Specific β-tubulin isotypes can functionally enhance or diminish epothilone B sensitivity in non-small cell lung cancer cells

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Gan, Pei Pei ^a   McCarroll, Joshua A ^a   Byrne, Frances L ^a   Garner, James ^a   Kavallaris, Maria ^a,b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TUBULIN; BETAII TUBULIN; BETAIII TUBULIN; BETAIVB TUBULIN; CASPASE 3; CASPASE 7; EPOTHILONE B; LIPOCORTIN 5; MEMBRANE PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; EPOTHILONE DERIVATIVE; TUBULIN;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; ENZYME ACTIVITY; GENE EXPRESSION PROFILING; GENE SILENCING; LUNG NON SMALL CELL CANCER; SENSITIVITY ANALYSIS; DRUG EFFECT; DRUG RESISTANCE; GENETICS; HUMAN; METABOLISM; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; EPOTHILONES; HUMANS; TUBULIN;

EID: 79959649836     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021717     Document Type: Article

References (31)

1. Lee JJ, Swain SM, (2008) The epothilones: translating from the laboratory to the clinic. Clin Cancer Res 14: 1618-1624.
2. Lee JJ, Kelly WK, (2009) Epothilones: tubulin polymerization as a novel target for prostate cancer therapy. Nat Clin Pract Oncol 6: 85-92.
3. Lin B, Catley L, LeBlanc R, Mitsiades C, Burger R, et al. (2005) Patupilone (epothilone B) inhibits growth and survival of multiple myeloma cells in vitro and in vivo. Blood 105: 350-357.
4. O'Reilly T, McSheehy PM, Wenger F, Hattenberger M, Muller M, et al. (2005) Patupilone (epothilone B, EPO906) inhibits growth and metastasis of experimental prostate tumors in vivo. Prostate 65: 231-240.
5. Rubin EH, Rothermel J, Tesfaye F, Chen T, Hubert M, et al. (2005) Phase I dose-finding study of weekly single-agent patupilone in patients with advanced solid tumors. J Clin Oncol 23: 9120-9129.
6. Bollag DM, McQueney PA, Zhu J, Hensens O, Koupal L, et al. (1995) Epothilones, a new class of microtubule-stabilizing agents with a taxol-like mechanism of action. Cancer Res 55: 2325-2333.
7. Kowalski RJ, Giannakakou P, Hamel E, (1997) Activities of the microtubule-stabilizing agents epothilones A and B with purified tubulin and in cells resistant to paclitaxel (Taxol(R)). J Biol Chem 272: 2534-2541.
8. Kamath K, Jordan MA, (2003) Suppression of microtubule dynamics by epothilone B is associated with mitotic arrest. Cancer Res 63: 6026-6031.
9. Dumontet C, Jordan MA, Lee FF, (2009) Ixabepilone: targeting betaIII-tubulin expression in taxane-resistant malignancies. Mol Cancer Ther 8: 17-25.
10. Kavallaris M, (2010) Microtubules and resistance to tubulin-binding agents. Nat Rev Cancer 10: 194-204.
11. Giannakakou P, Gussio R, Nogales E, Downing KH, Zaharevitz D, et al. (2000) 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 97: 2904-2909.
12. Mozzetti S, Iantomasi R, De Maria I, Prislei S, Mariani M, et al. (2008) Molecular mechanisms of patupilone resistance. Cancer Res 68: 10197-10204.
13. Verrills NM, Flemming CL, Liu M, Ivery MT, Cobon GS, et al. (2003) Microtubule alterations and mutations induced by desoxyepothilone B: implications for drug-target interactions. Chem Biol 10: 597-607.
14. Yang CP, Verdier-Pinard P, Wang F, Lippaine-Horvath E, He L, et al. (2005) A highly epothilone B-resistant A549 cell line with mutations in tubulin that confer drug dependence. Mol Cancer Ther 4: 987-995.
15. Gan PP, Pasquier E, Kavallaris M, (2007) Class III beta-tubulin mediates sensitivity to chemotherapeutic drugs in non small cell lung cancer. Cancer Res 67: 9356-9363.
16. Gan PP, Kavallaris M, (2008) Tubulin-targeted drug action: functional significance of class ii and class IVb beta-tubulin in vinca alkaloid sensitivity. Cancer Res 68: 9817-9824.
17. Risinger AL, Jackson EM, Polin LA, Helms GL, LeBoeuf DA, et al. (2008) The taccalonolides: microtubule stabilizers that circumvent clinically relevant taxane resistance mechanisms. Cancer Res 68: 8881-8888.
18. Phillips PA, Dudeja V, McCarroll JA, Borja-Cacho D, Dawra RK, et al. (2007) Triptolide induces pancreatic cancer cell death via inhibition of heat shock protein 70. Cancer Res 67: 9407-9416.
19. McCarroll JA, Gan PP, Liu M, Kavallaris M, (2010) betaIII-tubulin is a multifunctional protein involved in drug sensitivity and tumorigenesis in non-small cell lung cancer. Cancer Res 70: 4995-5003.
20. Vansteenkiste J, Lara PN Jr, Le Chevalier T, Breton JL, Bonomi P, et al. (2007) Phase II clinical trial of the epothilone B analog, ixabepilone, in patients with non small-cell lung cancer whose tumors have failed first-line platinum-based chemotherapy. J Clin Oncol 25: 3448-3455.
21. Blade K, Menick DR, Cabral F, (1999) Overexpression of class I, II or IVb beta-tubulin isotypes in CHO cells is insufficient to confer resistance to paclitaxel. J Cell Sci 112: 2213-2221.
22. Seve P, Dumontet C, (2008) Is class III beta-tubulin a predictive factor in patients receiving tubulin-binding agents? Lancet Oncol 9: 168-175.
23. Yang H, Cabral F, (2007) Heightened sensitivity to paclitaxel in Class IVa beta-tubulin-transfected cells is lost as expression increases. J Biol Chem 282: 27058-27066.
24. Nettles JH, Li H, Cornett B, Krahn JM, Snyder JP, et al. (2004) The binding mode of epothilone A on alpha,beta-tubulin by electron crystallography. Science 305: 866-869.
25. Giannakakou P, Sackett DL, Kang YK, Zhan Z, Buters JT, et al. (1997) Paclitaxel-resistant human ovarian cancer cells have mutant beta-tubulins that exhibit impaired paclitaxel-driven polymerization. J Biol Chem 272: 17118-17125.
26. Joe PA, Banerjee A, Luduena RF, (2008) The roles of cys124 and ser239 in the functional properties of human betaIII tubulin. Cell Motil Cytoskeleton 65: 476-486.
27. Freedman H, Huzil JT, Luchko T, Luduena RF, Tuszynski JA, (2009) Identification and characterization of an intermediate taxol binding site within microtubule nanopores and a mechanism for tubulin isotype binding selectivity. J Chem Inf Model 49: 424-436.
28. Magnani M, Ortuso F, Soro S, Alcaro S, Tramontano A, et al. (2006) The betaI/betaIII-tubulin isoforms and their complexes with antimitotic agents. Docking and molecular dynamics studies. Febs J 273: 3301-3310.
29. Gan PP, McCarroll JA, Po'uha ST, Kamath K, Jordan MA, et al. (2010) Microtubule dynamics, mitotic arrest, and apoptosis: drug-induced differential effects of betaIII-tubulin. Mol Cancer Ther 9: 1339-1348.
30. Milross CG, Mason KA, Hunter NR, Chung WK, Peters LJ, et al. (1996) Relationship of mitotic arrest and apoptosis to antitumor effect of paclitaxel [see comments]. Journal of the National Cancer Institute 88: 1308-1314.
31. Khawaja NR, Carre M, Kovacic H, Esteve MA, Braguer D, (2008) Patupilone-induced apoptosis is mediated by mitochondrial reactive oxygen species through Bim relocalization to mitochondria. Mol Pharmacol 74: 1072-1083.