Skip to main content
SpringerLink
Log in
Book cover

The Pathobiology of Breast Cancer pp 117–134Cite as

Stem Cells in Breast Cancer

  • Chapter
  • First Online:

  • 1037 Accesses

Abstract

In the mammary gland, DeOme et al. [1] demonstrated that fragments of different parenchymal portions were able to generate fully functional mammary outgrowths in mice, forming ductal and lobulo-alveolar structures composed by epithelial and myoepithelial cells. This seminal work demonstrated that stem cells in adult structures have the ability for self-renewal and for generating a differentiated progeny. The progeny from a single cell might comprise the epithelial population of a fully developed lactating mammary outgrowth in mice was further demonstrated by Kordon and Smith [2]. Russo and coworkers [3–5], demonstrated that cancer, started in terminal end buds (TEBs) present in the mammary gland of young virgin rats. The analysis of these structures by electron microscopy allowed them to characterize their cellular composition based upon cell and nuclear size, nuclear-cytoplasmic ratio, amount of chromatin condensation, electron density of the cytoplasm, number and distribution of organelles, and presence or absence of Mg++ and Na+K+-dependent ATPases. Based upon these criteria, in addition to myoepithelial cells, three types of epithelial cells were identified: Light, intermediate and dark cells [4, 5]. Dark cells were found to be the predominant type in TEBs, intermediate and myoepithelial cells were present in significantly lower percentages and light cells were only occasionally seen, therefore their percentage was combined with that of intermediate cells. The analysis of the DNA labeling index revealed that all the cell types proliferated, although at different rates, depending upon the type of cells and of their location within the mammary gland tree. Cell proliferation was maximal in intermediate cells located in TEBs, being significantly lower in dark and myoepithelial cells found in the same location. High cell proliferation was associated with greater incorporation of H3-DMBA, and a progressive dominance of intermediate cells in DMBA-induced intraductal proliferations (IDPs) and in ductal carcinomas [5, 6]. These results indicated that intermediate cells were not only the targets of the carcinogen but also the stem cells of mammary carcinomas. Bennett et al. [7] demonstrated that intermediate cells isolated from DMBA-induced mammary tumors originated two cell types in culture, the dark cell, representing a terminally differentiated cell or a class in transition to differentiation, and intermediate cells, which could represent an undifferentiated, or stem cell, a progenitor of dark and myoepithelial cells. Rudland and coworkers [8] isolated and characterized from the normal rat mammary gland and from DMBA-induced mammary adenocarcinomas epithelial cells that were cuboidal and gave rise to a mixture of cuboidal and spindle-shaped cells resembling fibroblasts. In confluent cultures, cuboidal cells acquired the morphology of a third type of cells, which were dark, polygonal and with many small vacuoles, resembling the dark cells ultrastructurally described by Russo et al. [5]. Chepko and Smith [9] differentiated three division-competent cell populations in the murine mammary epithelium, a subset of “large light cells” structurally and functionally compatible with early stages of secretory differentiation, “small light cells” that were the least differentiated, suggesting that the large light cells were a direct precursor to terminally differentiated cells, both secretory and myoepithelial, confirming the Russo’s work [5].

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  1. Deome KB, Faulkin LJ Jr, Bern HA, Blair PB (1959) Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice. Cancer Res 19:515–520

    CAS  PubMed  Google Scholar 

  2. Kordon EC, Smith GH (1998) An entire functional mammary gland may comprise the progeny from a single cell. Development 125:1921–1930

    CAS  PubMed  Google Scholar 

  3. Russo J, Saby J, Isenberg WM, Russo IH (1977) Pathogenesis of mammary carcinomas induced in rats by 7,12-dimethylbenz(a)anthracene. J Natl Cancer Inst 59:436–445

    Google Scholar 

  4. Russo J, Isenberg W, Ireland M, Russo I (1976) Ultrastructural changes in the mammary epithelial cell population during neoplastic development induced by a chemical carcinogen. Electron Microscopy Society of America Proceedings, pp 250–251

    Google Scholar 

  5. Russo J, Tait L, Russo IH (1983) Susceptibility of the mammary gland to carcinogenesis. III. The cell of origin of rat mammary carcinoma. Am J Pathol 113:50–66

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Russo J, Tay LK, Russo IH (1982) Differentiation of the mammary gland and susceptibility to carcinogenesis. Breast Cancer Res Treat 2:5–73

    Article  CAS  PubMed  Google Scholar 

  7. Bennett DC, Peachey LA, Durbin H, Rudland PS (1978) A possible mammary stem cell line. Cell 15:283–298

    Article  CAS  PubMed  Google Scholar 

  8. Rudland PS, Bennett DC, Warburton MJ (1980) Isolation and characterization of epithelial stem-cell cell lines from the rat mammary gland. Br J Cancer 41:666–668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Chepko G, Smith GH (1997) Three division-competent, structurally-distinct cellpopulations contribute to murine mammary epithelial renewal. Tissue Cell 29:239–253

    Article  CAS  PubMed  Google Scholar 

  10. Smith GH, Mehrel T, Roop DR (1990) Differential keratin gene expression in developing, differentiating, preneoplastic, and neoplastic mouse mammary epithelium. Cell Growth Differ 1:161–170

    CAS  PubMed  Google Scholar 

  11. Stingl J, Eaves CJ, Kuusk U, Emerman JT (1998) Phenotypic and functional characterization in vitro of a multipotent epithelial cell present in the normal adult human breast. Differentiation 63:201–213

    Article  CAS  PubMed  Google Scholar 

  12. Stingl J, Eaves CJ, Zandieh I, Emerman JT (2001) Characterization of bipotent mammary epithelial progenitor cells in normal adult human breast tissue. Breast Cancer Res Treat 67:93–109

    Article  CAS  PubMed  Google Scholar 

  13. 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

    CAS  PubMed  Google Scholar 

  14. Kenney NJ, Smith GH, Lawrence E, Barrett JC, Salomon DS (2001) Identification of stem cell units in the terminal end bud and duct of the mouse mammary gland. J Biomed Biotechnol 1:133–143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Spangrude GJ, Aihara Y, Weissman IL, Klein J (1988) The stem cell antigens Sca-1 and Sca-2 subdivide thymic and peripheral T lymphocytes into unique subsets. J Immunol 141:3697–3707

    CAS  PubMed  Google Scholar 

  16. Welm BE, Tepera SB, Venezia T, Graubert TA, Rosen JM, Goodell MA (2002) Sca-1(pos) cells in the mouse mammary gland represent an enriched progenitor cell population. Dev Biol 245:42–56

    Article  CAS  PubMed  Google Scholar 

  17. Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ, Lagutina I, Grosveld GC, Osawa M, Nakauchi H, Sorrentino BP (2001) The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 7:1028–1034

    Article  CAS  PubMed  Google Scholar 

  18. Alvi AJ, Clayton H, Joshi C, Enver T, Ashworth A, Vivanco MM, Dale TC, Smalley MJ (2003) Functional and molecular characterisation of mammary side population cells. Breast Cancer Res 5:R1–R8

    Article  PubMed  Google Scholar 

  19. Gudjonsson T, Villadsen R, Nielsen HL, Ronnov-Jessen L, Bissell MJ, Petersen OW (2002) Isolation, immortalization, and characterization of a human breast epithelial cell line with stem cell properties. Genes Dev 16:693–706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, Wicha MS (2003) In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 17:1253–1270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Jia Y, Qi C, Zhang Z, Zhu YT, Rao SM, Zhu YJ (2005) Peroxisome proliferator-activated receptor-binding protein null mutation results in defective mammary gland development. J Biol Chem 280:10766–10773

    Article  CAS  PubMed  Google Scholar 

  22. Couse JF, Korach KS (1999) Estrogen receptor null mice: what have we learned and where will they lead us? Endocr Rev 20:358–417

    Article  CAS  PubMed  Google Scholar 

  23. 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

    Article  CAS  PubMed  Google Scholar 

  24. Russo J, Russo IH (1997) Role of differentiation in the pathogenesis and prevention of breast cancer. Endocr Relat Cancer 4:7–21

    Article  CAS  Google Scholar 

  25. Petersen OW, Gudjonsson T, Villadsen R, Bissell MJ, Ronnov-Jessen L (2003) Epithelial progenitor cell lines as models of normal breast morphogenesis and neoplasia. Cell Prolif 36(Suppl 1):33–44

    Article  PubMed  PubMed Central  Google Scholar 

  26. Clarke RB, Anderson E, Howell A, Potten CS (2003) Regulation of human breast epithelial stem cells. Cell Prolif 36(Suppl 1):45–58

    Article  CAS  PubMed  Google Scholar 

  27. Clarke RB, Spence K, Anderson E, Howell A, Okano H, Potten CS (2005) A putative human breast stem cell population is enriched for steroid receptor-positive cells. Dev Biol 277:443–456

    Article  CAS  PubMed  Google Scholar 

  28. Clayton H, Titley I, Vivanco M (2004) Growth and differentiation of progenitor/stem cells derived from the human mammary gland. Exp Cell Res 297:444–460

    Article  CAS  PubMed  Google Scholar 

  29. Russo J, Fernandez SV, Russo PA, Fernbaugh R, Sheriff FS, Lareef HM, Garber J, Russo IH (2006) 17 beta estradiol induces transformation and tumorigenesis in human breast epithelial cells. FASEB J. 20:1622–1634

    Google Scholar 

  30. Huang Y, Fernandez S, Goodwin S, Russo PA, Russo IH, Sutter T, Russo J (2007) Epithelial to mesenchymal transition in human breast epithelial cells transformed by 17- beta- estradiol. Cancer Res 67:11147–11157

    Google Scholar 

  31. Russo J, Balogh GA, Chen J, Fernandez SV, Fernbaugh R, Heulings R, Mailo DA, Moral R, Russo PA, Sheriff F, Vanegas JE, Wang R, Russo IH (2006) The concept of stem cell in the mammary gland and its implication in morphogenesis, cancer and prevention. Front Biosci 11:151–172

    Article  CAS  PubMed  Google Scholar 

  32. Shim GJ, Wang L, Andersson S, Nagy N, Kis LL, Zhang Q, Makela S, Warner M, Gustafsson JA (2003) Disruption of the estrogen receptor beta gene in mice causes myeloproliferative disease resembling chronic myeloid leukemia with lymphoid blast crisis. Proc Natl Acad Sci U S A 100:6694–6699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Imamov O, Morani A, Shim GJ, Omoto Y, Thulin-Andersson C, Warner M, Gustafsson JA (2004) Estrogen receptor beta regulates epithelial cellular differentiation in the mouse ventral prostate. Proc Natl Acad Sci U S A 101:9375–9380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Pais V, Leav I, Lau KM, Jiang Z, Ho SM (2003) Estrogen receptor-beta expression in human testicular germ cell tumors. Clin Cancer Res 9:4475–4482

    CAS  PubMed  Google Scholar 

  35. Palmieri C, Saji S, Sakaguchi H, Cheng G, Sunters A, O’Hare MJ, Warner M, Gustafsson JA, Coombes RC, Lam EW (2004) The expression of oestrogen receptor (ER)-beta and its variants, but not ERalpha, in adult human mammary fibroblasts. J Mol Endocrinol 33:35–50

    Article  CAS  PubMed  Google Scholar 

  36. 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

    Article  CAS  PubMed  Google Scholar 

  37. Hu YF, Lau KM, Ho SM, Russo J (1998) Increased expression of estrogen receptor beta in chemically transformed human breast epithelial cells. Int J Oncol 12:1225–1228

    CAS  PubMed  Google Scholar 

  38. Russo J, Lareef MH, Tahin Q, Hu YF, Slater C, Ao X, Russo IH (2002) 17Beta-estradiol is carcinogenic in human breast epithelial cells. J Steroid Biochem Mol Biol 80:149–162

    Article  CAS  PubMed  Google Scholar 

  39. Lareef MH, Garber J, Russo PA, Russo IH, Heulings R, Russo J (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

    CAS  PubMed  Google Scholar 

  40. Fernandez SV, Russo IH, Lareef M, Balsara B, Russo J (2005) Comparative genomic hybridization of human breast epithelial cells transformed by estrogen and its metabolites. Int J Oncol 26:691–695

    CAS  PubMed  Google Scholar 

  41. Kehrl JH (1995) Hematopoietic lineage commitment: role of transcription factors. Stem Cells 13:223–241

    Article  CAS  PubMed  Google Scholar 

  42. Shivdasani RA, Orkin SH (1995) Erythropoiesis and globin gene expression in mice lacking the transcription factor NF-E2. Proc Natl Acad Sci U S A 92:8690–8694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Tsai S, Bartelmez S, Sitnicka E, Collins S (1994) Lymphohematopoietic progenitors immortalized by a retroviral vector harboring a dominant-negative retinoic acid receptor can recapitulate lymphoid, myeloid, and erythroid development. Genes Dev 8:2831–2841

    Article  CAS  PubMed  Google Scholar 

  44. Briggs JA, Burrus GR, Stickney BD, Briggs RC (1992) Cloning and expression of the human myeloid cell nuclear differentiation antigen: regulation by interferon alpha. J Cell Biochem 49:82–92

    Article  CAS  PubMed  Google Scholar 

  45. Briggs R, Dworkin L, Briggs J, Dessypris E, Stein J, Stein G, Lian J (1994) Interferon alpha selectively affects expression of the human myeloid cell nuclear differentiation antigen in late stage cells in the monocytic but not the granulocytic lineage. J Cell Biochem 54:198–206

    Article  CAS  PubMed  Google Scholar 

  46. Briggs RC, Briggs JA, Ozer J, Sealy L, Dworkin LL, Kingsmore SF, Seldin MF, Kaur GP, Athwal RS, Dessypris EN (1994) The human myeloid cell nuclear differentiation antigen gene is one of at least two related interferon-inducible genes located on chromosome 1q that are expressed specifically in hematopoietic cells. Blood 83:2153–2162

    CAS  PubMed  Google Scholar 

  47. Briggs RC, Kao WY, Dworkin LL, Briggs JA, Dessypris EN, Clark J (1994) Regulation and specificity of MNDA expression in monocytes, macrophages, and leukemia/B lymphoma cell lines. J Cell Biochem 56:559–567

    Article  CAS  PubMed  Google Scholar 

  48. Hamada T, Tashiro K, Tada H, Inazawa J, Shirozu M, Shibahara K, Nakamura T, Martina N, Nakano T, Honjo T (1996) Isolation and characterization of a novel secretory protein, stromal cell-derived factor-2 (SDF-2) using the signal sequence trap method. Gene 176:211–214

    Article  CAS  PubMed  Google Scholar 

  49. Lindahl T, Satoh MS, Poirier GG, Klungland A (1995) Post-translational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem Sci 20:405–411

    Article  CAS  PubMed  Google Scholar 

  50. Menissier-de Murcia J, Molinete M, Gradwohl G, Simonin F, de Murcia G (1989) Zinc-binding domain of poly(ADP-ribose)polymerase participates in the recognition of single strand breaks on DNA. J Mol Biol 210:229–233

    Article  CAS  PubMed  Google Scholar 

  51. Boulikas T (1991) Relation between carcinogenesis, chromatin structure and poly(ADP-ribosylation) (review). Anticancer Res 11:489–527

    CAS  PubMed  Google Scholar 

  52. Althaus FR, Hofferer L, Kleczkowska HE, Malanga M, Naegeli H, Panzeter PL, Realini CA (1994) Histone shuttling by poly ADP-ribosylation. Mol Cell Biochem 138:53–59

    Article  CAS  PubMed  Google Scholar 

  53. Malanga M, Pleschke JM, Kleczkowska HE, Althaus FR (1998) Poly(ADP-ribose) binds to specific domains of p53 and alters its DNA binding functions. J Biol Chem 273:11839–11843

    Article  CAS  PubMed  Google Scholar 

  54. Pleschke JM, Kleczkowska HE, Strohm M, Althaus FR (2000) Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J Biol Chem 275:40974–40980

    Article  CAS  PubMed  Google Scholar 

  55. Zahradka P, Ebisuzaki K (1982) A shuttle mechanism for DNA-protein interactions. The regulation of poly(ADP-ribose) polymerase. Eur J Biochem 127:579–585

    Article  CAS  PubMed  Google Scholar 

  56. Le Rhun Y, Kirkland JB, Shah GM (1998) Cellular responses to DNA damage in the absence of Poly(ADP-ribose) polymerase. Biochem Biophys Res Commun 245:1–10

    Article  PubMed  Google Scholar 

  57. Cosi C, Marien M (1999) Implication of poly (ADP-ribose) polymerase (PARP) in neurodegeneration and brain energy metabolism. Decreases in mouse brain NAD+ and ATP caused by MPTP are prevented by the PARP inhibitor benzamide. Ann N Y Acad Sci 890:227–239

    Article  CAS  PubMed  Google Scholar 

  58. Ha HC, Snyder SH (2000) Poly(ADP-ribose) polymerase-1 in the nervous system. Neurobiol Dis 7:225–239

    Article  CAS  PubMed  Google Scholar 

  59. Pieper AA, Verma A, Zhang J, Snyder SH (1999) Poly (ADP-ribose) polymerase, nitric oxide and cell death. Trends Pharmacol Sci 20:171–181

    Article  CAS  PubMed  Google Scholar 

  60. MacMahon B, Cole P, Lin TM, Lowe CR, Mirra AP, Ravnihar B, Salber EJ, Valaoras VG, Yuasa S (1970) Age at first birth and breast cancer risk. Bull World Health Organ 43:209–221

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Lambe M, Hsieh CC, Chan HW, Ekbom A, Trichopoulos D, Adami HO (1996) Parity, age at first and last birth, and risk of breast cancer: a population-based study in Sweden. Breast Cancer Res Treat 38:305–311

    Article  CAS  PubMed  Google Scholar 

  62. Kelsey JL, Gammon MD, John EM (1993) Reproductive factors and breast cancer. Epidemiol Rev 15:36–47

    CAS  PubMed  Google Scholar 

  63. Moon RC (1981) Influence of pregnancy and lactation on experimental mammary carcinogenesis. In: Pike MC, Siiteri PK, Welsch CW (eds) Banbury Report 8 hormones and breast cancer. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 353–394

    Google Scholar 

  64. Sinha DK, Pazik JE, Dao TL (1988) Prevention of mammary carcinogenesis in rats by pregnancy: effect of full-term and interrupted pregnancy. Br J Cancer 57:390–394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Yang J, Yoshizawa K, Nandi S, Tsubura A (1999) Protective effects of pregnancy and lactation against N-methyl-N-nitrosourea-induced mammary carcinomas in female Lewis rats. Carcinogenesis 20:623–628

    Article  PubMed  Google Scholar 

  66. Welsch CW (1985) Host factors affecting the growth of carcinogen-induced rat mammary carcinomas: a review and tribute to Charles Brenton Huggins. Cancer Res 45:3415–3443

    CAS  PubMed  Google Scholar 

  67. Russo J, Russo IH (1980) Influence of differentiation and cell kinetics on the susceptibility of the rat mammary gland to carcinogenesis. Cancer Res 40:2677–2687

    CAS  PubMed  Google Scholar 

  68. Swanson SM, Whitaker LM, Stockard CR, Myers RB, Oelschlager D, Grizzle WE, Juliana MM, Grubbs CJ (1997) Hormone levels and mammary epithelial cell proliferation in rats treated with a regimen of estradiol and progesterone that mimics the preventive effect of pregnancy against mammary cancer. Anticancer Res 17:4639–4645

    CAS  PubMed  Google Scholar 

  69. Rajkumar L, Guzman RC, Yang J, Thordarson G, Talamantes F, Nandi S (2001) Short-term exposure to pregnancy levels of estrogen prevents mammary carcinogenesis. Proc Natl Acad Sci U S A 98:11755–11759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Tay LK, Russo J (1981) Formation and removal of 7,12-dimethylbenz[a]anthracene--nucleic acid adducts in rat mammary epithelial cells with different susceptibility to carcinogenesis. Carcinogenesis 2:1327–1333

    Article  CAS  PubMed  Google Scholar 

  71. Russo IH, Koszalka M, Russo J (1991) Comparative study of the influence of pregnancy and hormonal treatment on mammary carcinogenesis. Br J Cancer 64:481–484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Russo J, Santucci-Pereira J, de Cicco RL, Sheriff F, Russo PA, Peri S, Slifker M, Ross E, Mello ML, Vidal BC, Belitskaya-Levy I, Arslan A, Zeleniuch-Jacquotte A, Bordas P, Lenner P, Ahman J, Afanasyeva Y, Hallmans G, Toniolo P, Russo IH (2011) Pregnancy-induced chromatin remodeling in the breast of postmenopausal women. Int J Cancer. doi:10.1002/ijc.27323

    Google Scholar 

  73. Belitskaya-Levy I, Zeleniuch-Jacquotte A, Russo J, Russo IH, Bordas P, Ahman J, Afanasyeva Y, Johansson R, Lenner P, Li X, de Cicco-Lopez RL, Peri S, Ross E, Russo PA, Santucci-Pereira J, Sheriff FS, Slifker M, Hallmans G, Toniolo P, Arslan AA (2011) Characterization of a genomic signature of pregnancy identified in the breast. Cancer Prev Res 4:1457–1464

    Article  Google Scholar 

  74. Thordarson G, Jin E, Guzman RC, Swanson SM, Nandi S, Talamantes F (1995) Refractoriness to mammary tumorigenesis in parous rats: is it caused by persistent changes in the hormonal environment or permanent biochemical alterations in the mammary epithelia? Carcinogenesis 16:2847–2853

    Article  CAS  PubMed  Google Scholar 

  75. Wagner KU, Boulanger CA, Henry MD, Sgagias M, Hennighausen L, Smith GH (2002) An adjunct mammary epithelial cell population in parous females: its role in functional adaptation and tissue renewal. Development 129:1377–1386

    CAS  PubMed  Google Scholar 

  76. Henry MD, Triplett AA, Oh KB, Smith GH, Wagner KU (2004) Parity-induced mammary epithelial cells facilitate tumorigenesis in MMTV-neu transgenic mice. Oncogene 23:6980–6985

    Article  CAS  PubMed  Google Scholar 

  77. Boulanger CA, Wagner KU, Smith GH (2005) Parity-induced mouse mammary epithelial cells are pluripotent, self-renewing and sensitive to TGF-beta1 expression. Oncogene 24:552–560

    Article  CAS  PubMed  Google Scholar 

  78. Trichopoulos D, Lagiou P, Adami HO (2005) Towards an integrated model for breast cancer etiology: the crucial role of the number of mammary tissue-specific stem cells. Breast Cancer Res 7:13–17

    Article  PubMed  Google Scholar 

  79. Srivastava P, Russo J, Russo IH (1997) Chorionic gonadotropin inhibits rat mammary carcinogenesis through activation of programmed cell death. Carcinogenesis 18:1799–1808

    Article  CAS  PubMed  Google Scholar 

  80. Srivastava P, Russo J, Russo IH (1999) Inhibition of rat mammary tumorigenesis by human chorionic gonadotropin associated with increased expression of inhibin. Mol Carcinog 26:10–19

    Article  CAS  PubMed  Google Scholar 

  81. Medina D, Kittrell FS (2003) p53 function is required for hormone-mediated protection of mouse mammary tumorigenesis. Cancer Res 63:6140–6143

    CAS  PubMed  Google Scholar 

  82. Medina D (2004) Breast cancer: the protective effect of pregnancy. Clin Cancer Res 10:380S–384S

    Article  CAS  PubMed  Google Scholar 

  83. Sivaraman L, Conneely OM, Medina D, O’Malley BW (2001) p53 is a potential mediator of pregnancy and hormone-induced resistance to mammary carcinogenesis. Proc Natl Acad Sci U S A 98:12379–12384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Ginger MR, Gonzalez-Rimbau MF, Gay JP, Rosen JM (2001) Persistent changes in gene expression induced by estrogen and progesterone in the rat mammary gland. Mol Endocrinol 15:1993–2009

    Article  CAS  PubMed  Google Scholar 

  85. Ginger MR, Rosen JM (2003) Pregnancy-induced changes in cell-fate in the mammary gland. Breast Cancer Res 5:192–197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. D’Cruz CM, Moody SE, Master SR, Hartman JL, Keiper EA, Imielinski MB, Cox JD, Wang JY, Ha SI, Keister BA, Chodosh LA (2002) Persistent parity-induced changes in growth factors, TGF-beta3, and differentiation in the rodent mammary gland. Mol Endocrinol 16:2034–2051

    Article  PubMed  CAS  Google Scholar 

  87. Russo J, Russo IH (2004) Endocrine control of breast development. In: Russo J, Russo IH (eds) Molecular basis of breast cancer: prevention and treatment, 1st edn. Springer, Berlin, pp 64–67

    Chapter  Google Scholar 

  88. Russo J, Russo IH (1997) Role of hCG and inhibin in breast cancer. Int J Cancer 4:297–306

    Google Scholar 

  89. Santucci-Pereira J, Russo J (2016) Biological basis of breast cancer. In: Russo J (ed) The pathobiology of breast cancer, chapter 10

    Google Scholar 

  90. Porter S, Scott SD, Sassoon EM, Williams MR, Jones JL, Girling AC, Ball RY, Edwards DR (2004) Dysregulated expression of adamalysin-thrombospondin genes in human breast carcinoma. Clin Cancer Res 10:2429–2440

    Article  CAS  PubMed  Google Scholar 

  91. Lind GE, Kleivi K, Meling GI, Teixeira MR, Thiis-Evensen E, Rognum TO, Lothe RA (2006) ADAMTS1, CRABP1, and NR3C1 identified as epigenetically deregulated genes in colorectal tumorigenesis. Cell Oncol 28:259–272

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Gustavsson H, Wang W, Jennbacken K, Welen K, Damber JE (2009) ADAMTS1, a putative anti-angiogenic factor, is decreased in human prostate cancer. BJU Int 104:1786–1790

    Article  CAS  PubMed  Google Scholar 

  93. Gill ZP, Perks CM, Newcomb PV, Holly JM (1997) Insulin-like growth factor-binding protein (IGFBP-3) predisposes breast cancer cells to programmed cell death in a non-IGF-dependent manner. J Biol Chem 272:25602–25607

    Article  CAS  PubMed  Google Scholar 

  94. Kim HS, Ingermann AR, Tsubaki J, Twigg SM, Walker GE, Oh Y (2004) Insulin-like growth factor-binding protein 3 induces caspase-dependent apoptosis through a death receptor-mediated pathway in MCF-7 human breast cancer cells. Cancer Res 64:2229–2237

    Article  CAS  PubMed  Google Scholar 

  95. Mahadev K, Raval G, Bharadwaj S, Willingham MC, Lange EM, Vonderhaar B, Salomon D, Prasad GL (2002) Suppression of the transformed phenotype of breast cancer by tropomyosin-1. Exp Cell Res 279:40–51

    Article  CAS  PubMed  Google Scholar 

  96. Bharadwaj S, Thanawala R, Bon G, Falcioni R, Prasad GL (2005) Resensitization of breast cancer cells to anoikis by tropomyosin-1: role of Rho kinase-dependent cytoskeleton and adhesion. Oncogene 24:8291–8303

    Article  CAS  PubMed  Google Scholar 

  97. Russo J, Ruso IH (eds) (2013) Methodological Approach to studying the human breast. In: Role of the trasnscriptome in breast cancer prevention. Springer, New York, pp 243–268

    Google Scholar 

  98. Russo J, Russo IH (1978) DNA labeling index and structure of the rat mammary gland as determinants of its susceptibility to carcinogenesis. J Natl Cancer Inst 61:1451–1459

    CAS  PubMed  Google Scholar 

  99. Russo IH, Russo J (1978) Developmental stage of the rat mammary gland as determinant of its susceptibility to 7,12-dimethylbenz[a]anthracene. J Natl Cancer Inst 61:1439–1449

    CAS  PubMed  Google Scholar 

  100. Russo J, Gusterson BA, Rogers AE, Russo IH, Wellings SR, van Zwieten MJ (1990) Comparative study of human and rat mammary tumorigenesis. Lab Invest 62:244–278

    CAS  PubMed  Google Scholar 

  101. Russo J (1983) Basis of cellular autonomy in the susceptibility to carcinogenesis. Toxicol Pathol 11:149–166

    Article  CAS  PubMed  Google Scholar 

  102. Russo J, Russo IH (1998) Role of pregnancy and chorionic gonadotropin in breast cancer prevention. In: Birkhauser MH, Rozenbaum H (eds) Proc IV European Congress on Menopause. ESKA, Paris, pp 133–142

    Google Scholar 

  103. Russo J, Russo IH (2004) Biological and molecular basis of breast cancer. Springer Verlag, Heidelberg

    Book  Google Scholar 

  104. Russo J, Rivera R, Russo IH (1992) Influence of age and parity on the development of the human breast. Breast Cancer Res Treat 23:211–218

    Article  CAS  PubMed  Google Scholar 

  105. Vessey MP, McPherson K, Roberts MM, Neil A, Jones L (1985) Fertility in relation to the risk of breast cancer. Br J Cancer 52:625–628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Kelsey JL, Horn-Ross PL (1993) Breast cancer: magnitude of the problem and descriptive epidemiology. Epidemiol Rev 15:7–16

    CAS  PubMed  Google Scholar 

  107. Russo I, Russo J (1994) Role of hCG and inhibin in breast-cancer (review). Int J Oncol 4:297–306

    CAS  PubMed  Google Scholar 

  108. Russo J, Balogh GA, Russo IH (2008) Full-term pregnancy induces a specific genomic signature in the human breast. Cancer Epidemiol Biomarkers Prev 17:51–66

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Fox Chase Cancer Center, Philadelphia, PA, USA

    Jose Russo

Authors
  1. Jose Russo
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Russo, J. (2016). Stem Cells in Breast Cancer. In: The Pathobiology of Breast Cancer. Springer, Cham. https://doi.org/10.1007/978-3-319-40815-6_6

Download citation

Publish with us

Policies and ethics

Search

Navigation