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Erschienen in: Brain Structure and Function 6/2004

01.09.2004 | Original Article

Regulation of external genitalia development by concerted actions of FGF ligands and FGF receptors

verfasst von: Yoshihiko Satoh, Ryuma Haraguchi, Tracy J. Wright, Suzanne L. Mansour, Juha Partanen, Mohammad K. Hajihosseini, Veraragavan P. Eswarakumar, Peter Lonai, Gen Yamada

Erschienen in: Brain Structure and Function | Ausgabe 6/2004

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Abstract

Members of the fibroblast growth factor (FGF) family play diverse roles during the development and patterning of various organs. In human and mice, 22 FGFs and four receptors derived from several splice variants are present. Redundant expression and function of FGF genes in organogenesis have been reported, but their roles in embryonic external genitalia, genital tubercle (GT), development have not been studied in detail. To address the role of FGF during external genitalia development, we have analyzed the expression of FGF genes (Fgf8, 9, 10) and receptor genes (Fgfr1, r2IIIb, r2IIIc) in GT of mice. Furthermore, Fgf10 and Fgfr2IIIb mutant mice were analyzed to elucidate their roles in embryonic external genitalia development. Fgfr2IIIb was expressed in urethral plate epithelium during GT development. Fgfr2IIIb mutant mice display urethral dysmorphogenesis. Marker gene analysis for urethral plate and bilateral mesenchymal formation suggests the existence of epithelial-mesenchymal interaction during urethral morphogenesis. Therefore, FGF10/FGFR2IIIb signals seem to constitute a developmental cascade for such morphogenesis.
Literatur
Zurück zum Zitat Arman E, Haffner-Krausz R, Gorivodsky M, Lonai P (1999) Fgfr2 is required for limb outgrowth and lung-branching morphogenesis. Proc Natl Acad Sci USA 96:11895–11899 CrossRefPubMed Arman E, Haffner-Krausz R, Gorivodsky M, Lonai P (1999) Fgfr2 is required for limb outgrowth and lung-branching morphogenesis. Proc Natl Acad Sci USA 96:11895–11899 CrossRefPubMed
Zurück zum Zitat Barlow AJ, Francis-West PH (1997) Ectopic application of recombinant BMP-2 and BMP-4 can change patterning of developing chick facial primordia. Development 124:391–398 PubMed Barlow AJ, Francis-West PH (1997) Ectopic application of recombinant BMP-2 and BMP-4 can change patterning of developing chick facial primordia. Development 124:391–398 PubMed
Zurück zum Zitat Baskin LS, Liu W, Bastacky J, Yucel S (2004) Anatomical studies of the mouse genital tubercle. Adv Exp Med Biol 545:103–121 PubMed Baskin LS, Liu W, Bastacky J, Yucel S (2004) Anatomical studies of the mouse genital tubercle. Adv Exp Med Biol 545:103–121 PubMed
Zurück zum Zitat Dassule HR, McMahon AP (1998) Analysis of epithelial-mesenchymal interactions in the initial morphogenesis of the mammalian tooth. Dev Biol 202:215–227 CrossRefPubMed Dassule HR, McMahon AP (1998) Analysis of epithelial-mesenchymal interactions in the initial morphogenesis of the mammalian tooth. Dev Biol 202:215–227 CrossRefPubMed
Zurück zum Zitat De Moerlooze L, Spencer-Dene B, Revest J, Hajihosseini M, Rosewell I, Dickson C (2000) An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organogenesis. Development 127:483–492 PubMed De Moerlooze L, Spencer-Dene B, Revest J, Hajihosseini M, Rosewell I, Dickson C (2000) An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organogenesis. Development 127:483–492 PubMed
Zurück zum Zitat Dolle P, Izpisua-Belmonte JC, Brown JM, Tickle C, Duboule D (1991) HOX-4 genes and the morphogenesis of mammalian genitalia. Genes Dev 5:1767–7 PubMed Dolle P, Izpisua-Belmonte JC, Brown JM, Tickle C, Duboule D (1991) HOX-4 genes and the morphogenesis of mammalian genitalia. Genes Dev 5:1767–7 PubMed
Zurück zum Zitat Dravis C, Yokoyama N, Chumley MJ, Cowan CA, Silvany RE, Shay J, Baker LA, Henkemeyer M (2004) Bidirectional signaling mediated by ephrin-B2 and EphB2 controls urorectal development. Dev Biol 271:272–290 CrossRefPubMed Dravis C, Yokoyama N, Chumley MJ, Cowan CA, Silvany RE, Shay J, Baker LA, Henkemeyer M (2004) Bidirectional signaling mediated by ephrin-B2 and EphB2 controls urorectal development. Dev Biol 271:272–290 CrossRefPubMed
Zurück zum Zitat Eswarakumar VP, Monsonego-Ornan E, Pines M, Antonopoulou I, Morriss-Kay GM, Lonai P (2002) The IIIc alternative of Fgfr2 is a positive regulator of bone formation. Development 129:3783–3793 PubMed Eswarakumar VP, Monsonego-Ornan E, Pines M, Antonopoulou I, Morriss-Kay GM, Lonai P (2002) The IIIc alternative of Fgfr2 is a positive regulator of bone formation. Development 129:3783–3793 PubMed
Zurück zum Zitat Ganan Y, Macias D, Duterque-Coquillaud M, Ros MA, Hurle JM (1996) Role of TGF beta s and BMPs as signals controlling the position of the digits and the areas of interdigital cell death in the developing chick limb autopod. Development 122:2349–2357 PubMed Ganan Y, Macias D, Duterque-Coquillaud M, Ros MA, Hurle JM (1996) Role of TGF beta s and BMPs as signals controlling the position of the digits and the areas of interdigital cell death in the developing chick limb autopod. Development 122:2349–2357 PubMed
Zurück zum Zitat Grothe C, Brand-Saberi B, Wilting J, Christ B (1996) Fibroblast growth factor receptor 1 in skeletal and heart muscle cells: expression during early avian development and regulation after notochord transplantation. Dev Dyn 206:310–317 CrossRefPubMed Grothe C, Brand-Saberi B, Wilting J, Christ B (1996) Fibroblast growth factor receptor 1 in skeletal and heart muscle cells: expression during early avian development and regulation after notochord transplantation. Dev Dyn 206:310–317 CrossRefPubMed
Zurück zum Zitat Hajihosseini MK, Lalioti MD, Arthaud S, Burgar HR, Brown JM, Twigg SR, Wilkie AO, Heath JK (2004) Skeletal development is regulated by fibroblast growth factor receptor 1 signalling dynamics. Development 131:325–335 CrossRefPubMed Hajihosseini MK, Lalioti MD, Arthaud S, Burgar HR, Brown JM, Twigg SR, Wilkie AO, Heath JK (2004) Skeletal development is regulated by fibroblast growth factor receptor 1 signalling dynamics. Development 131:325–335 CrossRefPubMed
Zurück zum Zitat Haraguchi R, Mo R, Hui C, Motoyama J, Makino S, Shiroishi T, Gaffield W, Yamada G (2001) Unique functions of Sonic hedgehog signaling during external genitalia development. Development 128:4241–4250 PubMed Haraguchi R, Mo R, Hui C, Motoyama J, Makino S, Shiroishi T, Gaffield W, Yamada G (2001) Unique functions of Sonic hedgehog signaling during external genitalia development. Development 128:4241–4250 PubMed
Zurück zum Zitat Haraguchi R, Suzuki K, Murakami R, Sakai M, Kamikawa M, Kengaku M, Sekine K, Kawano H, Kato S, Ueno N, Yamada G (2000) Molecular analysis of external genitalia formation: the role of fibroblast growth factor (Fgf) genes during genital tubercle formation. Development 127:2471–2479 PubMed Haraguchi R, Suzuki K, Murakami R, Sakai M, Kamikawa M, Kengaku M, Sekine K, Kawano H, Kato S, Ueno N, Yamada G (2000) Molecular analysis of external genitalia formation: the role of fibroblast growth factor (Fgf) genes during genital tubercle formation. Development 127:2471–2479 PubMed
Zurück zum Zitat Hsu TY, Chang SY, Wang TJ, Ou CY, Chen ZH, Hsu PH (2001) Prenatal sonographic appearance of Beare-Stevenson cutis gyrata syndrome: two- and three-dimensional ultrasonographic findings. Prenat Diagn 21:665–667 CrossRefPubMed Hsu TY, Chang SY, Wang TJ, Ou CY, Chen ZH, Hsu PH (2001) Prenatal sonographic appearance of Beare-Stevenson cutis gyrata syndrome: two- and three-dimensional ultrasonographic findings. Prenat Diagn 21:665–667 CrossRefPubMed
Zurück zum Zitat Johnson RL, Tabin CJ (1997) Molecular models for vertebrate limb development. Cell 90:979–990 CrossRefPubMed Johnson RL, Tabin CJ (1997) Molecular models for vertebrate limb development. Cell 90:979–990 CrossRefPubMed
Zurück zum Zitat Kawakami Y, Capdevila J, Buscher D, Itoh T, Rodriguez Esteban C, Izpisua Belmonte JC (2001) WNT signals control FGF-dependent limb initiation and AER induction in the chick embryo. Cell 104:891–900 CrossRefPubMed Kawakami Y, Capdevila J, Buscher D, Itoh T, Rodriguez Esteban C, Izpisua Belmonte JC (2001) WNT signals control FGF-dependent limb initiation and AER induction in the chick embryo. Cell 104:891–900 CrossRefPubMed
Zurück zum Zitat Kurzrock EA, Baskin LS, Li Y, Cunha GR (1999) Epithelial-mesenchymal interactions in development of the mouse fetal genital tubercle. Cells Tissues Organs 164:125–130 CrossRefPubMed Kurzrock EA, Baskin LS, Li Y, Cunha GR (1999) Epithelial-mesenchymal interactions in development of the mouse fetal genital tubercle. Cells Tissues Organs 164:125–130 CrossRefPubMed
Zurück zum Zitat Macatee TL, Hammond BP, Arenkiel BR, Francis L, Frank DU, Moon AM (2003) Ablation of specific expression domains reveals discrete functions of ectoderm- and endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 130:6361–6374 CrossRefPubMed Macatee TL, Hammond BP, Arenkiel BR, Francis L, Frank DU, Moon AM (2003) Ablation of specific expression domains reveals discrete functions of ectoderm- and endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 130:6361–6374 CrossRefPubMed
Zurück zum Zitat Min H, Danilenko DM, Scully SA, Bolon B, Ring BD, Tarpley JE, DeRose M, Simonet WS (1998) Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev 12:3156–3161 PubMed Min H, Danilenko DM, Scully SA, Bolon B, Ring BD, Tarpley JE, DeRose M, Simonet WS (1998) Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev 12:3156–3161 PubMed
Zurück zum Zitat Morgan EA, Nguyen SB, Scott V, Stadler HS (2003) Loss of Bmp7 and Fgf8 signaling in Hoxa13-mutant mice causes hypospadia. Development 130:3095–3109 CrossRefPubMed Morgan EA, Nguyen SB, Scott V, Stadler HS (2003) Loss of Bmp7 and Fgf8 signaling in Hoxa13-mutant mice causes hypospadia. Development 130:3095–3109 CrossRefPubMed
Zurück zum Zitat Murakami R, Mizuno T (1986) Proximal-distal sequence of development of the skeletal tissues in the penis of rat and the inductive effect of epithelium. J Embryol Exp Morphol 92:133–143 PubMed Murakami R, Mizuno T (1986) Proximal-distal sequence of development of the skeletal tissues in the penis of rat and the inductive effect of epithelium. J Embryol Exp Morphol 92:133–143 PubMed
Zurück zum Zitat Naiche LA, Papaioannou VE (2003) Loss of Tbx4 blocks hindlimb development and affects vascularization and fusion of the allantois. Development 130:2681–2693 CrossRefPubMed Naiche LA, Papaioannou VE (2003) Loss of Tbx4 blocks hindlimb development and affects vascularization and fusion of the allantois. Development 130:2681–2693 CrossRefPubMed
Zurück zum Zitat Ng JK, Kawakami Y, Buscher D, Raya A, Itoh T, Koth CM, Rodriguez Esteban C, Rodriguez-Leon J, Garrity DM, Fishman MC, Izpisua Belmonte JC (2002) The limb identity gene Tbx5 promotes limb initiation by interacting with Wnt2b and Fgf10. Development 129:5161–5170 PubMed Ng JK, Kawakami Y, Buscher D, Raya A, Itoh T, Koth CM, Rodriguez Esteban C, Rodriguez-Leon J, Garrity DM, Fishman MC, Izpisua Belmonte JC (2002) The limb identity gene Tbx5 promotes limb initiation by interacting with Wnt2b and Fgf10. Development 129:5161–5170 PubMed
Zurück zum Zitat Ohuchi H, Hori Y, Yamasaki M, Harada H, Sekine K, Kato S, Itoh N (2000) FGF10 acts as a major ligand for FGF receptor 2 IIIb in mouse multi-organ development. Biochem Biophys Res Commun 277:643–649 CrossRefPubMed Ohuchi H, Hori Y, Yamasaki M, Harada H, Sekine K, Kato S, Itoh N (2000) FGF10 acts as a major ligand for FGF receptor 2 IIIb in mouse multi-organ development. Biochem Biophys Res Commun 277:643–649 CrossRefPubMed
Zurück zum Zitat Ohuchi H, Nakagawa T, Yamamoto A, Araga A, Ohata T, Ishimaru Y, Yoshioka H, Kuwana T, Nohno T, Yamasaki M, Itoh N, Noji S (1997) The mesenchymal factor, FGF10, initiates and maintains the outgrowth of the chick limb bud through interaction with FGF8, an apical ectodermal factor. Development 124:2235–2244 PubMed Ohuchi H, Nakagawa T, Yamamoto A, Araga A, Ohata T, Ishimaru Y, Yoshioka H, Kuwana T, Nohno T, Yamasaki M, Itoh N, Noji S (1997) The mesenchymal factor, FGF10, initiates and maintains the outgrowth of the chick limb bud through interaction with FGF8, an apical ectodermal factor. Development 124:2235–2244 PubMed
Zurück zum Zitat Ornitz DM, Xu J, Colvin JS, McEwen DG, MacArthur CA, Coulier F, Gao G, Goldfarb M (1996) Receptor specificity of the fibroblast growth factor family. J Biol Chem 271:15292–15297 CrossRefPubMed Ornitz DM, Xu J, Colvin JS, McEwen DG, MacArthur CA, Coulier F, Gao G, Goldfarb M (1996) Receptor specificity of the fibroblast growth factor family. J Biol Chem 271:15292–15297 CrossRefPubMed
Zurück zum Zitat Orr-Urtreger A, Givol D, Yayon A, Yarden Y, Lonai P (1991) Developmental expression of two murine fibroblast growth factor receptors, flg and bek. Development 113:1419-1434 PubMed Orr-Urtreger A, Givol D, Yayon A, Yarden Y, Lonai P (1991) Developmental expression of two murine fibroblast growth factor receptors, flg and bek. Development 113:1419-1434 PubMed
Zurück zum Zitat Othman-Hassan K, Patel K, Papoutsi M, Rodriguez-Niedenfuhr M, Christ B, Wilting J (2001) Arterial identity of endothelial cells is controlled by local cues. Dev Biol 237:398–409 CrossRefPubMed Othman-Hassan K, Patel K, Papoutsi M, Rodriguez-Niedenfuhr M, Christ B, Wilting J (2001) Arterial identity of endothelial cells is controlled by local cues. Dev Biol 237:398–409 CrossRefPubMed
Zurück zum Zitat Partanen J, Schwartz L, Rossant J (1998) Opposite phenotypes of hypomorphic and Y766 phosphorylation site mutations reveal a function for Fgfr1 in anteroposterior patterning of mouse embryos. Genes Dev 12:2332–2344 PubMed Partanen J, Schwartz L, Rossant J (1998) Opposite phenotypes of hypomorphic and Y766 phosphorylation site mutations reveal a function for Fgfr1 in anteroposterior patterning of mouse embryos. Genes Dev 12:2332–2344 PubMed
Zurück zum Zitat Perriton CL, Powles N, Chiang C, Maconochie MK, Cohn MJ (2002) Sonic hedgehog signaling from the urethral epithelium controls external genital development. Dev Biol 247:26–46 CrossRefPubMed Perriton CL, Powles N, Chiang C, Maconochie MK, Cohn MJ (2002) Sonic hedgehog signaling from the urethral epithelium controls external genital development. Dev Biol 247:26–46 CrossRefPubMed
Zurück zum Zitat Peters KG, Werner S, Chen G, Williams LT (1992) Two FGF receptor genes are differentially expressed in epithelial and mesenchymal tissues during limb formation and organogenesis in the mouse. Development 114:233–243 PubMed Peters KG, Werner S, Chen G, Williams LT (1992) Two FGF receptor genes are differentially expressed in epithelial and mesenchymal tissues during limb formation and organogenesis in the mouse. Development 114:233–243 PubMed
Zurück zum Zitat Plikus M, Wang WP, Liu J, Wang X, Jiang TX, Chuong CM (2004) Morpho-regulation of ectodermal organs: integument pathology and phenotypic variations in K14-Noggin engineered mice through modulation of bone morphogenic protein pathway. Am J Pathol 164:1099–1114 PubMed Plikus M, Wang WP, Liu J, Wang X, Jiang TX, Chuong CM (2004) Morpho-regulation of ectodermal organs: integument pathology and phenotypic variations in K14-Noggin engineered mice through modulation of bone morphogenic protein pathway. Am J Pathol 164:1099–1114 PubMed
Zurück zum Zitat Powers CJ, McLeskey SW, Wellstein A (2000) Fibroblast growth factors, their receptors and signaling. Endocr Relat Cancer 7:165–197 PubMed Powers CJ, McLeskey SW, Wellstein A (2000) Fibroblast growth factors, their receptors and signaling. Endocr Relat Cancer 7:165–197 PubMed
Zurück zum Zitat Revest JM, Spencer-Dene B, Kerr K, De Moerlooze L, Rosewell I, Dickson C (2001) Fibroblast growth factor receptor 2-IIIb acts upstream of Shh and Fgf4 and is required for limb bud maintenance but not for the induction of Fgf8, Fgf10, Msx1, or Bmp4. Dev Biol 231:47–62 CrossRefPubMed Revest JM, Spencer-Dene B, Kerr K, De Moerlooze L, Rosewell I, Dickson C (2001) Fibroblast growth factor receptor 2-IIIb acts upstream of Shh and Fgf4 and is required for limb bud maintenance but not for the induction of Fgf8, Fgf10, Msx1, or Bmp4. Dev Biol 231:47–62 CrossRefPubMed
Zurück zum Zitat Sekine K, Ohuchi H, Fujiwara M, Yamasaki M, Yoshizawa T, Sato T, Yagishita N, Matsui D, Koga Y, Itoh N, Kato S (1999) Fgf10 is essential for limb and lung formation. Nat Genet 21:138–141 CrossRefPubMed Sekine K, Ohuchi H, Fujiwara M, Yamasaki M, Yoshizawa T, Sato T, Yagishita N, Matsui D, Koga Y, Itoh N, Kato S (1999) Fgf10 is essential for limb and lung formation. Nat Genet 21:138–141 CrossRefPubMed
Zurück zum Zitat Suzuki K, Bachiller D, Chen YP, Kamikawa M, Ogi H, Haraguchi R, Ogino Y, Minami Y, Mishina Y, Ahn K, Crenshaw EB, III, Yamada G (2003) Regulation of outgrowth and apoptosis for the terminal appendage: external genitalia: development by concerted actions of BMP signaling. Development 130:6209–6220 CrossRefPubMed Suzuki K, Bachiller D, Chen YP, Kamikawa M, Ogi H, Haraguchi R, Ogino Y, Minami Y, Mishina Y, Ahn K, Crenshaw EB, III, Yamada G (2003) Regulation of outgrowth and apoptosis for the terminal appendage: external genitalia: development by concerted actions of BMP signaling. Development 130:6209–6220 CrossRefPubMed
Zurück zum Zitat Suzuki K, Ogino Y, Murakami R, Satoh Y, Bachiller D, Yamada G (2002) Embryonic development of mouse external genitalia: insights into a unique mode of organogenesis. Evol Dev 4:133–141 CrossRefPubMed Suzuki K, Ogino Y, Murakami R, Satoh Y, Bachiller D, Yamada G (2002) Embryonic development of mouse external genitalia: insights into a unique mode of organogenesis. Evol Dev 4:133–141 CrossRefPubMed
Zurück zum Zitat Thesleff I, Partanen AM, Vainio S (1991) Epithelial-mesenchymal interactions in tooth morphogenesis: the roles of extracellular matrix, growth factors, and cell surface receptors. J Craniofac Genet Dev Biol 11:229–237 PubMed Thesleff I, Partanen AM, Vainio S (1991) Epithelial-mesenchymal interactions in tooth morphogenesis: the roles of extracellular matrix, growth factors, and cell surface receptors. J Craniofac Genet Dev Biol 11:229–237 PubMed
Zurück zum Zitat Tickle C, Eichele G (1994) Vertebrate limb development. Ann Rev Cell Biol 10:121–152 PubMed Tickle C, Eichele G (1994) Vertebrate limb development. Ann Rev Cell Biol 10:121–152 PubMed
Zurück zum Zitat Tucker AS, Yamada G, Grigoriou M, Pachnis V, Sharpe PT (1999) Fgf-8 determines rostral-caudal polarity in the first branchial arch. Development 126:51–61 PubMed Tucker AS, Yamada G, Grigoriou M, Pachnis V, Sharpe PT (1999) Fgf-8 determines rostral-caudal polarity in the first branchial arch. Development 126:51–61 PubMed
Zurück zum Zitat van der Werff JF, Nievelstein RA, Brands E, Luijsterburg AJ, Vermeij-Keers C (2000) Normal development of the male anterior urethra. Teratology 61:172–183 CrossRefPubMed van der Werff JF, Nievelstein RA, Brands E, Luijsterburg AJ, Vermeij-Keers C (2000) Normal development of the male anterior urethra. Teratology 61:172–183 CrossRefPubMed
Zurück zum Zitat Vargas RA, Maegawa GH, Taucher SC, Leite JC, Sanz P, Cifuentes J, Parra M, Munoz H, Maranduba CM, Passos-Bueno MR (2003) Beare-Stevenson syndrome: Two South American patients with FGFR2 analysis. Am J Med Genet 121:41–46 CrossRef Vargas RA, Maegawa GH, Taucher SC, Leite JC, Sanz P, Cifuentes J, Parra M, Munoz H, Maranduba CM, Passos-Bueno MR (2003) Beare-Stevenson syndrome: Two South American patients with FGFR2 analysis. Am J Med Genet 121:41–46 CrossRef
Zurück zum Zitat Wilkinson DG (1995) RNA detection using non-radioactive in situ hybridization. Curr Opin Biotechnol 6:20–23 CrossRefPubMed Wilkinson DG (1995) RNA detection using non-radioactive in situ hybridization. Curr Opin Biotechnol 6:20–23 CrossRefPubMed
Zurück zum Zitat Wright TJ, Mansour SL (2003) Fgf3 and Fgf10 are required for mouse otic placode induction. Development 130:3379–3390 CrossRefPubMed Wright TJ, Mansour SL (2003) Fgf3 and Fgf10 are required for mouse otic placode induction. Development 130:3379–3390 CrossRefPubMed
Zurück zum Zitat Xu X, Weinstein M, Li C, Naski M, Cohen RI, Ornitz DM, Leder P, Deng C (1998) Fibroblast growth factor receptor 2 (FGFR2)-mediated reciprocal regulation loop between FGF8 and FGF10 is essential for limb induction. Development 125:753–765 PubMed Xu X, Weinstein M, Li C, Naski M, Cohen RI, Ornitz DM, Leder P, Deng C (1998) Fibroblast growth factor receptor 2 (FGFR2)-mediated reciprocal regulation loop between FGF8 and FGF10 is essential for limb induction. Development 125:753–765 PubMed
Zurück zum Zitat Yamada G, Satoh Y, Baskin LS, Cunha GR (2003) Cellular and molecular mechanisms of development of the external genitalia. Differentiation 71:445–460 CrossRefPubMed Yamada G, Satoh Y, Baskin LS, Cunha GR (2003) Cellular and molecular mechanisms of development of the external genitalia. Differentiation 71:445–460 CrossRefPubMed
Zurück zum Zitat Yamaguchi TP, Bradley A, McMahon AP, Jones S (1999) A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126:1211–1223 PubMed Yamaguchi TP, Bradley A, McMahon AP, Jones S (1999) A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126:1211–1223 PubMed
Zurück zum Zitat Yonei-Tamura S, Endo T, Yajima H, Ohuchi H, Ide H, Tamura K (1999) FGF7 and FGF10 directly induce the apical ectodermal ridge in chick embryos. Dev Biol 211:133–143 CrossRefPubMed Yonei-Tamura S, Endo T, Yajima H, Ohuchi H, Ide H, Tamura K (1999) FGF7 and FGF10 directly induce the apical ectodermal ridge in chick embryos. Dev Biol 211:133–143 CrossRefPubMed
Metadaten
Titel
Regulation of external genitalia development by concerted actions of FGF ligands and FGF receptors
verfasst von
Yoshihiko Satoh
Ryuma Haraguchi
Tracy J. Wright
Suzanne L. Mansour
Juha Partanen
Mohammad K. Hajihosseini
Veraragavan P. Eswarakumar
Peter Lonai
Gen Yamada
Publikationsdatum
01.09.2004
Verlag
Springer-Verlag
Erschienen in
Brain Structure and Function / Ausgabe 6/2004
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-004-0419-9