Top

Journal of Mammary Gland Biology and Neoplasia

Published in:

01-10-2006

Comparative Mechanisms of Branching Morphogenesis in Diverse Systems

Authors: Pengfei Lu, Mark D. Sternlicht, Zena Werb

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

Abstract

Much progress has been made in recent years toward understanding mechanisms controlling branching morphogenesis, a fundamental aspect of development in a variety of invertebrate and vertebrate organs. To gain a deeper understanding of how branching morphogenesis occurs in the mammary gland, we compare and contrast the cellular and molecular events underlying this process in both invertebrate and vertebrate organs. Thus, in this review, we focus on the common themes that have emerged from such comparative analyses and discuss how they are implemented via a battery of signaling pathways to ensure proper branching morphogenesis in diverse systems.

Affolter M, Bellusci S, Itoh N, Shilo B, Thiery JP, Werb Z. Tube or not tube: remodeling epithelial tissues by branching morphogenesis. Dev Cell 2003;4(1):11–8.PubMed

Shah MM, Sampogna RV, Sakurai H, Bush KT, Nigam SK. Branching morphogenesis and kidney disease. Development 2004;131(7):1449–62.PubMed

Wiseman BS, Werb Z. Stromal effects on mammary gland development and breast cancer. Science 2002;296(5570):1046–9.PubMed

Ghabrial A, Luschnig S, Metzstein MM, Krasnow MA. Branching morphogenesis of the Drosophila tracheal system. Annu Rev Cell Dev Biol 2003;19:623–47.PubMed

Metzger RJ, Krasnow MA. Genetic control of branching morphogenesis. Science 1999;284(5420):1635–9.PubMed

Cabernard C, Neumann M, Affolter M. Cellular and molecular mechanisms involved in branching morphogenesis of the Drosophila tracheal system. J Appl Physiol 2004;97(6):2347–53.PubMed

Cardoso WV, Lu J. Regulation of early lung morphogenesis: questions, facts and controversies 10.1242/dev.02310. Development 2006;133(9):1611–24.PubMed

Wang J, Laurie GW. Organogenesis of the exocrine gland. Dev Biol 2004;273(1):1–22.PubMed

Robinson GW. Identification of signaling pathways in early mammary gland development by mouse genetics. Breast Cancer Res 2004;6(3):105–8.PubMed

10.

Hennighausen L, Robinson GW. Signaling pathways in mammary gland development. Dev Cell 2001;1(4):467–75.PubMed

11.

Hennighausen L, Robinson GW. Think globally, act locally: the making of a mouse mammary gland. Genes Dev 1998;12(4):449–55.PubMed

12.

Hogan BL, Kolodziej PA. Organogenesis: molecular mechanisms of tubulogenesis. Nat Rev Genet 2002;3(7):513–23.PubMed

13.

Lubarsky B, Krasnow MA. Tube morphogenesis: making and shaping biological tubes. Cell 2003;112(1):19–28.PubMed

14.

Nelson WJ. Tube morphogenesis: closure, but many openings remain. Trends Cell Biol 2003;13(12):615–21.PubMed

15.

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):1–17.PubMed

16.

Robinson GW, Karpf AB, Kratochwil K. Regulation of mammary gland development by tissue interaction. J Mammary Gland Biol Neoplasia 1999;4(1):9–19.PubMed

17.

Hens JR, Wysolmerski JJ. Key stages of mammary gland development: molecular mechanisms involved in the formation of the embryonic mammary gland. Breast Cancer Res 2005;7(5):220–4.PubMed

18.

Hennighausen L, Robinson GW. Information networks in the mammary gland. Nat Rev Mol Cell Biol 2005;6(9):715–25.PubMed

19.

Sternlicht MD. Key stages in mammary gland development: the cues that regulate ductal branching morphogenesis. Breast Cancer Res 2006;8(1):201.PubMed

20.

Brisken C. Hormonal control of alveolar development and its implications for breast carcinogenesis. J Mammary Gland Biol Neoplasia 2002;7(1):39–48.PubMed

21.

Chuang PT, McMahon AP. Branching morphogenesis of the lung: new molecular insights into an old problem. Trends Cell Biol 2003;13(2):86–91.PubMed

22.

Davies JA. Watching tubules glow and branch. Curr Opin Genet Dev 2005;15(4):364–70.PubMed

23.

Watanabe T, Costantini F. Real-time analysis of ureteric bud branching morphogenesis in vitro. Dev Biol 2004;271(1):98–108.PubMed

24.

Kispert A, Vainio S, Shen L, Rowitch DH, McMahon AP. Proteoglycans are required for maintenance of Wnt-11 expression in the ureter tips. Development 1996;122(11):3627–37.PubMed

25.

Shakya R, Watanabe T, Costantini F. The role of GDNF/Ret signaling in ureteric bud cell fate and branching morphogenesis. Dev Cell 2005;8(1):65–74.PubMed

26.

Schmidt-Ott KM, Yang J, Chen X, Wang H, Paragas N, Mori K, et al. Novel regulators of kidney development from the tips of the ureteric bud. J Am Soc Nephrol 2005;16(7):1993–2002.PubMed

27.

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(12):4013–22.PubMed

28.

Uv A, Cantera R, Samakovlis C. Drosophila tracheal morphogenesis: intricate cellular solutions to basic plumbing problems. Trends Cell Biol 2003;13(6):301–9.PubMed

29.

Samakovlis C, Hacohen N, Manning G, Sutherland DC, Guillemin K, Krasnow MA. Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 1996;122(5):1395–407.PubMed

30.

Weaver M, Dunn NR, Hogan BL. Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis. Development 2000;127(12):2695–704.PubMed

31.

Brophy PD, Ostrom L, Lang KM, Dressler GR. Regulation of ureteric bud outgrowth by Pax2-dependent activation of the glial derived neurotrophic factor gene. Development 2001;128(23):4747–56.PubMed

32.

Pichel JG, Shen L, Sheng HZ, Granholm AC, Drago J, Grinberg A, et al. Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 1996;382(6586):73–6.PubMed

33.

Sainio K, Suvanto P, Davies J, Wartiovaara J, Wartiovaara K, Saarma M, et al. Glial-cell-line-derived neurotrophic factor is required for bud initiation from ureteric epithelium. Development 1997;124(20):4077–87.PubMed

34.

Sato M, Kornberg TB. FGF is an essential mitogen and chemoattractant for the air sacs of the drosophila tracheal system. Dev Cell 2002;3(2):195–207.PubMed

35.

Cabernard C, Affolter M. Distinct roles for two receptor tyrosine kinases in epithelial branching morphogenesis in Drosophila. Dev Cell 2005;9(6):831–42.PubMed

36.

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):1–11.PubMed

37.

O’Brien LE, Zegers MM, Mostov KE. Opinion: Building epithelial architecture: insights from three-dimensional culture models. Nat Rev Mol Cell Biol 2002;3(7):531–7.PubMed

38.

Zegers MM, O’Brien LE, Yu W, Datta A, Mostov KE. Epithelial polarity and tubulogenesis in vitro. Trends Cell Biol 2003;13(4):169–76.PubMed

39.

Dor Y, Djonov V, Keshet E. Making vascular networks in the adult: branching morphogenesis without a roadmap. Trends Cell Biol 2003;13(3):131–6.PubMed

40.

Fisher CE, Michael L, Barnett MW, Davies JA. Erk MAP kinase regulates branching morphogenesis in the developing mouse kidney. Development 2001;128(21):4329–38.PubMed

41.

Tang MJ, Cai Y, Tsai SJ, Wang YK, Dressler GR. Ureteric bud outgrowth in response to RET activation is mediated by phosphatidylinositol 3-kinase. Dev Biol 2002;243(1):128–36.PubMed

42.

Reichman-Fried M, Dickson B, Hafen E, Shilo BZ. Elucidation of the role of breathless, a Drosophila FGF receptor homolog, in tracheal cell migration. Genes Dev 1994;8(4):428–39.PubMed

43.

Klambt C, Glazer L, Shilo BZ. Breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells. Genes Dev 1992;6(9):1668–78.PubMed

44.

Ghabrial A, Krasnow MA. Social interactions among epithelial cells during tracheal branching morphogenesis. Nature 2006;441:746–749.

45.

Hinck L, Silberstein GB. Key stages in mammary gland development: the mammary end bud as a motile organ. Breast Cancer Res 2005;7(6):245–51.PubMed

46.

Min H, Danilenko DM, Scully SA, Bolon B, Ring BD, Tarpley JE, et al. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev 1998;12(20):3156–61.PubMed

47.

Sekine K, Ohuchi H, Fujiwara M, Yamasaki M, Yoshizawa T, Sato T, et al. Fgf10 is essential for limb and lung formation. Nat Genet 1999;21(1):138–41.PubMed

48.

De Moerlooze L, Spencer-Dene B, Revest J, Hajihosseini M, Rosewell I, Dickson C. An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal–epithelial signalling during mouse organogenesis. Development 2000;127(3):483–92.PubMed

49.

Zhao H, Kegg H, Grady S, Truong HT, Robinson ML, Baum M, et al. Role of fibroblast growth factor receptors 1 and 2 in the ureteric bud. Dev Biol 2004;276(2):403–15.PubMed

50.

Dickson C, Spencer-Dene B, Dillon C, Fantl V. Tyrosine kinase signalling in breast cancer: fibroblast growth factors and their receptors. Breast Cancer Res 2000;2(3):191–6.PubMed

51.

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(1):53–60.PubMed

52.

Steinberg Z, Myers C, Heim VM, Lathrop CA, Rebustini IT, Stewart JS, et al. FGFR2b signaling regulates ex vivo submandibular gland epithelial cell proliferation and branching morphogenesis. Development 2005;132(6):1223–34.PubMed

53.

Entesarian M, Matsson H, Klar J, Bergendal B, Olson L, Arakaki R, et al. Mutations in the gene encoding fibroblast growth factor 10 are associated with aplasia of lacrimal and salivary glands. 2005;37(2):125–128.

54.

Miettinen PJ, Warburton D, Bu D, Zhao JS, Berger JE, Minoo P, et al. Impaired lung branching morphogenesis in the absence of functional EGF receptor. Dev Biol 1997;186(2):224–36.PubMed

55.

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 10.1210/en.2003-1112. Endocrinology 2004;145(7):3106–10.PubMed

56.

Bonnette SG, Hadsell DL. Targeted disruption of the IGF-I receptor gene decreases cellular proliferation in mammary terminal end buds. Endocrinology 2001;142(11):4937–45.PubMed

57.

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(2):476–81.PubMed

58.

Costantini F, Shakya R. GDNF/Ret signaling and the development of the kidney. BioEssays 2006;28(2):117–27.PubMed

59.

Hacohen N, Kramer S, Sutherland D, Hiromi Y, Krasnow MA. Sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 1998;92(2):253–63.PubMed

60.

Kim HJ, Bar-Sagi D. Modulation of signalling by Sprouty: a developing story. Nat Rev Mol Cell Biol 2004;5(6):441–50.PubMed

61.

Kramer S, Okabe M, Hacohen N, Krasnow MA, Hiromi Y. Sprouty: a common antagonist of FGF and EGF signaling pathways in Drosophila. Development 1999;126(11):2515–25.PubMed

62.

Reich A, Sapir A, Shilo B. Sprouty is a general inhibitor of receptor tyrosine kinase signaling. Development 1999;126(18):4139–47.PubMed

63.

Casci T, Vinos J, Freeman M. Sprouty, an intracellular inhibitor of Ras signaling. Cell 1999;96(5):655–65.PubMed

64.

Minowada G, Jarvis LA, Chi CL, Neubuser A, Sun X, Hacohen N, et al. Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. Development 1999;126(20):4465–75.PubMed

65.

Mason JM, Morrison DJ, Basson MA, Licht JD. Sprouty proteins: multifaceted negative-feedback regulators of receptor tyrosine kinase signaling. Trends Cell Biol 2006;16(1):45–54.PubMed

66.

Basson MA, Akbulut S, Watson-Johnson J, Simon R, Carroll TJ, Shakya R, et al. Sprouty1 is a critical regulator of GDNF/RET-mediated kidney induction. Dev Cell 2005;8(2):229–39.PubMed

67.

Mailleux AA, Tefft D, Ndiaye D, Itoh N, Thiery JP, Warburton D, et al. Evidence that SPROUTY2 functions as an inhibitor of mouse embryonic lung growth and morphogenesis. Mech Dev 2001;102(1–2):81–94.PubMed

68.

Tefft JD, Lee M, Smith S, Leinwand M, Zhao J, Bringas P, Jr., et al. Conserved function of mSpry-2, a murine homolog of Drosophila sprouty, which negatively modulates respiratory organogenesis. Curr Biol 1999;9(4):219–22.PubMed

69.

Niehrs C, Meinhardt H. Modular feedback. Nature 2002;417(6884):35–6.PubMed

70.

Tsang M, Friesel R, Kudoh T, Dawid IB. Identification of Sef, a novel modulator of FGF signalling. Nat Cell Biol 2002;4(2):165–9.PubMed

71.

Wakioka T, Sasaki A, Kato R, Shouda T, Matsumoto A, Miyoshi K, et al. Spred is a Sprouty-related suppressor of Ras signalling. Nature 2001;412(6847):647–51.PubMed

72.

Furthauer M, Lin W, Ang SL, Thisse B, Thisse C. Sef is a feedback-induced antagonist of Ras/MAPK-mediated FGF signalling. Nat Cell Biol 2002;4(2):170–4.PubMed

73.

Sivak JM, Petersen LF, Amaya E. FGF signal interpretation is directed by Sprouty and Spred proteins during mesoderm formation. Dev Cell 2005;8(5):689–701.PubMed

74.

Torii S, Kusakabe M, Yamamoto T, Maekawa M, Nishida E. Sef is a spatial regulator for Ras/MAP kinase signaling. Dev Cell 2004;7(1):33–44.PubMed

75.

Hashimoto S, Nakano H, Singh G, Katyal S. Expression of Spred and Sprouty in developing rat lung. Gene Expr Patterns 2002;2(3–4):347–53.PubMed

76.

Pepicelli CV, Lewis PM, McMahon AP. Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Curr Biol 1998;8(19):1083–6.PubMed

77.

Litingtung Y, Lei L, Westphal H, Chiang C. Sonic hedgehog is essential to foregut development. Nat Genet 1998;20(1):58–61.PubMed

78.

Jaskoll T, Leo T, Witcher D, Ormestad M, Astorga J, Bringas P, Jr., et al. Sonic hedgehog signaling plays an essential role during embryonic salivary gland epithelial branching morphogenesis. Dev Dyn 2004;229(4):722–32.PubMed

79.

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(22):5181–93.PubMed

80.

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(1):133–44.PubMed

81.

Michno K, Boras-Granic K, Mill P, Hui CC, Hamel PA. Shh expression is required for embryonic hair follicle but not mammary gland development. Dev Biol 2003;264(1):153–65.PubMed

82.

Gallego MI, Beachy PA, Hennighausen L, Robinson GW. Differential requirements for shh in mammary tissue and hair follicle morphogenesis. Dev Biol 2002;249(1):131–9.PubMed

83.

Chuang P-T, Kawcak TN, McMahon AP. Feedback control of mammalian Hedgehog signaling by the Hedgehog-binding protein, Hip1, modulates Fgf signaling during branching morphogenesis of the lung. Genes Dev 2003;17(3):342–347.PubMed

84.

Feng XH, Derynck R. Specificity and versatility in tgf-beta signaling through Smads. Annu Rev Cell Dev Biol 2005;21:659–93.PubMed

85.

Massague J, Chen YG. Controlling TGF-beta signaling. Genes Dev 2000;14(6):627–44.PubMed

86.

Vincent S, Ruberte E, Grieder NC, Chen CK, Haerry T, Schuh R, et al. DPP controls tracheal cell migration along the dorsoventral body axis of the Drosophila embryo. Development 1997;124(14):2741–50.PubMed

87.

Lu P, Minowada G, Martin GR. Increasing Fgf4 expression in the mouse limb bud causes polysyndactyly and rescues the skeletal defects that result from loss of Fgf8 function. Development 2006;133(1):33–42.PubMed

88.

Pizette S, Abate-Shen C, Niswander L. BMP controls proximodistal outgrowth, via induction of the apical ectodermal ridge, and dorsoventral patterning in the vertebrate limb. Development 2001;128(22):4463–74.PubMed

89.

Ahn K, Mishina Y, Hanks MC, Behringer RR, Crenshaw EB, 3rd. BMPR-IA signaling is required for the formation of the apical ectodermal ridge and dorsal–ventral patterning of the limb. Development 2001;128(22):4449–61.PubMed

90.

Pizette S, Niswander L. BMPs negatively regulate structure and function of the limb apical ectodermal ridge. Development 1999;126(5):883–94.PubMed

91.

Warburton D, Bellusci S, De Langhe S, Del Moral PM, Fleury V, Mailleux A, et al. Molecular mechanisms of early lung specification and branching morphogenesis. Pediatr Res 2005;57(5 Pt 2):26R–37R.PubMed

92.

Takahashi H, Ikeda T. Transcripts for two members of the transforming growth factor-beta superfamily BMP-3 and BMP-7 are expressed in developing rat embryos. Dev Dyn 1996;207(4):439–49.PubMed

93.

Eblaghie MC, Reedy M, Oliver T, Mishina Y, Hogan BL. Evidence that autocrine signaling through Bmpr1a regulates the proliferation, survival and morphogenetic behavior of distal lung epithelial cells. Dev Biol 2006;291(1):67–82.PubMed

94.

Miyazaki Y, Oshima K, Fogo A, Hogan BL, Ichikawa I. Bone morphogenetic protein 4 regulates the budding site and elongation of the mouse ureter. J Clin Invest 2000;105(7):863–73.PubMedCrossRef

95.

Michos O, Panman L, Vintersten K, Beier K, Zeller R, Zuniga A. Gremlin-mediated BMP antagonism induces the epithelial–mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development 2004;131(14):3401–10.PubMed

96.

Bush KT, Sakurai H, Steer DL, Leonard MO, Sampogna RV, Meyer TN, et al. TGF-beta superfamily members modulate growth, branching, shaping, and patterning of the ureteric bud. Dev Biol 2004;266(2):285–98.PubMed

97.

Serra R, Pelton RW, Moses HL. TGF beta 1 inhibits branching morphogenesis and N-myc expression in lung bud organ cultures. Development 1994;120(8):2153–61.PubMed

98.

Zhao J, Bu D, Lee M, Slavkin HC, Hall FL, Warburton D. Abrogation of transforming growth factor-beta type II receptor stimulates embryonic mouse lung branching morphogenesis in culture. Dev Biol 1996;180(1):242–57.PubMed

99.

Santos OF, Nigam SK. HGF-induced tubulogenesis and branching of epithelial cells is modulated by extracellular matrix and TGF-beta. Dev Biol 1993;160(2):293–302.PubMed

100.

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(12A): 2308–17.PubMed

101.

Letterio JJ, Geiser AG, Kulkarni AB, Roche NS, Sporn MB, Roberts AB. Maternal rescue of transforming growth factor-beta 1 null mice. Science 1994;264(5167):1936–8.PubMed

102.

Kaartinen V, Voncken JW, Shuler C, Warburton D, Bu D, Heisterkamp N, et al. Abnormal lung development and cleft palate in mice lacking TGF-beta 3 indicates defects of epithelial–mesenchymal interaction. Nat Genet 1995;11(4):415–21.PubMed

103.

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(6):2081–93.PubMed

104.

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(4):230–7.PubMed

105.

Serra R, Crowley MR. Mouse models of transforming growth factor beta impact in breast development and cancer. Endocr-Relat Cancer 2005;12(4):749–60.PubMed

106.

Joseph H, Gorska AE, Sohn P, Moses HL, Serra R. Overexpression of a kinase-deficient transforming growth factor-beta type II receptor in mouse mammary stroma results in increased epithelial branching. Mol Biol Cell 1999;10(4):1221–34.PubMed

107.

Crowley MR, Bowtell D, Serra R. TGF-beta, c-Cbl, and PDGFR-alpha the in mammary stroma. Dev Biol 2005;279(1):58–72.PubMed

108.

Cheng N, Bhowmick NA, Chytil A, Gorksa AE, Brown KA, Muraoka R, et al. Loss of TGF-beta type II receptor in fibroblasts promotes mammary carcinoma growth and invasion through upregulation of TGF-alpha-, MSP- and HGF-mediated signaling networks. Oncogene 2005;24(32):5053–68.PubMed

109.

Beer HD, Florence C, Dammeier J, McGuire L, Werner S, Duan DR. Mouse fibroblast growth factor 10: cDNA cloning, protein characterization, and regulation of mRNA expression. Oncogene 1997;15(18):2211–8.PubMed

110.

Lebeche D, Malpel S, Cardoso WV. Fibroblast growth factor interactions in the developing lung. Mech Dev 1999;86(1–2):125–36.PubMed

111.

Tomlinson DC, Grindley JC, Thomson AA. Regulation of Fgf10 gene expression in the prostate: identification of transforming growth factor-beta1 and promoter elements. Endocrinology 2004;145(4):1988–95.PubMed

112.

Heine UI, Munoz EF, Flanders KC, Roberts AB, Sporn MB. Colocalization of TGF-beta 1 and collagen I and III, fibronectin and glycosaminoglycans during lung branching morphogenesis. Development 1990;109(1):29–36.PubMed

113.

Silberstein GB, Strickland P, Coleman S, Daniel CW. Epithelium-dependent extracellular matrix synthesis in transforming growth factor-beta 1-growth-inhibited mouse mammary gland. J Cell Biol 1990;110(6):2209–19.PubMed

114.

Silberstein GB. Postnatal mammary gland morphogenesis. Microsc Res Tech 2001;52(2):155–62.PubMed

115.

White AC, Xu J, Yin Y, Smith C, Schmid G, Ornitz DM. FGF9 and SHH signaling coordinate lung growth and development through regulation of distinct mesenchymal domains. Development 2006;133(8):1507–17.PubMed

116.

Poladia DP, Kish K, Kutay B, Hains D, Kegg H, Zhao H, et al. Role of fibroblast growth factor receptors 1 and 2 in the metanephric mesenchyme. Dev Biol 2006;291(2):325–39.PubMed

117.

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(9):777–85.PubMed

118.

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-alpha knockout (ERKO) mouse. Breast Cancer Res Treat 2003;79(2):161–73.PubMed

119.

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(2):304–15.PubMed

120.

Luetteke NC, Qiu TH, Fenton SE, Troyer KL, Riedel RF, Chang A, et al. Targeted inactivation of the EGF and amphiregulin genes reveals distinct roles for EGF receptor ligands in mouse mammary gland development. Development 1999;126(12):2739–50.PubMed

121.

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(17):3923–33.PubMed

122.

Zhao J, Chen H, Peschon JJ, Shi W, Zhang Y, Frank SJ, et al. Pulmonary hypoplasia in mice lacking tumor necrosis factor-alpha converting enzyme indicates an indispensable role for cell surface protein shedding during embryonic lung branching morphogenesis. Dev Biol 2001;232(1):204–18.PubMed

123.

Kheradmand F, Rishi K, Werb Z. Signaling through the EGF receptor controls lung morphogenesis in part by regulating MT1-MMP-mediated activation of gelatinase A/MMP2. J Cell Sci 2002;115(Pt 4):839–48.PubMed

124.

Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001;17:463–516.PubMed

125.

Mott JD, Werb Z. Regulation of matrix biology by matrix metalloproteinases. Curr Opin Cell Biol 2004;16(5):558–64.PubMed

126.

Sakai T, Larsen M, Yamada KM. Fibronectin requirement in branching morphogenesis. Nature 2003;423(6942):876–81.PubMed

127.

Wessells NK, Cohen JH. Effects of collagenase on developing epithelia in vitro: lung, ureteric bud, and pancreas. Dev Biol 1968;18(3):294–309.PubMed

128.

Banerjee SD, Cohn RH, Bernfield MR. Basal lamina of embryonic salivary epithelia. Production by the epithelium and role in maintaining lobular morphology. J Cell Biol 1977;73(2):445–63.PubMed

129.

Nakanishi Y, Sugiura F, Kishi J, Hayakawa T. Collagenase inhibitor stimulates cleft formation during early morphogenesis of mouse salivary gland. Dev Biol 1986;113(1):201–6.PubMed

130.

Lelongt B, Trugnan G, Murphy G, Ronco PM. Matrix metalloproteinases MMP2 and MMP9 are produced in early stages of kidney morphogenesis but only MMP9 is required for renal organogenesis in vitro. J. Cell Biol. 1997;136(6):1363–1373.PubMed

131.

Lelongt B, Ronco P. Role of matrix metalloproteinases in kidney development and glomerulopathy: lessons from transgenic mice. Nephrol Dial Transplant 2002;17(Suppl 9):28–31.PubMed

132.

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(6):1123–33.PubMed

133.

Lukashev ME, Werb Z. ECM signalling: orchestrating cell behaviour and misbehaviour. Trends Cell Biol 1998;8(11):437–41.PubMed

134.

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(8):2906–17.PubMed

135.

Chen J, Diacovo TG, Grenache DG, Santoro SA, Zutter MM. The alpha(2) integrin subunit-deficient mouse: a multifaceted phenotype including defects of branching morphogenesis and hemostasis. Am J Pathol 2002;161(1):337–44.PubMed

136.

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(1):13–32.PubMed

137.

White DE, Kurpios NA, Zuo D, Hassell JA, Blaess S, Mueller U, et al. Targeted disruption of beta1-integrin in a transgenic mouse model of human breast cancer reveals an essential role in mammary tumor induction. Cancer Cell 2004;6(2):159–70.PubMed

138.

Hathaway HJ, Shur BD. Mammary gland morphogenesis is inhibited in transgenic mice that overexpress cell surface beta1,4-galactosyltransferase. Development 1996;122(9):2859–72.PubMed

139.

Muschler J, Levy D, Boudreau R, Henry M, Campbell K, Bissell MJ. A role for dystroglycan in epithelial polarization: loss of function in breast tumor cells. Cancer Res 2002;62(23):7102–9.PubMed

140.

Davies JA. Do different branching epithelia use a conserved developmental mechanism? BioEssays 2002;24(10):937–48.PubMed

141.

Kouros-Mehr H, Werb Z. Candidate regulators of mammary branching morphogenesis identified by genome-wide transcript analysis. Dev Dyn 2006;Oct 12; [Epub ahead of print].

142.

Basson MA, Watson-Johnson J, Shakya R, Akbulut S, Hyink D, Constantini FD, et al. Branching morphogenesis of the ureteric epithelium during kidney development is coordinated by the opposing functions of GDNF and Sprouty1. Dev Biol 2006; Nov 15;299(2):466–77.PubMed

143.

Chi L, Zhang S, Lin Y, Prunskaite-Hyyrylainen R, Vuolteenaho R, Itaranta P, et al. Sprouty proteins regulate ureteric branching by coordinating reciprocal epithelial Wnt11, mesenchymal Gdnf and stromal Fgf7 signalling during kidney development. Development 2004;131(14):3345–56.PubMed

Title: Comparative Mechanisms of Branching Morphogenesis in Diverse Systems
Authors: Pengfei Lu
Mark D. Sternlicht
Zena Werb
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/s10911-006-9027-z

Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Watch now

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras

Prof. Fabrice Barlesi

Developed by: Springer Medicine

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 3-4/2006

Pubertal Mammary Gland Development: Insights from Mouse Models

Analysis of Lactation Defects in Transgenic Mice

Milking Biological Diversity For All It’s Worth—What Do Other Model Systems Teach Us About Mammary Gland Development and Function?

The Mammary Bud as a Skin Appendage: Unique and Shared Aspects of Development

Alveolar and Lactogenic Differentiation

Mammary Gland Macrophages: Pleiotropic Functions in Mammary Development

Keynote webinar | Spotlight on antibody–drug conjugates in cancer