Regulation of early lung morphogenesis: Questions, facts and controversies

Development

Volumn 133, Issue 9, 2006, Pages 1611-1624

  Cardoso, Wellington V ^a   Lü, Jining ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR RECEPTOR 2; RETINOIC ACID; SONIC HEDGEHOG PROTEIN; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN;

ANGIOGENESIS; CELL DIFFERENTIATION; CELL FATE; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; ENDODERM; EPITHELIUM CELL; GENE MUTATION; LUNG ALVEOLUS; LUNG ALVEOLUS CELL; LUNG DEVELOPMENT; MESENCHYME; MOUSE; NONHUMAN; PHENOTYPE; PLEURA; PRIMORDIUM; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; RESPIRATORY SYSTEM; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; TRACHEA;

ANIMALS; CELL DIFFERENTIATION; EMBRYONIC INDUCTION; ENDODERM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LUNG; MODELS, BIOLOGICAL; MORPHOGENESIS; MUTATION; NEOVASCULARIZATION, PHYSIOLOGIC; ORGANOGENESIS; PULMONARY ALVEOLI; SIGNAL TRANSDUCTION; TRACHEA;

ERINACEIDAE;

EID: 33744524149     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02310     Document Type: Review

References (175)

1. Ang, S. L. and Rossant, J. (1994). HNF-3 beta is essential for node and notochord formation in mouse development. Cell 78, 561-574.
2. Aubin, J., Lemieux, M., Tremblay, M., Berard, J. and Jeannotte, L. (1997). Early postnatal lethality in Hoxa-5 mutant mice is attributable to respiratory tract defects. Dev. Biol. 192, 432-445.
3. Avilion, A. A., Nicolis, S. K., Pevny, L. H., Perez, L., Vivian, N. and Lovell-Badge, R. (2003). Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 17, 126-140.
4. Beer, H. D., Florence, C., Dammeier, J., McGuire, L., Werner, S. and Duan, D.R. (1997). Mouse fibroblast growth factor 10, cDNA cloning, protein characterization, and regulation of mRNA expression, Oncogene 15, 2211-2218.
5. Bellusci, S., Henderson, R., Winnier, G., Oikawa, T and Hogan, B. L. (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.
6. Bellusci, S., Furuta, Y., Rush, M. G., Henderson, R., Winnier, G. and Hogan, B. L. (1997a). Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 124, 53-63.
7. Bellusci, S., Grindley, J., Emoto, H., Itoh, N. and Hogan, B. L (1997b). Fibroblast growth f actor 10 (FGF 10) and branching morphogenesis in the embryonic mouse lung. Development 124, 4867-4878.
8. Bhushan, A., Itoh, N., Kato, S., Thiery, J. P., Czernichow, P., Bellusci, S. and Scharfmann, R. (2001). Fgf10 is essential for maintaining the proliferative capacity of epithelial progenitor cells during early pancreatic organogenesis. Development 128, 5109-5117.
9. Billings, P. C., Whitbeck, J. C., Adams, C. S. Abrams, W. R., Cohen, A. J., Engelsberg, B. N., Howard, P. S. and Rosenbloom, J. (2002). The transforming growth factor-beta-inducible matrix protein (beta)ig-h3 interacts with fibronectin. J. Biol, Chem. 277, 28003-28009.
10. Bogue, C. W., Lou, L J., Vasavada, H., Wilson, C. M. and Jacobs, H. C. (1996). Expression of Hoxb genes in the developing mouse foregut and lung. Am. J. Respir. Cell Mol. Biol. 15, 163-171.
11. Bort. R., Martinez-Barbera, J. P., Beddington, R. S. and Zaret K. S. (2004). Hex homeobox gene-dependent tissue positioning is required for organogenesis of the ventral pancreas. Development 131, 797-806.
12. Bourbon, J., Boucherat, O., Chailley-Heu, B. and Delacourt, C. (2005). Control mechanisms of lung alveolar development and their disorders in bronchopulmonary dysplasia. Pediatr. Res. 57, 38R-46R.
13. Bragg, A. D., Moses, H. L. and 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.
14. Brody, S. L., Yan, X. H., Wuerffel, M. K., Song, S. K. and Shapiro, S. D. (2000). Ciliogenesis and left-right axis defects in forkhead factor HFH-4-null mice. Am. J. Respir. Cell Mol. Biol. 23, 45-51.
15. Chapman, D. L., Garvey, N., Hancock, S., Alexiou, M., Agulnik. S. L, Gibson-Brown, J. J., Cebra-Thomas, J., Bollag, R. J., Silver, L. M. and Papaioannou, V. E. (1996). Expression of the T-box family genes, Tbxl -Tbx5, during early mouse development. Dev. Dyn. 206, 379-390.
16. Chen, C., Chen, H., Sun, J., Bringas, P., Jr, Chen, Y., Warburton, D. and Shi, W. (2005). Smad1 expression and function during mouse embryonic lung branching morphogenesis. Am. J. Physiol. Lung Cell Mot Physiol. 288, L1033-L1039.
17. Chen, J., Knowles, H. J., Hebert, J. L. and Hackett, B. P. (1998). Mutation of the mouse hepatocyte nuclear factor/forkhead homologue 4 gene results in an absence of cilia and random left-right asymmetry. J. Clin. Invest. 102, 1077-1082.
18. Chuang. P. T, Kawcak, T and McMahon, A. P. (2003). Feedback control of mammalian Hedgehog signaling by the Hedgehog-binding protein, Hip1, modulates Fgf signaling during branching morphogenesis of the lung. Genes Dev. 17, 342-347.
19. Colvin, J. S., Feldman, B., Nadeau, J. H., Goldfarb, M. and Ornitz, D. M. (1999). Genomic organization and embryonic expression of the mouse fibroblast growth factor 9 gene. Dev. Dyn. 216, 72-88.
20. Colvin, J. S., White, A. C., Pratt, S. J. and Ornitz, D. M. (2001). Lung hypoplasia and neonatal death in Fgf9-null mice identify this gene as an essential regulator of lung mesenchyme. Development 128, 2095-2106.
21. Daniely, Y., Liao, G., Dixon, D., Linnoila, R. I., Lori, A., Randell, S. H., Oren, M. and Jetten, A. M. (2004). Critical role of p63 in the development of a normal esophageal and tracheobronchial epithelium. Am. J. Physiol Cell Physiol. 287, C171-C181.
22. DasGupta, R. and Fuchs, E. (1999). Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126, 4557-4568.
23. De Langhe, S. P., Sala, F. G., Del Moral, P. M., Fairbanks, T. J., Yamada, K. M., Warburton, D., Burns, R. C. and 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.
24. De Moerlooze, L., Spencer-Dene, B. Revest. J., Hajihosseini, M., Rosewell, I. and 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.
25. Dean, C. H., Miller, L. A., Smith, A. N., Dufort, D., Lang, R. A. and Niswander, L. A. (2005). Canonical Wnt signaling negatively regulates branching morphogenesis of the lung and lacrimal gland. Dev. Biot 286, 270-286.
26. Del Moral, P. M., Sala, F. G., Tefft, D., Shi, W., Keshet, E., Bellusci, S. and Warburton, D. (2006). VEGF-A signaling through FIk-1 is a critical facilitator of early embryonic lung epithelial to endothelial crosstalk and branching morphogenesis. Dev Biol. 290, 177-188.
27. Demello, D. E., Sawyer, D. Galvin, N. and Reid, L. M. (1997). Early fetal development of lung vasculature. Am. J. Respir. Cell Mol. Biol. 16, 568-581.
28. Desai, T. J., Malpel, S., Flentke, G. R., Smith, S. M. and Cardoso, W. V. (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.
29. Desai, T. J., Chen, F., Lü, J., Qian, J., Niederreither, K., Dollé, P., Chambon, P. and Cardoso, W. V. (2006). Distinct roles for retinoic acid receptors alpha and beta in early lung morphogenesis. Dev Biol. 291, 12-24.
30. Dickman, E. D., Thaller, C. and Smith, S. M. (1997). Temporally-regulated retinoic acid depletion produces specific neural crest, ocular and nervous system defects. Development 124, 3111-3121.
31. Eblaghie, M. C., Reedy, M., Oliver, T, Mishina, Y. and Hogan, B. L. (2006). Evidence that autocrine signaling through Bmpr1a regulates the proliferation, survival and morphogenetic behavior of distal lung epithelial cells. Dev Biol. 291, 67-82.
32. Ellis, T., Gambardella, L., Horcher, M., Tschanz, S., Capol, J., Bertram, P, Jochum, W., Barrandon, Y. and Busslinger, M. (2001). The transcriptional repressor CDP (Cutl1) is essential for epithelial cell differentiation of the lung and the hair follicle. Genes Dev 15, 2307-2319.
33. Fischer, A., Viebahn, C. and Blum, M. (2002). FGF8 acts as a right determinant during establishment of the left-right axis in the rabbit. Curr Biol. 12, 1807-1816.
34. Ganga, M., Espinoza, H. M., Cox, C. J., Morton, L., Hjalt, T A., Lee, Y. and Amendt B. A. (2003). PITX2 isoform-specific regulation of atrial natriuretic factor expression: synergism and repression with Nkx2.5. J. Biol. Chem. 278, 22437-22445.
35. Gebb, S. A. and Shannon, J. M. (2000). Tissue interactions mediate early events in pulmonary vasculogenesis. Dev Dyn. 217, 159-169.
36. Hacohen, N., Kramer, S., Sutherland, D., Hiromi, Y. and Krasnow, M. A. (1998). sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92, 253-263.
37. Harris, K. S., Zhang, Z., McManus, M. T., Harfe, B. D. and Sun, X (2006). Dicer function is essential for lung epithelium morphogenesis. Proc. Natl. Acad. Sci. USA 103, 2208-2213.
38. Harada, H., Toyono, T., Toyoshima, K., Yamasaki, M., Itoh, N., Kato, S., Sekine, K. and Ohuchi, H. (2002). FGF10 maintains stem cell compartment in developing mouse incisors. Development 129, 1533-1541.
39. Heine, U. I., Munoz, E. F., Flanders, K. C., Roberts, A. B. and Sporn, M. B. (1990). Colocalization of TGF-beta 1 and collagen I and III, fibronectin and glycosaminoglycans during lung branching morphogenesis. Development 109, 29-36.
40. Hinck, L. (2004). The versatile roles of 'axon guidance' cues in tissue morphogenesis. Dev. Cell 7, 783-793.
41. Hui, C. C., Slusarski, D., Platt, K. A., Holmgren, R. and Joyner, A. L. (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.
42. Hyatt, B. A., Shangguan, X. and Shannon, J. M. (2004). FGF-10 induces SP-C and Bmp4 and regulates proximal-clistal patterning in embryonic tracheal epithelium. Am. J. Physiol. Lung Cell Mol. Physiol. 287, L1116-L1126.
43. Ioannides, A. S., Chaudhry, B., Henderson, D. J., Spitz, L and Copp, A. J. (2002). Dorsoventral patterning in oesophageal atresia with tracheo-oesophageal fistula: Evidence from a new mouse model. J. Pediatr Surg. 37, 185-191.
44. Ishii, Y., Rex, M., Scotting, P. J. and Yasugl, S. (1998). Region-specific expression of chicken Sox2 in the developing gut and lung epithelium: regulation by epithelial-mesenchymal interactions, Dev Dyn. 213, 464-475.
45. Ito, T., Udaka, N., Yazawa, T., Okudela, K., Hayashi, H., Sudo, T, Guillemot, F., Kageyama, R. and Kitamura, H. (2000). Basic helix-loop-helix transcription factors regulate the neuroendocrine differentiation of fetal mouse pulmonary epithelium. Development 127, 3913-3921.
46. Izvolsky, K. I., Zhong, L., Wei, L., Yu, Q., Nugent, M. A. and Cardoso, W. V. (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
47. Jakkaraju, S., Zhe, X., Pan, D. Choudhury, R. and Schuger, L. (2005). TIPs are tension-responsive proteins involved in myogenic versus adipogenic differentiation. Dev Cell 9, 39-49.
48. Jung, J., Zheng, M., Goldfarb, M. and Zaret, K. S. (1999). Initiation of mammalian liver development from endoderm by fibroblast growth factors. Science 284, 1998-2003.
49. Kaartinen, V., Voncken, J. W., Shuler, C., Warburton, D., Bu, D., Heisterkamp, N. and 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.
50. Kamimura, K., Fujise, M., Villa, F., Izumi, S., Habuchi, H., Kimata, K. and Nakato. H. (2001). Drosophila heparan sulfate 6-O-su(fotransferase (dHS6ST) gene. Structure, expression, and function in the formation of the tracheal system. J Biol. Chem. 276, 17014-1702 1.
51. Kelly, S. E., Bachurski, C. J., Burhans, M. S. and Glasser, S. W. (1996). Transcription of the lung-specific surfactant protein C gene is mediated by thyroid transcription factor 1. J. Biol. Chem. 271, 6881-6888.
52. Kim, H. J. and Bar-Sagi. D. (2004). Modulation of signalling by Sprouty: a developing story. Nat. Rev. Mol. Cell Biol. 5, 441-450.
53. Kim, M. O., Yun, S. J., Kim, I. S., Sohn, S. and Lee, E. H. (2003). Transforming growth factor-beta-inducible gene-h3 (beta(ig)-h3) promotes cell adhesion of human astrocytoma cells in vitro: implication of alpha6beta4 integrin. Neurosci. Lett. 336, 93-96,
54. Kimura, S., Hara, Y., Pineau, T., Fernandez-Salguero, P., Fox, C. H., Ward, J.M. and Gonzalez, F. J. (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.
55. Kitamura, K., Miura, H., Miyagawa-Tomita, S., Yanazawa, M., Katoh-Fukui, Y., Suzuki, R., Ohuchi, H., Suehiro, A., Motegi, Y., Nakahara, Y. et al. (1999). Mouse Pitx2 deficiency leads to anomalies of the ventral body wall, heart, extra- and periocular mesoderm and right pulmonary isomerism. Development 126, 5749-5758.
56. Kreidberg, J. A., Donovan, M. J., Goldstein, S. L., Rennke, H., Shepherd, K., Jones, R. C. and Jaenisch, R. (1996). Alpha 3 beta 1 integrin has a crucial role in kidney and lung organogenesis. Development 122, 3537-3547.
57. Kumar, M. and Melton, D. (2003). Pancreas specification: a budding question. Curr. Opin. Genet. Dev. 13,401-407.
58. Kuo, C. T., Morrisey, E. E., Anandappa, R., Sigrist, K., Lu, M. M., Parmacek, M. S., Soudais, C. and Leiden, J. M. (1997). GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev. 11, 1048-1060.
59. Lako, M., Strachan, T., Bullen, P., Wilson, D. I., Robson, S. C. and 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.
60. Lammert, E., Cleaver, O. and Melton, D. (2001). Induction of pancreatic differentiation by signals from blood vessels. Science 294, 564-567.
61. Lavine, K. J., Yu, K., White, A. C., Zhang, X., Smith, C., Partanen, J. and Ornitz, D. M. (2005). Endocardial and epicardial derived FGF signals regulate myocardial proliferation and differentiation in vivo. Dev. Cell 8, 85-95.
62. Lazzaro, D., Price, M., de Felice, M. and 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.
63. Lebeche, D., Malpel, S. and Cardoso, W. V (1999). Fibroblast growth factor interactions in the developing lung, Mech. Dev. 86, 125-136.
64. Letterio, J. J., Geiser, A. G., Kulkarni, A. B., Roche, N. S., Sporn, M. B. and Roberts, A. B. (1994). Maternal rescue of transforming growth factor-beta 1 null mice. Science 264, 1936-1938.
65. Li, C., Xiao, J., Hormi, K., Borok, Z. and Minoo, P. (2002). Wnt5a participates in distal lung morphogenesis, Dev. Biol. 248, 68-81.
66. Li, Y., Zhang, H., Choi, S. C., Litingtung, Y. and Chiang, C. (2004). Sonic hedgehog signaling regulates Gli3 processing, mesenchymal proliferation, and differentiation during mouse lung organogenesis. Dev. Biol. 270, 214-231.
67. Lim, L., Kalinichenko, V. V., Whitsett, J. A. and Costa, R. H. (2002). Fusion of lung lobes and vessels in mouse embryos heterozygous for the forkhead box f1 targeted allele. Am. J. Physiol. Lung Cell Mol. Physiol. 282, L1012-L1022.
68. Lin. C. R., Kioussi, C., O'Connell, S., Briata, P., Szeto, D., Liu, F, Izpisua-Belmonte, J. C. and Rosenfeld, M. G. (1999). Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature 401, 279-282.
69. Lin, Y., Zhang, S., Tuukkanen, J., Peltoketo, H., Pihlajaniemi, T and Vainio, S. (2003). Patterning parameters associated with the branching of the ureteric bud regulated by epithelia)-mesenchymal interactions. Int. J. Dev. Biol. 47, 3-13.
70. Litingtung, Y., Lei, L., Westphal, H. and Chiang, C. (1998). Sonic hedgehog is essential to foregut development. Nat Genet 20, 58-61.
71. Liu. Y., Jiang, H., Crawford, H. C. and Hogan, B. L. (2003), Role for ETS domain transcription factors Pea3/Erm in mouse lung development. Dev. Biol. 261, 10-24.
72. Liu, Y., Stein, E., Oliver, T., Li, Y., Brunken, W. J., Koch, M., Tessier-Lavigne, M. and Hogan, B. L. (2004). Novel role for Netrins in regulating epithelial behavior during lung branching morphogenesis. Curr. Biol. 14, 897-905.
73. Lowe, L. A., Yamada, S. and Kuehn, M. R. (2001). Genetic dissection of nodal function in patterning the mouse embryo. Development 128, 1831-1843.
74. Lu, J., Qian, J., Izvolsky, K. I. and Cardoso, W. V. (2004). Global analysis of genes differentially expressed in branching and non-branching regions of the mouse embryonic lung, Dev. Biol. 273, 418-435.
75. Lu, J., Izvolsky, K. I., Qian, J. and Cardoso, W. V. (2005a). Identification of FGF10 targets in the embryonic lung epithelium during bud morphogenesis. J. Biol. Chem. 280, 4834-4841,
76. Lu, J., Qian, J., Chen, F, Tang, X., Li, C. and Cardoso, W, V. (2005b) Differential expression of components of the microRNA machinery during mouse organogenesis. Biochem. Biophys. Res. Commun. 334, 319-323,
77. Lu, M. M., Yang, H., Zhang, L., Shu, W., Blair, D. G. and Morrisey, E. E. (2001). The bone morphogenic protein antagonist gremlin regulates proximal-distal patterning of the lung. Dev. Dyn. 222, 667-680.
78. Lu, W., Luo, Y., Kan, M. and McKeehan, W. L. (1999). Fibroblast growth factor-10. A second candidate stromal to epithelial cell andromedin in prostate. J. Biol. Chem. 274, 12827-12834.
79. Mahlapuu, M., Enerback, S. and Carlsson, P (2001). Haploinsufficiency of the forkhead gene Foxf1, a target for sonic hedgehog signaling, causes lung and foregut malformations. Development 128, 2397-2406.
80. Mailleux, A. A., Tefft, D., Ndiaye, D., Itoh, N., Thiery, J. P., Warburton, D. and Bellusci, S. (2001). Evidence that SPROUTY2 functions as an inhibitor of mouse embryonic lung growth and morphogenesis. Mech. Dev 102, 81-94.
81. Mailleux, A. A., Kelly, R., Veltmaat, J. M., De Langhe, S. P., Zaffran, S., Thiery, J. P. and 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.
82. Malpel, S., Mendelsohn, C. and Cardoso. W. V. (2000). Regulation of retinoic acid signaling during lung morphogenesis. Development 127, 3057-3067.
83. Martinez Barbera, J. P., Clements, M., Thomas, P., Rodriguez, T., Meloy, D., Kioussis, D. and Beddington, R. S. (2000). The homeobox gene Hex is required in definitive endodermal tissues for normal forebrain, liver and thyroid formation. Development 127, 2433-2445.
84. Massague, J. (2000). How cells read TGF-beta signals. Nat. Rev. Mol. Cell Biol. 1, 169-178.
85. Matsumoto, K., Yoshitomi, H., Rossant, J. and Zaret K. S. (2001). Liver organogenesis promoted by endothelial cells prior to vascular function. Science 294, 559-563.
86. Mendelsohn, C., Lohnes, D., Decimo, D., Lufkin, T., LeMeur, M., Chambon, P. and 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.
87. Meno, C., Shimono, A., Saijoh, Y., Yashiro, K., Mochida, K., Ohishi, S., Noji, S., Kondoh, H. and Hamada, H. (1998). lefty-1 is required for left-right determination as a regulator of lefty-2 and nodal. Cell 94, 287-297.
88. Metzger, R. J. and Krasnow, M. A. (1999). Genetic control of branching morphogenesis. Science 284, 1635-1639.
89. Michos, O., Panman, L., Vintersten, K., Beier, K., Zeller, R. and Zuniga, A. (2004). Gremlin-mediated BMP antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development 131, 3401-3410.
90. Miettinen, P. J., Warburton, D., Bu, D., Zhao, J. S., Berger, J. E., Minoo, P, Koivisto, T., Allen, L., Dobbs, L., Werb, Z. et al. (1997). Impaired lung branching morphogenesis in the absence of functional EGF receptor, Dev Biol. 186, 224-236.
91. Min, H., Danilenko, D. M., Scully, S. A., Bolon, B., Ring, B. D., Tarpley, J. E., DeRose, M. and Simonet W. S. (1998). Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev. 12, 3156-3161.
92. Minoo, P., Su, G., Drum, H., Bringas, P. and Kimura, S. (1999). Defects in tracheoesophageal and lung morphogenesis in Nkx2. 1(-/-) mouse embryos. Dev. Biol. 209, 60-71.
93. Moens, C. B., Auerbach, A. B., Conlon, R. A., Joyner, A. L. and Rossant, J. (1992). A targeted mutation reveals a role for N-myc in branching morphogenesis in the embryonic mouse lung. Genes Dev. 6, 691-704.
94. Mollard, R., Ghyselinck, N. B., Wendling, O., Chambon, P. and Mark, M. (2000). Stage-dependent responses of the developing lung to retinoic acid signaling. Int. J. Dev. Biol. 44, 457-462.
95. Morrisey, E. E., Tang, Z., Sigrist, K., Lu, M. M., Jiang, F., Ip, H. S. and Parmacek, M. S. (1998). GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes Dev. 12, 3579-3590.
96. Motoyama, J., Liu, J., Mo, R., Ding, Q., Post, M. and Hui, C. C. (1998). Essential function of Gli2 and Gli3 in the formation of lung, trachea and oesophagus. Nat. Genet. 20, 54-57.
97. Mucenski, M. L., Wert, S. E., Nation, J. M., Loudy, D. E., Huelsken, J., Birchmeier, W., Morrisey, E. E. and Whitsett, J. A. (2003). beta-Catenin is required for specification of proximal/distal cell fate during lung morphogenesis. J. Biol. Chem. 278, 40231-40238.
98. Muglia, L. J., Bae, D. S., Brown, T T., Vogt S. K., Alvarez, J. G., Sunday, M. E. and Majzoub, J. A. (1999). Proliferation and differentiation defects during lung development in corticotropin-releasing hormone-deficient mice. Am. J. Respir. Cell Mol. Biol. 20, 181-188.
99. Naiche, L. A. and Papaioannou, V. E. (2003). Loss of Tbx4 blocks hindlimb development and affects vascularization and fusion of the allantois. Development 130, 2681-2693.
100. Nelson, W. J. and Nusse, R. (2004). Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303, 1483-1487.
101. Nguyen, N. M., Miner, J. H., Pierce, R. A. and Senior, R. M. (2002). Laminin alpha 5 is required for lobar septation and visceral pleural basement membrane formation in the developing mouse lung. Dev. Biol. 246, 231-244.
102. Niederreither, K., Subbarayan, V, Dolle, P. and Chambon, R (1999). Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat. Genet 21, 444-448.
103. Nogawa, H., Morita, K. and Cardoso, W. V. (1998). Bud formation precedes the appearance of differential cell proliferation during branching morphogenesis of mouse lung epithelium in vitro. Dev. Dyn. 213, 228-235.
104. Norgaard, G. A., Jensen, J. N. and Jensen, J. (2003). FGH10 signaling maintains the pancreatic progenitor cell state revealing a novel role of Notch in organ development. Dev Biol. 264, 323-338.
105. Offield, M. F., Jetton, T. L., Labosky, P. A., Ray, M., Stein, R. W., Magnuson, M. A., Hogan, B. L. and Wright, C. V. (1996). PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 122, 983-995.
106. Oh, S. P. and Li, E. (1997). The signaling pathway mediated by the type IIB activin receptor controls axial patterning and lateral asymmetry in the mouse. Genes Dev. 11, 1812-1826.
107. Ohtsuka, N., Urase, K., Momoi, T. and Nogawa, H. (2001). Induction of bud formation of embryonic mouse tracheal epithelium by fibroblast growth factor plus transferrin in mesenchyme-free culture. Dev. Dyn. 222, 263-272.
108. Okubo, T. and Hogan, B. L. (2004). Hyperactive Wnt signaling changes the developmental potential of embryonic lung endoderm. J. Biol. 3, 11.
109. Okubo, T., Knoepfler, R S., Eisenman, R. N. and Hogan, B. L. (2005). Nmyc plays an essential role during lung development as a dosage-sensitive regulator of progenitor cell proliferation and differentiation. Development 132, 1363-1374.
110. Pan, Q., Li, C., Xiao, J., Kimura, S., Rubenstein, J., Puelles, L. and Minoo, P. (2004). In vivo characterization of the Nkx2.1 promoter/ enhancer elements in transgenic mice. Gene 331, 73-82.
111. Park, W. Y., Miranda, B., Lebeche, D., Hashimoto, G. and Cardoso, W. V. (1998). FGF-10 is a chemotactic factor for distal epithelial buds during lung development. Dev. Biol. 201, 125-134.
112. Pauling, M. H. and Vu, T. H. (2004). Mechanisms and regulation of lung vascular development. Curr. Top. Dev. Biol. 64, 73-99.
113. Pelton, R. W., Johnson, M. D., Perkett, E. A., Gold, L. I. and Moses, H. L. (1991). Expression of transforming growth factor-beta 1, -beta 2, and -beta 3 mRNA and protein in the murine lung. Am. J. Respir. Cell Mol. Biol. 5, 522-530.
114. Pepicelli, C. V., Lewis, R M. and McMahon, A. R (1998). Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Curr. Biol. 8, 1083-1086.
115. Perl, A. K., Wert, S. E., Nagy, A., Lobe, C. G. and Whitsett, J. A. (2002). Early restriction of peripheral and proximal cell lineages during formation of the lung. Proc. Natl. Acad. Sci. USA 99, 10482-10487.
116. Perl, A. K., Hokuto, I., Impagnatiello, M. A., Christofori, G. and Whitsett, J. A. (2003). Temporal effects of Sprouty on lung morphogenesis. Dev. Biol. 258, 154-168.
117. Peschon, J. J., Slack, J. L., Reddy, P., Stocking, K. L., Sunnarborg, S. W., Lee, D. C., Russell, W. E., Castner, B. J., Johnson, R. S., Fitzner, J. N. et al. (1998). An essential role for ectodomain shedding in mammalian development. Science 282, 1281-1284.
118. Quaggin, S. E., Schwartz, L., Cui, S., Igarashi, P., Deimling, J., Post, M. and Rossant J. (1999). The basic-helix-loop-helix protein pod1 is critically important for kidney and lung organogenesis. Development 126, 5771-5783.
119. Rankin, C. T., Bunton, T., Lawler, A. M. and Lee, S. J. (2000). Regulation of left-right patterning in mice by growth/differentiation factor-1. Nat. Genet. 24, 262-265.
120. Rawlins, E. L. and Hogan, B. L. (2005). Intercellular growth factor signaling and the development of mouse tracheal submucosal glands. Dev. Dyn. 233, 1378-1385.
121. Rossant, J., Zirngibl, R., Cado, D., Shago, M. and Giguere, V. (1991). Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis. Genes Dev. 5, 1333-1344.
122. Rossi, J. M., Dunn, N. R., Hogan, B. L. and Zaret, K. S. (2001). Distinct mesodermal signals, including BMPs from the septum transversurn mesenchyme, are required in combination for hepatogenesis from the endoderm. Genes Dev 15, 1998-2009.
123. Rubin, L. P., Kovacs, C. S., De Paepe, M. E., Tsai, S. W., Torday, J. S. and Kronenberg, H. M. (2004). Arrested pulmonary alveolar cytodifferentiation and defective surfactant synthesis in mice missing the gene for parathyroid hormone-related protein. Dev Dyn. 230, 278-289.
124. Sakiyama, J., Yamagishi, A. and Kuroiwa, A. (2003). Tbx4-Fgf10 system controls lung bud formation during chicken embryonic development. Development 130, 122 5-1234.
125. Samakovlis, C., Hacohen, N., Manning, G., Sutherland, D. C., Guillemin, K. and Krasnow, M. A. (1996). Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 122,1395-1407.
126. Sanford, L. P., Ormsby, I., Gittenberger-de Groot, A. C., Sariola, H., Friedman, R., Boivin, G. P., Cardell, E. L. and Doetschman, T. (1997). TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 124, 2659-2670.
127. Sekine, K., Ohuchi, H., Fujiwara, M., Yamasaki, M., Yoshizawa, T., Sato, T., Yagishita, N., Matsui, D., Koga, Y., Itoh, N. et al. (1999). Fgf10 is essential for limb and lung formation. Nat. Genet. 21, 138-141.
128. Serls, A. E., Doherty, S., Parvatiyar, P., Wells, J. M. and Deutsch, G. H. (2005). Different thresholds of fibroblast growth factors pattern the ventral foregut into liver and lung. Development 132, 35-47.
129. Serra, R., Pelton, R. W. and Moses, H. L. (1994). TGF beta 1 inhibits branching morphogenesis and N-myc expression in lung bud organ cultures. Development 120, 2153-2161.
130. Shannon, J. M. (1994). Induction of alveolar type II cell differentiation in fetal tracheal epithelium by grafted distal lung mesenchyme. Dev. Biol. 166, 600-614.
131. Shannon, J. M., McCormick-Shannon, K., Burhans, M. S., Shangguan, X., Srivastava, K. and Hyatt, B. A. (2003). Chondroitin sulfate proteoglycans are required for lung growth and morphogenesis in vitro. Am. J. Physiol. Lung Cell Mol. Physiol. 285, L1323-L1336.
132. Shiels, H., Li, X., Schumacker, R T., Maltepe, E., Padrid, R A., Sperling, A., Thompson, C. B. and Lindsten, T. (2000). TRAM deficiency leads to tracheal malformation with resulting alterations in air flow to the lungs. Am. J. Pathol. 157, 679-688.
133. Shikama, N., Lutz, W., Kretzschmar, R., Sauter, N., Roth, J. F., Marino, S., Wittwer, J., Scheldweiler, A. and Eckner, R. (2003). Essential function of p300 acetyltransferase activity in heart, lung and small intestine formation. EMBO J. 22, 5175-5185.
134. Shu, W., Jiang, Y. Q., Lu, M. M. and Morrisey, E. E. (2002). Wnt7b regulates mesenchymal proliferation and vascular development in the lung. Development 129, 4831-4842.
135. Shu, W., Guttentag, S., Wang, Z., Andl, T, Ballard, R, Lu, M. M., Piccolo, S., Birchmeler, W., Whitsett, J. A., Millar, S. E. et al. (2005). Wnt/beta-catenin signaling acts upstream of N-myc, BMP4, and FGF signaling to regulate proximal-clistal patterning in the lung. Dev. Biol. 283, 226-239.
136. Sock, E., Rettig, S. D., Enderich, J., Bosl, M. R., Tamm, E. R. and Wegner, M. (2004). Gene targeting reveals a widespread role for the high-mobility-group transcription factor Sox11 in tissue remodeling. Mol. Cell. Biol. 24, 6635-6644.
137. Stafford, D. and Prince, V. E. (2002). Retinoic acid signaling is required for a critical early step in zebrafish pancreatic development. Curr. Biol. 12, 1215-1220.
138. Steele-Perkins, G., Plachez, C., Butz, K. G., Yang, G., Bachurski, C. J., Kinsman, S. L., Litwack, E. D., Richards, L. J. and Gronostajski, R. M. (2005). The transcription factor gene Nfib is essential for both lung maturation and brain development. Mol. Cell. Biol. 25, 685-698.
139. Sterner-Kock, A., Thorey, I. S., Koli, K., Wempe, F., Otte, J., Bangsow, T., Kuhlmeier, K., Kirchner, T., Jin, S., Keski-Oja, J. et al. (2002). Disruption of the gene encoding the latent transforming growth factor-beta binding protein 4 (LTBP-4) causes abnormal lung development, cardiomyopathy, and colorectal cancer. Genes Dev. 16, 2264-2273.
140. Strickland, P., Shin, G. C., Plump, A., Tessier-Lavigne, M. and Hinck, L. (2006). Slit2 and netrin 1 act synergistically as adhesive cues to generate tubular bi-layers during ductal morphogenesis. Development 133, 823-832.
141. Sugahara, K., Iyama, K. I., Kimura, T., Sano, K., Darlington, G. J., Akiba, T. and Takiguchi, M. (2001). Mice lacking CCAAVenhancer-binding protein-alpha show hyperproliferation of alveolar type II cells and increased surfactant protein mRNAs. Cell Tissue Res. 306, 57-63.
142. Sutherland, D., Samakoviis, C. and Krasnow, M. A. (1996). branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 87, 1091-1101.
143. Sutliff, K. S. and Hutchins, G. M. (1994). Septation of the respiratory and digestive tracts in human embryos: crucial role of the tracheoesophageal sulcus. Anat. Rec. 238, 237-247.
144. Tebar, M., Destree, O., de Vree, W. J. and Have-Opbroek, A. A. (2001). Expression of Tcf/Lef and sFrp and localization of beta-catenin in the developing mouse lung. Mech. Dev. 109, 437-440.
145. Tefft, J. D., Lee, M., Smith, S., Leinwand, M., Zhao, J., Bringas, P., Jr, Crowe, D. L. and Warburton, D. (1999). Conserved function of mSpry-2, a murine homolog of Drosophila sprouty, which negatively modulates respiratory organogenesis. Curr. Biol. 9, 219-222.
146. Tefft, D., Lee, M., Smith, S., Crowe, D. L., Bellusci, S. and Warburton, D. (2002). mSprouty inhibits FGF10-activated MAP kinase by differentially binding to upstream target proteins. Am. J. Physiol. Lung Cell Mol. Physic. 283, L700-L706.
147. Tiso, N., Filippi, A., Pauls, S., Bortolussi, M. and Argenton, F. (2002). BMP signalling regulates anteroposterior endoderm patterning in zebrafish. Mech. Dev. 118, 29-37.
148. Tollet, J., Everett, A. W. and Sparrow, M. P. (2001). Spatial and temporal distribution of nerves, ganglia, and smooth muscle during the early pseudoglandular stage of fetal mouse lung development. Dev. Dyn. 221, 48-60.
149. Tomlinson, D. C., Grindley, J. C. and Thomson, A. A. (2004). Regulation of Fgf10 gene expression in the prostate: identification of transforming growth factor-beta1 and promoter elements. Endocrinology 145, 1988-1995.
150. Usui, H., Shibayama, M., Ohbayashi, N., Konishi, M., Takada, S. and Itoh, N. (2004). Fgf18 is required for embryonic lung alveolar development. Biochem. Biophys. Res. Commun. 322, 887-892.
151. Vergnes, L., Peterfy, M., Bergo, M. O., Young, S. G. and Reue, K. (2004). Lamin B1 is required for mouse development and nuclear integrity. Proc. Natl. Acad. Sci. USA 101, 10428-10433.
152. Volpe, M. V., Martin, A., Vosatka, R. J., Mazzoni, C. L. and Nielsen, H.C. (1997). Hoxb-5 expression in the developing mouse lung suggests a role in branching morphogenesis and epithelial cell fate. Histochem. Cell Biol. 108, 495-504.
153. Wan, H., Dingle, S., Xu, Y., Besnard, V., Kaestner, K. H., Ang, S. L., Wert, S., Stahlman, M. T and Whitsett J. A. (2005). Compensatory Roles of Foxa1 and Foxa2 during Lung Morphogenesis. J. Biol. Chem. 280, 13809-13816.
154. Wani, M. A., Wert, S. E. and Lingrel, J. B. (1999). Lung Kruppel-like factor, a zinc finger transcription factor, is essential for normal lung development. J. Biol. Chem. 274, 21180-21185.
155. Weaver, M., Yingling, J. M., Dunn, N. R., Bellusci, S. and Hogan, B. L. (1999). Bmp signaling regulates proximal-distal differentiation of endoderm in mouse lung development. Development 126, 4005-4015.
156. Weaver, M., Dunn, N. R. and Hogan, B. L. (2000). Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis. Development 127, 2695-2704.
157. Weaver, M., Batts, L. and Hogan, B. L. (2003). Tissue interactions pattern the mesenchyme of the embryonic mouse lung. Dev. Biol. 258, 169-184.
158. Weinstein, M., Xu, X., Ohyama, K. and Deng, C. X. (1998). FGFR-3 and FGFR-4 function cooperatively to direct alveogenesis in the murine lung. Development 125, 3615-3623.
159. Wells, J. M. and Melton, D. A. (1999). Vertebrate endoderm development. Annu. Rev. Cell Dev. Biol. 15, 393-410.
160. Wells, J. M. and Melton, D. A. (2000). Early mouse endoderm is patterned by soluble factors from adjacent germ layers. Development 127, 1563-1572.
161. Wendel, D. P., Taylor, D. G., Albertine, K. H., Keating, M. T. and Li, D.Y. (2000). Impaired distal airway development in mice lacking elastin. Am. J. Respir. Cell Mol. Biol. 23, 320-326.
162. Wert, S. E., Glasser, S. W., Korfhagen, T. R. and Whitsett, J. A. (1993). Transcriptional elements from the human SP-C gene direct expression in the primordial respiratory epithelium of transgenic mice. Dev Biol. 156, 426-443.
163. Williams, M. C. (2003). Alveolar type I cells: molecular phenotype and development. Annu. Rev. Physiol. 65, 669-695.
164. Wilson, J. G., Roth, C. B. and 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.
165. Winnier, G., Blessing, M., Labosky, P. A. and Hogan, B. L. (1995). Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9, 2105-2116.
166. Wongtrakool, C., Malpel, S., Gorenstein, J., Sedita, J., Ramirez, M. I., Underhill, T M. and Cardoso, W. V. (2003). Down-regulation of retinoic acid receptor alpha signaling is required for sacculation and type I cell formation in the developing lung. J. Biol. Chem. 278, 46911-46918.
167. Wood, H. B., May, G., Healy, L., Enver, T. and Morriss-Kay, G. M. (1997). CD34 expression patterns during early mouse development are related to modes of blood vessel formation and reveal additional sites of hematopoiesis. Blood 90, 2300-2311.
168. Yang, H., Lu, M. M., Zhang, L., Whitsett, J. A. and Morrisey, E. E. (2002). GATA6 regulates differentiation of distal lung epithelium. Development 129, 2233-2246.
169. Yang, Y., Beqaj, S., Kemp, R., Ariel, I. and Schuger, L. (2000). Stretch-induced alternative splicing of serum response factor promotes bronchial myogenesis and is defective in lung hypoplasia. J. Clin. Invest 106, 1321-1330.
170. Yuan, B., Li, C., Kimura, S., Engelhardt R. T., Smith, B. R. and Minoo, P. (2000). Inhibition of distal lung morphogenesis in Nkx2. 1(-/-) embryos. Dev. Dyn. 217, 180-190.
171. Zakin, L. D., Mazan, S., Maury, M., Martin, N., Guenet, J. L. and Brulet, P. (1998). Structure and expression of Wnt13, a novel mouse Wnt2 related gene. Mech. Dev. 73, 107-116.
172. Zaw-Tun, H. A. (11982). The tracheo-esophageal septum-fact or fantasy? Origin and development of the respiratory primordium and esophagus. Acta Anat. (Basel) 114, 1-21.
173. Zhao, J., Bu, D., Lee, M., Slavkin, H. C., Hall, F. L. and 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.
174. Zhao, J., Chen, H., Peschon, J. J., Shi, W., Zhang, Y., Frank, S. J. and Warburton, D. (2001). Pulmonary hypoplasia in mice lacking tumor necrosis factor-alpha converting enzyme indicates an indispensable role for cell surface protein shedding during embryonic lung branching morphogenesis. Dev. Biol. 232, 204-218.
175. Zhou, L., Dey, C. R., Wert, S. E. and Whitsett, J. A. (1996). Arrested lung morphogenesis in transgenic mice bearing an SP-C-TGF-beta 1 chimeric gene. Dev. Biol. 175, 227-238.