Wnt and FGF mediated epithelial-mesenchymal crosstalk during lung development

Developmental Dynamics

Volumn 244, Issue 3, 2015, Pages 342-366

  Volckaert, Thomas ^a,c,d   De Langhe, Stijn P ^a,b  

^a DEPARTMENT OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

Differentiation; Epithelium; Fgf10; Hippo; Progenitor; Wnt

Indexed keywords

BETA CATENIN; FIBROBLAST GROWTH FACTOR 10; WNT PROTEIN; FIBROBLAST GROWTH FACTOR;

CELL ADHESION; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL REGENERATION; EPITHELIAL MESENCHYMAL TRANSITION; LUNG ALVEOLUS EPITHELIUM; LUNG DEVELOPMENT; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CELL LINEAGE; CYTOLOGY; EMBRYOLOGY; HUMAN; LUNG; METABOLISM; PHYSIOLOGY; WNT SIGNALING PATHWAY;

AMPHIBIA; MAMMALIA;

ANIMALS; CELL LINEAGE; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROBLAST GROWTH FACTORS; HUMANS; LUNG; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84924137925     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.24234     Document Type: Review

References (268)

1. Aberle H, Bauer A, Stappert J, Kispert A, Kemler R. 1997. beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J 16:3797-3804.
2. Abler LL, Mansour SL, Sun X. 2009. Conditional gene inactivation reveals roles for Fgf10 and Fgfr2 in establishing a normal pattern of epithelial branching in the mouse lung. Dev Dyn 238:1999-2013.
3. Alanis DM, Chang DR, Akiyama H, Krasnow MA, Chen J. 2014. Two nested developmental waves demarcate a compartment boundary in the mouse lung. Nat Commun 5:3923.
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. Ameri J, Stahlberg A, Pedersen J, Johansson JK, Johannesson MM, Artner I, Semb H. 2010. FGF2 specifies hESC-derived definitive endoderm into foregut/midgut cell lineages in a concentration-dependent manner. Stem Cells 28:45-56.
6. 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.
7. Arora R, Metzger RJ, Papaioannou VE. 2012. Multiple roles and interactions of Tbx4 and Tbx5 in development of the respiratory system. PLoS Genet 8:e1002866.
8. Azzolin L, Zanconato F, Bresolin S, Forcato M, Basso G, Bicciato S, Cordenonsi M, Piccolo S. 2012. Role of TAZ as mediator of Wnt signaling. Cell 151:1443-1456.
9. Azzolin L, Panciera T, Soligo S, Enzo E, Bicciato S, Dupont S, Bresolin S, Frasson C, Basso G, Guzzardo V, Fassina A, Cordenonsi M, Piccolo S. 2014. YAP/TAZ incorporation in the beta-catenin destruction complex orchestrates the Wnt response. Cell 158:157-170.
10. Bachelder RE, Yoon SO, Franci C, de Herreros AG, Mercurio AM. 2005. Glycogen synthase kinase-3 is an endogenous inhibitor of Snail transcription: implications for the epithelial-mesenchymal transition. J Cell Biol 168:29-33.
11. Bao J, Zheng JJ, Wu D. 2012. The structural basis of DKK-mediated inhibition of Wnt/LRP signaling. Sci Signal 5:pe22.
12. Barkauskas CE, Cronce MJ, Rackley CR, Bowie EJ, Keene DR, Stripp BR, Randell SH, Noble PW, Hogan BL. 2013. Type 2 alveolar cells are stem cells in adult lung. J Clin Invest 123:3025-3036.
13. Barry ER, Morikawa T, Butler BL, Shrestha K, de la Rosa R, Yan KS, Fuchs CS, Magness ST, Smits R, Ogino S, Kuo CJ, Camargo FD. 2013. Restriction of intestinal stem cell expansion and the regenerative response by YAP. Nature 493:106-110.
14. Bellusci S, Henderson R, Winnier G, Oikawa T, Hogan BL. 1996. Evidence from normal expression and targeted misexpression that bone morphogenetic protein (Bmp-4) plays a role in mouse embryonic lung morphogenesis. Development 122:1693-1702.
15. 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.
16. Borges M, Linnoila RI, van de Velde HJ, Chen H, Nelkin BD, Mabry M, Baylin SB, Ball DW. 1997. An achaete-scute homologue essential for neuroendocrine differentiation in the lung. Nature 386:852-855.
17. Boucherat O, Nadeau V, Berube-Simard FA, Charron J, Jeannotte L. 2014. Crucial requirement of ERK/MAPK signaling in respiratory tract development. Development 141:3197-3211.
18. Bovolenta P, Esteve P, Ruiz JM, Cisneros E, Lopez-Rios J. 2008. Beyond Wnt inhibition: new functions of secreted Frizzled-related proteins in development and disease. J Cell Sci 121:737-746.
19. Brembeck FH, Schwarz-Romond T, Bakkers J, Wilhelm S, Hammerschmidt M, Birchmeier W. 2004. Essential role of BCL9-2 in the switch between beta-catenin's adhesive and transcriptional functions. Genes Dev 18:2225-2230.
20. Cabrita MA, Christofori G. 2008. Sprouty proteins, masterminds of receptor tyrosine kinase signaling. Angiogenesis 11:53-62.
21. Carraro G, Shrestha A, Rostkovius J, Contreras A, Chao CM, El Agha E, Mackenzie B, Dilai S, Guidolin D, Taketo MM, Gunther A, Kumar ME, Seeger W, De Langhe S, Barreto G, Bellusci S. 2014. miR-142-3p balances proliferation and differentiation of mesenchymal cells during lung development. Development 141:1272-1281.
22. Chang DR, Martinez Alanis D, Miller RK, Ji H, Akiyama H, McCrea PD, Chen J. 2013. Lung epithelial branching program antagonizes alveolar differentiation. Proc Natl Acad Sci USA 110:18042-18051.
23. Chellaiah AT, McEwen DG, Werner S, Xu J, Ornitz DM. 1994. Fibroblast growth factor receptor (FGFR) 3. Alternative splicing in immunoglobulin-like domain III creates a receptor highly specific for acidic FGF/FGF-1. J Biol Chem 269:11620-11627.
24. Chen C, Chen H, Sun J, Bringas P, Jr., Chen Y, Warburton D, Shi W. 2005. Smad1 expression and function during mouse embryonic lung branching morphogenesis. Am J Physiol Lung Cell Mol Physiol 288:L1033-1039.
25. Chen F, Desai TJ, Qian J, Niederreither K, Lu J, Cardoso WV. 2007. Inhibition of Tgf beta signaling by endogenous retinoic acid is essential for primary lung bud induction. Development 134:2969-2979.
26. Chen F, Cao Y, Qian J, Shao F, Niederreither K, Cardoso WV. 2010. A retinoic acid-dependent network in the foregut controls formation of the mouse lung primordium. J Clin Invest 120:2040-2048.
27. Chen J, Krasnow MA. 2012. Integrin Beta 1 suppresses multilayering of a simple epithelium. PLoS One 7:e52886.
28. Choi HJ, Huber AH, Weis WI. 2006. Thermodynamics of beta-catenin-ligand interactions: the roles of the N- and C-terminal tails in modulating binding affinity. J Biol Chem 281:1027-1038.
29. Chung C, Kim T, Kim M, Song H, Kim TS, Seo E, Lee SH, Kim H, Kim SK, Yoo G, Lee DH, Hwang DS, Kinashi T, Kim JM, Lim DS. 2013. Hippo-Foxa2 signaling pathway plays a role in peripheral lung maturation and surfactant homeostasis. Proc Natl Acad Sci USA 110:7732-7737.
30. Cohen ED, Wang Z, Lepore JJ, Lu MM, Taketo MM, Epstein DJ, Morrisey EE. 2007. Wnt/beta-catenin signaling promotes expansion of Isl-1-positive cardiac progenitor cells through regulation of FGF signaling. J Clin Invest 117:1794-1804.
31. Cohen ED, Ihida-Stansbury K, Lu MM, Panettieri RA, Jones PL, Morrisey EE. 2009. Wnt signaling regulates smooth muscle precursor development in the mouse lung via a tenascin C/PDGFR pathway. J Clin Invest 119:2538-2549.
32. Colvin JS, Feldman B, Nadeau JH, Goldfarb M, Ornitz DM. 1999. Genomic organization and embryonic expression of the mouse fibroblast growth factor 9 gene. Dev Dyn 216:72-88.
33. Colvin JS, White AC, Pratt SJ, Ornitz DM. 2001. Lung hypoplasia and neonatal death in Fgf9-null mice identify this gene as an essential regulator of lung mesenchyme. Development 128:2095-2106.
34. Conacci-Sorrell M, Simcha I, Ben-Yedidia T, Blechman J, Savagner P, Ben-Ze'ev A. 2003. Autoregulation of E-cadherin expression by cadherin-cadherin interactions: the roles of beta-catenin signaling, Slug, and MAPK. J Cell Biol 163:847-857.
35. Cordenonsi M, Zanconato F, Azzolin L, Forcato M, Rosato A, Frasson C, Inui M, Montagner M, Parenti AR, Poletti A, Daidone MG, Dupont S, Basso G, Bicciato S, Piccolo S. 2011. The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell 147:759-772.
36. Crawford HC, Fingleton BM, Rudolph-Owen LA, Goss KJ, Rubinfeld B, Polakis P, Matrisian LM. 1999. The metalloproteinase matrilysin is a target of beta-catenin transactivation in intestinal tumors. Oncogene 18:2883-2891.
37. Cruciat CM, Niehrs C. 2013. Secreted and transmembrane wnt inhibitors and activators. Cold Spring Harb Perspect Biol 5:a015081.
38. Dang TP, Eichenberger S, Gonzalez A, Olson S, Carbone DP. 2003. Constitutive activation of Notch3 inhibits terminal epithelial differentiation in lungs of transgenic mice. Oncogene 22:1988-1997.
39. Daniely Y, Liao G, Dixon D, Linnoila RI, Lori A, Randell SH, Oren M, Jetten AM. 2004. Critical role of p63 in the development of a normal esophageal and tracheobronchial epithelium. Am J Physiol Cell Physiol 287:C171-181.
40. Davidson G, Wu W, Shen J, Bilic J, Fenger U, Stannek P, Glinka A, Niehrs C. 2005. Casein kinase 1 gamma couples Wnt receptor activation to cytoplasmic signal transduction. Nature 438:867-872.
41. De Craene B, Berx G. 2013. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer 13:97-110.
42. De Langhe SP, Sala FG, Del Moral PM, Fairbanks TJ, Yamada KM, Warburton D, Burns RC, Bellusci S. 2005. Dickkopf-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.
43. De Langhe SP, Carraro G, Warburton D, Hajihosseini MK, Bellusci S. 2006. Levels of mesenchymal FGFR2 signaling modulate smooth muscle progenitor cell commitment in the lung. Dev Biol 299:52-62.
44. De Langhe SP, Carraro G, Tefft D, Li C, Xu X, Chai Y, Minoo P, Hajihosseini MK, Drouin J, Kaartinen V, Bellusci S. 2008. Formation and differentiation of multiple mesenchymal lineages during lung development is regulated by beta-catenin signaling. PLoS One 3:e1516.
45. De Moerlooze L, Spencer-Dene B, Revest JM, 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.
46. del Moral PM, De Langhe SP, Sala FG, Veltmaat JM, Tefft D, Wang K, Warburton D, Bellusci S. 2006. Differential role of FGF9 on epithelium and mesenchyme in mouse embryonic lung. Dev Biol 293:77-89.
47. 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.
48. Desai TJ, Chen F, Lu J, Qian J, Niederreither K, Dolle P, Chambon P, Cardoso WV. 2006. Distinct roles for retinoic acid receptors alpha and beta in early lung morphogenesis. Dev Biol 291:12-24.
49. Desai TJ, Brownfield DG, Krasnow MA. 2014. Alveolar progenitor and stem cells in lung development, renewal and cancer. Nature 507:190-194.
50. Deutsch G, Jung J, Zheng M, Lora J, Zaret KS. 2001. A bipotential precursor population for pancreas and liver within the embryonic endoderm. Development 128:871-881.
51. Dixit R, Ai X, Fine A. 2013. Derivation of lung mesenchymal lineages from the fetal mesothelium requires hedgehog signaling for mesothelial cell entry. Development 140:4398-4406.
52. Domyan ET, Sun X. 2011. Patterning and plasticity in development of the respiratory lineage. Dev Dyn 240:477-485.
53. Domyan ET, Ferretti E, Throckmorton K, Mishina Y, Nicolis SK, Sun X. 2011. Signaling through BMP receptors promotes respiratory identity in the foregut via repression of Sox2. Development 138:971-981.
54. Drees F, Pokutta S, Yamada S, Nelson WJ, Weis WI. 2005. Alpha-catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. Cell 123:903-915.
55. Eblaghie MC, Reedy M, Oliver T, Mishina Y, Hogan BL. 2006. Evidence that autocrine signaling through Bmpr1a regulates the proliferation, survival and morphogenetic behavior of distal lung epithelial cells. Dev Biol 291:67-82.
56. El Agha E, Al Alam D, Carraro G, MacKenzie B, Goth K, De Langhe SP, Voswinckel R, Hajihosseini MK, Rehan VK, Bellusci S. 2012. Characterization of a novel fibroblast growth factor 10 (Fgf10) knock-in mouse line to target mesenchymal progenitors during embryonic development. PLoS One 7:e38452.
57. El Agha E, Herold S, Al Alam D, Quantius J, MacKenzie B, Carraro G, Moiseenko A, Chao CM, Minoo P, Seeger W, Bellusci S. 2014. Fgf10-positive cells represent a progenitor cell population during lung development and postnatally. Development 141:296-306.
58. Fang D, Hawke D, Zheng Y, Xia Y, Meisenhelder J, Nika H, Mills GB, Kobayashi R, Hunter T, Lu Z. 2007. Phosphorylation of beta-catenin by AKT promotes beta-catenin transcriptional activity. J Biol Chem 282:11221-11229.
59. Finch PW, Cunha GR, Rubin JS, Wong J, Ron D. 1995. Pattern of keratinocyte growth factor and keratinocyte growth factor receptor expression during mouse fetal development suggests a role in mediating morphogenetic mesenchymal-epithelial interactions. Dev Dyn 203:223-240.
60. Firth AL, Dargitz CT, Qualls SJ, Menon T, Wright R, Singer O, Gage FH, Khanna A, Verma IM. 2014. Generation of multiciliated cells in functional airway epithelia from human induced pluripotent stem cells. Proc Natl Acad Sci USA 111:E1723-1730.
61. Fox E, Shojaie S, Wang J, Tseu I, Ackerley C, Bilodeau M, Post M. 2014. Three-dimensional culture and FGF signaling drive differentiation of murine pluripotent cells to distal lung epithelial cells. Stem Cells Dev.
62. Francavilla C, Rigbolt KT, Emdal KB, Carraro G, Vernet E, Bekker-Jensen DB, Streicher W, Wikstrom M, Sundstrom M, Bellusci S, Cavallaro U, Blagoev B, Olsen JV. 2013. Functional proteomics defines the molecular switch underlying FGF receptor trafficking and cellular outputs. Mol Cell 51:707-722.
63. Gan XQ, Wang JY, Xi Y, Wu ZL, Li YP, Li L. 2008. Nuclear Dvl, c-Jun, beta-catenin, and TCF form a complex leading to stabilization of beta-catenin-TCF interaction. J Cell Biol 180:1087-1100.
64. Gavrilova R, Babovic N, Lteif A, Eidem B, Kirmani S, Olson T, Babovic-Vuksanovic D. 2009. Vitamin A deficiency in an infant with PAGOD syndrome. Am J Med Genet A 149A:2241-2247.
65. Ghaedi M, Calle EA, Mendez JJ, Gard AL, Balestrini J, Booth A, Bove PF, Gui L, White ES, Niklason LE. 2013. Human iPS cell-derived alveolar epithelium repopulates lung extracellular matrix. J Clin Invest 123:4950-4962.
66. Goetz R, Mohammadi M. 2013. Exploring mechanisms of FGF signalling through the lens of structural biology. Nat Rev Mol Cell Biol 14:166-180.
67. Golzio C, Martinovic-Bouriel J, Thomas S, Mougou-Zrelli S, Grattagliano-Bessieres B, Bonniere M, Delahaye S, Munnich A, Encha-Razavi F, Lyonnet S, Vekemans M, Attie-Bitach T, Etchevers HC. 2007. Matthew-Wood syndrome is caused by truncating mutations in the retinol-binding protein receptor gene STRA6. Am J Hum Genet 80:1179-1187.
68. Gontan C, de Munck A, Vermeij M, Grosveld F, Tibboel D, Rottier R. 2008. Sox2 is important for two crucial processes in lung development: branching morphogenesis and epithelial cell differentiation. Dev Biol 317:296-309.
69. Gonzalez-Sancho JM, Greer YE, Abrahams CL, Takigawa Y, Baljinnyam B, Lee KH, Lee KS, Rubin JS, Brown AM. 2013. Functional consequences of Wnt-induced dishevelled 2 phosphorylation in canonical and noncanonical Wnt signaling. J Biol Chem 288:9428-9437.
70. Goss AM, Tian Y, Tsukiyama T, Cohen ED, Zhou D, Lu MM, Yamaguchi TP, Morrisey EE. 2009. Wnt2/2b and beta-catenin signaling are necessary and sufficient to specify lung progenitors in the foregut. Dev Cell 17:290-298.
71. Goss AM, Tian Y, Cheng L, Yang J, Zhou D, Cohen ED, Morrisey EE. 2011. Wnt2 signaling is necessary and sufficient to activate the airway smooth muscle program in the lung by regulating myocardin/Mrtf-B and Fgf10 expression. Dev Biol 356:541-552.
72. Green MD, Chen A, Nostro MC, d'Souza SL, Schaniel C, Lemischka IR, Gouon-Evans V, Keller G, Snoeck HW. 2011. Generation of anterior foregut endoderm from human embryonic and induced pluripotent stem cells. Nat Biotechnol 29:267-272.
73. Grindley JC, Bellusci S, Perkins D, Hogan BL. 1997. Evidence for the involvement of the Gli gene family in embryonic mouse lung development. Dev Biol 188:337-348.
74. Guha A, Vasconcelos M, Cai Y, Yoneda M, Hinds A, Qian J, Li G, Dickel L, Johnson JE, Kimura S, Guo J, McMahon J, McMahon AP, Cardoso WV. 2012. Neuroepithelial body microenvironment is a niche for a distinct subset of Clara-like precursors in the developing airways. Proc Natl Acad Sci USA 109:12592-12597.
75. Guo L, Degenstein L, Fuchs E. 1996. Keratinocyte growth factor is required for hair development but not for wound healing. Genes Dev 10:165-175.
76. Guo W, Keckesova Z, Donaher JL, Shibue T, Tischler V, Reinhardt F, Itzkovitz S, Noske A, Zurrer-Hardi U, Bell G, Tam WL, Mani SA, van Oudenaarden A, Weinberg RA. 2012. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 148:1015-1028.
77. Guseh JS, Bores SA, Stanger BZ, Zhou Q, Anderson WJ, Melton DA, Rajagopal J. 2009. Notch signaling promotes airway mucous metaplasia and inhibits alveolar development. Development 136:1751-1759.
78. Halder G, Johnson RL. 2011. Hippo signaling: growth control and beyond. Development 138:9-22.
79. Harris-Johnson KS, Domyan ET, Vezina CM, Sun X. 2009. beta-Catenin promotes respiratory progenitor identity in mouse foregut. Proc Natl Acad Sci USA 106:16287-16292.
80. Harunaga JS, Doyle AD, Yamada KM. 2014. Local and global dynamics of the basement membrane during branching morphogenesis require protease activity and actomyosin contractility. Dev Biol 394:197-205.
81. Harvey KF, Zhang X, Thomas DM. 2013. The Hippo pathway and human cancer. Nat Rev Cancer 13:246-257.
82. Hashimoto S, Chen H, Que J, Brockway BL, Drake JA, Snyder JC, Randell SH, Stripp BR. 2012. beta-Catenin-SOX2 signaling regulates the fate of developing airway epithelium. J Cell Sci 125:932-942.
83. He XC, Yin T, Grindley JC, Tian Q, Sato T, Tao WA, Dirisina R, Porter-Westpfahl KS, Hembree M, Johnson T, Wiedemann LM, Barrett TA, Hood L, Wu H, Li L. 2007. PTEN-deficient intestinal stem cells initiate intestinal polyposis. Nat Genet 39:189-198.
84. Heallen T, Zhang M, Wang J, Bonilla-Claudio M, Klysik E, Johnson RL, Martin JF. 2011. Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 332:458-461.
85. Heasman J, Crawford A, Goldstone K, Garner-Hamrick P, Gumbiner B, McCrea P, Kintner C, Noro CY, Wylie C. 1994. Overexpression of cadherins and underexpression of beta-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell 79:791-803.
86. Herzig M, Savarese F, Novatchkova M, Semb H, Christofori G. 2007. Tumor progression induced by the loss of E-cadherin independent of beta-catenin/Tcf-mediated Wnt signaling. Oncogene 26:2290-2298.
87. Heuberger J, Birchmeier W. 2010. Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb Perspect Biol 2:a002915.
88. Hines EA, Jones MK, Verheyden JM, Harvey JF, Sun X. 2013. Establishment of smooth muscle and cartilage juxtaposition in the developing mouse upper airways. Proc Natl Acad Sci USA 110:19444-19449.
89. Hines EA, Sun X. 2014. Tissue crosstalk in lung development. J Cell Biochem 115:1469-1477.
90. Hogan BL, Barkauskas CE, Chapman HA, Epstein JA, Jain R, Hsia CC, Niklason L, Calle E, Le A, Randell SH, Rock J, Snitow M, Krummel M, Stripp BR, Vu T, White ES, Whitsett JA, Morrisey EE. 2014. Repair and regeneration of the respiratory system: complexity, plasticity, and mechanisms of lung stem cell function. Cell Stem Cell 15:123-138.
91. Howe LR, Watanabe O, Leonard J, Brown AM. 2003. Twist is up-regulated in response to Wnt1 and inhibits mouse mammary cell differentiation. Cancer Res 63:1906-1913.
92. Hui CC, Slusarski D, Platt KA, Holmgren R, Joyner AL. 1994. Expression of three mouse homologs of the Drosophila segment polarity gene cubitus interruptus, Gli, Gli-2, and Gli-3, in ectoderm- and mesoderm-derived tissues suggests multiple roles during postimplantation development. Dev Biol 162:402-413.
93. Hyatt BA, Shangguan X, Shannon JM. 2004. FGF-10 induces SP-C and Bmp4 and regulates proximal-distal patterning in embryonic tracheal epithelium. Am J Physiol Lung Cell Mol Physiol 287:L1116-1126.
94. Imajo M, Miyatake K, Iimura A, Miyamoto A, Nishida E. 2012. A molecular mechanism that links Hippo signalling to the inhibition of Wnt/beta-catenin signalling. EMBO J 31:1109-1122.
95. Ito T, Udaka N, Yazawa T, Okudela K, Hayashi H, Sudo T, Guillemot F, Kageyama R, Kitamura H. 2000. Basic helix-loop-helix transcription factors regulate the neuroendocrine differentiation of fetal mouse pulmonary epithelium. Development 127:3913-3921.
96. Itoh K, Brott BK, Bae GU, Ratcliffe MJ, Sokol SY. 2005. Nuclear localization is required for Dishevelled function in Wnt/beta-catenin signaling. J Biol 4:3.
97. Jacobs IJ, Ku WY, Que J. 2012. Genetic and cellular mechanisms regulating anterior foregut and esophageal development. Dev Biol 369:54-64.
98. Johnson DE, Lu J, Chen H, Werner S, Williams LT. 1991. The human fibroblast growth factor receptor genes: a common structural arrangement underlies the mechanisms for generating receptor forms that differ in their third immunoglobulin domain. Mol Cell Biol 11:4627-4634.
99. Johnson L, Greenbaum D, Cichowski K, Mercer K, Murphy E, Schmitt E, Bronson RT, Umanoff H, Edelmann W, Kucherlapati R, Jacks T. 1997. K-ras is an essential gene in the mouse with partial functional overlap with N-ras. Genes Dev 11:2468-2481.
100. Johnston JJ, Olivos-Glander I, Killoran C, Elson E, Turner JT, Peters KF, Abbott MH, Aughton DJ, Aylsworth AS, Bamshad MJ, Booth C, Curry CJ, David A, Dinulos MB, Flannery DB, Fox MA, Graham JM, Grange DK, Guttmacher AE, Hannibal MC, Henn W, Hennekam RC, Holmes LB, Hoyme HE, Leppig KA, Lin AE, Macleod P, Manchester DK, Marcelis C, Mazzanti L, McCann E, McDonald MT, Mendelsohn NJ, Moeschler JB, Moghaddam B, Neri G, Newbury-Ecob R, Pagon RA, Phillips JA, Sadler LS, Stoler JM, Tilstra D, Walsh Vockley CM, Zackai EH, Zadeh TM, Brueton L, Black GC, Biesecker LG. 2005. Molecular and clinical analyses of Greig cephalopolysyndactyly and Pallister-Hall syndromes: robust phenotype prediction from the type and position of GLI3 mutations. Am J Hum Genet 76:609-622.
101. Jung J, Zheng M, Goldfarb M, Zaret KS. 1999. Initiation of mammalian liver development from endoderm by fibroblast growth factors. Science 284:1998-2003.
102. Kadzik RS, Morrisey EE. 2012. Directing lung endoderm differentiation in pluripotent stem cells. Cell Stem Cell 10:355-361.
103. Kadzik RS, Cohen ED, Morley MP, Stewart KM, Lu MM, Morrisey EE. 2014. Wnt ligand/Frizzled 2 receptor signaling regulates tube shape and branch-point formation in the lung through control of epithelial cell shape. Proc Natl Acad Sci USA 111:12444-12449.
104. 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.
105. Kawano Y, Kypta R. 2003. Secreted antagonists of the Wnt signalling pathway. J Cell Sci 116:2627-2634.
106. Kim SE, Huang H, Zhao M, Zhang X, Zhang A, Semonov MV, MacDonald BT, Garcia Abreu J, Peng L, He X. 2013. Wnt stabilization of beta-catenin reveals principles for morphogen receptor-scaffold assemblies. Science 340:867-870.
107. 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.
108. Kitagawa M, Hatakeyama S, Shirane M, Matsumoto M, Ishida N, Hattori K, Nakamichi I, Kikuchi A, Nakayama K. 1999. An F-box protein, FWD1, mediates ubiquitin-dependent proteolysis of beta-catenin. EMBO J 18:2401-2410.
109. Kong Y, Glickman J, Subramaniam M, Shahsafaei A, Allamneni KP, Aster JC, Sklar J, Sunday ME. 2004. Functional diversity of notch family genes in fetal lung development. Am J Physiol Lung Cell Mol Physiol 286:L1075-1083.
110. Konsavage WM, Jr., Kyler SL, Rennoll SA, Jin G, Yochum GS. 2012. Wnt/beta-catenin signaling regulates Yes-associated protein (YAP) gene expression in colorectal carcinoma cells. J Biol Chem 287:11730-11739.
111. Kotton DN, Morrisey EE. 2014. Lung regeneration: mechanisms, applications and emerging stem cell populations. Nat Med 20:822-832.
112. Krejci P, Aklian A, Kaucka M, Sevcikova E, Prochazkova J, Masek JK, Mikolka P, Pospisilova T, Spoustova T, Weis M, Paznekas WA, Wolf JH, Gutkind JS, Wilcox WR, Kozubik A, Jabs EW, Bryja V, Salazar L, Vesela I, Balek L. 2012. Receptor tyrosine kinases activate canonical WNT/beta-catenin signaling via MAP kinase/LRP6 pathway and direct beta-catenin phosphorylation. PLoS One 7:e35826.
113. Kumar ME, Bogard PE, Espinoza FH, Menke DB, Kingsley DM, Krasnow MA. 2014. Mesenchymal cells. Defining a mesenchymal progenitor niche at single-cell resolution. Science 346:1258810.
114. Kuphal F, Behrens J. 2006. E-cadherin modulates Wnt-dependent transcription in colorectal cancer cells but does not alter Wnt-independent gene expression in fibroblasts. Exp Cell Res 312:457-467.
115. Lako M, Strachan T, Bullen P, Wilson DI, Robson SC, Lindsay S. 1998. Isolation, characterisation and embryonic expression of WNT11, a gene which maps to 11q13.5 and has possible roles in the development of skeleton, kidney and lung. Gene 219:101-110.
116. Lazzaro D, Price M, de Felice M, Di Lauro R. 1991. The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development 113:1093-1104.
117. Lebeche D, Malpel S, Cardoso WV. 1999. Fibroblast growth factor interactions in the developing lung. Mech Dev 86:125-136.
118. Li C, Xiao J, Hormi K, Borok Z, Minoo P. 2002. Wnt5a participates in distal lung morphogenesis. Dev Biol 248:68-81.
119. Li C, Li A, Li M, Xing Y, Chen H, Hu L, Tiozzo C, Anderson S, Taketo MM, Minoo P. 2009. Stabilized beta-catenin in lung epithelial cells changes cell fate and leads to tracheal and bronchial polyposis. Dev Biol 334:97-108.
120. Li VS, Ng SS, Boersema PJ, Low TY, Karthaus WR, Gerlach JP, Mohammed S, Heck AJ, Maurice MM, Mahmoudi T, Clevers H. 2012. Wnt signaling through inhibition of beta-catenin degradation in an intact Axin1 complex. Cell 149:1245-1256.
121. Li Y, Zhang H, Choi SC, Litingtung Y, Chiang C. 2004. Sonic hedgehog signaling regulates Gli3 processing, mesenchymal proliferation, and differentiation during mouse lung organogenesis. Dev Biol 270:214-231.
122. Li Y, Litingtung Y, Ten Dijke P, Chiang C. 2007. Aberrant Bmp signaling and notochord delamination in the pathogenesis of esophageal atresia. Dev Dyn 236:746-754.
123. Li Y, Gordon J, Manley NR, Litingtung Y, Chiang C. 2008. Bmp4 is required for tracheal formation: a novel mouse model for tracheal agenesis. Dev Biol 322:145-155.
124. Lickert H, Bauer A, Kemler R, Stappert J. 2000. Casein kinase II phosphorylation of E-cadherin increases E-cadherin/beta-catenin interaction and strengthens cell-cell adhesion. J Biol Chem 275:5090-5095.
125. Lin JI, Poon CL, Harvey KF. 2013. The Hippo size control pathway: ever expanding. Sci Signal 6:pe4.
126. Litingtung Y, Lei L, Westphal H, Chiang C. 1998. Sonic hedgehog is essential to foregut development. Nat Genet 20:58-61.
127. Liu C, Li Y, Semenov M, Han C, Baeg GH, Tan Y, Zhang Z, Lin X, He X. 2002. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108:837-847.
128. Liu Y, Jiang H, Crawford HC, Hogan BL. 2003. Role for ETS domain transcription factors Pea3/Erm in mouse lung development. Dev Biol 261:10-24.
129. Longmire TA, Ikonomou L, Hawkins F, Christodoulou C, Cao Y, Jean JC, Kwok LW, Mou H, Rajagopal J, Shen SS, Dowton AA, Serra M, Weiss DJ, Green MD, Snoeck HW, Ramirez MI, Kotton DN. 2012. Efficient derivation of purified lung and thyroid progenitors from embryonic stem cells. Cell Stem Cell 10:398-411.
130. Lu MM, Yang H, Zhang L, Shu W, Blair DG, Morrisey EE. 2001. The bone morphogenic protein antagonist gremlin regulates proximal-distal patterning of the lung. Dev Dyn 222:667-680.
131. MacDonald BT, Tamai K, He X. 2009. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17:9-26.
132. Mahoney JE, Mori M, Szymaniak AD, Varelas X, Cardoso WV. 2014. The hippo pathway effector yap controls patterning and differentiation of airway epithelial progenitors. Dev Cell 30:137-150.
133. Mailleux AA, Kelly R, Veltmaat JM, De Langhe SP, Zaffran S, Thiery JP, Bellusci S. 2005. Fgf10 expression identifies parabronchial smooth muscle cell progenitors and is required for their entry into the smooth muscle cell lineage. Development 132:2157-2166.
134. Makita R, Uchijima Y, Nishiyama K, Amano T, Chen Q, Takeuchi T, Mitani A, Nagase T, Yatomi Y, Aburatani H, Nakagawa O, Small EV, Cobo-Stark P, Igarashi P, Murakami M, Tominaga J, Sato T, Asano T, Kurihara Y, Kurihara H. 2008. Multiple renal cysts, urinary concentration defects, and pulmonary emphysematous changes in mice lacking TAZ. Am J Physiol Renal Physiol 294:F542-553.
135. Malpel S, Mendelsohn C, Cardoso WV. 2000. Regulation of retinoic acid signaling during lung morphogenesis. Development 127:3057-3067.
136. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA. 2008. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133:704-715.
137. Mao J, Wang J, Liu B, Pan W, Farr GH, 3rd, Flynn C, Yuan H, Takada S, Kimelman D, Li L, Wu D. 2001. Low-density lipoprotein receptor-related protein-5 binds to Axin and regulates the canonical Wnt signaling pathway. Mol Cell 7:801-809.
138. Marcil A, Dumontier E, Chamberland M, Camper SA, Drouin J. 2003. Pitx1 and Pitx2 are required for development of hindlimb buds. Development 130:45-55.
139. Martinez Barbera JP, Clements M, Thomas P, Rodriguez T, Meloy D, Kioussis D, Beddington RS. 2000. The homeobox gene Hex is required in definitive endodermal tissues for normal forebrain, liver and thyroid formation. Development 127:2433-2445.
140. Mason IJ, Fuller-Pace F, Smith R, Dickson C. 1994. FGF-7 (keratinocyte growth factor) expression during mouse development suggests roles in myogenesis, forebrain regionalisation and epithelial-mesenchymal interactions. Mech Dev 45:15-30.
141. Metzger DE, Xu Y, Shannon JM. 2007. Elf5 is an epithelium-specific, fibroblast growth factor-sensitive transcription factor in the embryonic lung. Dev Dyn 236:1175-1192.
142. Metzger RJ, Klein OD, Martin GR, Krasnow MA. 2008. The branching programme of mouse lung development. Nature 453:745-750.
143. Miki T, Bottaro DP, Fleming TP, Smith CL, Burgess WH, Chan AM, Aaronson SA. 1992. Determination of ligand-binding specificity by alternative splicing: two distinct growth factor receptors encoded by a single gene. Proc Natl Acad Sci USA 89:246-250.
144. 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.
145. Miller MF, Cohen ED, Baggs JE, Lu MM, Hogenesch JB, Morrisey EE. 2012. Wnt ligands signal in a cooperative manner to promote foregut organogenesis. Proc Natl Acad Sci USA 109:15348-15353.
146. Mills AA, Zheng B, Wang XJ, Vogel H, Roop DR, Bradley A. 1999. p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398:708-713.
147. 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.
148. Minoo P, Su G, Drum H, Bringas P, Kimura S. 1999. Defects in tracheoesophageal and lung morphogenesis in Nkx2.1(-/-) mouse embryos. Dev Biol 209:60-71.
149. Morimoto M, Liu Z, Cheng HT, Winters N, Bader D, Kopan R. 2010. Canonical Notch signaling in the developing lung is required for determination of arterial smooth muscle cells and selection of Clara versus ciliated cell fate. J Cell Sci 123:213-224.
150. Morimoto M, Nishinakamura R, Saga Y, Kopan R. 2012. Different assemblies of Notch receptors coordinate the distribution of the major bronchial Clara, ciliated and neuroendocrine cells. Development 139:4365-4373.
151. Morrisey EE, Hogan BL. 2010. Preparing for the first breath: genetic and cellular mechanisms in lung development. Dev Cell 18:8-23.
152. 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.
153. Mou X, Wu Y, Cao H, Meng Q, Wang Q, Sun C, Hu S, Ma Y, Zhang H. 2012. Generation of disease-specific induced pluripotent stem cells from patients with different karyotypes of Down syndrome. Stem Cell Res Ther 3:14.
154. Mucenski ML, Nation JM, Thitoff AR, Besnard V, Xu Y, Wert SE, Harada N, Taketo MM, Stahlman MT, Whitsett JA. 2005. Beta-catenin regulates differentiation of respiratory epithelial cells in vivo. Am J Physiol Lung Cell Mol Physiol 289:L971-979.
155. 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.
156. Nyeng P, Norgaard GA, Kobberup S, Jensen J. 2008. FGF10 maintains distal lung bud epithelium and excessive signaling leads to progenitor state arrest, distalization, and goblet cell metaplasia. BMC Dev Biol 8:2.
157. Ochieng JK, Schilders K, Kool H, Boerema-De Munck A, Buscop-Van Kempen M, Gontan C, Smits R, Grosveld FG, Wijnen RM, Tibboel D, Rottier RJ. 2014. Sox2 regulates the emergence of lung basal cells by directly activating the transcription of Trp63. Am J Respir Cell Mol Biol 51:311-322.
158. Offield MF, Jetton TL, Labosky PA, Ray M, Stein RW, Magnuson MA, Hogan BL, Wright CV. 1996. PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 122:983-995.
159. Okubo T, Hogan BL. 2004. Hyperactive Wnt signaling changes the developmental potential of embryonic lung endoderm. J Biol 3:11.
160. Okubo T, Knoepfler PS, Eisenman RN, Hogan BL. 2005. Nmyc plays an essential role during lung development as a dosage-sensitive regulator of progenitor cell proliferation and differentiation. Development 132:1363-1374.
161. Olsen SK, Li JY, Bromleigh C, Eliseenkova AV, Ibrahimi OA, Lao Z, Zhang F, Linhardt RJ, Joyner AL, Mohammadi M. 2006. Structural basis by which alternative splicing modulates the organizer activity of FGF8 in the brain. Genes Dev 20:185-198.
162. Ornitz DM, Yin Y. 2012. Signaling networks regulating development of the lower respiratory tract. Cold Spring Harb Perspect Biol 4.
163. Orr-Urtreger A, Bedford MT, Burakova T, Arman E, Zimmer Y, Yayon A, Givol D, Lonai P. 1993. Developmental localization of the splicing alternatives of fibroblast growth factor receptor-2 (FGFR2). Dev Biol 158:475-486.
164. Ozawa M, Baribault H, Kemler R. 1989. The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J 8:1711-1717.
165. Park KS, Whitsett JA, Di Palma T, Hong JH, Yaffe MB, Zannini M. 2004. TAZ interacts with TTF-1 and regulates expression of surfactant protein-C. J Biol Chem 279:17384-17390.
166. Park WY, Miranda B, Lebeche D, Hashimoto G, Cardoso WV. 1998. FGF-10 is a chemotactic factor for distal epithelial buds during lung development. Dev Biol 201:125-134.
167. Peng T, Tian Y, Boogerd CJ, Lu MM, Kadzik RS, Stewart KM, Evans SM, Morrisey EE. 2013. Coordination of heart and lung co-development by a multipotent cardiopulmonary progenitor. Nature 500:589-592.
168. Pepicelli CV, Lewis PM, McMahon AP. 1998. Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Curr Biol 8:1083-1086.
169. Perl AK, Kist R, Shan Z, Scherer G, Whitsett JA. 2005. Normal lung development and function after Sox9 inactivation in the respiratory epithelium. Genesis 41:23-32.
170. Piedra J, Miravet S, Castano J, Palmer HG, Heisterkamp N, Garcia de Herreros A, Dunach M. 2003. p120 Catenin-associated Fer and Fyn tyrosine kinases regulate beta-catenin Tyr-142 phosphorylation and beta-catenin-alpha-catenin Interaction. Mol Cell Biol 23:2287-2297.
171. Plotnikov AN, Hubbard SR, Schlessinger J, Mohammadi M. 2000. Crystal structures of two FGF-FGFR complexes reveal the determinants of ligand-receptor specificity. Cell 101:413-424.
172. Post LC, Ternet M, Hogan BL. 2000. Notch/Delta expression in the developing mouse lung. Mech Dev 98:95-98.
173. Qi J, Wang J, Romanyuk O, Siu CH. 2006. Involvement of Src family kinases in N-cadherin phosphorylation and beta-catenin dissociation during transendothelial migration of melanoma cells. Mol Biol Cell 17:1261-1272.
174. Que J, Choi M, Ziel JW, Klingensmith J, Hogan BL. 2006. Morphogenesis of the trachea and esophagus: current players and new roles for noggin and Bmps. Differentiation 74:422-437.
175. Que J, Okubo T, Goldenring JR, Nam KT, Kurotani R, Morrisey EE, Taranova O, Pevny LH, Hogan BL. 2007. Multiple dose-dependent roles for Sox2 in the patterning and differentiation of anterior foregut endoderm. Development 134:2521-2531.
176. Que J, Luo X, Schwartz RJ, Hogan BL. 2009. Multiple roles for Sox2 in the developing and adult mouse trachea. Development 136:1899-1907.
177. Rajagopal J, Carroll TJ, Guseh JS, Bores SA, Blank LJ, Anderson WJ, Yu J, Zhou Q, McMahon AP, Melton DA. 2008. Wnt7b stimulates embryonic lung growth by coordinately increasing the replication of epithelium and mesenchyme. Development 135:1625-1634.
178. Ramasamy SK, Mailleux AA, Gupte VV, Mata F, Sala FG, Veltmaat JM, Del Moral PM, De Langhe S, Parsa S, Kelly LK, Kelly R, Shia W, Keshet E, Minoo P, Warburton D, Bellusci S. 2007. Fgf10 dosage is critical for the amplification of epithelial cell progenitors and for the formation of multiple mesenchymal lineages during lung development. Dev Biol 307:237-247.
179. Rankin SA, Thi Tran H, Wlizla M, Mancini P, Shifley ET, Bloor SD, Han L, Vleminckx K, Wert SE, Zorn AM. 2014. A Molecular atlas of Xenopus respiratory system development. Dev Dyn. doi: 10.1002/dvdy.24180.
180. Rawlins EL. 2008. Lung epithelial progenitor cells: lessons from development. Proc Am Thorac Soc 5:675-681.
181. Rawlins EL. 2010. The building blocks of mammalian lung development. Dev Dyn 240:463-476.
182. Rawlins EL, Clark CP, Xue Y, Hogan BL. 2009. The Id2+ distal tip lung epithelium contains individual multipotent embryonic progenitor cells. Development 136:3741-3745.
183. Reynolds SD, Zemke AC, Giangreco A, Brockway BL, Teisanu RM, Drake JA, Mariani T, Di PY, Taketo MM, Stripp BR. 2008. Conditional stabilization of beta-catenin expands the pool of lung stem cells. Stem Cells 26:1337-1346.
184. Rhee J, Buchan T, Zukerberg L, Lilien J, Balsamo J. 2007. Cables links Robo-bound Abl kinase to N-cadherin-bound beta-catenin to mediate Slit-induced modulation of adhesion and transcription. Nat Cell Biol 9:883-892.
185. Rimm DL, Koslov ER, Kebriaei P, Cianci CD, Morrow JS. 1995. Alpha 1(E)-catenin is an actin-binding and -bundling protein mediating the attachment of F-actin to the membrane adhesion complex. Proc Natl Acad Sci USA 92:8813-8817.
186. Rockich BE, Hrycaj SM, Shih HP, Nagy MS, Ferguson MA, Kopp JL, Sander M, Wellik DM, Spence JR. 2013. Sox9 plays multiple roles in the lung epithelium during branching morphogenesis. Proc Natl Acad Sci USA 110:E4456-4464.
187. Romano RA, Ortt K, Birkaya B, Smalley K, Sinha S. 2009. An active role of the DeltaN isoform of p63 in regulating basal keratin genes K5 and K14 and directing epidermal cell fate. PLoS One 4:e5623.
188. Rosato R, Veltmaat JM, Groffen J, Heisterkamp N. 1998. Involvement of the tyrosine kinase fer in cell adhesion. Mol Cell Biol 18:5762-5770.
189. Rossi JM, Dunn NR, Hogan BL, Zaret KS. 2001. Distinct mesodermal signals, including BMPs from the septum transversum mesenchyme, are required in combination for hepatogenesis from the endoderm. Genes Dev 15:1998-2009.
190. Roura S, Miravet S, Piedra J, Garcia de Herreros A, Dunach M. 1999. Regulation of E-cadherin/Catenin association by tyrosine phosphorylation. J Biol Chem 274:36734-36740.
191. Sakai T, Larsen M, Yamada KM. 2003. Fibronectin requirement in branching morphogenesis. Nature 423:876-881.
192. Sakiyama J, Yamagishi A, Kuroiwa A. 2003. Tbx4-Fgf10 system controls lung bud formation during chicken embryonic development. Development 130:1225-1234.
193. Sala FG, Del Moral PM, Tiozzo C, Alam DA, Warburton D, Grikscheit T, Veltmaat JM, Bellusci S. 2011. FGF10 controls the patterning of the tracheal cartilage rings via Shh. Development 138:273-282.
194. Sanson B, White P, Vincent JP. 1996. Uncoupling cadherin-based adhesion from wingless signalling in Drosophila. Nature 383:627-630.
195. Schlegelmilch K, Mohseni M, Kirak O, Pruszak J, Rodriguez JR, Zhou D, Kreger BT, Vasioukhin V, Avruch J, Brummelkamp TR, Camargo FD. 2011. Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 144:782-795.
196. Schlessinger J, Plotnikov AN, Ibrahimi OA, Eliseenkova AV, Yeh BK, Yayon A, Linhardt RJ, Mohammadi M. 2000. Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol Cell 6:743-750.
197. 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.
198. Serls AE, Doherty S, Parvatiyar P, Wells JM, Deutsch GH. 2005. Different thresholds of fibroblast growth factors pattern the ventral foregut into liver and lung. Development 132:35-47.
199. Shan L, Aster JC, Sklar J, Sunday ME. 2007. Notch-1 regulates pulmonary neuroendocrine cell differentiation in cell lines and in transgenic mice. Am J Physiol Lung Cell Mol Physiol 292:L500-509.
200. Shan L, Subramaniam M, Emanuel RL, Degan S, Johnston P, Tefft D, Warburton D, Sunday ME. 2008. Centrifugal migration of mesenchymal cells in embryonic lung. Dev Dyn 237:750-757.
201. Shannon JM. 1994. Induction of alveolar type II cell differentiation in fetal tracheal epithelium by grafted distal lung mesenchyme. Dev Biol 166:600-614.
202. Shannon JM, Hyatt BA. 2004. Epithelial-mesenchymal interactions in the developing lung. Annu Rev Physiol 66:625-645.
203. Sherwood RI, Chen TY, Melton DA. 2009. Transcriptional dynamics of endodermal organ formation. Dev Dyn 238:29-42.
204. Shifley ET, Kenny AP, Rankin SA, Zorn AM. 2012. Prolonged FGF signaling is necessary for lung and liver induction in Xenopus. BMC Dev Biol 12:27.
205. Shiratori M, Oshika E, Ung LP, Singh G, Shinozuka H, Warburton D, Michalopoulos G, Katyal SL. 1996. Keratinocyte growth factor and embryonic rat lung morphogenesis. Am J Respir Cell Mol Biol 15:328-338.
206. Shu W, Jiang YQ, Lu MM, Morrisey EE. 2002. Wnt7b regulates mesenchymal proliferation and vascular development in the lung. Development 129:4831-4842.
207. Shu W, Guttentag S, Wang Z, Andl T, Ballard P, Lu MM, Piccolo S, Birchmeier W, Whitsett JA, Millar SE, Morrisey EE. 2005. Wnt/beta-catenin signaling acts upstream of N-myc, BMP4, and FGF signaling to regulate proximal-distal patterning in the lung. Dev Biol 283:226-239.
208. Shu W, Lu MM, Zhang Y, Tucker PW, Zhou D, Morrisey EE. 2007. Foxp2 and Foxp1 cooperatively regulate lung and esophagus development. Development 134:1991-2000.
209. Silvis MR, Kreger BT, Lien WH, Klezovitch O, Rudakova GM, Camargo FD, Lantz DM, Seykora JT, Vasioukhin V. 2011. alpha-catenin is a tumor suppressor that controls cell accumulation by regulating the localization and activity of the transcriptional coactivator Yap1. Sci Signal 4:ra33.
210. Staal FJ, Noort Mv M, Strous GJ, Clevers HC. 2002. Wnt signals are transmitted through N-terminally dephosphorylated beta-catenin. EMBO Rep 3:63-68.
211. Sun J, Chen H, Chen C, Whitsett JA, Mishina Y, Bringas P, Jr., Ma JC, Warburton D, Shi W. 2008. Prenatal lung epithelial cell-specific abrogation of Alk3-bone morphogenetic protein signaling causes neonatal respiratory distress by disrupting distal airway formation. Am J Pathol 172:571-582.
212. 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.
213. Taderera JV. 1967. Control of lung differentiation in vitro. Dev Biol 16:489-512.
214. Tamai K, Zeng X, Liu C, Zhang X, Harada Y, Chang Z, He X. 2004. A mechanism for Wnt coreceptor activation. Mol Cell 13:149-156.
215. Tang N, Marshall WF, McMahon M, Metzger RJ, Martin GR. 2011. Control of mitotic spindle angle by the RAS-regulated ERK1/2 pathway determines lung tube shape. Science 333:342-345.
216. Tebar M, Destree O, de Vree WJ, Ten Have-Opbroek AA. 2001. Expression of Tcf/Lef and sFrp and localization of beta-catenin in the developing mouse lung. Mech Dev 109:437-440.
217. Thiery JP, Acloque H, Huang RY, Nieto MA. 2009. Epithelial-mesenchymal transitions in development and disease. Cell 139:871-890.
218. Tichelaar JW, Lu W, Whitsett JA. 2000. Conditional expression of fibroblast growth factor-7 in the developing and mature lung. J Biol Chem 275:11858-11864.
219. Tiozzo C, De Langhe S, Carraro G, Alam DA, Nagy A, Wigfall C, Hajihosseini MK, Warburton D, Minoo P, Bellusci S. 2009. Fibroblast growth factor 10 plays a causative role in the tracheal cartilage defects in a mouse model of Apert syndrome. Pediatr Res 66:386-390.
220. Tompkins DH, Besnard V, Lange AW, Wert SE, Keiser AR, Smith AN, Lang R, Whitsett JA. 2009. Sox2 is required for maintenance and differentiation of bronchiolar Clara, ciliated, and goblet cells. PLoS One 4:e8248.
221. Tompkins DH, Besnard V, Lange AW, Keiser AR, Wert SE, Bruno MD, Whitsett JA. 2011. Sox2 activates cell proliferation and differentiation in the respiratory epithelium. Am J Respir Cell Mol Biol 45:101-110.
222. Topol L, Jiang X, Choi H, Garrett-Beal L, Carolan PJ, Yang Y. 2003. Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent beta-catenin degradation. J Cell Biol 162:899-908.
223. Treutlein B, Brownfield DG, Wu AR, Neff NF, Mantalas GL, Espinoza FH, Desai TJ, Krasnow MA, Quake SR. 2014. Reconstructing lineage hierarchies of the distal lung epithelium using single-cell RNA-seq. Nature 509:371-375.
224. Tsao PN, Chen F, Izvolsky KI, Walker J, Kukuruzinska MA, Lu J, Cardoso WV. 2008. Gamma-secretase activation of notch signaling regulates the balance of proximal and distal fates in progenitor cells of the developing lung. J Biol Chem 283:29532-29544.
225. Tsao PN, Vasconcelos M, Izvolsky KI, Qian J, Lu J, Cardoso WV. 2009. Notch signaling controls the balance of ciliated and secretory cell fates in developing airways. Development 136:2297-2307.
226. Usui H, Shibayama M, Ohbayashi N, Konishi M, Takada S, Itoh N. 2004. Fgf18 is required for embryonic lung alveolar development. Biochem Biophys Res Commun 322:887-892.
227. Vallin J, Thuret R, Giacomello E, Faraldo MM, Thiery JP, Broders F. 2001. Cloning and characterization of three Xenopus slug promoters reveal direct regulation by Lef/beta-catenin signaling. J Biol Chem 276:30350-30358.
228. Van Haute L, De Block G, Liebaers I, Sermon K, De Rycke M. 2009. Generation of lung epithelial-like tissue from human embryonic stem cells. Respir Res 10:105.
229. Varelas X, Miller BW, Sopko R, Song S, Gregorieff A, Fellouse FA, Sakuma R, Pawson T, Hunziker W, McNeill H, Wrana JL, Attisano L. 2010. The Hippo pathway regulates Wnt/beta-catenin signaling. Dev Cell 18:579-591.
230. Volckaert T, De Langhe S. 2014. Lung epithelial stem cells and their niches: Fgf10 takes center stage. Fibrogenesis Tissue Repair 7:8.
231. Volckaert T, Dill E, Campbell A, Tiozzo C, Majka S, Bellusci S, De Langhe SP. 2011. Parabronchial smooth muscle constitutes an airway epithelial stem cell niche in the mouse lung after injury. J Clin Invest 121:4409-4419.
232. Volckaert T, Campbell A, Dill E, Li C, Minoo P, De Langhe S. 2013. Localized Fgf10 expression is not required for lung branching morphogenesis but prevents differentiation of epithelial progenitors. Development 140:3731-3742.
233. Wang D, Haviland DL, Burns AR, Zsigmond E, Wetsel RA. 2007. A pure population of lung alveolar epithelial type II cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 104:4449-4454.
234. Wang Y, Tian Y, Morley MP, Lu MM, Demayo FJ, Olson EN, Morrisey EE. 2013. Development and regeneration of Sox2+ endoderm progenitors are regulated by a Hdac1/2-Bmp4/Rb1 regulatory pathway. Dev Cell 24:345-358.
235. Wang Z, Shu W, Lu MM, Morrisey EE. 2005. Wnt7b activates canonical signaling in epithelial and vascular smooth muscle cells through interactions with Fzd1, Fzd10, and LRP5. Mol Cell Biol 25:5022-5030.
236. Watanabe H, Ma Q, Peng S, Adelmant G, Swain D, Song W, Fox C, Francis JM, Pedamallu CS, DeLuca DS, Brooks AN, Wang S, Que J, Rustgi AK, Wong KK, Ligon KL, Liu XS, Marto JA, Meyerson M, Bass AJ. 2014. SOX2 and p63 colocalize at genetic loci in squamous cell carcinomas. J Clin Invest 124:1636-1645.
237. 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.
238. Weaver M, Dunn NR, Hogan BL. 2000. Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis. Development 127:2695-2704.
239. Weaver M, Batts L, Hogan BL. 2003. Tissue interactions pattern the mesenchyme of the embryonic mouse lung. Dev Biol 258:169-184.
240. Weidenfeld J, Shu W, Zhang L, Millar SE, Morrisey EE. 2002. The WNT7b promoter is regulated by TTF-1, GATA6, and Foxa2 in lung epithelium. J Biol Chem 277:21061-21070.
241. Wessells NK. 1970. Mammalian lung development: interactions in formation and morphogenesis of tracheal buds. J Exp Zool 175:455-466.
242. West KP, Jr. 2002. Extent of vitamin A deficiency among preschool children and women of reproductive age. J Nutr 132:2857S-2866S.
243. White AC, Xu J, Yin Y, Smith C, Schmid G, Ornitz DM. 2006. FGF9 and SHH signaling coordinate lung growth and development through regulation of distinct mesenchymal domains. Development 133:1507-1517.
244. Whitsett JA, Clark JC, Picard L, Tichelaar JW, Wert SE, Itoh N, Perl AK, Stahlman MT. 2002. Fibroblast growth factor 18 influences proximal programming during lung morphogenesis. J Biol Chem 277:22743-22749.
245. Wilson JG, Roth CB, Warkany J. 1953. An analysis of the syndrome of malformations induced by maternal vitamin A deficiency. Effects of restoration of vitamin A at various times during gestation. Am J Anat 92:189-217.
246. Yamada S, Pokutta S, Drees F, Weis WI, Nelson WJ. 2005. Deconstructing the cadherin-catenin-actin complex. Cell 123:889-901.
247. Yan G, Fukabori Y, McBride G, Nikolaropolous S, McKeehan WL. 1993. Exon switching and activation of stromal and embryonic fibroblast growth factor (FGF)-FGF receptor genes in prostate epithelial cells accompany stromal independence and malignancy. Mol Cell Biol 13:4513-4522.
248. Yang A, Kaghad M, Wang Y, Gillett E, Fleming MD, Dotsch V, Andrews NC, Caput D, McKeon F. 1998. p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol Cell 2:305-316.
249. Yang A, Schweitzer R, Sun D, Kaghad M, Walker N, Bronson RT, Tabin C, Sharpe A, Caput D, Crum C, McKeon F. 1999. p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398:714-718.
250. Yates LL, Schnatwinkel C, Murdoch JN, Bogani D, Formstone CJ, Townsend S, Greenfield A, Niswander LA, Dean CH. 2010. The PCP genes Celsr1 and Vangl2 are required for normal lung branching morphogenesis. Hum Mol Genet 19:2251-2267.
251. Yates LL, Schnatwinkel C, Hazelwood L, Chessum L, Paudyal A, Hilton H, Romero MR, Wilde J, Bogani D, Sanderson J, Formstone C, Murdoch JN, Niswander LA, Greenfield A, Dean CH. 2013. Scribble is required for normal epithelial cell-cell contacts and lumen morphogenesis in the mammalian lung. Dev Biol 373:267-280.
252. Yayon A, Zimmer Y, Shen GH, Avivi A, Yarden Y, Givol D. 1992. A confined variable region confers ligand specificity on fibroblast growth factor receptors: implications for the origin of the immunoglobulin fold. EMBO J 11:1885-1890.
253. Yeh BK, Igarashi M, Eliseenkova AV, Plotnikov AN, Sher I, Ron D, Aaronson SA, Mohammadi M. 2003. Structural basis by which alternative splicing confers specificity in fibroblast growth factor receptors. Proc Natl Acad Sci USA 100:2266-2271.
254. Yi L, Domyan ET, Lewandoski M, Sun X. 2009. Fibroblast growth factor 9 signaling inhibits airway smooth muscle differentiation in mouse lung. Dev Dyn 238:123-137.
255. Yin Y, White AC, Huh SH, Hilton MJ, Kanazawa H, Long F, Ornitz DM. 2008. An FGF-WNT gene regulatory network controls lung mesenchyme development. Dev Biol 319:426-436.
256. Yin Y, Wang F, Ornitz DM. 2011. Mesothelial- and epithelial-derived FGF9 have distinct functions in the regulation of lung development. Development 138:3169-3177.
257. Yu FX, Guan KL. 2013. The Hippo pathway: regulators and regulations. Genes Dev 27:355-371.
258. Yu S, Poe B, Schwarz M, Elliot SA, Albertine KH, Fenton S, Garg V, Moon AM. 2010. Fetal and postnatal lung defects reveal a novel and required role for Fgf8 in lung development. Dev Biol 347:92-108.
259. Zeng X, Tamai K, Doble B, Li S, Huang H, Habas R, Okamura H, Woodgett J, He X. 2005. A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation. Nature 438:873-877.
260. Zhang S, Loch AJ, Radtke F, Egan SE, Xu K. 2013. Jagged1 is the major regulator of Notch-dependent cell fate in proximal airways. Dev Dyn 242:678-686.
261. Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M, Ornitz DM. 2006. Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J Biol Chem 281:15694-15700.
262. Zhang Y, Goss AM, Cohen ED, Kadzik R, Lepore JJ, Muthukumaraswamy K, Yang J, DeMayo FJ, Whitsett JA, Parmacek MS, Morrisey EE. 2008. A Gata6-Wnt pathway required for epithelial stem cell development and airway regeneration. Nat Genet 40:862-870.
263. Zhao B, Tumaneng K, Guan KL. 2011. The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat Cell Biol 13:877-883.
264. Zhao R, Fallon TR, Saladi SV, Pardo-Saganta A, Villoria J, Mou H, Vinarsky V, Gonzalez-Celeiro M, Nunna N, Hariri LP, Camargo F, Ellisen LW, Rajagopal J. 2014. Yap tunes airway epithelial size and architecture by regulating the identity, maintenance, and self-renewal of stem cells. Dev Cell 30:151-165.
265. Zhou BP, Deng J, Xia W, Xu J, Li YM, Gunduz M, Hung MC. 2004. Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol 6:931-940.
266. Zhou L, Graeff RW, McCray PB, Jr., Simonet WS, Whitsett JA. 1996. Keratinocyte growth factor stimulates CFTR-independent fluid secretion in the fetal lung in vitro. Am J Physiol 271:L987-994.
267. Zhou Q, Law AC, Rajagopal J, Anderson WJ, Gray PA, Melton DA. 2007. A multipotent progenitor domain guides pancreatic organogenesis. Dev Cell 13:103-114.
268. Zorn AM, Wells JM. 2009. Vertebrate endoderm development and organ formation. Annu Rev Cell Dev Biol 25:221-251.