Seminars in Oncology
Volume 35 , Pages S22-S27 , June 2008

Potential Mechanisms of Resistance to Microtubule Inhibitors

  • Maria Kavallaris

      Affiliations

    • Children's Cancer Institute Australia for Medical Research, Randwick, NSW, Australia.
    • Corresponding Author InformationAddress correspondence to Maria Kavallaris, PhD, Children's Cancer Institute Australia for Medical Research, High Street, PO Box 81, 2031 Randwick, NSW, Australia.
    • ,
  • Jean-Philippe Annereau

      Affiliations

    • Centre de Recherche Oncologie Expérimentale, Institut de Recherche Pierre Fabre, Toulouse, France.
    • ,
  • Jean-Marc Barret

      Affiliations

    • Centre de Recherche Oncologie Expérimentale, Institut de Recherche Pierre Fabre, Toulouse, France.

References 

  1. Schuetz EG, Beck WT, Schuetz JD. Modulators and substrates of P-glycoprotein and cytochrome P4503A coordinately up-regulate these proteins in human colon carcinoma cells. Mol Pharmacol. 1996;49:311–318
  2. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer. 2002;2:48–57
  3. Ueda K, Cardarelli C, Gottesman MM, Pastan I. Expression of a full-length cDNA for the human “MDR1” gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc Natl Acad Sci U S A. 1987;84:3004–3008
  4. Ambudkar SV, Dey S, Hrycyna CA, Ramachandra M, Pastan I, Gottesman MM. Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu Rev Pharmacol Toxicol. 1999;39:361–398
  5. Dean M, Rzhetsky A, Allikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res. 2001;11:1156–1166
  6. Kavallaris M. The role of multidrug resistance-associated protein (MRP) expression in multidrug resistance. Anticancer Drugs. 1997;8:17–25
  7. Grant CE, Valdimarsson G, Hipfner DR, Almquist KC, Cole SP, Deeley RG. Overexpression of multidrug resistance-associated protein (MRP) increases resistance to natural product drugs. Cancer Res. 1994;54:357–361
  8. Kruh GD, Chan A, Myers K, Gaughan K, Miki T, Aaronson SA. Expression complementary DNA library transfer establishes mrp as a multidrug resistance gene. Cancer Res. 1994;54:1649–1652
  9. Cole SP, Bhardwaj G, Gerlach JH, et al. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science. 1992;258:1650–1654
  10. Zaman GJ, Versantvoort CH, Smit JJ, et al. Analysis of the expression of MRP, the gene for a new putative transmembrane drug transporter, in human multidrug resistant lung cancer cell lines. Cancer Res. 1993;53:1747–1750
  11. Zaman GJ, Flens MJ, van Leusden MR, et al. The human multidrug resistance-associated protein MRP is a plasma membrane drug-efflux pump. Proc Natl Acad Sci U S A. 1994;91:8822–8826
  12. Breuninger LM, Paul S, Gaughan K, et al. Expression of multidrug resistance-associated protein in NIH/3T3 cells confers multidrug resistance associated with increased drug efflux and altered intracellular drug distribution. Cancer Res. 1995;55:5342–5347
  13. Cole SP, Sparks KE, Fraser K, et al. Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells. Cancer Res. 1994;54:5902–5910
  14. Flens MJ, Izquierdo MA, Scheffer GL, et al. Immunochemical detection of the multidrug resistance-associated protein MRP in human multidrug-resistant tumor cells by monoclonal antibodies. Cancer Res. 1994;54:4557–4563
  15. Hipfner DR, Gauldie SD, Deeley RG, Cole SP. Detection of the Mr 190,000 multidrug resistance protein, MRP, with monoclonal antibodies. Cancer Res. 1994;54:5788–5792
  16. Gottesman MM. Mechanisms of cancer drug resistance. Annu Rev Med. 2002;53:615–627
  17. Kruh GD, Gaughan KT, Godwin A, Chan A. Expression pattern of MRP in human tissues and adult solid tumor cell lines. J Natl Cancer Inst. 1995;87:1256–1258
  18. Burger H, Nooter K, Zaman GJ, et al. Expression of the multidrug resistance-associated protein (MRP) in acute and chronic leukemias. Leukemia. 1994;8:990–997
  19. Bordow SB, Haber M, Madafiglio J, Cheung B, Marshall GM, Norris MD. Expression of the multidrug resistance-associated protein (MRP) gene correlates with amplification and overexpression of the N-myc oncogene in childhood neuroblastoma. Cancer Res. 1994;54:5036–5040
  20. Giaccone G, van Ark-Otte J, Rubio GJ, et al. MRP is frequently expressed in human lung-cancer cell lines, in non–small-cell lung cancer and in normal lungs. Int J Cancer. 1996;66:760–767
  21. Verrills NM, Po'uha ST, Liu ML, et al. Alterations in gamma-actin and tubulin-targeted drug resistance in childhood leukemia. J Natl Cancer Inst. 2006;98:1363–1374
  22. Drukman S, Kavallaris M. Microtubule alterations and resistance to tubulin-binding agents (review). Int J Oncol. 2002;21:621–628
  23. Orr GA, Verdier-Pinard P, McDaid H, Horwitz SB. Mechanisms of Taxol resistance related to microtubules. Oncogene. 2003;22:7280–7295
  24. 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
  25. Banerjee A, Roach MC, Trcka P, Ludueña RF. Increased microtubule assembly in bovine brain tubulin lacking the type III isotype of β-tubulin. J Biol Chem. 1990;265:1794–1799
  26. Kavallaris M, Kuo DY, Burkhart CA, et al. Taxol-resistant epithelial ovarian tumors are associated with altered expression of specific beta-tubulin isotypes. J Clin Invest. 1997;100:1282–1293
  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;61:5803–5809
  28. Gan P, Pasquier E, Kavallaris M. Class III b-tubulin mediates sensitivity to chemotherapeutic drugs in non-small cell lung cancer. Cancer Res. 2007;67:9356–9363
  29. Verrills NM, Kavallaris M. Improving the targeting of tubulin-binding agents: Lessons from drug resistance studies. Curr Pharm Des. 2005;11:1719–1733
  30. Martello LA, Verdier-Pinard P, Shen HJ, et al. Elevated levels of microtubule destabilizing factors in a Taxol-resistant/dependent A549 cell line with an α-tubulin mutation. Cancer Res. 2003;63:1207–1213
  31. Zhang CC, Yang J-M, 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;16:1617–1624
  32. Alli E, Bash-Babula J, Yang J-M, Hait WN. Effect of stathmin on the sensitivity to antimicrotubule drugs in human breast cancer. Cancer Res. 2002;62:6864–6869
  33. Kruczynski A, Colpaert F, Tarayre JP, Mouillard P, Fahy J, Hill BT. Preclinical in vivo antitumor activity of vinflunine, a novel fluorinated vinca alkaloid. Cancer Chemother Pharmacol. 1998;41:437–447
  34. Etiévant C, Barret J-M, Kruczynski A, Perrin D, Hill BT. Vinflunine (20′,20′-difluoro-3′,4′-dihydrovinorelbine), a novel Vinca alkaloid, which participates in P-glycoprotein (Pgp)-mediated multidrug resistance in vivo and in vitro. Invest New Drugs. 1998;16:3–17
  35. Adams DJ, Knick VC. P-glycoprotein mediated resistance to 5′-nor-anhydro-vinblastine (Navelbine). Invest New Drugs. 1995;13:13–21
  36. Hill BT, Whelan RD, Shellard SA, McClean S, Hosking LK. Differential cytotoxic effects of docetaxel in a range of mammalian tumor cell lines and certain drug resistant sublines in vitro. Invest New Drugs. 1994;12:169–182
  37. Nielsen D, Skovsgaard T. P-glycoprotein as multidrug transporter: A critical review of current multidrug resistant cell lines. Biochim Biophys Acta. 1992;1139:169–183
  38. Etiévant C, Kruczynski A, Barret J-M, Tait AS, Kavallaris M, Hill BT. Markedly diminished drug resistance-inducing properties of vinflunine (20′,20′-difluoro-3′,4′-dihydrovinorelbine) relative to vinorelbine, identified in murine and human tumour cells in vivo and in vitro. Cancer Chemother Pharmacol. 2001;48:62–70
  39. Kruczynski A, Etiévant C, Perrin D, Chansard N, Duflos A, Hill BT. Characterization of cell death induced by vinflunine, the most recent Vinca alkaloid in clinical development. Br J Cancer. 2002;86:143–150
  40. Estève MA, Carré M, Bourgarel-Rey V, et al. Bcl-2 down-regulation and tubulin subtype composition are involved in resistance of ovarian cancer cells to vinflunine. Mol Cancer Ther. 2006;5:2824–2833
  41. Verrills NM, Walsh BJ, Cobon GS, Hains PG, Kavallaris M. Proteome analysis of vinca alkaloid response and resistance in acute lymphoblastic leukemia reveals novel cytoskeletal alterations. J Biol Chem. 2003;278:45082–45093
  42. Verrills NM, Kavallaris M. Drug resistance mechanisms in cancer cells: a proteomics perspective. Curr Opin Mol Ther. 2003;5:258–265
  43. Sinha P, Hütter G, Köttgen E, Dietel M, Schadendorf D, Lage H. Increased expression of epidermal fatty acid binding protein, cofilin, and 14-3-3-sigma (stratifin) detected by two-dimensional gel electrophoresis, mass spectrometry and microsequencing of drug-resistant human adenocarcinoma of the pancreas. Electrophoresis. 1999;20:2952–2960
  44. Sinha P, Kohl S, Fischer J, et al. Identification of novel proteins associated with the development of chemoresistance in malignant melanoma using two-dimensional electrophoresis. Electrophoresis. 2000;21:3048–3057

 Children's Cancer Institute Australia for Medical Research is affiliated with the University of New South Wales and Sydney Children's Hospital. M.K. is supported by grants and a Career Development Award from the National Health and Medical Research Council (NHMRC).Dr Kavallaris has no conflict of interest to declare. Drs Annereau and Barret are both employees of the Institut de Recherche Pierre Fabre, a private pharmaceutical company supporting the development of vinflunine.

PII: S0093-7754(08)00019-5

doi: 10.1053/j.seminoncol.2008.01.006

Seminars in Oncology
Volume 35 , Pages S22-S27 , June 2008

Article Tools

* Image Usage & Resolution