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Journal of Mammary Gland Biology and Neoplasia

Published in:

01-10-2006

Pubertal Mammary Gland Development: Insights from Mouse Models

Authors: Jillian Howlin, Jean McBryan, Finian Martin

Published in: Journal of Mammary Gland Biology and Neoplasia | Issue 3-4/2006

Abstract

During puberty the mammary gland develops from a rudimentary tree to a branched epithelial network of ducts which can support alveolar development and subsequent milk production during pregnancy and lactation. This process involves growth, proliferation, migration, branching, invasion, apoptosis and above all, tight regulation which allows these processes to take place simultaneously during the course of just a few weeks to create an adult gland. The process is under hormonal control and is thus coordinated with reproductive development. Mouse models, with overexpressed or knocked-out genes, have highlighted a number of pubertal mammary gland phenotypes and given significant insight into the regulatory mechanisms controlling this period of development. Here we review the published findings of the wide range of gene-manipulated mammary mouse models, documenting the common pubertal mammary gland phenotypes observed, and summarizing their contribution to our current understanding of how pubertal mammary gland development occurs.

Veltmaat JM, Mailleux AA, Thiery JP, Bellusci S. Mouse embryonic mammogenesis as a model for the molecular regulation of pattern formation. Differentiation 2003;71:1–17.PubMed

van Genderen C, Okamura RM, Farinas I, Quo RG, Parslow TG, Bruhn L, et al. Development of several organs that require inductive epithelial–mesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev 1994;8:2691–703.PubMed

Andl T, Reddy ST, Gaddapara T, Millar SE. WNT signals are required for the initiation of hair follicle development. Dev Cell 2002;2:643–53.PubMed

Mailleux AA, Spencer-Dene B, Dillon C, Ndiaye D, Savona-Baron C, Itoh N, et al. Role of FGF10/FGFR2b signaling during mammary gland development in the mouse embryo. Development 2002;129:53–60.PubMed

Satokata I, Ma L, Ohshima H, Bei M, Woo I, Nishizawa K, et al. Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation. Nat Genet 2000; 24:391–5.PubMed

Wysolmerski JJ, Philbrick WM, Dunbar ME, Lanske B, Kronenberg H, Broadus AE. Rescue of the parathyroid hormone-related protein knockout mouse demonstrates that parathyroid hormone-related protein is essential for mammary gland development. Development 1998;125:1285–94.PubMed

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

Hovey RC, Trott JF, Vonderhaar BK. Establishing a framework for the functional mammary gland: from endocrinology to morphology. J Mammary Gland Biol Neoplasia 2002;7:17–38.PubMed

Lewis MT, Ross S, Strickland PA, Sugnet CW, Jimenez E, Scott MP, et al. Defects in mouse mammary gland development caused by conditional haploinsufficiency of Patched-1. Development 1999;126:5181–93.PubMed

10.

Lewis MT, Ross S, Strickland PA, Sugnet CW, Jimenez E, Hui C, et al. The Gli2 transcription factor is required for normal mouse mammary gland development. Dev Biol 2001;238:133–44.PubMed

11.

Phippard DJ, Weber-Hall SJ, Sharpe PT, Naylor MS, Jayatalake H, Maas R, et al. Regulation of Msx-1, Msx-2, Bmp-2 and Bmp-4 during foetal and postnatal mammary gland development. Development 1996;122:2729–37.PubMed

12.

Robinson GW, McKnight RA, Smith GH, Hennighausen L. Mammary epithelial cells undergo secretory differentiation in cycling virgins but require pregnancy for the establishment of terminal differentiation. Development 1995;121:2079–90.PubMed

13.

Ball SM. The development of the terminal end bud in the prepubertal–pubertal mouse mammary gland. Anat Rec 1998;250:459–64.PubMed

14.

Williams JM, Daniel CW. Mammary ductal elongation: differentiation of myoepithelium and basal lamina during branching morphogenesis. Dev Biol 1983;97:274–90.PubMed

15.

Humphreys RC, Krajewska M, Krnacik S, Jaeger R, Weiher H, Krajewski S, et al. Apoptosis in the terminal endbud of the murine mammary gland: a mechanism of ductal morphogenesis. Development 1996;122:4013–22.PubMed

16.

Brisken C. Hormonal control of alveolar development and its implications for breast carcinogenesis. J Mammary Gland Biol Neoplasia 2002;7:39–48.PubMed

17.

Russo J, Moral R, Balogh GA, Mailo D, Russo IH. The protective role of pregnancy in breast cancer. Breast Cancer Res 2005;7:131–42.PubMed

18.

Andrechek ER, White D, Muller WJ. Targeted disruption of ErbB2/Neu in the mammary epithelium results in impaired ductal outgrowth. Oncogene 2005;24:932–7.PubMed

19.

Shillingford JM, Hennighausen L. Experimental mouse genetics—answering fundamental questions about mammary gland biology. Trends Endocrinol Metab 2001;12:402–8.PubMed

20.

Johnson M, Everitt B. Essential reproduction. London: Blackwell Science; 1997.

21.

Halban J. Die innere Sekretion von Ovarium und Placenta und ihre Bedeutung fuer die Function der Milchdruese. Mschr Geburtsh Gynaek 1900;496–503.

22.

Cunha GR, Young P, Hom YK, Cooke PS, Taylor JA, Lubahn DB. Elucidation of a role for stromal steroid hormone receptors in mammary gland growth and development using tissue recombinants. J Mammary Gland Biol Neoplasia 1997;2:393–402.PubMed

23.

Mueller SO, Clark JA, Myers PH, Korach KS. Mammary gland development in adult mice requires epithelial and stromal estrogen receptor alpha. Endocrinology 2002;143:2357–65.PubMed

24.

Mallepell S, Krust A, Chambon P, Brisken C. Paracrine signaling through the epithelial estrogen receptor alpha is required for proliferation and morphogenesis in the mammary gland. Proc Natl Acad Sci USA 2006;103:2196–201.PubMed

25.

Brisken C, Park S, Vass T, Lydon JP, O’Malley BW, Weinberg RA. A paracrine role for the epithelial progesterone receptor in mammary gland development. Proc Natl Acad Sci USA 1998;95:5076–81.PubMed

26.

Humphreys RC, Lydon JP, O’Malley BW, Rosen JM. Use of PRKO mice to study the role of progesterone in mammary gland development. J Mammary Gland Biol Neoplasia 1997;2:343–54.PubMed

27.

Atwood CS, Hovey RC, Glover JP, Chepko G, Ginsburg E, Robison WG, et al. Progesterone induces side-branching of the ductal epithelium in the mammary glands of peripubertal mice. J Endocrinol 2000;167:39–52.PubMed

28.

Schneider W, Ramachandran C, Satyaswaroop PG, Shyamala G. Murine progesterone receptor exists predominantly as the 83-kilodalton ‘A’ form. J Steroid Biochem Mol Biol 1991;38:285–91.PubMed

29.

Shyamala G, Yang X, Silberstein G, Barcellos-Hoff MH, Dale E. Transgenic mice carrying an imbalance in the native ratio of A to B forms of progesterone receptor exhibit developmental abnormalities in mammary glands. Proc Natl Acad Sci USA 1998;95:696–701.PubMed

30.

Conneely OM, Mulac-Jericevic B, Lydon JP, De Mayo FJ. Reproductive functions of the progesterone receptor isoforms: lessons from knock-out mice. Mol Cell Endocrinol 2001;179:97–103.PubMed

31.

Mulac-Jericevic B, Mullinax RA, DeMayo FJ, Lydon JP, Conneely OM. Subgroup of reproductive functions of progesterone mediated by progesterone receptor-B isoform. Science 2000;289:1751–4.PubMed

32.

Kingsley-Kallesen M, Mukhopadhyay SS, Wyszomierski SL, Schanler S, Schutz G, Rosen JM. The mineralocorticoid receptor may compensate for the loss of the glucocorticoid receptor at specific stages of mammary gland development. Mol Endocrinol 2002;16:2008–18.PubMed

33.

Reichardt HM, Horsch K, Grone HJ, Kolbus A, Beug H, Hynes N, et al. Mammary gland development and lactation are controlled by different glucocorticoid receptor activities. Eur J Endocrinol 2001;145:519–27.PubMed

34.

Welsh J, Wietzke JA, Zinser GM, Byrne B, Smith K, Narvaez CJ. Vitamin D-3 receptor as a target for breast cancer prevention. J Nutr 2003;133:2425S–33S.PubMed

35.

Zinser G, Packman K, Welsh J. Vitamin D(3) receptor ablation alters mammary gland morphogenesis. Development 2002;129:3067–76.PubMed

36.

Byrne IM, Flanagan L, Tenniswood MP, Welsh J. Identification of a hormone-responsive promoter immediately upstream of exon 1c in the human vitamin D receptor gene. Endocrinology 2000;141:2829–36.PubMed

37.

Kleinberg DL. Early mammary development: growth hormone and IGF-1. J Mammary Gland Biol Neoplasia 1997;2:49–57.PubMed

38.

Gallego MI, Binart N, Robinson GW, Okagaki R, Coschigano KT, Perry J, et al. Prolactin, growth hormone, and epidermal growth factor activate Stat5 in different compartments of mammary tissue and exert different and overlapping developmental effects. Dev Biol 2001;229:163–75.PubMed

39.

Horseman ND, Zhao W, Montecino-Rodriguez E, Tanaka M, Nakashima K, Engle SJ, et al. Defective mammopoiesis, but normal hematopoiesis, in mice with a targeted disruption of the prolactin gene. EMBO J 1997;16:6926–35.PubMed

40.

Ormandy CJ, Camus A, Barra J, Damotte D, Lucas B, Buteau H, et al. Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev 1997;11:167–78.PubMed

41.

Brisken C, Kaur S, Chavarria TE, Binart N, Sutherland RL, Weinberg RA, et al. Prolactin controls mammary gland development via direct and indirect mechanisms. Dev Biol 1999; 210:96–106.PubMed

42.

Naylor MJ, Lockefeer JA, Horseman ND, Ormandy CJ. Prolactin regulates mammary epithelial cell proliferation via autocrine/paracrine mechanism. Endocrine 2003;20:111–4.PubMed

43.

Edwards DP. The role of coactivators and corepressors in the biology and mechanism of action of steroid hormone receptors. J Mammary Gland Biol Neoplasia 2000;5:307–24.PubMed

44.

Xu J, Qiu Y, DeMayo FJ, Tsai SY, Tsai MJ, O’Malley BW. Partial hormone resistance in mice with disruption of the steroid receptor coactivator-1 (SRC-1) gene. Science 1998;279:1922–5.PubMed

45.

Weiss RE, Xu J, Ning G, Pohlenz J, O’Malley BW, Refetoff S. Mice deficient in the steroid receptor co-activator 1 (SRC-1) are resistant to thyroid hormone. EMBO J 1999;18:1900–4.PubMed

46.

Han SJ, DeMayo FJ, Xu J, Tsai SY, Tsai MJ, O’Malley BW. Steroid receptor coactivator (SRC)-1 and SRC-3 differentially modulate tissue-specific activation functions of the progesterone receptor. Mol Endocrinol 2006;20:45–55.PubMed

47.

Shim WS, DiRenzo J, DeCaprio JA, Santen RJ, Brown M, Jeng MH. Segregation of steroid receptor coactivator-1 from steroid receptors in mammary epithelium. Proc Natl Acad Sci USA 1999; 96:208–13.PubMed

48.

Xu J, Liao L, Ning G, Yoshida-Komiya H, Deng C, O’Malley BW. The steroid receptor coactivator SRC-3 (p/CIP/RAC3/AIB1/ACTR/TRAM-1) is required for normal growth, puberty, female reproductive function, and mammary gland development. Proc Natl Acad Sci USA 2000;97:6379–84.PubMed

49.

Howlin J, McBryan J, Napoletano S, Lambe T, McArdle E, Shioda T, et al. CITED1 homozygous null mice display aberrant pubertal mammary ductal morphogenesis. Oncogene 2006;25:1532–42.PubMed

50.

Shioda T, Lechleider RJ, Dunwoodie SL, Li H, Yahata T, de Caestecker MP, et al. Transcriptional activating activity of Smad4: roles of SMAD hetero-oligomerization and enhancement by an associating transactivator. Proc Natl Acad Sci USA 1998;95:9785–90.PubMed

51.

Shen Q, Zhang Y, Uray IP, Hill JL, Kim HT, Lu C, et al. The AP-1 transcription factor regulates postnatal mammary gland development. Dev Biol 2006;295:589–603.PubMed

52.

Zeps N, Bentel JM, Papadimitriou JM, D’Antuono MF, Dawkins HJ. Estrogen receptor-negative epithelial cells in mouse mammary gland development and growth. Differentiation 1998;62:221–6.PubMed

53.

Fendrick JL, Raafat AM, Haslam SZ. 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 1998;3:7–22.PubMed

54.

Ruan W, Newman CB, Kleinberg DL. Intact and amino-terminally shortened forms of insulin-like growth factor I induce mammary gland differentiation and development. Proc Natl Acad Sci U S A 1992;89:10872–6.PubMed

55.

Kleinberg DL, Ruan W, Catanese V, Newman CB, Feldman M. Non-lactogenic effects of growth hormone on growth and insulin-like growth factor-I messenger ribonucleic acid of rat mammary gland. Endocrinology 1990;126:3274–6.PubMedCrossRef

56.

Walden PD, Ruan W, Feldman M, Kleinberg DL. Evidence that the mammary fat pad mediates the action of growth hormone in mammary gland development. Endocrinology 1998;139:659–62.PubMed

57.

Ruan W, Kleinberg DL. Insulin-like growth factor I is essential for terminal end bud formation and ductal morphogenesis during mammary development. Endocrinology 1999;140:5075–81.PubMed

58.

Ruan W, Catanese V, Wieczorek R, Feldman M, Kleinberg DL. Estradiol enhances the stimulatory effect of insulin-like growth factor-I (IGF-I) on mammary development and growth hormone-induced IGF-I messenger ribonucleic acid. Endocrinology 1995;136:1296–302.PubMed

59.

Kleinberg DL. Role of IGF-I in normal mammary development. Breast Cancer Res Treat 1998;47:201–8.PubMed

60.

Richards RG, Klotz DM, Walker MP, Diaugustine RP. Mammary gland branching morphogenesis is diminished in mice with a deficiency of insulin-like growth factor-I (IGF-I), but not in mice with a liver-specific deletion of IGF-I. Endocrinology 2004;145:3106–10.PubMed

61.

Xie W, Paterson AJ, Chin E, Nabell LM, Kudlow JE. Targeted expression of a dominant negative epidermal growth factor receptor in the mammary gland of transgenic mice inhibits pubertal mammary duct development. Mol Endocrinol 1997;11:1766–81.PubMed

62.

Wiesen JF, Young P, Werb Z, Cunha GR. Signaling through the stromal epidermal growth factor receptor is necessary for mammary ductal development. Development 1999;126:335–44.PubMed

63.

Schroeder JA, Lee DC. Dynamic expression and activation of ERBB receptors in the developing mouse mammary gland. Cell Growth Differ 1998;9:451–64.PubMed

64.

Stern DF. ErbBs in mammary development. Exp Cell Res 2003;284:89–98.PubMed

65.

Sebastian J, Richards RG, Walker MP, Wiesen JF, Werb Z, Derynck R, et al. Activation and function of the epidermal growth factor receptor and erbB-2 during mammary gland morphogenesis. Cell Growth Differ 1998;9:777–85.PubMed

66.

Martinez-Lacaci I, Saceda M, Plowman GD, Johnson GR, Normanno N, Salomon DS, et al. Estrogen and phorbol esters regulate amphiregulin expression by two separate mechanisms in human breast cancer cell lines. Endocrinology 1995;136:3983–92.PubMed

67.

Soulez M, Parker MG. Identification of novel oestrogen receptor target genes in human ZR75-1 breast cancer cells by expression profiling. J Mol Endocrinol 2001;27:259–74.PubMed

68.

Luetteke NC, Qiu TH, Fenton SE, Troyer KL, Riedel RF, Chang A, et a1. Targeted inactivation of the EGF and amphiregulin genes reveals distinct roles for EGF receptor ligands in mouse mammary gland development. Development 1999;126:2739–50.PubMed

69.

Kenney NJ, Huang RP, Johnson GR, Wu JX, Okamura D, Matheny W, et al. Detection and location of amphiregulin and Cripto-1 expression in the developing postnatal mouse mammary gland. Mol Reprod Dev 1995;41:277–86.PubMed

70.

D’Cruz CM, Moody SE, Master SR, Hartman JL, Keiper EA, Imielinski MB, et al. Persistent parity-induced changes in growth factors, TGF-beta3, and differentiation in the rodent mammary gland. Mol Endocrinol 2002;16:2034–51.PubMed

71.

Sahin U, Weskamp G, Kelly K, Zhou HM, Higashiyama S, Peschon J, et al. Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J Cell Biol 2004;164:769–79.PubMed

72.

Sternlicht MD, Sunnarborg SW, Kouros-Mehr H, Yu Y, Lee DC, Werb Z. Mammary ductal morphogenesis requires paracrine activation of stromal EGFR via ADAM17-dependent shedding of epithelial amphiregulin. Development 2005;132:3923–33.PubMed

73.

Brisken C, Heineman A, Chavarria T, Elenbaas B, Tan J, Dey SK, et al. Essential function of Wnt-4 in mammary gland development downstream of progesterone signaling. Genes Dev 2000;14:650–4.PubMed

74.

Weber-Hall SJ, Phippard DJ, Niemeyer CC, Dale TC. Developmental and hormonal regulation of Wnt gene expression in the mouse mammary gland. Differentiation 1994;57:205–14.PubMed

75.

Gouon-Evans V, Lin EY, Pollard JW. Requirement of macrophages and eosinophils and their cytokines/chemokines for mammary gland development. Breast Cancer Res 2002;4:155–64.PubMed

76.

Gouon-Evans V, Rothenberg ME, Pollard JW. Postnatal mammary gland development requires macrophages and eosinophils. Development 2000;127:2269–82.PubMed

77.

Van Nguyen A, Pollard JW. Colony stimulating factor-1 is required to recruit macrophages into the mammary gland to facilitate mammary ductal outgrowth. Dev Biol 2002;247:11–25.PubMed

78.

Palframan RT, Collins PD, Severs NJ, Rothery S, Williams TJ, Rankin SM. Mechanisms of acute eosinophil mobilization from the bone marrow stimulated by interleukin 5: the role of specific adhesion molecules and phosphatidylinositol 3-kinase. J Exp Med 1998;188:1621–32.PubMed

79.

Sferruzzi-Perri AN, Robertson SA, Dent LA. Interleukin-5 transgene expression and eosinophilia are associated with retarded mammary gland development in mice. Biol Reprod 2003;69:224–33.PubMed

80.

Hinck L. The versatile roles of “axon guidance" cues in tissue morphogenesis. Dev Cell 2004;7:783–93.PubMed

81.

Morris JS, Stein T, Pringle MA, Davies CR, Weber-Hall S, Ferrier RK, et al. Involvement of axonal guidance proteins and their signaling partners in the developing mouse mammary gland. J Cell Physiol 2006;206:16–24.PubMed

82.

Srinivasan K, Strickland P, Valdes A, Shin GC, Hinck L. Netrin-1/neogenin interaction stabilizes multipotent progenitor cap cells during mammary gland morphogenesis. Dev Cell 2003;4:371–82.PubMed

83.

Andres AC, Ziemiecki A. Eph and ephrin signaling in mammary gland morphogenesis and cancer. J Mammary Gland Biol Neoplasia 2003;8:475–85.PubMed

84.

Nikolova Z, Djonov V, Zuercher G, Andres AC, Ziemiecki A. Cell-type specific and estrogen dependent expression of the receptor tyrosine kinase EphB4 and its ligand ephrin-B2 during mammary gland morphogenesis. J Cell Sci 1998;(111 Pt)18:2741–51.PubMed

85.

Munarini N, Jager R, Abderhalden S, Zuercher G, Rohrbach V, Loercher S, et al. Altered mammary epithelial development, pattern formation and involution in transgenic mice expressing the EphB4 receptor tyrosine kinase. J Cell Sci 2002;115:25–37.PubMed

86.

Daniel CW, Strickland P, Friedmann Y. Expression and functional role of E- and P-cadherins in mouse mammary ductal morphogenesis and growth. Dev Biol 1995;169:511–9.PubMed

87.

Radice GL, Ferreira-Cornwell MC, Robinson SD, Rayburn H, Chodosh LA, Takeichi M, et al. Precocious mammary gland development in P-cadherin-deficient mice. J Cell Biol 1997;139:1025–32.PubMed

88.

Fata JE, Werb Z, Bissell MJ. Regulation of mammary gland branching morphogenesis by the extracellular matrix and its remodeling enzymes. Breast Cancer Res 2004;6:1–11.PubMed

89.

Lee JM, Dedhar S, Kalluri R, Thompson EW. The epithelial–mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol 2006;172:973–81.PubMed

90.

Wiseman BS, Sternlicht MD, Lund LR, Alexander CM, Mott J, Bissell MJ, et al. Site-specific inductive and inhibitory activities of MMP-2 and MMP-3 orchestrate mammary gland branching morphogenesis. J Cell Biol 2003;162:1123–33.PubMed

91.

Sympson CJ, Talhouk RS, Alexander CM, Chin JR, Clift SM, Bissell MJ, et al. Targeted expression of stromelysin-1 in mammary gland provides evidence for a role of proteinases in branching morphogenesis and the requirement for an intact basement membrane for tissue-specific gene expression. J Cell Biol 1994;125:681–93.PubMed

92.

Thomasset N, Lochter A, Sympson CJ, Lund LR, Williams DR, Behrendtsen O, et al. Expression of autoactivated stromelysin-1 in mammary glands of transgenic mice leads to a reactive stroma during early development. Am J Pathol 1998;153:457–67.PubMed

93.

Sternlicht MD, Bissell MJ, Werb Z. The matrix metalloproteinase stromelysin-1 acts as a natural mammary tumor promoter. Oncogene 2000;19:1102–13.PubMed

94.

Fata JE, Leco KJ, Moorehead RA, Martin DC, Khokha R. Timp-1 is important for epithelial proliferation and branching morphogenesis during mouse mammary development. Dev Biol 1999;211:238–54.PubMed

95.

Silberstein GB, Daniel CW. Reversible inhibition of mammary gland growth by transforming growth factor-beta. Science 1987;237:291–3.PubMed

96.

Pollard JW. Tumour-stromal interactions. Transforming growth factor-beta isoforms and hepatocyte growth factor/scatter factor in mammary gland ductal morphogenesis. Breast Cancer Res 2001;3:230–7.PubMed

97.

Donovan J, Slingerland J. Transforming growth factor-beta and breast cancer: cell cycle arrest by transforming growth factor-beta and its disruption in cancer. Breast Cancer Res 2000;2:116–24.PubMed

98.

Silberstein GB, Flanders KC, Roberts AB, Daniel CW. Regulation of mammary morphogenesis: evidence for extracellular matrix-mediated inhibition of ductal budding by transforming growth factor-beta 1. Dev Biol 1992;152:354–62.PubMed

99.

Pierce DF Jr, Johnson MD, Matsui Y, Robinson SD, Gold LI, Purchio AF, et al. Inhibition of mammary duct development but not alveolar outgrowth during pregnancy in transgenic mice expressing active TGF-beta 1. Genes Dev 1993;7:2308–17.PubMed

100.

Ewan KB, Shyamala G, Ravani SA, Tang Y, Akhurst R, Wakefield L, et al. Latent transforming growth factor-beta activation in mammary gland: regulation by ovarian hormones affects ductal and alveolar proliferation. Am J Pathol 2002;160:2081–93.PubMed

101.

Wakefield LM, Piek E, Bottinger EP. TGF-beta signaling in mammary gland development and tumorigenesis. J Mammary Gland Biol Neoplasia 2001;6:67–82.PubMed

102.

Yang YA, Tang B, Robinson G, Hennighausen L, Brodie SG, Deng CX, et al. Smad3 in the mammary epithelium has a nonredundant role in the induction of apoptosis, but not in the regulation of proliferation or differentiation by transforming growth factor-beta. Cell Growth Differ 2002;13:123–30.PubMed

103.

Imbert A, Eelkema R, Jordan S, Feiner H, Cowin P. Delta N89 beta-catenin induces precocious development, differentiation, and neoplasia in mammary gland. J Cell Biol 2001;153:555–68.PubMed

104.

Bagheri-Yarmand R, Talukder AH, Wang RA, Vadlamudi RK, Kumar R. Metastasis-associated protein 1 deregulation causes inappropriate mammary gland development and tumorigenesis. Development 2004;131:3469–79.PubMed

105.

Wysolmerski JJ, McCaughern-Carucci JF, Daifotis AG, Broadus AE, Philbrick WM. Overexpression of parathyroid hormone-related protein or parathyroid hormone in transgenic mice impairs branching morphogenesis during mammary gland development. Development 1995;121:3539–47.PubMed

106.

Dunbar ME, Dann P, Brown CW, Van Houton J, Dreyer B, Philbrick WP, et al. Temporally regulated overexpression of parathyroid hormone-related protein in the mammary gland reveals distinct fetal and pubertal phenotypes. J Endocrinol 2001;171:403–16.PubMed

107.

Yant J, Buluwela L, Niranjan B, Gusterson B, Kamalati T. In vivo effects of hepatocyte growth factor/scatter factor on mouse mammary gland development. Exp Cell Res 1998;241:476–81.PubMed

108.

Ngan ES, Ma ZQ, Chua SS, DeMayo FJ, Tsai SY. Inducible expression of FGF-3 in mouse mammary gland. Proc Natl Acad Sci USA 2002;99:11187–92.PubMed

109.

Robinson GW, Hennighausen L. Inhibins and activins regulate mammary epithelial cell differentiation through mesenchymal–epithelial interactions. Development 1997;124:2701–8.PubMed

110.

Seagroves TN, Krnacik S, Raught B, Gay J, Burgess-Beusse B, Darlington GJ, et al. C/EBPbeta, but not C/EBPalpha, is essential for ductal morphogenesis, lobuloalveolar proliferation, and functional differentiation in the mouse mammary gland. Genes Dev 1998;12:1917–28.PubMed

111.

Muraoka RS, Lenferink AE, Simpson J, Brantley DM, Roebuck LR, Yakes FM, et al. Cyclin-dependent kinase inhibitor p27(Kip1) is required for mouse mammary gland morphogenesis and function. J Cell Biol 2001;153:917–32.PubMed

112.

Klinowska TC, Soriano JV, Edwards GM, Oliver JM, Valentijn AJ, Montesano R, et al. Laminin and beta1 integrins are crucial for normal mammary gland development in the mouse. Dev Biol 1999;215:13–32.PubMed

113.

Crowley MR, Head KL, Kwiatkowski DJ, Asch HL, Asch BB. The mouse mammary gland requires the actin-binding protein gelsolin for proper ductal morphogenesis. Dev Biol 2000;225:407–23.PubMed

114.

Vogel WF, Aszodi A, Alves F, Pawson T. Discoidin domain receptor 1 tyrosine kinase has an essential role in mammary gland development. Mol Cell Biol 2001;21:2906–17.PubMed

115.

Hathaway HJ, Shur BD. Mammary gland morphogenesis is inhibited in transgenic mice that overexpress cell surface beta1,4-galactosyltransferase. Development 1996;122:2859–72.PubMed

116.

Steffgen K, Dufraux K, Hathaway H. Enhanced branching morphogenesis in mammary glands of mice lacking cell surface beta1,4-galactosyltransferase. Dev Biol 2002;244:114–33.PubMed

117.

Chakravarty G, Hadsell D, Buitrago W, Settleman J, Rosen JM. p190-B RhoGAP regulates mammary ductal morphogenesis. Mol Endocrinol 2003;17:1054–65.PubMed

118.

Shillingford JM, Miyoshi K, Flagella M, Shull GE, Hennighausen L. Mouse mammary epithelial cells express the Na–K–Cl cotransporter, NKCC1: characterization, localization, and involvement in ductal development and morphogenesis. Mol Endocrinol 2002;16:1309–21.PubMed

119.

Stairs DB, Notarfrancesco KL, Chodosh LA. The serine/threonine kinase, Krct, affects endbud morphogenesis during murine mammary gland development. Transgenic Res 2005;14:919–40.PubMed

Title: Pubertal Mammary Gland Development: Insights from Mouse Models
Authors: Jillian Howlin
Jean McBryan
Finian Martin
Publication date: 01-10-2006
Publisher: Kluwer Academic Publishers-Plenum Publishers
Published in: Journal of Mammary Gland Biology and Neoplasia / Issue 3-4/2006
Print ISSN: 1083-3021
Electronic ISSN: 1573-7039
DOI: https://doi.org/10.1007/s10911-006-9024-2

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