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Mammary Gland Growth and Development from the Postnatal Period to Postmenopause: Ovarian Steroid Receptor Ontogeny and Regulation in the Mouse

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Abstract

Ovarian steroid hormones play a critical role inregulating mammary gland growth and development. Themammary gland sequentially acquires and cyclicallyexhibits proliferative responses to estrogen and/or progesterone from birth to postmenopause. Thefocus of this review is to presentour currentunderstanding of estrogen and progesterone receptordistribution in epithelial and stromal cells and theirfunctions in relation to mammary gland development.Insights gained from the study of the normal mammarygland are relevant to our understanding of theconditions which may predispose women to the developmentof breast cancer as well as to alterations inhormonal regulation that occur in breastcancer.

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References

  1. S. Z. Haslam (1987). Role of sex steroid hormones in normal mammary gland function. In M. C. Neville and C. W. Daniel (eds.), The Mammary Gland, Development, Regulation and Function, Plenum Press, New York, pp. 499-533.

    Google Scholar 

  2. S. Z. Haslam and G. Shyamala (1979). Effect of oestradiol progesterone receptors in normal mammary glands and its relationship to lactation. Biochem. J. 182:127-131.

    Google Scholar 

  3. S. Z. Haslam and G. Shyamala (1979). Progesterone receptors normal mammary glands of mice: Characterization and rela-tionship to development. Endocrinology 105:786-795.

    Google Scholar 

  4. S. Z. Haslam and G. Shyamala (1980). Progesterone receptors normal mammary gland: receptor modulations in relation to differentiation. J. Cell. Biol. 86:730-737.

    Google Scholar 

  5. S. Nandi (1958). Endocrine control of mammary gland develop-ment and function in the C3H/HeCrg1 mouse. J. Natl. Cancer Inst. 21:1039-1063.

    Google Scholar 

  6. S. Z. Haslam (1989). The ontogeny of mouse mammary gland responsiveness to ovarian steroid hormones. Endocrinology 125:2766-2772.

    Google Scholar 

  7. S. Z. Haslam (1988). Acquisition of estrogen-depende nt pro-gesterone receptors by normal mouse mammary gland. Ontog-eny of mammary progesterone receptors. J. Steroid Biochem. 31:9-13.

    Google Scholar 

  8. S. Z. Haslam (1988). Progesterone effects on deoxyribonucleic acid synthesis in normal mammary glands. Endocrinology 122:464-470.

    Google Scholar 

  9. S. Wang, L. J. Counterman, and S. Z. Haslam (1990). Progester-one action in normal mouse mammary gland. Endocrinology 127:2183-2189.

    Google Scholar 

  10. L. R. Lund, J. Romer, N. Thomasset, H. Solberg, C. Pyke, M. J. Bissell, K. Dano, and Z. Werb (1996). Two distinct phases of apoptosis inmammary gland involution: Proteinase-indepen-dent and-dependent pathways. Development 122:181-193.

    Google Scholar 

  11. A. M. Raafat, J. Song, J. M. Bennett, L. J. Hofseth, and S. Haslam (1997). Enhanced proliferative response to estrogen normal mouse mammary gland after long-term ovariectomy. (submitted).

  12. R. Narbaitz, W. E. Stumpf, and M. Sar (1980). Estrogen recep-tors in mammary gland primordia of fetal mouse. Anat. Embryol. 158:161-166.

    Google Scholar 

  13. S. Z. Haslam and K. A. Nummy (1992). The ontogeny cellular distribution of estrogen receptors in normal mouse mammary gland. J. Steroid Biochem. Mol. Biol. 42:589-595.

    Google Scholar 

  14. C.W. Daniel, G. B. Silberstein, and P. Strickland (1987). Direct action of 17 beta-estradiol on mouse mammary ducts analyzed by sustained release implants and steroid autoradiography. Cancer Res. 47:6052-6057.

    Google Scholar 

  15. T. G. Muldoon (1970). Mouse mammary tissue estrogen recep-tors: Ontogeny and molecular heterogeneity. In T. H. Hamilton, J. H. Clark and W. A. Sadler (eds.). Ontogeny of Receptors and Reproductive Hormone Action, Raven Press, New York, pp. 225-247.

    Google Scholar 

  16. S. Z. Haslam and G. Shyamala (1981). Relative distribution of estrogen and progesterone receptors among the epithelial, adipose, and connective tissue components of the normal mammary gland. Endocrinology 108:825-830.

    Google Scholar 

  17. W. P. Bocchinfuso and K. S. Korach (1997). Mammary gland development and tumorigenesis in estrogen receptor knockout mice. J. Mam. Gland Biol. Neoplasia 2:323-334.

    Google Scholar 

  18. K. S. Korach, J. F. Couse, S. W. Curtis, T. F. Washburn, J. Lindzey, K. S. Kimbro, E. M. Eddy, S. Migliaccio, S. M. Snedeker, D. B. Lubahn, D. W. Schomberg, and E. P. Smith (1996). Estrogen receptor gene disruption: Molecular characterization and experimental and clinical phenotypes. Rec. Prog. Horm. Res. 51:159-188.

    Google Scholar 

  19. G. R. Cunha, P. Young, Y. K. Hom, P. S. Coole, J. A. Taylor, and D. R. Lubahn (1997). Elucidation of a role for stromal steroid hormone receptors in mammary gland growth and development using tissue recombination experiments. J. Mam. Gland Biol. Neoplasia 2:393-402.

    Google Scholar 

  20. P. J. Shughrue, W. E. Stumpf, and M. Sar (1988). The distribu-tion of progesterone receptor in the 20-day-old fetal mouse: An autoradiographic study with [125I] progestin. Endocrinology 123:2382-2389.

    Google Scholar 

  21. S. Z. Haslam, L. J. Counterman, and A. R. St. John (1993). Hormonal basis for acquisition of estrogen-depende nt proges terone receptors in the normal mouse mammary gland. Steroid Biochem. (Life Sci. Adv.) 12:27.

    Google Scholar 

  22. G. Shyamala, W. Schneider, and D. Schott (1990). Develop mental regulation of murine mammary progesterone receptor gene expression. Endocrinology 126:2882-2889.

    Google Scholar 

  23. S. Z. Haslam, L. J. Counterman, and K. A. Nummy (1993). Effects of epidermal growth factor, estrogen, and progestin on DNA synthesis in mammary cell in vivo are determined by the developmental state of the gland. J. Cell. Physiol. 155:72-78.

    Google Scholar 

  24. J. P. Lydon, F. J. DeMayo, C. R. Funk, S. K. Mani, A. R. Hughes, C. J. Montgomery, G. Shyamala, O. M. Conneely, and B. W. O'Malley (1995). Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev. 9:2266-2278.

    Google Scholar 

  25. R. C. Humphreys, J. Lydon, B. W. O'Malley, and J. M. Rosen (1997). Mammary gland development is mediated by both stromal and epithelial progesterone receptors. Mol. Endocrinol. 11:801-811.

    Google Scholar 

  26. G. B. Silberstein, K. V. Horn, G. Shyamala, and C. W. Daniel (1996). Progesterone receptors in the mouse mammary duct: Distribution and developmental regulation. Cell Growth Diff. 7:945-952.

    Google Scholar 

  27. E. M. Keough and B. G. Wood (1979). Mammary gland devel opment during pregnancy in dwarf mouse mutant, little. Tissue Cell 11:773-780.

    Google Scholar 

  28. R. Das and B. K. Vonderhaar (1997). Prolactin as a mitogen in mammary cells. J. Mam. Gland. Biol. Neoplasia 2:29-39.

    Google Scholar 

  29. K. B. Horwitz and W. L. McGuire (1978). Actinomycin D prevents nuclear processing of estrogen receptor. J. Biol. Chem. 253:6319-6322.

    Google Scholar 

  30. K. B. Horwitz and W. L. McGuire (1978). Estrogen control of progesterone receptor in human breast cancer. Correlation with nuclear processing of estrogen receptor. J. Biol. Chem. 253:2223-2228.

    Google Scholar 

  31. L. D. Read, G. L. Greene, and B. S. Katzenellenbogen (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. 3:295-304.

    Google Scholar 

  32. M. Saceda, M. E. Lippman, P. Chambon, R. L. Lindsey, M. Ponglikitmongk ol, M. Puente, and M. B. Martin (1988). Regu-lation of the estrogen receptor in MCF-7 cells by estradiol. Mol. Endocrinol. 2:1157-1162.

    Google Scholar 

  33. A. Berkenstam, H. Glaumann, M. Martin, J. A. Gustafsson, and G. Norstedt (1989). Hormonal regulation of estrogen receptor messenger ribonucleic acid in T47Doc and MCF-7 breast can-cer cells. Mol. Endocrinol. 3:22-28.

    Google Scholar 

  34. G. Shyamala, W. Schneider, and M-C. Guiot (1992). Estrogen dependent regulation of estrogen receptor gene expression in normal mammary gland and its relationship to estrogenic sensitivity. Receptor. 2:121-128.

    Google Scholar 

  35. M. Edery, M. McGrath, L. Larson, and S. Nandi (1984). Corre-lation between in vitro growth and regulation of estrogen and progesterone receptors in rat mammary epithelial cells. Endocrinology 115:1691-1697.

    Google Scholar 

  36. T. G. Muldoon (1981). Interplay between estradiol and prolactin in the regulation of steroid hormone receptor levels, nature and functionality in normal mouse mammary tissue. Endocrinology 109:1339-1346.

    Google Scholar 

  37. M. Edery, W. Imagawa, L. Larson, and S. Nandi (1985). Regulation of estrogen and progesterone receptor levels in mouse mammary epithelial cells grown in serum-free collagen gel culture. Endocrinology 116:105-112.

    Google Scholar 

  38. S. Z. Haslam, L. J. Counterman, and K. A. Nummy (1992). EGF receptor regulation in normal mouse mammary gland. J. Cell. Physiol. 152:553-557.

    Google Scholar 

  39. S. Z. Haslam (1991). Stromal-epithelial interactions in normal and neoplastic mammary gland. Cancer Treat. Res. 53:401-420.

    Google Scholar 

  40. K. Hoshino (1978). In A. Yokoyama, H. Mizuno, and H. Naga-sawa (eds.), Physiology of Mammary Glands. University Park Press, Maryland, pp. 163-228.

    Google Scholar 

  41. S. Z. Haslam and L. J. Counterman (1991). Mammary stroma modulates hormonal responsiveness of mammary epithelium in vivo in the mouse. Endocrinology 129:2017-2023.

    Google Scholar 

  42. S. Coleman, G. B. Silberstein, and C. W. Daniel (1988). Ductal morphogenesis in the mouse mammary gland: Evidence supporting a role for epidermal growth factor. Dev. Biol. 127:304-315.

    Google Scholar 

  43. S. Z. Haslam (1988). Local versus systemically mediated effects of estrogen on normal mammary epithelial cell deoxyribonucleic acid synthesis. Endocrinology 122:860-867.

    Google Scholar 

  44. G. B. Silberstein, K. V. Horn, G. Shyamala, and C. W. Daniel (1994). Essential role of endogenous estrogen in directly stimulating mammary growth demonstrated by implants containing pure antiestrogens. Endocrinology 134:84-90.

    Google Scholar 

  45. B. K. Vonderhaar (1984). Hormones and growth factors in mammary gland development. In C.M. Veneziale (ed.), Control of Cell Growth and Proliferation, Van Nostrand-Reinh old, New York, pp. 11-33.

    Google Scholar 

  46. G. Scheffield and C. W. Welch (1987). Influence of submandibular salivary glands on hormone responsiveness of mouse mammary glands. Proc. Soc. Exp. Med. 186:368-377.

    Google Scholar 

  47. B. K. Vonderhaar (1987). Local effects of EGF, a TGF and EGF-like growth factors on lobuloalveolar development in the mouse mammary gland in vivo. J. Cell. Physiol. 132:581-584.

    Google Scholar 

  48. M. Snedeker, C. F. Brown, and R. P. DiAugustine (1991). Expression and functional properties of transforming growth factor alpha and epidermal growth factor during mouse mammary gland ductal morphogenesis. Proc. Natl. Acad. Sci. USA 88:276-280.

    Google Scholar 

  49. D. S. Liscia, G. Merlo, F. Ciardiello, N. Kim, G. H. Smith, R. Callahan, and D. S. Salomon (1990). Transforming growth factor-alpha messenger RNA localization in the developing adult rat and human mammary gland by in situ hybridization. Dev. Biol. 140:123-131.

    Google Scholar 

  50. C. W. Daniel and G. B. Silberstein (1987). Postnatal development of the rodent mammary gland. In M. C. Neville and C. W. Daniel (eds.), The Mammary Gland. Development, Regulation and Function, Plenum Press, New York, pp. 3-36.

    Google Scholar 

  51. G. Shyamala and A. Ferenczy (1984). Mammary fat pad may be a potential site for initiation of estrogen action in normal mouse mammary glands. Endocrinology 115:1078-1081.

    Google Scholar 

  52. D. P. Ankrapp, J. M. Bennett, and S. Z. Haslam (1998). The role of epidermal growth factor in the acquisition of ovarian steroid hormone responsiveness in the normal mouse mammary gland. J. Cell Physiol. 174:251-260.

    Google Scholar 

  53. D. M. Ignar-Trowbridge. K. G. Nelson, M. C. Bidwell, S. W. Curtis, T. F. Washburn, J. A. McLachlan, and K. S. Korach (1992). Coupling of dual signaling pathways: EGF action involves the estrogen receptor. Proc. Natl. Acad. Sci. USA 89:4658-4662.

    Google Scholar 

  54. S. W. Curtis, T. Washburn, C. Sewall, R. DiAugustine, J. Lind-zey, J. F. Couse, and K. S. Korach (1996). Physiological coupling of growth factor and steroid receptor signaling pathways: Estrogen receptor knockout mice lack estrogen-like response to epidermal growth factor. Proc. Natl. Acad. Sci. USA 93:12626-12630.

    Google Scholar 

  55. D. M. Ignar-Trowbridge. C. T. Teng, K. A. Ross, M. G. Parker, K. S. Korach, and J. A. McLachlan (1993). Peptide growth factors elicit estrogen receptor-dependen t transcriptional activation of an estrogen-responsi ve element. Mol. Endocrinol. 7:992-998.

    Google Scholar 

  56. B. S. Katzenellenboge n and M. J. Norman (1990). Multihormonal regulation of the progesterone receptor in MCF-7 human breast cancer cells: Interrelationships among insulin/insulin like growth factor-1, serum, and estrogen. Endocrinology 126:891-898.

    Google Scholar 

  57. G. Bunone, P. A. Briand, R. J. Miksicek, and D. Picard (1996). Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation. EMBO J. 15:2174-2183.

    Google Scholar 

  58. B. S. Katzenellenboge n (1996). Estrogen receptors: Bioactivities and interactions with cell signaling pathways. Biol. Reprod. 54:287-293.

    Google Scholar 

  59. K. J. Fowler, F. Walker, W. Alexander, M. L. Hibbs, E. C. Nice, R. M. Bohmer, G. B. Mann, C. Thumwood, R. Maglitto, J. A. Danks, R. Chetty, A. W. Burgess, and A. R. Dunn (1995). A mutation in the epidermal growth factor receptor in waved-2 mice has a profound effect on receptor biochemistry that results in impaired lactation. Proc. Natl. Acad. Sci. USA 92:1465-1469.

    Google Scholar 

  60. G. G. J.M. Kuiper and A. O. Brinkman (1994). Steroid hormone receptor phosphorylation: is there a physiological role? Mol. Cell. Endocrinol. 100:103-107.

    Google Scholar 

  61. N. L. Weigel, W. Bai, Y. Zhang, C. A. Beck, D. P. Edwards, and A. Poletti (1995). Phosphorylation and progesterone receptor function. J. Steroid Biochem. Mol. Biol. 53:509-514.

    Google Scholar 

  62. G. S. Takimoto, A. R. Hovland, D. M. Tasset, M. Y. Melville, L. Tung, and K. B. Horwitz (1996). Role of phosphorylation on DNA binding and transcriptional functions of human progesterone receptors. J. Biol. Chem. 271:13308-13316.

    Google Scholar 

  63. P. J. Keely, J. E. Wu, and S. A. Santoro (1995). The spatial and temporal expression of the a 2b 1 integrin and its ligands, collagen I, collagen IV, and laminin, suggests important roles in mouse mammary morphogenesis. Differentiation 59:1-13.

    Google Scholar 

  64. C. H. Streuli, C. Schmidhauser, N. Bailey, P. Yurchenko, A. P. Skubits, C. Roskelley, and M. J. Bissell (1995). Laminin mediates tissue-specific gene expression in mammary epithelia. J. Cell Biol. 129:591-603.

    Google Scholar 

  65. C. Q. Lin and M. J. Bissell (1993). Multi-faceted regulation of cell differentiation by extracellular matrix. FASEB J. 7:737-743.

    Google Scholar 

  66. J. Xie and S. Z. Haslam (1997). Extracellular matrix regulates ovarian hormone-depende nt proliferation of mouse mammary epithelial cells. Endocrinology 138:2466-2473.

    Google Scholar 

  67. S. Wang and S. Z. Haslam (1994). Serum-free primary culture of normal mouse mammary epithelial and stromal cells. In Vitro Cell. Dev. Biol. 30A:859-866.

    Google Scholar 

  68. S. Z. Haslam and M. L. Levely (1985). Estrogen responsiveness of normal mouse mammary cells in primary cell culture: Association of mammary fibroblasts with estrogenic regulation of progesterone receptors. Endocrinology 116:1835-1844.

    Google Scholar 

  69. S. Z. Haslam (1986). Mammary fibroblast influence on normal mouse mammary epithelial cell responses to estrogen in vitro. Cancer Res. 46:310-316.

    Google Scholar 

  70. R. White, J. A. Lees, M. Needham, J. Ham, and M. Parker (1987). Structural organization and expression of the mouse estrogen receptor. Mol. Endocrinol. 1:735-744.

    Google Scholar 

  71. G. G. J. M. Kuiper, E. Enmark, M. Pelto-Huikko, S. Nilsson, and J.-AÊ. Gustafsson (1996). Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. USA 93:5925-5930.

    Google Scholar 

  72. G. G. J. M. Kuiper, B. Carlsson, K. Grandien, E. Enmark, J. HaÈ ggblad, S. Nilsson, and J.-AÊ. Gustafsson (1997). Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α andβ. Endocrinology 123:863-870.

    Google Scholar 

  73. G. B. Tremblay, A. Tremblay, N. G. Copeland, D. J. Gilbert, N. A. Jenkins, F. Labrie, and V. Giguère (1997). Cloning, chromosomal localization, and functional analysis of the murine estrogen receptorβ. Mol. Endocrinol. 11:353-365.

    Google Scholar 

  74. B. S. Katzenellenbogen and K. S. Korach (1997). Editorial: A new actor in the estrogen receptor drama-enter ER-β. Endocrinology 138:861-862.

    Google Scholar 

  75. K. Paech, P. Webb, G. G. J. M. Kuiper, S. Nilsson, J.-Å. Gustafsson, P. J. Kushner, and T. S. Scanlan (1997). Differential ligand activation of estrogen receptors ERα and ERβ at AP1 sites. Science 277:1508-1510.

    Google Scholar 

  76. A. Huang, E. R. Leygue, L. Snell, L. C. Murphy, and P. H. Watson (1997). Expression of estrogen receptor variant messen-ger RNAs and determination of estrogen receptor status in human breast cancer. Am. J. Pathol. 150:1827-1833.

    Google Scholar 

  77. Q. X. Zhang, S. G. Hilsenbeck, S. A. Fuqua, and A. Borg (1996). Multiple splicing variants of the estrogen receptor are present in individual human breast tumors. J. Steroid Biochem. Mol. Biol. 59:251-260.

    Google Scholar 

  78. M. Sluyser (1994). Hormone resistance in cancer: The role of abnormal steroid receptors. Crit. Rev. Oncog. 5:539-554.

    Google Scholar 

  79. E. R. Leygue, P. H. Watson, and L. C. Murphy (1996). Estrogen receptor variants in normal human mammary tissue. J. Natl. Cancer Inst. 88:284-290.

    Google Scholar 

  80. U. Pfeffer (1996). Estrogen receptor mRNA variants. Do they have a physiological role? Ann. N.Y. Acad. Sci. 784:304-313.

    Google Scholar 

  81. U. Pfeffer, E. Fecarotta, G. Arena, A. Forlani, and G. Vidali (1996). Alternative splicing of the estrogen receptor primary transcript normally occurs in estrogen receptor positive tissues and cell lines. J. Steroid Biochem. Mol. Biol. 56:99-105.

    Google Scholar 

  82. C. G. Castles, S. A. W. Fuqua, D. M. Klotz, and S. M. Hill (1993). Expression of a constitutively active estrogen receptor in the estrogen receptor-negative BT-20 human breast cancer cell line. Cancer Res. 53:5934-5939.

    Google Scholar 

  83. D. R. Schott, G. Shyamala, W. Schneider, and G. Parry (1991). Molecular cloning, sequence analysis, and expression of complementary DNA encoding murine progesterone receptor. Biochemistry 30:7014-7020.

    Google Scholar 

  84. L. S. Dure, IV, W. T. Schrader, and B. W. O' Malley (1980). Covalent attachment of a progestational steroid to chick oviduct progesterone receptor by photoaffinity labeling. Nature 238:784-786.

    Google Scholar 

  85. K. B. Horwitz and P. S. Alexander (1983). In situ photo-linked nuclear progesterone receptors of human breast cancer cells: Subunit molecular weights after transformation and translocation. Endocrinology 113:2195-2210.

    Google Scholar 

  86. H. Loosfelt, F. Logeat, M. T. Vu Hai and E. Milgrom (1984). The rabbit progesterone receptor. Evidence for a single steroid-binding unit and characterization of receptor mRNA. J. Biol. Chem. 259:14196-14202.

    Google Scholar 

  87. T. T. Ilenchuk and M. R. Walters (1987). Rat uterine progesterone receptor analyzed by [3H]R5020 photoaffinity labeling: evidence that the A and B subunits are not equimolar. Endocri-nology 120:1449-1456.

    Google Scholar 

  88. W. Schneider, C. Ramachandran, P. G. Satyaswaroop, and G. Shyamala (1991). Murine progesterone receptor exists predom-inantly as the 83-kilodalton ‘A’ form. J. Steroid Biochem. Mol. Biol. 38:285-291.

    Google Scholar 

  89. E. Vegeto, M. M. Shahbaz, D. X. Wen, M. E. Goldman, B. W. O' Malley, and D. P. McDonnell (1993). Human progesterone receptor A form is a cell-and promoter-specific repressor of human progesterone receptor B function. Mol. Endocrinol. 7:1244-1255.

    Google Scholar 

  90. W. L. Kraus, K. E. Weis, and B. S. Katzenellenboge n (1995). Inhibitory cross talk between steroid hormone receptors: differential targeting of estrogen receptor in the repression of its transcriptional activity by agonist-and antagonist-occupied progestin receptors. Mol. Cell. Biol. 15:1847-1857.

    Google Scholar 

  91. J. A. Katzenellenboge n, B.W. O' Malley, and B. S. Katzenellen-bogen (1996). Tripartite steroid hormone receptor pharmacol-ogy: Interaction with multiple effector sites as a basis for the cell-and promoter-specific action of these hormones. Mol. Endocrinol. 10:119-131.

    Google Scholar 

  92. B. W. O' Malley, W. T. Schrader, S. Mani, C. Smith, N. L. Weigel, O. M. Conneely, and J. H. Clark (1995). An alternative ligand-independent pathway for activation of steroid receptors. Rec. Prog. Horm. Res. 50:333-347.

    Google Scholar 

  93. T. J. A. Key and M. C. Pike (1988). The role of oestrogens and progestagens in the epidemiology and prevention of breast cancer. Eur. J. Cancer Clin. Oncol. 24:29-43.

    Google Scholar 

  94. M. C. Pike, J. R. Daniels, and D. V. Spicer (1997). A hormonal contraceptive approach to reducing breast and ovarian cancer risk: An update. Endocrine-Related Cancer 4:125-133.

    Google Scholar 

  95. J. Russo and I. H. Russo (1997). Role of differentiation in the pathogenesis and prevention of breast cancer. Endocrine Related Cancer 4:7-21.

    Google Scholar 

  96. I. H. Russo and J. Russo (1996). Mammary gland neoplasia in long-term rodent studies. Environ. Health Perspect. 104:938-967.

    Google Scholar 

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Fendrick, J.L., Raafat, A.M. & Haslam, S.Z. Mammary Gland Growth and Development from the Postnatal Period to Postmenopause: Ovarian Steroid Receptor Ontogeny and Regulation in the Mouse. J Mammary Gland Biol Neoplasia 3, 7–22 (1998). https://doi.org/10.1023/A:1018766000275

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