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Development, Vol 122, Issue 6 1693-1702, Copyright © 1996 by Company of Biologists


JOURNAL ARTICLES

Evidence from normal expression and targeted misexpression that bone morphogenetic protein (Bmp-4) plays a role in mouse embryonic lung morphogenesis

S Bellusci, R Henderson, G Winnier, T Oikawa and BL Hogan
Howard Hughes Medical Institute, Department of Cell Biology, Vanderbilt University Medical Center, Nashville, TN 37232-2175, USA.

Epithelial-mesenchymal interactions are critical for the branching and differentiation of the lung, but the mechanisms involved are still unclear. To investigate this problem in mouse embryonic lung, we have studied the temporal and spatial expression of genes implicated in the morphogenesis of other organs. At 11.5 days p.c., hepatocyte nuclear factor-3beta (Hnf-3beta) is expressed uniformly throughout the epithelium, while Wnt-2 expression is confined to the distal mesenchyme. Sonic hedgehog (Shh) transcripts are found throughout the epithelium, with high levels in the distal tips of the terminal buds, while bone morphogenetic protein-4 (Bmp-4) transcripts are localized at high levels in the distal tips of the epithelium, with lower levels in the adjacent mesenchyme. Epithelial expression is also seen for Bmp-7, but transcripts are less dramatically upregulated at the distal tips. The Type I Bone morphogenetic protein receptor gene (Bmpr/Tfr-11/Brk-1) is expressed at low levels in the epithelium and in the distal mesenchyme. To investigate the role of Bmp-4 in lung development, we have misexpressed the gene throughout the distal epithelium of transgenic lungs using a surfactant protein C enhancer/promoter. From 15.5 days p.c., transgenic lungs are smaller than normal, with grossly distended terminal buds and, at birth, contain large air-filled sacs which do not support normal lung function. Labeling with BrdU reveals an inhibition of epithelia] proliferation in 15.5 days p.c. transgenic lungs. A small but significant stimulation of proliferation of mesenchymal cells is also observed, but this is accompanied by an increase in cell death. In situ hybridization with riboprobes for the proximal airway marker, CC10, and the distal airway marker, SP-C, shows normal differentiation of bronchiolar Clara cells but a reduction in the number of differentiated Type II cells in transgenic lungs. A model is proposed for the role of BMP4 and other signalling molecules in embryonic lung morphogenesis.
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DevelopmentHome page
T Ito, N Udaka, T Yazawa, K Okudela, H Hayashi, T Sudo, F Guillemot, R Kageyama, and H Kitamura
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DevelopmentHome page
L Karlsson, P Lindahl, J. Heath, and C Betsholtz
Abnormal gastrointestinal development in PDGF-A and PDGFR-(alpha) deficient mice implicates a novel mesenchymal structure with putative instructive properties in villus morphogenesis
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M Weaver, N. Dunn, and B. Hogan
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Development, January 6, 2000; 127(12): 2695 - 2704.
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L. Gerlach, M. Hutson, J. Germiller, D Nguyen-Luu, J. Victor, and K. Barald
Addition of the BMP4 antagonist, noggin, disrupts avian inner ear development
Development, January 1, 2000; 127(1): 45 - 54.
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Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
W. Shi, N. Heisterkamp, J. Groffen, J. Zhao, D. Warburton, and V. Kaartinen
TGF-beta 3-null mutation does not abrogate fetal lung maturation in vivo by glucocorticoids
Am J Physiol Lung Cell Mol Physiol, December 1, 1999; 277(6): L1205 - L1213.
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B. B. Brimhall, K. A. Sikorski, J. Torday, A. Shahsafaei, K. J. Haley, and M. E. Sunday
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R. J. Metzger and M. A. Krasnow
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Science, June 4, 1999; 284(5420): 1635 - 1639.
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A. T. Clark and J. F. Bertram
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Am. J. Respir. Cell Mol. Bio.Home page
L. J. Muglia, D. S. Bae, T. T. Brown, S. K. Vogt, J. G. Alvarez, M. E. Sunday, and J. A. Majzoub
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DevelopmentHome page
S. Quaggin, L Schwartz, S Cui, P Igarashi, J Deimling, M Post, and J Rossant
The basic-helix-loop-helix protein pod1 is critically important for kidney and lung organogenesis
Development, January 12, 1999; 126(24): 5771 - 5783.
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DevelopmentHome page
M Weaver, J. Yingling, N. Dunn, S Bellusci, and B. Hogan
Bmp signaling regulates proximal-distal differentiation of endoderm in mouse lung development
Development, January 9, 1999; 126(18): 4005 - 4015.
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S Noramly, A Freeman, and B. Morgan
beta-catenin signaling can initiate feather bud development
Development, January 8, 1999; 126(16): 3509 - 3521.
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DevelopmentHome page
O Pabst, R Zweigerdt, and H. Arnold
Targeted disruption of the homeobox transcription factor Nkx2-3 in mice results in postnatal lethality and abnormal development of small intestine and spleen
Development, January 5, 1999; 126(10): 2215 - 2225.
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DevelopmentHome page
M. Solloway and E. Robertson
Early embryonic lethality in Bmp5;Bmp7 double mutant mice suggests functional redundancy within the 60A subgroup
Development, January 4, 1999; 126(8): 1753 - 1768.
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Am. J. Respir. Cell Mol. Bio.Home page
R. Mollard and M. Dziadek
A Correlation between Epithelial Proliferation Rates, Basement Membrane Component Localization Patterns, and Morphogenetic Potential in the Embryonic Mouse Lung
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Genes Dev.Home page
M. Treier, A. S. Gleiberman, S. M. O'Connell, D. P. Szeto, J. A. McMahon, A. P. McMahon, and M. G. Rosenfeld
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DevelopmentHome page
L Laforest, C. Brown, G Poleo, J Geraudie, M Tada, M Ekker, and M. Akimenko
Involvement of the sonic hedgehog, patched 1 and bmp2 genes in patterning of the zebrafish dermal fin rays
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M Weinstein, X Xu, K Ohyama, and C. Deng
FGFR-3 and FGFR-4 function cooperatively to direct alveogenesis in the murine lung
Development, January 9, 1998; 125(18): 3615 - 3623.
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D. Roberts, D. Smith, D. Goff, and C. Tabin
Epithelial-mesenchymal signaling during the regionalization of the chick gut
Development, January 8, 1998; 125(15): 2791 - 2801.
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DevelopmentHome page
H Ohmichi, U Koshimizu, K Matsumoto, and T Nakamura
Hepatocyte growth factor (HGF) acts as a mesenchyme-derived morphogenic factor during fetal lung development
Development, January 4, 1998; 125(7): 1315 - 1324.
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J Jernvall, T Aberg, P Kettunen, S Keranen, and I Thesleff
The life history of an embryonic signaling center: BMP-4 induces p21 and is associated with apoptosis in the mouse tooth enamel knot
Development, January 1, 1998; 125(2): 161 - 169.
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GeneticsHome page
An Extensive 3' Regulatory Region Controls Expression of Bmp5 in Specific Anatomical Structures of the Mouse Embryo
Genetics, January 1, 1998; 148(1): 401 - 408.



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Genes Dev.Home page
K H Kaestner, D G Silberg, P G Traber, and G Schutz
The mesenchymal winged helix transcription factor Fkh6 is required for the control of gastrointestinal proliferation and differentiation.
Genes & Dev., June 15, 1997; 11(12): 1583 - 1595.
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G E Winnier, L Hargett, and B L Hogan
The winged helix transcription factor MFH1 is required for proliferation and patterning of paraxial mesoderm in the mouse embryo.
Genes & Dev., April 1, 1997; 11(7): 926 - 940.
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EndocrinologyHome page
E. A. Catlin, V. C. Tonnu, R. G. Ebb, B. A. Pacheco, T. F. Manganaro, R. M. Ezzell, P. K. Donahoe, and J. Teixeira
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DevelopmentHome page
S Bellusci, J Grindley, H Emoto, N Itoh, and B. Hogan
Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung
Development, January 12, 1997; 124(23): 4867 - 4878.
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DevelopmentHome page
P Lindahl, L Karlsson, M Hellstrom, S Gebre-Medhin, K Willetts, J. Heath, and C Betsholtz
Alveogenesis failure in PDGF-A-deficient mice is coupled to lack of distal spreading of alveolar smooth muscle cell progenitors during lung development
Development, January 10, 1997; 124(20): 3943 - 3953.
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Cold Spring Harb Symp Quant BiolHome page
B.L.M. Hogan, J. Grindley, S. Bellusci, N.R. Dunn, H. Emoto, and N. Itoh
Branching Morphogenesis of the Lung: New Models for a Classical Problem
Cold Spring Harb Symp Quant Biol, January 1, 1997; 62(0): 249 - 256.
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DevelopmentHome page
S Bellusci, Y Furuta, M. Rush, R Henderson, G Winnier, and B. Hogan
Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis
Development, January 1, 1997; 124(1): 53 - 63.
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DevelopmentHome page
A. Barlow and P. Francis-West
Ectopic application of recombinant BMP-2 and BMP-4 can change patterning of developing chick facial primordia
Development, January 1, 1997; 124(2): 391 - 398.
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B L Hogan
Bone morphogenetic proteins: multifunctional regulators of vertebrate development.
Genes & Dev., July 1, 1996; 10(13): 1580 - 1594.
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S. Monkley, S. Delaney, D. Pennisi, J. Christiansen, and B. Wainwright
Targeted disruption of the Wnt2 gene results in placentation defects
Development, January 11, 1996; 122(11): 3343 - 3353.
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Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
V. V. Kalinichenko, Y. Zhou, B. Shin, D. B. Stolz, S. C. Watkins, J. A. Whitsett, and R. H. Costa
Wild-type levels of the mouse Forkhead Box f1 gene are essential for lung repair
Am J Physiol Lung Cell Mol Physiol, June 1, 2002; 282(6): L1253 - L1265.
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