Epithelial-mesenchymal interactions in the developing lung

Annual Review of Physiology

Volumn 66, Issue , 2004, Pages 625-645

  Shannon, John M ^a   Hyatt, Brian A ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Gene expression; Growth factors; Lung development; Tissue interactions

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN 4; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR 18; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 3; FIBROBLAST GROWTH FACTOR 4; FIBROBLAST GROWTH FACTOR RECEPTOR; KERATINOCYTE GROWTH FACTOR; NOGGIN; PLATELET DERIVED GROWTH FACTOR; RETINOIC ACID; SOMATOMEDIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GLI1; VASCULOTROPIN; WNT PROTEIN;

CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; DNA MICROARRAY; EMBRYOLOGY; EPITHELIUM; GENE EXPRESSION; HUMAN; LUNG DEVELOPMENT; MESENCHYME; MESODERM; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TISSUE INTERACTION; ANIMAL; EMBRYO; ENDODERM; LUNG; PHYSIOLOGY; PRENATAL DEVELOPMENT;

ANIMALS; EMBRYO; EMBRYONIC AND FETAL DEVELOPMENT; ENDODERM; EPITHELIUM; HUMANS; LUNG; MESODERM;

EID: 2342620855     PISSN: 00664278     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.physiol.66.032102.135749     Document Type: Review

References (118)

1. Crapo JD, Barry BE, Gehr P, Bachofen M, Weibel ER. 1982. Cell number and cell characteristics of the normal human lung. Am. Rev. Respir. Dis. 125:332-37
2. Williams MC. 2003. Alveolar type I cells: phenotype and development. Annu. Rev. Physiol. 65:669-95
3. Fehrenbach H. 2001. Alveolar epithelial type II cell: defender of the alveolus redevisited. Respir. Res. 2:33-46
4. Spooner BS, Wessells NK. 1970. Mammalian lung development: interactions in primordium formation and bronchial morphogenesis. J. Exp. Zool. 175:445-54
5. Wells JM, Melton DA. 1999. Vertebrate endoderm development. Annu. Rev. Cell Dev. Biol. 15:393-410
6. Iannaccone PM, Zhou X, Khokha M, Boucher D, Kuehn MR. 1992. Insertional mutation of a gene involved in growth regulation of the early mouse embryo. Dev. Dyn. 194:198-208
7. Conlon FL, Lyons KM, Takaesu N, Barth KS, Kispert A, et al. 1994. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development 120:1919-28
8. Lowe LA, Yamada S, Kuehn MR. 2001. Genetic dissection of nodal function in patterning the mouse embryo. Development 128:1831-43
9. Gao X, Sedgwick T, Shi YB, Evans T. 1998. Distinct functions are implicated for the GATA-4, -5, and -6 transcription factors in the regulation of intestine epithelial cell differentiation. Mol. Cell Biol. 18:2901-11
10. Kuo CT, Morrisey EE, Anandappa R, Sigrist K, Lu MM, et al. 1997. GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev. 11:1048-60
11. Molkentin JD, Lin Q, Duncan SA, Olson EN. 1997. Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev. 11:1061-72
12. Morrisey EE, Tang Z, Sigrist K, Lu MM, Jiang F, et al. 1998. GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes Dev. 12:3579-90
13. Wegner M. 1999. From head to toes: the multiple facets of Sox proteins. Nucleic Acids Res. 27:1409-20
14. Hudson C, Clements D, Friday RV, Stott D, Woodland HR. 1997. Xsox17-α and -β mediate endoderm formation in Xenopus. Cell 91:397-405
15. Clements D, Woodland HR. 2000. Changes in embryonic cell fate produced by expression of an endodermal transcription factor, Xsox17. Mech. Dev. 99:65-70
16. Kanai-Azuma M, Kanai Y, Gad JM, Tajima Y, Taya C, et al. 2002. Depletion of definitive gut endoderm in Sox17-null mutant mice. Development 129:2367-79
17. Kaestner KH, Katz J, Liu Y, Drucker DJ, Schutz G. 1999. Inactivation of the winged helix transcription factor HNF3alpha affects glucose homeostasis and islet glucagon gene expression in vivo. Genes Dev. 13:495-504
18. Weinstein DC, Ruiz i Altaba A, Chen WS, Hoodless P, Prezioso VR, et al. 1994. The winged-helix transcription factor HNF-3 beta is required for notochord development in the mouse embryo. Cell 78:575-88
19. Ang SL, Wierda A, Wong D, Stevens KA, Cascio S, et al. 1993. The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of HNF3/forkhead proteins. Development 119:1301-15
20. Rudnick D. 1933. Developmental capacities of the chick lung in chorioallantoic grafts. J. Exp. Zool. 66:125-54
21. Dameron F. 1961. Etude de la morphogénèse de la bronche de l'embryon de Poulet associée à differents mesenchymes en culture in vitro. C. R. Acad. Sci. 262:1642-45
22. Sampaolo G, Sampaolo L. 1959. Observations histologiques sur le poumon de foetus de Cobaye, cultivé in vitro. C. R. Assoc. Anat. 45:707-14
23. Taderera JT. 1967. Control of lung differentiation in vitro. Dev. Biol. 16:489-512
24. Masters JRW. 1976. Epithelial-mesenchymal interaction during lung development: the effect of mesenchymal mass. Dev. Biol 51:98-108
25. Wessells N. 1970. Mammalian lung development: interactions in formation and morphogenesis of tracheal buds. J. Exp. Zool. 175:455-66
26. Lawson KA. 1972. The role of mesenchyme in the morphogenesis and functional differentiation of rat salivary epithelium. J. Embryol. Exp. Morphol. 27:497-513
27. Ball WD. 1974. Development of the rat salivary glands. III. Mesenchymal specificity in the morphogenesis of the embryonic submaxillary and sublingual glands of the rat. J. Exp. Zool. 188:277-88
28. Lawson KA. 1974. Mesenchyme specificity in rodent salivary gland development: the response of salivary epithelium to lung mesenchyme in vitro. J. Embryol. Exp. Morphol. 32:469-93
29. Alescio T, Cassini A. 1962. Induction in vitro of tracheal buds by pulmonary mesenchyme grafted on tracheal epithelium. J. Exp. Zool. 150:83-94
30. Sakakura T, Nishizuka Y, Dawe CJ. 1976. Mesenchyme-dependent morphogenesis and epithelium-specific cytodifferentiation in mouse mammary gland. Science 194:1439-41
31. Shannon JM. 1994. Induction of alveolar type II cell differentiation in fetal tracheal epithelium by grafted distal lung mesenchyme. Dev. Biol. 166:600-14
32. Lin Y, Zhang S, Rehn M, Itaranta P, Tuukkanen J, et al. 2001. Induced repatterning of type XVIII collagen expression in ureter bud from kidney to lung type: association with sonic hedgehog and ectopic surfactant protein C. Development 128:1573-85
33. Shannon JM, Nielsen LD, Gebb SA, Randell SH. 1998. Mesenchyme specifies epithelial differentiation in reciprocal recombinants of embryonic lung and trachea. Dev. Dyn. 212:482-94
34. Grant M, Cutts N, Brody J. 1983. Alterations in lung basement membrane during fetal growth and type 2 cell development. Dev. Biol. 97:173-83
35. Adamson I, King G. 1984. Sex-related differences in cellular composition and surfactant synthesis of developing fetal rat lungs. Am. Rev. Respir. Dis. 129:130-34
36. Bluemink JG, Van Maurik P, Lawson KA. 1976. Intimate cell contacts at the epithelial/mesenchymal interface in embryonic mouse lung. J. Ultrastruct. Res. 55:257-70
37. Shannon JM, Deterding RR. 1997. Epithelial-mesenchymal interactions in lung development. In Lung Growth and Development, ed. JA McDonald, pp. 81-118. New York: Dekker
38. Cardoso WV. 2001. Molecular regulation of lung development. Annu. Rev. Physiol. 63:471-94
39. Warburton D, Schwarz M, Tefft D, Flores-Delgado G, Anderson KD, Cardoso WV. 2000. The molecular basis of lung morphogenesis. Mech. Dev. 92:55-81
40. Gospodarowicz D, Ferrara N, Schweigerer L, Neufeld G. 1987. Structural characterization and biological functions of fibroblast growth factor. Endocr. Rev. 8:95-114
41. McKeehan WL, Wang F, Kan M. 1998. The heparan sulfate-fibroblast growth factor family: diversity of structure and function. Prog. Nucleic Acid Res. Mol. Biol. 59:135-76
42. Guillonneau X, Regnier-Ricard F, Dupuis C, Courtois Y, Mascarelli F. 1997. FGF2-stimulated release of endogenous FGF1 is associated with reduced apoptosis in retinal pigmented epithelial cells. Exp. Cell Res. 233:198-206
43. 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 124:4867-78
44. Urtreger AO. 1993. Developmental localization of the splicing alternatives of fibroblast growth factor receptor-2 (FGFR2). Dev. Biol. 158:475-86
45. Sutherland D, Samakovlis C, Krasnow MA. 1996. branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 87:1091-101
46. 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. 201:125-34
47. Weaver M, Dunn NR, Hogan BL. 2000. Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis. Development 127:2695-704
48. Min H, Danilenko DM, Scully SA, Bolon B, Ring BD, et al. 1998. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev. 12:3156-61
49. Sekine K, Ohuchi H, Fujiwara M, Yamasaki M, Yoshizawa T, et al. 1999. Fgf10 is essential for limb and lung formation. Nat. Genet. 21:138-41
50. Ohtsuka N, Urase K, Momoi T, Nogawa H. 2001. Induction of bud formation of embryonic mouse tracheal epithelium by fibroblast growth factor plus transferrin in mesenchyme-free culture. Dev. Dyn. 222:263-72
51. Shannon JM, Gebb SA, Nielsen LD. 1999. Induction of alveolar type II cell differentiation in embryonic tracheal epithelium in mesenchyme-free culture. Development 126:1675-88
52. Bellusci S, Furuta Y, Rush MG, Henderson R, Winnier G, Hogan BLM. 1997. Involvement of Sonic hedgehog (Shh) in mouse enbryonic lung growth and morphogenesis. Development 124:53-63
53. Urase K, Mukasa T, Igarashi H, Ishii Y, Yasugi S, et al. 1996. Spatial expression of Sonic hedgehog in the lung epithelium during branching morphogenesis. Biochem. Biophys. Res. Commun. 225:161-66
54. Litingtung Y, Lei L, Westphal H, Chiang C. 1998. Sonic hedgehog is essential to foregut development. Nat. Genet. 20:58-61
55. Pepicelli CV, Lewis PM, McMahon AP. 1998. Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Curr. Biol. 8:1083-86
56. Lebeche D, Malpel S, Cardoso WV. 1999. Fibroblast growth factor interactions in the developing lung. Mech. Dev. 86:125-36
57. Sakiyama J, Yamagishi A, Kuroiwa A. 2003. Tbx4-Fgf10 system controls lung bud formation during chicken embryonic development. Development 130:1225-34
58. Cebra-Thomas JA, Bromer J, Gardner R, Lam GK, Sheipe H, Gilbert SF. 2003. T-box gene products are required for mesenchymal induction of epithelial branching in the embryonic mouse lung. Dev. Dyn. 226:82-90
59. 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
60. 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 128:2095-106
61. Weaver M, Batts L, Hogan BL. 2003. Tissue interactions pattern the mesenchyme of the embryonic mouse lung. Dev. Biol. 258:169-84
62. Simonet WS, DeRose ML, Bucay N, Nguyen HQ, Wert SE, et al. 1995. Pulmonary malformation in transgenic mice expressing human keratinocyte growth factor in the lung. Proc. Natl. Acad. Sci. USA 92:12461-65
63. Ulich TR, Yi ES, Longmuir K, Yin S, Bilta R, et al. 1994. Keratinocyte growth factor is a growth factor for type II pneumocytes in vivo. J. Clin. Invest. 93:1298-306
64. Tichelaar JW, Lu W, Whitsett JA. 2000. Conditional expression of fibroblast growth factor-7 in the developing and mature lung. J. Biol Chem. 275:11858-64
65. Shiratori M, Oshika E, Ung LP, Singh G, Shinozuka H, et al. 1996. Keratinocyte growth factor and embryonic rat lung morphogenesis. Am. J. Respir. Cell Mol. Biol. 15:328-38
66. 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. Lung Cell Mol. Physiol. 271:L987-94
67. Cardoso WV, Itoh A, Nogawa H, Mason I, Brody JS. 1997. FGF-1 and FGF-7 induce distinct patterns of growth and differentiation in embryonic lung epithelium. Dev. Dyn. 208:398-405
68. Deterding RR, Jacoby CR, Shannon JM. 1996. Acidic fibroblast growth factor and keratinocyte growth factor stimulate fetal rat pulmonary epithelial growth. Am. J. Physiol. Lung Cell Mol. Physiol. 271:L495-505
69. Chelly N, Mouhieddine-Gueddiche OB, Barlier-Mur AM, Chailley-Heu B, Bourbon JR. 1999. Keratinocyte growth factor enhances maturation of fetal rat lung type II cells. Am. J. Respir. Cell Mol. Biol. 20:423-32
70. Sugahara K, Rubin JS, Mason RJ, Aronsen EL, Shannon JM. 1995. Keratinocyte growth factor increases mRNAs for SP-A and SP-B in rat alveolar type II cells in culture. Am. J. Physiol. Lung Cell Mol. Physiol. 269:L344-50
71. Shannon JM, Pan T, Nielsen LD, Edeen KE, Mason RJ. 2001. Lung fibroblasts improve differentiation of rat type II cells in primary culture. Am. J. Respir. Cell Mol. Biol. 24:235-44
72. Guo L, Degenstein L, Fuchs E. 1996. Keratinocyte growth factor is required for hair development but not for wound healing. Genes Dev. 10:165-75
73. Peters K, Werner S, Liao X, Wert S, Whitsett J, Williams L. 1994. Targeted expression of a dominant-negative FGF receptor blocks branching morphogenesis and epithelial differentiation of the mouse lung. EMBO J. 13:3296-301
74. Celli G, LaRochelle WJ, Mackem S, Sharp R, Merlino G. 1998. Soluble dominant-negative receptor uncovers essential roles for fibroblast growth factors in multi-organ induction and patterning. EMBO J. 17:1642-55
75. Arman E, Haffner-Krausz R, Chen Y, Heath JK, Lonai P. 1998. Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc. Natl. Acad. Sci. USA 95:5082-87
76. 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 96:11895-99
77. De Moerlooze L, Spencer-Dene B, Revest J, Hajihosseini M, Rosewell I, Dickson C. 2000. An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organogenesis. Development 127:483-92
78. Hokuto I, Perl AK, Whitsett JA. 2003. Prenatal, but not postnatal, inhibition of fibroblast growth factor receptor signaling causes emphysema. J. Biol. Chem. 278:415-21
79. Perl AK, Hokuto I, Impagnatiello MA, Christofori G, Whitsett JA. 2003. Temporal effects of Sprouty on lung morphogenesis. Dev. Biol. 258:154-68
80. Weinstein M, Xu X, Ohyama K, Deng CX. 1998. FGFR-3 and FGFR-4 function cooperatively to direct alveogenesis in the murine lung. Development 125:3615-23
81. Ciruna BG, Schwartz L, Harpal K, Yamaguchi TP, Rossant J. 1997. Chimeric analysis of fibroblast growth factor receptor-1 (Fgfr1) function: a role for FGFR1 in morphogenetic movement through the primitive streak. Development 124:2829-41
82. Ornitz DM. 2000. FGFs, heparan sulfate and FGFRs: complex interactions essential for development. BioEssays 22:108-12
83. Mason IJ. 1994. The ins and outs of fibroblast growth factors. Cell 78:547-52
84. Toriyama K, Muramatsu H, Hoshino T, Torii S, Muramatsu T. 1997. Evaluation of heparin-binding growth factors in rescuing morphogenesis of heparitinase-treated mouse embryonic lung explants. Differentiation 61:161-67
85. Roman J, Schuyler W, McDonald JA, Roser S. 1998. Heparin inhibits lung branching morphogenesis: potential role of smooth muscle cells in cleft formation. Am. J. Med. Sci. 316:368-78
86. Izvolsky KI, Shoykhet D, Yang Y, Yu Q, Nugent MA, Cardoso WV. 2003. Heparan sulfate-FGF10 interactions during lung morphogenesis. Dev. Biol. 258:185-200
87. Deepa SS, Umehara Y, Higashiyama S, Itoh N, Sugahara K. 2002. Specific molecular interactions of oversulfated chondroitin sulfate E with various heparin-binding growth factors. Implications as a physiological binding partner in the brain and other tissues. J. Biol. Chem. 277:43707-16
88. Smith C, Hilfer S, Searls R, Nathanson M, Allodoli M. 1990. Effects of β-D-xyloside on differentiation of the respiratory epithelium in the fetal mouse lung. Dev. Biol. 138:42-52
89. Spooner BS, Bassett KE, Spooner BS Jr. 1993. Embryonic lung morphogenesis in organ culture: experimental evidence for a proteoglycan function in the extracellular matrix. Trans. Kans. Acad. Sci. 96:46-55
90. Smith C, Webster E, Nathanson M, Searls R, Hilfer S. 1990. Altered patterns of proteoglycan deposition during maturation of the fetal mouse lung. Cell Diff. Dev. 32:83-96
91. 90a. Shannon JM, McCormick-Shannon K, Burhans MS, Shangguan X, Srivastava K, Hyatt BA. 2003. Chondroitin sulfate proteoglycans are required for lung growth and morphogenesis in vitro. Am. J. Physiol. Lung Cell Mol. Physiol. In press
92. Ingham PW, McMahon AP. 2001. Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15:3059-87
93. McMahon AP, Ingham PW, Tabin CJ. 2003. Developmental roles and clinical significance of hedgehog signaling. Curr. Top. Dev. Biol. 53:1-114
94. 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
95. Miller LA, Wert SE, Whitsett JA. 2001. Immunolocalization of sonic hedgehog (Shh) in developing mouse lung. J. Histochem. Cytochem. 49:1593-604
96. Chen Y, Strahl G. 1996. Dual roles for patched in sequestering and transducing Hedgehog. Cell 87:553-63
97. Chuang PT, McMahon AP. 1999. Vertebrate Hedgehog signalling modulated by induction of a Hedgehog-binding protein. Nature 397:617-21
98. Chuang PT, Kawcak T, McMahon AP. 2003. Feedback control of mammalian Hedgehog signaling by the Hedgehog-binding protein, Hip1, modulates Fgf signaling during branching morphogenesis of the lung. Genes Dev. 17:342-47
99. Mahlapuu M, Enerback S, Carlsson P. 2001. Haploinsufficiency of the forkhead gene Foxf1, a target for sonic hedgehog signaling, causes lung and foregut malformations. Development 128:2397-406
100. Lim L, Kalinichenko W, Whitsett JA, Costa RH. 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:L1012-22
101. Platt KA, Michaud J, Joyner AL. 1997. Expression of the mouse Gli and Ptc genes is adjacent to embryonic sources of hedgehog signals suggesting a conservation of pathways between flies and mice. Mech. Dev. 62:121-35
102. Grindley JC, Bellusci S, Perkins D, Hogan BLM. 1997. Evidence for the involvement of the Gli gene family in embryonic mouse lung development. Dev. Biol. 188:337-48
103. Park HL, Bai C, Platt KA, Matise MP, Beeghly A, et al. 2000. Mouse Gli1 mutants are viable but have defects in SHH signaling in combination with a Gli2 mutation. Development 127:1593-605
104. Wodarz A, Nusse R. 1998. Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 14:59-88
105. Huelsken J, Birchmeier W. 2001. New aspects of Wnt signaling pathways in higher vertebrates. Curr. Opin. Genet. Dev. 11:547-53
106. Shu W, Jiang YQ, Lu MM, Morrisey EE. 2002. Wnt7b regulates mesenchymal proliferation vascular development in the lung. Development 129:4831-42
107. 105a. Mucenski ML, Wert SE, Natian JM, Loudy DE, Huelsken J, et al. 2003. Beta-catenin is required for the specification of proximal/distal cell fate during lung morphogenesis. J. Biol. Chem. In press
108. Slusarski DC, Corces VG, Moon RT. 1997. Interaction of Wnt a Frizzled homologue triggers G-protein-linked phosphatidylinositol signalling. Nature 390:410-13
109. Li C, Xiao J, Hormi K, Borok Z, Minoo P. 2002. Wnt5a participates in distal lung morphogenesis. Dev. Biol. 248:68-81
110. Hogan BL. 1996. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10:1580-94
111. Weaver M, Yingling JM, Dunn NR, Bellusci S, Hogan BL. 1999. Bmp signaling regulates proximal-distal differentiation of endoderm in mouse lung development. Development 126:4005-15
112. Bellusci S, Henderson R, Winnier G, Oikawa T, Hogan BLM. 1996. Evidence from normal expression and targeted misexpression that Bone Morphogenetic Protein-4 (Bmp-4) plays a role in mouse embryonic lung morphogenesis. Development 122:1693-702
113. 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. 222:667-80
114. Shi W, Zhao J, Anderson KD, Warburton D. 2001. Gremlin negatively modulates BMP-4 induction of embryonic mouse lung branching morphogenesis. Am. J. Physiol. Lung Cell Mol. Physiol. 280:L1030-39
115. Hyatt BA, Shangguan X, Shannon JM. 2002. BMP4 modulates fibroblast growth factor-mediated induction of proximal and distal lung differentiation in mouse embryonic tracheal epithelium in mesenchyme-free culture. Dev. Dyn. 225:153-65
116. Bragg AD, Moses HL, Serra R. 2001. Signaling to the epithelium is not sufficient to mediate all of the effects of transforming growth factor beta and bone morphogenetic protein 4 on murine embryonic lung development. Mech. Dev. 109:13-26
117. Liu Y, Hogan BL. 2002. Differential gene expression in the distal tip endoderm of the embryonic mouse lung. Gene Expr. Patterns 2:229-33
118. Lin S, Shannon JM. 2002. Microarray analysis of gene expression in the embryonic lung. Chest 121:808-81