Abstract
We performed tissue recombination experiments to discover the mesenchymal influences on differentiation of epithelia in chicken digestive organs. Epithelia and mesenchymes were taken from the lung, esophagus, proventriculus, gizzard, small intestine and large intestine of 6-day chicken embryos and recombined in various associations and cultivated in vitro for 6 days. Rather unexpectedly, embryonic chicken pepsinogen (ECPg) gene, a marker of the proventricular epithelium, was induced in the gizzard epithelium, which does not express ECPg in normal development, by the proventricular and lung mesenchymes. In the second half of this study, we investigated the mode of action of mesenchymal cells on ECPg expression in gizzard epithelial cells more precisely using the cell aggregate culture system, in which gizzard epithelial cells were mixed with proventricular, gizzard or lung mesenchymal cells. We found that supporting action of lung mesenchymal cells on ECPg expression was even stronger than that of proventricular mesenchymal cells, and suggest that the action of lung mesenchyme may be due partly to the enhancement of epithelial cell proliferation. According to the results of this study, together with many facts obtained so far, we will discuss a new model for restricted expression of ECPg in the proventricular epithelium in normal development.
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Brauker JH, Trautman MS, Bernfield M (1991) Syndecan, a cell surface proteoglycan, exhibits a molecular polymorphism during lung development. Dev Biol 147:285–292
Ekblom P (1981) Determination and differentiation of the nephron. Med Biol 59:139–160
Frumkin A, Rangini Z, Ben-Yehuda A, Gruenbaum, Y, Fainsod A (1991) A chicken caudal homolog, CHox-cad, is expressed in the epiblast with posterior localization and in the early endodermal lineage. Development 112:207–219
Frumkin A, Pillemer G, Haffner R, Tarcic N, Gruenbaum Y, Fainsod A (1994) A role of CdxA in gut closure and intestinal epithelia differentiation. Development 120:253–263
Fukuda K, Ichinose M, Saiga H, Shiokawa K, Yasugi S (1994a) Developmental changes of DNA methylation pattern of embryonic chick pepsinogen gene. J Biochem 115:502–506
Fukuda K, Ishii Y, Saiga H, Shiokawa K, Yasugi S (1994b) Mesenchymal regulation of epithelial gene expression in developing avian stomach: 5′-flanking region of pepsinogen gene can mediate mesenchymal influence on its expression. Development 120:3487–3495
Goldwin GV, Opperman LA (1980) Induction of supernumerary tracheal buds and the stimulation of DNA synthesis in the embryonic chick lung and trachea by epidermal growth factor. J Embryol Exp Morphol 60:235–243
Grobstein C (1953) Epithelio-mesenchymal specificity in the morphogenesis of mouse submandibular rudiments in vitro. J Exp Zool 124:383–413
Grobstein C (1955) Inductive interaction in the development of mouse metanephros. J Exp Zool 130:319–340
Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:48–92
Hayashi K, Yasugi S, Mizuno T (1988) Isolation and structural analysis of embryonic chicken pepsinogen gene: Avian homologue of chymosin gene. Biochem Biophys Res Commun 152: 776–782
Minoo P, King RJ (1994) Epithelial-mesenchymal interactions in lung development. Annu Rev Physiol 56:13–45
Mizuno T, Yasugi S (1990) Susceptibility of epithelia to directive influences of mesenchymes during organogenesis: Uncoupling of morphogenesis and cytodifferentiation. Cell Differ Dev 31: 151–159
Mori Y, Yoshida K, Morita T, Nakanishi Y (1994) Branching morphogenesis of mouse embryonic submandibular epithelia cultured under three different conditions. Dev Growth Differ 36: 529–539
Nakanishi Y, Uematsu J, Takamatsu H, Fukuda Y, Yoshida K (1993) Removal of heparan sulfate chains halted epithelial branching morphogenesis of the developing mouse submandibular gland in vitro. Dev Growth Differ 35:371–384
Nogawa H, Ito T (1995) Branching morphogenesis of embryonic mouse lung epithelium in mesenchyme-free culture. Development 121:1015–1022
Nogawa H, Mizuno T (1981) Mesenchymal control over elongation and branching morphogensis in salivary gland development. J Embryol Exp Morphol 64:209–221
Peters K, Werner S, Liao X, Wert S, Whisett J, Williams L (1994) Targeted expression of a dominant negative FGF receptor blocks branching morphogenesis and epithelial differentiation of the mouse lung. EMBO J 13:3296–3301
Peterson CA, Grainger RM (1985) Differentiation of embryonic chck feather-forming and scale-forming tissue in transfilter cultures. Dev Biol 111:8–25
Riso J (1983) Morphology of epitheiao-mesenchymal interaction during lung development of the mouse. Cell Differ 13:309–318
Ruoslahti E, Yamaguchi Y (1991) Proteoglycans a smodulators of growth factor activities. Cell 64:867–869
Saint-Marie G (1962) A paraffin embedding technique for studies employing immunofluorescence. J Histochem Cytochem 10: 250–256
Saxén L, Karkinen-Jääkeläinen M, Lehtone S, Nordling S, Wartiovaara J (1976) Inductive tissue interactions. In: Poste G, Nicolson GL (eds) The cell surface (Animal embryogenesis and development) North-Holland Publishing Company, Amsterdam
Schuger L, Varani J, Mitra R Jr, Gilbride K (1993) Retinoic acid stimulates mouse lung development by a mechanism involving epithelial-mesenchymal interaction and regulation of epidermal growth factor receptors. Dev Biol 159:462–473
Seth R, Chum L, Wu F, Wuenschell C, Hall FL, Slavkin HC, 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
Spooner BS, Wessells NK (1970) Mammalian lung development: Interactions in primodium formation and bronchial morphogenesis. J Exp Zool 175:445–454
Sub E, Chen L, Taylor J, Traber PG (1994) A homeodomain protein related to caudal regulates intestine-specific gene transcription. Mol Cell Biol 14:7340–7351
Takiguchi K, Yasugi S, Mizuno T (1986) Gizzard epithelium of chick embryos can express embryonic pepsinogen antigen, a marker protein of proventriculus. Roux's Arch Dev Biol 195: 475–483
Takiguchi K, Yasugi S, Mizuno T (1988a) Developmental changes in the ability fo express embryonic pepsinogen in the stomach epithelia of chick embryos. Roux's Arch Dev Biol 197:56–62
Takiguchi K, Yasugi S, Mizuno T (1988b) Pepsinogen induction in chick stomach epithelia by reaggregated proventricular mesenchymal cells in vitro. Dev Growth Differ 30:241–250
Takiguchi-Hayashi K, Yasugi S (1990) Transfilter analysis of the inductive influence of proventricular mesenchyme on stomach epithelial differentiation of chick embryos. Roux's Arch Dev Biol 198:460–466
Urase K, Yasugi S (1993) Induction and inhibition of epithelial differentiation by the mixed cell aggregates of the mesenchymes from the chicken embryonic digestive tract. Dev Growth Differ 35:33–40
Warburton D, Seth R, Shum L, Horcher PG, Hall FL, Werb Z, Slavkin HC (1992) Epigenetic role of epidermal growth factor expression and signaling in embryonic mouse lung morphogenesis. Dev Biol 149:123–133
Wilkinson DG (1992) Wholemount in situ hybridization of vertebrate embryos. In: Wilkinson DG (ed) in situ Hybridization: A practical approach. IRL Press, Oxford, pp 75–83
Yasugi S (1993) Role of epithelial-mesenchymal interaction in differentiation of epithelium of vertebrate digestive organs. Dev Growth Differ 35:1–9
Yasugi S (1994) Regulation of pepsinogen gene expression in epithelial cells of vertebrate stomach during development. Int J Dev Biol 38:273–279
Yasugi S, Mizuno T (1990) Mesenchymal-epithelial interactions in the organogenesis of digestive tract. Zool Sci 7:159–170
Yasugi S, Matsushita S, Mizuno T (1985) Gland formation induced in the allantoic and small-intestinal endoderm by the proventricular mesenchyme is not coupled with pepsinogen expression. Differentiation 30:47–52
Yasugi S, Hayashi K, Takiguchi K, Mizuno T, Mochii M, Kodama R, Agata K, Eguchi G (1987) Immunological relationships among embryonic and adult chicken pepsinogens: A study with monoclonal and polyclonal antibodies. Dev Growth Differ 29:85–91
Yasugi S, Kedinger M, Simmon-Assmann P, Bouziges F, Haffen K (1989) Differentiation of proventricular epithelium in xenoplastic associations with mesenchymal or fibroblastic cells. Roux's Arch Dev Biol 198:114–117
Yokouchi Y, Sakiyama J, Kuroiwa A (1995) Coordinated expression of Abd-B subfamily genes of the HoxA cluster in the developing digestive tract of chick embryo. Dev Biol 169:76–89
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Urase, K., Fukuda, K., Ishii, Y. et al. Analysis of mesenchymal influence on the pepsinogen gene expression in the epithelium of chicken embryonic digestive tract. Roux's Arch Dev Biol 205, 382–390 (1996). https://doi.org/10.1007/BF00377218
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DOI: https://doi.org/10.1007/BF00377218