Class III β-tubulin overexpression in ovarian clear cell and serous carcinoma as a marker for poor overall survival after platinum/taxane chemotherapy and sensitivity to patupilone

American Journal of Obstetrics and Gynecology

Volumn 209, Issue 1, 2013, Pages 62.e1-62.e9

  Roque, Dana M ^a   Bellone, Stefania ^a   Buza, Natalia ^a   Romani, Chiara ^b   Cocco, Emiliano ^a   Bignotti, Eliana ^b   Ravaggi, Antonella ^b   Rutherford, Thomas J ^a   Schwartz, Peter E ^a   Pecorelli, Sergio ^b   Santin, Alessandro D ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BRESCIA   (Italy)

Author keywords

Class III tubulin; Epothilone; Ovarian clear cell carcinoma; Ovarian serous carcinoma; Paclitaxel resistance; Prognostic marker

Indexed keywords

BETA TUBULIN; CLASS III BETA TUBULIN; EPOTHILONE B; MULTIDRUG RESISTANCE PROTEIN; PACLITAXEL; SMALL INTERFERING RNA; T 7402; TAXANE DERIVATIVE; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER PATIENT; CANCER RESISTANCE; CELL VIABILITY; CHEMOSENSITIVITY; CLEAR CELL CARCINOMA; CONTROLLED STUDY; CYSTADENOMA; FEMALE; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IC 50; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; OVARIAN CLEAR CELL CARCINOMA; OVARY CARCINOMA; OVERALL SURVIVAL; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE SECTION; TREATMENT OUTCOME; TUMOR CELL LINE;

EID: 84880132723     PISSN: 00029378     EISSN: 10976868     Source Type: Journal    
DOI: 10.1016/j.ajog.2013.04.017     Document Type: Article

References (54)

1. Seigel R, Naishadham D, Jemal A. Cancer statistics-2012.CA Cancer J Clin 2012;62:10-29.
2. American Cancer Society. Global Cancer Facts and Figures, 2nd edition. Atlanta, GA.
3. Aris A. Endometriosis-associated ovarian cancer: A ten-year cohort study of women living in the Estrie Region of Quebec, Canada. J Ovarian Res 2010;3:2-7.
4. Kennedy AW, Biscotti CV, Hart WR, Webster KD. Ovarian clear cell adenocarcinoma. Gynecol Oncol 1989;32:342-9. (Pubitemid 19074926)
5. Goff BA, Sainz de la Cuesta R, Muntz HG, et al. Clear cell carcinoma of the ovary: A distinct histologic type with poor prognosis and resistance to platinum-based chemotherapy in stage III disease. Gynecol Oncol 1996;60:412-7. (Pubitemid 26077628)
6. Del Carmen MG, Birrer M, Schorge JO. Clear cell carcinoma of the ovary: A review of the literature. Gynecol Oncol 2012;126:481-90.
7. Japanese Gynecologic Cancer Committee. Annual report on Japanese gynecologic cancer committee. Acta Obstet Gynaecol Jpn 2009; 61:936.
8. Hoskins PJ, Le N, Gilks B, et al. Low-stage ovarian clear cell carcinoma: Population-based outcomes in British Columbia, Canada, with evidence for a survival benefit as a result of irradiation. J Clin Oncol 2012;30:1656-62.
9. Chan JK, Teoh D, Hu JM, Shin JY, Osann K, Kapp DS. Do clear cell ovarian carcinomas have poorer prognosis compared to other epithelial cell types? A study of 1411 clear cell ovarian cancers. Gynecol Onicol 2008:370-6.
10. Jenison EL, Montag AG, Griffiths T, et al. Clear cell adenocarcinoma of the ovary: A clinical analysis and comparison with serous carcinoma. Gynecol Oncol 1989;32:65-71. (Pubitemid 19029870)
11. Crotzer DR, Sun CC, Coleman RL, Wolf JK, Levenback CF, Gershenson DM. Lack of effective systemic therapy for recurrent clear cell carcinoma of the ovary. Gynecol Oncol 2007;105:404-8. (Pubitemid 46590333)
12. Pectasides D, Fountzilas G, Aravantinos G, Kalofonos C, Efstathiou H, Farmakis D. Advanced stage clear-cell epithelial ovarian cancer: The Hellenic Cooperative Oncology Group experience. Gynecol Oncol 2006;102:285-91. (Pubitemid 44041640)
13. Behbakht K, Randall TC, Benjamin I, Morgan MA, King S, Rubin SC. Clinical characteristics of clear cell carcinoma of the ovary. Gynecol Oncol 1998;70:255-8. (Pubitemid 28430939)
14. Winter WE, Maxwell L, Tian C, Carlson JW, Ozols RF, Rose PG. Prognostic factors for stage III epithelial ovarian cancer: A Gynecologic Oncology Group study. J Clin Oncol 2007;24: 3621-7. (Pubitemid 47372600)
15. Anglesio M, Carey MS, Köbel M, MacKay H, Huntsman DG, Vancouver Ovarian Clear Cell Symposium Speakers. Clear cell carcinoma of the ovary: A report from the first Ovarian Clear Cell Symposium, June 24th, 2010. Gynecol Oncol 2011;121:407-15.
16. Kajiyama H, Kiyosumi, Suzuki S, Kazuhiko I, Michiyasu K. Survival impact of adjuvant paclitaxel and carboplatin for early-stage ovarian clear-cell carcinoma with complete surgical staging. Gynecol Obstet Invest 2011;72:252-6.
17. Utsunomiya H, Akahira J, Tanno S, et al. Paclitaxel-platinum combination chemotherapy for advanced or recurrent ovarian clear cell adenocarcinoma: A multicenter trial. Int J Gynecol Cancer 2006;16:52-6.
18. Hoskins WJ, Bundy BN, Thigpen JT, Omura GA. The influence of cytoreductive surgery on recurrence-free interval and survival in small volume stage III epithelial ovarian cancer: A Gynecologic Oncology Group study. Gynecol Oncol 1992;47:159-66. (Pubitemid 23001322)
19. 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: 1282-93. (Pubitemid 27386315)
20. Ferlini C, Raspaglio G, Cicchillitti L, et al. Looking at drug resistance mechanisms for microtubule interacting drugs: Does TUBB3 work?CurrCancer Drug Targets 2007;7:704-12.
21. Magnani M, Ortuso F, Soro S, Alcaro S, Tramontano A, Botta M. The b-I/b-III-tubulin isoforms and their complexes with antimitotic agent: Docking and molecular dynamics studies. FEBS J 2006;273:3301-10. (Pubitemid 43990933)
22. Hari M, Yang H, Zeng C, Canizales M, Cabral F. Expression of class III-b tubulin reduces microtubule assembly and confers resistance to paclitaxel. Cell Motil Cytoskeleton 2003;56:45-56. (Pubitemid 37059485)
23. Seve P, Dumontet C, Reiman T. Role of class III b-tubulin in predicting chemoresistance in non-small cell lung cancer. Lung Cancer 2010;67:136-43.
24. Tommasi S, Mangia A, Lacalamita R, et al. Cytoskeleton and paclitaxel sensitivity in breast cancer: The role of b-tubulin s. Int J Cancer 2007;120:2078-85. (Pubitemid 46555844)
25. Sève P, Reiman T, Lai R, et al. Class III b-tubulin is a marker of paclitaxel resistance in carcinomas of unknown primary site. Cancer Chemother Pharmacol 2007;60:27-34. (Pubitemid 46643714)
26. Ferrandina G, Zannoni GF, Matrinelli E, et al. Class III b-tubulin overexpression is a marker of poor clinical outcome in advanced ovarian cancer patients. Clin Cancer Res 2006;12: 2774-9.
27. Ohishi Y, Oda Y, Basaki Y, et al. Expression of beta-tubulin isotypes in human primary ovarian carcinoma. Gynecol Oncol 2007;105: 586-92. (Pubitemid 46734190)
28. Umezu T, Shibata K, Kajiyama H, et al. Taxol resistance among the different histological subtypes of ovarian cancer may be associated with the expression of class III b-tubulin. Int J Gynaecol Pathol 2008;27:207-12. (Pubitemid 351450662)
29. Bollag DM, McQueney PA, Zhu J, et al. Epothilones, a new class of microtubulestabilizing agents with a taxol-like mechanism of action. Cancer Res 1995;55:2325-33.
30. Mozzetti S, Iantomasi R, De Maria I, et al. Molecular mechanisms of patupilone resistance. Cancer Res 2008;68:10197-204.
31. Nobili S, Landini I, Mazzei T, Mini E. Overcoming tumor multidrug resistance using drugs able to evade p-glycoprotein or to exploit its expression. Med Res Rev 2011;32:1220-62.
32. Raspaglio G, Filippetti F, Prislei S, et al. Hypoxia induces class III beta-tubulin gene expression by HIF-1a binding to its 3'-flanking region. Gene 2008;409:100-8.
33. El-Sahwi K, Bellone S, Cocco E, et al. In vitro activity of pertuzumab in combination with trastuzumab in uterine serous papillary adenocarcinoma. Br J Cancer 2010;102: 134-43.
34. Tassi RA, Bignotti E, Rossi E, et al. Overexpression of mammaglobin B in epithelial ovarian carcinomas. Gynecol Oncol 2007;105: 578-85. (Pubitemid 46734187)
35. Roque DM, Bellone S, English DP, et al. Tubulin-b-III overexpression by uterine serous carcinomas is a marker for poor overall survival after platinum/taxane chemotherapy and sensitivity to epothilones. Cancer 2013. Accepted for publication 01/02/2013.
36. Armitage AO. Tumor proliferation rate and response to chemotherapy. Ann Int Med 1992;116:771-3.
37. Borst P, Evers R, Kool M, Wijnholds J. A family of drug transporters: The multidrug resistance-associated proteins. J Natl Cancer Inst 2000;92:1295-302. (Pubitemid 30662093)
38. Goff BA, Ries JA, Els LP, Coltrera MD, Gown AM. Immunophenotype of ovarian cancer as predictor of clinical outcome: Evaluation at primary surgery and second-look procedure. Gynecol Oncol 1998;70:378-85. (Pubitemid 28473638)
39. Itamochi H, Kigawa J, Sugiyama T, Kikuchi Y, Suzuki M, Terakawa N. Low proliferation activity may be associated with chemoresistance in clear cell carcinoma of the ovary. Obstet Gynecol 2002;100:281-7. (Pubitemid 34874791)
40. Itamochi H, Kigawa J, Terakawa N. Mechanisms of chemoresistance and poor prognosis in ovarian clear cell carcinoma. Cancer Sci 2008;99:653-8. (Pubitemid 351448066)
41. Carrara L, Guzzo F, Roque DM, et al. Differential in vitro sensitivity to patupilone versus paclitaxel in uterine and ovarian carcinosarcoma cell lines is linked to tubulin-beta-III expression. Gynecol Oncol 2012;125:231-6.
42. Tian Q, Stepaniants SB, Mao M, et al. Integrated genomic and proteomic analyses of gene expression in mammalian cells. Mol Cell Proteomics 2004;3:960-9. (Pubitemid 40361231)
43. Arao S, Suwa H, Mandai M, et al. Expression of multidrug resistance gene and localization of p-glycoprotein in human primary ovarian cancer. Cancer Res 1994;54:1355-9.
44. Huang KT, Chen YH, Walker AM. Inaccuracies in MTS assays: Major distorting effects of medium, serum albumin, and fatty acids. Bio-Techniques 2004;37:406-12. (Pubitemid 39180914)
45. Wang P, Henning SM, Heber D. Limitations of MTT and MTS-based assays for measurement of antiproliferative activity of green tea polyphenols. PLOS One 2010;5:e10202.
46. Parmar MK, Ledermann JA, Colombo N, et al. Paclitaxel plus platinum-based chemotherapy versus conventional platinum-based chemotherapy in women with relapsed ovarian cancer: The ICON4/AGO-OVAR-2.2 trial. Lancet 2003;361:2099-106.
47. Bystricky B, Chau I. Patupilone in cancer treatment. Expert Opin Investig Drugs 2011;20: 107-17.
48. Colombo N, Kutarska E, Dimopoulos M, et al. Randomized, open-label, phase III study comparing patupilone (EPO906) with pegylated liposomal doxorubicin in platinum-refractory or-resistant patients with recurrent epithelial ovarian, primary fallopian tube, or primary peritoneal cancer. J Clin Oncol 2012;30:3841-7.
49. De Geest K, Blessing JA, Morris RT, et al. Phase II clinical trial of ixabepilone in patients with recurrent or persistent platinum-and taxane-resistant ovarian or primary peritoneal cancer: A Gynecologic Oncology Group study. J Clin Oncol 2009;28:149-53.
50. Rubin EH, Rothermel J, Tesfaye F, et al. Phase I dose-finding study of weekly singleagent patupilone in patients with advanced solid tumors. J Clin Oncol 2005;23:9120-9.
51. Weigland KC, Shah SP, Al-Agha OM, et al. AIRD1A mutations in endometriosis-associated ovarian carcinoma. N Engl J Med 2010;363: 1532-43.
52. Alduaij A, Hansen K, Karim TA, et al. Clear cell carcinomas of the Mullerian system: "does the pathogenesis vary depending on their nuclear grade and their association with endometriosis?" An immunohistochemical analysis. Pathol Res Int 2012;2012:674748.
53. Gan PP, Pasquier E, Kavallaris M. Class III tubulin mediates sensitivity to chemotherapeutic drugs in non-small cell lung cancer. Cancer Res 2007;67:9356-63. (Pubitemid 47535925)
54. Gan PP, McCarroll JA, Bryne FL, Garner J, Kavallaris M. Specific-b-III tubulin isotypes can functionally enhance or diminish epothilone B sensitivity in non-small cell lung cancer cells. PLOS One 2011;6:e217.