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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				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.

				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. [Abstract] [PDF]

				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. [Abstract] [PDF]

				E. A. Catlin, V. C. Tonnu, R. G. Ebb, B. A. Pacheco, T. F. Manganaro, R. M. Ezzell, P. K. Donahoe, and J. Teixeira Mullerian Inhibiting Substance Inhibits Branching Morphogenesis and Induces Apoptosis in Fetal Rat Lung Endocrinology, February 1, 1997; 138(2): 790 - 796. [Abstract] [Full Text] [PDF]

				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. [Abstract] [PDF]

				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. [Abstract] [PDF]

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				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. [Abstract] [PDF]

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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. [Abstract] [PDF]

				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. [Abstract] [Full Text] [PDF]