar
  20. Jacrot, A. U., Riodel, J., Picot, F., Mouriguand, C., Beriel, H., and Potier, P., (1983). Action of taxol on human tumors translated into athymic mice,C. R. Acad. Sci. USA 297, 597–600.Google Scholar
  21. Jordan, M. A.,et al. (1993). Does mitotic block induced in HeLa cells by low concentrations of taxol and vinblastine result in cell death, ASCB Annual Meeting.Google Scholar
  22. Kim, H., Binder, L. I., and Rosenbaum, J. L. (1979). The periodic associateion of MAP2 with brain microtubulesin vitro, J. Cell. Biol. 80, 266–276.PubMedGoogle Scholar
  23. Kumar, N. (1981). Taxol-induced polymerization of purified tubulin,J. Biol. Chem. 256(20), 10435–10441.PubMedGoogle Scholar
  24. Lavelle, F., Fizames, C.et al. (1989). Experimental properties of RP 56976, a taxol derivative,Proc. AACR 30, 566.Google Scholar
  25. Lowry, O. H., Rosenbrough, N. J.,et al. (1951). Protein measurement with the Folin phenol reagent,J. Biol. Chem. 193, 265–275.PubMedGoogle Scholar
  26. Luduena, R. F., Fellous, A., McManus, L., Jordan, M. A., and Nunez, J. (1984). Contrasting effects of Tau and microtubule-associated protein 2 in the vinblastine-induced aggregation of tubulin,J. Biol. Chem. 259, 12890–12898.PubMedGoogle Scholar
  27. Murphy, D. B., and Borisy, G. G. (1975). Association of high molecular weight proteins with microtubules and their role in microtubule assemblyin vitro, Proc. Natl. Acad. Sci. USA 72, 2696–2700.PubMedGoogle Scholar
  28. Murphy, D. B., Vallee, R. B. and Borisy, G. G. (1977). Identity and polymerization-stimulatory activity of non-tubulin proteins associated with microtubule,Biochemistry 16, 2598–2605.PubMedGoogle Scholar
  29. Murphy, W. K., Fossella, F. V., Winn, R. J.,et al. (1993). Phase II study of taxol in patients with untreated advanced non-small-cells lung cancer,J. Natl. Cancer Inst. 85, 384.PubMedGoogle Scholar
  30. Pazdur, R., Kudelka, A. P., Kavanagh, J. J., Cohen, P. R., and Raber, M. N. (1993). The taxoids: Paclitaxel (Taxol®) and docetaxel (Taxotere®),Cancer Treat. Rev.,19, 351–386.PubMedGoogle Scholar
  31. Penningroth, S. M., Cleveland, D. W., and Kirchner, M. W. (1976).In vitro studies of the regulation of microtubule assembly, inCell Motility, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, pp. 1233–1258.Google Scholar
  32. Raff, E. C. (1979). The control of microtubule assemblyin vivo, Int. Rev. Cytol. 59, 1–96.PubMedGoogle Scholar
  33. Ringel, I., and Horwitz, S. B. (1991). Studies with RP 56976 (Taxotere): A synthetic analogue of taxol,J. Nat. Cancer Inst. 83(4), 288–291.PubMedGoogle Scholar
  34. Riondel, J., Jacrot, M., Picot, F., Beriel, H., Mouriquand, C., and Potier, P. (1988). Antineoplastic activity of two taxol derivatives in an ovarian tumor xenografted into nude mice,Anticancer Res. 8, 387–390.PubMedGoogle Scholar
  35. Rose, W. C. (1992). Taxol: A review of its preclinicalin vivo antitumor activity,Anticancer Drugs 3, 311–321.PubMedGoogle Scholar
  36. Rowinsky, E. K., Donehower, R. C., Jones, R. J., and Tucker, R. W. (1988). Microtubule changes and cytotoxicity in leukemic cell lines treated with taxol. Cancer Res.48, 4093–4100.PubMedGoogle Scholar
  37. Schiff, P. B., and Horwitz, S. B. (1981). Taxol assembles tubulin in the absence of exogeneous guanosine 5′-triphosphate or microtubule-associated proteins,Biochemistry 20, 3247–3252.PubMedGoogle Scholar
  38. Schiff, P. B., Fant, J., and Horwitz, S. B. (1979). Promotion of microtubule assemblyin vitro by taxol,Nature 22, 665–667.Google Scholar
  39. Shelanski, M. L., Gaskin, F., and Cantor, C. R. (1973). Microtubule assembly in the absence of added nucleotides,Proc. Natl. Acad. Sci. (USA) 70, 765–768.Google Scholar
  40. Verweij, J., Clavel, M., and Chevalier, B. (1994). Paclitaxel (Taxol™) and docetaxel (Taxotere™): Not simply two of a kind,Ann. Oncol. 5, 495–505.PubMedGoogle Scholar
  41. Weingarten, M. D., Lockwood, A. H., Hwo, S. Y.et al. (1975). A protein factor essential for microtubule assembly,Proc. Natl. Acad. Sci. USA 72, 1848–1852.PubMedGoogle Scholar
  42. Wiche, G., Oberkanins, C., and Himmler, A. (1991). Molecular structure and function of microtubule-associated proteins,Int. Rev. Cytol. 124, 217–273.PubMedGoogle Scholar

Copyright information

© Plenum Publishing Corporation 1996

Authors and Affiliations

  • Yves Fromes
    • 1
  • P. Gounon
    • 2
  • R. Veitia
    • 1
  • M. C. Bissery
    • 3
  • A. Fellous
    • 1
  1. 1.Institut de Génétique MoléculaireHôpital Saint LouisParisFrance
  2. 2.Institut PasteurParis Cedex 15France
  3. 3.Rhône-Poulenc-RorerVitry-sur-SeineFrance

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