Logo of envhperEnvironmental Health PerspectivesBrowse ArticlesAbout EHPGeneral InformationAuthorsMediaProgramsPartnerships
Environ Health Perspect. 1989 Mar; 80: 85–99.
PMCID: PMC1567615
Research Article

Growth control and differentiation in mammary epithelial cells.


Growth and differentiation of the mammary gland are controlled by various hormones and other environmental factors. The role of hormones and growth factors in mammary development is discussed with regard to animal species, physiological stages, and the various experimental systems in vitro. In the female embryo, mammary morphogenesis is induced by the mesenchyme and is hormone independent, whereas androgens cause the partial necrosis of mammary epithelium in the male. Ductal growth during adolescence requires estrogen and prolactin or growth hormone. During pregnancy, progesterone participates in the development of the lobuloalveolar structure of the gland. After parturition, changes in the hormonal environment lead to production and secretion of milk. Proliferation and differentiation of mammary epithelium can be induced in culture systems. Insulin and epidermal growth factor (EGF) stimulate mammary cell proliferation in vitro. EGF is required for the optimal growth of the mammary gland during pregnancy. EGF also appears to play an important role in mammary tumorigenesis in certain mouse strains. Production of milk proteins can be induced in vitro by the synergistic interactions of prolactin, insulin, and glucocorticoids and is inhibited by EGF and progesterone. Complete or partial sequencing of several milk protein genes and comparative analysis have led to identification of a sequence of high homology and conservation in the 5' flanking region that is likely to be involved in the regulation of milk protein gene expression.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (3.5M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • NANDI S. Endocrine control of mammarygland development and function in the C3H/ He Crgl mouse. J Natl Cancer Inst. 1958 Dec;21(6):1039–1063. [PubMed]
  • LYONS WR, LI CH, JOHNSON RE. The hormonal control of mammary growth and lactation. Recent Prog Horm Res. 1958;14:219–254. [PubMed]
  • Banerjee MR. Responses of mammary cells to hormones. Int Rev Cytol. 1976;47:1–97. [PubMed]
  • Topper YJ, Freeman CS. Multiple hormone interactions in the developmental biology of the mammary gland. Physiol Rev. 1980 Oct;60(4):1049–1106. [PubMed]
  • Porter JC. Proceedings: Hormonal regulation of breast development and activity. J Invest Dermatol. 1974 Jul;63(1):85–92. [PubMed]
  • RAYNAUD A, RAYNAUD J. Les processus de la destruction de la deuxième paire inguinale d'ébauches mammaires des foetus males de souris. C R Seances Soc Biol Fil. 1953 Dec;147(23-24):1962–1967. [PubMed]
  • Daniel CW, Berger JJ, Strickland P, Garcia R. Similar growth pattern of mouse mammary epithelium cultivated in collagen matrix in vivo and in vitro. Dev Biol. 1984 Jul;104(1):57–64. [PubMed]
  • Williams JM, Daniel CW. Mammary ductal elongation: differentiation of myoepithelium and basal lamina during branching morphogenesis. Dev Biol. 1983 Jun;97(2):274–290. [PubMed]
  • Joshi K, Smith JA, Perusinghe N, Monoghan P. Cell proliferation in the human mammary epithelium. Differential contribution by epithelial and myoepithelial cells. Am J Pathol. 1986 Aug;124(2):199–206. [PMC free article] [PubMed]
  • Emerman JT, Vogl AW. Cell size and shape changes in the myoepithelium of the mammary gland during differentiation. Anat Rec. 1986 Nov;216(3):405–415. [PubMed]
  • Berger JJ, Daniel CW. Stromal DNA synthesis is stimulated by young, but not serially aged, mouse mammary epithelium. Mech Ageing Dev. 1983 Nov-Dec;23(3-4):277–284. [PubMed]
  • Kute TE, Linville C, Mehta RG, Moon RC. Cell kinetics in normal and neoplastic mammary tissues by flow cytometric analyses. Cytometry. 1985 Jul;6(4):362–367. [PubMed]
  • Shipman LJ, Docherty AH, Knight CH, Wilde CJ. Metabolic adaptations in mouse mammary gland during a normal lactation cycle and in extended lactation. Q J Exp Physiol. 1987 Jul;72(3):303–311. [PubMed]
  • Sakakura T, Nishizuka Y. Effect of thymectomy on mammary tumorigenesis, noduligenesis, and mammogenesis in the mouse. Gan. 1967 Oct;58(5):441–450. [PubMed]
  • Oka T, Perry JW, Topper YJ. Changes in insulin responsiveness during development of mammary epithelium. J Cell Biol. 1974 Aug;62(2):550–556. [PMC free article] [PubMed]
  • SILVER M. The onset of allometric mammary growth in the female hooded Norway rat. J Endocrinol. 1953 Nov;10(1):35–45. [PubMed]
  • Shyamala G, Ferenczy A. Mammary fat pad may be a potential site for initiation of estrogen action in normal mouse mammary glands. Endocrinology. 1984 Sep;115(3):1078–1081. [PubMed]
  • Sheffield LG, Welsch CW. Cholera-toxin-enhanced growth of human breast cancer cell lines in vitro and in vivo: interaction with estrogen. Int J Cancer. 1985 Oct 15;36(4):479–483. [PubMed]
  • Silberstein GB, Strickland P, Trumpbour V, Coleman S, Daniel CW. In vivo, cAMP stimulates growth and morphogenesis of mouse mammary ducts. Proc Natl Acad Sci U S A. 1984 Aug;81(15):4950–4954. [PMC free article] [PubMed]
  • Sheffield LG, Sinha YN, Welsch CW. Cholera toxin treatment increases in vivo growth and development of the mouse mammary gland. Endocrinology. 1985 Nov;117(5):1864–1869. [PubMed]
  • Lee AE. The proliferative action of oestriol. J Endocrinol. 1980 Feb;84(2):289–294. [PubMed]
  • Vonderhaar BK, Greco AE. Effect of thyroid status on development of spontaneous mammary tumors in primiparous C3H mice. Cancer Res. 1982 Nov;42(11):4553–4561. [PubMed]
  • Haslam SZ, Shyamala G. Relative distribution of estrogen and progesterone receptors among the epithelial, adipose, and connective tissue components of the normal mammary gland. Endocrinology. 1981 Mar;108(3):825–830. [PubMed]
  • Haslam SZ, Shyamala G. Progesterone receptors in normal mammary glands of mice: characterization and relationship to development. Endocrinology. 1979 Sep;105(3):786–795. [PubMed]
  • Terada N, Wakimoto H, Oka T. Regulation of milk protein synthesis by progesterone in cultured mouse mammary gland. J Steroid Biochem. 1988 Jan;29(1):99–104. [PubMed]
  • Kurachi H, Oka T. Changes in epidermal growth factor concentrations of submandibular gland, plasma and urine of normal and sialoadenectomized female mice during various reproductive stages. J Endocrinol. 1985 Aug;106(2):197–202. [PubMed]
  • Byyny RL, Orth DN, Cohen S, Doyne ES. Epidermal growth factor: effects of androgens and adrenergic agents. Endocrinology. 1974 Sep;95(3):776–782. [PubMed]
  • Bullock LP, Barthe PL, Mowszowicz I, Orth DN, Bardin CW. The effect of progestins on submaxillary gland epidermal growth factor: demonstration of androgenic, synandrogenic and antiandrogenic actions. Endocrinology. 1975 Jul;97(1):189–195. [PubMed]
  • Barkley MS, Geschwind II, Bradford GE. The gestational pattern of estradiol, testosterone and progesterone secretion in selected strains of mice. Biol Reprod. 1979 May;20(4):733–738. [PubMed]
  • Okamoto S, Oka T. Evidence for physiological function of epidermal growth factor: pregestational sialoadenectomy of mice decreases milk production and increases offspring mortality during lactation period. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6059–6063. [PMC free article] [PubMed]
  • Oka T, Tsutsumi O, Kurachi H, Okamoto S. The role of epidermal growth factor in normal and neoplastic growth of mouse mammary epithelial cells. Cancer Treat Res. 1988;40:343–362. [PubMed]
  • Daniel CW, Silberstein GB, Strickland P. Reinitiation of growth in senescent mouse mammary epithelium in response to cholera toxin. Science. 1984 Jun 15;224(4654):1245–1247. [PubMed]
  • Kratochwil K. Development and loss of androgen responsiveness in the embryonic rudiment of the mouse mammary gland. Dev Biol. 1977 Dec;61(2):358–365. [PubMed]
  • Wasner G, Hennermann I, Kratochwil K. Ontogeny of mesenchymal androgen receptors in the embryonic mouse mammary gland. Endocrinology. 1983 Nov;113(5):1771–1780. [PubMed]
  • HOSHINO K. Morphogenesis and growth potentiality of mammary glands in mice. I. Transplantability and growth potentiality of mammary tissue of virgin mice. J Natl Cancer Inst. 1962 Nov;29:835–851. [PubMed]
  • Levine JF, Stockdale FE. Cell-cell interactions promote mammary epithelial cell differentiation. J Cell Biol. 1985 May;100(5):1415–1422. [PMC free article] [PubMed]
  • Wakimoto H, Oka T. Involvement of collagen formation in the hormonally induced functional differentiation of mouse mammary gland in organ culture. J Biol Chem. 1983 Mar 25;258(6):3775–3779. [PubMed]
  • Enami J, Nandi S. Hormonal control of milk protein synthesis in cultured mouse mammary explants. Cell Differ. 1977 Oct;6(3-4):217–227. [PubMed]
  • Ono M, Oka T. The differential actions of cortisol on the accumulation of alpha-lactalbumin and casein in midpregnant mouse mammary gland in culture. Cell. 1980 Feb;19(2):473–480. [PubMed]
  • Takemoto T, Nagamatsu Y, Oka T. Casein and alpha-lactalbumin messenger RNAs during the development of mouse mammary gland. Isolation, partial purification, and translation in a cell-free system. Dev Biol. 1980 Aug;78(2):247–257. [PubMed]
  • Dev IK, Harvey RJ. Sources of one-carbon units in the folate pathway of Escherichia coli. J Biol Chem. 1982 Feb 25;257(4):1980–1986. [PubMed]
  • Fitzgerald DK, Colvin B, Mawal R, Ebner KE. Enzymic assay for galactosyl transferase activity of lactose synthetase and alpha-lactalbumin in purified and crude systems. Anal Biochem. 1970 Jul;36(1):43–61. [PubMed]
  • Hori C, Oka T. Induction by lithium ion of multiplication of mouse mammary epithelium in culture. Proc Natl Acad Sci U S A. 1979 Jun;76(6):2823–2827. [PMC free article] [PubMed]
  • Nagamatsu Y, Oka T. Purification and characterization of mouse alpha-lactalbumin and preparation of its antibody. Biochem J. 1980 Jan 1;185(1):227–237. [PMC free article] [PubMed]
  • Schultz GS, Ebner KE. Measurement of alpha-lactalbumin in serum and mammary tumors of rats by radioimmunoassay. Cancer Res. 1977 Dec;37(12):4482–4488. [PubMed]
  • Richards DA, Rodgers JR, Supowit SC, Rosen JM. Construction and preliminary characterization of the rat casein and alpha-lactalbumin cDNA clones. J Biol Chem. 1981 Jan 10;256(1):526–532. [PubMed]
  • Hennighausen LG, Steudle A, Sippel AE. Nucleotide sequence of cloned cDNA coding for mouse epsilon casein. Eur J Biochem. 1982 Sep 1;126(3):569–572. [PubMed]
  • Hennighausen LG, Sippel AE. Characterization and cloning of the mRNAs specific for the lactating mouse mammary gland. Eur J Biochem. 1982 Jun 15;125(1):131–141. [PubMed]
  • Hennighausen LG, Sippel AE, Hobbs AA, Rosen JM. Comparative sequence analysis of the mRNAs coding for mouse and rat whey protein. Nucleic Acids Res. 1982 Jun 25;10(12):3733–3744. [PMC free article] [PubMed]
  • Yoshimura M, Banerjee MR, Oka T. Nucleotide sequence of a cDNA encoding mouse beta casein. Nucleic Acids Res. 1986 Oct 24;14(20):8224–8224. [PMC free article] [PubMed]
  • Hall L, Emery DC, Davies MS, Parker D, Craig RK. Organization and sequence of the human alpha-lactalbumin gene. Biochem J. 1987 Mar 15;242(3):735–742. [PMC free article] [PubMed]
  • Yu-Lee LY, Richter-Mann L, Couch CH, Stewart AF, Mackinlay AG, Rosen JM. Evolution of the casein multigene family: conserved sequences in the 5' flanking and exon regions. Nucleic Acids Res. 1986 Feb 25;14(4):1883–1902. [PMC free article] [PubMed]
  • ELIAS JJ. Cultivation of adult mouse mammary gland in hormone-enriched synthetic medium. Science. 1957 Oct 25;126(3278):842–843. [PubMed]
  • Taketani Y, Oka T. Epidermal growth factor stimulates cell proliferation and inhibits functional differentiation of mouse mammary epithelial cells in culture. Endocrinology. 1983 Sep;113(3):871–877. [PubMed]
  • Yang J, Richards J, Bowman P, Guzman R, Enami J, McCormick K, Hamamoto S, Pitelka D, Nandi S. Sustained growth and three-dimensional organization of primary mammary tumor epithelial cells embedded in collagen gels. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3401–3405. [PMC free article] [PubMed]
  • Yang NS, Kube D, Park C, Furmanski P. Growth of human mammary epithelial cells on collagen gel surfaces. Cancer Res. 1981 Oct;41(10):4093–4100. [PubMed]
  • Yang J, Guzman R, Richards J, Jentoft V, DeVault MR, Wellings SR, Nandi S. Primary culture of human mammary epithelial cells embedded in collagen gels. J Natl Cancer Inst. 1980 Aug;65(2):337–343. [PubMed]
  • Emerman JT, Pitelka DR. Maintenance and induction of morphological differentiation in dissociated mammary epithelium on floating collagen membranes. In Vitro. 1977 May;13(5):316–328. [PubMed]
  • Imagawa W, Tomooka Y, Nandi S. Serum-free growth of normal and tumor mouse mammary epithelial cells in primary culture. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4074–4077. [PMC free article] [PubMed]
  • Wicha MS, Lowrie G, Kohn E, Bagavandoss P, Mahn T. Extracellular matrix promotes mammary epithelial growth and differentiation in vitro. Proc Natl Acad Sci U S A. 1982 May;79(10):3213–3217. [PMC free article] [PubMed]
  • Wicha MS. Interaction of rat mammary epithelium with extracellular matrix components. Prog Clin Biol Res. 1984;145:129–142. [PubMed]
  • Levine JF, Stockdale FE. 3T3-L1 adipocytes promote the growth of mammary epithelium. Exp Cell Res. 1984 Mar;151(1):112–122. [PubMed]
  • HARDY MH. The development in vitro of the mammary glands of the mouse. J Anat. 1950 Oct;84(4):388–393. [PMC free article] [PubMed]
  • Oka T, Topper YJ. Hormone-dependent accumulation of rough endoplasmic reticulum in mouse mammary epithelial cells in vitro. J Biol Chem. 1971 Dec 25;246(24):7701–7707. [PubMed]
  • Devinoy E, Houdebine LM, Ollivier-Bousquet M. Role of glucocorticoids and progesterone in the development of rough endoplasmic reticulum involved in casein biosynthesis. Biochimie. 1979;61(4):453–461. [PubMed]
  • Mills ES, Topper YJ. Some ultrastructural effects of insulin, hydrocortisone, and prolactin on mammary gland explants. J Cell Biol. 1970 Feb;44(2):310–328. [PMC free article] [PubMed]
  • Rosen JM, Matusik RJ, Richards DA, Gupta P, Rodgers JR. Multihormonal regulation of casein gene expression at the transcriptional and posttransciptional levels in the mammary gland. Recent Prog Horm Res. 1980;36:157–193. [PubMed]
  • Delouis C, Combaud ML. Lack of mitotic effects of insulin during synthesis of casein induced by prolactin in pseudopregnant rabbit mammary gland organ cultures. J Endocrinol. 1977 Mar;72(3):393–394. [PubMed]
  • du Bois M, Elias JJ. Subpopulations of cells in immature mouse mammary gland as detected by proliferative responses to hormones in organ culture. Dev Biol. 1984 Nov;106(1):70–75. [PubMed]
  • Ichinose RR, Nandi S. Influence of hormones on lobulo-alveolar differentiation of mouse mammary glands in vitro. J Endocrinol. 1966 Aug;35(4):331–340. [PubMed]
  • Wood BG, Washburn LL, Mukherjee AS, Banerjee MR. Hormonal regulation of lobulo-alveolar growth, functional differentiation and regression of whole mouse mammary gland in organ culture. J Endocrinol. 1975 Apr;65(1):1–6. [PubMed]
  • Dilley WG, Nandi S. Rat mammary gland differentiation in vitro in the absence of steroids. Science. 1968 Jul 5;161(3836):59–60. [PubMed]
  • Tonelli QJ, Sorof S. Epidermal growth factor requirement for development of cultured mammary gland. Nature. 1980 May 22;285(5762):250–252. [PubMed]
  • Ceriani RL. Fetal mammary gland differentiation in vitro in response to hormones. II. Biochemical findings. Dev Biol. 1970 Apr;21(4):530–546. [PubMed]
  • Voytovich AE, Topper YJ. Hormone-dependent differentiation of immature mouse mammary gland in vitro. Science. 1967 Dec 8;158(3806):1326–1327. [PubMed]
  • Vonderhaar BK, Topper YJ. A role of the cell cycle in hormone-dependent differentiation. J Cell Biol. 1974 Nov;63(2 Pt 1):707–712. [PMC free article] [PubMed]
  • Richards J, Hamamoto S, Smith S, Pasco D, Guzman R, Nandi S. Response of end bud cells from immature rat mammary gland to hormones when cultured in collagen gel. Exp Cell Res. 1983 Aug;147(1):95–109. [PubMed]
  • Katiyar VN, Enami J, Nandi S. Effect of polypeptide hormones on stimulation of casein secretion by mouse mammary epithelial cells grown on floating collagen gels. In Vitro. 1978 Sep;14(9):771–774. [PubMed]
  • Salomon DS, Liotta LA, Kidwell WR. Differential response to growth factor by rat mammary epithelium plated on different collagen substrata in serum-free medium. Proc Natl Acad Sci U S A. 1981 Jan;78(1):382–386. [PMC free article] [PubMed]
  • McGrath M, Palmer S, Nandi S. Differential response of normal rat mammary epithelial cells to mammogenic hormones and EGF. J Cell Physiol. 1985 Nov;125(2):182–191. [PubMed]
  • Strum JM, Hillman EA. Human breast epithelium in organ culture: effect of hormones on growth and morphology. In Vitro. 1981 Jan;17(1):33–43. [PubMed]
  • Hillman EA, Valerio MG, Halter SA, Barrett-Boone LA, Trump BF. Long-term explant culture of normal mammary epithelium. Cancer Res. 1983 Jan;43(1):245–257. [PubMed]
  • Hammond SL, Ham RG, Stampfer MR. Serum-free growth of human mammary epithelial cells: rapid clonal growth in defined medium and extended serial passage with pituitary extract. Proc Natl Acad Sci U S A. 1984 Sep;81(17):5435–5439. [PMC free article] [PubMed]
  • Stampfer M, Hallowes RC, Hackett AJ. Growth of normal human mammary cells in culture. In Vitro. 1980 May;16(5):415–425. [PubMed]
  • Yang J, Balakrishnan A, Hamamoto S, Beattie CW, Das Gupta TK, Wellings SR, Nandi S, Gupta TK. Different mitogenic and phenotypic responses of human breast epithelial cells grown in two versus three dimensions. Exp Cell Res. 1986 Dec;167(2):563–569. [PubMed]
  • McGrath CM, Soule HD. Renewal inhibition of human mammary cell growth in vitro: cortisol and the recruitment of cells to terminal differentiation. J Cell Physiol. 1983 Sep;116(3):385–396. [PubMed]
  • Friedberg SH, Oka T, Topper YJ. Development of insulin-sensitivity by mouse mammary gland in vitro. Proc Natl Acad Sci U S A. 1970 Nov;67(3):1493–1500. [PMC free article] [PubMed]
  • Juergens WG, Stockdale FE, Topper YJ, Elias JJ. Hormone-dependent differentiation of mammary gland in vitro. Proc Natl Acad Sci U S A. 1965 Aug;54(2):629–634. [PMC free article] [PubMed]
  • Stockdale FE, Topper YJ. The role of DNA synthesis and mitosis in hormone-dependent differentiation. Proc Natl Acad Sci U S A. 1966 Oct;56(4):1283–1289. [PMC free article] [PubMed]
  • Ptashne K, Stockdale FE, Conlon S. Initiation of DNA synthesis in mammary epithelium and mammary tumors by lithium ions. J Cell Physiol. 1980 Apr;103(1):41–46. [PubMed]
  • Hori C, Oka T. Vanadate enhances the stimulatory action of insulin on DNA synthesis in cultured mouse mammary gland. Biochim Biophys Acta. 1980 Dec 11;610(2):235–240. [PubMed]
  • Turkington RW. The role of epithelial growth factor in mammary gland development in vitro. Exp Cell Res. 1969 Sep;57(1):79–85. [PubMed]
  • Majumder GC, Turkington RW. Stimulation of mammary epithelial cell proliferation in vitro by protein factor(s) present in serum. Endocrinology. 1971 Jun;88(6):1506–1510. [PubMed]
  • Inagaki Y, Kohmoto K. Changes in Scatchard plots for insulin binding to mammary epithelial cells from cycling, pregnant, and lactating mice. Endocrinology. 1982 Jan;110(1):176–182. [PubMed]
  • Chou CK, Dull TJ, Russell DS, Gherzi R, Lebwohl D, Ullrich A, Rosen OM. Human insulin receptors mutated at the ATP-binding site lack protein tyrosine kinase activity and fail to mediate postreceptor effects of insulin. J Biol Chem. 1987 Feb 5;262(4):1842–1847. [PubMed]
  • Chomczynski P, Qasba P, Topper YJ. Essential role of insulin in transcription of the rat 25,000 molecular weight casein gene. Science. 1984 Dec 14;226(4680):1326–1328. [PubMed]
  • Nagamatsu Y, Oka T. The differential actions of cortisol on the synthesis and turnover of alpha-lactalbumin and casein and on accumulation of their mRNA in mouse mammary gland in organ culture. Biochem J. 1983 May 15;212(2):507–515. [PMC free article] [PubMed]
  • Terada N, Ono M, Nagamatsu Y, Oka T. The reversal of cortisol-induced inhibition of alpha-lactalbumin production by prostaglandins in the mouse mammary gland in culture. J Biol Chem. 1982 Oct 10;257(19):11199–11202. [PubMed]
  • Campbell SM, Rosen JM, Hennighausen LG, Strech-Jurk U, Sippel AE. Comparison of the whey acidic protein genes of the rat and mouse. Nucleic Acids Res. 1984 Nov 26;12(22):8685–8697. [PMC free article] [PubMed]
  • Banerjee MR, Terry PM, Sakai S, Lin FK, Ganguly R. Hormonal regulation of casein messenger RNA (mRNA). In Vitro. 1978 Jan;14(1):128–139. [PubMed]
  • Chomczynski P, Qasba P, Topper YJ. Transcriptional and post-transcriptional roles of glucocorticoid in the expression of the rat 25,000 molecular weight casein gene. Biochem Biophys Res Commun. 1986 Jan 29;134(2):812–818. [PubMed]
  • Skarda J, Urbanova E, Houdebine LM, Delouis C, Bilek J. Effects of insulin, cortisol and prolactin on lipid, protein and casein syntheses in goat mammary tissue in organ culture. Reprod Nutr Dev. 1982;22(2):379–386. [PubMed]
  • Bolander FF., Jr Enhanced endocrine sensitivity in mouse mammary glands: hormonal requirements for induction and maintenance. Endocrinology. 1984 Aug;115(2):630–633. [PubMed]
  • Sakai S, Enami J, Nandi S, Banerjee MR. Prolactin receptor on dissociated mammary epithelial cells at different stages of development. Mol Cell Endocrinol. 1978 Dec;12(3):285–298. [PubMed]
  • Suard YM, Kraehenbuhl JP, Aubert ML. Dispersed mammary epithelial cells. Receptors of lactogenic hormones in virgin, pregnant, and lactating rabbits. J Biol Chem. 1979 Oct 25;254(20):10466–10475. [PubMed]
  • McNeilly AS, Friesen HG. Binding of prolactin to the rabbit mammary gland during pregnancy. J Endocrinol. 1977 Sep;74(3):507–508. [PubMed]
  • Bohnet HG, Gómez F, Friesen HG. Prolactin and estrogen binding sites in the mammary gland of the lactating and non-lactating rat. Endocrinology. 1977 Oct;101(4):1111–1121. [PubMed]
  • Djiane J, Durand P. Prolactin-progesterone antagonism in self regulation of prolactin receptors in the mammary gland. Nature. 1977 Apr 14;266(5603):641–643. [PubMed]
  • Taketani Y, Oka T. Hormonal regulation of the synthesis of casein and alpha-lactalbumin in a primary mammary cell culture system. Horm Metab Res. 1986 Feb;18(2):119–125. [PubMed]
  • Djiane J, Clauser H, Kelly PA. Rapid down-regulation of prolactin receptors in mammary gland and liver. Biochem Biophys Res Commun. 1979 Oct 29;90(4):1371–1378. [PubMed]
  • Djiane J, Houdebine LM, Kelly PA. Correlation between prolactin-receptor interaction, down-regulation of receptors, and stimulation of casein and deoxyribonucleic acid biosynthesis in rabbit mammary gland explants. Endocrinology. 1982 Mar;110(3):791–795. [PubMed]
  • Sheth NA, Tikekar SS, Ranadive KJ, Sheth AR. Influence of bromoergocryptine on estrogen-modulated prolactin receptors of mouse mammary gland. Mol Cell Endocrinol. 1978 Nov;12(2):167–176. [PubMed]
  • Akers RM, Bauman DE, Goodman GT, Capuco AV, Tucker HA. Prolactin regulation of cytological differentiation of mammary epithelial cells in periparturient cows. Endocrinology. 1981 Jul;109(1):31–40. [PubMed]
  • Skarda J, Urbanová E, Becka S, Houdebine LM, Delouis C, Píchová D, Pícha J, Bílek J. Effect of bovine growth hormone on development of goat mammary tissue in organ culture. Endocrinol Exp. 1982 Mar;16(1):19–31. [PubMed]
  • Nicholas KR, Sankaran L, Topper YJ. The induction of alpha-lactalbumin in rat mammary explants in the absence of exogenous prolactin: effects of progesterone and estrogen. Endocrinology. 1981 Sep;109(3):978–980. [PubMed]
  • Wilson GD, Woods KL, Walker RA, Howell A. Effect of prolactin on lactalbumin production by normal and malignant human breast tissue in organ culture. Cancer Res. 1980 Feb;40(2):486–489. [PubMed]
  • Bisbee CA. Prolactin effects on ion transport across cultured mouse mammary epithelium. Am J Physiol. 1981 Mar;240(3):C110–C115. [PubMed]
  • Bisbee CA. Transepithelial electrophysiology of cultured mouse mammary epithelium: sensitivity to prolactins. Am J Physiol. 1981 Nov;241(5):E410–E413. [PubMed]
  • Bolander FF., Jr Possible roles of calcium and calmodulin in mammary gland differentiation in vitro. J Endocrinol. 1985 Jan;104(1):29–34. [PubMed]
  • Servely JL, Geuens GM, Martel P, Houdebine LM, de Brabander M. Effect of tubulozole, a new synthetic microtubule inhibitor, on the induction of casein gene expression by prolactin. Biol Cell. 1987;59(2):121–127. [PubMed]
  • Akers RM. Lactogenic hormones: binding sites, mammary growth, secretory cell differentiation, and milk biosynthesis in ruminants. J Dairy Sci. 1985 Feb;68(2):501–519. [PubMed]
  • Mauvais-Jarvis P, Kuttenn F, Gompel A, Malet C, Fournier S. Interaction estradiol-progestérone au niveau des cellules mammaires humaines normales et pathologiques. Ann Endocrinol (Paris) 1986;47(3):179–187. [PubMed]
  • Calaf G, Russo IH, Roi LD, Russo J. Effects of peptides and steroid hormones on cell kinetic parameters of normal human breast tissue in organ culture. In Vitro Cell Dev Biol. 1986 Mar;22(3 Pt 1):135–140. [PubMed]
  • van Bogaert LJ, Quinones J, Craynest MP. Estriol-induced dose-dependent DNA synthesis in normal human mammary epithelium in vitro. Eur J Cell Biol. 1980 Jun;21(2):234–236. [PubMed]
  • van Bogaert LJ, van Craynest MP, Abarca-Quinones J. Direct influence of the three natural estrogens on human mammary gland in vitro. Horm Metab Res. 1982 Nov;14(11):598–601. [PubMed]
  • McGrath CM. Augmentation of the response of normal mammary epithelial cells to estradiol by mammary stroma. Cancer Res. 1983 Mar;43(3):1355–1360. [PubMed]
  • Chambon M, Cavalie-Barthez G, Veith F, Vignon F, Hallowes R, Rochefort H. Effect of estradiol on nonmalignant human mammary cells in primary culture. Cancer Res. 1984 Dec;44(12 Pt 1):5733–5743. [PubMed]
  • Sankaran L, Qasba P, Topper YJ. Effects of estrogen-depletion on rat casein gene expression. Biochem Biophys Res Commun. 1984 Dec 14;125(2):682–689. [PubMed]
  • Sheffield LG, Ayslworth CF, Welsch CW. Cyclic nucleotides and protein phosphorylation in mouse mammary glands: effects of estrogen and progesterone administered in vivo. Proc Soc Exp Biol Med. 1987 Jul;185(3):283–290. [PubMed]
  • Caulfield JJ, Bolander FF., Jr Involvement of protein kinase C in mouse mammary gland development. J Endocrinol. 1986 Apr;109(1):29–34. [PubMed]
  • Smith GH. Functional differentiation of virgin mouse mammary epithelium in explant culture is dependent upon extracellular proline. J Cell Physiol. 1987 May;131(2):190–199. [PubMed]
  • Yang J, Guzman R, Richards J, Imagawa W, McCormick K, Nandi S. Growth factor- and cyclic nucleotide-induced proliferation of normal and malignant mammary epithelial cells in primary culture. Endocrinology. 1980 Jul;107(1):35–41. [PubMed]
  • Taketani Y, Oka T. Biological action of epidermal growth factor and its functional receptors in normal mammary epithelial cells. Proc Natl Acad Sci U S A. 1983 May;80(9):2647–2650. [PMC free article] [PubMed]
  • Enomoto K, Cossu MF, Edwards C, Oka T. Induction of distinct types of spontaneous electrical activities in mammary epithelial cells by epidermal growth factor and insulin. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4754–4758. [PMC free article] [PubMed]
  • Enomoto K, Cossu MF, Maeno T, Edwards C, Oka T. Involvement of the Ca2+-dependent K+ channel activity in the hyperpolarizing response induced by epidermal growth factor in mammary epithelial cells. FEBS Lett. 1986 Jul 28;203(2):181–184. [PubMed]
  • Boutwell RK. The function and mechanism of promoters of carcinogenesis. CRC Crit Rev Toxicol. 1974 Jan;2(4):419–443. [PubMed]
  • Taketani Y, Oka T. Tumor promoter 12-O-tetradecanoylphorbol 13-acetate, like epidermal growth factor, stimulates cell proliferation and inhibits differentiation of mouse mammary epithelial cells in culture. Proc Natl Acad Sci U S A. 1983 Mar;80(6):1646–1649. [PMC free article] [PubMed]
  • Gorden P, Carpentier JL, Cohen S, Orci L. Epidermal growth factor: morphological demonstration of binding, internalization, and lysosomal association in human fibroblasts. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5025–5029. [PMC free article] [PubMed]
  • Vonderhaar BK, Nakhasi HL. Bifunctional activity of epidermal growth factor on alpha- and kappa-casein gene expression in rodent mammary glands in vitro. Endocrinology. 1986 Sep;119(3):1178–1184. [PubMed]
  • Kurachi H, Okamoto S, Oka T. Evidence for the involvement of the submandibular gland epidermal growth factor in mouse mammary tumorigenesis. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5940–5943. [PMC free article] [PubMed]
  • Salomon DS, Zwiebel JA, Bano M, Losonczy I, Fehnel P, Kidwell WR. Presence of transforming growth factors in human breast cancer cells. Cancer Res. 1984 Sep;44(9):4069–4077. [PubMed]
  • Dickson RB, Huff KK, Spencer EM, Lippman ME. Induction of epidermal growth factor-related polypeptides by 17 beta-estradiol in MCF-7 human breast cancer cells. Endocrinology. 1986 Jan;118(1):138–142. [PubMed]
  • Rao KV, Fox CF. Epidermal growth factor stimulates tyrosine phosphorylation of human glucocorticoid receptor in cultured cells. Biochem Biophys Res Commun. 1987 Apr 14;144(1):512–519. [PubMed]
  • Silberstein GB, Daniel CW. Reversible inhibition of mammary gland growth by transforming growth factor-beta. Science. 1987 Jul 17;237(4812):291–293. [PubMed]
  • Bhattacharya A, Vonderhaar BK. Thyroid hormone regulation of prolactin binding to mouse mammary glands. Biochem Biophys Res Commun. 1979 Jun 27;88(4):1405–1411. [PubMed]
  • Vonderhaar BK, Bhattacharya A, Alhadi T, Liscia DS, Andrew EM, Young JK, Ginsburg E, Bhattacharjee M, Horn TM. Isolation, characterization, and regulation of the prolactin receptor. J Dairy Sci. 1985 Feb;68(2):466–488. [PubMed]
  • Houdebine LM, Devinoy E, Delouis C. Role of spermidine in casein gene expression in the rabbit. Biochimie. 1978;60(8):735–741. [PubMed]
  • Skarda J, Urbanová E, Houdebine LM, Delouis C, Bílek J. Hormonal control of casein synthesis in mammary explants from pregnant goats. Endokrinologie. 1982 Jun;79(2):301–307. [PubMed]
  • Vonderhaar BK, Tang E, Lyster RR, Nascimento MC. Thyroid hormone regulation of epidermal growth factor receptor levels in mouse mammary glands. Endocrinology. 1986 Aug;119(2):580–585. [PubMed]
  • Oberkotter LV, Farmer LC, Farber M. Thyroid hormone-binding inhibitor in normal, pregnant, and lactating rat and postmenopausal human breast tissue. Endocrinology. 1985 Aug;117(2):511–514. [PubMed]
  • Moon RC, Mehta RG. Anticarcinogenic effects of retinoids in animals. Adv Exp Med Biol. 1986;206:399–411. [PubMed]
  • Chakraborty S, Menon R, Banerjee MR. Influence of some dietary chemopreventive agents on the expression of functional differentiation of the mouse mammary gland in vitro. Int J Cancer. 1987 Jun 15;39(6):752–759. [PubMed]
  • Komura H, Wakimoto H, Chen CF, Terakawa N, Aono T, Tanizawa O, Matsumoto K. Retinoic acid enhances cell responses to epidermal growth factor in mouse mammary gland in culture. Endocrinology. 1986 Apr;118(4):1530–1536. [PubMed]
  • Zile MH, Cullum ME, Roltsch IA, DeHoog JV, Welsch CW. Effect of moderate vitamin A supplementation and lack of dietary vitamin A on the development of mammary tumors in female rats treated with low carcinogenic dose levels of 7,12-dimethylbenz(a)anthracene. Cancer Res. 1986 Jul;46(7):3495–3503. [PubMed]
  • Chatterjee M, Banerjee MR. N-Nitrosodiethylamine-induced nodule-like alveolar lesion and its prevention by a retinoid in BALB/c mouse mammary glands in the whole organ in culture. Carcinogenesis. 1982;3(7):801–804. [PubMed]
  • Sankaran L, Topper YJ. Effect of vitamin A deprivation on maintenance of rat mammary tissue and on the potential of the epithelium for hormone-dependent milk protein synthesis. Endocrinology. 1982 Oct;111(4):1061–1067. [PubMed]
  • Mehta RG, Moon RC. Role of hormones on the induction of retinoic acid binding protein in mouse mammary gland organ culture. Carcinogenesis. 1985 Aug;6(8):1103–1107. [PubMed]
  • Bhattacharjee M, Wientroub S, Vonderhaar BK. Milk protein synthesis by mammary glands of vitamin D-deficient mice. Endocrinology. 1987 Sep;121(3):865–874. [PubMed]
  • Narbaitz R, Sar M, Stumpf WE, Huang S, DeLuca HF. 1,25-Dihydroxyvitamin D3 target cells in rat mammary gland. Horm Res. 1981;15(4):263–269. [PubMed]
  • Mezzetti G, Barbiroli B, Oka T. 1,25-Dihydroxycholecalciferol receptor regulation in hormonally induced differentiation of mouse mammary gland in culture. Endocrinology. 1987 Jun;120(6):2488–2493. [PubMed]
  • McGrath CM, Soule HD. Calcium regulation of normal human mammary epithelial cell growth in culture. In Vitro. 1984 Aug;20(8):652–662. [PubMed]
  • Oka T, Perry JW, Terada N. The regulatory function of spermidine in hormonal control of the development of mouse mammary gland in culture. Fed Proc. 1982 Dec;41(14):3073–3077. [PubMed]
  • Rillema JA, Linebaugh BE, Mulder JA. Regulation of casein synthesis by polyamines in mammary gland explants of mice. Endocrinology. 1977 Feb;100(2):529–536. [PubMed]
  • Rillema JA. Activation of casein synthesis by prostaglandins plus spermidine in mammary gland explants of mice. Biochem Biophys Res Commun. 1976 May 3;70(1):45–49. [PubMed]
  • Bolander FF., Jr The relationship between adenosine diphosphate-ribosylation and mammary gland differentiation. J Cell Biochem. 1985;29(4):361–372. [PubMed]
  • Bolander FF., Jr The interrelationships among poly(ADP-ribosyl)ation, DNA synthesis and mammary gland differentiation. Biochem Biophys Res Commun. 1986 May 29;137(1):359–363. [PubMed]

Articles from Environmental Health Perspectives are provided here courtesy of National Institute of Environmental Health Science


Save items

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


  • MedGen
    Related information in MedGen
  • PubMed
    PubMed citations for these articles
  • Substance
    PubChem chemical substance records that cite the current articles. These references are taken from those provided on submitted PubChem chemical substance records.

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...