Estrogen signaling and the dna damage response in hormone dependent breast cancers

Frontiers in Oncology

Volumn 4 MAY, Issue , 2014, Pages

  Caldon, C E ^a,b  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Brca1; Breast cancer; Ddr; DNA damage response; DNA repair; Estrogen receptor; P53; Tamoxifen

Indexed keywords

ABELSON KINASE; ATM PROTEIN; ATR PROTEIN; BRCA1 PROTEIN; BRCA2 PROTEIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; CLASPIN; DNA DEPENDENT PROTEIN KINASE; DOXORUBICIN; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FANCONI ANEMIA GROUP D2 PROTEIN; PEPTIDES AND PROTEINS; PROTEIN MDM2; PROTEIN P53; PROTEIN TIMELESS; RAD17 PROTEIN; TAMOXIFEN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER PROGNOSIS; CELL CYCLE CHECKPOINT; CELL PROLIFERATION; DNA DAMAGE; DNA REPAIR; HORMONE DEPENDENT BREAST CANCER; HUMAN; NONHUMAN; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

EID: 84904599047     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2014.00106     Document Type: Article

References (92)

1. Yager JD, Davidson NE. Estrogen carcinogenesis in breast cancer. N Engl J Med (2006) 354(3):270-82. doi:10.1056/NEJMra050776
2. Thomas HV, Reeves GK, Key TJ. Endogenous estrogen and postmenopausal breast cancer: a quantitative review. Cancer Causes Control (1997) 8(6):922-8. doi:10.1023/A:1018476631561
3. Musgrove EA, Sutherland RL. Biological determinants of endocrine resistance in breast cancer. Nat Rev Cancer (2009) 9(9):631-43. doi:10.1038/nrc2713
4. Williamson LM, Lees-Miller SP. Estrogen receptor α-mediated transcription induces cell cycle-dependent DNA double-strand breaks. Carcinogenesis (2011) 32(3):279-85. doi:10.1093/carcin/bgq255
5. Liehr JG. Is estradiol a genotoxic mutagenic carcinogen? Endocr Rev (2000) 21(1):40-54. doi:10.1210/er.21.1.40
6. O'Connell P, Pekkel V, Allred DC, Fuqua SAW, Osborne CK, Clark GM. Analysis of loss of heterozygosity in 399 premalignant breast lesions at 15 genetic loci. J Natl Cancer Inst (1998) 90(9):697-703. doi:10.1093/jnci/90.9.697
7. Li JJ, Weroha SJ, Lingle WL, Papa D, Salisbury JL, Li SA. Estrogen mediates aurora-A overexpression, centrosome amplification, chromosomal instability, and breast cancer in female ACI rats. Proc Natl Acad Sci U S A (2004) 101(52):18123-8. doi:10.1073/pnas.0408273101
8. Halazonetis TD, Gorgoulis VG, Bartek J. An oncogene-induced DNA damage model for cancer development. Science (2008) 319(5868):1352-5. doi:10.1126/science.1140735
9. Pallis A, Karamouzis M. DNA repair pathways and their implication in cancer treatment. Cancer Metastasis Rev (2010) 29(4):677-85. doi:10.1007/s10555-010-9258-8
10. Risbridger GP, Davis ID, Birrell SN, Tilley WD. Breast and prostate cancer: more similar than different. Nat Rev Cancer (2010) 10(3):205-12. doi:10.1038/nrc2795
11. Guo X, Yang C, Qian X, Lei T, Li Y, Shen H, et al. Estrogen receptor α regulates ATM expression through miRNAs in breast cancer. Clin Cancer Res (2013) 19(18):4994-5002. doi:10.1158/1078-0432.ccr-12-3700
12. Lewandowski SA, Thiery J, Jalil A, Leclercq G, Szczylik C, Chouaib S. Opposite effects of estrogen receptors alpha and beta on MCF-7 sensitivity to the cytotoxic action of TNF and p53 activity. Oncogene (2005) 24(30):4789-98. doi:10.1038/sj.onc.1208595
13. Thomas C, Strom A, Lindberg K, Gustafsson J-A. Estrogen receptor beta decreases survival of p53-defective cancer cells after DNA damage by impairing G2/M checkpoint signaling. Breast Cancer Res Treat (2011) 127(2):417-27. doi:10.1007/s10549-010-1011-z
14. Meltser V, Ben-Yehoyada M, Shaul Y. c-Abl tyrosine kinase in the DNA damage response: cell death and more. Cell Death Differ (2011) 18(1):2-4. doi:10.1038/cdd.2010.132
15. Pedram A, Razandi M, Evinger AJ, Lee E, Levin ER. Estrogen inhibits ATR signaling to cell cycle checkpoints and DNA repair. Mol Biol Cell (2009) 20(14):3374-89. doi:10.1091/mbc.E09-01-0085
16. Song L, Lin C, Wu Z, Gong H, Zeng Y, Wu J, et al. miR-18a Impairs DNA damage response through downregulation of ataxia telangiectasia mutated (ATM) kinase. PLoS One (2011) 6(9):e25454. doi:10.1371/journal.pone.0025454
17. Goodwin JF, Schiewer MJ, Dean JL, Schrecengost RS, de Leeuw R, Han S, et al. A hormone-DNA repair circuit governs the response to genotoxic insult. Cancer Discov (2013) 3(11):1254-71. doi:10.1158/2159-8290.cd-13-0108
18. Ju B-G, Lunyak VV, Perissi V, Garcia-Bassets I, Rose DW, Glass CK, et al. A topoisomerase IIß-mediated dsDNA break required for regulated transcription. Science (2006) 312(5781):1798-802. doi:10.1126/science.1127196
19. Medunjanin S, Weinert S, Schmeisser A, Mayer D, Braun-Dullaeus RC. Interaction of the double-strand break repair kinase DNA-PK and estrogen receptor-α. Mol Biol Cell (2010) 21(9):1620-8. doi:10.1091/mbc.E09-08-0724
20. Toillon R-A, Magné N, Laïos I, Castadot P, Kinnaert E, Van Houtte P, et al. Estrogens decrease γ-ray-induced senescence and maintain cell cycle progression in breast cancer cells independently of p53. Int J Radiat Oncol Biol Phys (2007) 67(4):1187-200. doi:10.1016/j.ijrobp.2006.11.040
21. Jones LP, Tilli MT, Assefnia S, Torre K, Halama ED, Parrish A, et al. Activation of estrogen signaling pathways collaborates with loss of Brca1 to promote development of ERα-negative and ERα-positive mammary preneoplasia and cancer. Oncogene (2007) 27(6):794-802. doi:10.1038/sj.onc.1210674
22. Rebbeck TR. Prophylactic oophorectomy in BRCA1 and BRCA2 mutation carriers. Eur J Cancer (2002) 38(Suppl 6):15-7. doi:10.1016/S0959-8049(02)00269-1
23. Fan S, Ma YX, Wang C, Yuan RQ, Meng Q, Wang JA, et al. Role of direct interaction in BRCA1 inhibition of estrogen receptor activity. Oncogene (2001) 20(1):77-87. doi:10.1038/sj.onc.1204073
24. Xu J, Fan S, Rosen EM. Regulation of the estrogen-inducible gene expression profile by the breast cancer susceptibility gene BRCA1. Endocrinology (2005) 146(4):2031-47. doi:10.1210/en.2004-0409
25. Ma Y, Fan S, Hu C, Meng Q, Fuqua SA, Pestell RG, et al. BRCA1 regulates acetylation and ubiquitination of estrogen receptor-α. Mol Endocrinol (2010) 24(1):76-90. doi:10.1210/me.2009-0218
26. Razandi M, Pedram A, Rosen EM, Levin ER. BRCA1 inhibits membrane estrogen and growth factor receptor signaling to cell proliferation in breast cancer. Mol Cell Biol (2004) 24(13):5900-13. doi:10.1128/mcb.24.13.5900-5913.2004
27. La Rosa P, Pesiri V, Marino M, Acconcia F. 17β-Estradiol-induced cell proliferation requires estrogen receptor (ER) α monoubiquitination. Cell Signal (2011) 23(7):1128-35. doi:10.1016/j.cellsig.2011.02.006
28. Wang C, Fan S, Li Z, Fu M, Rao M, Ma Y, et al. Cyclin D1 antagonizes BRCA1 repression of estrogen receptor α activity. Cancer Res (2005) 65(15):6557-67. doi:10.1158/0008-5472.can-05-0486
29. Jeffy BD, Hockings JK, Kemp MQ, Morgan SS, Hager JA, Beliakoff J, et al. An estrogen receptor-α/p300 complex activates the BRCA-1 promoter at an AP-1 site that binds Jun/Fos transcription factors: repressive effects of p53 on BRCA-1 transcription. Neoplasia (2005) 7(9):873-82. doi:10.1593/neo.05256
30. Crowe D, Lee M. New role for nuclear hormone receptors and coactivators in regulation of BRCA1-mediated DNA repair in breast cancer cell lines. Breast Cancer Res (2006) 8(1):R1. doi:10.1186/bcr1416
31. Hosey AM, Gorski JJ, Murray MM, Quinn JE, Chung WY, Stewart GE, et al. Molecular basis for estrogen receptor α deficiency in BRCA1-linked breast cancer. J Natl Cancer Inst (2007) 99(22):1683-94. doi:10.1093/jnci/djm207
32. Hurd C, Khattree N, Alban P, Nag K, Jhanwar SC, Dinda S, et al. Hormonal regulation of the p53 tumor suppressor protein in T47D human breast carcinoma cell line. J Biolo Chem (1995) 270(48):28507-10. doi:10.1074/jbc.270.48.28507
33. Hurd C, Khattree N, Dinda S, Alban P, Moudgil VK. Regulation of tumor suppressor proteins, p53 and retinoblastoma, by estrogen and antiestrogens in breast cancer cells. Oncogene (1997) 15(8):991-5. doi:10.1038/sj.onc.1201233
34. Hurd C, Dinda S, Khattree N, Moudgil VK. Estrogen-dependent and independent activation of the P1 promoter of the p53 gene in transiently transfected breast cancer cells. Oncogene (1999) 18(4):1067-72. doi:10.1038/sj.onc.1202398
35. Okumura N, Saji S, Eguchi H, Hayashi S-I, Saji S, Nakashima S. Estradiol stabilizes p53 protein in breast cancer cell line, MCF-7. Cancer Sci (2002) 93(8):867-73. doi:10.1111/j.1349-7006.2002.tb01331.x
36. Molinari AM, Bontempo P, Schiavone EM, Tortora V, Verdicchio MA, Napolitano M, et al. Estradiol induces functional inactivation of p53 by intracellular redistribution. Cancer Res (2000) 60(10):2594-7.
37. Berger C, Qian Y, Chen X. The p53-estrogen receptor loop in cancer. Curr Mol Med (2013) 13(8):1229-40. doi:10.2174/15665240113139990065
38. Konduri SD, Medisetty R, Liu W, Kaipparettu BA, Srivastava P, Brauch H, et al. Mechanisms of estrogen receptor antagonism toward p53 and its implications in breast cancer therapeutic response and stem cell regulation. Proc Natl Acad Sci U S A (2010) 107(34):15081-6. doi:10.1073/pnas.1009575107
39. Bailey ST, Shin H, Westerling T, Liu XS, Brown M. Estrogen receptor prevents p53-dependent apoptosis in breast cancer. Proc Natl Acad Sci U S A (2012) 109(44):18060-5. doi:10.1073/pnas.1018858109
40. Liu G, Schwartz JA, Brooks SC. Estrogen receptor protects p53 from deactivation by human double minute-2. Cancer Res (2000) 60(7):1810-4.
41. Saji S, Okumura N, Eguchi H, Nakashima S, Suzuki A, Toi M, et al. MDM2 enhances the function of estrogen receptor α in human breast cancer cells. Biochem Biophys Res Commun (2001) 281(1):259-65. doi:10.1006/bbrc.2001.4339
42. Brekman A, Singh K, Polotskaia A, Kundu N, Bargonetti J. A p53-independent role of Mdm2 in estrogen-mediated activation of breast cancer cell proliferation. Breast Cancer Res (2011) 13(1):R3. doi:10.1186/bcr2804
43. Duong V, Boulle N, Daujat S, Chauvet J, Bonnet S, Neel H, et al. Differential regulation of estrogen receptor α turnover and transactivation by MDM2 and stress-inducing agents. Cancer Res (2007) 67(11):5513-21. doi:10.1158/0008-5472.can-07-0967
44. Becker KA, Lu S, Dickinson ES, Dunphy KA, Mathews L, Schneider SS, et al. Estrogen and progesterone regulate radiation-induced p53 activity in mammary epithelium through TGF-β-dependent pathways. Oncogene (2005) 24(42):6345-53. doi:10.1038/sj.onc.1208787
45. Shirley SH, Rundhaug JE, Tian J, Cullinan-Ammann N, Lambertz I, Conti CJ, et al. Transcriptional regulation of estrogen receptor-α by p53 in human breast cancer cells. Cancer Res (2009) 69(8):3405-14. doi:10.1158/0008-5472.can-08-3628
46. Liu G, Schwartz JA, Brooks SC. p53 down-regulates ER-responsive genes by interfering with the binding of ER to ERE. Biochem Biophys Res Commun (1999) 264(2):359-64. doi:10.1006/bbrc.1999.1525
47. Lion M, Bisio A, Tebaldi T, De Sanctis V, Menendez D, Resnick MA, et al. Interaction between p53 and estradiol pathways in transcriptional responses to chemotherapeutics. Cell Cycle (2013) 12(8):1211-24. doi:10.4161/cc.24309
48. Díaz-Cruz ES, Furth PA. Deregulated estrogen receptor α and p53 heterozygosity collaborate in the development of mammary hyperplasia. Cancer Res (2010) 70(10):3965-74. doi:10.1158/0008-5472.can-09-3450
49. Schultz-Norton JR, Ziegler YS, Nardulli AM. ERα-associated protein networks. Trends Endocrinol Metab (2011) 22(4):124-9. doi:10.1016/j.tem.2010.11.005
50. Chen D, Lucey MJ, Phoenix F, Lopez-Garcia J, Hart SM, Losson R, et al. T:G mismatch-specific thymine-DNA glycosylase potentiates transcription of estrogen-regulated genes through direct interaction with estrogen receptor α. J Biol Chem (2003) 278(40):38586-92. doi:10.1074/jbc.M304286200
51. Teo AKC, Oh HK, Ali RB, Li BFL. The modified human DNA repair enzyme O 6-methylguanine-DNA methyltransferase is a negative regulator of estrogen receptor-mediated transcription upon alkylation DNA damage. Mol Cell Biol (2001) 21(20):7105-14. doi:10.1128/mcb.21.20.7105-7114.2001
52. Wada-Hiraike O, Yano T, Nei T, Matsumoto Y, Nagasaka K, Takizawa S, et al. The DNA mismatch repair gene hMSH2 is a potent coactivator of oestrogen receptor α. Br J Cancer (2005) 92(12):2286-91. doi:10.1038/sj.bjc.6602614
53. Likhite VS, Cass EI, Anderson SD, Yates JR, Nardulli AM. Interaction of estrogen receptor α with 3-methyladenine DNA glycosylase modulates transcription and DNA repair. J Biol Chem (2004) 279(16):16875-82. doi:10.1074/jbc.M313155200
54. Boulay F, Perdiz D. 17β-estradiol modulates UVB-induced cellular responses in estrogen receptors positive human breast cancer cells. J Photochem Photobiol B (2005) 81(3):143-53. doi:10.1016/j.jphotobiol.2005.05.008
55. Evans MD, Butler JM, Nicoll K, Cooke MS, Lunec J. 17β-oestradiol attenuates nucleotide excision repair. FEBS Lett (2003) 535(1-3):153-8. doi:10.1016/S0014-5793(02)03898-X
56. Curtis CD, Thorngren DL, Ziegler YS, Sarkeshik A, Yates JR, Nardulli AM. Apurinic/apyrimidinic endonuclease 1 alters estrogen receptor activity and estrogen-responsive gene expression. Mol Endocrinol (2009) 23(9):1346-59. doi:10.1210/me.2009-0093
57. Schultz-Norton JR, Walt KA, Ziegler YS, McLeod IX, Yates JR, Raetzman LT, et al. The deoxyribonucleic acid repair protein Flap endonuclease-1 modulates estrogen-responsive gene expression. Mol Endocrinol (2007) 21(7):1569-80. doi:10.1210/me.2006-0519
58. Spillman MA, Bowcock AM. BRCA1 and BRCA2 mRNA levels are coordinately elevated in human breast cancer cells in response to estrogen. Oncogene (1996) 13(8):1639-45.
59. Malone JL, Nelson AC, Lieberman R, Anderson S, Holt JT. Oestrogen-mediated phosphorylation and stabilization of BRCA2 protein in breast. J Pathol (2009) 217(3):380-8. doi:10.1002/path.2458
60. Boutros R, Dozier C, Ducommun B. The when and wheres of CDC25 phosphatases. Curr Opin Cell Biol (2006) 18(2):185-91. doi:10.1016/j.ceb.2006.02.003
61. Ru Lee W, Chen C-C, Liu S, Safe S. 17β-estradiol (E2) induces cdc25A gene expression in breast cancer cells by genomic and non-genomic pathways. J Cell Biochem (2006) 99(1):209-20. doi:10.1002/jcb.20902
62. Caldon CE, Sergio CM, Schutte J, Boersma MN, Sutherland RL, Carroll JS, et al. Estrogen regulation of cyclin E2 requires cyclin D1 but not c-Myc. Mol Cell Biol (2009) 29(17):4623-39. doi:10.1128/mcb.00269-09
63. Caldon CE, Daly RJ, Sutherland RL, Musgrove EA. Cell cycle control in breast cancer cells. J Cell Biochem (2006) 97(2):261-74. doi:10.1002/jcb.20690
64. Roos WP, Kaina B. DNA damage-induced cell death: from specific DNA lesions to the DNA damage response and apoptosis. Cancer Lett (2013) 332(2):237-48. doi:10.1016/j.canlet.2012.01.007
65. Gompel A, Somaï S, Chaouat M, Kazem A, Kloosterboer HJ, Beusman I, et al. Hormonal regulation of apoptosis in breast cells and tissues. Steroids (2000) 65(10-11):593-8. doi:10.1016/S0039-128X(00)00172-0
66. Toillon RA, Magné N, Laïos I, Lacroix M, Duvillier H, Lagneaux L, et al. Interaction between estrogen receptor alpha, ionizing radiation and (anti-) estrogens in breast cancer cells. Breast Cancer Res Treat (2005) 93(3):207-15. doi:10.1007/s10549-005-5148-0
67. Tommiska J, Bartkova J, Heinonen M, Hautala L, Kilpivaara O, Eerola H, et al. The DNA damage signalling kinase ATM is aberrantly reduced or lost in BRCA1/BRCA2-deficient and ER/PR/ERBB2-triple-negative breast cancer. Oncogene (2007) 27(17):2501-6. doi:10.1038/sj.onc.1210885
68. Egawa C, Miyoshi Y, Taguchi T, Tamaki Y, Noguchi S. Quantitative analysis of BRCA1 and BRCA2 mRNA expression in sporadic breast carcinomas and its relationship with clinicopathological characteristics. Jpn J Cancer Res (2001) 92(6):624-30. doi:10.1111/j.1349-7006.2001.tb01140.x
69. Egawa C, Miyoshi Y, Taguchi T, Tamaki Y, Noguchi S. High BRCA2 mRNA expression predicts poor prognosis in breast cancer patients. Int J Cancer (2002) 98(6):879-82. doi:10.1002/ijc.10231
70. He X, Zheng Z, Song T, Wei C, Ma H, Ma Q, et al. c-Abl regulates estrogen receptor α transcription activity through its stabilization by phosphorylation. Oncogene (2010) 29(15):2238-51. doi:10.1038/onc.2009.513
71. Zhao H, Ou-Yang F, Chen IF, Hou MF, Yuan SS, Chang HL, et al. Enhanced resistance to tamoxifen by the c-ABL proto-oncogene in breast cancer. Neoplasia (2010) 12(3):214-23. doi:10.1593/neo.91576
72. Cybulski C, Huzarski T, Byrski T, Gronwald J, Debniak T, Jakubowska A, et al. Estrogen receptor status in CHEK2-positive breast cancers: implications for chemoprevention. Clin Genet (2009) 75(1):72-8. doi:10.1111/j.1399-0004.2008.01111.x
73. Weischer M, Nordestgaard BG, Pharoah P, Bolla MK, Nevanlinna H, Van't Veer LJ, et al. CHEK2*1100delC heterozygosity in women with breast cancer associated with early death, breast cancer-specific death, and increased risk of a second breast cancer. J Clin Oncol (2012) 30(35):4308-16. doi:10.1200/jco.2012.42.7336
74. Verlinden L, Vanden Bempt I, Eelen G, Drijkoningen M, Verlinden I, Marchal K, et al. The E2F-regulated gene Chk1 Is highly expressed in triple-negative estrogen receptor-/progesterone receptor-/HER-2- breast carcinomas. Cancer Res (2007) 67(14):6574-81. doi:10.1158/0008-5472.can-06-3545
75. Groep P, Hoelzel M, Buerger H, Joenje H, Winter J, Diest P. Loss of expression of FANCD2 protein in sporadic and hereditary breast cancer. Breast Cancer Res Treat (2008) 107(1):41-7. doi:10.1007/s10549-007-9534-7
76. Hori M, Shimazaki J, Inagawa S, Itabashi M, Hori M. Overexpression of MDM2 oncoprotein correlates with possession of estrogen receptor alpha and lack of MDM2 mRNA splice variants in human breast cancer. Breast Cancer Res Treat (2002) 71(1):77-84. doi:10.1023/a:1013350419426
77. Miller LD, Smeds J, George J, Vega VB, Vergara L, Ploner A, et al. An expression signature for p53 status in human breast cancer predicts mutation status, transcriptional effects, and patient survival. Proc Natl Acad Sci USA (2005) 102(38):13550-5. doi:10.1073/pnas.0506230102
78. Schultz-Norton JR, Gabisi VA, Ziegler YS, McLeod IX, Yates JR, Nardulli AM. Interaction of estrogen receptor α with proliferating cell nuclear antigen. Nucleic Acids Res (2007) 35(15):5028-38. doi:10.1093/nar/gkm533
79. Kataoka A, Sadanaga N, Mimori K, Ueo H, Barnard GF, Sugimachi K, et al. Overexpression of hRad17 mRNA in human breast cancer: correlation with lymph node metastasis. Clin Cancer Res (2001) 7(9):2815-20.
80. Rakha EA, Reis-Filho JS, Ellis IO. Basal-like breast cancer: a critical review. J Clin Oncol (2008) 26(15):2568-81. doi:10.1200/jco.2007.13.1748
81. Secreto FJ, Monroe DG, Dutta S, Ingle JN, Spelsberg TC. Estrogen receptor α/β isoforms, but not βcx, modulate unique patterns of gene expression and cell proliferation in Hs578T cells. J Cell Biochem (2007) 101(5):1125-47. doi:10.1002/jcb.21205
82. Tozlu-Kara S, Roux V, Andrieu C, Vendrell J, Vacher S, Lazar V, et al. Oligonucleotide microarray analysis of estrogen receptor α-positive postmenopausal breast carcinomas: identification of HRPAP20 and TIMELESS as outstanding candidate markers to predict the response to tamoxifen. J Mol Endocrinol (2007) 39(4):305-18. doi:10.1677/jme-07-0001
83. Going JJ, Nixon C, Dornan ES, Boner W, Donaldson MM, Morgan IM. Aberrant expression of TopBP1 in breast cancer. Histopathology (2007) 50(4):418-24. doi:10.1111/j.1365-2559.2007.02622.x
84. Forma E, Krzeslak A, Bernaciak M, Romanowicz-Makowska H, Brys M. Expression of TopBP1 in hereditary breast cancer. Mol Biol Rep (2012) 39(7):7795-804. doi:10.1007/s11033-012-1622-z
85. Wozniak K, Kolacinska A, Blasinska-Morawiec M, Morawiec-Bajda A, Morawiec Z, Zadrozny M, et al. The DNA-damaging potential of tamoxifen in breast cancer and normal cells. Arch Toxicol (2007) 81(7):519-27. doi:10.1007/s00204-007-0188-3
86. Hemminki K, Rajaniemi H, Lindahl B, Moberger B. Tamoxifen-induced DNA adducts in endometrial samples from breast cancer patients. Cancer Res (1996) 56(19):4374-7.
87. Stearns V, Gelmann EP. Does tamoxifen cause cancer in humans? J Clin Oncol (1998) 16(2):779-92.
88. Berry DA, Cirrincione C, Henderson IC, Citron ML, Budman DR, Goldstein LJ, et al. Estrogen-receptor status and outcomes of modern chemotherapy for patients with node-positive breast cancer. JAMA (2006) 295(14):1658-67. doi:10.1001/jama.295.14.1658
89. Pritchard JE, Dillon PM, Conaway MR, Silva CM, Parsons SJ. A mechanistic study of the effect of doxorubicin/adriamycin on the estrogen response in a breast cancer model. Oncology (2012) 83(6):305-20. doi:10.1159/000341394
90. Sui M, Jiang D, Hinsch C, Fan W. Fulvestrant (ICI 182,780) sensitizes breast cancer cells expressing estrogen receptor α to vinblastine and vinorelbine. Breast Cancer Res Treat (2010) 121(2):335-45. doi:10.1007/s10549-009-0472-4
91. Tokuda E, Seino Y, Arakawa A, Saito M, Kasumi F, Hayashi S-I, et al. Estrogen receptor-α directly regulates sensitivity to paclitaxel in neoadjuvant chemotherapy for breast cancer. Breast Cancer Res Treat (2012) 133(2):427-36. doi:10.1007/s10549-011-1758-x
92. Fernández-Cuesta L, Anaganti S, Hainaut P, Olivier M. Estrogen levels act as a rheostat on p53 levels and modulate p53-dependent responses in breast cancer cell lines. Breast Cancer Res Treat (2011) 125(1):35-42. doi:10.1007/s10549-010-0819-x