C/EBPα is required for lung maturation at birth

Development

Volumn 133, Issue 6, 2006, Pages 1155-1164

  Martis, Prithy C ^a   Whitsett, Jeffrey A ^a   Xu, Yan ^a   Perl, Anne Karina T ^a   Wan, Huajing ^a   Ikegami, Machiko ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

ABCA3; CCAAT enhancer binding protein ; FOXA2; Lung maturation; Mouse; Pulmonary surfactant; Respiratory epithelial cell differentiation; TTF1

Indexed keywords

ATP BINDING CASSETTE TRANSPORTER 3; CCAAT ENHANCER BINDING PROTEIN ALPHA; FAS ANTIGEN; HEPATOCYTE NUCLEAR FACTOR 3BETA; LUNG SURFACTANT; LUNG SURFACTANT EXTRACT; SP A PROTEIN; SP B PROTEIN; SP C PROTEIN; SP D PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TITF1; TRANSFORMING GROWTH FACTOR BETA2; UNCLASSIFIED DRUG; FOXA2 PROTEIN, MOUSE; LIPID; TRANSFORMING GROWTH FACTOR BETA;

ADAPTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREATHING MECHANICS; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIUM CELL; FETUS; FETUS LUNG MATURATION; GENE DELETION; GENETIC CODE; GENETIC PREDISPOSITION; GENETIC RISK; GESTATIONAL AGE; HOMEOSTASIS; LAMELLAR BODY; LIPOGENESIS; LUNG ALVEOLUS CELL; LUNG FUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RESPIRATORY FAILURE; ANIMAL; BIOSYNTHESIS; CYTOLOGY; DNA MICROARRAY; ENZYMOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; LUNG; METABOLISM; NEWBORN; PREGNANCY; PRENATAL DEVELOPMENT; SMOOTH MUSCLE; TIME; TRANSGENIC MOUSE; VASCULARIZATION;

ANIMALIA;

ANIMALS; ANIMALS, NEWBORN; CCAAT-ENHANCER-BINDING PROTEIN-ALPHA; CELL DIFFERENTIATION; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEPATOCYTE NUCLEAR FACTOR 3-BETA; LIPIDS; LUNG; MICE; MICE, TRANSGENIC; MUSCLE, SMOOTH; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREGNANCY; PROTEIN BIOSYNTHESIS; TIME FACTORS; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA2;

EID: 33645729295     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02273     Document Type: Article

References (72)

1. Alam, T., An, M. R. and Papaconstantinou, J. (1992). Differential expression of three C/EBP isoforms in multiple tissues during the acute phase response. J. Biol. Chem. 267, 5021-5024.
2. Attisano, L. and Wrana, J. L. (2000). Smads as transcriptional co-modulators. Curr. Opin. Cell Biol. 12, 235-243.
3. Bachurski, C. J., Yang, G. H., Currier, T. A., Gronostajski, R. M. and Hong, D. (2003). Nuclear factor I/thyroid transcription factor 1 interactions modulate surfactant protein C transcription. Mol. Cell. Biol. 23, 9014-9024.
4. Barlier-Mur, A. M., Chailley-Heu, B., Pinteur, C., Henrion-Caucle, A., Delacourt, C. and Bourbon, J. R. (2003). Maturational factors modulate transcription factors CCAAT/enhancer-binding proteins alpha, beta, delta, and peroxisome proliferator-activated receptor-gamma in fetal rat lung epithelial cells. Am. J. Respir Cell Mol. Biol. 29, 620-626.
5. Bartlett, G. R. (1959). Phosphorous assay in column chromatography. J. Biol. Chem. 234, 466-468,
6. Bartram, U. and Speer, C. P (2004). The role of transforming growth factor beta in lung development and disease. Chest 125, 754-765.
7. Besnard, V., Wert, S. E., Hull, W. M. and Whitsett, J. A. (2004). Immunohistochemical localization of Foxa1 and Foxa2 in mouse embryos and adult tissues. Gene Expr Patterns 5, 193-208,
8. Birkenmeier, E. H., Gwynn, B., Howard, S., Jerry, J., Gordon, J. I., Landschulz, W. H. and McKnight, S. L. (1989). Tissue-specific expression, developmental regulation, and genetic mapping of the gene encoding CCAAT/enhancer binding protein. Genes Dev 3, 1146-1156.
9. Burgess-Beusse, B. L. and Darlington, G. J. (1998). C/EBPα is critical for the neonatal acute-phase response to inflammation. Mol. Cell. Biol. 18, 7269-7277.
10. Cao, Z., Umek, R. M. and McKnight, S. L. (1991). Regulated expression of three C/EBP isoforms during adipose conversion of 3T3-L1 cells. Genes Dev 5, 1538-1552.
11. Cardoso, W. V. (2001). Molecular regulation of lung development. Annu. Rev Physiol. 63, 471-494.
12. Cardoso, W. V., Itolh, A., Nogawa, H., Mason, I. and Brody, J. S. (1997). FGF-1 and FGF-7 induce distinct patterns of growth and differentiation in embryonic lung epithelium. Dev Dyn. 208, 398-405.
13. Cassel, T. N. and Nord, M. (2003). C/EBP transcription factors in lung epithelium. Am. J. PhysioL 285, 1-773-1-781.
14. Clark, J. C., Wert, S. E., Bachurski, C. J., Stahlman, M. T., Stripp, B. R., Weaver, T E. and Whitsett, J. A. (1995). Targeted disruption of the surfactant protein B gene disrupts surfactant homeostasis, causing respiratory failure in newborn mice. Proc. Natl. Acad. Sci. USA 92, 7794-7798,
15. Clark, J. C., Tichelaar, J. W., Wert, S. E., Itoh, N., Perl, A. K., Stahlman, M.T. and Whitsett, J. A. (2001). FGF-10 disrupts lung morphogenesis and causes pulmonary adenomas in vivo. Am. J. Physiol. 280, 1-705-1-715.
16. Das, D. K. (1980). Fatty acid synthesis in fetal lung. Biochem. Biophys. Res. Commun. 92, 867-87 5.
17. deFelice, M., Silberschmidt, D., DiLauro, R., Xu, Y., Wert, S. E., Weaver, T E., Bachurski, C. J., Clark, J. C. and Whitsett, J. A. (2003). TTF-1 phosphorylation is required for peripheral lung morphogenesis, perinatal survival, and tissue-specific gene expression. J. Biol. Chem. 278, 35574-35583.
18. De Simone, V. and Cortese, R. (1992). Transcription factors and liver-specific genes. Biochim. Biophys. Acta 1132, 119-126.
19. Dennis, G., Jr, Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C. and Lempicki, R. A. (2003). DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4, P3.
20. Dranoff, G., Crawford, A. D., Sadelain, M., Ream, B., Rashid, A., Bronson, R. T., Dickersin, G. R., Bachurski, C. J., Mark, E. L., Whitsett, J. A. et al. (1994). Involvement of granulocyte-macrophage colony-stimulating factor in pulmonary homeostasis. Science 264, 713-716.
21. Flodby, P., Barlow, C., Kylefjord, H., Ahrlund-Richter, L. and Xanthopoulos, K. G. (1996). Increased hepatic cell proliferation and lung abnormalities in mice deficient in CCAAT/enhancer binding protein alpha. J. Biol. Chem. 271, 24753-24760.
22. Glasser, S. W., Burhans, M. S., Korfhagen, T. R., Na, C. L., Sly, P. D., Ross, G. F, Ikegami, M. and Whitsett, J. A. (2001). Altered stability of pulmonary surfactant in SP-C deficient mice. Proc. Natl. Acad. Sci. USA 98, 6366-6371.
23. Hallman, M. and Gluck, L. (1976). Phosphaticylglycerol in lung surfactant. III. Possible modifier of surfactant function. J. Lipid Res. 17, 257-262.
24. Halmos, B., Huettner, C. S., Kocher, O., Ferenczi, K., Karp, D. D. and Tenen, D. G. (2002). Down-regulation and antiproliferative role of C/ EBPalpha in lung cancer, Cancer Res. 62, 528-534.
25. He, Y and Crouch, E. (2002). Surfactant protein D gene regulation. Interactions among the conserved CCAAT/enhancer-binding protein elements. J. Biol. Chem. 277, 19530-19537.
26. Ikegami, M., Dhami, R. and Schuchman, E. H. (2003). Alveolar lipoproteinosis in an acid sphingomyelinase-deficient mouse model of Niemann-Pick disease. Am. J. Physiol. 284, 1-518-1-525.
27. Irizarry; R. A., Bolstad, B. M., Collin, F., Cope, L. M., Hobbs, B. and Speed, T. R (2003a). Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15.
28. Irizarry; R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U. and Speed, T. P. (2003b). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4,249-264.
29. Jaskoll, T., Choy, H. A. and Melnick, M. (1996). The glucocorticoid-glucocorticoid receptor signal transduction pathway, transforming growth factor-beta, and embryonic mouse lung development in vivo. Pediatr. Res. 39, 749-759.
30. 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.
31. Lebeche, D., Malpel, S. and Cardoso, W. V. (1999). Fibroblast growth factor interactions in the developing lung. Mech. Dev 86, 125-136.
32. Lee, Y. H., Sauer, B., Johnson, P. F. and Gonzalez, F. J. (1997). Disruption of the c/ebp alpha gene in adult mouse liver MoL Cell. Biol. 17, 6014-6022.
33. Lekstrom-Himes, J. and Xanthopoulos, K. G. (1998). Biological role of the CCAAT/enhancer-binding protein family of transcription factors. J. Biol. Chem. 273, 28545-28548.
34. Li, F., Rosenberg, E., Smith, C. I., Notarfrancesco, K., Reisher, S. R., Shuman, H. and Feinstein, S. I. (1995). Correlation of expression of transcription factor C/EBP alpha and surfactant protein genes in lung cells. Am. J. Physiol. 269, L241 -L247.
35. MacDougald, O. A. and Lane, M. D. (1995). Transcriptional regulation of gene expression during adipocyte differentiation. Annu. Rev Biochem. 64, 345-373.
36. Mason, R. J., Nellenbogen, J. and Clements, J. A. (1976). Isolation of disaturated phosphatidylcholine with osmium tetroxide. J. Lipid Res. 17, 281-284.
37. Mason, R. J., Pan, T., Edeen, K. E., Nielsen, L. D., Zhang, E, Longphre, M., Eckart, M. R. and Neben, S. (2003). Keratinocyte growth factor and the transcription factors C/EBP alpha, C/EBP delta, and SREBP-1 c regulate fatty acid synthesis in alveolar type II cells. J. Clin. Invest. 112, 244-255.
38. Massagué, J. (1998). TGF-beta signal transduction. Annu. Rev. Biochem. 67, 753-791.
39. Matlapudi, A., Wang, M., Rosenberg, E., Ewing, J. R. and Feinstein, S. I. (2002). A role for C/EBP delta in human surfactant protein A (SP-A) gene expression. Biochim. Biophys. Acta 1575, 91-98.
40. 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.
41. Morrisey, E. E., Ip, H. S., Lu, M. M. and Parmacelk, M. S. (1996). GATA-6: a zinc finger transcription factor that is expressed in multiple cell lineages derived from lateral mesoderm. Dev Biol. 177, 309-322.
42. 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. Bio/. Chem. 278, 40231-40238.
43. Nogee, L. M., Wert, S. E., Proffit, S. A., Hull, W. M. and Whitsett, J. A. (2000). Allelic heterogeneity in hereditary surfactant protein B (SP-B) deficiency. Am. J. Respir. Crit. Care Med. 161, 973-981.
44. Nord, M., Lag, M., Cassel, T. N., Randmark, M., Becher, R., Barnes, H. J., Schwarze, R E., Gustafsson, J. A. and Lund, J. (1998). Regulation of CCSP (PC-BP/uteroglobin) expression in primary cultures of lung cells: involvement of C/EBP. DNA Cell Biol. 17, 481-492.
45. Perl, A. K., Tichelaar, J. W. and Whitsett, J. A. (2002). Conditional gene expression in the respiratory epithelium of the mouse. Transgenic Res. 11, 21-29.
46. Perl, A. K. T., Wert, S. E., Loudly, D. E., Shan, Z., Blair, P. A. and Whitsett, J. A. (2005). Conditional recombination reveals distinct subsets of epithelial cells in trachea, bronchi, and alveoli. Am. J. Respir. Cell Mol. Biol. 33, 455-462.
47. Pope, T. S. and Rooney, S. A. (1987). Effects of glucocorticoid and thyroid hormones on regulatory enzymes of fatty acid synthesis and glycogen metabolism in developing fetal rat lung. Biochim. Biophys. Acta. 918, 141-148.
48. Portnoy, J., Curran-Everett, D. and Mason, R. J. (2004). Keratinocyte growth factor stimulates alveolar type II cell proliferation through the extracellular signal-regulated kinase and phosphaticlylinositol 3-OH pathways. Am. J. Respir Cell Mol. Biol. 30, 901-907.
49. Ramji, D. P. and Foka, P. (2002). CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem. J. 365, 561-575.
50. Randell, S. H. and Young, S. L. (2004). In Fetal and Neonatal Physiology (ed. R. A. Polin, W. W. Fox and S. H. Abman), pp. 1034-1040. Philadelphia: Saunders.
51. Ridsdale, R. and Post, M. (2004). Surfactant lipid synthesis and lamellar body formation in glycogen-laden type II cells. Am. J. PhysioL 287, 1-743-1-751.
52. Rosen, E. D. and Spigelman, B. M. (2000). Molecular regulation of adipogenesis. Annu. Rev Cell Dev Biol. 16, 145-17 1.
53. Rosenberg, E., Li, F., Reisher, S. R., Wang, M., Gonzales, L. W., Ewing, J. R., Malek, S., Ballard, P. L., Notarfrancesco, K., Shuman, H. et al. (2002). Members of the C/EBP transcription factor family stimulate expression of the human and rat surfactant protein A (SP-A) genes. Biochim. Biophys. Acta 1575, 82-90.
54. Sa, G., Das, T and Mukherjea, M. (1990). Relationship between fatty acid synthesis, transport and total lipid content during human fetal lung development. Indian J. Biochem. Biophys. 27, 43-47.
55. Shi, Y. and Massague, J. (2003). Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113, 685-700.
56. Shulenin, S., Nogee, L. M., Annilo, T., Wert, S. E., Whitsett, J. A. and Dean, M. (2004). ABC43 gene mutations in newborns with fatal surfactant deficiency N. Engl. J. Med. 350, 1296-1303.
57. Stahlman, M. T, Gray, M. E. and Whitsett, J. A. (1996). Expression of thyroid transcription factor-1 (TTF-1) in fetal and neonatal human lung. J. Histochern. Cytochem. 44, 673-678.
58. Stahlman, M. T, Gray, M. E., Hull, W. M. and Whitsett, J. A. (2002). Immunolocalization of surfactant protein-D (SP-D) in human fetal, newborn, and adult tissues. J. Histochem. Cytochem. 50, 651-660.
59. Sugahara, K., Sadohara, T., Sugita, M., Iyama, K. and Takiguchi, M. (1999). Differential expression of CCAAT enhancer binding protein family in rat alveolar epithelial cell proliferation and in acute lung injury. Cell Tissue Res. 297, 261-270.
60. Sugahara, K., Iyama, K., Kimura, T., Sano, K., Darlington, G. J., Akiba, T. and Takiguchi, M. (2001). Mice lacking CCAAT/ enhancer binding protein-α show hyperproliferation of alveolar type II cells and increased surfactant protein mRNAs. Cell Tissue Res. 306, 57-63.
61. Takiguchi, M. (1998). The C/EBP family of transcription factors in the liver and other organs. Int. J. Exp. Pathol. 79, 369-391.
62. Tong, Q., Tsai, J., Tan, G., Dalgin, G. and Hotamisligil, G. S. (2005). Interaction between GATA and the C/EBP family of transcription factors is critical in GATA-mediated suppression of adipocyte differentiation. MoL Cell. BioL 25, 706-715.
63. Tusher, V. G., Tibshirani, R. and Chu, G. (2001). Significance analysis of microarrays applies to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98, 5116-5121.
64. Wan, H., Xu, Y., Ikegami, M., Stahlman, M. T, Kaestner, K. H., Ang, S. L. and Whitsett, J. A. (2004). Foxa2 is required for transition to air breathing at birth. Proc. Natt. Acad. Sci. USA 101, 14449-14454.
65. 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 Foxal and Foxa2 during lung morphogenesis. J. Biol. Chem. 280, 13809-13816.
66. Wang, N. D., Finegold, M. J., Bradley, A., Ou, C. N., Abdelsayed, S. V., Wilde, M. D., Taylor, L. R., Wilson, D. R. and Darlington, G. J. (1995). Impaired energy homeostasis in C/EBP alpha knockout mice. Science 269, 1108-1112.
67. Whitsett, J. A., Budden, A., Hull, W. M., Clark, J. C. and O'Reilly, M. A. (1992). Transforming growth factor-beta inhibits surfactant protein A expression in vitro. Biochim. Biophys. Acta 1123, 257-262.
68. Whitsett, J. A., Wert, S. E. and Trapnell, B. C. (2004). Genetic disorders influencing lung formation and function at birth. Hum. Mol. Genet. 13, R207-R215.
69. Xu, Y., Clark, J. C., Aronow, B. J., Dey, C. R., Liu, C., Wooldridge, J. L. and Whitsett, J. A. (2003). Transcriptional adaptation to cystic fibrosis transmembrane conductance regulator deficiency. J. Biol. Chem. 278, 7674-7682.
70. Yano, T., Mason, R. J., Pan, T, Deterding, R. R., Nielsen, L. D. and Shannon, J. M. (2000). KGF regulates pulmonary elpithelial proliferation and surfactant protein gene expression in adult rat lung. Am. J. Physiol. 279, L1146-L1158.
71. Zhang, F., Pan, T., Nielsen, L. D. and Mason, R. J. (2004). Lipogenesis in fetal rat lung: importance of C/EBPalpha, SREBP-1c, and stearoyl-CoA desaturase. Am. J. Respir. Cell Mol. Biol. 30, 174-183.
72. Zhou, L., Dey, C. R., Wert, S. E. and Whitsett, J. A. (1996). Arrested lung morphogenesis in transgenic mice bearing an SP-C-TGF-β1 chimeric gene. Dev Biol. 175, 227-238,