The development, application and limitations of breast cancer cell lines to study tamoxifen and aromatase inhibitor resistance

Journal of Steroid Biochemistry and Molecular Biology

Volumn 131, Issue 3-5, 2012, Pages 83-92

  Wong, Cynthie ^a   Chen, Shiuan ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

Aromatase inhibitors; Endocrine resistance; Models; Tamoxifen

Indexed keywords

4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; ALVESPIMYCIN; ANASTROZOLE; AROMATASE INHIBITOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN; ESTROGEN RECEPTOR; EXEMESTANE; FULVESTRANT; GEFITINIB; HORMONE RECEPTOR; INTERFERON REGULATORY FACTOR 1; LAPATINIB; LETROZOLE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROGESTERONE RECEPTOR; PROTEIN BCL 2; PROTEIN BCL W; PROTEIN KINASE B; RAF PROTEIN; TAMOXIFEN; TRANSCRIPTION FACTOR RELA; TRASTUZUMAB; UNINDEXED DRUG; WNT PROTEIN;

APOPTOSIS; BREAST CANCER; BREAST METASTASIS; CANCER CELL CULTURE; CANCER COMBINATION CHEMOTHERAPY; CANCER GROWTH; CANCER HORMONE THERAPY; CANCER MODEL; CANCER PATIENT; CANCER RESISTANCE; CELL PROLIFERATION; CROSS RESISTANCE; ESTROGEN SYNTHESIS; GENE EXPRESSION PROFILING; HUMAN; MICROARRAY ANALYSIS; NONHUMAN; POSTMENOPAUSE; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS, HORMONAL; AROMATASE INHIBITORS; BREAST NEOPLASMS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; SELECTIVE ESTROGEN RECEPTOR MODULATORS; TAMOXIFEN; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84862900458     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2011.12.005     Document Type: Review

References (90)

1. S. Nilsson, S. Makela, E. Treuter, M. Tujague, J. Thomsen, G. Andersson, E. Enmark, K. Pettersson, M. Warner, and J.A. Gustafsson Mechanisms of estrogen action Physiol. Rev. 81 2001 1535 1565
2. G.G. Kuiper, E. Enmark, M. Pelto-Huikko, S. Nilsson, and J.A. Gustafsson Cloning of a novel receptor expressed in rat prostate and ovary Proc. Natl. Acad. Sci. U.S.A. 93 1996 5925 5930
3. S. Mosselman, J. Polman, and R. Dijkema ER beta: identification and characterization of a novel human estrogen receptor FEBS Lett. 392 1996 49 53
4. B. Hanstein, S. Djahansouzi, P. Dall, M.W. Beckmann, and H.G. Bender Insights into the molecular biology of the estrogen receptor define novel therapeutic targets for breast cancer Eur. J. Endocrinol. 150 2004 243 255
5. D.J. Slamon, G.M. Clark, S.G. Wong, W.J. Levin, A. Ullrich, and W.L. McGuire Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene Science 235 1987 177 182
6. W.D. Foulkes, I.E. Smith, and J.S. Reis-Filho Triple-negative breast cancer N. Engl. J. Med. 363 2010 1938 1948
7. J.M. Esteban, Z. Warsi, M. Haniu, P. Hall, J.E. Shively, and S. Chen Detection of intratumoral aromatase in breast carcinomas. An immunohistochemical study with clinicopathologic correlation Am. J. Pathol. 140 1992 337 343
8. W.R. Miller, and J. O'Neill The importance of local synthesis of estrogen within the breast Steroids 50 1987 537 548
9. S.E. Bulun, T.M. Price, J. Aitken, M.S. Mahendroo, and E.R. Simpson A link between breast cancer and local estrogen biosynthesis suggested by quantification of breast adipose tissue aromatase cytochrome P450 transcripts using competitive polymerase chain reaction after reverse transcription J. Clin. Endocrinol. Metab. 77 1993 1622 1628
10. N. Harada Aberrant expression of aromatase in breast cancer tissues J. Steroid Biochem. Mol. Biol. 61 1997 175 184
11. D. Zhou, and S. Chen Identification and characterization of a cAMP-responsive element in the region upstream from promoter 1.3 of the human aromatase gene Arch. Biochem. Biophys. 371 1999 179 190
12. M. Baum, A.U. Budzar, J. Cuzick, J. Forbes, J.H. Houghton, J.G. Klijn, and T. Sahmoud Anastrozole alone or in combination with tamoxifen versus tamoxifen alone for adjuvant treatment of postmenopausal women with early breast cancer: first results of the ATAC randomised trial Lancet 359 2002 2131 2139
13. A. Howell, J. Cuzick, M. Baum, A. Buzdar, M. Dowsett, J.F. Forbes, G. Hoctin-Boes, J. Houghton, G.Y. Locker, and J.S. Tobias Results of the ATAC (Arimidex, Tamoxifen, Alone or in Combination) trial after completion of 5 years' adjuvant treatment for breast cancer Lancet 365 2005 60 62
14. M. Dowsett, I.E. Smith, S.R. Ebbs, J.M. Dixon, A. Skene, C. Griffith, I. Boeddinghaus, J. Salter, S. Detre, M. Hills, S. Ashley, S. Francis, and G. Walsh Short-term changes in Ki-67 during neoadjuvant treatment of primary breast cancer with anastrozole or tamoxifen alone or combined correlate with recurrence-free survival Clin. Cancer Res. 11 2005 951s 958s
15. A.S. Coates, A. Keshaviah, B. Thurlimann, H. Mouridsen, L. Mauriac, J.F. Forbes, R. Paridaens, M. Castiglione-Gertsch, R.D. Gelber, M. Colleoni, I. Lang, L. Del Mastro, I. Smith, J. Chirgwin, J.M. Nogaret, T. Pienkowski, A. Wardley, E.H. Jakobsen, K.N. Price, and A. Goldhirsch Five years of letrozole compared with tamoxifen as initial adjuvant therapy for postmenopausal women with endocrine-responsive early breast cancer: update of study BIG 1-98 J. Clin. Oncol. 25 2007 486 492
16. D.J. Zhou, D. Pompon, and S.A. Chen Stable expression of human aromatase complementary DNA in mammalian cells: a useful system for aromatase inhibitor screening Cancer Res. 50 1990 6949 6954
17. S. Masri, S. Phung, X. Wang, X. Wu, Y.C. Yuan, L. Wagman, and S. Chen Genome-wide analysis of aromatase inhibitor-resistant, tamoxifen-resistant, and long-term estrogen-deprived cells reveals a role for estrogen receptor Cancer Res. 68 2008 4910 4918
18. M.M. Gottardis, S.P. Robinson, P.G. Satyaswaroop, and V.C. Jordan Contrasting actions of tamoxifen on endometrial and breast tumor growth in the athymic mouse Cancer Res. 48 1988 812 815
19. V.C. Jordan, E. Phelps, and J.U. Lindgren Effects of anti-estrogens on bone in castrated and intact female rats Breast Cancer Res. Treat. 10 1987 31 35
20. V.C. Jordan Selective estrogen receptor modulation: concept and consequences in cancer Cancer Cell 5 2004 207 213
21. H. Nawata, D. Bronzert, and M.E. Lippman Isolation and characterization of a tamoxifen-resistant cell line derived from MCF-7 human breast cancer cells J. Biol. Chem. 256 1981 5016 5021
22. J.M. Knowlden, I.R. Hutcheson, H.E. Jones, T. Madden, J.M. Gee, M.E. Harper, D. Barrow, A.E. Wakeling, and R.I. Nicholson Elevated levels of epidermal growth factor receptor/c-erbB2 heterodimers mediate an autocrine growth regulatory pathway in tamoxifen-resistant MCF-7 cells Endocrinology 144 2003 1032 1044
23. N. Brunner, T.L. Frandsen, C. Holst-Hansen, M. Bei, E.W. Thompson, A.E. Wakeling, M.E. Lippman, and R. Clarke MCF7/LCC2: a 4-hydroxytamoxifen resistant human breast cancer variant that retains sensitivity to the steroidal antiestrogen ICI 182,780 Cancer Res. 53 1993 3229 3232
24. A.E. Lykkesfeldt, M.W. Madsen, and P. Briand Altered expression of estrogen-regulated genes in a tamoxifen-resistant and ICI 164,384 and ICI 182,780 sensitive human breast cancer cell line, MCF-7/TAMR-1 Cancer Res. 54 1994 1587 1595
25. S. Massarweh, C.K. Osborne, C.J. Creighton, L. Qin, A. Tsimelzon, S. Huang, H. Weiss, M. Rimawi, and R. Schiff Tamoxifen resistance in breast tumors is driven by growth factor receptor signaling with repression of classic estrogen receptor genomic function Cancer Res. 68 2008 826 833
26. S. Meng, D. Tripathy, S. Shete, R. Ashfaq, B. Haley, S. Perkins, P. Beitsch, A. Khan, D. Euhus, C. Osborne, E. Frenkel, S. Hoover, M. Leitch, E. Clifford, E. Vitetta, L. Morrison, D. Herlyn, L.W. Terstappen, T. Fleming, T. Fehm, T. Tucker, N. Lane, J. Wang, and J. Uhr HER-2 gene amplification can be acquired as breast cancer progresses Proc. Natl. Acad. Sci. U.S.A. 101 2004 9393 9398
27. A. Lipton, K. Leitzel, S.M. Ali, L. Demers, H.A. Harvey, H.A. Chaudri-Ross, D. Evans, R. Lang, W. Hackl, P. Hamer, and W. Carney Serum HER-2/neu conversion to positive at the time of disease progression in patients with breast carcinoma on hormone therapy Cancer 104 2005 257 263
28. R.A. Campbell, P. Bhat-Nakshatri, N.M. Patel, D. Constantinidou, S. Ali, and H. Nakshatri Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor alpha: a new model for anti-estrogen resistance J. Biol. Chem. 276 2001 9817 9824
29. Y.L. Chung, M.L. Sheu, S.C. Yang, C.H. Lin, and S.H. Yen Resistance to tamoxifen-induced apoptosis is associated with direct interaction between Her2/neu and cell membrane estrogen receptor in breast cancer Int. J. Cancer 97 2002 306 312
30. C.C. Benz, G.K. Scott, J.C. Sarup, R.M. Johnson, D. Tripathy, E. Coronado, H.M. Shepard, and C.K. Osborne Estrogen-dependent, tamoxifen-resistant tumorigenic growth of MCF-7 cells transfected with HER2/neu Breast Cancer Res. Treat. 24 1992 85 95
31. R.J. Pietras, J. Arboleda, D.M. Reese, N. Wongvipat, M.D. Pegram, L. Ramos, C.M. Gorman, M.G. Parker, M.X. Sliwkowski, and D.J. Slamon HER-2 tyrosine kinase pathway targets estrogen receptor and promotes hormone-independent growth in human breast cancer cells Oncogene 10 1995 2435 2446
32. P. Le Goff, M.M. Montano, D.J. Schodin, and B.S. Katzenellenbogen Phosphorylation of the human estrogen receptor. Identification of hormone-regulated sites and examination of their influence on transcriptional activity J. Biol. Chem. 269 1994 4458 4466
33. S.F. Arnold, D.P. Vorojeikina, and A.C. Notides Phosphorylation of tyrosine 537 on the human estrogen receptor is required for binding to an estrogen response element J. Biol. Chem. 270 1995 30205 30212
34. S. Kato, H. Endoh, Y. Masuhiro, T. Kitamoto, S. Uchiyama, H. Sasaki, S. Masushige, Y. Gotoh, E. Nishida, H. Kawashima, D. Metzger, and P. Chambon Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase Science 270 1995 1491 1494
35. D. Szapary, Y. Huang, and S.S. Simons Jr. Opposing effects of corepressor and coactivators in determining the dose-response curve of agonists, and residual agonist activity of antagonists, for glucocorticoid receptor-regulated gene expression Mol. Endocrinol. 13 1999 2108 2121
36. S.L. Anzick, J. Kononen, R.L. Walker, D.O. Azorsa, M.M. Tanner, X.Y. Guan, G. Sauter, O.P. Kallioniemi, J.M. Trent, and P.S. Meltzer A.I.B1, a steroid receptor coactivator amplified in breast and ovarian cancer Science 277 1997 965 968
37. P. Webb, P. Nguyen, J. Shinsako, C. Anderson, W. Feng, M.P. Nguyen, D. Chen, S.M. Huang, S. Subramanian, E. McKinerney, B.S. Katzenellenbogen, M.R. Stallcup, and P.J. Kushner Estrogen receptor activation function 1 works by binding p160 coactivator proteins Mol. Endocrinol. 12 1998 1605 1618
38. J. Font de Mora, and M. Brown AIB1 is a conduit for kinase-mediated growth factor signaling to the estrogen receptor Mol. Cell. Biol. 20 2000 5041 5047
39. S.Y. Jiang, and V.C. Jordan Growth regulation of estrogen receptor-negative breast cancer cells transfected with complementary DNAs for estrogen receptor J. Natl. Cancer Inst. 84 1992 580 591
40. D.A. Zajchowski, R. Sager, and L. Webster Estrogen inhibits the growth of estrogen receptor-negative, but not estrogen receptor-positive, human mammary epithelial cells expressing a recombinant estrogen receptor Cancer Res. 53 1993 5004 5011
41. G. Lazennec, and B.S. Katzenellenbogen Expression of human estrogen receptor using an efficient adenoviral gene delivery system is able to restore hormone-dependent features to estrogen receptor-negative breast carcinoma cells Mol. Cell. Endocrinol. 149 1999 93 105
42. R.S. Tolhurst, R.S. Thomas, F.J. Kyle, H. Patel, M. Periyasamy, A. Photiou, P.T. Thiruchelvam, C.F. Lai, M. Al-Sabbagh, R.A. Fisher, S. Barry, T. Crnogorac-Jurcevic, L.A. Martin, M. Dowsett, R. Charles Coombes, T. Kamalati, S. Ali, and L. Buluwela Transient over-expression of estrogen receptor-alpha in breast cancer cells promotes cell survival and estrogen-independent growth Breast Cancer Res. Treat. 128 2011 357 368
43. A.E. Lykkesfeldt, S.S. Larsen, and P. Briand Human breast cancer cell lines resistant to pure anti-estrogens are sensitive to tamoxifen treatment Int. J. Cancer 61 1995 529 534
44. M. Fan, P.S. Yan, C. Hartman-Frey, L. Chen, H. Paik, S.L. Oyer, J.D. Salisbury, A.S. Cheng, L. Li, P.H. Abbosh, T.H. Huang, and K.P. Nephew Diverse gene expression and DNA methylation profiles correlate with differential adaptation of breast cancer cells to the antiestrogens tamoxifen and fulvestrant Cancer Res. 66 2006 11954 11966
45. T. Frogne, R.V. Benjaminsen, K. Sonne-Hansen, B.S. Sorensen, E. Nexo, A.V. Laenkholm, L.M. Rasmussen, D.J. Riese 2nd, P. de Cremoux, J. Stenvang, and A.E. Lykkesfeldt Activation of ErbB3, EGFR and Erk is essential for growth of human breast cancer cell lines with acquired resistance to fulvestrant Breast Cancer Res. Treat. 114 2009 263 275
46. X. Rao, G. Di Leva, M. Li, F. Fang, C. Devlin, C. Hartman-Frey, M.E. Burow, M. Ivan, C.M. Croce, and K.P. Nephew MicroRNA-221/222 confers breast cancer fulvestrant resistance by regulating multiple signaling pathways Oncogene 30 2011 1082 1097
47. N. Brunner, B. Boysen, S. Jirus, T.C. Skaar, C. Holst-Hansen, J. Lippman, T. Frandsen, M. Spang-Thomsen, S.A. Fuqua, and R. Clarke MCF7/LCC9: an antiestrogen-resistant MCF-7 variant in which acquired resistance to the steroidal antiestrogen ICI 182,780 confers an early cross-resistance to the nonsteroidal antiestrogen tamoxifen Cancer Res. 57 1997 3486 3493
48. Z. Gu, R.Y. Lee, T.C. Skaar, K.B. Bouker, J.N. Welch, J. Lu, A. Liu, Y. Zhu, N. Davis, F. Leonessa, N. Brunner, Y. Wang, and R. Clarke Association of interferon regulatory factor-1, nucleophosmin, nuclear factor-kappaB, and cyclic AMP response element binding with acquired resistance to Faslodex (ICI 182,780) Cancer Res. 62 2002 3428 3437
49. Y. Ning, R.B. Riggins, J.E. Mulla, H. Chung, A. Zwart, and R. Clarke IFNgamma restores breast cancer sensitivity to fulvestrant by regulating STAT1, IFN regulatory factor 1, NF-kappaB, BCL2 family members, and signaling to caspase-dependent apoptosis Mol. Cancer Ther. 9 2010 1274 1285
50. S. Masri, S. Phung, X. Wang, and S. Chen Molecular characterization of aromatase inhibitor-resistant, tamoxifen-resistant and LTEDaro cell lines J. Steroid Biochem. Mol. Biol. 118 2010 277 282
51. L.A. Martin, I. Farmer, S.R. Johnston, S. Ali, C. Marshall, and M. Dowsett Enhanced estrogen receptor (ER) alpha, ERBB2, and MAPK signal transduction pathways operate during the adaptation of MCF-7 cells to long term estrogen deprivation J. Biol. Chem. 278 2003 30458 30468
52. R.J. Santen, R.X. Song, R. McPherson, R. Kumar, L. Adam, M.H. Jeng, and W. Yue The role of mitogen-activated protein (MAP) kinase in breast cancer J. Steroid Biochem. Mol. Biol. 80 2002 239 256
53. C.M. Chan, L.A. Martin, S.R. Johnston, S. Ali, and M. Dowsett Molecular changes associated with the acquisition of oestrogen hypersensitivity in MCF-7 breast cancer cells on long-term oestrogen deprivation J. Steroid Biochem. Mol. Biol. 81 2002 333 341
54. M. Dowsett, L.A. Martin, I. Smith, and S. Johnston Mechanisms of resistance to aromatase inhibitors J. Steroid Biochem. Mol. Biol. 95 2005 167 172
55. R.X. Song, G. Mor, F. Naftolin, R.A. McPherson, J. Song, Z. Zhang, W. Yue, J. Wang, and R.J. Santen Effect of long-term estrogen deprivation on apoptotic responses of breast cancer cells to 17beta-estradiol J. Natl. Cancer Inst. 93 2001 1714 1723
56. P.Y. Maximov, J.S. Lewis-Wambi, and V.C. Jordan The paradox of oestradiol-induced breast cancer cell growth and apoptosis Curr. Signal Transduct. Ther. 4 2009 88 102
57. G.J. Sabnis, D. Jelovac, B. Long, and A. Brodie The role of growth factor receptor pathways in human breast cancer cells adapted to long-term estrogen deprivation Cancer Res. 65 2005 3903 3910
58. C.M. Staka, R.I. Nicholson, and J.M. Gee Acquired resistance to oestrogen deprivation: role for growth factor signalling kinases/oestrogen receptor cross-talk revealed in new MCF-7X model Endocr. Relat. Cancer 12 Suppl. 1 2005 S85 S97
59. D. Jelovac, G. Sabnis, B.J. Long, L. Macedo, O.G. Goloubeva, and A.M. Brodie Activation of mitogen-activated protein kinase in xenografts and cells during prolonged treatment with aromatase inhibitor letrozole Cancer Res. 65 2005 5380 5389
60. G. Sabnis, A. Schayowitz, O. Goloubeva, L. Macedo, and A. Brodie Trastuzumab reverses letrozole resistance and amplifies the sensitivity of breast cancer cells to estrogen Cancer Res. 69 2009 1416 1428
61. H.B. Nair, N.B. Kirma, M. Ganapathy, R.K. Vadlamudi, and R.R. Tekmal Estrogen receptor-beta activation in combination with letrozole blocks the growth of breast cancer tumors resistant to letrozole therapy Steroids 76 2011 792 796
62. R.J. Santen, R.X. Song, Z. Zhang, R. Kumar, M.H. Jeng, S. Masamura, J. Lawrence Jr. , L.P. MacMahon, W. Yue, and L. Berstein Adaptive hypersensitivity to estrogen: mechanisms and clinical relevance to aromatase inhibitor therapy in breast cancer treatment J. Steroid Biochem. Mol. Biol. 95 2005 155 165
63. R.J. Santen, R.X. Song, Z. Zhang, R. Kumar, M.H. Jeng, A. Masamura, J. Lawrence Jr. , L. Berstein, and W. Yue Long-term estradiol deprivation in breast cancer cells up-regulates growth factor signaling and enhances estrogen sensitivity Endocr. Relat. Cancer 12 Suppl. 1 2005 S61 S73
64. M. Edery, J. Goussard, L. Dehennin, R. Scholler, J. Reiffsteck, and M.A. Drosdowsky Endogenous oestradiol-17beta concentration in breast tumours determined by mass fragmentography and by radioimmunoassay: relationship to receptor content Eur. J. Cancer 17 1981 115 120
65. D.S. Millington Determination of hormonal steroid concentrations in biological extracts by high resolution mass fragmentography J. Steroid Biochem. 6 1975 239 245
66. J.R. Pasqualini, G. Chetrite, C. Blacker, M.C. Feinstein, L. Delalonde, M. Talbi, and C. Maloche Concentrations of estrone, estradiol, and estrone sulfate and evaluation of sulfatase and aromatase activities in pre- and postmenopausal breast cancer patients J. Clin. Endocrinol. Metab. 81 1996 1460 1464
67. S.R. Johnston, G. Saccani-Jotti, I.E. Smith, J. Salter, J. Newby, M. Coppen, S.R. Ebbs, and M. Dowsett Changes in estrogen receptor, progesterone receptor, and pS2 expression in tamoxifen-resistant human breast cancer Cancer Res. 55 1995 3331 3338
68. T. Kuukasjarvi, J. Kononen, H. Helin, K. Holli, and J. Isola Loss of estrogen receptor in recurrent breast cancer is associated with poor response to endocrine therapy J. Clin. Oncol. 14 1996 2584 2589
69. J. Shou, S. Massarweh, C.K. Osborne, A.E. Wakeling, S. Ali, H. Weiss, and R. Schiff Mechanisms of tamoxifen resistance: increased estrogen receptor-HER2/neu cross-talk in ER/HER2-positive breast cancer J. Natl. Cancer Inst. 96 2004 926 935
70. R. Kumar, M. Mandal, A. Lipton, H. Harvey, and C.B. Thompson Overexpression of HER2 modulates bcl-2, bcl-XL, and tamoxifen-induced apoptosis in human MCF-7 breast cancer cells Clin. Cancer Res. 2 1996 1215 1219
71. Y. Wang, D. Zhou, S. Phung, S. Masri, D. Smith, and S. Chen SGK3 is an estrogen-inducible kinase promoting estrogen-mediated survival of breast cancer cells Mol. Endocrinol. 25 2011 72 82
72. A.C. Crawford, R.B. Riggins, A.N. Shajahan, A. Zwart, and R. Clarke Co-inhibition of BCL-W and BCL2 restores antiestrogen sensitivity through BECN1 and promotes an autophagy-associated necrosis PLoS One 5 2010 e8604
73. P.E. Lonning Exploring the lack of cross-resistance between aromatase inhibitors: evidence for a difference? Anticancer Drugs 19 Suppl. 2 2008 S11 S13
74. S. Masri, K. Lui, S. Phung, J. Ye, D. Zhou, X. Wang, and S. Chen Characterization of the weak estrogen receptor alpha agonistic activity of exemestane Breast Cancer Res. Treat. 116 2009 461 470
75. E.A. Ariazi, A. Leitao, T.I. Oprea, B. Chen, T. Louis, A.M. Bertucci, C.G. Sharma, S.D. Gill, H.R. Kim, H.A. Shupp, J.R. Pyle, A. Madrack, A.L. Donato, D. Cheng, J.R. Paige, and V.C. Jordan Exemestane's 17-hydroxylated metabolite exerts biological effects as an androgen Mol. Cancer Ther. 6 2007 2817 2827
76. S. Chen An omics approach to determine the mechanisms of acquired aromatase inhibitor resistance OMICS 15 2011 347 352
77. W.R. Miller, and A. Larionov Changes in expression of oestrogen regulated and proliferation genes with neoadjuvant treatment highlight heterogeneity of clinical resistance to the aromatase inhibitor, letrozole Breast Cancer Res. 12 2010 R52
78. R.B. Riggins, R.S. Schrecengost, M.S. Guerrero, and A.H. Bouton Pathways to tamoxifen resistance Cancer Lett. 256 2007 1 24
79. A.L. Harris, S. Nicholson, J.R. Sainsbury, J. Farndon, and C. Wright Epidermal growth factor receptors in breast cancer: association with early relapse and death, poor response to hormones and interactions with neu J. Steroid Biochem. 34 1989 123 131
80. H. Yamauchi, A. O'Neill, R. Gelman, W. Carney, D.Y. Tenney, S. Hosch, and D.F. Hayes Prediction of response to antiestrogen therapy in advanced breast cancer patients by pretreatment circulating levels of extracellular domain of the HER-2/c-neu protein J. Clin. Oncol. 15 1997 2518 2525
81. K. Leitzel, Y. Teramoto, K. Konrad, V.M. Chinchilli, G. Volas, H. Grossberg, H. Harvey, L. Demers, and A. Lipton Elevated serum c-erbB-2 antigen levels and decreased response to hormone therapy of breast cancer J. Clin. Oncol. 13 1995 1129 1135
82. Y. Liu, D. el-Ashry, D. Chen, I.Y. Ding, and F.G. Kern MCF-7 breast cancer cells overexpressing transfected c-erbB-2 have an in vitro growth advantage in estrogen-depleted conditions and reduced estrogen-dependence and tamoxifen-sensitivity in vivo Breast Cancer Res. Treat. 34 1995 97 117
83. H. Kurokawa, A.E. Lenferink, J.F. Simpson, P.I. Pisacane, M.X. Sliwkowski, J.T. Forbes, and C.L. Arteaga Inhibition of HER2/neu (erbB-2) and mitogen-activated protein kinases enhances tamoxifen action against HER2-overexpressing, tamoxifen-resistant breast cancer cells Cancer Res. 60 2000 5887 5894
84. M. Dowsett Overexpression of HER-2 as a resistance mechanism to hormonal therapy for breast cancer Endocr. Relat. Cancer 8 2001 191 195
85. C. Wong, and S. Chen Heat shock protein 90 inhibitors: new mode of therapy to overcome endocrine resistance Cancer Res. 69 2009 8670 8677
86. A. Polychronis, H.D. Sinnett, D. Hadjiminas, H. Singhal, J.L. Mansi, D. Shivapatham, S. Shousha, J. Jiang, D. Peston, N. Barrett, D. Vigushin, K. Morrison, E. Beresford, S. Ali, M.J. Slade, and R.C. Coombes Preoperative gefitinib versus gefitinib and anastrozole in postmenopausal patients with oestrogen-receptor positive and epidermal-growth-factor-receptor-positive primary breast cancer: a double-blind placebo-controlled phase II randomised trial Lancet Oncol. 6 2005 383 391
87. L.S. Schwartzberg, S.X. Franco, A. Florance, L. O'Rourke, J. Maltzman, and S. Johnston Lapatinib plus letrozole as first-line therapy for HER-2+ hormone receptor-positive metastatic breast cancer Oncologist 15 2010 122 129
88. A.F. Leary, S. Drury, S. Detre, S. Pancholi, A.E. Lykkesfeldt, L.A. Martin, M. Dowsett, and S.R. Johnston Lapatinib restores hormone sensitivity with differential effects on estrogen receptor signaling in cell models of human epidermal growth factor receptor 2-negative breast cancer with acquired endocrine resistance Clin. Cancer Res. 16 2010 1486 1497
89. T.W. Miller, B.T. Hennessy, A.M. Gonzalez-Angulo, E.M. Fox, G.B. Mills, H. Chen, C. Higham, C. Garcia-Echeverria, Y. Shyr, and C.L. Arteaga Hyperactivation of phosphatidylinositol-3 kinase promotes escape from hormone dependence in estrogen receptor-positive human breast cancer J. Clin. Invest. 120 2010 2406 2413
90. J.M. Hoskins, L.A. Carey, and H.L. McLeod CYP2D6 and tamoxifen: DNA matters in breast cancer Nat. Rev. Cancer 9 2009 576 586