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Published in: Journal of Mammary Gland Biology and Neoplasia 2/2013

01-06-2013

Wnt-Signalling in the Embryonic Mammary Gland

Authors: Kata Boras-Granic, Paul A. Hamel

Published in: Journal of Mammary Gland Biology and Neoplasia | Issue 2/2013

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Abstract

The first member of the Wnt-family ligands was identified 30 years ago as a factor in mouse mammary tumours whose expression was deregulated due to the promoter activity emanating from the proximal integration of the Mouse Mammary Tumour Virus genome (Nusse and Varmus, Embo J 31:2670–84, 2012). The Wnt-ligands invoke a number of molecular-genetic signalling cascades fundamental to the patterning of developing tissues and organs during embryogenesis as well as during postnatal development. The Wnt-signalling cascade that controls the activities of β-catenin and the T-cell Factor (Tcf)/Lympoid enhancer factor (Lef1) plays a fundamental role in control of all stages of embryonic mammary gland development. We provide here a brief overview of the known aspects of Wnt-signalling activities in the embryonic mammary gland and its interactions with other signalling cascades in this developing tissue.
Literature
1.
go back to reference Nusse R, Varmus H. Three decades of Wnts: a personal perspective on how a scientific field developed. EMBO J. 2012;31:2670–84.CrossRefPubMed Nusse R, Varmus H. Three decades of Wnts: a personal perspective on how a scientific field developed. EMBO J. 2012;31:2670–84.CrossRefPubMed
3.
go back to reference James RG, Conrad WH, Moon RT. Beta-catenin-independent Wnt pathways: signals, core proteins, and effectors. Methods Mol Biol. 2008;468:131–44.CrossRefPubMed James RG, Conrad WH, Moon RT. Beta-catenin-independent Wnt pathways: signals, core proteins, and effectors. Methods Mol Biol. 2008;468:131–44.CrossRefPubMed
4.
go back to reference Wansleeben C, Meijlink F. The planar cell polarity pathway in vertebrate development. Dev Dyn. 2011;240:616–26.CrossRefPubMed Wansleeben C, Meijlink F. The planar cell polarity pathway in vertebrate development. Dev Dyn. 2011;240:616–26.CrossRefPubMed
5.
6.
go back to reference Lapébie P, Borchiellini C, Houliston E. Dissecting the PCP pathway: one or more pathways?: does a separate Wnt-Fz-Rho pathway drive morphogenesis? Bioessays. 2011;33:759–68.CrossRefPubMed Lapébie P, Borchiellini C, Houliston E. Dissecting the PCP pathway: one or more pathways?: does a separate Wnt-Fz-Rho pathway drive morphogenesis? Bioessays. 2011;33:759–68.CrossRefPubMed
7.
go back to reference Chu EY, Hens J, Andl T, Kairo A, Yamaguchi TP, Brisken C, et al. Canonical WNT signaling promotes mammary placode development and is essential for initiation of mammary gland morphogenesis. Development. 2004;131:4819–29.CrossRefPubMed Chu EY, Hens J, Andl T, Kairo A, Yamaguchi TP, Brisken C, et al. Canonical WNT signaling promotes mammary placode development and is essential for initiation of mammary gland morphogenesis. Development. 2004;131:4819–29.CrossRefPubMed
8.
go back to reference van Amerongen R. Alternative Wnt pathways and receptors. Cold Spring Harb Perspect Biol. 2012;4. van Amerongen R. Alternative Wnt pathways and receptors. Cold Spring Harb Perspect Biol. 2012;4.
9.
go back to reference van Amerongen R, Fuerer C, Mizutani M, Nusse R. Wnt5a can both activate and repress Wnt/β-catenin signaling during mouse embryonic development. Dev Biol. 2012;369:101–14.CrossRefPubMed van Amerongen R, Fuerer C, Mizutani M, Nusse R. Wnt5a can both activate and repress Wnt/β-catenin signaling during mouse embryonic development. Dev Biol. 2012;369:101–14.CrossRefPubMed
10.
go back to reference Veltmaat JM, Van Veelen W, Thiery JP, Bellusci S. Identification of the mammary line in mouse by Wnt10b expression. Dev Dyn. 2004;229:349–56.CrossRefPubMed Veltmaat JM, Van Veelen W, Thiery JP, Bellusci S. Identification of the mammary line in mouse by Wnt10b expression. Dev Dyn. 2004;229:349–56.CrossRefPubMed
11.
go back to reference Kikuchi A, Yamamoto H, Sato A, Matsumoto S. Wnt5a: its signalling, functions and implication in diseases. Acta Physiol (Oxf). 2012;204:17–33. Kikuchi A, Yamamoto H, Sato A, Matsumoto S. Wnt5a: its signalling, functions and implication in diseases. Acta Physiol (Oxf). 2012;204:17–33.
12.
go back to reference Uysal-Onganer P, Kypta RM. Wnt11 in 2011—the regulation and function of a non-canonical Wnt. Acta Physiol (Oxf). 2012;204:52–64. Uysal-Onganer P, Kypta RM. Wnt11 in 2011—the regulation and function of a non-canonical Wnt. Acta Physiol (Oxf). 2012;204:52–64.
13.
go back to reference Christiansen JH, Dennis CL, Wicking CA, Monkley SJ, Wilkinson DG, Wainwright BJ. Murine Wnt-11 and Wnt-12 have temporally and spatially restricted expression patterns during embryonic development. Mech Dev. 1995;51:341–50. Christiansen JH, Dennis CL, Wicking CA, Monkley SJ, Wilkinson DG, Wainwright BJ. Murine Wnt-11 and Wnt-12 have temporally and spatially restricted expression patterns during embryonic development. Mech Dev. 1995;51:341–50.
14.
go back to reference Dunbar ME, Wysolmerski JJ. Parathyroid hormone-related protein: a developmental regulatory molecule necessary for mammary gland development. J Mammary Gland Biol Neoplasia. 1999;4:21–34.CrossRefPubMed Dunbar ME, Wysolmerski JJ. Parathyroid hormone-related protein: a developmental regulatory molecule necessary for mammary gland development. J Mammary Gland Biol Neoplasia. 1999;4:21–34.CrossRefPubMed
15.
go back to reference Boras-Granic K, Chang H, Grosschedl R, Hamel PA. Lef1 is required for the transition of Wnt signaling from mesenchymal to epithelial cells in the mouse embryonic mammary gland. Dev Biol. 2006;295:219–31.CrossRefPubMed Boras-Granic K, Chang H, Grosschedl R, Hamel PA. Lef1 is required for the transition of Wnt signaling from mesenchymal to epithelial cells in the mouse embryonic mammary gland. Dev Biol. 2006;295:219–31.CrossRefPubMed
16.
go back to reference van Genderen C, Okamura RM, Fariñas 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.CrossRefPubMed van Genderen C, Okamura RM, Fariñas 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.CrossRefPubMed
17.
go back to reference 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 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
18.
go back to reference Foley J, Dann P, Hong J, Cosgrove J, Dreyer B, Rimm D, et al. Parathyroid hormone-related protein maintains mammary epithelial fate and triggers nipple skin differentiation during embryonic breast development. Development. 2001;128:513–25.PubMed Foley J, Dann P, Hong J, Cosgrove J, Dreyer B, Rimm D, et al. Parathyroid hormone-related protein maintains mammary epithelial fate and triggers nipple skin differentiation during embryonic breast development. Development. 2001;128:513–25.PubMed
19.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
20.
go back to reference Wansbury O, Mackay A, Kogata N, Mitsopoulos C, Kendrick H, Davidson K, et al. Transcriptome analysis of embryonic mammary cells reveals insights into mammary lineage establishment. Breast Cancer Res. 2011;13:R79.CrossRefPubMed Wansbury O, Mackay A, Kogata N, Mitsopoulos C, Kendrick H, Davidson K, et al. Transcriptome analysis of embryonic mammary cells reveals insights into mammary lineage establishment. Breast Cancer Res. 2011;13:R79.CrossRefPubMed
21.
go back to reference Jesse S, Koenig A, Ellenrieder V, Menke A. Lef-1 isoforms regulate different target genes and reduce cellular adhesion. Int J Cancer. 2010;126:1109–20.PubMed Jesse S, Koenig A, Ellenrieder V, Menke A. Lef-1 isoforms regulate different target genes and reduce cellular adhesion. Int J Cancer. 2010;126:1109–20.PubMed
22.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
23.
go back to reference Lindvall C, Zylstra CR, Evans N, West RA, Dykema K, Furge KA, et al. The Wnt co-receptor Lrp6 is required for normal mouse mammary gland development. PLoS One. 2009;4:e5813.CrossRefPubMed Lindvall C, Zylstra CR, Evans N, West RA, Dykema K, Furge KA, et al. The Wnt co-receptor Lrp6 is required for normal mouse mammary gland development. PLoS One. 2009;4:e5813.CrossRefPubMed
24.
25.
go back to reference Al Alam D, Green M, Tabatabai Irani R, Parsa S, Danopoulos S, Sala FG, et al. Contrasting expression of canonical Wnt signaling reporters TOPGAL, BATGAL and Axin2(LacZ) during murine lung development and repair. PLoS One. 2011;6:e23139.CrossRefPubMed Al Alam D, Green M, Tabatabai Irani R, Parsa S, Danopoulos S, Sala FG, et al. Contrasting expression of canonical Wnt signaling reporters TOPGAL, BATGAL and Axin2(LacZ) during murine lung development and repair. PLoS One. 2011;6:e23139.CrossRefPubMed
26.
go back to reference DasGupta R, Fuchs E. Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development. 1999;126:4557–68.PubMed DasGupta R, Fuchs E. Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development. 1999;126:4557–68.PubMed
27.
go back to reference Cheon SS, Cheah AYL, Turley S, Nadesan P, Poon R, Clevers H, et al. beta-Catenin stabilization dysregulates mesenchymal cell proliferation, motility, and invasiveness and causes aggressive fibromatosis and hyperplastic cutaneous wounds. Proc Natl Acad Sci U S A. 2002;99:6973–8.CrossRefPubMed Cheon SS, Cheah AYL, Turley S, Nadesan P, Poon R, Clevers H, et al. beta-Catenin stabilization dysregulates mesenchymal cell proliferation, motility, and invasiveness and causes aggressive fibromatosis and hyperplastic cutaneous wounds. Proc Natl Acad Sci U S A. 2002;99:6973–8.CrossRefPubMed
28.
go back to reference Ferrer-Vaquer A, Piliszek A, Tian G, Aho RJ, Dufort D, Hadjantonakis A-K. A sensitive and bright single-cell resolution live imaging reporter of Wnt/ß-catenin signaling in the mouse. BMC Dev Biol. 2010;10:121.CrossRefPubMed Ferrer-Vaquer A, Piliszek A, Tian G, Aho RJ, Dufort D, Hadjantonakis A-K. A sensitive and bright single-cell resolution live imaging reporter of Wnt/ß-catenin signaling in the mouse. BMC Dev Biol. 2010;10:121.CrossRefPubMed
29.
go back to reference Currier N, Chea K, Hlavacova M, Sussman DJ, Seldin DC, Dominguez I. Dynamic expression of a LEF-EGFP Wnt reporter in mouse development and cancer. Genesis. 2010;48:183–94.PubMed Currier N, Chea K, Hlavacova M, Sussman DJ, Seldin DC, Dominguez I. Dynamic expression of a LEF-EGFP Wnt reporter in mouse development and cancer. Genesis. 2010;48:183–94.PubMed
30.
go back to reference Jho E, Zhang T, Domon C, Joo C-K, Freund J-N, Costantini F. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol. 2002;22:1172–83.CrossRefPubMed Jho E, Zhang T, Domon C, Joo C-K, Freund J-N, Costantini F. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol. 2002;22:1172–83.CrossRefPubMed
31.
go back to reference Moriyama A, Kii I, Sunabori T, Kurihara S, Takayama I, Shimazaki M, et al. GFP transgenic mice reveal active canonical Wnt signal in neonatal brain and in adult liver and spleen. Genesis. 2007;45:90–100.CrossRefPubMed Moriyama A, Kii I, Sunabori T, Kurihara S, Takayama I, Shimazaki M, et al. GFP transgenic mice reveal active canonical Wnt signal in neonatal brain and in adult liver and spleen. Genesis. 2007;45:90–100.CrossRefPubMed
32.
go back to reference Maretto S, Cordenonsi M, Dupont S, Braghetta P, Broccoli V, Hassan AB, et al. Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci U S A. 2003;100:3299–304.CrossRefPubMed Maretto S, Cordenonsi M, Dupont S, Braghetta P, Broccoli V, Hassan AB, et al. Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci U S A. 2003;100:3299–304.CrossRefPubMed
33.
go back to reference Nakaya M, Biris K, Tsukiyama T, Jaime S, Rawls JA, Yamaguchi TP. Wnt3a links left-right determination with segmentation and anteroposterior axis elongation. Development. 2005;132:5425–36.CrossRefPubMed Nakaya M, Biris K, Tsukiyama T, Jaime S, Rawls JA, Yamaguchi TP. Wnt3a links left-right determination with segmentation and anteroposterior axis elongation. Development. 2005;132:5425–36.CrossRefPubMed
34.
go back to reference Mohamed OA, Clarke HJ, Dufort D. Beta-catenin signaling marks the prospective site of primitive streak formation in the mouse embryo. Dev Dyn. 2004;231:416–24.CrossRefPubMed Mohamed OA, Clarke HJ, Dufort D. Beta-catenin signaling marks the prospective site of primitive streak formation in the mouse embryo. Dev Dyn. 2004;231:416–24.CrossRefPubMed
35.
go back to reference Lustig B, Jerchow B, Sachs M, Weiler S, Pietsch T, Karsten U, et al. Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol Cell Biol. 2002;22:1184–93.CrossRefPubMed Lustig B, Jerchow B, Sachs M, Weiler S, Pietsch T, Karsten U, et al. Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol Cell Biol. 2002;22:1184–93.CrossRefPubMed
36.
go back to reference Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 2007;449:1003–7.CrossRefPubMed Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 2007;449:1003–7.CrossRefPubMed
37.
go back to reference Lindvall C, Evans NC, Zylstra CR, Li Y, Alexander CM, Williams BO. The Wnt signaling receptor Lrp5 is required for mammary ductal stem cell activity and Wnt1-induced tumorigenesis. J Biol Chem. 2006;281:35081–7.CrossRefPubMed Lindvall C, Evans NC, Zylstra CR, Li Y, Alexander CM, Williams BO. The Wnt signaling receptor Lrp5 is required for mammary ductal stem cell activity and Wnt1-induced tumorigenesis. J Biol Chem. 2006;281:35081–7.CrossRefPubMed
38.
go back to reference Ahn Y, Sims C, Logue JM, Weatherbee SD, Krumlauf R. Lrp4 and Wise interplay controls the formation and patterning of mammary and other skin appendage placodes by modulating Wnt signaling. Development. 2013;140:583–93.CrossRefPubMed Ahn Y, Sims C, Logue JM, Weatherbee SD, Krumlauf R. Lrp4 and Wise interplay controls the formation and patterning of mammary and other skin appendage placodes by modulating Wnt signaling. Development. 2013;140:583–93.CrossRefPubMed
39.
go back to reference Gu B, Sun P, Yuan Y, Moraes RC, Li A, Teng A, et al. Pygo2 expands mammary progenitor cells by facilitating histone H3 K4 methylation. J Cell Biol. 2009;185:811–26.CrossRefPubMed Gu B, Sun P, Yuan Y, Moraes RC, Li A, Teng A, et al. Pygo2 expands mammary progenitor cells by facilitating histone H3 K4 methylation. J Cell Biol. 2009;185:811–26.CrossRefPubMed
40.
go back to reference Voutilainen M, Lindfors PH, Lefebvre S, Ahtiainen L, Fliniaux I, Rysti E, et al. Ectodysplasin regulates hormone-independent mammary ductal morphogenesis via NF-κB. Proc Natl Acad Sci U S A. 2012;109:5744–9.CrossRefPubMed Voutilainen M, Lindfors PH, Lefebvre S, Ahtiainen L, Fliniaux I, Rysti E, et al. Ectodysplasin regulates hormone-independent mammary ductal morphogenesis via NF-κB. Proc Natl Acad Sci U S A. 2012;109:5744–9.CrossRefPubMed
41.
go back to reference Yu H-MI, Jerchow B, Sheu T-J, Liu B, Costantini F, Puzas JE, et al. The role of Axin2 in calvarial morphogenesis and craniosynostosis. Development. 2005;132:1995–2005.CrossRefPubMed Yu H-MI, Jerchow B, Sheu T-J, Liu B, Costantini F, Puzas JE, et al. The role of Axin2 in calvarial morphogenesis and craniosynostosis. Development. 2005;132:1995–2005.CrossRefPubMed
42.
go back to reference van Amerongen R, Bowman AN, Nusse R. Developmental stage and time dictate the fate of Wnt/β-catenin-responsive stem cells in the mammary gland. Cell Stem Cell. 2012;11:387–400.CrossRefPubMed van Amerongen R, Bowman AN, Nusse R. Developmental stage and time dictate the fate of Wnt/β-catenin-responsive stem cells in the mammary gland. Cell Stem Cell. 2012;11:387–400.CrossRefPubMed
43.
go back to reference Zeng YA, Nusse R. Wnt proteins are self-renewal factors for mammary stem cells and promote their long-term expansion in culture. Cell Stem Cell. 2010;6:568–77.CrossRefPubMed Zeng YA, Nusse R. Wnt proteins are self-renewal factors for mammary stem cells and promote their long-term expansion in culture. Cell Stem Cell. 2010;6:568–77.CrossRefPubMed
44.
go back to reference Stevens JR, Miranda-Carboni GA, Singer MA, Brugger SM, Lyons KM, Lane TF. Wnt10b deficiency results in age-dependent loss of bone mass and progressive reduction of mesenchymal progenitor cells. J Bone Miner Res. 2010;25:2138–47.CrossRefPubMed Stevens JR, Miranda-Carboni GA, Singer MA, Brugger SM, Lyons KM, Lane TF. Wnt10b deficiency results in age-dependent loss of bone mass and progressive reduction of mesenchymal progenitor cells. J Bone Miner Res. 2010;25:2138–47.CrossRefPubMed
45.
go back to reference Roose J, Huls G, van Beest M, Moerer P, van der Horn K, Goldschmeding R, et al. Synergy between tumor suppressor APC and the beta-catenin-Tcf4 target Tcf1. Science. 1999;285:1923–6.CrossRefPubMed Roose J, Huls G, van Beest M, Moerer P, van der Horn K, Goldschmeding R, et al. Synergy between tumor suppressor APC and the beta-catenin-Tcf4 target Tcf1. Science. 1999;285:1923–6.CrossRefPubMed
46.
go back to reference Sakakura T, Nishizuka Y, Dawe CJ. Mesenchyme-dependent morphogenesis and epithelium-specific cytodifferentiation in mouse mammary gland. Science. 1976;194:1439–41.CrossRefPubMed Sakakura T, Nishizuka Y, Dawe CJ. Mesenchyme-dependent morphogenesis and epithelium-specific cytodifferentiation in mouse mammary gland. Science. 1976;194:1439–41.CrossRefPubMed
47.
go back to reference Sakakura T, Sakagami Y, Nishizuka Y. Persistence of responsiveness of adult mouse mammary gland to induction by embryonic mesenchyme. Dev Biol. 1979;72:201–10.CrossRefPubMed Sakakura T, Sakagami Y, Nishizuka Y. Persistence of responsiveness of adult mouse mammary gland to induction by embryonic mesenchyme. Dev Biol. 1979;72:201–10.CrossRefPubMed
48.
go back to reference Hiremath M, Dann P, Fischer J, Butterworth D, Boras-Granic K, Hens J, et al. Parathyroid hormone-related protein activates Wnt signaling to specify the embryonic mammary mesenchyme. Development. 2012;139:4239–49.CrossRefPubMed Hiremath M, Dann P, Fischer J, Butterworth D, Boras-Granic K, Hens J, et al. Parathyroid hormone-related protein activates Wnt signaling to specify the embryonic mammary mesenchyme. Development. 2012;139:4239–49.CrossRefPubMed
49.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
50.
go back to reference Oyama K, Mohri Y, Sone M, Nawa A, Nishimori K. Conditional knockout of Lgr4 leads to impaired ductal elongation and branching morphogenesis in mouse mammary glands. Sex Dev. 2011;5:205–12.CrossRefPubMed Oyama K, Mohri Y, Sone M, Nawa A, Nishimori K. Conditional knockout of Lgr4 leads to impaired ductal elongation and branching morphogenesis in mouse mammary glands. Sex Dev. 2011;5:205–12.CrossRefPubMed
51.
go back to reference Tsukamoto AS, Grosschedl R, Guzman RC, Parslow T, Varmus HE. Expression of the int-1 gene in transgenic mice is associated with mammary gland hyperplasia and adenocarcinomas in male and female mice. Cell. 1988;55:619–25.CrossRefPubMed Tsukamoto AS, Grosschedl R, Guzman RC, Parslow T, Varmus HE. Expression of the int-1 gene in transgenic mice is associated with mammary gland hyperplasia and adenocarcinomas in male and female mice. Cell. 1988;55:619–25.CrossRefPubMed
52.
go back to reference Nusse R, Varmus HE. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell. 1982;31:99–109.CrossRefPubMed Nusse R, Varmus HE. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell. 1982;31:99–109.CrossRefPubMed
53.
go back to reference Kwan H, Pecenka V, Tsukamoto A, Parslow TG, Guzman R, Lin TP, et al. Transgenes expressing the Wnt-1 and int-2 proto-oncogenes cooperate during mammary carcinogenesis in doubly transgenic mice. Mol Cell Biol. 1992;12:147–54.PubMed Kwan H, Pecenka V, Tsukamoto A, Parslow TG, Guzman R, Lin TP, et al. Transgenes expressing the Wnt-1 and int-2 proto-oncogenes cooperate during mammary carcinogenesis in doubly transgenic mice. Mol Cell Biol. 1992;12:147–54.PubMed
54.
go back to reference Nusse R, Theunissen H, Wagenaar E, Rijsewijk F, Gennissen A, Otte A, et al. The Wnt-1 (int-1) oncogene promoter and its mechanism of activation by insertion of proviral DNA of the mouse mammary tumor virus. Mol Cell Biol. 1990;10:4170–9.PubMed Nusse R, Theunissen H, Wagenaar E, Rijsewijk F, Gennissen A, Otte A, et al. The Wnt-1 (int-1) oncogene promoter and its mechanism of activation by insertion of proviral DNA of the mouse mammary tumor virus. Mol Cell Biol. 1990;10:4170–9.PubMed
55.
go back to reference Ougolkov AV, Billadeau DD. Inhibition of glycogen synthase kinase-3. Methods Mol Biol. 2008;468:67–75.CrossRefPubMed Ougolkov AV, Billadeau DD. Inhibition of glycogen synthase kinase-3. Methods Mol Biol. 2008;468:67–75.CrossRefPubMed
56.
go back to reference Takebe N, Harris PJ, Warren RQ, Ivy SP. Targeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathways. Nat Rev Clin Oncol. 2011;8:97–106.CrossRefPubMed Takebe N, Harris PJ, Warren RQ, Ivy SP. Targeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathways. Nat Rev Clin Oncol. 2011;8:97–106.CrossRefPubMed
57.
go back to reference Närhi K, Tummers M, Ahtiainen L, Itoh N, Thesleff I, Mikkola ML. Sostdc1 defines the size and number of skin appendage placodes. Dev Biol. 2012;364:149–61.CrossRefPubMed Närhi K, Tummers M, Ahtiainen L, Itoh N, Thesleff I, Mikkola ML. Sostdc1 defines the size and number of skin appendage placodes. Dev Biol. 2012;364:149–61.CrossRefPubMed
58.
go back to reference Lee MY, Racine V, Jagadpramana P, Sun L, Yu W, Du T, et al. Ectodermal influx and cell hypertrophy provide early growth for all murine mammary rudiments, and are differentially regulated among them by Gli3. PLoS One. 2011;6:e26242.CrossRefPubMed Lee MY, Racine V, Jagadpramana P, Sun L, Yu W, Du T, et al. Ectodermal influx and cell hypertrophy provide early growth for all murine mammary rudiments, and are differentially regulated among them by Gli3. PLoS One. 2011;6:e26242.CrossRefPubMed
59.
go back to reference Veltmaat JM, Relaix F, Le LT, Kratochwil K, Sala FG, van Veelen W, et al. Gli3-mediated somitic Fgf10 expression gradients are required for the induction and patterning of mammary epithelium along the embryonic axes. Development. 2006;133:2325–35.CrossRefPubMed Veltmaat JM, Relaix F, Le LT, Kratochwil K, Sala FG, van Veelen W, et al. Gli3-mediated somitic Fgf10 expression gradients are required for the induction and patterning of mammary epithelium along the embryonic axes. Development. 2006;133:2325–35.CrossRefPubMed
60.
go back to reference Eblaghie MC, Song S-J, Kim J-Y, Akita K, Tickle C, Jung H-S. Interactions between FGF and Wnt signals and Tbx3 gene expression in mammary gland initiation in mouse embryos. J Anat. 2004;205:1–13.CrossRefPubMed Eblaghie MC, Song S-J, Kim J-Y, Akita K, Tickle C, Jung H-S. Interactions between FGF and Wnt signals and Tbx3 gene expression in mammary gland initiation in mouse embryos. J Anat. 2004;205:1–13.CrossRefPubMed
61.
go back to reference Mustonen T, Ilmonen M, Pummila M, Kangas AT, Laurikkala J, Jaatinen R, et al. Ectodysplasin A1 promotes placodal cell fate during early morphogenesis of ectodermal appendages. Development. 2004;131:4907–19.CrossRefPubMed Mustonen T, Ilmonen M, Pummila M, Kangas AT, Laurikkala J, Jaatinen R, et al. Ectodysplasin A1 promotes placodal cell fate during early morphogenesis of ectodermal appendages. Development. 2004;131:4907–19.CrossRefPubMed
62.
go back to reference 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 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
63.
go back to reference Ruffner H, Sprunger J, Charlat O, Leighton-Davies J, Grosshans B, Salathe A, et al. R-Spondin potentiates Wnt/β-catenin signaling through orphan receptors LGR4 and LGR5. PLoS One. 2012;7:e40976.CrossRefPubMed Ruffner H, Sprunger J, Charlat O, Leighton-Davies J, Grosshans B, Salathe A, et al. R-Spondin potentiates Wnt/β-catenin signaling through orphan receptors LGR4 and LGR5. PLoS One. 2012;7:e40976.CrossRefPubMed
64.
go back to reference Carmon KS, Gong X, Lin Q, Thomas A, Liu Q. R-spondins function as ligands of the orphan receptors LGR4 and LGR5 to regulate Wnt/beta-catenin signaling. Proc Natl Acad Sci U S A. 2011;108:11452–7.CrossRefPubMed Carmon KS, Gong X, Lin Q, Thomas A, Liu Q. R-spondins function as ligands of the orphan receptors LGR4 and LGR5 to regulate Wnt/beta-catenin signaling. Proc Natl Acad Sci U S A. 2011;108:11452–7.CrossRefPubMed
Metadata
Title
Wnt-Signalling in the Embryonic Mammary Gland
Authors
Kata Boras-Granic
Paul A. Hamel
Publication date
01-06-2013
Publisher
Springer US
Published in
Journal of Mammary Gland Biology and Neoplasia / Issue 2/2013
Print ISSN: 1083-3021
Electronic ISSN: 1573-7039
DOI
https://doi.org/10.1007/s10911-013-9280-x

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