Molecular Mechanisms of Early Lung Specification and Branching Morphogenesis

Pediatric Research

Volumn 57, Issue 5, 2005, Pages 26R-37R

  Warburton, David ^a   Bellusci, Saverio ^a   De Langhe, Stijn ^a   Del Moral, PIERRE MARIE ^a   Fleury, Vincent ^a   Mailleux, Arnaud ^a   Tefft, Denise ^a   Unbekandt, Mathieu ^a   Wang, Kasper ^a   Shi, Wwe ^a  

^a LABORATOIRE DE PHYSIQUE DE LA MATIÈRE CONDENSÉE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; FIBROBLAST GROWTH FACTOR; SONIC HEDGEHOG PROTEIN; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; WNT PROTEIN;

BRANCHING MORPHOGENESIS; CELL PROTECTION; CELL REGENERATION; EXTRACELLULAR MATRIX; GAS DIFFUSION; GROWTH REGULATION; HUMAN; HUMAN CELL; LUNG PARENCHYMA; MOLECULAR MECHANICS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STEREOTYPY; SURFACE PROPERTY; TISSUE SPECIFICITY; TRACHEA;

ANIMALS; CELL LINEAGE; DROSOPHILA; EPITHELIUM; ESOPHAGUS; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LARYNX; LIGANDS; LUNG; MODELS, BIOLOGICAL; MUTATION; NEOVASCULARIZATION, PHYSIOLOGIC; PEPTIDES; PROTEIN ISOFORMS; SIGNAL TRANSDUCTION; TRACHEA; TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR BETA; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WNT PROTEINS;

EID: 17844393409     PISSN: 00313998     EISSN: 15300447     Source Type: Journal    
DOI: 10.1203/01.PDR.0000159570.01327.ED     Document Type: Review

References (154)

1. Warburton D, Schwarz M, Tefft D, Flores-Delgado G, Anderson KD, Cardoso WV 2000 The molecular basis of lung morphogenesis. Mech Dev 92:55-81
2. Affolter M, Bellusci S, Itoh B, Shilo B, Thiery JP, Werb Z 2003 Tube or not tube: remodeling epithelial tissues via branching morphogenesis. Dev Cell 4:11-18
3. Rudnick D 1933 Developmental capacities of the chick lung in chorioallantoic grafts. J Exp Zool 66:125-153
4. Alescio T, Cassini A 1962 Induction in vitro of tracheal buds by pulmonary mesenchyme grafted on tracheal epithelium. J Exp Zool 150:83-94
5. Taderara JV 1967 Control of lung differentiation in vitro. Dev Biol 16:489-512
6. Spooner BS, Wessells NK 1970 Mammalian lung development: interactions in primordium formation and bronchial morphogenesis. J Exp Zool 175:445-454
7. Wessells NK 1970 Mammalian lung development: interactions in formation and morphogenesis of tracheal buds. J Exp Zool 175:455-466
8. Shannon JM 1994 Induction of alveolar type II cell differentiation in fetal tracheal epithelium by grafted distal lung mesenchyme. Dev Biol 166:600-614
9. Shannon JM, Nielsen LD, Gebb SA, Randell SH 1998 Mesenchyme specifies epithelial differentiation in reciprocal recombinants of embryonic lung and trachea. Dev Dyn 212:482-494
10. Shannon JM, Hyatt BA 2004 Epithelial-mesenchymal interactions in the developing lung. Annu Rev Physiol 66:625-645
11. Peters K, Werner S, Liao X, Wert S, Whitsett J, Williams L 1994 Targeted expression of a dominant negative FGF receptor blocks branching morphogenesis and epithelial differentiation of mouse lung. EMBO J 13:3296-3301
12. Celli G, LaRochelle WJ, Mackem S, Sharp R, Merlino G 1998 Soluble dominant-negative receptor uncovers essential roles for fibroblast growth factors in multi-organ induction and patterning. EMBO J 17:1642-1655
13. 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
14. Park WY, Miranda B, Lebeche D, Hashimoto G, Cardoso WV 1998 FGF-10 is a chemotactic factor for distal epithelial buds during development. Dev Biol 201:125-134
15. 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
16. Ang SL, Rossant J 1994 HNF-3 beta is essential or node and notochord formation in mouse development. Cell 78:561-574
17. Chisaka O, Capecchi MR 1991 Regionally restricted developmental defects resulting from targeted disruption of the mouse homeobox gene hox-1.5. Nature 350:473-479
18. Manley NR, Capecchi MR 1995 The role of Hoxa-3 in mouse thymus and thyroid development. Development 121:1989-2003
19. Aubin J, Lemieux M, Tremblay M, Berard J, Jeannotte L 1997 Early postnatal lethality in Hoxa-5 mutant mice is attributable to respiratory tract defects. Dev Biol 192:432-445
20. Kinkead R, LeBlanc M, Gulemetova R, Lalancette-Hebert M, Lemieux M, Mandeville I, Jeannotte L 2004 Respiratory adaptations to lung morphological defects in adult mice lacking Hoxa5 gene function. Pediatr Res 56:553-562
21. Chytil F 1985 Vitamin A and lung development. Pediatr Pulmonol 1(3 suppl):S115-S117
22. Mendelsohn C, Lohnes D, Decimo D, Lufkin T, LeMeur M, Chambon P, Mark M 1994 Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 120:2749-2771
23. Motoyama J, Liu J, Mo R, Ding Q, Post M, Hui CC 1998 Essential function of Gli2 and Gli3 in the formation of lung, trachea and oesophagus. Nat Genet 20:54-57
24. Desai TJ, Malpel S, Flentke GR, Smith SM, Cardoso WV 2004 Retinoic acid selectively regulates Fgf10 expression and maintains cell identity in the prospective lung field of the developing foregut. Dev Biol 273:402-415
25. Perl AK, Wert SE, Nagy A, Lobe CG, Whitsett JA 2002 Early restriction of peripheral and proximal cell lineages during formation of the lung. Proc Natl Acad Sci U S A 99:10482-10487
26. Supp DM, Witte DP, Potter SS, Brueckner M 1997 Mutation of an axonemal dynein affects left-right symmetry in inversus viscerum mice. Nature 389:963-966
27. Lin CR, Kioussi C, O’Connell S, Briata P, Szeto D, Liu F, Izpisua-Belmonte JC, Rosenfeld MG 1999 Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature 401:279-282
28. Kimura S, Hara Y, Pineau T, Fernandez-Salguero P, Fox CH, Ward JM, Gonzalez FJ 1996 The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes Dev 10:60-69
29. Minoo P, Hamdan H, Bu D, Warburton D, Stepanik P, deLemos R 1995 TTF-1 regulates lung epithelial morphogenesis. Dev Biol 172:694-698
30. Litingtung Y, Lei L, Westphal H, Chiang C 1998 Sonic hedgehog is essential to foregut development. Nat Genet 20:58-61
31. Pepicelli CV, Lewis PM, McMahon AP 1998 Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Curr Biol 8:1083-1086
32. Mahlapuu M, Enerback S, Carlsson P 2001 Haploinsufficiency of the forkhead gene Fox f1, a target for sonic hedgehog signaling, causes lung and foregut malformations. Development 128:2397-2406
33. Miller LA, Wert SE, Clark JC, Xu Y, Perl AK, Whitsett JA 2004 Role of Sonic hedgehog in patterning of tracheal-bronchial cartilage and the peripheral lung. Dev Dyn 231:57-71
34. Li Y, Zhang H, Choi SC, Litingtung Y, Chiang C 2004 Sonic hedgehog signaling regulates Gli3 processing, mesenchyme proliferation, and differentiation during mouse lung organogenesis. Dev Biol 270:214-231
35. Crisera CA, Maldonado TS, Longaker MT, Gittes GK 2000 Defective fibroblast growth factor signaling allows for nonbranching growth of the respiratory-derived fistula tract in esophageal atresia with tracheoesophageal fistula. J Pediatr Surg 35:1421-1425
36. Kim PC, Mo R, Hui Cc C 2001 Murine models of VACTERL syndrome: role of sonic hedgehog signaling pathway. J Pediatr Surg 36:381-384
37. Spilde T, Bhatia A, Ostlie D, Marosky J, Holcomb G III, Synder CL, Gittes GK 2003 A role for sonic hedgehog signaling in the pathogenesis of human tracheoesophageal fistula. J Pediatr Surg 38:465-468
38. Spilde TL, Bhatia AM, Mehta SS, Hembree MJ, Preuett BL, Ostlie DJ, Prasadan K, Li Z, Synder CL, Gittes GK 2004 Aberrant fibroblast growth factor receptor 2 signalling in esophageal atresia in tracheoesophageal fistula. J Pediatr Surg 39:537-539
39. Cardoso WV 2000 Lung morphogenesis revisted: old facts, current ideas. Dev Dyn 219:121-130
40. Hogan BL 1999 Morphogenesis. Cell 96:225-233
41. Warburton D, Bellusci S 2004 The molecular genetics of lung morphogenesis and injury repair. Paediatr Respir Rev 5(suppl A):S283-S287
42. Michos O, Panman L, Vintersten K, Beier K, Zeller R, Zuniga A 2004 Gremlin-mediated BMP antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development 131:3401-3410
43. Weaver M, Yingling JM, Dunn NR, Bellusci S, Hogan BL 1999 Bmp signaling regulates proximal-distal differentiation of endoderm in mouse lung development. Development 126:4005-4015
44. Bellusci S, Henderson R, Winnier G, Oikawa T, Hogan BL 1996 Evidence from normal expression and targeted misexpression that bone morphogenetic protein-4 (Bmp-4) plays a role in mouse embryonic lung morphogenesis. Development 122:1693-1702
45. Takahashi H, Ikeda T 1996 Transcripts for two members of the transforming growth factor superfamily BMP-3 and BMP-7 are expressed in developing rat embryos. Dev Dyn 207:439-449
46. King JA, Marker PC, Seung KJ, Kingsley DM 1994 BMP5 and the molecular, skeletal, and soft-tissue alterations in short ear mice. Dev Biol 166:112-122
47. Chen CK, Kuhnlein RP, Eulenberg KG, Vincent S, Affolter M, Schuh R 1998 The transcription factors KNIRPS and KNIRPS RELATED control cell migration and branch morphogenesis during Drosophila tracheal development. Development 125:4959-4968
48. Ribeiro C, Ebner A, Affolter M 2002 in vivo imaging reveals different cellular functions for FGF and Dpp signaling in tracheal branching morphogenesis. Dev Cell 2:677-683
49. Lane KB, Machado RD, Pauciulo MW, Thomson JR, Phillips JA III, Loyd JE, Nichols WC, Trembath RC 2000 Heterozygous germline mutations in BMPR2, encoding a TGF-beta receptor, cause familial primary pulmonary hypertension. The International PPH Consortium. Nat Genet 26:81-84
50. Miettinen PJ, Berger JE, Meneses J, Phung Y, Pedersen RA, Werb Z, Derynck R 1995 Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature 376:337-341
51. Miettinen PJ, Warburton D, Bu D, Zhao JS, Berger JE, Minoo P, Koivisto T Allen L, Dobbs L, Werb Z, Derynck R 1997 Impaired lung branching morphogenesis in the absence of functional EGF receptor. Dev Biol 186:224-236
52. Goldin GV, Opperman LA 1980 Induction of supernumerary tracheal buds and the stimulation of DNA synthesis in the embryonic chick lung and trachea by epidermal growth factor. J Embryol Exp Morphol 60:235-243
53. Warburton D, Seth R, Shum L, Horcher PG, Hall FL, Werb Z, Slavkin HC 1992 Epigenetic role of epidermal growth factor expression and signalling in embryonic mouse lung morphogenesis. Dev Biol 149:123-133
54. Seth R, Shum L, Wu F, Wuenschell C, Hall FL, Slavkin HC, Warburton D 1993 Role of epidermal growth factor expression in early mouse embryo lung branching morphogenesis in culture: antisense oligodeoxynucleotide inhibitory strategy. Dev Biol 158:555-559
55. Zhao J, Chen H, Wang YL, Warburton D 2001 Abrogation of tumor necrosis factor-alpha converting enzyme inhibits embryonic lung morphogenesis in culture. Int J Dev Biol 45:623-631
56. Bellusci S, Grindley J, Emoto H, Itoh N, Hogan BL 1997 Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 124:4867-4878
57. Weaver M, Dunn NR, Hogan BL 2000 BMP4 and Fgf10 play opposing roles during lung bud morphogenesis. Development 127:2695-2704
58. Tefft JD, Lee M, Smith S, Lienwand M, Zhao J, Bringas P Jr, Crowe DL, Warburton D 1999 Conserved function of mSpry-2, a murine homolog of Drosophila sprouty, which negatively modulates respiratory organogenesis. Curr Biol 9:219-222
59. Lebeche D, Malpel S, Cardoso WV 1999 Fibroblast growth factor interactions in the developing lung. Mech Dev 86:125-136
60. Ornitz DM, Xu J, Colvin JS, McEwen DG, MacArthur CA, Coulier E, Gao G, Goldfarb M 1995 Receptor specificity of the fibroblast growth factor family. J Biol Chem 271:15292-15297
61. Peters K, Werner S, Liao X, Wert S, Whitsett J, Williams L 1994 Targeted expression of a dominant negative FGF receptor block branching morphogenesis and epithelial differentiation of the mouse lung. EMBO J 13:3296-3301
62. Arman E, Haffner-Krausz R, Chen Y, Heath JK, Lonai P 1998 Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc Natl Acad Sci U S A 95:5082-5087
63. 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
64. De Moerlooze L, Spencer-Dene B, Revest J, Hajihosseini M, RosewelI I, Dickson C 2000 An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signaling during mouse organogenesis. Development 127:482-492
65. 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
66. Hokuto I, Perl AK, Whitsett JA 2003 Prenatal, but not postnatal, inhibition of fibroblast growth factor receptor signaling causes emphysema. J Biol Chem 278:415-421
67. Ornitz DM, Itoh N 2001 Fibroblast growth factors. Genome Biol 2:REVIEWS3005
68. Chailley-Heu B, Boucherat O, Barlier-Mur AM, Bourbon JR 2004 FGF18 is up-regulated in the postnatal rat lung and enhances elastogenesis in myofibroblasts. Am J Physiol Lung Cell Mol Physiol 288:L43-L51
69. Park WY, Miranda B, Lebeche D, Hashimoto G, Cardoso WV 1998 FGF-10 is a chemotactic factor for distal epithelial buds during development. Dev Biol 201:125-134
70. 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
71. 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
72. 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 organ development. Biochem Biophys Res Commun 277:643-649
73. Mailleux AA, Tefft D, Ndiaye D, Itoh N, Thiery JP, Warburton D, Bellusci S 2001 Evidence that SPROUTY2 functions as an inhibitor of mouse embryonic lung growth and morphogenesis. Mech Dev 102:82-94
74. Sutherland D, Samakovlis C, Krasnow MA 1996 branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 87:1091-1101
75. Ahmad SM, Baker BS 2002 Sex-specific deployment of FGF signaling in Drosophila recruits mesodermal cells into the male genital imaginal disc. Cell 109:651-661
76. Hacohen N, Kramer S, Sutherland D, Hiromi Y, Krasnow MA 1998 sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92:253-263
77. Casci T, Vinos J, Freeman M 1999 Sprouty, an intracellular inhibitor of Ras signaling. Cell 96:655-665
78. Tefft D, Lee M, Smith S, Crowe DL, Bellusci S, Warburton D 2002 mSprouty2 inhibits FGF10-activated MAP kinase by different binding to upstream target proteins. Am J Physiol Lung Cell Mol Physiol 283:L700-L706
79. Hadari YR, Kouhara H, Lax I, Schlessinger J 1998 Binding of Shp2 tyrosine phosphatase to FRS2 is essential for fibroblast growth factor-induced PC12 cell differentiation. Mol Cell Biol 18:3966-3973
80. Schaeffer HJ, Weber MJ 1999 Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol Cell Biol 19:2435-2444
81. Minowada G, Jarvis LA, Chi CL, Neubuser A, Sun X, Hacohen N, Krasnow MA, Martin GR 1999 Vertebrate Sprouty genes are induced by FGF signaling and cause chondrodysplasia when overexpressed. Development 126:4465-4475
82. Lee MK, Zhao J, Smith SM, Tefft JD, Bringas P, Hwang C, Warburton D 1998 The Shc66 and 46 kD isoforms are differentially downregulated at parturition in the fetal mouse lung. Pediatr Res 44:850-859
83. Lim J, Wong ES, Ong SH, Yusoff P, Low BC, Guy GR 2000 Sprouty proteins are targeted to membrane ruffles upon growth factor receptor tyrosine kinase activation. Identification of a novel translocation domain. J Biol Chem 275:32837-32845
84. Yigzaw Y, Cartin L, Pierre S, Scholich K, Patel TB 2001 The C terminus of sprouty is important for modulation of cellular migration and proliferation. J Biol Chem 276:22742-22747
85. Wong ES, Lim J, Low BC, Chen Q, Guy GR 2001 Evidence for direct interaction between Sprouty and Cbl. J Biol Chem 276:5866-5875
86. Hashimoto S, Nakano H, Singh G, Katyal S 2002 Expression of Spred and Sprouty in developing rat lung. Mech Dev 119(suppl 1):S303-S309
87. Miyoshi K, Wakioka T, Nishinakamura H, Kamio M, Yang L, Inoue M, Hasegawa M, Yonemitsu Y, Komiya S, Yoshimura A 2004 The Sprouty-related protein, Spred, inhibits cell motility, metastasis, and Rho-mediated actin reorganization. Oncogene 23:5567-5576
88. Nobuhisa I, Kato R, Inoue H, Takizawa M, Okita K, Yoshimura A, Taga T 2004 Spred-2 suppresses aorta-gonad-mesonephros hematopoiesis by inhibiting MAP kinase activation. J Exp Med 199:737-742
89. Kato R, Nonami A, Taketomi T, Wakioka T, Kuroiwa A, Matsuda Y, Yoshimura A 2003 Molecular cloning of mammalian Spred-3 which suppresses tyrosine kinase-mediated Erk activation. Biochem Biophys Res Commun 302:767-772
90. Smith CI, Webster EH, Nathanson MA, Searls RI, Hilfer SR 1990 Altered patterns of proteoglycan deposition during maturation of the fetal mouse lung. Cell Differ Dev 32:83-96
91. Spooner BS, Bassett KE, Spooner BS Jr 1993 Embryonic lung morphogenesis in organ culture: experimental evidence of a proteoglycan function in the extracellular matrix. Trans Kans Acad Sci 96:46-55
92. Toriyama K, Muramatsu H, Hoshino T, Torii S, Muramatsu T 1997 Evaluation of heparin-binding growth factors in rescuing morphogenesis of heparitinase-treated mouse embryonic lung explants. Differentiation 61:161-167
93. Izvolsky KI, Zhong L, Wei L, Yu Q, Nugent MA, Cardoso WV 2003 Heparan sulfates expressed in the distal lung are required for Fgf10 binding to the epithelium and for airway branching. Am J Physiol Lung Cell Mol Physiol 285:L838-L846
94. Izvolsky KI, Shoykhet D, Yang Y, Yu Q, Nugent MA, Cardoso WV 2003 Heparan sulfate-FGF10 interactions during lung morphogenesis. Dev Biol 258:185-200
95. Shannon JM, McCormick-Shannon K, Burhans MS, Shangguan X, Srivastava K, Hyatt BA 2003 Chondroitin sulfate proteoglycans are required for lung growth and morphogenesis in vitro. Am J Physiol Lung Cell Mol Physiol 285:L1323-L1336
96. van Tuyl M, Post M 2000 From fruitflies to mammals: mechanisms of signaling via the Sonic hedgehog pathway in lung development. Respir Res 1:30-35
97. Pepicelli CV, Lewis PM, McMahon AP 1998 Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Curr Biol 8:1083-1086
98. Bellusci S, Furuta Y, Rush MG, Henderson R, Winnier G, Hogan BL 1997 Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 124:53-63
99. Chuang PT, McMahon AP 1999 Vertebrate Hedgehog signaling modulated by induction of a Hedgehog-binding protein. Nature 397:617-621
100. Massague J 1998 TGF-beta signal transduction. Ann Rev Biochem 67:753-791
101. Pelton RW, Saxena B, Jones M, Moses HL, Gold LI 1991 Immunohistochemical localization of TGF beta 1, TGF beta 2, a TGF beta 3 in the mouse embryo: expression patterns suggest multiple roles during embryonic development. J Cell Biol 115:1091-1105
102. Millan FA, Denhez F, Kondaiah P, Akhurst RJ 1991 Embryonic gene expression patterns of TGF beta 1, beta 2 and beta 3 suggest different developmental functions in vivo. Development 111:131-143
103. Schmid P, Cox D, Bilbe G, Maier R, McMaster GK 1991 Differential expression of TGF beta 1, beta 2 and beta 3 genes during mouse embryogenesis. Development 111:117-130
104. McLennan IS, Poussart Y, Koishi K 2000 Development of skeletal muscles in transforming growth factor-beta 1 (TGF-beta1) null-mutant mice. Dev Dyn 217:250-256
105. Bragg AD, Moses HL, Serra R 2001 Signaling to the epithelium is not sufficient to mediate all of the effects of transforming growth factor beta and bone morphogenetic protein 4 on murine embryonic lung development. Mech Dev 109:13-26
106. Bartram U, Molin DG, Wisse LJ, Mohamad A, Sanford LP, Doetschman T, Speer C, Poelmann RE, Gittenberger-de Groot AC 2001 Double-outlet right ventricle and overriding tricuspid valve reflect disturbances of looping, myocardialization, endocardial cushion differentiation, and apoptosis in TGF-beta(2)-knockout mice. Circulation 103:2745-2752
107. Kaartinen V, Voncken W, Shuler C, Warburton D, Bu D, Heisterkamp N, Groffen J 1995 Abnormal lung development and cleft palate in mice lacking TGF-beta 3 indicates defects of epithelial-mesenchymal interaction. Nat Genet 11:415-421
108. Buckley S, Bui KC, Hussain M, Warburton D 1996 Dynamics of TGF-beta 3 peptide activity during rat alveolar epithelial cell proliferative recoevery from acute hyperoxia. Am J Physiol 271:L54-L60
109. Zhao J, Sime PJ, Bringas P Jr, Tefft JD, Buckley S, Bu D, Gauldie J, Warburton D 1999 Spatial-specific TGF-beta1 adenoviral expression determines morphogenetic phenotypes in embryonic mouse lung. Eur J Cell Biol 78:715-725
110. Zhou L, Dey CR, Wert SE, Whitsett JA 1996 Arrested lung morphogenesis in transgenic mice bearing an SP-C-TGF-beta 1 chimeric gene. Dev Biol 175:227-228
111. Serra R, Pelton RW, Moses HL 1994 TGF beta 1 inhibits branching morphogenesis and N-myc expression in lung bud organ cultures. Development 120:2153-2161
112. Zhao J, Bu D, Lee M, Slavkin HC, Hall FL, Warburton D 1996 Abrogation of transforming growth factor-beta type II receptor stimulates embryonic mouse lung branching morphogenesis in culture. Dev Biol 180:242-257
113. Zhao J, Sime PJ, Bringas P Jr., Gauldie J, Warburton D 1999 Adenovirus-mediated decorin gene transfer prevents TGF-beta1-induced inhibition of lung morphogenesis. Am J Physiol 277:L412-L422
114. Zhao J, Crowe DL, Castillo C, Wuenschell C, Chai Y, Warburton D 2000 Smad7 is a TGF-beta inducible attenuator of Smad2/3-mediated inhibition of embryonic lung morphogenesis. Mech Dev 93:71-81
115. Zhao J, Lee M, Smith S, Warburton D 1998 Abrogation of Smad3 and Smad2 or of Smad 4 gene expression positively regulates murine embryonic lung branching mophogenesis in culture. Dev Biol 194:182-195
116. Zhao J, Shi W, Chen H, Warburton D 2000 Smad7 and Smad6 differentially modulates transforming growth factor beta-induced inhibition of embryonic lung morphogenesis. J Biol Chem 275:23992-23997
117. Gauldie J, Galt T, Bonniaud P, Robbins C, Kelly M, Warburton D 2003 Transfer of the active form of transforming growth factor-beta 1 gene to newborn rat lung induces changes consistent with bronchopulmonary dysplasia. Am J Pathol 163:2575-2584
118. Sime PJ, Xing Z, Graham FL, Csaky KG, Gauldie J 1997 Adenovector-mediated gene transfer of active transforming growth factor-beta 1 induces prolonged severe fibrosis in rat lung. J Clin Invest 100:768-776
119. Zhao J, Shi W, Wang YL, Chen H, Bringas P Jr., Datto MB, Frederick JP, Wang XF, Warburton D 2002 Smad3 deficiency attenuates bleomycin-induced pulmonary fibrosis in mice. Am J Physiol Lung Cell Mol Physiol 282:L585-L593
120. Gebb SA, Shannon JM 2002 Tissue interactions mediate early events in pulmonary vasculogenesis. Dev Dyn 217:159-169
121. Miquerol L, Gertsenstein M, Harpal K, Rossant J, Nagy A 1999 Multiple developmental roles of VEGF suggested by a LacZ-tagged allele. Dev Biol 212:307-322
122. Acarregui MJ, Penisten SC, Goss KL, Ramirez K, Snyder JM 1999 Vascular endothelial growth factor gene expression in human fetal lung in vitro. Am J Respir Cell Mol Biol 20:14-23
123. Maede S, Suzuki S, Suzuki T, Endo M, Moriya T, Chida M, Kondo T, Sasano H 2002 Analysis of intrapulmonary vessels and epithelial-endothelial interactions in the human developing lung. Lab Invest 82:293-301
124. Brown KR, England KM, Goss KL, Snyder JM, Acarregui MJ 2001 VEGF induces airway epithelial cell proliferation in human fetal lung in vitro. Am J Physiol Lung Cell Mol Physiol 281:L1001-L1010
125. Kasahara Y, Tuder RM, Taraseviciene-Stewart L, Le Cras TD, Abman S, Hirth PK, Waltenberger J, Voelkel NF 2000 Inhibition of VEGF receptors causes lung cell apoptosis and emphysema. J Clin Invest 106:1311-1319
126. Zeng X, Wert SE, Federici R, Peters KG, Whitsett JA 1998 VEGF enhances pulmonary vasculogenesis and disrupts lung morphogenesis in vivo. Dev Dyn 211:215-227
127. Gerber HP, Hillan KJ, Ryan AM, Kowalski J, Keller GA, Rangell L, Wright BD, Radtke F, Aguet M, Ferrara N 1999 VEGF is required for growth and survival in neonatal mice. Development 126:1149-1159
128. Corne J, Chupp G, Lee CG, Homer RJ, Zhu Z, Chen Q, Ma B, Du Y, Roux F, McArdle J, Waxman AB, Elias JA 2002 IL-13 stimulates vascular endothelial cell growth factor and protects against hyperoxic acute lung injury. J Clin Invest 106:783-791
129. Compernolle V, Brusselmans K, Acker T, Hoet P, Tjwa M, Beck H, Plaisance S, Dor Y, Keshet E, Lupu F, Nemery B, Dewerchin M, Van Veldhoven P, Plate K, Moons L, Collen D, Carmeliet P 2002 Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med 8:702-710
130. Farnebo F, Piehl F, Lagercrantz J 1999 Restricted expression pattern of vegf-d in the adult and fetal mouse: high expression in the embryonic lung. Biochem Biophys Res Commun 257:891-894
131. Makinen T, Jussila L, Veikkola T, Karpanen T, Kettunen MI, Pulkkanen KJ, Kauppinen R, Jackson DG, Kubo H, Nishikawa S, Yla-Herttuala S, Alitalo K 2001 Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3. Nat Med 7:199-205
132. Veikkola T, Jussila L, Makinen T, Karpanen T, Jeltsch M, Petrova TV, Kubo H, Thurston G, McDonald DM, Achen MG, Stacker SA, Alitalo K 2001 Signalling via vascular endothelial growth factor receptor-3 is sufficient for lymphangiogenesis in transgenic mice. EMBO J 20:1223-1231
133. Cao Y, Linden P, Farnebo J, Cao R, Eriksson A, Kumar V, Qi JH, Claesson-Welsh L, Alitalo K 1998 Vascular endothelial growth factor C induces angiogenesis in vivo. Proc Natl Acad Sci U S A 95:14389-14394
134. Pinson KI, Brennan J, Monkley S, Avery BJ, Skarnes WC 2000 An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 407:535-538
135. Tamai K, Semenov M, Kato Y, Spokony R, Liu C, Katsuyama Y, Hess F, Saint-Jeannet JP, He X 2000 LDL-receptor-related proteins in Wnt signal transduction. Nature 407:530-535
136. Wehrli M, Dougan ST, Caldwell K, O’Keefe L, Schwartz S, Vaizel-Ohayon D, Schejter E, Tomlinson A, DiNardo S 2000 arrow encodes an LDL-receptor-related protein essential for Wingless signalling. Nature 407:527-530
137. Heisenberg CP, Tada M, Rauch GJ, Saude L, Concha ML, Geisler R, Stemple DL, Smith JC, Wilson SW 2000 Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405:76-81
138. Torres MA, Yang-Snyder JA, Purcell SM, DeMarais AA, McGrew LL, Moon RT 1996 Activities of the Wnt-1 class of secreted signaling factors are antagonized by the Wnt-5A class and by a dominant negative cadherin in early Xenopus development. J Cell Biol 133:1123-1137
139. 2+ signaling. Mech Dev 106:61-76
140. Ishitani T, Kishida S, Hyodo-Miura J, Ueno N, Yasuda J, Waterman M, Shibuya H, Moon RT, Ninomiya-Tsuji J, Matsumoto K 2003 The TAK1-NLK mitogen-activated protein kinase cascade functions in the Wnt-5a/Ca(2+) pathway to antagonize Wnt/beta-catenin signaling. Mol Cell Biol 23:131-139
141. Mao B, Wu W, Davidson G, Marhold J, Li M, Mechler BM, Delius H, Hoppe D, Stannek P, Walter C, Glinka A, Niehrs C 2002 Kremen proteins are Dickkopf receptors that regulate Wnt/beta-catenin signalling. Nature 417:664-667
142. Kawano Y, Kypta R 2003 Secreted antagonists of the Wnt signaling pathway. J Cell Sci 116:2627-2634
143. Mao B, Niehrs C 2003 Kremen2 modulates Dickkopf2 activity during Wnt/LRP6 signaling. Gene 302:179-183
144. Hoang BH, Kubo T, Healey JH, Yang R, Nathan SS, Kolb EA, Mazza B, Meyers PA, Gorlick R 2004 Dickkopf 3 inhibits invasion and motility of Saos-2 osteosarcoma cells by modulating the Wnt-beta-catenin pathway. Cancer Res 64:2734-2739
145. Tebar M, Destree O, de Vree WJ, Ten Have-Opbroek AA 2001 Expression of Tcf/Lef and sFrp and localization of beta-catenin the developing mouse lung. Mech Dev 109:437-440
146. DasGupta R, Fuchs E 1999 Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126:4557-4568
147. Maretto S, Cordenonsi M, Dupont S, Braghetta P, Broccoli V, Hassan AB, Volpin D, Bressan GM, Piccolo S 2003 Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci U S A 100:3299-3304
148. Derynck R, Zhang YE 2003 Smad-dependent and Smad-independent pathways in TGF-beta family signaling. Nature 425:577-584
149. De Langhe S, Sala FG, Del Moral P-M, Fairbanks TJ, Yamada KM, Warburton D, Burns RC, Bellusci S 2005 Dickopf-1 (DKK1) reveals that fibronectin is a major target of Wnt signaling in branching morphogenesis of the mouse embryonic lung. Dev Biol 277:316-331
150. Mucenski ML, Wert SE, Nation JM, Loudy DE, Huelsken J, Birchmeier W, Morrisey EE, Whitsett JA 2003 Beta-Catenin is required for specification of proximal/distal cell fate during lung morphogenesis. J Biol Chem 278:40231-40238
151. Okubo T, Hogan BL 2004 Hyperactive Wnt signaling changes the developmental potential of embryonic lung endoderm. J Biol 3:11
152. Fleury V 1999 Two symmetries linking biological and physical branching morphogenesis. In: Fleury V, Gouyet J-F, Leonetti M (eds) Branching in Nature: Dynamics and Morphogenesis of Branching Structures, from Cell to River Networks. Springer, Paris
153. Blewett CJ, Zgleszewski SE, Chinoy MR, Krummel TM, Cilley RE 1996 Bronchial ligation enhances murine fetal lung development in whole-organ culture. J Pediatr Surg 31:869-877
154. Liu Y, Stein E, Oliver T, Li Y, Brunken WJ, Koch M, Tessier-Lavigne M, Hogan BL 2004 Novel role for Netrins in regulating epithelial behavior during lung branching morphogenesis. Curr Biol 14:897-905