Assessment of topoisomerase II α status in breast cancer by quantitative PCR, gene expression microarrays, immunohistochemistry, and fluorescence in Situ hybridization

American Journal of Pathology

Volumn 178, Issue 4, 2011, Pages 1453-1460

  Romero, Atocha ^a   Martín, Miguel ^b   Cheang, Maggie C U ^c   García Asenjo, José Antonio López ^d   Oliva, Belén ^e   He, Xiaping ^c   De La Hoya, Miguel ^a   Sáenz, Jose Ángel García ^a   Fernández, Manuel Arroyo ^a   Rubio, Eduardo Díaz ^a   Perou, Charles M ^c   Llopis, Trinidad Caldés ^a  

^a HOSPITAL CLÍNICO SAN CARLOS   (Spain)

^b HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d HOSPITAL UNIVERSITARIO PRÍNCIPE DE ASTURIAS   (Spain)

^e Ministry of Environment   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; DNA TOPOISOMERASE (ATP HYDROLYSING); EPIDERMAL GROWTH FACTOR RECEPTOR 2; TOPOISOMERASE 2 ALPHA; UNCLASSIFIED DRUG;

ADJUVANT CHEMOTHERAPY; ADULT; AGED; ARTICLE; BREAST CANCER; BREAST TUMOR; CANCER LOCALIZATION; CELL PROLIFERATION; CLINICAL FEATURE; CLINICAL TRIAL; COHORT ANALYSIS; DIAGNOSTIC TEST ACCURACY STUDY; DISEASE SEVERITY; DNA MICROARRAY; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; NUCLEOTIDE SEQUENCE; PREDICTIVE VALUE; PRIORITY JOURNAL; PROGNOSIS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION;

EID: 79953659342     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2010.12.042     Document Type: Article

References (47)

1. Ryberg M, Nielsen D, Cortese G, Nielsen G, Skovsgaard T, Andersen P: New insight into epirubicin cardiac toxicity: competing risks analysis of 1097 breast cancer patients. J Natl Cancer Inst 2008, 100:1058-1067
2. Diamandidou E, Buzdar AU, Smith TL, Frye D, Witjaksono M, Hortobagyi GN: Treatment-related leukemia in breast cancer patients treated with fluorouracil-doxorubicin-cyclophosphamide combination adjuvant chemotherapy: the University of Texas M.D. Anderson Cancer Center experience. J Clin Oncol 1996, 14:2722-2723
3. Tewey KM, Rowe TC, Yang L, Halligan BD, Liu LF: Adriamycin-induced DNA damage mediated by mammalian DNA topoisomerase II. Science 1984, 226:466-468 (Pubitemid 14012819)
4. Minotti G, Menna P, Salvatorelli E, Cairo G, Gianni L: Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev 2004, 56:185-229 (Pubitemid 38720829)
5. Osheroff N: Biochemical basis for the interaction of type I and type II topoisomerases with DNA. Pharmacol Ther 1989, 41:233-241
6. Wang JC: DNA topoisomerase. Annu Rev Biochem 1996, 58:635-692
7. Davies SM, Robson CN, Davies SL, Hickson ID: Nuclear topoisomerase II levels correlate with the sensitivity of mammalian cells to intercalating agents and epipodophyllotoxins. J Biol Chem 1988, 263:17724-17729 (Pubitemid 19029341)
8. Asano T, An T, Mayes J, Zwelling LA, Kleinerman ES: Transfection of human topoisomerase IIa into etoposide-resistant cells: transient increase in sensitivity followed by down-regulation of the endogenous gene. Biochem J 1996, 319:307-313 (Pubitemid 26394773)
9. Withoff S, Keith WN, Knol AJ, Coutts JC, Hoare SF, Mulder NH, de Vries EG: Selection of a subpopulation with fewer DNA topoisomerase II alpha gene copies in a doxorubicin-resistant cell line panel. Br J Cancer 1996, 74:502-507 (Pubitemid 26279042)
10. Withoff S, de Vries EGE, Keith WN, Nienhuis EF, van der Graaf WT, Uges DR, Mulder NH: Differential expression of DNA topoisomerase II alpha and -beta in P-gp and MRP-negative VM26, mAMSA and mitoxantrone-resistant sublines of the human SCLC cell line GLC4. Br J Cancer 1996, 74:1869-1876 (Pubitemid 27007129)
11. Järvinen TA, Tanner M, Rantanen V, Bärlund M, Borg A, Grénman S, Isola J: Amplification and deletion of topoisomerase II associate with HER-2 amplification and affect sensitivity to topoisomerase II inhibitor doxorubicin in breast cancer. Am J Pathol 2000, 156:839-847 (Pubitemid 30626942)
12. Thor AD, Berry DA, Budman DR, Muss HB, Kute T, Henderson IC, Barcos M, Cirrincione C, Edgerton S, Allred C, Norton L, Liu ET: ErbB-2, p53, and efficacy of adjuvant therapy in lymph node-positive breast cancer. J Natl Cancer Inst 1998, 90:1346-1360 (Pubitemid 28439959)
13. Paik S, Bryant J, Park C, Fisher B, Tan-Chiu E, Hyams D, Fisher ER, Lippman ME, Wickerham DL, Wolmark N: erbB-2 and response to doxorubicin in patients with axillary lymph node-positive, hormone receptor-negative breast cancer. J Natl Cancer Inst 1998, 90:1361-1370 (Pubitemid 28439960)
14. Paik S, Bryant J, Tan-Chiu E, Yothers G, Park C, Wickerham DL, Wolmark N: ERBB2 and choice of adjuvant chemotherapy for invasive breast cancer: National Surgical Adjuvant Breast and Bowel Project Protocol B-15. J Natl Cancer Inst 2000, 92:1991-1998 (Pubitemid 32045895)
15. Pritchard KI, Shepherd LE, O'Malley FP, Andrulis IL, Tu D, Bramwell VH, Levine MN: ERBB2 and responsiveness of breast cancer to adjuvant chemotherapy. N Engl J Med 2006, 354:2103-2111 (Pubitemid 43736610)
16. Gennari A, Sormani MP, Pronzato P, Puntoni M, Colozza M, Pfeffer U, Bruzzi P: ERBB2 status and efficacy of adjuvant anthracyclines in early breast cancer: a pooled analysis of randomized trials. J Natl Cancer Inst 2008, 100:14-20 (Pubitemid 351767337)
17. Petit T, Wilt M, Velten M, Millond R, Rodier JF, Borel C, Mors R, Haegelé P, Eber M, Ghnassia JP: Comparative value of tumour grade, hormonal receptors, Ki-67, HER-2 and topoisomerase II alpha status as predictive markers in breast cancer patients treated with neoadjuvant anthracycline-based chemotherapy. Eur J Cancer 2004, 40:205-211 (Pubitemid 38077022)
18. Sparano JA, Goldstein L, Childs B, Shak S, Brassard D, Badve S, Baehner FL, Bugarini R, Rowley S, Perez E, Shulman LN, Martino S, Davidson NE, Sledge GW, Gray R: Relationship between topoisomerase 2A RNA expression and recurrence after adjuvant chemotherapy for breast cancer. Clin Cancer Res 2009, 15:7693-7700
19. O'Malley FP, Chia S, Tu D, Shepherd LE, Levine MN, Bramwell VH, Andrulis IL, Pritchard KI: Topoisomerase II alpha and responsiveness of breast cancer to adjuvant chemotherapy. J Natl Cancer Inst 2009, 101:644-650
20. Harris LN, Broadwater G, Abu-Khalaf M, Cowan D, Thor AD, Budman D, Cirrincione CT, Berry DA, Winer EP, Hudis CA, Hayes DF, Friedman P, Ellis M, Dressler L: Topoisomerase II{alpha} amplification does not predict benefit from dose-intense cyclophosphamide, doxorubicin, and fluorouracil therapy in ERBB2-amplified early breast cancer: results of CALGB 8541/150013. J Clin Oncol 2009, 27:3430-3436
21. Tuccari G, Rizzo A, Giuffrè G, Barresi G: Immunocytochemical detection of DNA topoisomerase type II in primary breast carcinomas: correlation with clinico-pathological features. Virchows Arch A Pathol Anat Histopathol 1993, 423:51-55 (Pubitemid 23256417)
22. Lynch BJ, Guinee DG Jr, Holden JA: Human DNA topoisomerase II-alpha: a new marker of cell proliferation in invasive breast cancer. Hum Pathol 1997, 28:1180-1188 (Pubitemid 27446604)
23. Nakopoulou L, Lazaris AC, Kavantzas N: DNA topoisomerase II alfa inmunoreactivity as a marker of aggressiveness in invasive breast cancer. Pathobiology 2000, 68:137-143 (Pubitemid 32110322)
24. Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, Davies S, Fauron C, He X, Hu Z, Quackenbush JF, Stijleman IJ, Palazzo J, Marron JS, Nobel AB, Mardis E, Nielsen TO, Ellis MJ, Perou CM, Bernard PS: Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 2009, 27:1160-1167
25. Prat A, Parker JS, Karginova O, Fan C, Livasy C, Herschkowitz JI, He X, Perou CM: Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 2010, 12:R68
26. Kreuzer KA, Lass U, Landt O, Nitsche A, Laser J, Ellerbrok H, Pauli G, Huhn D, Schmidt CA: Highly sensitive and specific fluorescence reverse transcription-PCR assay for pseudogene-free detection of beta-actin transcripts as quantitative reference. Clin Chem 1999, 45:297-300 (Pubitemid 29079135)
27. Elston CW, Ellis IO: Pathological prognostic factors in breast cancer, I: the value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 1991, 19:403-410
28. Hellemans P, van Dan PA, Geysken M, Oosterom AT, Buytaert PH, van Marck E: Immunohistochemical study of topoisomerase II α expression in primary ductal carcinoma of the breast. J Clin Pathol 1995, 48:147-150
29. Järvinen TA, Kononen J, Pelto-Huikko M, Isola J: Expression of topoisomerase II alpha is associated with rapid cell proliferation, aneuploidy, and c-ERBB2 overexpression in breast cancer. Am J Pathol 1996, 148:2073-2082 (Pubitemid 26170530)
30. Boege F, Andersen A, Jensen S, Zeidler R, Kreipe H: Proliferation- associated nuclear antigen ki-64 is identical with topoisomerase IIα: delineation of a carboxyl-terminal epitope with peptide antibodies. Am J Pathol 1996, 146:1302-1308
31. Shvero J, Koren R, Shvili I, Yaniv E, Sadov R, Hadar T: Expression of human DNA topoisomerase II-alpha in squamous cell carcinoma of the larynx and its correlation with clinicopathologic variables. Am J Clin Pathol 2008, 130:934-939
32. Wong N, Yeo W, Wong WL, Wong NL, Chan KY, Mo FK, Koh J, Chan SL, Chan AT, Lai PB, Ching AK, Tong JH, Ng HK, Johnson PJ, To KF: TOP2A overexpression in hepatocellular carcinoma correlates with early age onset, shorter patients survival and chemoresistance. Int J Cancer 2009, 124:644-652
33. Perou CM, Sørlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lønning PE, Børresen-Dale AL, Brown PO, Botstein D: Molecular portraits of human breast tumors. Nature 2000, 406:747-752
34. Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, Karaca G, Troester MA, Tse CK, Edmiston S, Deming SL, Geradts J, Cheang MC, Nielsen TO, Moorman PG, Earp HS, Millikan RC: Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 2006, 295:2492-2502 (Pubitemid 43854964)
35. Rouzier R, Perou CM, Symmans WF, Ibrahim N, Cristofanilli M, Anderson K, Hess KR, Stec J, Ayers M, Wagner P, Morandi P, Fan C, Rabiul I, Ross JS, Hortobagyi GN, Pusztai L: Breast cancer molecular subtypes respond differently to preoperative chemotherapy. Clin Cancer Res 2005, 11:5678-5685 (Pubitemid 41170290)
36. Durbecq V, Paesmans M, Cardoso F, Desmedt C, Di Leo A, Chan S, Friedrichs K, Pinter T, Van Belle S, Murray E, Bodrogi I, Walpole E, Lesperance B, Korec S, Crown J, Simmonds P, Perren JT, Leroy J, Rouas G, Sotiriou C, Piccart M, Larsimon D: Topoisomerase-II alpha expression as a predictive marker in a population of advanced breast cancer patients randomly treated either with single-agent doxorubicin or single-agent docetaxel. Mol Cancer Ther 2004, 3:1207-1214 (Pubitemid 39440165)
37. Di Leo A, Larsimont D, Gancberg D, Jarvinen T, Beauduin M, Vindevoghel A, Michel J, Focan CH, Ries F, Gobert PH, Closon-Dejardin MT, Dolci S, Rouas G, Paesmans M, Lobelle JP, Isola J, Piccart MJ: HER-2 and topo-isomerase IIα as predictive markers in a population of nodepositive breast cancer patients randomly treated with adjuvant CMF or epirubicin plus cyclophosphamide. Ann Oncol 2001, 12:1081-1089 (Pubitemid 32834488)
38. Cardoso F, Di Leo A, Larsimont D, Gancberg D, Rouas G, Dolci S, Ferreira F, Paesmans M, Piccart M: Evaluation of HER-2, p53, bcl-2, topoisomerase II-α, heat shock proteins 27 and 70 in primary breast cancer and metastatic ipsilateral axillary lymph nodes. Ann Oncol 2001, 12:615-620
39. Arriola E, Rodriguez-Pinilla SM, Lambros MB, Jones RL, James M, Savage K, Smith IE, Dowsett M, Reis-Filho JS: Topoisomerase II alpha amplification may predict benefit from adjuvant anthracyclines in HER2 positive early breast cancer. Breast Cancer Res Treat 2007, 106:181-189 (Pubitemid 350045015)
40. Muller RE, Parkers RK, Andrulis I, O'Malley FP: Amplification of the TOP2A gene does not predict high levels of topoisomerase II alpha protein in human breast tumor samples. Genes Chromosomes Cancer 2004, 39:288-297 (Pubitemid 38326310)
41. Olsen KE, Knudsen H, Rasmussen BB, Balslev E, Knoop A, Ejlertsen B, Nielsen KV, Schönau A, Overgaard J; Danish Breast Cancer Co-operative Group: Amplification of ERBB2 and TOP2A and deletion of TOP2A genes in breast cancer investigated by new FISH probes. Acta Oncol 2004, 43:35-42 (Pubitemid 38283171)
42. Knoop AS, Knudsen H, Balslev E, Rasmussen BB, Overgaard J, Nielsen KV, Schonau A, Gunnarsdóttir K, Olsen KE, Mouridsen H, Ejlertsen B; Danish Breast Cancer Cooperative Group: Retrospective analysis of topoisomerase IIa amplifications and deletions as predictive markers in primary breast cancer patients randomly assigned to cyclophosphamide, methotrexate, and fluorouracil or cyclophosphamide, epirubicin, and fluorouracil: Danish Breast Cancer Cooperative Group. J Clin Oncol 2005, 23:7483-7490 (Pubitemid 46291811)
43. Park K, Han S, Gwak GH, Kim HJ, Kim J, Kim KM: Topoisomerase II-alpha gene deletion is not frequent as its amplification in breast cancer. Breast Cancer Res Treat 2006, 98:337-342 (Pubitemid 44195604)
44. Scandinavian Breast Group Trial 9401, Tanner M, Isola J, Wiklund T, Erikstein B, Kellokumpu-Lehtinen P, Malmström P, Wilking N, Nilsson J, Bergh J: Topoisomerase IIalpha gene amplification predicts favorable treatment response to tailored and dose-escalated anthracycline-based adjuvant chemotherapy in HER-2/neu-amplified breast cancer: Scandinavian Breast Group Trial 9401. J Clin Oncol 2006, 24:2428-2436
45. Hannemann J, Kristel P, van Tinteren H, Bontenbal M, van Hoesel QG, Smit WM, Nooij MA, Voest EE, van der Wall E, Hupperets P, de Vries EG, Rodenhuis S, van de Vijver MJ: Molecular subtypes of breast cancer and amplification of topoisomerase IIa: predictive role in dose intensive adjuvant chemotherapy. Br J Cancer 2006, 95:1334-1341 (Pubitemid 44760082)
46. Desmedt C, Azambuja E, Larsimont D, Haibe-Kains FL, Rouas G, Selleslags J, Delaloge S, Duhem C, Kains J-P, Carly B, Maerevoet M, Vindevoghel A, Cardoso F, Durbecq V, Nogaret J-M, Veys I, Scobbens J-C, Noterman D, Salgado R, Di Leo, A, D'Hondt V, Piccart M, Sotiriou C: Predicting the efficacy of anthracyclines in breast cancer (BC): The results of the TOP trial and their validation in the BIG 00-01 trial. Abstract 1893. Presented at the AACR Annual Meeting, April 18-22, 2009, Denver, CO
47. Chia SK, Ung K, Bramwekk VH, Tu D, Perou CM, Ellis MJ, Pernard PS, Vickery T, Shepherd LE, Nielsen TO: Prognostic and Predictive impact of biologic classification by qRT-PCR with a 50-gene subtype predictor (PAM50) for adjuvant tamoxifen in premenopausal breast cancer: Results from the NCIC CTG MA.12 randomized trial. Abstract 508. Presented at the ASCO Annual Meeting, June 4-8, 2010, Chicago, IL