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Am J Physiol Lung Cell Mol Physiol 282: L1253-L1265, 2002. First published January 12, 2002; doi:10.1152/ajplung.00463.2001
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Vol. 282, Issue 6, L1253-L1265, June 2002

Wild-type levels of the mouse Forkhead Box f1 gene are essential for lung repair

Vladimir V. Kalinichenko1, Yan Zhou1, Brian Shin1, Donna Beer Stolz2, Simon C. Watkins2, Jeffrey A. Whitsett3, and Robert H. Costa1

1 Department of Molecular Genetics, College of Medicine, University of Illinois at Chicago, Chicago, Illinois 60607-7170; 2 Center for Biologic Imaging, University of Pittsburgh, Pittsburgh, Pennsylvania 15261; and 3 Division of Pulmonary Biology, Children's Hospital Medical Center, Cincinnati, Ohio 45229-3039

The Forkhead Box (Fox) family of transcription factors plays important roles in regulating expression of genes involved in cellular proliferation and differentiation. In a previous study, we showed that newborn foxf1(+/-) mice with diminished Foxf1 levels exhibited abnormal formation of pulmonary alveoli and capillaries and died postnatally. Interestingly, surviving newborn foxf1(+/-) mice exhibited increased pulmonary Foxf1 levels and normal adult lung morphology, suggesting that wild-type Foxf1 levels are required for lung development and function. The present study was conducted to determine whether adult foxf1(+/-) mice were able to undergo lung repair similar to that observed in wild-type mice. We demonstrated that adult foxf1(+/-) mice died from severe lung hemorrhage after butylated hydroxytoluene (BHT) lung injury and that this phenotype was associated with a 10-fold decrease in pulmonary Foxf1 expression and increased alveolar endothelial cell apoptosis that disrupted capillary integrity. Furthermore, BHT-induced lung hemorrhage of adult foxf1(+/-) mice was associated with a drastic reduction in expression of the Flk-1, bone morphogenetic protein-4, surfactant protein B, platelet endothelial cell adhesion molecule, and vascular endothelial cadherin genes, whereas the expression of these genes was either transiently diminished or increased in wild-type lungs after BHT injury. Because these proteins are critical for lung morphogenesis and endothelial homeostasis, their decreased mRNA levels are likely contributing to BHT-induced lung hemorrhage in foxf1(+/-) mice. Collectively, our data suggest that sustained expression of Foxf1 is essential for normal lung repair and endothelial cell survival in response to pulmonary cell injury.

winged helix deoxyribonucleic acid-binding domain; Flk-1; bone morphogenetic protein-4; surfactant protein B; platelet endothelial cell adhesion molecule-1; vascular endothelial cadherin; butylated hydroxytoluene lung injury; endothelial cells


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