Mammary gland development

Wiley Interdisciplinary Reviews: Developmental Biology

Volumn 1, Issue 4, 2012, Pages 533-557

  Macias, Hector ^a   Hinck, Lindsay ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIREGULIN; BONE MORPHOGENETIC PROTEIN; DICKKOPF 1 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 4; ESTROGEN; FIBROBLAST GROWTH FACTOR 10; GROWTH HORMONE; LACTADHERIN; NETRIN 1; NEU DIFFERENTIATION FACTOR; PARATHYROID HORMONE RELATED PROTEIN; PARATHYROID HORMONE RELATED PROTEIN RECEPTOR; PROGESTERONE; PROLACTIN; REELIN; SLIT2 PROTEIN; SOMATOMEDIN C; SONIC HEDGEHOG PROTEIN; T BOX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GLI3; TRANSCRIPTION FACTOR PAX3; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; UNINDEXED DRUG; WNT10B PROTEIN; WNT11 PROTEIN; WNT3 PROTEIN; WNT5A PROTEIN; WNT6 PROTEIN;

APOPTOSIS; AUTOPHAGY; BRANCHING MORPHOGENESIS; BREAST CANCER; BREAST DEVELOPMENT; BREAST DUCT; CELL COMMUNICATION; CELL DIFFERENTIATION; CHEMICAL CUE; CHONDRODYSPLASIA; EMBRYO DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; GENE; GENE EXPRESSION; HORMONAL REGULATION; INVOLUTION; LACTATION; LARON SYNDROME; MAMMARY GLAND; MAMMARY STEM CELL; NIPPLE; NONHUMAN; POLAND SYNDROME; PREGNANCY; PUBERTY; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; WEANING; WNT SIGNALING PATHWAY;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; FEMALE; HORMONES; HUMANS; MAMMALS; MAMMARY GLANDS, ANIMAL; MAMMARY GLANDS, HUMAN; MORPHOGENESIS; STEM CELLS;

EID: 84871436562     PISSN: 17597684     EISSN: 17597692     Source Type: Journal    
DOI: 10.1002/wdev.35     Document Type: Review

References (167)

1. Oftedal OT. The mammary gland and its origin during synapsid evolution. J Mammary Gland Biol Neoplasia 2002, 7:225-252.
2. Balinsky BI. On the prenatal growth of the mammary gland rudiment in the mouse. J Anat 1950, 84:227-235.
3. Propper AY. Wandering epithelial cells in the rabbit embryo milk line. A preliminary scanning electron microscope study. Dev Biol 1978, 67:225-231.
4. Howard BA, Gusterson BA. Human breast development. J Mammary Gland Biol Neoplasia 2000, 5:119-137.
5. Cunha GR, Young P, Christov K, Guzman R, Nandi S, Talamantes F, Thordarson G. Mammary phenotypic expression induced in epidermal cells by embryonic mammary mesenchyme. Acta Anat (Basel) 1995, 152:195-204.
6. Kratochwil K. Organ specificity in mesenchymal induction demonstrated in the embryonic development of the mammary gland of the mouse. Dev Biol 1969, 20:46-71.
7. Sakakura T, Nishizuka Y, Dawe CJ. Mesenchyme-dependent morphogenesis and epithelium-specific cytodifferentiation in mouse mammary gland. Science 1976, 194:1439-1441.
8. Robinson GW, Karpf AB, Kratochwil K. Regulation of mammary gland development by tissue interaction. J Mammary Gland Biol Neoplasia 1999, 4:9-19.
9. Sakakura T, Sakagami Y, Nishizuka Y. Dual origin of mesenchymal tissues participating in mouse mammary gland embryogenesis. Dev Biol 1982, 91:202-207.
10. Chu EY, Hens J, Andl T, Kairo A, Yamaguchi TP, Brisken C, Glick A, Wysolmerski JJ, Millar SE. Canonical WNT signaling promotes mammary placode development and is essential for initiation of mammary gland morphogenesis. Development 2004, 131:4819-4829.
11. Veltmaat JM, Van Veelen W, Thiery JP, Bellusci S. Identification of the mammary line in mouse by Wnt10b expression. Dev Dyn 2004, 229:349-356.
12. van Genderen C, Okamura RM, Farinas I, Quo RG, Parslow TG, Bruhn L, Grosschedl R. Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev 1994, 8:2691-2703.
13. Jerome-Majewska LA, Jenkins GP, Ernstoff E, Zindy F, Sherr CJ, Papaioannou VE. Tbx3, the ulnar-mammary syndrome gene, and Tbx2 interact in mammary gland development through a p19Arf/p53-independent pathway. Dev Dyn 2005, 234:922-933.
14. Bamshad M, Lin RC, Law DJ, Watkins WC, Krakowiak PA, Moore ME, Franceschini P, Lala R, Holmes LB, Gebuhr TC, et al. Mutations in human TBX3 alter limb, apocrine and genital development in ulnar-mammary syndrome. Nat Genet 1997, 16:311-315.
15. Cho KW, Kim JY, Song SJ, Farrell E, Eblaghie MC, Kim HJ, Tickle C, Jung HS. Molecular interactions between Tbx3 and Bmp4 and a model for dorsoventral positioning of mammary gland development. Proc Natl Acad Sci U S A 2006, 103:16788-16793.
16. Davenport TG, Jerome-Majewska LA, Papaioannou VE. Mammary gland, limb and yolk sac defects in mice lacking Tbx3, the gene mutated in human ulnar mammary syndrome. Development 2003, 130:2263-2273.
17. Veltmaat JM, Relaix F, Le LT, Kratochwil K, Sala FG, van Veelen W, Rice R, Spencer-Dene B, Mailleux AA, Rice DP, et al. Gli3-mediated somitic Fgf10 expression gradients are required for the induction and patterning of mammary epithelium along the embryonic axes. Development 2006, 133:2325-2335.
18. Mailleux AA, Kelly R, Veltmaat JM, De Langhe SP, Zaffran S, Thiery JP, Bellusci S. Fgf10 expression identifies parabronchial smooth muscle cell progenitors and is required for their entry into the smooth muscle cell lineage. Development 2005, 132:2157-2166.
19. Baban A, Torre M, Bianca S, Buluggiu A, Rossello MI, Calevo MG, Valle M, Ravazzolo R, Jasonni V, Lerone M. Poland syndrome with bilateral features: case description with review of the literature. Am J Med Genet A 2009, 149A:1597-1602.
20. Hatsell SJ, Cowin P. Gli3-mediated repression of Hedgehog targets is required for normal mammary development. Development 2006, 133:3661-3670.
21. Wang C, Ruther U, Wang B. The Shh-independent activator function of the full-length Gli3 protein and its role in vertebrate limb digit patterning. Dev Biol 2007, 305:460-469.
22. Aoto K, Nishimura T, Eto K, Motoyama J. Mouse GLI3 regulates Fgf8 expression and apoptosis in the developing neural tube, face, and limb bud. Dev Biol 2002, 251:320-332.
23. Panchal H, Wansbury O, Parry S, Ashworth A, Howard B. Neuregulin3 alters cell fate in the epidermis and mammary gland. BMC Dev Biol 2007, 7:105.
24. Howard BA, Gusterson BA. The characterization of a mouse mutant that displays abnormal mammary gland development. Mamm Genome 2000, 11:234-237.
25. Howard B, Panchal H, McCarthy A, Ashworth A. Identification of the scaramanga gene implicates Neuregulin3 in mammary gland specification. Genes Dev 2005, 19:2078-2090.
26. Eblaghie MC, Song SJ, Kim JY, Akita K, Tickle C, Jung HS. Interactions between FGF and Wnt signals and Tbx3 gene expression in mammary gland initiation in mouse embryos. J Anat 2004, 205:1-13.
27. Fliniaux I, Mikkola ML, Lefebvre S, Thesleff I. Identification of dkk4 as a target of Eda-A1/Edar pathway reveals an unexpected role of ectodysplasin as inhibitor of Wnt signalling in ectodermal placodes. Dev Biol 2008, 320:60-71.
28. Mustonen T, Pispa J, Mikkola ML, Pummila M, Kangas AT, Pakkasjarvi L, Jaatinen R, Thesleff I. Stimulation of ectodermal organ development by Ectodysplasin-A1. Dev Biol 2003, 259:123-136.
29. Monreal AW, Ferguson BM, Headon DJ, Street SL, Overbeek PA, Zonana J. Mutations in the human homologue of mouse dl cause autosomal recessive and dominant hypohidrotic ectodermal dysplasia. Nat Genet 1999, 22:366-369.
30. Cowin P, Wysolmerski J. Molecular mechanisms guiding embryonic mammary gland development. Cold Spring Harb Perspect Biol 2010, 2:a003251.
31. Hogg NA, Harrison CJ, Tickle C. Lumen formation in the developing mouse mammary gland. J Embryol Exp Morphol 1983, 73:39-57.
32. Blatchford DR, Quarrie LH, Tonner E, McCarthy C, Flint DJ, Wilde CJ. Influence of microenvironment on mammary epithelial cell survival in primary culture. J Cell Physiol 1999, 181:304-311.
33. Ewald AJ, Brenot A, Duong M, Chan BS, Werb Z. Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis. Dev Cell 2008, 14:570-581.
34. Debnath J, Mills KR, Collins NL, Reginato MJ, Muthuswamy SK, Brugge JS. The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 2002, 111:29-40.
35. Hens JR, Dann P, Zhang JP, Harris S, Robinson GW, Wysolmerski J. BMP4 and PTHrP interact to stimulate ductal outgrowth during embryonic mammary development and to inhibit hair follicle induction. Development 2007, 134:1221-1230.
36. Kratochwil K, Schwartz P. Tissue interaction in androgen response of embryonic mammary rudiment of mouse: identification of target tissue for testosterone. Proc Natl Acad Sci U S A 1976, 73:4041-4044.
37. Juppner H, Abou-Samra AB, Freeman M, Kong XF, Schipani E, Richards J, Kolakowski LF Jr. Hock J, Potts JT Jr. Kronenberg HM, et al. A G protein-linked receptor for parathyroid hormone and parathyroid hormone-related peptide. Science 1991, 254:1024-1026.
38. 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, 121:3539-3547.
39. Jobert AS, Zhang P, Couvineau A, Bonaventure J, Roume J, Le Merrer M, Silve C. Absence of functional receptors for parathyroid hormone and parathyroid hormone-related peptide in Blomstrand chondrodysplasia. J Clin Invest 1998, 102:34-40.
40. Wysolmerski JJ, Cormier S, Philbrick WM, Dann P, Zhang JP, Roume J, Delezoide AL, Silve C. Absence of functional type 1 parathyroid hormone (PTH)/PTH-related protein receptors in humans is associated with abnormal breast development and tooth impaction. J Clin Endocrinol Metab 2001, 86:1788-1794.
41. 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, 125:1285-1294.
42. Foley J, Dann P, Hong J, Cosgrove J, Dreyer B, Rimm D, Dunbar M, Philbrick W, Wysolmerski J. Parathyroid hormone-related protein maintains mammary epithelial fate and triggers nipple skin differentiation during embryonic breast development. Development 2001, 128:513-525.
43. Williams JM, Daniel CW. Mammary ductal elongation: differentiation of myoepithelium and basal lamina during branching morphogenesis. Dev Biol 1983, 97:274-290.
44. Trott JF, Vonderhaar BK, Hovey RC. Historical perspectives of prolactin and growth hormone as mammogens, lactogens and galactagogues-agog for the future! J Mammary Gland Biol Neoplasia 2008, 13:3-11.
45. Gallego MI, Binart N, Robinson GW, Okagaki R, Coschigano KT, Perry J, Kopchick JJ, Oka T, Kelly PA, Hennighausen L. 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, 229:163-175.
46. Ruan W, Kleinberg DL. Insulin-like growth factor I is essential for terminal end bud formation and ductal morphogenesis during mammary development. Endocrinology 1999, 140:5075-5081.
47. Zhou Y, Xu BC, Maheshwari HG, He L, Reed M, Lozykowski M, Okada S, Cataldo L, Coschigamo K, Wagner TE, et al. A mammalian model for Laron syndrome produced by targeted disruption of the mouse growth hormone receptor/binding protein gene (the Laron mouse). Proc Natl Acad Sci U S A 1997, 94:13215-13220.
48. 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, 145:3106-3110.
49. Cannata D, Lann D, Wu Y, Elis S, Sun H, Yakar S, Lazzarino DA, Wood TL, Leroith D. Elevated circulating IGF-I promotes mammary gland development and proliferation. Endocrinology 2010, 151:5751-5761.
50. Bohlke K, Cramer DW, Trichopoulos D, Mantzoros CS. Insulin-like growth factor-I in relation to premenopausal ductal carcinoma in situ of the breast. Epidemiology 1998, 9:570-573.
51. Hankinson SE, Willett WC, Colditz GA, Hunter DJ, Michaud DS, Deroo B, Rosner B, Speizer FE, Pollak M. Circulating concentrations of insulin-like growth factor-I and risk of breast cancer. Lancet 1998, 351:1393-1396.
52. Lieberman ME, Maurer RA, Gorski J. Estrogen control of prolactin synthesis in vitro. Proc Natl Acad Sci U S A 1978, 75:5946-5949.
53. Silberstein GB, Daniel CW. Elvax 40P implants: sustained, local release of bioactive molecules influencing mammary ductal development. Dev Biol 1982, 93:272-278.
54. Daniel CW, Silberstein GB, Strickland P. Direct action of 17 β-estradiol on mouse mammary ducts analyzed by sustained release implants and steroid autoradiography. Cancer Res 1987, 47:6052-6057.
55. Silberstein GB, Van Horn K, Shyamala G, Daniel CW. Essential role of endogenous estrogen in directly stimulating mammary growth demonstrated by implants containing pure antiestrogens. Endocrinology 1994, 134:84-90.
56. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci U S A 1993, 90:11162-11166.
57. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, Mahler JF, Sar M, Korach KS, Gustafsson JA, Smithies O. Generation and reproductive phenotypes of mice lacking estrogen receptor β. Proc Natl Acad Sci U S A 1998, 95:15677-15682.
58. 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, 62:221-226.
59. Mallepell S, Krust A, Chambon P, Brisken C. Paracrine signaling through the epithelial estrogen receptor α is required for proliferation and morphogenesis in the mammary gland. Proc Natl Acad Sci U S A 2006, 103:2196-2201.
60. Nandi S. Endocrine control of mammary-gland development and function in the C3H/He Crgl mouse. J Natl Cancer Inst Monogr 1958, 21:1039-1063.
61. Nandi S. Hormonal control of mammogenesis and lactogenesis in the C3H/He Crgl mouse. Univ Calif Berkeley Publ Zoo 1959, 65:1-128.
62. Feng Y, Manka D, Wagner KU, Khan SA. Estrogen receptor-α expression in the mammary epithelium is required for ductal and alveolar morphogenesis in mice. Proc Natl Acad Sci U S A 2007, 104:14718-14723.
63. Coleman S, Silberstein GB, Daniel CW. Ductal morphogenesis in the mouse mammary gland: evidence supporting a role for epidermal growth factor. Dev Biol 1988, 127:304-315.
64. Kenney NJ, Bowman A, Korach KS, Barrett JC, Salomon DS. Effect of exogenous epidermal-like growth factors on mammary gland development and differentiation in the estrogen receptor-α knockout (ERKO) mouse. Breast Cancer Res Treat 2003, 79:161-173.
65. Luetteke NC, Qiu TH, Fenton SE, Troyer KL, Riedel RF, Chang A, Lee DC. Targeted inactivation of the EGF and amphiregulin genes reveals distinct roles for EGF receptor ligands in mouse mammary gland development. Development 1999, 126:2739-2750.
66. Ciarloni L, Mallepell S, Brisken C. Amphiregulin is an essential mediator of estrogen receptor α function in mammary gland development. Proc Natl Acad Sci U S A 2007, 104:5455-5460.
67. 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, 132:3923-3933.
68. Wiesen JF, Young P, Werb Z, Cunha GR. Signaling through the stromal epidermal growth factor receptor is necessary for mammary ductal development. Development 1999, 126:335-344.
69. Chakravorti S, Sheffield L. Acidic and basic fibroblast growth factor mRNA and protein in mouse mammary glands. Endocrine 1996, 4:175-182.
70. Lu P, Ewald AJ, Martin GR, Werb Z. Genetic mosaic analysis reveals FGF receptor 2 function in terminal end buds during mammary gland branching morphogenesis. Dev Biol 2008, 321:77-87.
71. Silberstein GB, Daniel CW. Reversible inhibition of mammary gland growth by transforming growth factor-β. Science 1987, 237:291-293.
72. Ewan KB, Shyamala G, Ravani SA, Tang Y, Akhurst R, Wakefield L, Barcellos-Hoff MH. Latent transforming growth factor-β activation in mammary gland: regulation by ovarian hormones affects ductal and alveolar proliferation. Am J Pathol 2002, 160:2081-2093.
73. Ingman WV, Robertson SA. Mammary gland development in transforming growth factor β1 null mutant mice: systemic and epithelial effects. Biol Reprod 2008, 79:711-717.
74. Joseph H, Gorska AE, Sohn P, Moses HL, Serra R. Overexpression of a kinase-deficient transforming growth factor-β type II receptor in mouse mammary stroma results in increased epithelial branching. Mol Biol Cell 1999, 10:1221-1234.
75. Cheng N, Bhowmick NA, Chytil A, Gorksa AE, Brown KA, Muraoka R, Arteaga CL, Neilson EG, Hayward SW, Moses HL. Loss of TGF-β type II receptor in fibroblasts promotes mammary carcinoma growth and invasion through upregulation of TGF-α-, MSP- and HGF-mediated signaling networks. Oncogene 2005, 24:5053-5068.
76. Gorska AE, Joseph H, Derynck R, Moses HL, Serra R. Dominant-negative interference of the transforming growth factor β type II receptor in mammary gland epithelium results in alveolar hyperplasia and differentiation in virgin mice. Cell Growth Differ 1998, 9:229-238.
77. Nelson CM, Vanduijn MM, Inman JL, Fletcher DA, Bissell MJ. Tissue geometry determines sites of mammary branching morphogenesis in organotypic cultures. Science 2006, 314:298-300.
78. Roarty K, Serra R. Wnt5a is required for proper mammary gland development and TGF-β-mediated inhibition of ductal growth. Development 2007, 134:3929-3939.
79. 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, 4:371-382.
80. Strickland P, Shin GC, Plump A, Tessier-Lavigne M, Hinck L. Slit2 and netrin 1 act synergistically as adhesive cues to generate tubular bi-layers during ductal morphogenesis. Development 2006, 133:823-832.
81. Khialeeva E, Lane TF, Carpenter EM. Disruption of reelin signaling alters mammary gland morphogenesis. Development 2011, 138:767-776.
82. Ensslin MA, Shur BD. The EGF repeat and discoidin domain protein, SED1/MFG-E8, is required for mammary gland branching morphogenesis. Proc Natl Acad Sci U S A 2007, 104:2715-2720.
83. Atabai K, Fernandez R, Huang X, Ueki I, Kline A, Li Y, Sadatmansoori S, Smith-Steinhart C, Zhu W, Pytela R, et al. Mfge8 is critical for mammary gland remodeling during involution. Mol Biol Cell 2005, 16:5528-5537.
84. Lee S, Medina D, Tsimelzon A, Mohsin SK, Mao S, Wu Y, Allred DC. Alterations of gene expression in the development of early hyperplastic precursors of breast cancer. Am J Pathol 2007, 171:252-262.
85. Baillo A, Giroux C, Ethier SP. Knock-down of amphiregulin inhibits cellular invasion in inflammatory breast cancer. J Cell Physiol 2011.
86. Djonov V, Andres AC, Ziemiecki A. Vascular remodelling during the normal and malignant life cycle of the mammary gland. Microsc Res Tech 2001, 52:182-189.
87. Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery CA Jr, Shyamala G, Conneely OM, O'Malley BW. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 1995, 9:2266-2278.
88. 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 U S A 1998, 95:5076-5081.
89. Seagroves TN, Lydon JP, Hovey RC, Vonderhaar BK, Rosen JM. C/EBPβ (CCAAT/enhancer binding protein) controls cell fate determination during mammary gland development. Mol Endocrinol 2000, 14:359-368.
90. Shyamala G, Schneider W, Schott D. Developmental regulation of murine mammary progesterone receptor gene expression. Endocrinology 1990, 126:2882-2889.
91. Mulac-Jericevic B, Lydon JP, DeMayo FJ, Conneely OM. Defective mammary gland morphogenesis in mice lacking the progesterone receptor B isoform. Proc Natl Acad Sci U S A 2003, 100:9744-9749.
92. 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, 289:1751-1754.
93. Richer JK, Jacobsen BM, Manning NG, Abel MG, Wolf DM, Horwitz KB. Differential gene regulation by the two progesterone receptor isoforms in human breast cancer cells. J Biol Chem 2002, 277:5209-5218.
94. Graham JD, Yeates C, Balleine RL, Harvey SS, Milliken JS, Bilous AM, Clarke CL. Characterization of progesterone receptor A and B expression in human breast cancer. Cancer Res 1995, 55:5063-5068.
95. Fata JE, Kong YY, Li J, Sasaki T, Irie-Sasaki J, Moorehead RA, Elliott R, Scully S, Voura EB, Lacey DL, et al. The osteoclast differentiation factor osteoprotegerin-ligand is essential for mammary gland development. Cell 2000, 103:41-50.
96. Beleut M, Rajaram RD, Caikovski M, Ayyanan A, Germano D, Choi Y, Schneider P, Brisken C. Two distinct mechanisms underlie progesterone-induced proliferation in the mammary gland. Proc Natl Acad Sci U S A 2010, 107:2989-2994.
97. Mukherjee A, Soyal SM, Li J, Ying Y, He B, DeMayo FJ, Lydon JP. Targeting RANKL to a specific subset of murine mammary epithelial cells induces ordered branching morphogenesis and alveologenesis in the absence of progesterone receptor expression. FASEB J 2010, 24:4408-4419.
98. Fernandez-Valdivia R, Mukherjee A, Creighton CJ, Buser AC, DeMayo FJ, Edwards DP, Lydon JP. Transcriptional response of the murine mammary gland to acute progesterone exposure. Endocrinology 2008, 149:6236-6250.
99. Schramek D, Leibbrandt A, Sigl V, Kenner L, Pospisilik JA, Lee HJ, Hanada R, Joshi PA, Aliprantis A, Glimcher L, et al. Osteoclast differentiation factor RANKL controls development of progestin-driven mammary cancer. Nature 2010, 468:98-102.
100. Gonzalez-Suarez E, Jacob AP, Jones J, Miller R, Roudier-Meyer MP, Erwert R, Pinkas J, Branstetter D, Dougall WC. RANK ligand mediates progestin-induced mammary epithelial proliferation and carcinogenesis. Nature 2010, 468:103-107.
101. Ormandy CJ, Camus A, Barra J, Damotte D, Lucas B, Buteau H, Edery M, Brousse N, Babinet C, Binart N, et al. Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev 1997, 11:167-178.
102. Horseman ND, Zhao W, Montecino-Rodriguez E, Tanaka M, Nakashima K, Engle SJ, Smith F, Markoff E, Dorshkind K. Defective mammopoiesis, but normal hematopoiesis, in mice with a targeted disruption of the prolactin gene. EMBO J 1997, 16:6926-6935.
103. Naylor MJ, Lockefeer JA, Horseman ND, Ormandy CJ. Prolactin regulates mammary epithelial cell proliferation via autocrine/paracrine mechanism. Endocrine 2003, 20:111-114.
104. Brisken C, Kaur S, Chavarria TE, Binart N, Sutherland RL, Weinberg RA, Kelly PA, Ormandy CJ. Prolactin controls mammary gland development via direct and indirect mechanisms. Dev Biol 1999, 210:96-106.
105. Vomachka AJ, Pratt SL, Lockefeer JA, Horseman ND. Prolactin gene-disruption arrests mammary gland development and retards T-antigen-induced tumor growth. Oncogene 2000, 19:1077-1084.
106. Han Y, Watling D, Rogers NC, Stark GR. JAK2 and STAT5, but not JAK1 and STAT1, are required for prolactin-induced β-lactoglobulin transcription. Mol Endocrinol 1997, 11:1180-1188.
107. Cui Y, Riedlinger G, Miyoshi K, Tang W, Li C, Deng CX, Robinson GW, Hennighausen L. Inactivation of Stat5 in mouse mammary epithelium during pregnancy reveals distinct functions in cell proliferation, survival, and differentiation. Mol Cell Biol 2004, 24:8037-8047.
108. Wagner KU, Krempler A, Triplett AA, Qi Y, George NM, Zhu J, Rui H. Impaired alveologenesis and maintenance of secretory mammary epithelial cells in Jak2 conditional knockout mice. Mol Cell Biol 2004, 24:5510-5520.
109. Naylor MJ, Li N, Cheung J, Lowe ET, Lambert E, Marlow R, Wang P, Schatzmann F, Wintermantel T, Schuetz G, et al. Ablation of β1 integrin in mammary epithelium reveals a key role for integrin in glandular morphogenesis and differentiation. J Cell Biol 2005, 171:717-728.
110. Galbaugh T, Feeney YB, Clevenger CV. Prolactin receptor-integrin cross-talk mediated by SIRPα in breast cancer cells. Mol Cancer Res 2010, 8:1413-1424.
111. Srivastava S, Matsuda M, Hou Z, Bailey JP, Kitazawa R, Herbst MP, Horseman ND. Receptor activator of NF-κB ligand induction via Jak2 and Stat5a in mammary epithelial cells. J Biol Chem 2003, 278:46171-46178.
112. Fernandez-Valdivia R, Mukherjee A, Ying Y, Li J, Paquet M, DeMayo FJ, Lydon JP. The RANKL signaling axis is sufficient to elicit ductal side-branching and alveologenesis in the mammary gland of the virgin mouse. Dev Biol 2009, 328:127-139.
113. Oakes SR, Rogers RL, Naylor MJ, Ormandy CJ. Prolactin regulation of mammary gland development. J Mammary Gland Biol Neoplasia 2008, 13:13-28.
114. D'Cruz CM, Moody SE, Master SR, Hartman JL, Keiper EA, Imielinski MB, Cox JD, Wang JY, Ha SI, Keister BA, et al. Persistent parity-induced changes in growth factors, TGF-β3, and differentiation in the rodent mammary gland. Mol Endocrinol 2002, 16:2034-2051.
115. Balogh GA, Heulings R, Mailo DA, Russo PA, Sheriff F, Russo IH, Moral R, Russo J. Genomic signature induced by pregnancy in the human breast. Int J Oncol 2006, 28:399-410.
116. Li M, Liu X, Robinson G, Bar-Peled U, Wagner KU, Young WS, Hennighausen L, Furth PA. Mammary-derived signals activate programmed cell death during the first stage of mammary gland involution. Proc Natl Acad Sci U S A 1997, 94:3425-3430.
117. Marti A, Feng Z, Altermatt HJ, Jaggi R. Milk accumulation triggers apoptosis of mammary epithelial cells. Eur J Cell Biol 1997, 73:158-165.
118. Marti A, Ritter PM, Jager R, Lazar H, Baltzer A, Schenkel J, Declercq W, Vandenabeele P, Jaggi R. Mouse mammary gland involution is associated with cytochrome c release and caspase activation. Mech Dev 2001, 104:89-98.
119. Song J, Sapi E, Brown W, Nilsen J, Tartaro K, Kacinski BM, Craft J, Naftolin F, Mor G. Roles of Fas and Fas ligand during mammary gland remodeling. J Clin Invest 2000, 106:1209-1220.
120. Baxter FO, Came PJ, Abell K, Kedjouar B, Huth M, Rajewsky K, Pasparakis M, Watson CJ. IKKβ/2 induces TWEAK and apoptosis in mammary epithelial cells. Development 2006, 133:3485-3494.
121. Kreuzaler PA, Staniszewska AD, Li W, Omidvar N, Kedjouar B, Turkson J, Poli V, Flavell RA, Clarkson RW, Watson CJ. Stat3 controls lysosomal-mediated cell death in vivo. Nat Cell Biol 2011.
122. Creamer BA, Sakamoto K, Schmidt JW, Triplett AA, Moriggl R, Wagner KU. Stat5 promotes survival of mammary epithelial cells through transcriptional activation of a distinct promoter in Akt1. Mol Cell Biol 2010, 30:2957-2970.
123. Schwertfeger KL, Richert MM, Anderson SM. Mammary gland involution is delayed by activated Akt in transgenic mice. Mol Endocrinol 2001, 15:867-881.
124. Maroulakou IG, Oemler W, Naber SP, Klebba I, Kuperwasser C, Tsichlis PN. Distinct roles of the three Akt isoforms in lactogenic differentiation and involution. J Cell Physiol 2008, 217:468-477.
125. Clarkson RW, Boland MP, Kritikou EA, Lee JM, Freeman TC, Tiffen PG, Watson CJ. The genes induced by signal transducer and activators of transcription (STAT)3 and STAT5 in mammary epithelial cells define the roles of these STATs in mammary development. Mol Endocrinol 2006, 20:675-685.
126. Chapman RS, Lourenco PC, Tonner E, Flint DJ, Selbert S, Takeda K, Akira S, Clarke AR, Watson CJ. Suppression of epithelial apoptosis and delayed mammary gland involution in mice with a conditional knockout of Stat3. Genes Dev 1999, 13:2604-2616.
127. Kritikou EA, Sharkey A, Abell K, Came PJ, Anderson E, Clarkson RW, Watson CJ. A dual, non-redundant, role for LIF as a regulator of development and STAT3-mediated cell death in mammary gland. Development 2003, 130:3459-3468.
128. Abell K, Bilancio A, Clarkson RW, Tiffen PG, Altaparmakov AI, Burdon TG, Asano T, Vanhaesebroeck B, Watson CJ. Stat3-induced apoptosis requires a molecular switch in PI(3)K subunit composition. Nat Cell Biol 2005, 7:392-398.
129. Tonner E, Barber MC, Travers MT, Logan A, Flint DJ. Hormonal control of insulin-like growth factor-binding protein-5 production in the involuting mammary gland of the rat. Endocrinology 1997, 138:5101-5107.
130. Ning Y, Hoang B, Schuller AG, Cominski TP, Hsu MS, Wood TL, Pintar JE. Delayed mammary gland involution in mice with mutation of the insulin-like growth factor binding protein 5 gene. Endocrinology 2007, 148:2138-2147.
131. Lund LR, Bjorn SF, Sternlicht MD, Nielsen BS, Solberg H, Usher PA, Osterby R, Christensen IJ, Stephens RW, Bugge TH, et al. Lactational competence and involution of the mouse mammary gland require plasminogen. Development 2000, 127:4481-4492.
132. Lilla JN, Joshi RV, Craik CS, Werb Z. Active plasma kallikrein localizes to mast cells and regulates epithelial cell apoptosis, adipocyte differentiation, and stromal remodeling during mammary gland involution. J Biol Chem 2009, 284:13792-13803.
133. Sympson CJ, Talhouk RS, Alexander CM, Chin JR, Clift SM, Bissell MJ, Werb Z. 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, 125:681-693.
134. Fata JE, Leco KJ, Voura EB, Yu HY, Waterhouse P, Murphy G, Moorehead RA, Khokha R. Accelerated apoptosis in the Timp-3-deficient mammary gland. J Clin Invest 2001, 108:831-841.
135. Witty JP, Wright JH, Matrisian LM. Matrix metalloproteinases are expressed during ductal and alveolar mammary morphogenesis, and misregulation of stromelysin-1 in transgenic mice induces unscheduled alveolar development. Mol Biol Cell 1995, 6:1287-1303.
136. Wiseman BS, Sternlicht MD, Lund LR, Alexander CM, Mott J, Bissell MJ, Soloway P, Itohara S, Werb Z. Site-specific inductive and inhibitory activities of MMP-2 and MMP-3 orchestrate mammary gland branching morphogenesis. J Cell Biol 2003, 162:1123-1133.
137. Clarkson RW, Watson CJ. Microarray analysis of the involution switch. J Mammary Gland Biol Neoplasia 2003, 8:309-319.
138. Schedin P. Pregnancy-associated breast cancer and metastasis. Nat Rev Cancer 2006, 6:281-291.
139. Bemis LT, Schedin P. Reproductive state of rat mammary gland stroma modulates human breast cancer cell migration and invasion. Cancer Res 2000, 60:3414-3418.
140. McDaniel SM, Rumer KK, Biroc SL, Metz RP, Singh M, Porter W, Schedin P. Remodeling of the mammary microenvironment after lactation promotes breast tumor cell metastasis. Am J Pathol 2006, 168:608-620.
141. Ghosh K, Hartmann LC, Reynolds C, Visscher DW, Brandt KR, Vierkant RA, Scott CG, Radisky DC, Sellers TA, Pankratz VS, et al. Association between mammographic density and age-related lobular involution of the breast. J Clin Oncol 2010, 28:2207-2212.
142. Milanese TR, Hartmann LC, Sellers TA, Frost MH, Vierkant RA, Maloney SD, Pankratz VS, Degnim AC, Vachon CM, Reynolds CA, et al. Age-related lobular involution and risk of breast cancer. J Natl Cancer Inst 2006, 98:1600-1607.
143. Daniel CW, De Ome KB, Young JT, Blair PB, Faulkin LJ Jr. The in vivo life span of normal and preneoplastic mouse mammary glands: a serial transplantation study. Proc Natl Acad Sci U S A 1968, 61:53-60.
144. Daniel CW, Young LJ, Medina D, DeOme KB. The influence of mammogenic hormones on serially transplanted mouse mammary gland. Exp Gerontol 1971, 6:95-101.
145. Young LJ, Medina D, DeOme KB, Daniel CW. The influence of host and tissue age on life span and growth rate of serially transplanted mouse mammary gland. Exp Gerontol 1971, 6:49-56.
146. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, Wu L, Lindeman GJ, Visvader JE. Generation of a functional mammary gland from a single stem cell. Nature 2006, 439:84-88.
147. Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, Li HI, Eaves CJ. Purification and unique properties of mammary epithelial stem cells. Nature 2006, 439:993-997.
148. Stingl J, Eaves CJ, Zandieh I, Emerman JT. Characterization of bipotent mammary epithelial progenitor cells in normal adult human breast tissue. Breast Cancer Res Treat 2001, 67:93-109.
149. Clarke RB. Isolation and characterization of human mammary stem cells. Cell Prolif 2005, 38:375-386.
150. Chepko G, Smith GH. Three division-competent, structurally-distinct cell populations contribute to murine mammary epithelial renewal. Tissue Cell 1997, 29:239-253.
151. Kordon EC, Smith GH. An entire functional mammary gland may comprise the progeny from a single cell. Development 1998, 125:1921-1930.
152. Moraes RC, Zhang X, Harrington N, Fung JY, Wu MF, Hilsenbeck SG, Allred DC, Lewis MT. Constitutive activation of smoothened (SMO) in mammary glands of transgenic mice leads to increased proliferation, altered differentiation and ductal dysplasia. Development 2007, 134:1231-1242.
153. Asselin-Labat ML, Sutherland KD, Barker H, Thomas R, Shackleton M, Forrest NC, Hartley L, Robb L, Grosveld FG, van der Wees J, et al. Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation. Nat Cell Biol 2007, 9:201-209.
154. Booth BW, Boulanger CA, Smith GH. Alveolar progenitor cells develop in mouse mammary glands independent of pregnancy and lactation. J Cell Physiol 2007, 212:729-736.
155. Knoblich JA. Asymmetric cell division: recent developments and their implications for tumour biology. Nat Rev Mol Cell Biol 2010, 11:849-860.
156. Smith GH, Medina D. A morphologically distinct candidate for an epithelial stem cell in mouse mammary gland. J Cell Sci 1988, 90(Pt 1):173-183.
157. Daniel CW, Young LJ. Influence of cell division on an aging process. Life span of mouse mammary epithelium during serial propagation in vivo. Exp Cell Res 1971, 65:27-32.
158. Fernandez-Gonzalez R, Illa-Bochaca I, Welm BE, Fleisch MC, Werb Z, Ortiz-de-Solorzano C, Barcellos-Hoff MH. Mapping mammary gland architecture using multi-scale in situ analysis. Integr Biol (Camb) 2009, 1:80-89.
159. Farnie G, Clarke RB. Mammary stem cells and breast cancer-role of Notch signalling. Stem Cell Rev 2007, 3:169-175.
160. Visbal AP, Lewis MT. Hedgehog signaling in the normal and neoplastic mammary gland. Curr Drug Targets 2010, 11:1103-1111.
161. Wend P, Holland JD, Ziebold U, Birchmeier W. Wnt signaling in stem and cancer stem cells. Semin Cell Dev Biol 2010, 21:855-863.
162. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR. Ross DT, Johnsen H, Akslen LA, et al. Molecular portraits of human breast tumours. Nature 2000, 406:747-752.
163. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003, 100:3983-3988.
164. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997, 3:730-737.
165. Visvader JE. Cells of origin in cancer. Nature 2011, 469:314-322.
166. Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH, Asselin-Labat ML, Gyorki DE, Ward T, Partanen A, et al. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med 2009, 15:907-913.
167. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, Hilsenbeck SG, Pavlick A, Zhang X, Chamness GC, et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 2008, 100:672-679.