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Erschienen in: Discover Oncology 2/2017

27.02.2017 | Original Paper

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

verfasst von: M. Angeles Lillo, Cydney Nichols, Tiffany N. Seagroves, Gustavo A. Miranda-Carboni, Susan A. Krum

Erschienen in: Discover Oncology | Ausgabe 2/2017

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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.
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Literatur
1.
Zurück zum Zitat 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):4097–4110CrossRefPubMedPubMedCentral 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):4097–4110CrossRefPubMedPubMedCentral
2.
Zurück zum Zitat 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 4:1724–1730CrossRef 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 4:1724–1730CrossRef
3.
Zurück zum Zitat 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):e41CrossRefPubMedPubMedCentral 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):e41CrossRefPubMedPubMedCentral
4.
Zurück zum Zitat 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):199–208CrossRefPubMedPubMedCentral 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):199–208CrossRefPubMedPubMedCentral
5.
Zurück zum Zitat Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV (2007) Human exposure to bisphenol A (BPA). Reprod Toxicol 24(2):139–177CrossRefPubMed Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV (2007) Human exposure to bisphenol A (BPA). Reprod Toxicol 24(2):139–177CrossRefPubMed
6.
Zurück zum Zitat 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):1055–1070CrossRefPubMedPubMedCentral 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):1055–1070CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat 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):391–395CrossRefPubMed 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):391–395CrossRefPubMed
8.
Zurück zum Zitat 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):111–118CrossRefPubMed 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):111–118CrossRefPubMed
9.
Zurück zum Zitat 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):4252–4263 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):4252–4263
10.
Zurück zum Zitat 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):2279–2286PubMed 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):2279–2286PubMed
11.
Zurück zum Zitat 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):116–127CrossRefPubMed 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):116–127CrossRefPubMed
12.
Zurück zum Zitat 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):8190–8195CrossRefPubMedPubMedCentral 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):8190–8195CrossRefPubMedPubMedCentral
13.
Zurück zum Zitat 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):e63902CrossRefPubMedPubMedCentral 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):e63902CrossRefPubMedPubMedCentral
14.
Zurück zum Zitat 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 54:58–65CrossRefPubMed 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 54:58–65CrossRefPubMed
15.
Zurück zum Zitat 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):1614–1619CrossRefPubMedPubMedCentral 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):1614–1619CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat 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):80–86CrossRefPubMed 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):80–86CrossRefPubMed
17.
Zurück zum Zitat 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):910–915CrossRefPubMedPubMedCentral 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):910–915CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat 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):383–390CrossRefPubMed 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):383–390CrossRefPubMed
19.
Zurück zum Zitat Weber Lozada K, Keri RA (2011) Bisphenol A increases mammary cancer risk in two distinct mouse models of breast cancer. Biol Reprod 85(3):490–497CrossRefPubMedPubMedCentral Weber Lozada K, Keri RA (2011) Bisphenol A increases mammary cancer risk in two distinct mouse models of breast cancer. Biol Reprod 85(3):490–497CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat 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):1040–1046PubMedPubMedCentral 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):1040–1046PubMedPubMedCentral
21.
Zurück zum Zitat 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):23–28CrossRefPubMedPubMedCentral 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):23–28CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat 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):167–178CrossRefPubMedPubMedCentral 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):167–178CrossRefPubMedPubMedCentral
23.
Zurück zum Zitat 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):175–180CrossRefPubMed 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):175–180CrossRefPubMed
24.
Zurück zum Zitat 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):399–412CrossRefPubMed 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):399–412CrossRefPubMed
25.
Zurück zum Zitat 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):369–377PubMedPubMedCentral 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):369–377PubMedPubMedCentral
26.
Zurück zum Zitat 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):212–218CrossRefPubMed 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):212–218CrossRefPubMed
27.
Zurück zum Zitat 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):e94725CrossRefPubMedPubMedCentral 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):e94725CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat 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):41–47PubMed 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):41–47PubMed
29.
Zurück zum Zitat 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):e211CrossRefPubMedPubMedCentral 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):e211CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat 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–S289CrossRef 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–S289CrossRef
31.
Zurück zum Zitat Ailles LE, Weissman IL (2007) Cancer stem cells in solid tumors. Curr Opin Biotechnol 18(5):460–466CrossRefPubMed Ailles LE, Weissman IL (2007) Cancer stem cells in solid tumors. Curr Opin Biotechnol 18(5):460–466CrossRefPubMed
32.
Zurück zum Zitat 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):176–193CrossRefPubMed 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):176–193CrossRefPubMed
33.
Zurück zum Zitat 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):5506–5511CrossRefPubMed 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):5506–5511CrossRefPubMed
34.
Zurück zum Zitat 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. 29 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. 29
35.
Zurück zum Zitat 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):947–956CrossRefPubMedPubMedCentral 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):947–956CrossRefPubMedPubMedCentral
37.
Zurück zum Zitat 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):27288–27301CrossRefPubMedPubMedCentral 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):27288–27301CrossRefPubMedPubMedCentral
38.
Zurück zum Zitat 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):4598–4603CrossRefPubMedPubMedCentral 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):4598–4603CrossRefPubMedPubMedCentral
39.
Zurück zum Zitat 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):1354–1365CrossRefPubMed 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):1354–1365CrossRefPubMed
40.
Zurück zum Zitat 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 16:251–255 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 16:251–255
41.
Zurück zum Zitat 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):1671–1673 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):1671–1673
42.
Zurück zum Zitat 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):3983–3988CrossRefPubMedPubMedCentral 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):3983–3988CrossRefPubMedPubMedCentral
43.
Zurück zum Zitat 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):555–567CrossRefPubMedPubMedCentral 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):555–567CrossRefPubMedPubMedCentral
44.
Zurück zum Zitat Cailleau R, Young R, Olive M, Reeves WJ Jr (1974) Breast tumor cell lines from pleural effusions. J Natl Cancer Inst 53(3):661–674CrossRefPubMed Cailleau R, Young R, Olive M, Reeves WJ Jr (1974) Breast tumor cell lines from pleural effusions. J Natl Cancer Inst 53(3):661–674CrossRefPubMed
45.
Zurück zum Zitat 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):295–304CrossRefPubMed 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):295–304CrossRefPubMed
46.
Zurück zum Zitat Simpson E, Santen RJ (2015) Celebrating 75 years of oestradiol. J Mol Endocrinol 55(3):T1–T20CrossRefPubMed Simpson E, Santen RJ (2015) Celebrating 75 years of oestradiol. J Mol Endocrinol 55(3):T1–T20CrossRefPubMed
47.
Zurück zum Zitat 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):35986–35993CrossRefPubMed 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):35986–35993CrossRefPubMed
48.
Zurück zum Zitat 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):149–157CrossRefPubMed 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):149–157CrossRefPubMed
49.
Zurück zum Zitat 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):255–261CrossRefPubMed 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):255–261CrossRefPubMed
50.
Zurück zum Zitat Takeuchi T, Tsutsumi O (2002) Serum bisphenol A concentrations showed gender differences, possibly linked to androgen levels. Biochem Biophys Res Commun 291(1):76–78CrossRefPubMed Takeuchi T, Tsutsumi O (2002) Serum bisphenol A concentrations showed gender differences, possibly linked to androgen levels. Biochem Biophys Res Commun 291(1):76–78CrossRefPubMed
51.
Zurück zum Zitat 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 14:379CrossRefPubMedPubMedCentral 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 14:379CrossRefPubMedPubMedCentral
52.
Zurück zum Zitat Pike MC, Spicer DV, Dahmoush L, Press MF (1993) Estrogens, progestogens, normal breast cell proliferation, and breast cancer risk. Epidemiol Rev 15(1):17–35CrossRefPubMed Pike MC, Spicer DV, Dahmoush L, Press MF (1993) Estrogens, progestogens, normal breast cell proliferation, and breast cancer risk. Epidemiol Rev 15(1):17–35CrossRefPubMed
53.
Zurück zum Zitat 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):221–231CrossRefPubMed 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):221–231CrossRefPubMed
54.
Zurück zum Zitat 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):R45CrossRefPubMedPubMedCentral 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):R45CrossRefPubMedPubMedCentral
55.
Zurück zum Zitat 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):9339–9344CrossRefPubMed 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):9339–9344CrossRefPubMed
56.
Zurück zum Zitat 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):1264–1268PubMedPubMedCentral 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):1264–1268PubMedPubMedCentral
57.
Zurück zum Zitat 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):1253–1270CrossRefPubMedPubMedCentral 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):1253–1270CrossRefPubMedPubMedCentral
58.
Zurück zum Zitat 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):e28068CrossRefPubMedPubMedCentral 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):e28068CrossRefPubMedPubMedCentral
59.
Zurück zum Zitat 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):1833–1844CrossRefPubMed 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):1833–1844CrossRefPubMed
60.
Zurück zum Zitat 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):40–48CrossRefPubMed 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):40–48CrossRefPubMed
61.
Zurück zum Zitat 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):17969–17978CrossRefPubMed 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):17969–17978CrossRefPubMed
62.
Zurück zum Zitat 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):6725–6740CrossRefPubMedPubMedCentral 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):6725–6740CrossRefPubMedPubMedCentral
63.
Zurück zum Zitat 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):1011–1014CrossRefPubMed 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):1011–1014CrossRefPubMed
64.
Zurück zum Zitat 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):907–913CrossRefPubMed 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):907–913CrossRefPubMed
65.
Zurück zum Zitat 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):e88034CrossRefPubMedPubMedCentral 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):e88034CrossRefPubMedPubMedCentral
66.
Zurück zum Zitat 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):75–95CrossRefPubMedPubMedCentral 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):75–95CrossRefPubMedPubMedCentral
67.
Zurück zum Zitat 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):11603–11608CrossRefPubMedPubMedCentral 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):11603–11608CrossRefPubMedPubMedCentral
68.
Zurück zum Zitat Ropero AB, Soria B, Nadal A (2002) A nonclassical estrogen membrane receptor triggers rapid differential actions in the endocrine pancreas. Mol Endocrinol 16(3):497–505CrossRefPubMed Ropero AB, Soria B, Nadal A (2002) A nonclassical estrogen membrane receptor triggers rapid differential actions in the endocrine pancreas. Mol Endocrinol 16(3):497–505CrossRefPubMed
69.
Zurück zum Zitat Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414(6859):105–111CrossRefPubMed Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414(6859):105–111CrossRefPubMed
70.
Zurück zum Zitat 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):2813–2820CrossRef 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):2813–2820CrossRef
71.
Zurück zum Zitat Visvader JE, Lindeman GJ (2008) Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 8(10):755–768CrossRefPubMed Visvader JE, Lindeman GJ (2008) Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 8(10):755–768CrossRefPubMed
72.
Zurück zum Zitat 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):1514–1520CrossRefPubMedPubMedCentral 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):1514–1520CrossRefPubMedPubMedCentral
73.
Zurück zum Zitat 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 : JAT 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 : JAT
74.
Zurück zum Zitat 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):264–279CrossRefPubMedPubMedCentral 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):264–279CrossRefPubMedPubMedCentral
75.
Zurück zum Zitat 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):1289–1297CrossRefPubMed 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):1289–1297CrossRefPubMed
76.
Zurück zum Zitat 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):33–43CrossRefPubMed 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):33–43CrossRefPubMed
Metadaten
Titel
Bisphenol A Induces Sox2 in ER+ Breast Cancer Stem-Like Cells
verfasst von
M. Angeles Lillo
Cydney Nichols
Tiffany N. Seagroves
Gustavo A. Miranda-Carboni
Susan A. Krum
Publikationsdatum
27.02.2017
Verlag
Springer US
Erschienen in
Discover Oncology / Ausgabe 2/2017
Print ISSN: 1868-8497
Elektronische ISSN: 2730-6011
DOI
https://doi.org/10.1007/s12672-017-0286-5

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