Topoisomerase 2 alpha: A real predictor of anthracycline efficacy?

Clinical and Translational Oncology

Volumn 14, Issue 3, 2012, Pages 163-168

  Romero, Atocha ^a   Caldés, Trinidad ^a   Díaz Rubio, Eduardo ^a   Martín, Miguel ^b  

^a HOSPITAL CLÍNICO SAN CARLOS   (Spain)

^b HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

Author keywords

Anthracyclines; Predictive factor; TOP2A; Topoisomerase

Indexed keywords

ANTHRACYCLINE DERIVATIVE; CYCLOPHOSPHAMIDE; DNA TOPOISOMERASE (ATP HYDROLYSING); DOCETAXEL; DOXORUBICIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIRUBICIN; FLUOROURACIL; METHOTREXATE; REACTIVE OXYGEN METABOLITE; TOPOISOMERASE 2 ALPHA; TRASTUZUMAB; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CENTROMERE; CHROMOSOME 17; CHROMOSOME DUPLICATION; COPY NUMBER VARIATION; DRUG EFFICACY; DRUG MEGADOSE; DRUG TARGETING; GENE; GENE AMPLIFICATION; GENE EXPRESSION; HUMAN; OVERALL SURVIVAL; PREDICTIVE VALUE; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; RECURRENCE FREE SURVIVAL; TOPOISOMERASE 2 ALPHA GENE; TUMOR GROWTH;

ANIMALS; ANTHRACYCLINES; ANTIGENS, NEOPLASM; ANTINEOPLASTIC AGENTS; BIOMARKERS, PHARMACOLOGICAL; BREAST NEOPLASMS; CARCINOMA; DNA TOPOISOMERASES, TYPE II; DNA-BINDING PROTEINS; FEMALE; HUMANS; MODELS, BIOLOGICAL; PREDICTIVE VALUE OF TESTS; PROGNOSIS; TREATMENT OUTCOME; TUMOR MARKERS, BIOLOGICAL;

EID: 84860714177     PISSN: 1699048X     EISSN: 16993055     Source Type: Journal    
DOI: 10.1007/s12094-012-0779-1     Document Type: Article

References (74)

1. Tewey KM, Rowe TC, Yang L et al (1984) Adriamycin-induced DNA damage mediated by mammalian DNA topoisomerase II. Science 226:466-468 (Pubitemid 14012819)
2. Early Breast Cancer Trialists' Collaborative Group (EBCTCG) (2005) Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 365:1687-1717
3. Järvinen TA, Kononen J, Pelto-Huikko M, Isola J (1996) Expression of topoisomerase IIalpha is associated with rapid cell proliferation, aneuploidy, and c-erbB2 overexpression in breast cancer. Am J Pathol 148:2073-2082 (Pubitemid 26170530)
4. Wang JC (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol 3:430-440 (Pubitemid 34685700)
5. Osheroff N, Zechiedrich EL, Gale KC (1991) Catalytic function of DNA topoisomerase II. BioEssays 13:269-275 (Pubitemid 121000508)
6. Earnshaw WC, Halligan B, Cooke CA et al (1985) Topoisomerase II is a structural component of mitotic chromosome scaffolds. J Cell Biol 100:1706-1715 (Pubitemid 15099293)
7. Uemura T, Ohkura H, Adachi Y et al (1987) DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50:917-925
8. Brown PO, Cozzarelli NR (1979) A sign inversion mechanism for enzymatic supercoiling of DNA. Science 206:1081-1083 (Pubitemid 10208881)
9. Liu LF, Liu CC, Alberts BM (1980) Type II DNA topoisomerases: enzymes that can unknot a topologically knotted DNA molecule via a reversible double-strand break. Cell 19:697-707 (Pubitemid 10134849)
10. Drake FH, Hofmann GA, Bartus HF et al (1989). Biochemical and pharmacological properties of p170 and p180 forms of topoisomerase II. Biochemistry 28:8154-8160 (Pubitemid 19252897)
11. Goswami PC, Sheren J, Albee LD et al (2000) Cell cycle in coupled variation topoisomerase IIalpha mRNA is regulated by the 30-untranslated region. Possible role of redoxsensitive protein binding in mRNA accumulation. J Biol Chem 275:38384-38392 (Pubitemid 32009162)
12. Christensen MO, Larsen MK, Barthelmes HU et al (2002) Dynamics of human DNA topoisomerases II? and II ß in living cells. J Cell Biol 157:31-44 (Pubitemid 34847828)
13. Sandri MI, Hochhauser D, Ayton P et al (1996) Differential expression of the topoisomerase II? and ß genes in human breast cancer. Br J Cancer 73:1518-1524 (Pubitemid 26235376)
14. Isaacs RJ, Harris AL, Hickson ID (1996) Regulation of the human topoisomerase IIalpha gene promoter in confluence-arrested cells. J Biol Chem 271:16741-16747 (Pubitemid 26239038)
15. Goswami PC, Roti Roti JL, Hunt CR (1996) The cell cycle-coupled expression of topoisomerase IIalpha during S phase is regulated M. by mRNA stability and is disrupted by heat shock or ionizing radiation. Mol Cell Biol 16:1500-1508 (Pubitemid 26095620)
16. Wells NJ, Hickson ID (1995) Human topoisomerase II alpha is phosphorylated in a cell-cycle phase-dependent manner by a proline-directed kinase. Eur J Biochem 231:491-497
17. Carpenter AJ, Porter AC (2004) Construction, characterization, and complementation of a conditional-lethal DNA topoisomerase IIalpha mutant human cell line. Mol Biol Cell 15:5700-5711 (Pubitemid 39564760)
18. Errington F, Willmore E, Tilby MJ et al (1999) Murine transgenic cells lacking DNA topoisomerase IIbeta are resistant to acridines and mitoxantrone: analysis of cytotoxicity and cleavable complex formation. Mol Pharmacol 56:1309-1316
19. Turley H, Comley M, Houlbrook S et al (1997) The distribution and expression of the two isoforms of DNA topoisomerase II in normal and neoplastic human tissues. Br J Cancer 75:1340-1346 (Pubitemid 27179826)
20. McPherson JP, Goldenberg GJ (1998) Induction of apoptosis by deregulated expression of DNA topoisomerase II alpha. Cancer Res 58:4519-4524 (Pubitemid 28480606)
21. Felix CA (1998) Secondary leukemias induced by topoisomerase targeted drugs. Biochim BioPhys Acta 1400:233-255 (Pubitemid 28475107)
22. Wong N, Yeo W, Wong WL et al (2009) TOP2A overexpression in hepatocellular carcinoma correlates with early age onset, shorter patients survival and chemoresistance. Int J Cancer 124:644-652
23. Shvero J, Koren R, Shvili I et al (2008) Expression of human DNA Topoisomerase II-alpha in squamous cell carcinoma of the larynx and its correlation with clinicopathologic variables. Am J Clin Pathol 130:934-939
24. Bredel M, Pollack IF, Hamilton RL et al (2002) DNA topoisomerase II alpha predicts progression free and overall survival in pediatric malignant non-brainstem gliomas. In J Cancer 99:817-820 (Pubitemid 34575698)
25. Nakopoulou L, Lazaris AC, Kavantzas N (2000) DNA topoisomerase II alpha immunoreactivity as a marker of aggressiveness in invasive breast cancer. Pathobiology 68:137-143 (Pubitemid 32110322)
26. Petit T, Wilt M, Velten M et al (2004) Comparative value of tumor 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 40:2005-2211
27. Romero A, Martín M, Cheang MC et al (2011) Assessment of Topoisomerase II ? status in breast cancer by quantitative PCR, gene expression microarrays, immunohistochemistry, and fluorescence in situ hybridization. Am J Pathol 178:1453-1460
28. Parker JS, Mullins M, Cheang MC et al (2009) Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 27:1160-1167
29. Depowski PL, Rosenthal SI, Brien TP et al (2000) Topoisomerase IIalpha expression in breast cancer: correlation with outcome variables. Mod Pathol 13:542-547 (Pubitemid 30332106)
30. Brase JC, Schmidt M, Fischbach T et al (2010) ERBB2 and TOP2A in breast cancer: a comprehensive analysis of gene ampli? cation, RNA levels, and protein expression and their influence on prognosis and prediction. Clin Cancer Res 16:2391-2401
31. Rody A, Karn T, Ruckhäberle E et al (2009) Gene expression of topoisomerase II alpha (TOP2A) by microarray analysis is highly prognostic in estrogen receptor (ER) positive breast cancer. Breast Cancer Res Treat 113:457-466
32. DeAtley SM, Aksenov MY, Aksenova MV et al (1999) Antioxidants protect against reactive oxygen species associated with doxorubicine-treated cardiomyocytes. Cancer Lett 136:41-46 (Pubitemid 29142300)
33. Sarvazyan N (1996) Visualization of doxorubicininduced oxidative stress in isolated cardiac myocytes. Am J Physiol 271:H2079-H2085
34. Ravid A, Rocker D, Machlenkin A et al (1999) 1,25-Dihydroxyvitamin D3 enhances the susceptibility of breast cancer cells to doxorubicin-induced oxidative damage. Cancer Res 59:862-867 (Pubitemid 29086740)
35. Minotti G, Menna P, Salvatorelli E et al (2004) Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev 56:185-229 (Pubitemid 38720829)
36. Ross WE, Glaubiger DL, Kohn KW (1978) Proteinassociated DNA breaks in cells treated with adriamycin or ellipticine. Biochim Biophys Acta 519:23-30 (Pubitemid 8371696)
37. Zwelling LA, Michaels S, Erickson LC et al (1981) Protein-associated deoxyribonucleic acid strand breaks in L1210 cells treated with the deoxyribonucleic acid intercalating agents 4'-(9acridinylamino) methanesulfon-m-anisidide and adriamycin. Biochemistry 20:6553-6563 (Pubitemid 12186507)
38. Tewey KM, Chen GL, Nelson EM, Liu LF (1984) Intercalative antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II. J Biol Chem 259:9182-9187 (Pubitemid 14098903)
39. Davies SM, Robson CN, Davies SL, Hickson ID (1988) Nuclear topoisomerase II levels correlate with the sensitivity of mammalian cells to intercalating agents and epipodophyllotoxins. J Biol Chem 263:17724-17729 (Pubitemid 19029341)
40. Gudkov AV, Zelnick CR, Kazarov AR et al (1993) Isolation of genetic suppressor elements, inducing resistance to topoisomerase II-interactive cytotoxic drugs, from human topoisomerase II cDNA. Proc Natl Acad Sci U S A 90:3231-3235 (Pubitemid 23111339)
41. Mo YY, Ameiss KA, Beck WT (1998) Overexpression of human DNA topoisomerase II alpha by fusion to enhanced green fluorescent protein. Biotechniques 25:1052-1057 (Pubitemid 29005820)
42. Thor AD, Berry DA, Budman DR et al (1998) ErbB-2, p53, and ef? cacy of adjuvant therapy in lymph node-positive breast cancer. J Natl Cancer Inst 90:1346-1360 (Pubitemid 28439959)
43. Paik S, Bryant J, Park C et al (1998) ErbB-2 and response to doxorubicin in patients with axillary lymph node-positive, hormone receptor-negative breast cancer J Natl Cancer Inst 90:1361-1370 (Pubitemid 28439960)
44. Paik S, Bryant J, Tan-Chiu E et al (2000) ERBB2 and choice of adjuvant chemotherapy for invasive breast cancer: National Surgical Adjuvant Breast and Bowel Project Protocol B-15. J Natl Cancer Inst 92:1991-1998 (Pubitemid 32045895)
45. Pritchard KI, Shepherd LE, O'Malley FP et al (2006) ERBB2 and responsiveness of breast cancer to adjuvant chemotherapy. N Engl J Med 354: 2103-2111 (Pubitemid 43736610)
46. Gennari A, Sormani MP, Pronzato P et al (2008) ERBB2 status and ef? cacy of adjuvant anthracyclines in early breast cancer: a pooled analysis of randomized trials. J Natl Cancer Inst 100:14-20 (Pubitemid 351767337)
47. De Laurentiis M, Arpino G, Massarelli E et al (2005) A meta-analysis on the interaction between HER-2 expression and response to endocrine treatment in advanced breast cancer. Clin Cancer Res 11:4741-4748 (Pubitemid 41557193)
48. Bartlett JM, Munro A, Cameron DA et al (2008) Type 1 receptor tyrosine kinase profiles identify patients with enhanced bene? t from anthracyclines in the BR9601 adjuvant breast cancer chemotherapy trial. J Clin Oncol 26:5027-5035
49. Olsen KE, Knudsen H, Rasmussen BB et al; Danish Breast Cancer Co-operative Group (2004) Ampli? cation of ERBB2 and TOP2A and deletion of TOP2A genes in breast cancer investigated by new FISH probes. Acta Oncol 43:35-42 (Pubitemid 38283171)
50. Järvinen TA, Tanner M, Bärlund M et al (1999) Characterization of topoisomerase II alpha gene ampli? cation and deletion in breast cancer. Genes Chromosomes Cancer 26:142-150 (Pubitemid 29416439)
51. Press MF, Sauter G, Buyse M et al (2011) Alteration of topoisomerase II-alpha gene in human breast cancer: association with responsiveness to anthracycline-based chemotherapy. J Clin Oncol 29:859-867
52. Scandinavian Breast Group Trial 9401, Tanner M, Isola J, Wiklund T et al (2006) Topoisomerase II alpha gene ampli? cation predicts favorable treatment response to tailored and dose-escalated anthracycline-based adjuvant chemotherapy in HER-2/ neu-ampli? ed breast cancer: Scandinavian Breast Group Trial 9401. J Clin Oncol 24:2428-2436 (Pubitemid 46630618)
53. Arriola E, Rodriguez-Pinilla SM, Lambros MB et al (2007) Topoisomerase II alpha ampli? cation may predict bene? t from adjuvant anthracyclines in HER2 positive early breast cancer. Breast Cancer Res Treat 106:181-189 (Pubitemid 350045015)
54. Knoop AS, Knudsen H, Balslev E et al; Danish Breast Cancer Cooperative Group (2005) Retrospective analysis of topoisomerase IIa ampli? cations and deletions as predictive markers in primary breast cancer patients randomly assigned to cyclophosphamide, methotrexate, and fluorouracil or cyclophosphamide, epirubicin, and fluorouracil. J Clin Oncol 23:7483-7490 (Pubitemid 46291811)
55. O'Malley FP, Chia S, Tu D et al (2009) Topoisomerase II alpha and responsiveness of breast cancer to adjuvant chemotherapy. J Natl Cancer Inst 101:644-650
56. Harris LN, Broadwater G, Abu-Khalaf M et al (2009) Topoisomerase II {alpha} amplification does not predict bene? t from dose-intense cyclophosphamide, doxorubicin, and fluorouracil therapy in ERBB2-ampli? ed early breast cancer: results of CALGB 8541/150013. J Clin Oncol 27:3430-3436
57. Hannemann J, Kristel P, van Tinteren H et al (2006) Molecular subtypes of breast cancer and ampli? cation of topoisomerase IIa: predictive role in dose intensive adjuvant chemotherapy. Br J Cancer 95:1334-1341 (Pubitemid 44760082)
58. Bartlett JM, Munro AF, Dunn JA et al (2010) Predictive markers of anthracycline benefit: a prospectively planned analysis of the UK National Epirubicin Adjuvant Trial (NEAT/BR9601). Lancet Oncol 11:266-274
59. Di Leo A, Isola J, Piette F et al (2008) A metaanalysis of phase III trials evaluating the predictive value of HER2 and topoisomerase II alpha in early breast cancer patients treated with CMF or anthracyclines-based adjuvant therapy. Presented at the 31st Annual San Antonio Breast Cancer Symposium, 10-14 December, 2008, San Antonio, TX, abstr 705
60. Di Leo A, Desmedt C, Bartlett JMS et al (2011) HER2 and TOP2A as predictive markers for anthracycline-containing chemotherapy regimens as adjuvant treatment of breast cancer: a meta-analysis of individual patient data. Lancet Oncol 12:1134-1142
61. Järvinen TA, Holli K, Kuukasjärvi T, Isola JJ (1998). Predictive value of topoisomerase IIalpha and other prognostic factors for epirubicin chemotherapy in advanced breast cancer. Br J Cancer 77:2267-2273 (Pubitemid 28263952)
62. Petit T, Wilt M, Velten M et al (2004) 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 40:205-211 (Pubitemid 38077022)
63. Desmedt C, Di Leo A, de Azambuja E et al (2011) Multifactorial approach to predicting resistance to anthracyclines. J Clin Oncol 29:1578-1586
64. G Estevez L, Fortes JL, Adrover E et al (2009) Doxorubicin and cyclophosphamide followed by weekly docetaxel as neoadjuvant treatment of early breast cancer: analysis of biological markers in a GEICAM phase II study. Clin Transl Oncol 11:54-59
65. Durbecq V, Paesmans M, Cardoso F et al (2004) 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 3:1207-1214 (Pubitemid 39440165)
66. Brase JC, Schmidt M, Fischbach T et al (2010) ERBB2 and TOP2A in breast cancer: a comprehensive analysis of gene ampli? cation, RNA levels, and protein expression and their influence on prognosis and prediction. Clin Cancer Res 16:2391-2401
67. O'Malley FP, Chia S, Tu D et al (2011) Topoisomerase II alpha protein and responsiveness of breast cancer to adjuvant chemotherapy with CEF compared to CMF in the NCIC CTG randomized MA.5 adjuvant trial. Breast Cancer Res Treat 128:401-409
68. Fritz P, Cabrera CM, Dippon J et al (2005) cerbB2 and topoisomerase IIalpha protein expression independently predict poor survival in primary human breast cancer: a retrospective study. Breast Cancer Res 7:R374-384
69. Sparano JA, Goldstein LJ, Childs BH et al (2009) Relationship between topoisomerase 2A RNA expression and recurrence after adjuvant chemotherapy for breast cancer. Clin Cancer Res 15: 7693-7700
70. Martin M, Romero A, Cheang MC et al (2011) Genomic predictors of response to doxorubicin versus docetaxel in primary breast cancer. Breast Cancer Res Treat 128:127-136
71. Prat A, Parker JS, Karginova O et al (2010) Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 12:R68
72. Carey LA, Perou CM, Livasy CA et al (2006) Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 295:2492-2502 (Pubitemid 43854964)
73. Rouzier R, Perou CM, Symmans WF et al (2005) Breast cancer molecular subtypes respond differently to preoperative chemotherapy. Clin Cancer Res 11:5678-5685 (Pubitemid 41170290)
74. Symmans WF, Peintinger F, Hatzis C et al (2007) Measurement of residual breast cancer burden to predict survival after neoadjuvant chemotherapy. J Clin Oncol 25:4414-4422 (Pubitemid 350013847)