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Gene Expression in Alveolar Development

  • Jacques R. Bourbon
Chapter
Part of the Clinical Physiology Series book series (CLINPHY)

Abstract

Respiratjory epithelium, strictly defined as the epithelium of distal lung that lines walls of respiratory bronchioles and alveoli, is composed of two cell types known as alveolar type I and II cells or type I and II pneumocytes. The former is a flat, attenuated, terminally differentiated cell through which air—blood gas exchanges occur. The latter is a cuboidal cell that elaborates and releases all the phospholipid and protein components of pulmonary surfactant (87, 113); it also serves as a progenitor cell for itself and for the type I cell that does not divide (64). Although it belongs to the bronchiolar epithelium at the junction of conducting and respiratory portions of the lung, the nonciliated bronchiolar, or Clara, cell shares features with the type II pneumocyte since, in addition to secretory products proper to this cell type, it also releases some surfactant protein components (87). It also represents the progenitor for itself and for the basal and ciliated cells in the renewal process of the epithelium (64). These cell types, however, represent only a small part of all epithelial lung cell phenotypes. In total, pulmonary epithelium comprises at least 11 differentiated cell types that, to a large extent, determine lung function. To understand phenotypic differentiation in the distal parts of the lung, we need to investigate (1) how lung-specific identity is determined, and (2), how distal cell lineages are specified relative to those of more proximal parts of the lung, the epithelial cells of conducting airways.

Keywords

Lung Development Surfactant Protein Alveolar Type Keratinocyte Growth Factor Clara Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Acarregui, M.J., J.M. Snyder, M.D. Mitchell, and C.R. Mendelson. Prostaglandins regulate surfactant protein A (SP-A) gene expression in human fetal lung in vitro. Endocrinology 90: 1105–1113, 1990.CrossRefGoogle Scholar
  2. 2.
    Adams, J.C. and F.M. Watt. Regulation of development and differentiation by the extra-cellular matrix. Development 117: 1183–1198, 1993.PubMedGoogle Scholar
  3. 3.
    Adamson, I.Y.R., G.M. King, and L. Young. Influence of extracellular matrix and collagen components on alveolar type 2 cell morphology and function. In Vitro Cell. Dev. Biol. 25: 494–502, 1989.PubMedCrossRefGoogle Scholar
  4. 4.
    Adamson, I.Y.R. and L. Young. Alveolar type II cell growth on a pulmonary endothelial extracellular matrix. Am. J. Physiol. 270 (Lung Cell. Mol. Physiol. 14): L1017 - L1022, 1996.PubMedGoogle Scholar
  5. 5.
    Adamson, I.Y.R., L. Young, and G.M. King. Reciprocal epithelial:fibroblast interactions in the control of fetal and adult rat lung cells in culture. Exp. Lung Res. 17: 821–835, 1991.PubMedCrossRefGoogle Scholar
  6. 6.
    Alcorn, J.L., E. Gao, Q. Chen, M.E. Smith, R.D. Gerard, and C.R. Mendelson. Genomic elements involved in transcriptional regulation of the rabbit surfactant protein-A gene. Mol. Endocrinol. 7: 1072–1085, 1993.PubMedCrossRefGoogle Scholar
  7. 7.
    Ang, S.L. and J. Rossant. HNF-3ß is essential for node and notochord formation in mouse development. Cell 78: 561–574, 1994.PubMedCrossRefGoogle Scholar
  8. 8.
    Ang, S.L., A. Wierda, D. Wong, K.A. Stevens, S. Cascio, J. Rossant, and K.S. Zaret. The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of the HNF3/forkhead proteins. Development 119: 1301–1315, 1993.PubMedGoogle Scholar
  9. 9.
    Aubin, J., M. Lemieux, M. Trembly, J. Berard, and L. Jeannotte. Early postnatal lethality in Hoxa-5 mutant mice is attributable to respiratory tract defects. Dev. Biol. 192: 432–445, 1997.PubMedCrossRefGoogle Scholar
  10. 10.
    Bachurski, C.J., G.S. Pryhuber, S. Glasser, S.E. Kelly, and J.A. Whitsett.Tumor necrosis factor-a inhibits surfactant protein C gene transcription. J. Biol. Chem. 270: 19402–19407, 1995.PubMedCrossRefGoogle Scholar
  11. 11.
    Batenburg, J.J. and R.H. Elfring. Pre-translational regulation by glucocorticoid of fatty acid and phosphatidylcholine synthesis in type II cells from fetal rat lung. FEBS Lett. 307: 164–168, 1992.PubMedCrossRefGoogle Scholar
  12. 12.
    Bedetti, C.D., J. Singh, G. Singh, S.L. Katyal, and M.L. Wong-Chong. Ultrastructural localization of rat Clara cell 10kD secretory protein by the immunogold technique using polyclonal and monoclonal antibodies. J. Histochem. Cytochem. 35: 789–794, 1987.PubMedCrossRefGoogle Scholar
  13. 13.
    Behringer, R.R., D.A. Crony, V.M. Tennyson, R.L. Brinster, R.D. Palmiter, and D.J. Wolgemuth. Sequences 5’ of the homeobox of the hox-1,4 gene direct tissue specific expression of lacZ during mouse development. Development 117: 823–833, 1993.PubMedGoogle Scholar
  14. 14.
    Bellusci, S., Y. Furuta, M.G. Rush, R. Henderson, G. Winnier, and B.L.M. Hogan. Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 124: 53–63, 1997.PubMedGoogle Scholar
  15. 15.
    Bellusci S., J. Grindley, H. Emoto, N. Itoh, and B.L.M. Hogan. Fibroblast growth factor 10 (FGF 10) and branching morphogenesis in the embryonic mouse lung. Development 124: 4867–4878, 1997.PubMedGoogle Scholar
  16. 16.
    Bellusci S., R. Henderson, G. Winnier, T. Oikawa, and B.L.M. Hogan. Evidence from normal expression and targeted overexpression that Bone Morphogenetic Protein-4 (BMP-4) plays a role in mouse embryonic lung morphogenesis. Development 122: 1693–1702, 1996.PubMedGoogle Scholar
  17. 17.
    Berard, J., L. Gaboury, M. Landers, Y. de Repentigny, B. Houle, R. Kothary, and W.E.C. Bradley. Hyperplasia and tumors in lung, breast and other tissues in mice carrying a RAR-ß4-like transgene. EMBO J. 13: 5570–5580, 1994.PubMedGoogle Scholar
  18. 18.
    Bernacki, S.H., C. Nervi, T.M. Volberg, and A.M. Jetten. Homeobox 1.3 expression: induction by retinoic acid in bronchial fibroblasts. Am. J. Respir.Cell Mol. Biol. 7: 3–9, 1992.PubMedCrossRefGoogle Scholar
  19. 19.
    Bingle, C.D. and J.D. Gitlin. Identification of hepatocyte nuclear factor-3 binding sites in the Clara cell secretory protein gene. Biochem. J. 295: 227–232, 1993.PubMedGoogle Scholar
  20. 20.
    Bingle, C.D. and S. Gowan. Molecular cloning of the forkhead transcription factor HNF3a from a human pulmonary adenocarcinoma cell line. Biochim. Biophys. Acta 1307: 17–20, 1996.PubMedCrossRefGoogle Scholar
  21. 21.
    Bingle, C.D., B.P. Hackett, M. Moxley, W. Longmore, and J.D. Gitlin. Role of HNF-3a and HNF-3ß in Clara cell secretory protein gene expression in the bronchiolar epithelium. Biochem. J. 308: 197–202, 1995.PubMedGoogle Scholar
  22. 22.
    Blau, H., D.E. Guzowski, Z.A. Siddiqi, E.M. Scarpelli, and R.S. Bienkowski. Fetal type 2 pneumocytes form alveolar like structures and maintain long term differentiation on extracellular matrix. J. Cell. Physiol. 136: 203–214, 1988.PubMedCrossRefGoogle Scholar
  23. 23.
    Boggaram, V. and C. Mendelson. Transcriptional regulation of the gene encoding the major surfactant protein (SP-A) in rabbit fetal lung. J. Biol. Chem. 263: 19060–19065, 1988.PubMedGoogle Scholar
  24. 24.
    Bogue, C.F., I. Gross, H. Vasavada, D.W. Dynia, C.M. Wilson, and H.C. Jacobs. Identification of Hox genes in newborn lung and effects of gestational age and retinoic acid on their expression. Am. J. Physiol. 266 (Lung Cell. Mol. Physiol. 10 ): L448 - L454, 1994.Google Scholar
  25. 25.
    Bogue, C.F., H.C. Jacobs, D.W. Dynia, C.M. Wilson, and I. Gross. Retinoic acid increases surfactant protein mRNA in fetal rat lung in culture. Am. J. Physiol. 271 (Lung Cell. Mol. Physiol. 15 ): L862 - L868, 1996.Google Scholar
  26. 26.
    Bogue, C.F., L.J. Lou, and H.C. Jacobs. Expression of Hoxb genes in the developing mouse foregut and lung. Am. J. Respir. Cell Mol. Biol. 15: 163–171, 1996.PubMedCrossRefGoogle Scholar
  27. 27.
    Bohinski, R.J., R. Di Lauro, and J.A. Whitsett. The lung-specific surfactant protein B gene promoter is a target for thyroid transcription factor 1 and hepatocyte nuclear factor 3, indicating common factors for organ-specific gene expression along the foregut axis. Mol. Cell. Biol. 14: 5671–5681, 1994.PubMedCrossRefGoogle Scholar
  28. 28.
    Bohinski, R.J., J.A. Huffman, J.A. Whitsett, and D.L. Lanier. Cis-active elements controlling lung cell-specific expression of human pulmonary surfactant protein B gene. J. Biol. Chem. 268: 11160–11166, 1993.PubMedGoogle Scholar
  29. 29.
    Boström, H., K. Willets, M. Pekny, P. Levéen, P. Lindhal, H. Hedstrand, M. Pekna, M. Hell-ström, S. Gebre-Medhin, M. Schalling, M. Nilsson, S. Kurland, J. Törnell, J.K. Heath, and C. Betscholtz. PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 85: 863–873, 1996.PubMedCrossRefGoogle Scholar
  30. 30.
    Bourbon, J.R. and C. Fraslon. Developmental aspects of the alveolar epithelium and the pulmonary surfactant system. In: Pulmonary Surfactant: Biochemical, Functional, Regulatory and Clinical Concepts, edited by J.R. Bourbon. Boca Raton, FL: CRC Press, 1991, p. 257–324.Google Scholar
  31. 31.
    Braun, H. and G. Suske. Combinatorial action of HNF3 and Sp family transcription factors in the activation of the rabbit uteroglobin/CC10 promoter. J. Biol. Chem. 273: 9821–9828, 1998.PubMedCrossRefGoogle Scholar
  32. 32.
    Breed, D.R., L.R. Margraf, J.L. Alcorn, and C. Mendelson. Transcription factor C/EBPS in fetal lung: developmental regulation and effects of cyclic adenosine 3’,5’-monophosphate and glucocorticoids. Endocrinology 138: 5527–5534, 1997.PubMedCrossRefGoogle Scholar
  33. 33.
    Brinkman, V., H. Foroutan, M. Sachs, K.M. Weidner, and W. Birchmeier. Hepatocyte growth factor/scatter factor induces a variety of tissue specific morphogenic programs in epithelial cells. J. Cell Biol. 131: 1573–1586, 1995.CrossRefGoogle Scholar
  34. 34.
    Bruno, M.D., R.J. Bohinski, J.E. Carter, K.A. Foss, and J.A. Whitsett. Structure and function of the mouse surfactant protein B gene. Am. J. Physiol. 268 (Lung Cell. Mol. Physiol. 12 ): L381 - L389, 1995.Google Scholar
  35. 35.
    Bruno, M.D., R.J. Bohinski, K.M. Huelsman, J.A. Whitsett, and T.R. Korfhagen. Lung cell-specific expression of the murine surfactant protein A(SP-A) gene is mediated by interactions between the SP-A promoter and thyroid transcription factor-1. J. Biol. Chem. 270: 6531–6536, 1995.PubMedCrossRefGoogle Scholar
  36. 36.
    Caniggia, I., J. Liu, R. Han, J. Wang, A.K. Tanswell, G. Laurie, and M. Post. Identification of receptors binding fibronectin and laminin on fetal rat lung cells. Am. J. Physiol. 270 (Lung Cell. Mol. Physiol. 14 ): L459 - L468, 1996.Google Scholar
  37. 37.
    Caniggia, I., K. Tanswell, and M. Post. Temporal and spatial differences in glycosaminoglycan synthesis by fetal lung fibroblasts. Exp. Cell Res. 202: 252–258, 1992.PubMedCrossRefGoogle Scholar
  38. 38.
    Caniggia, I., I. Tseu, R.N. Han, B.T. Smith, A. K. Tanswell, and M. Post. Spatial and temporal differences in fibroblast behavior in fetal rat lung. Am. J. Physiol. 261 (Lung Cell. Mol. Physiol. 5 ): L424 - L433, 1991.Google Scholar
  39. 39.
    Cardoso, W.V. Transcription factors and pattern formation in the developing lung. Am. J. Physiol. 269 (Lung Cell. Mol. Physiol. 13 ): L429 - L442, 1995.Google Scholar
  40. 40.
    Cardoso, W.V., A. Itoh, H. Nogawa, I. Mason, and J.S. Brody. FGF-1 and FGF-7 induce distinct patterns of growth and differentiation in embryonic lung epithelium. Dev. Dyn. 298: 398–405, 1997.CrossRefGoogle Scholar
  41. 41.
    Cardoso, W.V., S.A. Mitsialis, J.S. Brody, and M.C. Williams. Retinoic acid alters the expression of pattern-related genes in the developing lung. Dev. Dyn. 207: 47–59, 1996.PubMedCrossRefGoogle Scholar
  42. 42.
    Cardoso, W.V., M.C. Williams, S.A. Mitsialis, M. Joyce-Brady, A.K. Rishi, and J.S. Brody. Retinoic acid induces changes in the pattern of airway branching and alters epithelial cell differentiation in the developing lung in vitro. Am. J. Respir. Cell Mol. Biol. 12: 464–476, 1995.PubMedCrossRefGoogle Scholar
  43. 43.
    Chelly, N., O.-B. Mouhieddine-Gueddiche, A.-M. Barlier-Mur, B. Chailley-Heu, and J.R. Bourbon. Keratinocyte growth factor enhances maturation of fetal rat lung type II cells. Am. J. Respir. Cell Mol. Biol. 20: in press, 1999.Google Scholar
  44. 44.
    Chen, Q., V. Boggaram, and C.R. Mendelson. Rabbit lung surfactant protein A (SP-A) gene: identification of a lung-specific DNAse I hypersensitive site in the 5’-flanking region. Am. J. Physiol. 262 (Lung Cell. Mol. Physiol. 6 ): L662 - L671, 1992.Google Scholar
  45. 45.
    Chinoy, M.R., M.T. Antonio-Santiago, and E.M. Scarpelli. Maturation of undifferentiated lung epithelial cells into type II cells in vitro: a temporal process that parallels cell differentiation in vivo. Anat. Rec. 240: 545–554, 1994.PubMedCrossRefGoogle Scholar
  46. 46.
    Chisaka, O. and M.R. Capecchi. Regionally restricted developmental defects resulting from targeted disruption of the mouse homeobox gene hox-1,5. Nature 350: 473–479, 1991.PubMedCrossRefGoogle Scholar
  47. 47.
    Civitareale, D., R. Lonigro, A.J. Sinclair, and R. Di Lauro. A thyroid-specific nuclear protein essential for tissue expression of the thyroglobulin promoter. EMBO J. 8: 2537–2542, 1989.PubMedGoogle Scholar
  48. 48.
    Clark, K.L., E.D. Halay, E. Lai, and K.S. Burley. Co-crystal structure of the HNF-3/fork head DNA recognition motif resembles histone H5. Nature 364: 412–420, 1993.PubMedCrossRefGoogle Scholar
  49. 49.
    Clevidence, D.E., D.G. Overdier, R.S. Peterson, A. Porcella, H. Ye, K.E. Paulson, and R.H. Costa. Members of the HNF-3/forkhead family of transcription factors exhibit distinct cellular expression patterns in lung and regulate the surfactant protein B promoter. Dev. Biol. 166: 195–209, 1994.PubMedCrossRefGoogle Scholar
  50. 50.
    Clevidence, D.E., D.G. Overdier, W. Tao, X. Qian, L. Pani, E. Lai, and R.H. Costa. Identification of nine tissue-specific transcription factors of the hepatocyte nuclear factor 3/forkhead DNA-binding domain family. Proc. Natl. Acad. Sci. USA 90: 3948–3952, 1993.PubMedCrossRefGoogle Scholar
  51. 51.
    Cole, T.J., J.A. Blendy, A.P. Monaghan, K. Krieglstein, W. Schmid, A. Aguzzi, G. Fantuzzi, E. Hummler, K. Unsicker, and G. Schütz. Targeted disruption of the glucocorticoid receptor gene blocks chromaffin cell development and severely retards lung maturation. Genes Dev. 9: 1608–1621, 1995.PubMedCrossRefGoogle Scholar
  52. 52.
    Costa, R.H., D.R. Grayson, and J.E. Darnell, Jr. Multiple hepatocyte-enriched nuclear factors function in the regulation of transthyretin and al-antitrypsin. Mol. Cell. Biol. 9: 1415–1425, 1989.PubMedGoogle Scholar
  53. 53.
    Damante, G. and R. Di Lauro. Thyroid specific gene expression. Biochim. Biophys. Acta 1218: 255–266, 1994.PubMedCrossRefGoogle Scholar
  54. 54.
    Danto, S.I., J.M. Shannon, Z. Borok, S.M. Zabski, and D.E. Crandall. Reversible trans-differentiation of alveolar epithelial cells. Am. J. Respir. Cell Mol. Biol. 12: 497–502, 1995.PubMedCrossRefGoogle Scholar
  55. 55.
    Danto, S.I., S.M. Zabski, and E.D. Crandall. Reactivity of alveolar epithelial cells in primary culture with type I cell monoclonal antibodies. Am. J. Respir. Cell Mol. Biol. 6: 296–306, 1992.PubMedCrossRefGoogle Scholar
  56. 56.
    De Bortoli, C., B. Chailley-Heu, and J.R. Bourbon. Production of transforming growth factor (TGF) 13 by fetal lung cells. Biol. Cell 84: 215–218, 1995.PubMedCrossRefGoogle Scholar
  57. 57.
    Degryse, E., M.M. De Santi, M. Dietrich, D. Ali Hadj, J.-F. Spetz, D. Villeval, and G. Lungarella. A human SP-C promoter fragment targets al-proteinase inhibitor gene expression to lung alveolar type II cells in transgenic mice. Transgenie Res. 5: 139–143, 1996.CrossRefGoogle Scholar
  58. 58.
    Dekowski, S.A., M. Pajeau, and R.J. Panos. Keratinocyte growth factor and keratinocyte growth factor mRNA content in late gestation fetal and neonatal rat lung. Pediatr. Res. 39: 56A, 1996.Google Scholar
  59. 59.
    De Simone, V. and R. Cortese. Transcription factors and liver-specific genes. Biochim. Byophys. Acta 1132: 119–126, 1992.CrossRefGoogle Scholar
  60. 60.
    Deterding, R.R. and J.M. Shannon. Proliferation and differentiation of fetal rat pulmonary epithelium in the absence of mesenchyme. J. Clin. Invest. 95: 2963–2972, 1995.PubMedCrossRefGoogle Scholar
  61. 61.
    Dobbs, L.G., M.C. Williams, and A.E. Brandt. Changes in biochemical characteristics and pattern of lectin binding of alveolar type II cells with time in culture. Biochim. Biophys. Acta 846: 155–166, 1985.PubMedCrossRefGoogle Scholar
  62. 62.
    Dobbs, L.G., M.C. Williams, and R. Gonzalez. Monoclonal antibodies to apical surfaces of rat alveolar type I cells bind to surfaces of cultured, but not freshly isolated, type II cells. Biochim. Biophys. Acta 970: 146–156, 1988.PubMedCrossRefGoogle Scholar
  63. 63.
    Dollé, P., E. Ruberte, P. Leroy, G. Morriss-Kay, and P. Chambon. Retinoic acid receptors and cellular retinoid binding proteins. I. A systematic study of their differential pattern of transcription during mouse organogenesis. Development 110: 1133–1151, 1990.PubMedGoogle Scholar
  64. 64.
    Evans, M.J. and S.G. Shami. Lung cell kinetics. In: Lung Cell Biology, Vol. 41, edited by D. Massaro. New York: Marcel Dekker, 1989, p. 1–36.Google Scholar
  65. 65.
    Farrell, P.M., J.R. Bourbon, R.H. Notter, L. Marin, L. Nogee, and J.A. Whitsett. Relationships among surfactant fraction lipids, proteins and biophysical properties in the developing lung. Biochim. Biophys. Acta 1044: 84–90, 1990.PubMedCrossRefGoogle Scholar
  66. 66.
    Fisher, J.H., F. McCormack, S.S. Park, T. Stelzner, J.M. Shannon, and T. Hofmann. In vivo regulation of surfactant by glucocorticoids. Am. J. Respir. Cell Mol. Biol. 5: 63–70, 1991.Google Scholar
  67. 67.
    Flodby, P., C. Barlow, H. Kylefjord, L. Ährlund-Richert, and K.G. Xanthopoulos. Increased hepatic cell proliferation and lung abnormalities in mice deficient in CCAAT/enhancer binding protein a. J. Biol. Chem. 271: 24753–24780, 1996.PubMedCrossRefGoogle Scholar
  68. 68.
    Fraslon, C. and J.J. Batenburg. Pre-translational regulation of lipid synthesizing enzymes and surfactant proteins in fetal rat lung in explant culture. FEBS Lett. 325: 285–290, 1993.PubMedCrossRefGoogle Scholar
  69. 69.
    Fraslon, C. and J.R. Bourbon. Comparison of effects of epidermal and insulin-like growth factors, gastrin-releasing peptide and retinoic acid on fetal lung cell growth and maturation in vitro. Biochim. Biophys. Acta 1123: 65–75, 1992.PubMedCrossRefGoogle Scholar
  70. 70.
    Fraslon, C. and J.R. Bourbon. Retinoids control surfactant phospholipid biosynthesis in fetal rat lung. Am. J. Physiol. 266 (Lung Cell. Mol. Physiol. 10 ): L705 - L712, 1993.Google Scholar
  71. 71.
    Fraslon, C., B. Chailley-Heu, J.J. Batenburg, R. Elfring, and J.R. Bourbon. Ontogeny of surfactant proteins and lipid-synthesizng enzymes in cultured fetal lung epithelial cells. Am. J. Physiol. 267 (Lung Cell. Mol. Physiol. 11 ): L375 - L383, 1994.Google Scholar
  72. 72.
    Fraslon, C., T. Lacaze-Masmonteil, V. Zupan, B. Chailley-Heu, and J.R. Bourbon. Fetal rat lung type II cell differentiation in serum-free isolated cell culture: modulation and inhibition. Am. J. Physiol. 264 (Lung Cell. Mol. Physiol. 8 ): L504 - L516, 1993.Google Scholar
  73. 73.
    Gao, E., J.L. Alcorn, and C.R. Mendelson. Identification of enhancers in the 5’-flanking region of the rabbit surfactant protein A (SP-A) gene and characterization of their binding proteins. J. Biol. Chem. 268: 19697–19709, 1993.PubMedGoogle Scholar
  74. 74.
    Gatherer, D., P.T. Dijke, D.T. Baird, and R.J. Arkhurst. Expression of TGF- I isoforms during first trimester human embryogenesis. Development 110: 445–460, 1990.PubMedGoogle Scholar
  75. 75.
    Gehring, W.J., M. Affolter, and T. Bürglin. Homeodomain proteins. Annu. Rev. Biochem. 63: 487–526, 1994.PubMedCrossRefGoogle Scholar
  76. 76.
    Glasser, S.W., T.R. Korfhagen, S.E. Wert, M.D. Bruno, K.M. McWilliams, D.K. Vorbroker, and J.A. Whitsett. Genetic element from human surfactant protein SP-C gene confers bronchiolar-alveolar cell specificity in transgenic mice. Am. J. Physiol. 261 (Lung Cell. Mol. Physiol. 5 ): L349 - L356, 1991.Google Scholar
  77. 77.
    Guazzi, S., R. Lonigro, L. Pinotello, E. Bonicelli, R. DiLauro, and F. Mavilio. The thyroid transcription factor-1 is a candidate target for regulation by Hox proteins. EMBO J. 13: 3339–3347, 1994.PubMedGoogle Scholar
  78. 78.
    Guazzi, S., M. Price, M. De Felice, G. Damante, M.-G. Mattei, and R. DiLauro. Thyroid nuclear factor 1 (TTF-1) contains a homeodomain and displays a novel DNA binding specificity. EMBO J. 9: 3631–3639, 1990.PubMedGoogle Scholar
  79. 79.
    Guo, L., L. Degenstein, and E. Fuchs. Keratinocyte growth factor is required for hair development but not for wound healing. Genes Dev. 10: 165–175, 1996.PubMedCrossRefGoogle Scholar
  80. 80.
    Gupta, R.P., S.E. Patton, A.M. Jetten, and G.E.R. Hook. Purification, characterization and proteinase activity of a Clara-cell secretory protein from the pulmonary extracellular lining of rabbits. Biochem. J. 248: 337–344, 1987.PubMedGoogle Scholar
  81. 81.
    Hackett, B.P., S.L. Brody, M. Liang, I.D. Zeitz, L.A. Bruns, and J.D. Gitlin. Primary structure of hepatocyte nuclear factor/forkhead factor homologue 4 and characterization of gene expression in the respiratory and reproductive epithelium. Proc. Natl. Acad. Sci. USA 92: 4249–4253, 1995.PubMedCrossRefGoogle Scholar
  82. 82.
    Hackett, B.P., N. Shimizu, and J.D. Gitlin. Clara cell secretory protein gene expression in bronchiolar epithelium. Am. J. Physiol. 262 (Lung Cell. Mol. Physiol. 6 ): L399 - L404, 1992.Google Scholar
  83. 83.
    Hirning, U., P. Schmid, W.A. Schultz, G. Rettenberger, and H. Hameister. A comparative analysis of N-myc and c-myc expression and cellular proliferation in mouse organogenesis. Mech. Dev. 33: 119–126, 1991.PubMedCrossRefGoogle Scholar
  84. 84.
    Ikeda, K., J.C. Clark, J.R. Shaw-White, M.T. Stahlman, C. Bouteil, and J.A. Whitsett. Gene structure and expression of human TTF-1 in respiratory epithelial cells. J. Biol. Chem. 270: 8108–8114, 1995.PubMedCrossRefGoogle Scholar
  85. 85.
    Ikeda, K., J.R. Shaw-White, S. Wert, and J.A. Whitsett. Hepatocyte nuclear factor 3 activates transcription of thyroid transcription factor 1 in respiratory epithelial cells. Mol. Cell. Biol. 16: 3626–3636, 1996.PubMedGoogle Scholar
  86. 86.
    Jaskol’, T., H.A. Choy, and M. Melnick. The glucocorticoid-glucocorticoid receptor signal transduction pathway, transforming growth factor-ß, and embryonic mouse lung development in vivo. Pediatr. Res. 39: 749–759, 1996.CrossRefGoogle Scholar
  87. 87.
    Johansson, J., T. Curstedt, and B. Robertson. The proteins of the surfactant system. Eur. Respir. J. 7: 372–391, 1994.PubMedCrossRefGoogle Scholar
  88. 88.
    Jones, C.A., R.G. Cayabyab, K.Y.C. Kwong, C. Stotts, B. Wong, H. Hamsdan, P. Minoo, and R. de Lemos. Undetectable interleukin (IL)-10 and persistent IL-8 expression early in hyaline membrane disease: a possible developmental basis for the predisposition to chronic lung inflammation in preterm newborns. Pediatr. Res. 39: 966–975, 1996.PubMedCrossRefGoogle Scholar
  89. 89.
    Juliano, R.L. and S. Haskill. Signal transduction from the extracellular matrix. J. Cell Biol. 120: 577–585, 1993.PubMedCrossRefGoogle Scholar
  90. 90.
    Kaartinen, V., J.W. Voncken, C. Shuler, D. Warburton, D. Bu, N. Heisterkamp, and J. Groffen. Abnormal lung development and cleft palate in mice lacking TGF-ß3 indicates defects of epithelial mesenchymal interaction. Nat. Genet. 11: 415–421, 1995.PubMedCrossRefGoogle Scholar
  91. 91.
    Kalina, M., R.J. Mason, and J.M. Shannon. Surfactant protein C is expressed in alveolar type II cells but not in Clara cells of rat lung. Am. J. Respir. Cell Mol. Biol. 6: 594–600, 1992.PubMedCrossRefGoogle Scholar
  92. 92.
    Kappen, C. Hox genes in the lung. Am. J. Respir. Cell Mol. Biol. 15: 156–162, 1996.PubMedCrossRefGoogle Scholar
  93. 93.
    Kasper, M., D. Schuh, and M. Muller. Bauhinia purpurea lectin (BPA) binding of rat type I pneumocytes: alveolar epithelial alterations after radiation-induced lung injury. Exp. Toxicol. Pathol. 46: 361–367, 1994.PubMedCrossRefGoogle Scholar
  94. 94.
    Kawada, H., J.M. Shannon, and R.J. Mason. Improved maintenance of adult rat type II cell differentiation in vitro: effect of serum-free hormonally defined medium and a reconstituted basement membrane. Am. J. Respir. Cell Mol. Biol. 3: 33–43, 1990.PubMedCrossRefGoogle Scholar
  95. 95.
    Kelly, S.E., C.J. Bachurski, M.S. Burhans, and S.W. Glasser. Transcription of the lung-specific surfactant protein C gene is mediated by thyroid transcription factor 1. J. Biol. Chem. 271: 6881–6888, 1996.PubMedCrossRefGoogle Scholar
  96. 96.
    Khoor, A., M.E. Gray, W.M. Hull, J.A. Whitsett, and M.T. Stahlman.Developmental expression of SP-A and SP-A mRNA in the proximal and distal respiratory epithelium in the human fetus and newborn. J. Histochem. Cytochem. 41: 1311–1319, 1993.PubMedCrossRefGoogle Scholar
  97. 97.
    Kimura, S., Y. Hara, T. Pineau, P. Fernandez-Salguero, C.H. Fox, J.M. Ward, and F.J. Gonzalez. 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, 1996.PubMedCrossRefGoogle Scholar
  98. 98.
    Kleinman, H.K., M.L. McGarvey, J.R. Hassell, V.L. Star, F.B. Cannon, G.W. Laurie, and G.R. Martin. Basement membrane complexes with biological activity. Biochem. USA 28: 312–318, 1986.CrossRefGoogle Scholar
  99. 99.
    Kouretas, D., A.M. Karinch, A. Rishi, K. Melchers, and J. Floros. Conservation analysis of rat and human SP-A gene identifies 5’ flanking sequences of rat SP-A that bind rat lung nuclear proteins. Exp. Lung Res. 19: 485–503, 1993.PubMedCrossRefGoogle Scholar
  100. 100.
    Kubiak, J., M.M. Mitra, R. Steve, J.D. Hunt, R Davies, and B.R. Pitt.Transforming growth factor-a gene expression in late-gestation fetal rat lung. Pediatr. Res. 31: 286–290, 1992.PubMedCrossRefGoogle Scholar
  101. 101.
    Kumar, N.M., S.L. Sigurdson, D. Sheppard, and J.S. Lwebuga-Mukasa. Differential modulation of integrin receptor and extracellular matrix laminin by transforming growth factor-ß1 in rat alveolar epithelial cells. Exp. Cell Res. 221: 385–394, 1995.PubMedCrossRefGoogle Scholar
  102. 102.
    Lacaze-Masmonteil, T., C. Fraslon, J. Bourbon, M. Raymondjean, and A. Khan. Characterization of the rat pulmonary surfactant protein A promoter. Eur. J. Biochem. 206: 613–623, 1992.PubMedCrossRefGoogle Scholar
  103. 103.
    Lai, E., V.R. Prezioso, W. Tao, W. Chen, and J.E. Darnell, Jr. Hepatocyte nuclear factor 3A belongs to a gene family in mammals that is homologous to the Drosophila homeotic gene fork head. Genes Dev. 5: 416–427, 1991.PubMedCrossRefGoogle Scholar
  104. 104.
    Langston, C., K. Kida, M. Reed, and W.M. Thurlbeck. Human lung growth in late gestation and in the neonate. Am. Rev. Respir. Dis. 129: 607–613, 1984.PubMedGoogle Scholar
  105. 105.
    Lazzaro, D., M. Price, M. De Felice, and R. Di Lauro. The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development 113: 1093–1104, 1991.PubMedGoogle Scholar
  106. 106.
    Li, F., E. Rosenberg, C.I. Smith, K. Notarfrancesco, S.R. Reisher, H. Shuman, and S.I. Feinstein. Correlation of expression of transcription factor C/EBPa and surfactant protein genes in lung cells. Am. J. Physiol. 269 (Lung Cell. Mol. Physiol. 13 ): L241 - L247, 1995.Google Scholar
  107. 107.
    Liu, R., C.S. Harvey, and S.E. McGowan. Retinoic acid increases elastin in neonatal rat lung fibroblast cultures. Am. J. Physiol. 265 (Lung Cell. Mol. Physiol. 9 ): L430 - L437, 1993.Google Scholar
  108. 108.
    Luzi, P., M. Anceschi, and D.S. Strayer. Glucocorticoid responsiveness conferred by a cloned DNA binding protein. Receptor 5: 93–103, 1995.PubMedGoogle Scholar
  109. 109.
    Luzi, P. and D.S. Strayer. Binding proteins that amplify surfactant protein B gene expression: isolation and characterization. Biochem. Biophys. Res.Commun. 208: 153–160, 1995.PubMedCrossRefGoogle Scholar
  110. 110.
    Manley, N.R. and M.R. Capecchi. The role of Hoxa-3 in the thymus and thyroid development. Development 121: 1989–2003, 1995.PubMedGoogle Scholar
  111. 111.
    Mantile, G., L. Miele, E. Cordella-Miele, G. Singh, S.L. Katyal, and A.B. Mukherjee. Human Clara cell 10-kDa protein is the counterpart of rabbit uteroglobin. J. Biol. Chem. 25: 20343–20351, 1993.Google Scholar
  112. 112.
    Margraf, L.R., J.R. Tomashefski, Jr, M.C. Bruce, and B.B. Dahms. Morphometric analysis of the lung in bronchopulmonary dysplasia. Am. Rev. Respir. Dis. 143: 391–400, 1991.PubMedCrossRefGoogle Scholar
  113. 113.
    Marin, L. The type II pneumocyte. In: Pulmonary Surfactant: Biochemical, Functional, Regulatory and Clinical Concepts, edited by J.R. Bourbon, Boca Raton, FL: CRC Press, 1991, p. 15–36.Google Scholar
  114. 114.
    Massaro, G.D. and D. Massaro. Formation of pulmonary alveoli and gas-exchange surface area: quantitation and regulation. Annu. Rev. Physiol. 58: 73–92, 1996.PubMedCrossRefGoogle Scholar
  115. 115.
    Massaro, G.D. and D. Massaro. Postnatal treatment with retinoic acid increases the number of pulmonary alveoli in rats. Am. J. Physiol. 270 (Lung Cell. Mol. Physiol. 14 ): L305 - L310, 1996.Google Scholar
  116. 116.
    Matter, M.L. and G.W. Laurie. A novel laminin E8 cell adhesion site required for lung alveolar formation in vitro. J. Cell Biol. 124: 1083–1090, 1994.PubMedCrossRefGoogle Scholar
  117. 117.
    Melnick, M., H.A. Choy, and T. Jaskoll. Glucocorticoids, tumor necrosis factor-a, and epidermal growth factor regulation of pulmonary morphogenesis: a multivariate in vitro analysis of their related actions. Dev. Dyn. 205: 365–378, 1996.PubMedCrossRefGoogle Scholar
  118. 118.
    Mendelsohn, C., D. Lohnes, D. Decimo, T. Lufkin, M. LeMeur, P. Chambon, and M. Mark. Function of retinoic acid receptors (RARs) during development. II. Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 120: 2749–2771, 1994.PubMedGoogle Scholar
  119. 119.
    Metzler, M.D. and J.M. Snyder. Retinoic acid differentially regulates expression of surfactant-associated proteins in human lung. Endocrinology 133: 1990–1998, 1993.PubMedCrossRefGoogle Scholar
  120. 120.
    Michael, L.F., J.L. Alcorn, E. Gao, and C.R. Mendelson. Characterization of the cyclic adenosine 3’-5’-monophosphate response element of the rabbit surfactant protein-A gene: evidence for transactivators distinct from CREB/ATF family members. Mol. Endocrinol. 10: 159–170, 1996.PubMedCrossRefGoogle Scholar
  121. 121.
    Michael, L.F., M.A. Lazar, and C.R. Mendelson. Peroxisome proliferator-activated receptor yl expression is induced during cyclic adenosine monophosphate-stimulated differentiation of alveolar type II pneumonocytes. Endocrinology 138: 3695–3703, 1997.PubMedCrossRefGoogle Scholar
  122. 122.
    Miettinen, P.J., J.E. Berger, J. Meneses, Y. Phung, R.A. Pedersen, Z. Werb, and R. Derynck. Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature 376: 337–341, 1995.PubMedCrossRefGoogle Scholar
  123. 123.
    Millan, F.A., F. Denhez, P. Kondaiah, and R.J. Arkhurst. Embryonic gene expression patterns of TGF-ß1, 132 and 133 suggest different developmental functions in vivo. Development 111: 131–144, 1991.PubMedGoogle Scholar
  124. 124.
    Minoo, P., H. Hamdam, D. Bu, D. Warburton, P. Stepanik, and R. de Lemos. TTF-1 regulates lung epithelial morphogenesis. Dev. Biol. 172: 694–698, 1995.PubMedCrossRefGoogle Scholar
  125. 125.
    Miura, N., H. Kakinuma, M. Sato, N. Aiba, K. Terada, and N. Sugiyama. Mouse forkhead (winged helix) gene LUN encodes a transactivator that acts in the lung. Genomics 50: 346–356, 1998.PubMedCrossRefGoogle Scholar
  126. 126.
    Moens, C.B., A.B. Auerbach, R.A. Conlon, A.L. Joyner, and J. Rossant. A targeted mutation reveals a role for N-myc in the embryonic mouse lung. Genes Dev. 6: 691–704, 1992.PubMedCrossRefGoogle Scholar
  127. 127.
    Monaghan, A.P., K.H. Kaestner, E. Grau, and G. Schütz. Postimplantation expression patterns indicate a role for the mouse fork head/HNF-3 a, ß and y genes in determination of the definitive endoderm, chordamesoderm and neurectoderm. Development 119: 567–578, 1993.PubMedGoogle Scholar
  128. 128.
    Muglia, L., L. Jacobson, P. Dikkes, and J.A. Majzoub. Corticotropin-releasing hormone deficiency reveals major fetal but not adult glucocorticoid need. Nature 373: 427–432, 1995.PubMedCrossRefGoogle Scholar
  129. 129.
    Murgrauer, G., F.W. Alt, and P. Ekblom. N-myc proto-oncogene expression during organogenesis in the developing mouse as revealed by in situ hybridization. J. Cell Biol. 107: 1325–1335, 1988.CrossRefGoogle Scholar
  130. 130.
    Nogawa, H. and T. Ito. Branching morphogenesis of embryonic mouse lung epithelium in mesenchyme-free culture. Development 121: 1015–1022, 1995.PubMedGoogle Scholar
  131. 131.
    Odom, M.J., J. Snyder, and C. Mendelson. Adenosine 3’, 5’-monophosphate analogs and ß-adrenergic agonists induce the synthesis of the major surfactant apoprotein in human fetal lung in vitro. Endocrinology 1212: 1155–1163, 1987.CrossRefGoogle Scholar
  132. 132.
    Orr-Urtreger, A., M.T. Bedford, T. Burakova, E. Arman, Y. Zimmer, A. Yayon, D. Givol, and P. Lonai. Developmental localization of the splicing alternatives of fibroblast growth factor receptor-2 (FGFR2). Dev. Biol. 158: 475–486, 1993.PubMedCrossRefGoogle Scholar
  133. 133.
    Panos, R.J., J.S. Rubin, S.A. Aaronson, and R.J. Mason. Keratinocyte growth factor and hepatocyte growth factor/scatter factor are heparin-binding growth factors for alveolar type II cells in fibroblast-conditioned medium. J. Clin. Invest. 92: 969–977, 1993.PubMedCrossRefGoogle Scholar
  134. 134.
    Peters, K., S. Werner, X. Liao, S. Wert, J. Whitsett, and L. Williams. Targeted expression of a dominant negative FGF receptor blocks branching morphogenesis and epithelial differentiation of the mouse lung. EMBO J. 13: 3296–3301, 1994.PubMedGoogle Scholar
  135. 135.
    Peterson, R.L., L. Lim, H.G. Ye, H.P. Zhou, D.G. Overdier, and R.H. Costa. The winged helix transcriptional factor HFH-8 is expressed in the mesoderm of the primitive streak stage of mouse embryos and its cellular derivatives. Mech. Dev. 69: 53–69, 1997.PubMedCrossRefGoogle Scholar
  136. 136.
    Pierrou, S., M. Hellqvist, L. Samuelsson, S. Enerbäck, and P. Carlsson. Cloning and characterization of seven human forkhead proteins: binding site specificity and DNA binding. EMBO J. 13: 5002–5012, 1994.PubMedGoogle Scholar
  137. 137.
    Rannels, S.R., C. Stinson Fisher, L.J. Heuser, and D.E. Rannels. Culture of type II pneumocytes on a type II-cell derived fibronectin-rich matrix. Am. J. Physiol. 253 (Cell Physiol. 22 ): C759 - C765, 1987.Google Scholar
  138. 138.
    Rannels, S.R., J.A. Yarnell, C. Stinson Fisher, J.P. Fabisiak, and D.E. Rannels. Role of laminin in maintenance of type II pneumocyte morphology and function. Am. J. Physiol. 253 (Cell Physiol. 22 ): C835 - C845, 1987.Google Scholar
  139. 139.
    Ray, M.K., C.-Y. Chen, R.J. Schwartz, and F.J. De Mayo. Transcriptional regulation of a mouse Clara cell-specific protein (mCC10) gene by the NKx transcription factor family members thyroid transcription factor 1 and cardiac muscle-specific homeobox protein (CSX). Mol. Cell. Biol. 16: 2056–2064, 1996.PubMedGoogle Scholar
  140. 140.
    Rindfleisch, M.S., J.D. Hasday, V. Taciak, K. Broderick, and R.M. Viscardi. Potential role of interleukin-1 in the development of bronchopulmonary dysplasia. J. Interferon Cytokine Res. 16: 365–373, 1996.PubMedCrossRefGoogle Scholar
  141. 141.
    Ruocco, S., A. Lallemand, J.M. Tournier, and D. Gaillard. Expression and localization of epidermal growth factor, transforming growth factor-a, and localization of their common receptor in fetal human lung development. Pediatr. Res. 39: 448–455, 1996.PubMedCrossRefGoogle Scholar
  142. 142.
    Rust, K., L. Bingle, W. Mariencheck, A. Persson, and E.C. Crouch. Characterization of the human surfactant protein D promoter: transcriptional regulation of SP-D gene expression by glucocorticoids. Am. J. Respir. Cell Mol. Biol. 14: 121–130, 1996.PubMedCrossRefGoogle Scholar
  143. 143.
    Ryan, R.M., M.M. Mineo-Kuhn, C.M. Kramer, and J.N. Finkelstein. Growth factors alter neonatal type II alveolar epithelial cell proliferation. Am. J. Physiol. 266 (Lung Cell. Mol. Physiol. 10 ): L17 - L22, 1994.Google Scholar
  144. 144.
    Sanford, L.P., I. Ormsby, A.C. Gittenberg-de Groot, H. Sariola, R. Friedman, G.P. Boivin, E.L. Cardell, and T. Doetschman. TGF(32 knockout mice have multiple developmental defects that are non-overlapping with other TGFII knockout phenotypes. Development 124: 2659–2670, 1997.PubMedGoogle Scholar
  145. 145.
    Sawai, S., A. Shimono, Y. Wakamatsu, C. Palmes, K. Hanaoka, and H. Kondoh. Defects of embryonic organogenesis resulting from targeted disruption of the N-myc gene in the mouse. Development 117: 1445–1455, 1993.PubMedGoogle Scholar
  146. 146.
    Sawaya, P.L. and D.S. Luse. Two members of the HNF-3 family have opposite effects on a lung transcriptional element; HNF-3a stimulates and HNF-3ß inhibits activity of region I from Clara cell secretory protein (CCSP) promoter. J. Biol. Chem. 268: 22211–22216, 1994.Google Scholar
  147. 147.
    Sawaya, P.L., B.R. Stripp, J.A. Whitsett, and D.S. Luse. The lung-specific CC10 gene is regulated by transcription factors from the AP-1, octamer, and hepatocyte nuclear factor 3 families. Mol. Cell. Biol. 13: 3860–3871, 1993.PubMedGoogle Scholar
  148. 148.
    Schellase, D.E., P.A. Emrie, J.H. Fisher, and J.M. Shannon. Ontogeny of surfactant apoproteins in the rat. Pediatr. Res. 26: 167–174, 1989.CrossRefGoogle Scholar
  149. 149.
    Schmid, P., D. Cox, G. Bilbe, R. Maier, and G.K. McMaster. Differential expression of TGF ß1, ß2 and ß3 genes during mouse embryogenesis. Development 111: 117–130, 1991.PubMedGoogle Scholar
  150. 150.
    Serra, R., R.W. Pelton, and H.L. Moses. TGFß1 inhibits branching morphogenesis and N-myc expression in lung bud organ cultures Development 120: 2153–2161, 1994.PubMedGoogle Scholar
  151. 151.
    Shahar, I., E. Fireman, M. Topilsky, J. Grief, S. Kivity, Z. Spirer, and S. Ben Efraim. Effect of IL-6 on alveolar fibroblast proliferation in interstitial lung diseases. Clin. Immunol. Immunopathol. 79: 244–251, 1996.PubMedCrossRefGoogle Scholar
  152. 152.
    Shannon, J.M. Induction of alveolar type II cell differentiation in fetal tracheal epithelium by grafted distal lung mesenchyme. Dev. Biol. 166: 600–614, 1994.PubMedCrossRefGoogle Scholar
  153. 153.
    Shannon, J.M., P.A. Emrie, J.H. Fisher, Y. Kuroki, S.D. Jennings, and R.J. Mason. Effect of a reconstituted basement membrane on expression of surfactant apoproteins in cultured adult rat alveolar type II cells. Am. J. Respir. Cell Mol. Biol. 2: 183–192, 1990.PubMedCrossRefGoogle Scholar
  154. 154.
    Shannon, J.M., S.D. Jennings, and L.D. Nielsen. Modulation of alveolar type II cell differentiated function in vitro. Am. J. Physiol. 262 (Lung Cell. Mol Physiol. 6 ): L427 - L436, 1992.Google Scholar
  155. 155.
    Shannon, J.M., R.J. Mason, and S.D. Jennings. Functional differentiation of alveolar type II epithelial cell in vitro: effects of cell shape, cell-matrix interaction and cell-cell interactions. Biochim. Biophys. Acta 931: 143–156, 1987.PubMedCrossRefGoogle Scholar
  156. 156.
    Shannon, J.M., L.D. Nielsen, S.A. Gebb, and S.H. Randell. Mesenchyme specifies epithelial differentiation in reciprocal recombinants of embryonic lung and trachea. Dev. Dyn. 212: 482–494, 1998.PubMedCrossRefGoogle Scholar
  157. 157.
    Shiratori, M., E. Oshika, L.P. Ung, G. Singh, H. Shinozuka, D. Warburton, G. Michalopoulos, and S.L. Katyal. Keratinocyte growth factor and embryonic rat lung morpho-genesis. Am. J. Respir. Cell Mol. Biol. 15: 328–338, 1996.PubMedCrossRefGoogle Scholar
  158. 158.
    Simonet, W.S., M.L. DeRose, N. Bucay, H.Q. Nguyen, S.E. Wert, L. Zhou, T.R. Ulich, A. Thomason, D.M. Danilenko, and J.A. Whitsett. Pulmonary malformation in trans-genic mice expressing human keratinocyte growth factor in the lung. Proc. Natl. Acad. Sci. USA 92: 12461–12465, 1995.PubMedCrossRefGoogle Scholar
  159. 159.
    Singh, G., J. Singh, S.L. Katyal, W.E. Brown, J.A. Kramps, I.L. Paradis, J.H. Dauber, T.A. MacPherson, and N. Squeglia. Identification, cellular localization, isolation, and characterization of human Cara cell-specific 10 KD protein. J. Histochem. Cytochem. 36: 73–80, 1988.PubMedCrossRefGoogle Scholar
  160. 160.
    Smith, C.I., E. Rosenberg, S.R. Reisher, F. Li, P. Kefalides, A.B. Fisher, and S.I. Feinstein. Sequence of rat surfactant protein A gene and functional mapping of its upstream region. Am. J. Physiol. 269 (Lung Cell. Mol. Physiol. 13 ): L603 - L612, 1995.Google Scholar
  161. 161.
    Sonnenberg, E., D. Meyer, K.M. Weidner, and C. Birchmeier. Scatter factor/hepatocyte growth factor and its receptor, the c-met tyrosine kinase, can mediate a signal exchange between mesenchyme and epithelia during mouse development. J. Cell Biol. 123: 223–235, 1993.PubMedCrossRefGoogle Scholar
  162. 162.
    Stahlman, M.T., M.E. Gray, and J.A. Whitsett. Expression of thyroid transcription factor-1 (TTF-1) in fetal and neonatal human lung. J. Histochem. Cytochem. 44: 673–678, 1996.PubMedCrossRefGoogle Scholar
  163. 163.
    Stahlman, M.T., M.E. Gray, and J.A. Whitsett. Temporal-spatial distribution of hepatocyte nuclear factor-3ß in developing human lung and other foregut derivatives. Histochem. Cytochem. 46: 955–962, 1998.CrossRefGoogle Scholar
  164. 164.
    Stanton, B.R., A.S. Perkins, L. Tessarollo, D.A. Sassoon, and L.F. Parada. Loss of N-myc function results in embryonic lethality and failure of the epithelial component of the embryo to develop. Genes Dev. 6: 2235–2247, 1992.PubMedCrossRefGoogle Scholar
  165. 165.
    Strayer, D.S., S. Yang, and H.H. Jerng. Surfactant protein A—binding proteins. Characterization and structures. J. Biol. Chem. 268: 18679–18684, 1993.PubMedGoogle Scholar
  166. 166.
    Stripp, B.R., P.L. Sawaya, D.S. Luse, K.A. Wikenheiser, S.E. Wert, J.A. Huffman, D.L. Lattier, G. Singh, S.L. Katyal, and J.A. Whitsett. Cis-acting elements that confer lung epithelial cell expression of the CC10 gene. J. Biol. Chem. 267: 14703–14712, 1992.PubMedGoogle Scholar
  167. 167.
    Strum, J.M., R.S. Compton, S.L. Katyal, and G. Singh. The regulated expression of mRNA for Clara cell protein in the developing airways of the rat, as revealed by in situ hybridization. Tissue Cell 24: 461–474, 1992.PubMedCrossRefGoogle Scholar
  168. 168.
    Stuempfle, K.J., M. Koptides, P.G. Quinn, and J. Floros. In vitro analysis of rat surfactant protein A gene expression. Am. J. Physiol. 270 (Lung Cell. Mol. Physiol. 14): L504 - L516, 1996.Google Scholar
  169. 169.
    Sugahara, K., J.S. Rubin, R.J. Mason, E.L. Aronsen, and J.M. Shannon. Keratinocyte growth factor increases mRNAs for SP-A and SP-B in adult rat alveolar type II cells in culture. Am. J. Physiol. 269 (Lung Cell. Mol. Physiol. 13 ): L344 - L350, 1995.Google Scholar
  170. 170.
    Ten Have-Opbroek, A.A.W. The development of the lungs in mammals: an analysis of concepts and findings. Am. J. Anat. 162: 201–219, 1981.PubMedCrossRefGoogle Scholar
  171. 171.
    Toonen, R.F.G., S. Gowan, and C.D. Bingle. The lung enriched transcription factor TTF-1 and the ubiquitously expressed proteins Sp-1 and Sp-3 interact with elements located in the minimal promoter of the rat Clara cell secretory protein gene. Biochem. J. 316: 467–473, 1996.PubMedGoogle Scholar
  172. 172.
    Torday, J.S. and S. Kourembanas. Fetal rat lung fibroblasts produce a TGF ß homolog that blocks alveolar type II cell maturation. Dev. Biol. 139: 35–41, 1990.PubMedCrossRefGoogle Scholar
  173. 173.
    Ulich, T.R., E.S. Yi, K. Longmuir, S. Yin, R. Blitz, C. F. Morris, R. Housley, and G.F. Pierce. Keratinocyte growth factor is a growth factor for type II pneumocytes in vivo. J. Clin. Invest. 93: 1298–1306, 1994.PubMedCrossRefGoogle Scholar
  174. 174.
    Venkatesh, V.C., B.C. Planer, M. Schwartz, J.N. Vanderbilt, R.T. White, and P.L. Ballard. Characterization of the promoter of human pulmonary surfactant protein B gene. Am. J. Physiol. 268 (Lung Cell. Mol. Physiol. 12 ): L674 - L682, 1995.Google Scholar
  175. 175.
    Wang, J., M. Kuliszewski, W. Yee, L. Sedlackova, J. Xu, I. Tseu, and M. Post. Cloning and characterization of glucocorticoid-induced genes in fetal rat lung fibroblasts: transforming growth factor 13. J. Biol. Chem. 270: 2722–2728, 1995.PubMedCrossRefGoogle Scholar
  176. 176.
    Wang, J., P. Souza, M. Kuliszewski, A.K. Tanswell, and M. Post. Expression of surfactant proteins in embryonic rat lung. Am. J. Respir. Cell Mol. Biol. 10: 222–229, 1994.PubMedCrossRefGoogle Scholar
  177. 177.
    Weigel, D., G. Jurgens, F. Kuttner, E. Seifert, and H. Jäckle. The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell 57: 645–658, 1989.PubMedCrossRefGoogle Scholar
  178. 178.
    Weinstein, D.C., A. Ruizi Altaba, W.S. Chen, P. Hoodless, V.R. Prezioso, T.M. Jessell, and J.E. Darnell. The winged-helix transcription factor HNF-3ß is required for notochord development in the mouse embryo. Cell 78: 575–585, 1994.PubMedCrossRefGoogle Scholar
  179. 179.
    Wert, S.E., S.W. Glasser, T.R. Korfhagen, and J.A. Whittsett. Transcriptional elements from the human SP-C gene direct expression in the primordial respiratory epithelium of transgenic mice. Dev. Biol. 156: 426–443, 1993.PubMedCrossRefGoogle Scholar
  180. 180.
    White, R.T., D. Damm, J. Miller, K. Spratt, J. Schilling, S. Hawgood, B. Benson, and B. Cordell. Isolation and characterization of the human pulmonary surfactant apoprotein gene. Nature 317: 361–363, 1985.PubMedCrossRefGoogle Scholar
  181. 181.
    Whitsett, J.A. and J.E. Baatz. Hydrophobic surfactant proteins SP-B and SP-C: molecular biology, structure and function. In: Pulmonary Surfactant, from Molecular Biology to Clinical Practice, edited by B. Robertson, L.M.G. van Golde, and J.J. Batenburg. Amsterdam: Elsevier, 1992, p. 55–75.Google Scholar
  182. 182.
    Whitsett, J.A., J.C. Clark, J.R. Wispé, and G.S. Pryhuber. Effects of TNF-a and phorbol ester on human surfactant protein and MnSOD gene transcription in vitro. Am. J. Physiol. 262 (Lung Cell. Mol. Physiol. 6 ): L688 - L693, 1992.Google Scholar
  183. 183.
    Whitsett, J.A., T.E. Weaver, M.A. Lieberman, J.C. Clark, and C. Daugherty. Differential effects of epidermal growth factor and transforming growth factor-1–3 on synthesis of Mr = 35,000 surfactant-associated protein in fetal lung. J. Biol. Chem. 262: 7908–7913, 1987.PubMedGoogle Scholar
  184. 184.
    Wikenheiser, K.A. and J.A. Whitsett. Tumor progression and cellular differentiation of pulmonary adenocarcinomas in SV40 large T transgenic mice. Am. J. Respir. Cell Mol. Biol. 16: 713–723, 1997.PubMedCrossRefGoogle Scholar
  185. 185.
    Williams, M.C., Y.-X. Cao, A. Hinds, A.K. Rishi, and A. Wetterwald. T1a protein is developmentally regulated and expressed by alveolar type I cells, choroid plexus, and ciliary epithelia of adult rats. Am. J. Respir. Cell Mol. Biol. 14: 577–585, 1996.PubMedCrossRefGoogle Scholar
  186. 186.
    Wolf, M., J. Klug, R. Hackenberg, M. Gessler, K.-H. Grzeschik, M. Beato, and G. Suske. Human CC10, the homologue of rabbit uteroglobin: genomic cloning, chromosomal localization and expression in endometrial cell lines. Hum. Mol. Genet. 1: 371–378, 1992.PubMedCrossRefGoogle Scholar
  187. 187.
    Wu, J.E. and S.A. Santoro. Differential expression of integrin a subunits supports distinct roles during lung branching morphogenesis. Dev. Dyn. 206: 169–181, 1996.PubMedCrossRefGoogle Scholar
  188. 188.
    Wuenschell, C.W., M.E. Sunday, G. Singh, R. Minoo, H.C. Slavkin, and D. Warburton. Embryonic mouse lung epithelial progenitor cells co-express immunohistochemical markers of diverse mature cell lineages. J. Histochem. Cytochem. 44: 112–123, 1996.CrossRefGoogle Scholar
  189. 189.
    Yan, C., M. Ghaffari, J.A. Whitsett, X. Zeng, Z. Sever, and S. Lin. Retinoic acid receptor activation of SP-B gene transcription in respiratory epithelial cells. Am. J. Physiol. 275 (Lung Cell. Mol. Physiol. 19 ): L239 - L246, 1998.Google Scholar
  190. 190.
    Yan, C., Z. Sever, and J.A. Whitsett. Upstream enhancer activity in the human surfactant protein B gene is mediated by thyroid transcription factor 1. J. Biol. Chem. 270: 24852–24857, 1995.PubMedCrossRefGoogle Scholar
  191. 191.
    Yan, C. and J.A. Whitsett. Protein kinase A activation of the surfactant protein B gene is mediated by phosphorylation of thyroid transcription factor 1. J. Biol. Chem. 272: 17327–17332, 1997.PubMedCrossRefGoogle Scholar
  192. 192.
    Yee, W., J. Wang, J. Liu, I. Tseu, M. Kuliszewski, and M. Post. Glucocorticoid-induced tropoelastin expression is mediated via transforming growth factor-ß3. Am. J. Physiol. 270 (Lung Cell. Mol. Physiol. 14 ): L992 - L1001, 1996.Google Scholar
  193. 193.
    Zhao, Y. and S.L. Young. Expression of transforming growth factor-ß type II receptor in rat lung is regulated during development. Am. J. Physiol. 269 (Lung Cell. Mol. Physiol. 13 ): L419 - L426, 1995.Google Scholar
  194. 194.
    Zhou, L., C.R. Dey, S.E. Wert, and J.A. Whitsett. Arrested lung morphogenesis in trans-genic mice bearing an SP-C-TGF-ß1 chimeric gene Dev. Biol. 175: 227–238, 1996.PubMedCrossRefGoogle Scholar
  195. 195.
    Zhou, L., L. Lim, R.H. Costa, and J.A. Whitsett. Thyroid transcription factor-1, hepatocyte nuclear factor-3ß, surfactant protein B, C, and Clara cell secretory protein in developing mouse lung. J. Histochem. Cytochem. 44: 1183–1193, 1996.PubMedCrossRefGoogle Scholar

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© American Physiological Society 1999

Authors and Affiliations

  • Jacques R. Bourbon

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