Modulating microtubule stability enhances the cytotoxic response of cancer cells to paclitaxel

Cancer Research

Volumn 71, Issue 17, 2011, Pages 5806-5817

  Ahmed, Ahmed Ashour ^a,b,c   Wang, Xiaoyan ^a,d   Lu, Zhen ^a   Goldsmith, Juliet ^b,c   Le, Xiao Feng ^a   Grandjean, Geoffrey ^a   Bartholomeusz, Geoffrey ^a   Broom, Bradley ^a   Bast Jr , Robert C ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d SHANDONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; CASPASE 3; CASPASE 7; PACLITAXEL; SMALL INTERFERING RNA; TUBULIN;

APOPTOSIS; ARTICLE; CANCER CELL; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; GENE IDENTIFICATION; GENE SILENCING; GENETIC SCREENING; HUMAN; HUMAN CELL; MICROSCOPY; MICROTUBULE; MICROTUBULE STABILITY; PRIORITY JOURNAL;

CELL LINE, TUMOR; CYTOTOXINS; DRUG RESISTANCE, NEOPLASM; HUMANS; MICROTUBULES; NEOPLASMS; PACLITAXEL; RNA, SMALL INTERFERING; TUBULIN MODULATORS;

EID: 80052245462     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-0025     Document Type: Article

References (46)

1. Schiff PB, Horwitz SB. Taxol assembles tubulin in the absence of exogenous guanosine 50-triphosphate or microtubule-associated proteins. Biochemistry 1981;20:3247-52.
2. Schiff PB, Horwitz SB. Taxol stabilizes microtubules in mouse fibroblast cells. Proc Natl Acad Sci U S A 1980;77:1561-5. (Pubitemid 10073801)
3. Martin M, Rodriguez-Lescure A, Ruiz A, Alba E, Calvo L, Ruiz-Borrego M, et al. Randomized phase 3 trial of fluorouracil, epirubicin, and cyclophosphamide alone or followed by Paclitaxel for early breast cancer. J Natl Cancer Inst 2008;100:805-14. (Pubitemid 351809668)
4. McGuire WP, Hoskins WJ, Brady MF, Kucera PR, Partridge EE, Look KY, et al. Cyclophosphamide and cisplatin versus paclitaxel and cisplatin: a phase III randomized trial in patients with suboptimal stage III/IV ovarian cancer (from the Gynecologic Oncology Group). Semin Oncol 1996;23:40-7. (Pubitemid 26391379)
5. Nogales E, Wolf SG, Khan IA, Luduena RF, Downing KH. Structure of tubulin at 6.5 A and location of the taxol-binding site. Nature 1995;375:424-7.
6. Horwitz SB. Taxol (paclitaxel): mechanisms of action. Ann Oncol 1994;5 Suppl 6:S3-6.
7. Parness J, Horwitz SB. Taxol binds to polymerized tubulin in vitro. J Cell Biol 1981;91:479-87. (Pubitemid 12215635)
8. Schibler MJ, Cabral F. Taxol-dependent mutants of Chinese hamster ovary cells with alterations in alpha- and beta-tubulin. J Cell Biol 1986;102:1522-31. (Pubitemid 16038095)
9. Cabral F, Abraham I, Gottesman MM. Isolation of a taxol-resistant Chinese hamster ovary cell mutant that has an alteration in alpha-tubulin. Proc Natl Acad Sci U S A 1981;78:4388-91. (Pubitemid 11010207)
10. McCarroll JA, Gan PP, Liu M, Kavallaris M. BetaIII-tubulin is a multi-functional protein involved in drug sensitivity and tumorigenesis in non-small cell lung cancer. Cancer Res 2010;70:4995-5003.
11. Kavallaris M, Kuo DY, Burkhart CA, Regl DL, Norris MD, Haber M, et al. Taxol-resistant epithelial ovarian tumors are associated with altered expression of specific beta-tubulin isotypes. J Clin Invest 1997;100:1282-93. (Pubitemid 27386315)
12. Martello LA, Verdier-Pinard P, Shen HJ, He L, Torres K, Orr GA, et al. Elevated levels of microtubule destabilizing factors in a Taxol-resistant/ dependent A549 cell line with an alpha-tubulin mutation. Cancer Res 2003;63:1207-13. (Pubitemid 36355832)
13. Ahmed AA, Mills AD, Ibrahim AE, Temple J, Blenkiron C, Vias M, et al. The extracellular matrix protein TGFBI induces microtubule stabilization and sensitizes ovarian cancers to paclitaxel. Cancer Cell 2007;12:514-27. (Pubitemid 350199074)
14. Ahmed AA, Lu Z, Jennings NB, Etemadmoghadam D, Capalbo L, Jacamo RO, et al. SIK2 is a centrosome kinase required for bipolar mitotic spindle formation that provides a potential target for therapy in ovarian cancer. Cancer Cell 2010;18:109-21.
15. Broom BM, Sulman EP, Do KA, Edgerton ME. Bagged gene shaving for the robust clustering of high-throughput data. Int J Bioinform Res Appl 2010;6:326-43.
16. Chen PW, Lin SJ, Tsai SC, Lin JH, Chen MR, Wang JT, et al. Regulation of microtubule dynamics through phosphorylation on stathmin by Epstein-Barr virus kinase BGLF4. J Biol Chem 2010;285:10053-63.
17. Manna T, Thrower DA, Honnappa S, Steinmetz MO, Wilson L. Regulation of microtubule dynamic instability in vitro by differentially phosphorylated stathmin. J Biol Chem 2009;284:15640-9.
18. Kojima Y, Miyoshi H, Clevers HC, Oshima M, Aoki M, Taketo MM. Suppression of tubulin polymerization by the LKB1-microtubule-associated protein/microtubule affinity-regulating kinase signaling. J Biol Chem 2007;282:23532-40. (Pubitemid 47311954)
19. Wang JZ, Grundke-Iqbal I, Iqbal K. Kinases and phosphatases and tau sites involved in Alzheimer neurofibrillary degeneration. Eur J Neurosci 2007;25:59-68. (Pubitemid 46098893)
20. Yamamoto H, Yamauchi E, Taniguchi H, Ono T, Miyamoto E. Phosphorylation of microtubule-associated protein tau by Ca2+/calmodulin-dependent protein kinase II in its tubulin binding sites. Arch Biochem Biophys 2002;408:255-62. (Pubitemid 36027047)
21. Drewes G, Ebneth A, Mandelkow EM. MAPs, MARKs and microtubule dynamics. Trends Biochem Sci 1998;23:307-11. (Pubitemid 28461897)
22. Gundersen GG, Bulinski JC. Distribution of tyrosinated and nontyrosinated alpha-tubulin during mitosis. J Cell Biol 1986;102:1118-26. (Pubitemid 16013169)
23. Gundersen GG, Kalnoski MH, Bulinski JC. Distinct populations of microtubules: tyrosinated and nontyrosinated alpha tubulin are distributed differently in vivo. Cell 1984;38:779-89. (Pubitemid 15176108)
24. Amos LA, Schlieper D. Microtubules and maps. Adv Protein Chem 2005;71:257-98. (Pubitemid 41446931)
25. Rouzier R, Rajan R, Wagner P, Hess KR, Gold DL, Stec J, et al. Microtubule-associated protein tau: a marker of paclitaxel sensitivity in breast cancer. Proc Natl Acad Sci U S A 2005;102:8315-20. (Pubitemid 40800086)
26. Kar S, Fan J, Smith MJ, Goedert M, Amos LA. Repeat motifs of tau bind to the insides of microtubules in the absence of taxol. EMBO J 2003;22:70-7. (Pubitemid 36091270)
27. Ahmed AA, Vias M, Iyer NG, Caldas C, Brenton JD. Microarray segmentation methods significantly influence data precision. Nucleic Acids Res 2004;32:e50.
28. Schmid JA, Birbach A. IkappaB kinase beta (IKKbeta/IKK2/IKBKB) - a key molecule in signaling to the transcription factor NF-kappaB. Cytokine Growth Factor Rev 2008;19:157-65. (Pubitemid 351382281)
29. Hacker H, Karin M. Regulation and function of IKK and IKK-related kinases. Sci STKE 2006;2006:re13.
30. Ganta S, Amiji M. Coadministration of Paclitaxel and curcumin in nanoemulsion formulations to overcome multidrug resistance in tumor cells. Mol Pharm 2009;6:928-39.
31. Annunziata CM, Stavnes HT, Kleinberg L, Berner A, Hernandez LF, Birrer MJ, et al. Nuclear factor kappaB transcription factors are coexpressed and convey a poor outcome in ovarian cancer. Cancer 2010;116:3276-84.
32. Zhang D, Qiu L, Jin X, Guo Z, Guo C. Nuclear factor-kappaB inhibition by parthenolide potentiates the efficacy of Taxol in non-small cell lung cancer in vitro and in vivo. Mol Cancer Res 2009;7:1139-49.
33. Jin X, Qiu L, Zhang D, Zhang M, Wang Z, Guo Z, et al. Chemosensitization in non-small cell lung cancer cells by IKK inhibitor occurs via NF-kappaB and mitochondrial cytochrome c cascade. J Cell Mol Med 2009;13:4596-607.
34. Krieg A, Le Negrate G, Reed JC. RIP2-beta: a novel alternative mRNA splice variant of the receptor interacting protein kinase RIP2. Mol Immunol 2009;46:1163-70.
35. Paulsen RD, Cimprich KA. The ATR pathway: fine-tuning the fork. DNA Repair (Amst) 2007;6:953-66.
36. Manfredi JJ, Parness J, Horwitz SB. Taxol binds to cellular microtubules. J Cell Biol 1982;94:688-96. (Pubitemid 13241201)
37. Gimenez-Bonafe P, Tortosa A, Perez-Tomas R. Overcoming drug resistance by enhancing apoptosis of tumor cells. Curr Cancer Drug Targets 2009;9:320-40.
38. Wilson TR, Johnston PG, Longley DB. Anti-apoptotic mechanisms of drug resistance in cancer. Curr Cancer Drug Targets 2009;9:307-19.
39. Ashkenazi A. Directing cancer cells to self-destruct with pro-apoptotic receptor agonists. Nat Rev Drug Discov 2008;7:1001-12.
40. Gascoigne KE, Taylor SS. Cancer cells display profound intra- and interline variation following prolonged exposure to antimitotic drugs. Cancer Cell 2008;14:111-22.
41. Rosen DG, Mercado-Uribe I, Yang G, Bast RC Jr., Amin HM, Lai R, et al. The role of constitutively active signal transducer and activator of transcription 3 in ovarian tumorigenesis and prognosis. Cancer 2006;107:2730-40. (Pubitemid 44845630)
42. Huang S, Chang IS, Lin W, Ye W, Luo RZ, Lu Z, et al. ARHI (DIRAS3), an imprinted tumour suppressor gene, binds to importins and blocks nuclear import of cargo proteins. Biosci Rep 2010;30:159-68.
43. McDermott U, Settleman J. Personalized cancer therapy with selective kinase inhibitors: an emerging paradigm in medical oncology. J Clin Oncol 2009;27:5650-9.
44. Zhuang SH, Hung YE, Hung L, Robey RW, Sackett DL, Linehan WM, et al. Evidence for microtubule target engagement in tumors of patients receiving ixabepilone. Clin Cancer Res 2007;13:7480-6.
45. Gianni L, Kearns CM, Giani A, Capri G, Vigano L, Lacatelli A, et al. Nonlinear pharmacokinetics and metabolism of paclitaxel and its pharmacokinetic/pharmacodynamic relationships in humans. J Clin Oncol 1995;13:180-90.
46. Marchetti P, Urien S, Cappellini GA, Ronzino G, Ficorella C. Weekly administration of paclitaxel: theoretical and clinical basis. Crit Rev Oncol Hematol 2002;44 Suppl:S3-13.