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© 2004 Oxford University Press
ARTICLE |
Mechanisms of Tamoxifen Resistance: Increased Estrogen Receptor-HER2/neu Cross-Talk in ER/HER2–Positive Breast Cancer
Affiliations of authors: The Breast Center (JS, SM, CKO, HW, RS) and the Departments of Medicine (JS, SM, CKO, HW, RS) and Molecular and Cellular Biology (CKO), Baylor College of Medicine, Houston, TX; Cancer and Infection Bioscience, AstraZeneca, Macclesfield, Cheshire, UK (AEW); Department of Cancer Medicine, Imperial College of Science, Technology & Medicine, London, UK (SA)
Correspondence to: Rachel Schiff, PhD, Breast Center, Baylor College of Medicine, One Baylor Plaza, MS 600, Houston, TX 77030 (e-mail: rschiff{at}breastcenter.tmc.edu)
Background: Patients receiving adjuvant tamoxifen whose tumors express high levels of both HER2/neu (HER2) and the estrogen receptor (ER) coactivator AIB1 often develop tamoxifen resistance. We used a breast cancer model system with high expression of AIB1 and HER2 to investigate the possible mechanisms underlying this resistance. Methods: MCF-7 breast cancer cells, which express high levels of AIB1, and a tamoxifen-resistant derivative cell line engineered to overexpress HER2 (MCF-7/HER2-18) were treated with estrogen, tamoxifen, epidermal growth factor (EGF), or heregulin in the absence or presence of the EGF receptor (EGFR) tyrosine kinase inhibitor gefitinib. We analyzed phosphorylation of signaling intermediates by immunoblotting, ER transcriptional activity with reporter gene constructs and immunoblot analysis of endogenous gene products, promoter assembly by chromatin immunoprecipitation (ChIP) assay, and tumor cell growth in vitro by anchorage-independent colony formation and in vivo using xenografts in nude mice. Results: MCF-7/HER2-18 tumors were completely growth inhibited by estrogen deprivation but were growth stimulated by tamoxifen. Molecular cross-talk between the ER and HER2 pathways was increased in the MCF-7/HER-2 cells compared with MCF-7 cells, with cross-phosphorylation and activation of both the ER and the EGFR/HER2 receptors, the signaling molecules AKT and ERK 1,2 mitogen-activated protein kinase (MAPK), and AIB1 itself with both estrogen and tamoxifen treatment. Tamoxifen recruited coactivator complexes (ER, AIB1, CBP, p300) to the ER-regulated pS2 gene promoter in MCF-7/HER2-18 cells and corepressor complexes (NCoR, histone deacetylase 3) in MCF-7 cells. Gefitinib pretreatment blocked receptor cross-talk, reestablished corepressor complexes with tamoxifen-bound ER on target gene promoters, eliminated tamoxifen's agonist effects, and restored its antitumor activity both in vitro and in vivo in MCF-7/HER2-18 cells. Conclusions: Tamoxifen behaves as an estrogen agonist in breast cancer cells that express high levels of AIB1 and HER2, resulting in de novo resistance. Gefitinib's ability to eliminate this cross-talk and to restore tamoxifen's antitumor effects should be tested in the clinic. [J Natl Cancer Inst 2004; 96:926–35]
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- Tamoxifen: Dr. Jekyll and Mr. Hyde?
- Daniel F. Hayes
J Natl Cancer Inst 2004 96: 895-897.[Extract] [Full Text] [PDF]
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V. S. Likhite, F. Stossi, K. Kim, B. S. Katzenellenbogen, and J. A. Katzenellenbogen Kinase-Specific Phosphorylation of the Estrogen Receptor Changes Receptor Interactions with Ligand, Deoxyribonucleic Acid, and Coregulators Associated with Alterations in Estrogen and Tamoxifen Activity Mol. Endocrinol., December 1, 2006; 20(12): 3120 - 3132. [Abstract] [Full Text] [PDF]
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S. Massarweh and R. Schiff Resistance to endocrine therapy in breast cancer: exploiting estrogen receptor/growth factor signaling crosstalk Endocr. Relat. Cancer, December 1, 2006; 13(Supplement_1): S15 - S24. [Abstract] [Full Text] [PDF]
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J M W Gee, V E Shaw, S E Hiscox, R A McClelland, N K Rushmere, and R I Nicholson Deciphering antihormone-induced compensatory mechanisms in breast cancer and their therapeutic implications Endocr. Relat. Cancer, December 1, 2006; 13(Supplement_1): S77 - S88. [Abstract] [Full Text] [PDF]
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G. E. Weitsman, L. Li, G. P. Skliris, J. R. Davie, K. Ung, Y. Niu, L. Curtis-Snell, L. Tomes, P. H. Watson, and L. C. Murphy Estrogen Receptor-{alpha} Phosphorylated at Ser118 Is Present at the Promoters of Estrogen-Regulated Genes and Is Not Altered Due to HER-2 Overexpression. Cancer Res., October 15, 2006; 66(20): 10162 - 10170. [Abstract] [Full Text] [PDF]
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R. Lupu and J. A. Menendez Targeting Fatty Acid Synthase in Breast and Endometrial Cancer: An Alternative to Selective Estrogen Receptor Modulators? Endocrinology, September 1, 2006; 147(9): 4056 - 4066. [Abstract] [Full Text] [PDF]
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S. Massarweh, C. K. Osborne, S. Jiang, A. E. Wakeling, M. Rimawi, S. K. Mohsin, S. Hilsenbeck, and R. Schiff Mechanisms of Tumor Regression and Resistance to Estrogen Deprivation and Fulvestrant in a Model of Estrogen Receptor-Positive, HER-2/neu-Positive Breast Cancer Cancer Res., August 15, 2006; 66(16): 8266 - 8273. [Abstract] [Full Text] [PDF]
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B. Moy and P. E. Goss Estrogen Receptor Pathway: Resistance to Endocrine Therapy and New Therapeutic Approaches. Clin. Cancer Res., August 15, 2006; 12(16): 4790 - 4793. [Abstract] [Full Text] [PDF]
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H. Wu, L. Sun, Y. Zhang, Y. Chen, B. Shi, R. Li, Y. Wang, J. Liang, D. Fan, G. Wu, et al. Coordinated Regulation of AIB1 Transcriptional Activity by Sumoylation and Phosphorylation J. Biol. Chem., August 4, 2006; 281(31): 21848 - 21856. [Abstract] [Full Text] [PDF]
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X. Lin, Y. Yu, H. Zhao, Y. Zhang, J. Manela, and D. A. Tonetti Overexpression of PKC{alpha} is required to impart estradiol inhibition and tamoxifen-resistance in a T47D human breast cancer tumor model Carcinogenesis, August 1, 2006; 27(8): 1538 - 1546. [Abstract] [Full Text] [PDF]
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R. Kim, M. Kaneko, K. Arihiro, M. Emi, K. Tanabe, S. Murakami, A. Osaki, and K. Inai Extranuclear expression of hormone receptors in primary breast cancer Ann. Onc., August 1, 2006; 17(8): 1213 - 1220. [Abstract] [Full Text] [PDF]
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P. D. Ryan and P. E. Goss Adjuvant Hormonal Therapy in Peri- and Postmenopausal Breast Cancer Oncologist, July 1, 2006; 11(7): 718 - 731. [Abstract] [Full Text] [PDF]
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V. C. Jordan Pak up your breast tumor--and grow! J Natl Cancer Inst, May 17, 2006; 98(10): 657 - 659. [Full Text] [PDF]
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W. Xia, S. Bacus, P. Hegde, I. Husain, J. Strum, L. Liu, G. Paulazzo, L. Lyass, P. Trusk, J. Hill, et al. A model of acquired autoresistance to a potent ErbB2 tyrosine kinase inhibitor and a therapeutic strategy to prevent its onset in breast cancer PNAS, May 16, 2006; 103(20): 7795 - 7800. [Abstract] [Full Text] [PDF]
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S. Glaros, N. Atanaskova, C. Zhao, D. F. Skafar, and K. B. Reddy Activation Function-1 Domain of Estrogen Receptor Regulates the Agonistic and Antagonistic Actions of Tamoxifen Mol. Endocrinol., May 1, 2006; 20(5): 996 - 1008. [Abstract] [Full Text] [PDF]
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D. S. Oh, M. A. Troester, J. Usary, Z. Hu, X. He, C. Fan, J. Wu, L. A. Carey, and C. M. Perou Estrogen-Regulated Genes Predict Survival in Hormone Receptor-Positive Breast Cancers J. Clin. Oncol., April 10, 2006; 24(11): 1656 - 1664. [Abstract] [Full Text] [PDF]
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M. P. Goetz, V. J. Suman, J. N. Ingle, A. M. Nibbe, D. W. Visscher, C. A. Reynolds, W. L. Lingle, M. Erlander, X.-J. Ma, D. C. Sgroi, et al. A two-gene expression ratio of homeobox 13 and interleukin-17B receptor for prediction of recurrence and survival in women receiving adjuvant tamoxifen. Clin. Cancer Res., April 1, 2006; 12(7 Pt 1): 2080 - 2087. [Abstract] [Full Text] [PDF]
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R. M. O'Regan, C. Osipo, E. Ariazi, E. S. Lee, K. Meeke, C. Morris, A. Bertucci, M. A.B. Sarker, R. Grigg, and V. C. Jordan Development and therapeutic options for the treatment of raloxifene-stimulated breast cancer in athymic mice. Clin. Cancer Res., April 1, 2006; 12(7): 2255 - 2263. [Abstract] [Full Text] [PDF]
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W. R. Harrington, S. H. Kim, C. C. Funk, Z. Madak-Erdogan, R. Schiff, J. A. Katzenellenbogen, and B. S. Katzenellenbogen Estrogen Dendrimer Conjugates that Preferentially Activate Extranuclear, Nongenomic Versus Genomic Pathways of Estrogen Action Mol. Endocrinol., March 1, 2006; 20(3): 491 - 502. [Abstract] [Full Text] [PDF]
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S. P. Linke, T. M. Bremer, C. D. Herold, G. Sauter, and C. Diamond A Multimarker Model to Predict Outcome in Tamoxifen-Treated Breast Cancer Patients Clin. Cancer Res., February 15, 2006; 12(4): 1175 - 1183. [Abstract] [Full Text] [PDF]
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S. K. Rayala, J. Mascarenhas, R. K. Vadlamudi, and R. Kumar Altered localization of a coactivator sensitizes breast cancer cells to tumor necrosis factor-induced apoptosis. Mol. Cancer Ther., February 1, 2006; 5(2): 230 - 237. [Abstract] [Full Text] [PDF]
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A. E. Gururaj, S. K. Rayala, R. K. Vadlamudi, and R. Kumar Novel Mechanisms of Resistance to Endocrine Therapy: Genomic and Nongenomic Considerations Clin. Cancer Res., February 1, 2006; 12(3): 1001s - 1007s. [Abstract] [Full Text] [PDF]
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I. Shin, T. Miller, and C. L. Arteaga ErbB Receptor Signaling and Therapeutic Resistance to Aromatase Inhibitors Clin. Cancer Res., February 1, 2006; 12(3): 1008s - 1012s. [Abstract] [Full Text] [PDF]
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S. R.D. Johnston Clinical Efforts to Combine Endocrine Agents with Targeted Therapies against Epidermal Growth Factor Receptor/Human Epidermal Growth Factor Receptor 2 and Mammalian Target of Rapamycin in Breast Cancer Clin. Cancer Res., February 1, 2006; 12(3): 1061s - 1068s. [Abstract] [Full Text] [PDF]
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 B. Van Den Bossche, S. Van Belle, F. De Winter, A. Signore, and C. Van de Wiele Early Prediction of Endocrine Therapy Effect in Advanced Breast Cancer Patients Using 99mTc-Depreotide Scintigraphy J. Nucl. Med., January 1, 2006; 47(1): 6 - 13. [Abstract] [Full Text] [PDF]
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N. Normanno, M. Di Maio, E. De Maio, A. De Luca, A. de Matteis, A. Giordano, F. Perrone, and on behalf of the NCI-Naples Breast Cancer Group Mechanisms of endocrine resistance and novel therapeutic strategies in breast cancer Endocr. Relat. Cancer, December 1, 2005; 12(4): 721 - 747. [Abstract] [Full Text] [PDF]
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H. Leong, J. R. Sloan, P. D. Nash, and G. L. Greene Recruitment of Histone Deacetylase 4 to the N-Terminal Region of Estrogen Receptor {alpha} Mol. Endocrinol., December 1, 2005; 19(12): 2930 - 2942. [Abstract] [Full Text] [PDF]
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H. J. Huang, P. Neven, M. Drijkoningen, R. Paridaens, H. Wildiers, E. Van Limbergen, P. Berteloot, F. Amant, I. Vergote, and M. R. Christiaens Hormone receptors do not predict the HER2/neu status in all age groups of women with an operable breast cancer Ann. Onc., November 1, 2005; 16(11): 1755 - 1761. [Abstract] [Full Text] [PDF]
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X. Cui, R. Schiff, G. Arpino, C. K. Osborne, and A. V. Lee Biology of Progesterone Receptor Loss in Breast Cancer and Its Implications for Endocrine Therapy J. Clin. Oncol., October 20, 2005; 23(30): 7721 - 7735. [Abstract] [Full Text] [PDF]
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G. M. Springett, L. Bonham, A. Hummer, I. Linkov, D. Misra, C. Ma, G. Pezzoni, S. Di Giovine, J. Singer, H. Kawasaki, et al. Lysophosphatidic Acid Acyltransferase-{beta} Is a Prognostic Marker and Therapeutic Target in Gynecologic Malignancies Cancer Res., October 15, 2005; 65(20): 9415 - 9425. [Abstract] [Full Text] [PDF]
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A. M. Sieuwerts, M. E. Meijer-van Gelder, M. Timmermans, A. M.A.C. Trapman, R. R. Garcia, M. Arnold, A. J.W. Goedheer, H. Portengen, J. G.M. Klijn, and J. A. Foekens How ADAM-9 and ADAM-11 Differentially From Estrogen Receptor Predict Response to Tamoxifen Treatment in Patients with Recurrent Breast Cancer: a Retrospective Study Clin. Cancer Res., October 15, 2005; 11(20): 7311 - 7321. [Abstract] [Full Text] [PDF]
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A. Goldhirsch, J. H. Glick, R. D. Gelber, A. S. Coates, B. Thurlimann, H.-J. Senn, and and Panel Members Meeting Highlights: International Expert Consensus on the Primary Therapy of Early Breast Cancer 2005 Ann. Onc., October 1, 2005; 16(10): 1569 - 1583. [Abstract] [Full Text] [PDF]
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 F. F. Zheng, R.-C. Wu, C. L. Smith, and B. W. O'Malley Rapid Estrogen-Induced Phosphorylation of the SRC-3 Coactivator Occurs in an Extranuclear Complex Containing Estrogen Receptor Mol. Cell. Biol., September 15, 2005; 25(18): 8273 - 8284. [Abstract] [Full Text] [PDF]
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