Breast Cancer Stem Cells and Their Role in Resistance to Endocrine Therapy

Hormones and Cancer

Volumn 2, Issue 2, 2011, Pages 91-103

  O'Brien, Ciara S ^a   Farnie, Gillian ^a   Howell, Sacha J ^a   Clarke, Robert B ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Cancer stem cells; Endocrine therapy; Oestrogen receptor alpha; Resistance

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ALDEHYDE DEHYDROGENASE; ANTINEOPLASTIC AGENT; AROMATASE INHIBITOR; CD24 ANTIGEN; DNA METHYLTRANSFERASE INHIBITOR; DOCETAXEL; DOXORUBICIN; EGF 30008; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTRADIOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; FULVESTRANT; GAMMA SECRETASE INHIBITOR; GEFITINIB; HERMES ANTIGEN; HISTONE DEACETYLASE INHIBITOR; LAPATINIB; LETROZOLE; NOTCH RECEPTOR; PROGESTERONE RECEPTOR; TAMOXIFEN; TRANSCRIPTION FACTOR FOXC1; TRASTUZUMAB; TRICHOSTATIN A; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 1; VORINOSTAT;

ANTIGEN EXPRESSION; ANTINEOPLASTIC ACTIVITY; BREAST CANCER; BREAST CANCER STEM CELL; BREAST EPITHELIUM; CANCER CELL CULTURE; CANCER COMBINATION CHEMOTHERAPY; CANCER HORMONE THERAPY; CANCER RESISTANCE; CANCER STEM CELL; CELL DIFFERENTIATION; CHEMOSENSITIZATION; DRUG POTENTIATION; DRUG WITHDRAWAL; ENZYME ACTIVITY; EPIGENETICS; GENE EXPRESSION REGULATION; GENE REPRESSION; HEMATOLOGIC MALIGNANCY; HORMONE RESISTANCE; HUMAN; MESENCHYMAL STEM CELL; MONOTHERAPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SOLID TUMOR; STEM CELL;

ANIMALS; ANTINEOPLASTIC AGENTS, HORMONAL; BREAST NEOPLASMS; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; NEOPLASTIC STEM CELLS;

EID: 79952616429     PISSN: 18688497     EISSN: 18688500     Source Type: Journal    
DOI: 10.1007/s12672-011-0066-6     Document Type: Review

References (114)

1. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, Wu L, Lindeman GJ, Visvader JE (2006) Generation of a functional mammary gland from a single stem cell. Nature 439: 84-88.
2. Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, Li HI, Eaves CJ (2006) Purification and unique properties of mammary epithelial stem cells. Nature 439: 993-997.
3. Bonnet D, Dick JE (1997) Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3: 730-737.
4. Kelly PN, Dakic A, Adams JM, Nutt SL, Strasser A (2007) Tumor growth need not be driven by rare cancer stem cells. Science 317: 337.
5. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ (2008) Efficient tumour formation by single human melanoma cells. Nature 456: 593-598.
6. Farnie G, Clarke RB, Spence K, Pinnock N, Brennan K, Anderson NG, Bundred NJ (2007) Novel cell culture technique for primary ductal carcinoma in situ: role of Notch and epidermal growth factor receptor signalling pathways. J Natl Cancer Inst 99: 616-627.
7. Park SY, Lee HE, Li H, Shipitsin M, Gelman R, Polyak K (2010) Heterogeneity for stem cell-related markers according to tumor subtype and histologic stage in breast cancer. Clin Cancer Res 16: 876-887.
8. Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, Bernard L, Viale G, Pelicci PG, Di Fiore PP (2010) Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 140: 62-73.
9. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, Lander ES (2009) Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138: 645-659.
10. Kakarala M, Brenner DE, Korkaya H, Cheng C, Tazi K, Ginestier C, Liu S, Dontu G, Wicha MS (2009) Targeting breast stem cells with the cancer preventive compounds curcumin and piperine. Breast Cancer Res Treat 122(3): 777-785.
11. Musgrove EA, Sutherland RL (2009) Biological determinants of endocrine resistance in breast cancer. Nat Rev Cancer 9: 631-643.
12. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63: 5821-5828.
13. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB (2004) Identification of human brain tumour initiating cells. Nature 432: 396-401.
14. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100: 3983-3988.
15. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ (2005) Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 65: 10946-10951.
16. O'Brien CA, Pollett A, Gallinger S, Dick JE (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445: 106-110.
17. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, De Maria R (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445: 111-115.
18. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, Pierotti MA, Daidone MG (2005) Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 65: 5506-5511.
19. Cameron EE, Bachman KE, Myohanen S, Herman JG, Baylin SB (1999) Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat Genet 21: 103-107.
20. Lyko F, Brown R (2005) DNA methyltransferase inhibitors and the development of epigenetic cancer therapies. J Natl Cancer Inst 97: 1498-1506.
21. Bovenzi V, Momparler RL (2001) Antineoplastic action of 5-aza-2′-deoxycytidine and histone deacetylase inhibitor and their effect on the expression of retinoic acid receptor beta and estrogen receptor alpha genes in breast carcinoma cells. Cancer Chemother Pharmacol 48: 71-76.
22. Meyer MJ, Fleming JM, Ali MA, Pesesky MW, Ginsburg E, Vonderhaar BK (2009) Dynamic regulation of CD24 and the invasive, CD44posCD24neg phenotype in breast cancer cell lines. Breast Cancer Res 11: R82.
23. Storms RW, Trujillo AP, Springer JB, Shah L, Colvin OM, Ludeman SM, Smith C (1999) Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. Proc Natl Acad Sci USA 96: 9118-9123.
24. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S, Schott A, Hayes D, Birnbaum D, Wicha MS, Dontu G (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1: 555-567.
25. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, Hur MH, Diebel ME, Monville F, Dutcher J, Brown M, Viens P, Xerri L, Bertucci F, Stassi G, Dontu G, Birnbaum D, Wicha MS (2009) Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 69: 1302-1313.
26. Fillmore CM, Kuperwasser C (2008) Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res 10: R25.
27. Horwitz KB, Dye WW, Harrell JC, Kabos P, Sartorius CA (2008) Rare steroid receptor-negative basal-like tumorigenic cells in luminal subtype human breast cancer xenografts. Proc Natl Acad Sci USA 105: 5774-5779.
28. Zhang M, Atkinson RL, Rosen JM (2010) Selective targeting of radiation-resistant tumor-initiating cells. Proc Natl Acad Sci USA 107: 3522-3527.
29. Creighton CJ, Li X, Landis M, Dixon JM, Neumeister VM, Sjolund A, Rimm DL, Wong H, Rodriguez A, Herschkowitz JI, Fan C, Zhang X, He X, Pavlick A, Gutierrez MC, Renshaw L, Larionov AA, Faratian D, Hilsenbeck SG, Perou CM, Lewis MT, Rosen JM, Chang JC (2009) Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci USA 106: 13820-13825.
30. Howell A, Wardley AM (2005) Overview of the impact of conventional systemic therapies on breast cancer. Endocr Relat Cancer 12(Suppl 1): S9-S16.
31. Mallepell S, Krust A, Chambon P, Brisken C (2006) Paracrine signalling through the epithelial estrogen receptor alpha is required for proliferation and morphogenesis in the mammary gland. Proc Natl Acad Sci USA 103: 2196-2201.
32. Brisken C, Kaur S, Chavarria TE, Binart N, Sutherland RL, Weinberg RA, Kelly PA, Ormandy CJ (1999) Prolactin controls mammary gland development via direct and indirect mechanisms. Dev Biol 210: 96-106.
33. Coleman S, Silberstein GB, Daniel CW (1988) Ductal morphogenesis in the mouse mammary gland: evidence supporting a role for epidermal growth factor. Dev Biol 127: 304-315.
34. Brisken C, Park S, Vass T, Lydon JP, O'Malley BW, Weinberg RA (1998) A paracrine role for the epithelial progesterone receptor in mammary gland development. Proc Natl Acad Sci USA 95: 5076-5081.
35. Keeling JW, Ozer E, King G, Walker F (2000) Oestrogen receptor alpha in female fetal, infant, and child mammary tissue. J Pathol 191: 449-451.
36. Korach KS, Couse JF, Curtis SW, Washburn TF, Lindzey J, Kimbro KS, Eddy EM, Migliaccio S, Snedeker SM, Lubahn DB, Schomberg DW, Smith EP (1996) Estrogen receptor gene disruption: molecular characterization and experimental and clinical phenotypes. Recent Prog Horm Res 51: 159-186, discussion 186-158.
37. Russo J, Ao X, Grill C, Russo IH (1999) Pattern of distribution of cells positive for estrogen receptor alpha and progesterone receptor in relation to proliferating cells in the mammary gland. Breast Cancer Res Treat 53: 217-227.
38. Clarke RB, Howell A, Potten CS, Anderson E (1997) Dissociation between steroid receptor expression and cell proliferation in the human breast. Cancer Res 57: 4987-4991.
39. Beleut M, Rajaram RD, Caikovski M, Ayyanan A, Germano D, Choi Y, Schneider P, Brisken C (2010) Two distinct mechanisms underlie progesterone-induced proliferation in the mammary gland. Proc Natl Acad Sci USA 107: 2989-2994.
40. Asselin-Labat ML, Shackleton M, Stingl J, Vaillant F, Forrest NC, Eaves CJ, Visvader JE, Lindeman GJ (2006) Steroid hormone receptor status of mouse mammary stem cells. J Natl Cancer Inst 98: 1011-1014.
41. Asselin-Labat ML, Vaillant F, Sheridan JM, Pal B, Wu D, Simpson ER, Yasuda H, Smyth GK, Martin TJ, Lindeman GJ, Visvader JE (2010) Control of mammary stem cell function by steroid hormone signalling. Nature 465(7299): 798-802.
42. Sleeman KE, Kendrick H, Robertson D, Isacke CM, Ashworth A, Smalley MJ (2007) Dissociation of estrogen receptor expression and in vivo stem cell activity in the mammary gland. J Cell Biol 176: 19-26.
43. Raouf A, Zhao Y, To K, Stingl J, Delaney A, Barbara M, Iscove N, Jones S, McKinney S, Emerman J, Aparicio S, Marra M, Eaves C (2008) Transcriptome analysis of the normal human mammary cell commitment and differentiation process. Cell Stem Cell 3: 109-118.
44. Shipitsin M, Campbell LL, Argani P, Weremowicz S, Bloushtain-Qimron N, Yao J, Nikolskaya T, Serebryiskaya T, Beroukhim R, Hu M, Halushka MK, Sukumar S, Parker LM, Anderson KS, Harris LN, Garber JE, Richardson AL, Schnitt SJ, Nikolsky Y, Gelman RS, Polyak K (2007) Molecular definition of breast tumor heterogeneity. Cancer Cell 11: 259-273.
45. Sorlie T, Tibshirani R, Parker J, Hastie T, Marron JS, Nobel A, Deng S, Johnsen H, Pesich R, Geisler S, Demeter J, Perou CM, Lonning PE, Brown PO, Borresen-Dale AL, Botstein D (2003) Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci USA 100: 8418-8423.
46. Dowsett M, Houghton J, Iden C, Salter J, Farndon J, A'Hern R, Sainsbury R, Baum M (2006) Benefit from adjuvant tamoxifen therapy in primary breast cancer patients according oestrogen receptor, progesterone receptor, EGF receptor and HER2 status. Ann Oncol 17: 818-826.
47. Howell A, Cuzick J, Baum M, Buzdar A, Dowsett M, Forbes JF, Hoctin-Boes G, Houghton J, Locker GY, Tobias JS (2005) Results of the ATAC (Arimidex, Tamoxifen, Alone or in Combination) trial after completion of 5 years' adjuvant treatment for breast cancer. Lancet 365: 60-62.
48. Gelber RD, Cole BF, Goldhirsch A, Rose C, Fisher B, Osborne CK, Boccardo F, Gray R, Gordon NH, Bengtsson NO, Sevelda P (1996) Adjuvant chemotherapy plus tamoxifen compared with tamoxifen alone for postmenopausal breast cancer: meta-analysis of quality-adjusted survival. Lancet 347: 1066-1071.
49. Giltnane JM, Ryden L, Cregger M, Bendahl PO, Jirstrom K, Rimm DL (2007) Quantitative measurement of epidermal growth factor receptor is a negative predictive factor for tamoxifen response in hormone receptor positive premenopausal breast cancer. J Clin Oncol 25: 3007-3014.
50. Knowlden JM, Hutcheson IR, Jones HE, Madden T, Gee JM, Harper ME, Barrow D, Wakeling AE, Nicholson RI (2003) Elevated levels of epidermal growth factor receptor/c-erbB2 heterodimers mediate an autocrine growth regulatory pathway in tamoxifen-resistant MCF-7 cells. Endocrinology 144: 1032-1044.
51. Massarweh S, Osborne CK, Jiang S, Wakeling AE, Rimawi M, Mohsin SK, Hilsenbeck S, Schiff R (2006) 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 66: 8266-8273.
52. Pancholi S, Lykkesfeldt A, Hilmi C, Banerjee S, Leary A, Drury S, Johnston S, Dowsett M, Martin LA (2008) ERBB2 influences the subcellular localization of the estrogen receptor in tamoxifen-resistant MCF-7 cells leading to the activation of AKT and p90RSK. Endocr Relat Cancer 15: 985.
53. Sarwar N, Kim JS, Jiang J, Peston D, Sinnett HD, Madden P, Gee JM, Nicholson RI, Lykkesfeldt AE, Shousha S, Coombes RC, Ali S (2006) Phosphorylation of ERalpha at serine 118 in primary breast cancer and in tamoxifen-resistant tumours is indicative of a complex role for ERalpha phosphorylation in breast cancer progression. Endocr Relat Cancer 13: 851-861.
54. Hiscox S, Morgan L, Green TP, Barrow D, Gee J, Nicholson RI (2006) Elevated Src activity promotes cellular invasion and motility in tamoxifen resistant breast cancer cells. Breast Cancer Res Treat 97: 263-274.
55. Campbell RA, Bhat-Nakshatri P, Patel NM, Constantinidou D, Ali S, Nakshatri H (2001) Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor alpha: a new model for anti-estrogen resistance. J Biol Chem 276: 9817-9824.
56. Leary AF, Drury S, Detre S, Pancholi S, Lykkesfeldt AE, Martin LA, Dowsett M, Johnston SR (2010) Lapatinib restores hormone sensitivity with differential effects on estrogen receptor signalling in cell models of human epidermal growth factor receptor 2-negative breast cancer with acquired endocrine resistance. Clin Cancer Res 16: 1486-1497.
57. Johnston S, Pippen J Jr, Pivot X, Lichinitser M, Sadeghi S, Dieras V, Gomez HL, Romieu G, Manikhas A, Kennedy MJ, Press MF, Maltzman J, Florance A, O'Rourke L, Oliva C, Stein S, Pegram M (2009) Lapatinib combined with letrozole versus letrozole and placebo as first-line therapy for postmenopausal hormone receptor-positive metastatic breast cancer. J Clin Oncol 27: 5538-5546.
58. Hebbard L, Steffen A, Zawadzki V, Fieber C, Howells N, Moll J, Ponta H, Hofmann M, Sleeman J (2000) CD44 expression and regulation during mammary gland development and function. J Cell Sci 113(Pt 14): 2619-2630.
59. Korkaya H, Paulson A, Iovino F, Wicha MS (2008) HER2 regulates the mammary stem/progenitor cell population driving tumorigenesis and invasion. Oncogene 27: 6120-6130.
60. Magnifico AAL, Campaner S, Delia D, Castiglioni F, Gasparini P, Sozzi GFE, Menard S, Tagliabue E (2009) Tumor-initiating cells of HER2-positive carcinoma cell lines express the highest oncoprotein levels and are sensitive to trastuzumab. Clin Cancer Res 15: 2010-2021.
61. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, Hilsenbeck SG, Pavlick A, Zhang X, Chamness GC, Wong H, Rosen J, Chang JC (2008) Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 100: 672-679.
62. Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, Huang Y, Hu X, Su F, Lieberman J, Song E (2007) let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 131: 1109-1123.
63. Yalcin-Ozuysal O, Fiche M, Guitierrez M, Wagner KU, Raffoul W, Brisken C (2010) Antagonistic roles of Notch and p63 in controlling mammary epithelial cell fates. Cell Death Differ 17(10): 1600-1612.
64. Dontu G, Jackson KW, McNicholas E, Kawamura MJ, Abdallah WM, Wicha MS (2004) Role of Notch signalling in cell-fate determination of human mammary stem/progenitor cells. Breast Cancer Res 6: R605-R615.
65. Stylianou S, Clarke RB, Brennan K (2006) Aberrant activation of notch signalling in human breast cancer. Cancer Res 66: 1517-1525.
66. Harrison H, Farnie G, Howell SJ, Rock RE, Stylianou S, Brennan KR, Bundred NJ, Clarke RB (2010) Regulation of breast cancer stem cell activity by signalling through the Notch4 receptor. Cancer Res 70: 709-718.
67. Rizzo P, Miao H, D'Souza G, Osipo C, Song LL, Yun J, Zhao H, Mascarenhas J, Wyatt D, Antico G, Hao L, Yao K, Rajan P, Hicks C, Siziopikou K, Selvaggi S, Bashir A, Bhandari D, Marchese A, Lendahl U, Qin JZ, Tonetti DA, Albain K, Nickoloff BJ, Miele L (2008) Cross-talk between notch and the estrogen receptor in breast cancer suggests novel therapeutic approaches. Cancer Res 68: 5226-5235.
68. Osipo C, Patel P, Rizzo P, Clementz AG, Hao L, Golde TE, Miele L (2008) ErbB-2 inhibition activates Notch-1 and sensitizes breast cancer cells to a gamma-secretase inhibitor. Oncogene 27: 5019-5032.
69. Zang S, Chen F, Dai J, Guo D, Tse W, Qu X, Ma D, Ji C (2010) RNAi-mediated knockdown of Notch-1 leads to cell growth inhibition and enhanced chemosensitivity in human breast cancer. Oncol Rep 23: 893-899.
70. Hao L, Rizzo P, Osipo C, Pannuti A, Wyatt D, Cheung LW, Sonenshein G, Osborne BA, Miele L (2010) Notch-1 activates estrogen receptor-alpha-dependent transcription via IKKalpha in breast cancer cells. Oncogene 29: 201-213.
71. Phillips TM, McBride WH, Pajonk F (2006) The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 98: 1777-1785.
72. Kok M, Koornstra RH, Margarido TC, Fles R, Armstrong NJ, Linn SC, Van't Veer LJ, Weigelt B (2009) Mammosphere-derived gene set predicts outcome in patients with ER-positive breast cancer. J Pathol 218: 316-326.
73. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715.
74. Hiscox S, Jiang WG, Obermeier K, Taylor K, Morgan L, Burmi R, Barrow D, Nicholson RI (2006) Tamoxifen resistance in MCF7 cells promotes EMT-like behaviour and involves modulation of beta-catenin phosphorylation. Int J Cancer 118: 290-301.
75. Hiscox S, Jordan NJ, Morgan L, Green TP, Nicholson RI (2007) Src kinase promotes adhesion-independent activation of FAK and enhances cellular migration in tamoxifen-resistant breast cancer cells. Clin Exp Metastasis 24: 157-167.
76. Hiscox S, Jordan NJ, Smith C, James M, Morgan L, Taylor KM, Green TP, Nicholson RI (2008) Dual targeting of Src and ER prevents acquired antihormone resistance in breast cancer cells. Breast Cancer Res Treat 115(1): 57-67.
77. Zhou Y, Yau C, Gray JW, Chew K, Dairkee SH, Moore DH, Eppenberger U, Eppenberger-Castori S, Benz CC (2007) Enhanced NF kappa B and AP-1 transcriptional activity associated with antiestrogen resistant breast cancer. BMC Cancer 7: 59.
78. Borley AC, Hiscox S, Gee J, Smith C, Shaw V, Barrett-Lee P, Nicholson RI (2008) Anti-oestrogens but not oestrogen deprivation promote cellular invasion in intercellular adhesion-deficient breast cancer cells. Breast Cancer Res 10: R103.
79. Hiscox S, Jiang WG (1997) Regulation of endothelial CD44 expression and endothelium-tumour cell interactions by hepatocyte growth factor/scatter factor. Biochem Biophys Res Commun 233: 1-5.
80. Dhasarathy A, Kajita M, Wade PA (2007) The transcription factor snail mediates epithelial to mesenchymal transitions by repression of estrogen receptor-alpha. Mol Endocrinol 21: 2907-2918.
81. Ye Y, Xiao Y, Wang W, Yearsley K, Gao JX, Barsky SH (2008) ERalpha suppresses slug expression directly by transcriptional repression. Biochem J 416: 179-187.
82. Herschkowitz JI, Simin K, Weigman VJ, Mikaelian I, Usary J, Hu Z, Rasmussen KE, Jones LP, Assefnia S, Chandrasekharan S, Backlund MG, Yin Y, Khramtsov AI, Bastein R, Quackenbush J, Glazer RI, Brown PH, Green JE, Kopelovich L, Furth PA, Palazzo JP, Olopade OI, Bernard PS, Churchill GA, van Dyke T, Perou CM (2007) Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol 8: R76.
83. Perou CM, Sorlie 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, Lonning PE, Borresen-Dale AL, Brown PO, Botstein D (2000) Molecular portraits of human breast tumours. Nature 406: 747-752.
84. Sims AH, Howell A, Howell SJ, Clarke RB (2007) Origins of breast cancer subtypes and therapeutic implications. Nat Clin Pract Oncol 4: 516-525.
85. Bloushtain-Qimron N, Yao J, Snyder EL, Shipitsin M, Campbell LL, Mani SA, Hu M, Chen H, Ustyansky V, Antosiewicz JE, Argani P, Halushka MK, Thomson JA, Pharoah P, Porgador A, Sukumar S, Parsons R, Richardson AL, Stampfer MR, Gelman RS, Nikolskaya T, Nikolsky Y, Polyak K (2008) Cell type-specific DNA methylation patterns in the human breast. Proc Natl Acad Sci USA 105: 14076-14081.
86. Lower EE, Glass EL, Bradley DA, Blau R, Heffelfinger S (2005) Impact of metastatic estrogen receptor and progesterone receptor status on survival. Breast Cancer Res Treat 90: 65-70.
87. Fehm T, Krawczyk N, Solomayer EF, Becker-Pergola G, Durr-Storzer S, Neubauer H, Seeger H, Staebler A, Wallwiener D, Becker S (2008) ERalpha-status of disseminated tumour cells in bone marrow of primary breast cancer patients. Breast Cancer Res 10: R76.
88. Lapidus RG, Ferguson AT, Ottaviano YL, Parl FF, Smith HS, Weitzman SA, Baylin SB, Issa JP, Davidson NE (1996) Methylation of estrogen and progesterone receptor gene 5′ CpG islands correlates with lack of estrogen and progesterone receptor gene expression in breast tumors. Clin Cancer Res 2: 805-810.
89. Ottaviano YL, Issa JP, Parl FF, Smith HS, Baylin SB, Davidson NE (1994) Methylation of the estrogen receptor gene CpG island marks loss of estrogen receptor expression in human breast cancer cells. Cancer Res 54: 2552-2555.
90. Badia E, Oliva J, Balaguer P, Cavailles V (2007) Tamoxifen resistance and epigenetic modifications in breast cancer cell lines. Curr Med Chem 14: 3035-3045.
91. Croker AK, Goodale D, Chu J, Postenka C, Hedley BD, Hess DA, Allan AL (2008) High aldehyde dehydrogenase and expression of cancer stem cell markers selects for breast cancer cells with enhanced malignant and metastatic ability. J Cell Mol Med 13(8): 2236-2252.
92. Sheridan C, Kishimoto H, Fuchs RK, Mehrotra S, Bhat-Nakshatri P, Turner CH, Goulet R Jr, Badve S, Nakshatri H (2006) CD44+/CD24- breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res 8: R59.
93. Ouhtit A, Abd Elmageed ZY, Abdraboh ME, Lioe TF, Raj MH (2007) In vivo evidence for the role of CD44s in promoting breast cancer metastasis to the liver. Am J Pathol 171: 2033-2039.
94. Hiscox S, Jordan NJ, Jiang W, Harper M, McClelland R, Smith C, Nicholson RI (2006) Chronic exposure to fulvestrant promotes overexpression of the c-Met receptor in breast cancer cells: implications for tumour-stroma interactions. Endocr Relat Cancer 13: 1085-1099.
95. Hiscox S, Morgan L, Barrow D, Dutkowskil C, Wakeling A, Nicholson RI (2004) Tamoxifen resistance in breast cancer cells is accompanied by an enhanced motile and invasive phenotype: inhibition by gefitinib ('Iressa', ZD1839). Clin Exp Metastasis 21: 201-212.
96. Mine S, Fujisaki T, Kawahara C, Tabata T, Iida T, Yasuda M, Yoneda T, Tanaka Y (2003) Hepatocyte growth factor enhances adhesion of breast cancer cells to endothelial cells in vitro through up-regulation of CD44. Exp Cell Res 288: 189-197.
97. Harrell JC, Dye WW, Allred DC, Jedlicka P, Spoelstra NS, Sartorius CA, Horwitz KB (2006) Estrogen receptor positive breast cancer metastasis: altered hormonal sensitivity and tumor aggressiveness in lymphatic vessels and lymph nodes. Cancer Res 66: 9308-9315.
98. Harrell JC, Dye WW, Harvell DM, Pinto M, Jedlicka P, Sartorius CA, Horwitz KB (2007) Estrogen insensitivity in a model of estrogen receptor positive breast cancer lymph node metastasis. Cancer Res 67: 10582-10591.
99. Kabos PDW, Elias A, Horwitz KB, Sartorius CA (2008) The chemoresistant population of luminal subtype human breast cancer cells expresses a basal phenotype. San Antonio Breast Cancer Symposium Proceedings, Abstract presentation.
100. Farmer P, Bonnefoi H, Anderle P, Cameron D, Wirapati P, Becette V, Andre S, Piccart M, Campone M, Brain E, Macgrogan G, Petit T, Jassem J, Bibeau F, Blot E, Bogaerts J, Aguet M, Bergh J, Iggo R, Delorenzi M (2009) A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer. Nat Med 15: 68-74.
101. Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, Oh EY, Gaber MW, Finklestein D, Allen M, Frank A, Bayazitov IT, Zakharenko SS, Gajjar A, Davidoff A, Gilbertson RJ (2007) A perivascular niche for brain tumor stem cells. Cancer Cell 11: 69-82.
102. Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland AB, Shi Q, McLendon RE, Bigner DD, Rich JN (2006) Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 66: 7843-7848.
103. Sharma D, Blum J, Yang X, Beaulieu N, Macleod AR, Davidson NE (2005) Release of methyl CpG binding proteins and histone deacetylase 1 from the Estrogen receptor alpha (ER) promoter upon reactivation in ER-negative human breast cancer cells. Mol Endocrinol 19: 1740-1751.
104. Zhou Q, Atadja P, Davidson NE (2007) Histone deacetylase inhibitor LBH589 reactivates silenced estrogen receptor alpha (ER) gene expression without loss of DNA hypermethylation. Cancer Biol Ther 6: 64-69.
105. Ferguson AT, Lapidus RG, Baylin SB, Davidson NE (1995) Demethylation of the estrogen receptor gene in estrogen receptor-negative breast cancer cells can reactivate estrogen receptor gene expression. Cancer Res 55: 2279-2283.
106. Yang X, Ferguson AT, Nass SJ, Phillips DL, Butash KA, Wang SM, Herman JG, Davidson NE (2000) Transcriptional activation of estrogen receptor alpha in human breast cancer cells by histone deacetylase inhibition. Cancer Res 60: 6890-6894.
107. Yang X, Phillips DL, Ferguson AT, Nelson WG, Herman JG, Davidson NE (2001) Synergistic activation of functional estrogen receptor (ER)-alpha by DNA methyltransferase and histone deacetylase inhibition in human ER-alpha-negative breast cancer cells. Cancer Res 61: 7025-7029.
108. Fan J, Yin WJ, Lu JS, Wang L, Wu J, Wu FY, Di GH, Shen ZZ, Shao ZM (2008) ER alpha negative breast cancer cells restore response to endocrine therapy by combination treatment with both HDAC inhibitor and DNMT inhibitor. J Cancer Res Clin Oncol 134: 883-890.
109. Fortunati N, Bertino S, Costantino L, De Bortoli M, Compagnone A, Bandino A, Catalano MG, Boccuzzi G (2010) Valproic acid restores ER alpha and antiestrogen sensitivity to ER alpha-negative breast cancer cells. Mol Cell Endocrinol 314: 17-22.
110. Zhou Q, Shaw PG, Davidson NE (2008) Inhibition of histone deacetylase suppresses EGF signalling pathways by destabilizing EGFR mRNA in ER-negative human breast cancer cells. Breast Cancer Res Treat 117(2): 443-451.
111. Rayala SK, Molli PR, Kumar R (2006) Nuclear p21-activated kinase 1 in breast cancer packs off tamoxifen sensitivity. Cancer Res 66: 5985-5988.
112. Balasenthil S, Sahin AA, Barnes CJ, Wang RA, Pestell RG, Vadlamudi RK, Kumar R (2004) p21-activated kinase-1 signalling mediates cyclin D1 expression in mammary epithelial and cancer cells. J Biol Chem 279: 1422-1428.
113. Holm C, Rayala S, Jirstrom K, Stal O, Kumar R, Landberg G (2006) Association between Pak1 expression and subcellular localization and tamoxifen resistance in breast cancer patients. J Natl Cancer Inst 98: 671-680.
114. Munster PN, Lacevic M, Schmitt M, Bicaku E, Marchion D, Stephens A, Sullivan L, Minton S (2008) Phase II trial of vorinostat, a histone deacetylase inhibitor to restore the hormone sensitivity to the anti-estrogen tamoxifen in patients with advanced breast cancer having failed prior aromatase inhibitor therapy. J Clin Oncol 26: 3501.