Lung Cancer
Volume 67, Issue 2 , Pages 136-143 , February 2010

The role of βIII tubulin in predicting chemoresistance in non-small cell lung cancer

  • Pascal Sève

      Affiliations

    • Université de Lyon, Lyon F-69008, France
    • INSERM U.590, Lyon F-69008, France
    • Hospices Civils de Lyon, Lyon F-69003, France
    • Corresponding Author InformationCorresponding author at: Department of Internal Medicine, Hospices Civils de Lyon and University Claude Bernard, Lyon, France. Tel.: +33 472 413 300; fax: +33 472 413 121.
  • ,
  • Tony Reiman

      Affiliations

    • Faculty of Medicine, Dalhousie University, Department of Medical Oncology, Saint John Regional Hospital, Saint John, NB, Canada
  • ,
  • Charles Dumontet

      Affiliations

    • Université de Lyon, Lyon F-69008, France
    • INSERM U.590, Lyon F-69008, France
    • Hospices Civils de Lyon, Lyon F-69003, France

Received 7 August 2009 ,Accepted 16 September 2009.

References 

  1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics. CA Cancer J Clin. 2009;59:225–249
  2. Ferlay J, Autier P, Boniol M, Heanue M, Colombet M, Boyle P. Estimates of the cancer incidence and mortality in Europe in 2006. Ann Oncol. 2007;18:581–592
  3. Horner MJ, Ries LAG, Krapcho M, Neyman N, Aminou R, Howlader N, et al., editors. SEER cancer statistics review, 1975–2006. Bethesda, MD: National Cancer Institute; 2009. http://seer.cancer.gov/csr/1975_2006/, based on November 2008 SEER data submission, posted to the SEER web site, 2009.
  4. Arriagada R, Bergman B, Dunant A, Le Chevalier T, Pignon JP, Vansteenkiste J, et al. Cisplatin-based adjuvant chemotherapy in patients with completely resected non-small-cell lung cancer. N Engl J Med. 2004;350:351–360
  5. Douillard JY, Rosell R, De Lena M, Carpagnano F, Ramlau R, Gonzalez-Larriba JL. Adjuvant vinorelbine plus cisplatin versus observation in patients with completely resected stage IB-IIIA non-small-cell lung cancer (Adjuvant Navelbine International Trialist Association [ANITA]): a randomised controlled trial. Lancet Oncol. 2006;7:719–727
  6. Winton T, Livingston R, Johnson D, Rigns J, Johnston M, Butts C, et al. Vinorelbine plus cisplatin vs. observation in resected non-small-cell lung cancer. N Engl J Med. 2005;352:2589–2597
  7. NCCN clinical practice guidelines in oncology non-small cell lung cancer V.2.2009 accessed via http://www.nccn.org/professionals/physician_gls/PDF/nscl.pdf.
  8. Sève P, Dumontet C. Chemoresistance in non-small cell lung cancer. Curr Med Chem Anticancer Agents. 2005;5:73–88
  9. Azuma K, Sasada T, Kawahara A, Takamori S, Hattori S, Ikeda J, et al. Expression of ERCC1 and class III βIII tubulin in non-small cell lung cancer patients treated with carboplatin and paclitaxel. Lung Cancer. 2009;64:326–333
  10. Azuma K, Sasada T, Kawahara A, Hattori S, Kinoshita T, Takamori S, et al. Expression of ERCC1 and class III beta-tubulin in non-small cell lung cancer patients treated with a combination of cisplatin/docetaxel and concurrent thoracic irradiation. Cancer Chemother Pharmacol. 2009;64:565–573
  11. Olaussen KA, Dunant A, Fouret P, Brambilla E, Andre F, Haddad V, et al. DNA repair by ERCC1 in non-small cell lung cancer and cisplatin-based adjuvant chemotherapy. N Engl J Med. 2006;355:983–991
  12. Font A, Sanchez JM, Taron M, Martinez-Balibrea E, Sanchez JJ, Manzano JL, et al. Weekly regimen of irinotecan/docetaxel in previously treated non-small cell lung cancer patients and correlation with uridine diphosphate glucuronosyltransferase 1A1 (UGT1A1) polymorphism. Invest New Drugs. 2003;21:435–443
  13. Han JY, Lim HS, Shin ES, Yoo YK, Park YH, Lee JE, et al. Comprehensive analysis of UGT1A polymorphisms predictive for pharmacokinetics and treatment outcome in patients with non-small-cell lung cancer treated with irinotecan and cisplatin. J Clin Oncol. 2006;24:2237–2244
  14. Rosell R, Danenberg KD, Alberola V, Bepler G, Sanchez JJ, Camps C, et al. Ribonucleotide reductase messenger RNA expression and survival in gemcitabine/cisplatin-treated advanced non-small cell lung cancer patients. Clin Cancer Res. 2004;10:1318–1325
  15. Sève P, Dumontet C. Is class III β-tubulin a predictive factor in patients receiving tubulin-binding agents?. Lancet Oncol. 2008;9:168–175
  16. Sève P, Reiman T, Lai R, Hanson J, Santos C, Johnson L, et al. Class III beta-tubulin is a marker of paclitaxel resistance in carcinomas of unknown primary site. Cancer Chemother Pharmacol. 2007;60:27–34
  17. Jordan MA. Mechanism of action of antitumor drugs that interact with microtubules and tubulin. Curr Med Chem Anticancer Agents. 2002;2:1–17
  18. Dumontet C, Sikic BI. Mechanisms of action and resistance to antitubulin agents: microtubule dynamics, drug transport, and cell death. J Clin Oncol. 1999;17:1061–1070
  19. Jordan MA, Wilson L. Microtubules as a target for anticancer drugs. Nat Rev Cancer. 2004;4:253–265
  20. Monzo M, Rosell R, Sanchez J, Lee JS, O’Brate A, Gonzalez-Larriba JL, et al. Paclitaxel resistance in non-small-cell lung cancer associated with beta-tubulin gene mutations. J Clin Oncol. 1999;17:1786–1793
  21. Burkhart CA, Kavallaris M, Horwitz SB. The role of β-tubulin isotypes in resistance to antimitotic drugs. Biochim Biophys Acta. 2001;1471:1–9
  22. Wehbe H, Kearney CM, Pinney KG. Combretastatin A-4 resistance in H640 human lung carcinomas demonstrates distinctive alterations in β-tubulin isotype expression. Anticancer Res. 2005;25:3865–3870
  23. Kavallaris M, Burkhart CA, Horwitz SB. Antisense oligonucleotides to class III β-tubulin sensitize drug-resistant cells to Taxol. Br J Cancer. 1999;80:1020–1025
  24. Gan PP, Pasquier E, Kavallaris M. Class III (beta)-tubulin mediates sensitivity to chemotherapeutic drugs in non small cell lung cancer. Cancer Res. 2007;67:9356–9363
  25. McCarroll JA, Gan PP, Kavallaris M. Novel role of βIII tubulin in tumorigenesis and drug sensitivity in non-small cell lung cancer. In: Proceedings of the 100th annual meeting of the American association for cancer research. Denver, CO, 2009 April 18–22. Philadelphia (PA). 2009;p. 3337;[Abstract]. Accessed via http://aacrmeetingabstracts.org/
  26. Okuda K, Sasaki H, Dumontet C, Kawano O, Yukiue H, Yokoyama T, et al. Expression of excision repair cross-complementation group 1 and class III βIII tubulin predict survival after chemotherapy for completely resected non-small cell lung cancer. Lung Cancer. 2008;62:105–112
  27. Hayashi Y, Kuriyama H, Umezu H, Tanaka J, Yoshimasu T, Furukawa T, et al. Class III β-tubulin expression in tumor cells is correlated with resistance to docetaxel in patients with completely resected non-small cell lung cancer. Inter Med. 2009;48:203–208
  28. Sève P, Lai R, Ding K, Winton T, Butts C, Mackey J, et al. Class III β-tubulin expression and benefit from adjuvant cisplatin/vinorelbine chemotherapy in operable non-small cell lung cancer: analysis of NCIC JBR.10. Clin Cancer Res. 2007;13:994–999
  29. Rosell R, Scagliotti G, Danenberg KD, Lord RV, Bepler G, Novello S, et al. Transcripts in pretreatment biopsies from a three-arm randomized trial in metastatic non-small-cell lung cancer. Oncogene. 2003;22:3548–3552
  30. Dumontet C, Isaac S, Souquet PJ, Bejui-Thivolet F, Pacheco Y, Peloux N. Expression of class III beta tubulin in non-small cell lung cancer is correlated with resistance to taxane chemotherapy. Bull Cancer. 2005;92:E25–E30
  31. Sève P, Issac S, Tredan O, Souquet PJ, Pacheco Y, Perol M, et al. Expression of class III β-tubulin is predictive of patient outcome in patients with non-small cell lung cancer receiving vinorelbine-based chemotherapy. Clin Cancer Res. 2005;11:5481–5486
  32. Sève P, Mackey J, Isaac S, Tredan O, Souquet PJ, Perol M, et al. Class III β-tubulin expression in tumor cells predicts response and outcome in patients with non-small cell lung cancer receiving paclitaxel. Mol Cancer Ther. 2005;4:2001–2007
  33. Koh Y, Jang B, Lee S, Kim D, Im S, Chung D, et al. Expression of class III beta-tubulin correlates with unfavorable survival outcome in patients with resected non-small cell lung cancer. In: ASCO molecular markers meeting; 2008. p. 69 [Abstract]. Accessed via http://www.asco.org/ASCOv2/Meetings/Abstracts.
  34. Zalcman G, Levallet G, Bergot E, Antoine M, Creveuil C, Brambilla E, et al. Evaluation of class III beta-tubulin (bTubIII) expression as a prognostic marker in patients with resectable non-small cell lung cancer (NSCLC) treated by perioperative chemotherapy (CT) in the phase III trial IFCT-0002. J Clin Oncol. 2009;27(15S):7526;[Abstract]
  35. Reiman T, Sève P, Vataire A, Dunant A, Rosell R, Graziano S, et al. Prognostic value of class III b-tubulin (TUBB3) in operable non-small cell lung cancer (NSCLC) and predictive value for adjuvant cisplatin-based chemotherapy (CT): a validation study on three randomized trials. J Clin Oncol. 2008;26(15S):7506;[Abstract]
  36. Nettles JH, Li H, Cornett B, Krahn JM, Snyder JP, Downing KH. The binding mode of epothilone A on alpha-, beta-tubulin by electron crystallography. Science. 2004;305:866–869
  37. Verrils NM, Flemming CL, Liu M, Ivery MT, Cobon GS, Norris MD, et al. Microtubule alterations and mutations induced by desoxyepothilone B: implications for drug-target interaction. Chem Biol. 2003;10:597–607
  38. Magnini N, Ortuso F, Soro S, Alcaro S, Tramontano A, Botta M, et al. The βI/βIII-tubulin isoforms and their complexes with antimitotic agents. FEBS J. 2006;273:3301–3310
  39. Dumontet C, Jordan MA, Lee FFY. Ixabepilone: targeting βIII-tubulin expression in taxane-resistant malignancies. Mol Cancer Ther. 2009;8:17–25
  40. Mozzetti S, Iantomasi R, De Maria I, Prislei S, Mariani M, Camperchioli A, et al. Molecular mechanisms of patupilone resistance. Cancer Res. 2008;68:10197–10204
  41. Lee FY, Covello KL, Castaneda S, Hawken DR, Kan D, Lewin A, et al. Synergistic antitumor activity of ixabepilone (BMS-247550) plus bevacizumab in multiple in vivo tumor models. Clin Cancer Res. 2008;14(24):8123–8131
  42. Larkin JM, Kaye SB. Potential clinical applications of epothilones: a review of phase II studies. Ann Oncol. 2007;18(Suppl. 5):v28–v34
  43. Perez EA, Lerzo G, Pivot X, Thomas E, Vahdat L, Bosserman L, et al. Efficacy and safety of ixabepilone (BMS-247550) in a phase II study of patients with advanced breast cancer resistant to an anthracycline, a taxane, and capecitabine. J Clin Oncol. 2007;25:3407–3414
  44. Roche H, Yelle L, Cognetti F, Mauriac L, Bunnell C, Sparano J, et al. Phase II clinical trial of Ixabepilone (BMS-247550), an epothilone B analog, as first-line therapy in patients with metastatic breast cancer previously treated with anthracycline chemotherapy. J Clin Oncol. 2007;25:3415–3420
  45. Thomas ES, Gomez HL, Li RK, Cheng HC, Fein LE, Chan VF, et al. Ixabepilone plus capecitabine for metastatic breast cancer progressing after anthracycline and taxane treatment. J Clin Oncol. 2007;25:5210–5217
  46. Thomas E, Tabernero J, Fornier M, Conte P, Fumoleau P, Lluch A, et al. Phase II clinical trial of Ixabepilone (BMS-247550), an epothilone B analog, in patients with taxane-resistant metastatic breast cancer. J Clin Oncol. 2007;25:3399–3406
  47. Vansteenkiste J, Lara PN, Le Chevalier T, Breton JL, Bonomi P, Sandler AB, et al. 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. 2007;25:3448–3455
  48. Sanchez J, Mellemgaard A, Perry M, Zatloukal P, Hamm J, Belani CP, et al. Efficacy and safety of patupilone every 3 weeks in patients with non-small cell lung cancer: a phase I/II trial. J Clin Oncol. 2006;24(18S):7104;[Abstract]
  49. Gatzemeier U, von Pawl J, Eschbach C, Brune A, Wagner A. Phase II trial of the novel epothilone ZK-EPO as second-line therapy in patients with stage IIIB or stage IV non-small-cell lung cancer. EJC Suppl. 2007;5:6568;[Abstract]
  50. Yee L, Lynch T, Villalona-Calero M, Rizvi N, Gabrail N, Sandler A, et al. A phase II study of KOS-862 (Epothilone D) as second-line therapy in non-small cell lung cancer. J Clin Oncol. 2005;23(16S):7127;[Abstract]
  51. Zatloukal P, Mellemgaard A, Sanchez JM, Perry MC, Hamm JT. Activity of patupilone in advanced or metastatic non-small cell lung cancer: a phase II study. Ann Oncol 2008;19(8S):296P. [Abstract].
  52. Abrey LE, Wen P, Govindan R, Reimers H, Rigas JR, Robins HI, et al. Patupilone for the treatment of recurrent/progressive brain metastases in patients (pts) with non-small cell lung cancer (NSCLC): an open-label phase II study. J Clin Oncol. 2008;26(15S):2033;[Abstract]
  53. Ardavanis A, Koumna S, Fragos I, Malliou S, Kyriakou F, Mantzaris I, et al. Erlotinib monotherapy in patients with advanced non-small cell lung cancer: an effective approach with low toxicity. Anticancer Res. 2008;28:2409–2415
  54. Russo F, Bearz A, Pampaloni G Investigators of Italian Pemetrexed Monotherapy of NSCLC Group. Pemetrexed single agent chemotherapy in previously treated patients with locally advanced or metastatic non-small cell lung cancer. BMC Cancer. 2008;8:216
  55. Smit EF, Burgers SA, Biesma B, Smit HJ, Eppinga P, Dingemans AM, et al. Randomized phase II and pharmacogenetic study of pemetrexed compared with pemetrexed plus carboplatin in pretreated patients with advanced non-small cell lung cancer. J Clin Oncol. 2009;27:2038–2045
  56. Zhou ZT, Xu XH, Wei Q, Lu MQ, Wang J, Wen CH. Erlotinib in advanced non-small cell lung cancer after gefitinib failure. Cancer Chemother Pharmacol. 2009;64:1123–1127
  57. Dabholkar M, Vionnet J, Bostick-Bruton F, Yu JJ, Reed E. Messenger RNA levels of XPAC and ERCC1 in ovarian cancer tissue correlate with response to platinum-based chemotherapy. J Clin Invest. 1994;94:703–708
  58. Metzger R, Leichman CG, Danenberg KD, Danenberg PV, Lenz HJ, Hayashi K, et al. ERCC1 mRNA levels complement thymidylate synthase mRNA levels in predicting response and survival for gastric cancer patients receiving combination cisplatin and fluorouracil chemotherapy. J Clin Oncol. 1998;16:309–316
  59. Ceppi P, Volante M, Novello S, Rapa I, Danenberg KD, Danenberg PV, et al. ERCC1 and RRM1 gene expression but not EGFR are predictive of shorter survival in advanced non-small cell lung cancer treated with cisplatin and gemcitabine. Ann Oncol. 2006;17:1818–1825
  60. Lord RV, Brabender J, Gandara D, Alberola V, Camps C, Domine M, et al. Low ERCC1 expression correlates with prolonged survival after cisplatin plus gemcitabine chemotherapy in non-small cell lung cancer. Clin Cancer Res. 2002;8:2286–2291
  61. Cobo M, Isla D, Massuti B, Montes A, Sanchez JM, Provencio M, et al. Customizing cisplatin based on quantitative excision repair cross-complementing 1 mRNA expression: a phase III trial in non-small cell lung cancer. J Clin Oncol. 2007;25:2747–2754
  62. Bepler G, Sharma S, Cantor A, Gautam A, Haura E, Simon G, et al. RRM1 and PTEN as prognostic parameters for overall and disease-free survival in patients with non-small-cell lung cancer. J Clin Oncol. 2004;22:1878–1885
  63. Souglakos J, Boukovinas I, Taron M, Mendez P, Mavroudis D, Tripaki M, et al. Ribonucleotide reductase subunits M1 and M2 mRNA expression levels and clinical outcome of lung adenocarcinoma patients treated with docetaxel/gemcitabine. Br J Cancer. 2008;98:1710–1715
  64. Simon G, Sharma A, Li X, Hazelton T, Walsh F, Williams C, et al. Feasibility and efficacy of molecular analysis-directed individualized therapy in advanced non-small cell lung cancer. J Clin Oncol. 2007;25:2741–2746
  65. Chattopadhyay S, Moran RG, Goldman ID. Pemetrexed: biochemical and cellular pharmacology, mechanisms, and clinical applications. Mol Cancer Ther. 2007;6:404–417
  66. Bepler G, Sommers KE, Cantor A, Li X, Sharma A, Williams C, et al. Clinical efficacy and predictive molecular markers of neoadjuvant gemcitabine and pemetrexed in resectable non-small cell lung cancer. J Thorac Oncol. 2008;3:1112–1118
  67. Quinn JE, James CR, Stewart GE, Mulligan JM, White P, Chang GK, et al. BRCA1 mRNA expression levels predict for overall survival in ovarian cancer after chemotherapy. Clin Cancer Res. 2007;13:7413–7420
  68. Taron M, Rosell R, Felip E, Mendez P, Souglakos J, Ronco MS, et al. BRCA1 mRNA expression levels as an indicator of chemoresistance in lung cancer. Hum Mol Genet. 2004;13:2443–2449
  69. Rosell R, Perez-Roca L, Sanchez JJ, Cobo M, Moran T, Chaib I, et al. Customized treatment in non-small cell lung cancer based on EGFR mutations and BRCA1 mRNA expression. PLoS ONE. 2009;4:e5133
  70. Tsao MS, Zhu C, Ding K, Strumpf D, Pintilie M, Meyerson M, et al. A 15-gene expression signature prognostic for survival and predictive for adjuvant chemotherapy benefit in JBR.10 patients. J Clin Oncol. 2008;26(15S):7510;[Abstract]

PII: S0169-5002(09)00491-7

doi: 10.1016/j.lungcan.2009.09.007

Lung Cancer
Volume 67, Issue 2 , Pages 136-143 , February 2010