Abstract
MCF-10F, an ERα negative human breast epithelial cell line derived from normal breast tissue, is able to form ductal structures in a tridimensional collagen matrix system. MCF-10F cells that are estrogen transformed (trMCF cells) progressively express phenotypes of in vitro cell transformation, including colony formation in agar methocel and loss of the ductulogenic capacity. Selection of these trMCF cells for invasiveness identified cells (bcMCF) that formed tumors in severe combined immunodeficient mice. The cell lines derived from those tumors (caMCF) were poorly differentiated ER, PR, and ERBB2 negative adenocarcinomas. These characteristics are similar to the human basal cell-like carcinomas. This in vitro–in vivo model demonstrates the importance of the basal cell type as a stem cell that reconstitutes the branching pattern of the breast and that is also target of a carcinogenic insult leading to transformation and cancer.
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Bouchardy C, Fioretta G, Verkooijen HM, Vlastos G, Schaefer P, Delaloye J-F, Neyroud-Caspar I, Balmer Majno S, Wespi Y, Forni M, Chappuis P, Sappino A-P, Rapiti E (2007) Recent increase of breast cancer incidence among women under the age of forty. Br J Cancer 96:1743–1746
Turner NC, Reis-Filho JS (2006) Basal-like breast cancer and the BRCA1 phenotype. Oncogene 25:5846–5853
Tawfik O, Kimler BF, Davis M, Stasik C, Lai SM, Mayo MS, Fan F, Donahue JK, Damjanov I, Thomas P, Connor C, Jewell WR, Smith H, Fabian CJ (2007) Grading invasive ductal carcinoma of the breast: advantages of using automated proliferation index instead of mitotic count. Virchows Arch 450(6):627–636
Perou CM, Sørlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, PergamenschikovA WC, Zhu SX, Lønning PE, Børresen-Dale AL, Brown PO, Botstein D (2000) Molecular portraits of human breast tumours. Nature 406:747–752
Sorlie T, Perou CM, Tibshirani R et al (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 98:10869–10874
Sorlie T, Tibshirani R, Parker J et al (2003) Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci U S A 100:8418–8423
van de Rijn M, Perou CM, Tibshirani R et al (2002) Expression of cytokeratins 17 and 5 identifies a group of breast carcinomas with poor clinical outcome. Am J Pathol 161:1991–1996
Rakha EA, El-Sayed ME, Green AR, Lee AH, Robertson JF, Ellis IO (2007) Prognostic markers in triple-negative breast cancer. Cancer 109:25–32
Chlebowski RT, Chen Z, Anderson GL, Rohan T, Aragaki A, Lane D, Dolan NC, Paskett ED, McTiernan A, Hubbell FA, Adams-Campbell LL, Prentice R (2005) Ethnicity and breast cancer: factors influencing differences in incidence and outcome. J Natl Cancer Inst 97:439–448
Newman LA, Mason J, Cote D, Vin Y, Carolin K, Bouwman D, Colditz GA (2002) African-American ethnicity, socioeconomic status, and breast cancer survival: a meta-analysis of 14 studies involving over 10,000 African-American and 40,000 White American patients with carcinoma of the breast. Cancer 94:2844–2854
Li CI, Malone KE, Daling JR (2002) Differences in breast cancer hormone receptor status and histology by race and ethnicity among women 50 years of age and older. Cancer Epidemiol Biomarkers Prev 11:601–607
Joslyn SA (2002) Hormone receptors in breast cancer: racial differences in distribution and survival. Breast Cancer Res Treat 73:45–59
Lippman ME (1993) The development of biological therapies for breast cancer. Science 259:631–632
Cunningham JE, Butler WM (2004) Racial disparities in female breast cancer in South Carolina: clinical evidence for a biological basis. Breast Cancer Res Treat 88:161–176
Millikan RC, Newman B, Tse CK, Moorman PG, Conway K, Dressler LG, Smith LV, Labbok MH, Geradts J, Bensen JT, Jackson S, Nyante S, Livasy C, Carey L, Earp HS, Perou CM (2008) Epidemiology of basal-like breast cancer. Breast Cancer Res Treat 109:123–139
Vona-Davis L, Rose DP (2009) The influence of socioeconomic disparities on breast cancer tumor biology and prognosis: a review. J Womens Health (Larchmt) 18(6):883–893
Troester MA, Swift-Scanlan T (2009) Challenges in studying the etiology of breast cancer subtypes. Breast Cancer Res 11(3):104
Lin NU, Claus E, Sohl J, Razzak AR, Arnaout A, Winer EP (2008) Sites of distant recurrence and clinical outcomes in patients with metastatic triple-negative breast cancer: high incidence of central nervous system metastases. Cancer 113(10):2638–2645
Anderson WF, Jatoi I, Devesa SS (2005) Distinct breast cancer incidence and prognostic patterns in the NCI’s SEER program: suggesting a possible link between etiology and outcome. Breast Cancer Res Treat 90:127–137
Wang X, Chao L, Li X, Ma G, Chen L, Zang Y, Zhou G (2010) Elevated expression of phosphorylated c-Jun NH2-terminal kinase in basal-like and “triple-negative” breast cancers. Hum Pathol 41:401–403
Bauer KR, Brown M, Cress RD, Parise CA, Caggiano V (2007) Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)- negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype: a population-based study from the California cancer Registry. Cancer 109:1721–1728
Cheang MC, Voduc D, Bajdik C, Leung S, McKinney S, Chia SK, Perou CM, Nielsen TO (2008) Basal-like breast cancer defined by five biomarkers has superior prognostic value than triple-negative phenotype. Clin Cancer Res 14:1368–1376
Phipps AI, Malone KE, Porter PL, Daling JR, Li CI (2008) Body size and risk of luminal, HER2-overexpressing, and triple-negative breast cancer in postmenopausal women. Cancer Epidemiol Biomarkers Prev 17:2078–2086
Russo IH, Russo J (2004) In vitro models for human breast cancer. In: Molecular basis of breast cancer prevention and treatment. Springer, Heidelberg, pp 227–80
Russo J, Hasan Lareef M, Balogh G, Guo S, Russo IH (2003) Estrogen and its metabolites are carcinogenic agents in human breast epithelial cells. J Steroid Biochem Mol Biol 87:1–25
Lareef MH, Garber J, Russo PA et al (2005) The estrogen antagonist ICI-182-780 does not inhibit the transformation phenotypes induced by 17-beta-estradiol and 4-OH estradiol in human breast epithelial cells. Int J Oncol 26:423–429
Fernandez SV, Russo IH, Russo J (2006) Estradiol and its metabolites 4-hydroxyestradiol and 2-hydroxyestradiol induce mutations in human breast epithelial cells. Int J Cancer 118:1862–1868
Russo J, Lareef MH, Tahin Q et al (2002) 17 Beta-estradiol is carcinogenic in human breast epithelial cells. J Steroid Biochem Mol Biol 80:149–162
Russo J, Fernandez SV, Russo PA et al (2006) 17-Beta-estradiol induces transformation and tumorigenesis in human breast epithelial cells. FASEB J 20:1622–1634
Huang Y, Fernandez SV, Goodwin S, Russo PA, Russo IH, Sutter TR, Russo J (2007) Epithelial to mesenchymal transition in human breast epithelial cells transformed by 17β-estradiol. Cancer Res 67:11147–11157
Russo J, Gusterson BA, Rogers AE et al (1990) Comparative study of human and rat mammary tumorigenesis. Lab Invest 62:244–278
Calaf G, Zhang PL, Alvarado MV, Estrada S, Russo J (1995) C-Ha-ras enhances the neoplastic transformation of human breast epithelial cells treated with chemical carcinogens. Int J Oncol 6:5–11
Charafe-Jauffret E, Ginestier C, Monville F, Finetti P, Adelaide J, Cervera N, Fekairi S, Xerri L, Jacquemier J, Brinbaum D, Bertucci F (2006) Gene expression profiling of breast cell lines identifies potential new basal markers. Oncogene 25:2273–2284
Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T, Clark L et al (2006) A collection of breast cancer cell lines for the study of funtionally distinct cancer subtypes. Cancer Cell 10:515–527
Sarrio D, Rodriguez-Pinilla SM, Hardisson D, Cano A, Moreno-Bueno G, Palacios J (2008) Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res 68:989–997
Moustakas A, Heldin C-H (2007) Signaling networks guiding epithelial-mesenchymal transitions during embryogenesis and cancer progression. Cancer Sci 98:1512–1520
Peinado H, Olmeda D, Cano A (2007) Snail, ZEB and bHLH factors in tumor progression: an alliance against the epithelial phenotype? Nature Rev 7:415–428
Han H-J, Russo J, Kohwi Y, Kohwi-Shigematsu T (2008) SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis. Nature 452:187–195
Klopocki E, Kristiansen G, Wild PJ, Klaman I, Castanos-Velez E, Singer G, Stohr R, Sauter G, Leibiger H, Essers L, Weber B, Hermann K, Rosenthal A, Hartmann A, Dahl E (2004) Loss of SFRP1 is associated with breast cancer progression and poor prognosis in early stage tumors. Int J Oncol 25:641–649
Henshall SM, Horvath LG, Quinn DI, Eggleton SA, Grygiel JJ, Stricker PD, Biankin AV, Kench JG, Sutherland RL (2006) Zinc-alpha2-glycoprotein expression as a predictor of metastatic prostate cancer following radical prostatectomy. J Natl Cancer Inst 98(19):1420–1424
Lapointe J, Li C, Higgins JP, van de Rijn M, Bair E, Montgomery K, Ferrari M, Egevad L, Rayford W, Bergerheim U, Ekman P, DeMarzo AM, Tibshirani R, Botstein D, Brown PO, Brooks JD, Pollack JR (2004) Gene expression profiling identifies clinically relevant subtypes of prostate cancer. Proc Natl Acad Sci U S A 101:811–816
Park D, Kåresen R, Axcrona U, Noren T, Sauer T (2007) Expression pattern of adhesion molecules (E-cadherin, alpha-, beta-, gamma-catenin and claudin-7), their influence on survival in primary breast carcinoma, and their corresponding axillary lymph node metastasis. APMIS 115:52–65
Sauer T, Pedersen MK, Ebeltoft K, Naess O (2005) Reduced expression of Claudin-7 in fine needle aspirates from breast carcinomas correlate with grading and metastatic disease. Cytopathology 16:193–198
Usami Y, Chiba H, Nakayama F, Ueda J, Matsuda Y, Sawada N, Komori T, Ito A, Yokozaki H (2006) Reduced expression of claudin-7 correlates with invasion and metastasis in squamous cell carcinoma of the esophagus. Hum Pathol 37:569–577
Usami Y, Satake S, Nakayama F, Matsumoto M, Ohnuma K, Komori T, Semba S, Ito A, Yokozaki H (2008) Snail-associated epithelial-mesenchymal transition promotes oesophageal squamous cell carcinoma motility and progression. J Pathol 215:330–339
Gosens I, Sessa A, den Hollander AI, Letteboer SJ, Belloni V, Arends ML, Le Bivic A, Cremers FP, Broccoli V, Roepman R (2007) FERM protein EPB4iL5 is a novel member of the mammalian CRB-MPP5 polarity complex. Exp Cell Res 313:3959–3970
Xu L, Begum S, Hearn JD, Hynes RO (2006) GPR56, an atypical G protein-coupled receptor, binds tissue transglutaminase, TG2, and inhibits melanoma tumor growth and metastasis. Proc Natl Acad Sci U S A 103:9023–9028
Xu L, Hynes RO (2007) GRP56 and TG2: possible roles in suppression of tumor growth by the microenvironment. Cell Cycle 6:160–165
Kwak MK, Lee HJ, Hur K, Parkdo J, Lee HS, Kim WH, Lee KU, Choe KJ, Guilford P, Yang HK (2008) Expression of Krüppel-like factor 5 in human gastric carcinomas. J Cancer Res Clin Oncol 134:163–167
Haase D, Meister M, Muley T, Hess J, Teurich S, Schnabel P, Hartenstein B, Angel P (2007) FMRD3, a novel putative tumour suppressor in NSCLC. Oncogene 26:4464–4468
Kairouz R, Parmar J, Lyons RJ, Swarbrick A, Musgrove EA, Daly RJ (2005) Hormonal regulation of the Grb14 signal modulator and its role in cell cycle progression of MCF-7 human breast cancer cells. J Cell Physiol 203:85–93
Lyons RJ, Deane R, Lynch DK, Ye ZS, Sanderson GM, Eyre HJ, Sutherland GR, Daly RJ (2001) Identification of a novel human tankyrase through its interaction with the adaptor protein Grb14. J Biol Chem 276:17172–17180
Rodrigues-Ferreira S, Di Tommaso A, Dimitrov A, Cazaubon S, Gruel N, Colasson H, Nicolas A, Chaverot N, Molinié V, Reyal F, Sigal-Zafrani B, Terris B, Delattre O, Radvanyi F, Perez F, Vincent-Salomon A, Nahmias C (2009) 8p22 MTUS1 gene product ATIP3 is a novel anti-mitotic protein underexpressed in invasive breast carcinoma of poor prognosis. PLoS One 4:e7239
Frank B, Bermejo JL, Hemminki K, Sutter C, Wappenschmidt B, Meindl A, Kiechle-Bahat M, Bugert P, Schmutzler RK, Bartram CR, Burwinkel B (2007) Copy number variant in the candidate tumor suppressor gene MTUS1 and familial breast cancer risk. Carcinogenesis 28:1442–1445
Di Benedetto M, Bièche I, Deshayes F, Vacher S, Nouet S, Collura V, Seitz I, Louis S, Pineau P, Amsellem-Ouazana D, Couraud PO, Strosberg AD, Stoppa-Lyonnet D, Lidereau R, Nahmias C (2006) Structural organization and expression of human MTUS1, a candidate 8p22 tumor suppressor gene encoding a family of angiotensin II AT2 receptor-interacting proteins, ATIP. Gene 380:127–136
Zuern C, Heimrich J, Kaufmann R, Richter KK, Settmacher U, Wanner C, Galle J, Seibold S (2010) Down-regulation of MTUS1 in human colon tumors. Oncol Rep 23:183–189
Huang D, Yu B, Deng Y, Sheng W, Peng Z, Qin W, Du X (2010) SFRP4 was overexpressed in colorectal carcinoma. J Cancer Res Clin Oncol 136:395–401
Saini S, Liu J, Yamamura S, Majid S, Kawakami K, Hirata H, Dahiya R (2009) Functional significance of secreted Frizzled-related protein 1 in metastatic renal cell carcinomas. Cancer Res 69:6815–6822
Hu J, Dong A, Fernandez-Ruiz V, Shan J, Kawa M, Martínez-Ansó E, Prieto J, Qian C (2009) Blockade of Wnt signaling inhibits angiogenesis and tumor growth in hepatocellular carcinoma. Cancer Res 69:6951–6959
Lin YW, Chung MT, Lai HC, De Yan M, Shih YL, Chang CC, Yu MH (2009) Methylation analysis of SFRP genes family in cervical adenocarcinoma. J Cancer Res Clin Oncol 135:1665–1674
Gauger KJ, Hugh JM, Troester MA, Schneider SS (2009) Down-regulation of sfrp1 in a mammary epithelial cell line promotes the development of a cd44high/cd24low population which is invasive and resistant to anoikis. Cancer Cell Int 9:11
Cheng H, Liu P, Wang ZC, Zou L, Santiago S, Garbitt V, Gjoerup OV, Iglehart JD, Miron A, Richardson AL, Hahn WC, Zhao JJ (2009) SIK1 couples LKB1 to p53-dependent anoikis and suppresses metastasis. Sci Signal 2:ra35
Takemori H, Katoh Hashimoto Y, Nakae J, Olson EN, Okamoto M (2009) Inactivation of HDAC5 by SIK1 in AICAR-treated C2C12 myoblasts. Endocr J 56:121–130
Kowanetz M, Lönn P, Vanlandewijck M, Kowanetz K, Heldin CH, Moustakas A (2008) TGFbeta induces SIK to negatively regulate type I receptor kinase signaling. J Cell Biol 182:655–662
Ding L, Niu C, Zheng Y, Xiong Z, Liu Y, Lin J, Sun H, Huang K, Yang W, Li X, Ye Q (2011) FHL1 interacts with estrogen receptors and regulates breast cancer cell growth. J Cell Mol Med 15:72–85
Lin J, Ding L, Jin R, Zhang H, Cheng L, Qin X, Chai J, Ye Q (2009) Four and a half LIM domains 1 and receptor interacting protein of 140kDa (RIP140) interact and cooperate in estrogen signaling. Int J Biochem Cell Biol 41:1613–1618
Engin F, Bertin T, Ma O, Jiang MM, Wang L, Sutton RE, Donehower LA, Lee B (2009) Notch signaling contributes to the pathogenesis of human osteosarcomas. Hum Mol Genet 18:1464–1470
Miyazono K (2009) Transforming growth factor-beta signaling in epithelial-mesenchymal transition and progression of cancer. Proc Jpn Acad Ser B Phys Biol Sci 85:314–323
Pennanen PT, Sarvilinna NS, Ylikomi TJ (2009) Gene expression changes during the development of estrogen-independent and antiestrogen-resistant growth in breast cancer cell culture models. Anticancer Drugs 20:51–58
Matsuo K, Owens JM, Tonko M, Elliott C, Chambers TJ, Wagner EF (2000) Fosl1 is a transcriptional target of c-Fos during osteoclast differentiation. Nat Genet 24:184–187
Young MR, Colburn NH (2006) Fra-1 a target for cancer prevention or intervention. Gene 379:1–11
Wang HY, Zhang JY, Cui JT, Tan XH, Li WM, Gu J, Lu YY (2010) Expression status of S100A14 and S100A4 correlates with metastatic potential and clinical outcome in colorectal cancer after surgery. Oncol Rep 23:45–52
Hua J, Chen D, Fu H, Zhang R, Shen W, Liu S, Sun K, Sun X (2010) Short hairpin RNA-mediated inhibition of S100A4 promotes apoptosis and suppresses proliferation of BGC823 gastric cancer cells in vitro and in vivo. Cancer Lett 292:41–47
Boye K, Mælandsmo GM (2010) S100A4 and metastasis: a small actor playing many roles. Am J Pathol 176:528–535
Ismail TM, Zhang S, Fernig DG, Gross S, Martin-Fernandez ML, See V, Tozawa K, Tynan CJ, Wang G, Wilkinson MC, Rudland PS, Barraclough R (2010) Self-association of calcium-binding protein S100A4 and metastasis. J Biol Chem 285:914–922
Russo J, Hu YF, Yang X, Russo IH (2000) Developmental, cellular and molecular basis of human breast cancer. J Natl Cancer Inst Monogr 27:17–38
Tiezzi DG, Fernandez SV, Russo J (2007) Epithelial to mesenchymal transition during breast cancer progression. Int J Oncol 31:823–827
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Work supported by grant U01 ES/CA 12771 from the National Institute of Environmental Health Sciences (NIEHS) and the National Cancer Institute (NCI), NIH, DHHS. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIEHS or NCI, NIH.
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Russo, J., Russo, I.H. (2011). The Role of the Basal Stem Cell of the Human Breast in Normal Development and Cancer. In: Rhim, J., Kremer, R. (eds) Human Cell Transformation. Advances in Experimental Medicine and Biology, vol 720. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-0254-1_10
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