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Hormones and Cancer

, Volume 8, Issue 2, pp 90–99 | Cite as

Bisphenol A Induces Sox2 in ER+ Breast Cancer Stem-Like Cells

  • M. Angeles Lillo
  • Cydney Nichols
  • Tiffany N. Seagroves
  • Gustavo A. Miranda-Carboni
  • Susan A. KrumEmail author
Original Paper

Abstract

Bisphenol A (BPA) is an endocrine disrupting compound used in food and beverage plastic containers and has been shown to increase breast cancer cellular proliferation. However, the concentrations of BPA used in these experiments are far higher than the physiological levels of BPA detected in the human body. We observed in vitro that exposure of MCF-7 cells to physiological concentrations of BPA failed to increase cell proliferation or to induce canonical estrogen-responsive genes (pS2 and progesterone receptor (PR)), in contrast to 17β-estradiol (E2) treatment. However, MCF-7 cells treated with 10 nM BPA induced ALDH1 expression, a marker of human mammary stem cells. When treated with 10 nM BPA, mammospheres derived either from MCF-7 cells, a patient-derived xenograft, or the normal mouse mammary gland exhibited increased size; however, these effects were not observed in MDA-MB-231 mammospheres. Mechanistically, BPA induced SOX2 mRNA and protein in MCF-7 mammospheres, resulting from enhanced CREB phosphorylation, and subsequent binding of pCREB to a SOX2 downstream enhancer. These findings suggest that physiological levels of BPA increase estrogen receptor-positive breast cancer tumor maintenance through enhanced cancer stem-like cell activity via direct regulation of SOX2 transcription.

Keywords

Cancer Stem Cell SOX2 Expression Breast Cancer Stem Cell Mammary Stem Cell Breast Stem Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

This work was supported by a grant from Susan G. Komen for the Cure to SAK (KG110317); the National Cancer Institute (CA138488 to T.N.S.); and intramural support from the West Cancer Center in Memphis, TN (to T.N.S.).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

12672_2017_286_Fig7_ESM.gif (5 kb)
Supplementary Figure 1

Proliferation of MCF-7 cells after one week of hormone treatment. MCF-7 cells were treated for one week with either 10 nM E2, BPA or control vehicle (EtOH) and then counted by hemocytometer, *p < 0.0001. (GIF 4 kb)

12672_2017_286_MOESM1_ESM.tif (774 kb)
High Resolution Image (TIFF 774 kb)
12672_2017_286_Fig8_ESM.gif (7 kb)
Supplementary Figure 2

BPA does not induce phosphorylation of CREB in MDA-MB-231 cells. Protein from MDA-MB-231 cells treated with 10 nM E2, BPA or EtOH for 15 min was harvested and immunoblotting was performed with pCREB antibody, total CREB and β-tubulin (loading control). (GIF 6 kb)

12672_2017_286_MOESM2_ESM.tif (725 kb)
High Resolution Image (TIFF 725 kb)
12672_2017_286_Fig9_ESM.gif (77 kb)
Supplementary Figure 3

MCF-7 mammospheres are enriched in stem cells. (A) Expression of the stem cell genes NANOG, SOX2 and OCT4 was compared in adherent and MCF-7 spheres by quantitative RT-PCR. (B) Primary and secondary MCF-7 mammospheres. Magnification bar, 1 mm. (GIF 76 kb)

12672_2017_286_MOESM3_ESM.tif (2.8 mb)
High Resolution Image (TIFF 2874 kb)
12672_2017_286_Fig10_ESM.gif (171 kb)
Supplementary Figure 4

Additional fields of view of MCF-7 mammospheres treated with hormones. Magnification bar, 400 μm. (GIF 170 kb)

12672_2017_286_MOESM4_ESM.tif (3.9 mb)
High Resolution Image (TIFF 4011 kb)

References

  1. 1.
    Zoeller RT, Brown TR, Doan LL, Gore AC, Skakkebaek NE, Soto AM et al (2012) Endocrine-disrupting chemicals and public health protection: a statement of principles from the Endocrine Society. Endocrinology 153(9):4097–4110CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Signorile PG, Spugnini EP, Citro G, Viceconte R, Vincenzi B, Baldi F et al (2012) Endocrine disruptors in utero cause ovarian damages linked to endometriosis. Front Biosci 4:1724–1730CrossRefGoogle Scholar
  3. 3.
    Prins GS, Tang WY, Belmonte J, Ho SM (2008) Developmental exposure to bisphenol A increases prostate cancer susceptibility in adult rats: epigenetic mode of action is implicated. Fertil Steril 89(2 Suppl):e41CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Soto AM, Brisken C, Schaeberle C, Sonnenschein C (2013) Does cancer start in the womb? Altered mammary gland development and predisposition to breast cancer due to in utero exposure to endocrine disruptors. J Mammary Gland Biol Neoplasia 18(2):199–208CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV (2007) Human exposure to bisphenol A (BPA). Reprod Toxicol 24(2):139–177CrossRefPubMedGoogle Scholar
  6. 6.
    Vandenberg LN, Chahoud I, Heindel JJ, Padmanabhan V, Paumgartten FJ, Schoenfelder G (2010) Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ Health Perspect 118(8):1055–1070CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Calafat AM, Kuklenyik Z, Reidy JA, Caudill SP, Ekong J, Needham LL (2005) Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ Health Perspect 113(4):391–395CrossRefPubMedGoogle Scholar
  8. 8.
    Kim HS, Han SY, Yoo SD, Lee BM, Park KL (2001) Potential estrogenic effects of bisphenol-A estimated by in vitro and in vivo combination assays. J Toxicol Sci 26(3):111–118CrossRefPubMedGoogle Scholar
  9. 9.
    Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT et al (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139(10):4252–4263Google Scholar
  10. 10.
    Krishnan AV, Stathis P, Permuth SF, Tokes L, Feldman D (1993) Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology 132(6):2279–2286PubMedGoogle Scholar
  11. 11.
    Vandenberg LN, Maffini MV, Wadia PR, Sonnenschein C, Rubin BS, Soto AM (2007) Exposure to environmentally relevant doses of the xenoestrogen bisphenol-A alters development of the fetal mouse mammary gland. Endocrinology 148(1):116–127CrossRefPubMedGoogle Scholar
  12. 12.
    Tharp AP, Maffini MV, Hunt PA, VandeVoort CA, Sonnenschein C, Soto AM (2012) Bisphenol A alters the development of the rhesus monkey mammary gland. Proc Natl Acad Sci U S A 109(21):8190–8195CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Wadia PR, Cabaton NJ, Borrero MD, Rubin BS, Sonnenschein C, Shioda T et al (2013) Low-dose BPA exposure alters the mesenchymal and epithelial transcriptomes of the mouse fetal mammary gland. PLoS One 8(5):e63902CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Paulose T, Speroni L, Sonnenschein C, Soto AM (2015) Estrogens in the wrong place at the wrong time: fetal BPA exposure and mammary cancer. Reprod Toxicol 54:58–65CrossRefPubMedGoogle Scholar
  15. 15.
    Betancourt AM, Eltoum IA, Desmond RA, Russo J, Lamartiniere CA (2010) In utero exposure to bisphenol A shifts the window of susceptibility for mammary carcinogenesis in the rat. Environ Health Perspect 118(11):1614–1619CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Durando M, Kass L, Piva J, Sonnenschein C, Soto AM, Luque EH et al (2007) Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats. Environ Health Perspect 115(1):80–86CrossRefPubMedGoogle Scholar
  17. 17.
    Jenkins S, Raghuraman N, Eltoum I, Carpenter M, Russo J, Lamartiniere CA (2009) Oral exposure to bisphenol A increases dimethylbenzanthracene-induced mammary cancer in rats. Environ Health Perspect 117(6):910–915CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Murray TJ, Maffini MV, Ucci AA, Sonnenschein C, Soto AM (2007) Induction of mammary gland ductal hyperplasias and carcinoma in situ following fetal bisphenol A exposure. Reprod Toxicol 23(3):383–390CrossRefPubMedGoogle Scholar
  19. 19.
    Weber Lozada K, Keri RA (2011) Bisphenol A increases mammary cancer risk in two distinct mouse models of breast cancer. Biol Reprod 85(3):490–497CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Acevedo N, Davis B, Schaeberle CM, Sonnenschein C, Soto AM (2013) Perinatally administered bisphenol A as a potential mammary gland carcinogen in rats. Environ Health Perspect 121(9):1040–1046PubMedPubMedCentralGoogle Scholar
  21. 21.
    Miyakoshi T, Miyajima K, Takekoshi S, Osamura RY (2009) The influence of endocrine disrupting chemicals on the proliferation of ERalpha knockdown-human breast cancer cell line MCF-7; new attempts by RNAi technology. Acta Histochem Cytochem 42(2):23–28CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Sengupta S, Obiorah I, Maximov PY, Curpan R, Jordan VC (2013) Molecular mechanism of action of bisphenol and bisphenol A mediated by oestrogen receptor alpha in growth and apoptosis of breast cancer cells. Br J Pharmacol 169(1):167–178CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Lapensee EW, Tuttle TR, Fox SR, Ben-Jonathan N (2009) Bisphenol A at low nanomolar doses confers chemoresistance in estrogen receptor-alpha-positive and -negative breast cancer cells. Environ Health Perspect 117(2):175–180CrossRefPubMedGoogle Scholar
  24. 24.
    Buteau-Lozano H, Velasco G, Cristofari M, Balaguer P, Perrot-Applanat M (2008) Xenoestrogens modulate vascular endothelial growth factor secretion in breast cancer cells through an estrogen receptor-dependent mechanism. J Endocrinol 196(2):399–412CrossRefPubMedGoogle Scholar
  25. 25.
    Fernandez SV, Huang Y, Snider KE, Zhou Y, Pogash TJ, Russo J (2012) Expression and DNA methylation changes in human breast epithelial cells after bisphenol A exposure. Int J Oncol 41(1):369–377PubMedPubMedCentralGoogle Scholar
  26. 26.
    Dong S, Terasaka S, Kiyama R (2011) Bisphenol A induces a rapid activation of Erk1/2 through GPR30 in human breast cancer cells. Environ Pollut 159(1):212–218CrossRefPubMedGoogle Scholar
  27. 27.
    Li M, Guo J, Gao W, Yu J, Han X, Zhang J et al (2014) Bisphenol AF-induced endogenous transcription is mediated by ERalpha and ERK1/2 activation in human breast cancer cells. PLoS One 9(4):e94725CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Zhang W, Fang Y, Shi X, Zhang M, Wang X, Tan Y (2012) Effect of bisphenol A on the EGFR-STAT3 pathway in MCF-7 breast cancer cells. Mol Med Rep 5(1):41–47PubMedGoogle Scholar
  29. 29.
    Gao H, Yang BJ, Li N, Feng LM, Shi XY, Zhao WH et al (2015) Bisphenol A and hormone-associated cancers: current progress and perspectives. Medicine 94(1):e211CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Kang KS, Trosko JE (2011) Stem cells in toxicology: fundamental biology and practical considerations. Toxicological sciences : an official journal of the Society of Toxicology 120(Suppl 1):S269–S289CrossRefGoogle Scholar
  31. 31.
    Ailles LE, Weissman IL (2007) Cancer stem cells in solid tumors. Curr Opin Biotechnol 18(5):460–466CrossRefPubMedGoogle Scholar
  32. 32.
    Trosko JE (2009) Review paper: cancer stem cells and cancer nonstem cells: from adult stem cells or from reprogramming of differentiated somatic cells. Vet Pathol 46(2):176–193CrossRefPubMedGoogle Scholar
  33. 33.
    Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D et al (2005) Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 65(13):5506–5511CrossRefPubMedGoogle Scholar
  34. 34.
    Huang MZ, Li YQ, Zhang HL, Nan FF (2010) Breast cancer stromal fibroblasts promote the generation of CD44(+)CD24(−) cells through SDF-1/CXCR4 interaction. J Exp Clin Canc Res. 29Google Scholar
  35. 35.
    Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP et al (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122(6):947–956CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Young RA (2011) Control of the embryonic stem cell state. Cell 144(6):940–954CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Seymour T, Twigger AJ, Kakulas F (2015) Pluripotency genes and their functions in the normal and aberrant breast and brain. Int J Mol Sci 16(11):27288–27301CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Roy S, Gascard P, Dumont N, Zhao J, Pan D, Petrie S et al (2013) Rare somatic cells from human breast tissue exhibit extensive lineage plasticity. Proc Natl Acad Sci U S A 110(12):4598–4603CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Leis O, Eguiara A, Lopez-Arribillaga E, Alberdi MJ, Hernandez-Garcia S, Elorriaga K et al (2012) Sox2 expression in breast tumours and activation in breast cancer stem cells. Oncogene 31(11):1354–1365CrossRefPubMedGoogle Scholar
  40. 40.
    Nadal A, Diaz M, Valverde MA (2001) The estrogen trinity: membrane, cytosolic, and nuclear effects. News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society 16:251–255Google Scholar
  41. 41.
    Quesada I, Fuentes E, Viso-Leon MC, Soria B, Ripoll C, Nadal A (2002) Low doses of the endocrine disruptor bisphenol-A and the native hormone 17beta-estradiol rapidly activate transcription factor CREB. FASEB journal : official publication of the Federation of American Societies for Experimental Biology 16(12):1671–1673Google Scholar
  42. 42.
    Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100(7):3983–3988CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M et al (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1(5):555–567CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Cailleau R, Young R, Olive M, Reeves WJ Jr (1974) Breast tumor cell lines from pleural effusions. J Natl Cancer Inst 53(3):661–674CrossRefPubMedGoogle Scholar
  45. 45.
    Read LD, Greene GL, Katzenellenbogen BS (1989) Regulation of estrogen receptor messenger ribonucleic acid and protein levels in human breast cancer cell lines by sex steroid hormones, their antagonists, and growth factors. Mol Endocrinol 3(2):295–304CrossRefPubMedGoogle Scholar
  46. 46.
    Simpson E, Santen RJ (2015) Celebrating 75 years of oestradiol. J Mol Endocrinol 55(3):T1–T20CrossRefPubMedGoogle Scholar
  47. 47.
    Routledge EJ, White R, Parker MG, Sumpter JP (2000) Differential effects of xenoestrogens on coactivator recruitment by estrogen receptor (ER) alpha and ERbeta. J Biol Chem 275(46):35986–35993CrossRefPubMedGoogle Scholar
  48. 48.
    Matthews JB, Twomey K, Zacharewski TR (2001) In vitro and in vivo interactions of bisphenol A and its metabolite, bisphenol A glucuronide, with estrogen receptors alpha and beta. Chem Res Toxicol 14(2):149–157CrossRefPubMedGoogle Scholar
  49. 49.
    Sajiki J, Takahashi K, Yonekubo J (1999) Sensitive method for the determination of bisphenol-A in serum using two systems of high-performance liquid chromatography. J Chromatogr B Biomed Sci Appl 736(1–2):255–261CrossRefPubMedGoogle Scholar
  50. 50.
    Takeuchi T, Tsutsumi O (2002) Serum bisphenol A concentrations showed gender differences, possibly linked to androgen levels. Biochem Biophys Res Commun 291(1):76–78CrossRefPubMedGoogle Scholar
  51. 51.
    Wang J, Jenkins S, Lamartiniere CA (2014) Cell proliferation and apoptosis in rat mammary glands following combinational exposure to bisphenol A and genistein. BMC Cancer 14:379CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Pike MC, Spicer DV, Dahmoush L, Press MF (1993) Estrogens, progestogens, normal breast cell proliferation, and breast cancer risk. Epidemiol Rev 15(1):17–35CrossRefPubMedGoogle Scholar
  53. 53.
    Singh M, McGinley JN, Thompson HJ (2000) A comparison of the histopathology of premalignant and malignant mammary gland lesions induced in sexually immature rats with those occurring in the human. Laboratory investigation; a journal of technical methods and pathology 80(2):221–231CrossRefPubMedGoogle Scholar
  54. 54.
    Sprague BL, Trentham-Dietz A, Hedman CJ, Wang J, Hemming JD, Hampton JM et al (2013) Circulating serum xenoestrogens and mammographic breast density. Breast cancer research : BCR 15(3):R45CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL et al (2006) Cancer stem cells—perspectives on current status and future directions: AACR workshop on cancer stem cells. Cancer Res 66(19):9339–9344CrossRefPubMedGoogle Scholar
  56. 56.
    Ling GQ, Chen DB, Wang BQ, Zhang LS (2012) Expression of the pluripotency markers Oct3/4, Nanog and Sox2 in human breast cancer cell lines. Oncol Lett 4(6):1264–1268PubMedPubMedCentralGoogle Scholar
  57. 57.
    Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ et al (2003) In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 17(10):1253–1270CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Jung JW, Park SB, Lee SJ, Seo MS, Trosko JE, Kang KS (2011) Metformin represses self-renewal of the human breast carcinoma stem cells via inhibition of estrogen receptor-mediated OCT4 expression. PLoS One 6(11):e28068CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Favaro R, Appolloni I, Pellegatta S, Sanga AB, Pagella P, Gambini E et al (2014) Sox2 is required to maintain cancer stem cells in a mouse model of high-grade oligodendroglioma. Cancer Res 74(6):1833–1844CrossRefPubMedGoogle Scholar
  60. 60.
    Gangemi RM, Griffero F, Marubbi D, Perera M, Capra MC, Malatesta P et al (2009) SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity. Stem Cells 27(1):40–48CrossRefPubMedGoogle Scholar
  61. 61.
    Chen Y, Shi L, Zhang L, Li R, Liang J, Yu W et al (2008) The molecular mechanism governing the oncogenic potential of SOX2 in breast cancer. J Biol Chem 283(26):17969–17978CrossRefPubMedGoogle Scholar
  62. 62.
    Stolzenburg S, Rots MG, Beltran AS, Rivenbark AG, Yuan X, Qian H et al (2012) Targeted silencing of the oncogenic transcription factor SOX2 in breast cancer. Nucleic Acids Res 40(14):6725–6740CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Asselin-Labat ML, Shackleton M, Stingl J, Vaillant F, Forrest NC, Eaves CJ et al (2006) Steroid hormone receptor status of mouse mammary stem cells. J Natl Cancer Inst 98(14):1011–1014CrossRefPubMedGoogle Scholar
  64. 64.
    Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH et al (2009) Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med 15(8):907–913CrossRefPubMedGoogle Scholar
  65. 65.
    Deng H, Zhang XT, Wang ML, Zheng HY, Liu LJ, Wang ZY (2014) ER-alpha36-mediated rapid estrogen signaling positively regulates ER-positive breast cancer stem/progenitor cells. PLoS One 9(2):e88034CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Vandenberg LN, Maffini MV, Sonnenschein C, Rubin BS, Soto AM (2009) Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr Rev 30(1):75–95CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Nadal A, Ropero AB, Laribi O, Maillet M, Fuentes E, Soria B (2000) Nongenomic actions of estrogens and xenoestrogens by binding at a plasma membrane receptor unrelated to estrogen receptor alpha and estrogen receptor beta. Proc Natl Acad Sci U S A 97(21):11603–11608CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Ropero AB, Soria B, Nadal A (2002) A nonclassical estrogen membrane receptor triggers rapid differential actions in the endocrine pancreas. Mol Endocrinol 16(3):497–505CrossRefPubMedGoogle Scholar
  69. 69.
    Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414(6859):105–111CrossRefPubMedGoogle Scholar
  70. 70.
    Kakarala M, Wicha MS (2008) Implications of the cancer stem-cell hypothesis for breast cancer prevention and therapy. Journal of clinical oncology : official journal of the American Society of Clinical Oncology 26(17):2813–2820CrossRefGoogle Scholar
  71. 71.
    Visvader JE, Lindeman GJ (2008) Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 8(10):755–768CrossRefPubMedGoogle Scholar
  72. 72.
    DeRose YS, Wang G, Lin YC, Bernard PS, Buys SS, Ebbert MT et al (2011) Tumor grafts derived from women with breast cancer authentically reflect tumor pathology, growth, metastasis and disease outcomes. Nat Med 17(11):1514–1520CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Lillo MA, Nichols C, Perry C, Runke S, Krutilina R, Seagroves TN, et al. (2016) Methylparaben stimulates tumor initiating cells in ER+ breast cancer models. Journal of applied toxicology : JATGoogle Scholar
  74. 74.
    Wend P, Runke S, Wend K, Anchondo B, Yesayan M, Jardon M et al (2013) WNT10B/beta-catenin signalling induces HMGA2 and proliferation in metastatic triple-negative breast cancer. EMBO molecular medicine 5(2):264–279CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR, Eeckhoute J et al (2006) Genome-wide analysis of estrogen receptor binding sites. Nat Genet 38(11):1289–1297CrossRefPubMedGoogle Scholar
  76. 76.
    Carroll JS, Liu XS, Brodsky AS, Li W, Meyer CA, Szary AJ et al (2005) Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122(1):33–43CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • M. Angeles Lillo
    • 1
    • 5
  • Cydney Nichols
    • 2
  • Tiffany N. Seagroves
    • 3
    • 5
  • Gustavo A. Miranda-Carboni
    • 4
    • 5
  • Susan A. Krum
    • 1
    • 5
    Email author
  1. 1.Department of Orthopaedic Surgery and Biomedical EngineeringUniversity of Tennessee Health Science CenterMemphisUSA
  2. 2.Department of MicrobiologyImmunology and Molecular Genetics, UCLALos AngelesUSA
  3. 3.Department of PathologyUniversity of Tennessee Health Science CenterMemphisUSA
  4. 4.Department of MedicineUniversity of Tennessee Health Science CenterMemphisUSA
  5. 5.Center for Cancer ResearchUniversity of Tennessee Health Science CenterMemphisUSA

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