Abrogation of transforming growth factor-β type II receptor stimulates embryonic mouse lung branching morphogenesis in culture

Developmental Biology

Volumn 180, Issue 1, 1996, Pages 242-257

  Zhao, Jingsong ^a   Bu, Ding ^a   Lee, Matt ^a   Slavkin, Harold C ^a,c   Hall, Frederick L ^b   Warburton, David ^a,b  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LUNG DEVELOPMENT; MESENCHYME; MORPHOGENESIS; MOUSE; NONHUMAN; ORGAN CULTURE; PRIORITY JOURNAL; TISSUE INDUCTION;

ANIMALIA;

EID: 0030602054     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1996.0298     Document Type: Article

References (58)

1. Alescio, T., and Cassini, A. (1962). Induction in vitro of tracheal buds by pulmonary mesenchyme grafted onto tracheal epithelium. J. Exp. Zool. 150, 83-94.
2. Araki, N., Robinson, F.D., and Nishimoto, S. K. (1993). Rapid and sensitive method for quantitation of bone Gla protein mRNA using competitive polymerase chain reaction. J. Bone Miner. Res. 8, 313-322.
3. Bonström, H., Willetts, K., Pekny, M., Levéen, P., Lindahl, P., Hedstrand, H., Pekna, M., Hellström, M., Gebre-Medhin, S., Schalling, M., Nilsson, M., Kurland, S., Törnell, J., Heath, J. K., and Betsholtz, C. (1996). PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 85, 863-873.
4. Bruskin, A., Jackson, J., Bishop, J. M., McCarley, D. J., and Schatzman, R. C. (1990). Six amino acids from the retroviral gene gag greatly enhance the transforming potential of the oncogene verb-B. Oncogene 5, 15-24.
5. Chai, Y., Mah, A., Crohin, C., Groff, S., Bringas, P., Jr., Le, T., Santos, V., and Slavkin, H. C. (1994). Specific transforming growth factor-β subtypes regulate embryonic mouse Meckel's cartilage and tooth development. Dev. Biol. 162, 85-103.
6. Chen, R. H., Ebner, R., and Derynck, R. (1993). Inactivation of the type II receptor reveals two receptor pathways for the diverse TGF-beta activities. Science 260, 1335-1338.
7. Ferguson, M. W. J. (1988). Palate development. Development 103(Suppl.), 41-60.
8. Girard, F., Strausfeld, U., Fernandez, A., and Lamb, N. J. C. (1991). Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell 67, 1169-1179.
9. Hall, F. L., Benya, P., Padilla, S., Carbonaro-Hall, D., Williams, R., Buckley, S., and Warburton, D. (1996). TGF-β type II receptor signaling: Intrinsic/associated casein kinase activity, receptor interactions, and functional effects of blocking antibodies. Biochem. J. 316, 303-310.
10. Heine, U. I., Munoz, E. F., Flanders, K. C., Roberts, A. B., and Sporn, M. B. (1990). Colocalization of TGF-beta 1 and collagen I and III, fibronectin and glycosaminoglycans during lung branching morphogenesis. Development 109, 29-36.
11. Inagaki, M., Moustakas, A., Lin, H. Y., Lodish, H. F., and Carr, B. I. (1993). Growth inhibition by transforming growth factor beta (TGF-beta)type I is restored in TGF-beta-resistant hepatomacells after expression of TGF-beta receptor type II cDNA. Proc. Natl. Acad. Sci. USA 90, 5359-5363.
12. Iseki, S., Osumi-Yamashita, N., Miyazono, K., Franzen, P., Ichijo, H., Ohtani, H., Hayashi, Y., and Eto, K. (1995). Localization of transforming growth factor-beta type I and type II receptors in mouse development. Exp. Cell Res. 219, 339-347.
13. Jaskoll, T. F., Don Wheeler, G., Johnson, R., and Slavkin, H. C. (1988). Embryonic mouse lung morphogenesis and type II cytodifferentiation in serumless, chemically defined medium using prolonged in vitro cultures. Cell Differ. 24, 105-117.
14. Kaartinen, V., Voncken, J. W., Shuler, C., Warburton, D., Bu, D., Heisterkamp, N., and Groffen, J. (1995). Abnormal lung development and cleft palate in mice lacking TGF-β3 indicates defects of epithelial-mesenchymal interaction. Nature Genet. 11, 415-421.
15. Laiho, M., Decaprio, J. A., Ludlow, J. W., Livingston, D.M., and Massagué, J. (1990). Growth inhibition by TGF-beta linked to suppression of retinoblastoma protein phosphorylation. Cell 62, 175-185.
16. Lawler, S., Candia, A. F., Ebner, R., Shum, L., Lopez, A. R., Moses, H. L., Wright, C. V., and Derynck, R. (1994). The murine type II TGF-beta receptor has a coincident embryonic expression and binding preference for TGF-beta 1. Development 120, 165-175.
17. Lin, H. Y., Wang, X. F., Ng-Eaton, E., Weinberg, R. A., and Lodish, H. F. (1992). Expression cloning of the TGF-beta type II receptor, a functional transmembrane serine/threonine kinase. Cell 68, 775-785.
18. Lopez-Casillas, F., Wrana, J. L., and Massagué, J. (1993). Betaglycan presents ligand to the TGF beta signaling receptor. Cell 73, 1435-1444.
19. Lopez-Casillas, F., Payne, H. M., Andres, J. L., and Massagué, J. (1994). Betaglycan can act as a dual modulator of TGF-beta access to signaling receptors: Mapping of ligand binding and GAG attachment sites. J. Cell Biol. 124, 557-568.
20. Marcus-Sekura, C. J. (1988). Techniques for using antisense oligonucleotides to study gene expression. Anal. Biochem. 172, 289-295.
21. Massagué, J., Cheifetz, S., Boyd, F. T., and Andres, J. L. (1990). TGF-beta receptors and TGF-beta binding proteoglycans: recent progress in identifying their functional properties. Ann. NY Acad. Sci. 593, 59-72.
22. Massagué, J., Heino, J., and Laiho, M. (1991). Mechanisms in TGF-beta action. Ciba Found. Symp. 157, 51-59.
23. Mercola, M., and Stiles, C. D. (1988). Growth factor superfamilies and mammalian embryogenesis. Development 102, 451-460.
24. Miettinen, P. J., Berger, J. E., Meneses, J., Phung, Y., Pedersen, R. A., Werb, Z., and Derynck, R. (1995). Epithelial immaturity and failure in mice lacking epidermal growth factor receptor. Nature 376, 337-341.
25. Minoo, P., Ham dan, H., Bu, D., Warburton, D., Stepanik, P., and deLemos, R. (1995). TTF-1 regulates lung epithelial morphogenesis. Dev. Biol. 112, 694-698.
26. Minoo, P., and King, R. J. (1994). Epithelial-mesenchymal interactions in lung development. Annu. Rev. Physiol. 56, 13-45.
27. Moses, H. L., Yang, E. Y., and Pietenpol, J. A. (1991). Regulation of epithelial proliferation by TGF-beta. Ciba Found. Symp. 157, 66-74.
28. Moustakas, A., Lin, H. Y., Henis, Y. I., Plamondon, J., O'Connor McCourt, M. D., and Lodish, H. F. (1993). The transforming growth factor beta receptors types I, II, and III form hetero-oligomeric complexes in the presence of ligand. J. Biol. Chem. 268, 22215-22218.
29. Neckers, L., and Whitesell, L. (1993). Antisense technology: Biological utility and practical considerations. Am. J. Physiol. 265, L1-L12.
30. Pelton, R. W., Johnson, M. D., Perkett, E. A., Gold, L. I., and Moses, H. L. (1991). Expression of transforming growth factor-beta 1, -beta 2, and -beta 3 mRNA and protein in the murine lung. Am. J. Respir. Cell Mol. Biol. 5, 522-530.
31. Peters, K., Werner, S., Liao, X., Wert, S., Whitsett, J., and Williams, L. (1994). Targeted expression of a dominant negative FGF receptor blocks branching morphogenesis and epithelial differentiation of the mouse lung. EMBO J. 5, 3296-3301.
32. Prelich, G., Tan, C. K., Kostura, M., Matthews, M. B., So, A. G., Downey, K.M., and Stillman, B. (1987). Functional identity of proliferating cell nuclear antigen and a DNA polymerase-delta auxiliary protein. Nature 326, 517-520.
33. Raaberg, L., Nexo, E., Poulsen, S. S., and Jorgensen, P. E. (1995a). An immunologic approach to induction of epidermal growth factor deficiency: Induction and characterization of autoantibodies to epidermal growth factor in rats. Pediatr. Res. 37, 169-174.
34. Raaberg, L., Nexo, E., Jorgensen, P.E., Poulsen, S.S., and Jakab, M. (1995b). Fetal effects of epidermal growth factor deficiency induced in rats by autoantibodies against epidermal growth factor. Pediatr. Res. 37, 175-181.
35. Raaberg, L., Nexo, E., Buckley, S., Luo, W., and Snead, M. L. (1991). Epidermal growth factor transcription, translation and signal transduction by rat type II pneumocytes in culture. Am. J. Respir. Cell Mom. Biol. 6, 44-49.
36. Roberts, A. B., Flanders, K. C., Heine, U. I., Jakowlew, S. B., Kondaiah, P., Kim, S. J., and Sporn, M. B. (1990). Transforming growth factor-beta: Multifunctional regulator of differentiation and development. Philos Trans. R. Soc. London [Biol]. 327, 145-154.
37. Sanger, R., Nickren, S., and Coulson, R. R. (1977). DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5463-5467.
38. Serra, R., and Moses, H. L. (1995). pRb is necessary for inhibition of N-myc expression by TGF-β 1 in embryonic lung organ cultures. Development 121, 3057-3066.
39. Serra, R., Pelton, R. W., and Moses, H. L. (1994). TGF beta 1 inhibits branching morphogenesis and N-myc expression in lung bud organ cultures. Development 120, 2153-2161.
40. Seth, R., Shum, L., Wu, F., Wuenschell, C., Hall, F. L., Slavkin, H. C., and Warburton, D. (1993). Role of epidermal growth factor expression in early mouse embryo lung branching morphogenesis in culture: Antisense oligodeoxynucleotide inhibitory strategy. Dev. Biol. 158, 555-559.
41. Shannon, J. M. (1994). Induction of alveolar type II cell differentiation in fetal tracheal epithelium by grafted distal lung mesenchyme. Dev. Biol. 166, 600-614.
42. Smith, R., Peters, G., and Dickson, C. (1995). Genomic organization of the mouse cyclin D 1 gene (Cyl-1). Genomics 25, 85-92.
43. Sporn, M. B., and Roberts, A.B. (1990). TGF-beta: Problems and prospects. Cell. Regul. 1, 875-882.
44. Souza, P., Kuliszewski, M., Wang, J., Tseu, I., Tanswell, A. K., and Post, M. (1995). PDGF-AA and its receptor influence early lung branching via an epithelial-mesenchymal interaction. Development 121, 2559-2567.
45. Tan, C. K., Castillo, C., So, A. G., and Downey, K.M. (1986). An auxiliary protein for DNA polymerase-delta from fetal calf thymus. J. Biol. Chem. 261, 12310-12316.
46. Vainio, S., Karavanova, I., Jowett, A., and Thesleff, I. (1993). Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell 75, 45-58.
47. Wagner, R. W. (1994). Gene inhibition using antisense oligodeoxynucleotides. Nature 372, 333-335.
48. Wang, X. F., Lin, H. Y., Ng Eaton, E., Downward, J., Lodish, H. F., and Weinberg, R. A. (1991). Expression cloning and characterization of the TGF-beta type III receptor. Cell 67, 797-805.
49. Wang, J., Kuliszewski, M., Yee, W., Sedlackova, L., Xu, J., Tseu, I., and Post, M. (1995). Cloning and expression of glucocorticoid-induced genes in fetal rat lung fibroblasts. J. Biol. Chem. 270, 2722-2728.
50. Warburton, D. (1991). Epigenetic autocrine and paracrine factors regulating lung morphogenesis: A paradigm for lung repair. Chest 99, 15S-18S.
51. Warburton, D., Seth, R., Shum, L., Horcher, P. G., Hall, F. L., Werb, Z., and Slavkin, H. C. (1992). Epigenetic role of epidermal growth factor expression and signaling in embryonic mouse lung morphogenesis. Dev. Biol. 149, 123-133.
52. Wrana, J. L., Attisano, L., Carcamo, J., Zentella, A., Doody, J., Laiho, M., Wang, X. F., and Massagué, J. (1992). TGF beta signals through a heteromeric protein kinase receptor complex. Cell 71, 1003-1014.
53. Wrana, J. L., Attisano, L., Wieser, R., Ventura, F., and Massagué, J. (1994). Mechanism of activation of the TGF-beta receptor. Nature 370, 341-347.
54. Zhao, J., Araki, N., and Nishimoto, S. K. (1995). Quantitation of matrix Gla protein mRNA by competitive polymerase chain reaction using glyceraldehyde-3-phosphate dehydrogenase as an internal control. Gene 155, 159-165.
55. Zhao, J., and Nishimoto, S. K. (1995). An RNA-competitive polymerase chain reaction method for human matrix γ-carboxyglutamic acid protein mRNA measurement. Anal. Biochem. 228, 162-164.
56. Zhao, J., and Nishimoto, S. K. (1996). Matrix Gla protein gene expression is elevated during postnatal development. Matrix Biol. 15, 131-40.
57. Zhao, Y., and Young, S. L. (1995). Expression of transforming growth factor-β type II receptor in rat lung is regulated during development. Am. J. Physiol. 269, L419-L426.
58. Zhou, L., Dey, C. R., Wert, S. E., and Whitsett, J. A. (1996). Arrested lung morphogenesis in transgenic mice bearing an SP-C-TGF-beta 1 chimeric gene. Dev. Biol. 175, 227-238.