Skip to main content
Log in

Connective tissue is involved in adult epithelial development of the small intestine during anuran metamorphosis in vitro

  • Original Articles
  • Published:
Roux's archives of developmental biology Aims and scope Submit manuscript

Summary

The role of connective tissue in metamorphic changes of the small intestinal epithelium inXenopus laevis tadpoles was investigated by using organ culture techniques and electron microscopy. Tissue fragments isolated from various parts of the small intestine at stage 57 were cultivated. Larval cell death of the epithelium was induced by thyroid hormone in all fragments, whereas adult epithelial development was observed only in fragments isolated from the anterior intestinal region containing the typhlosole where most of the larval connective tissue was localized. The epithelium was then cultivated in recombination with homologous or heterologous non-epithelial components. The adult epithelium developed only in recombinants containing a thick connective tissue layer from the typhlosole. There was no regional difference in the developmental potency of the epithelium itself. In all explants where adult epithelium developed, the connective tissue increased in cell density just beneath the epithelium, which was rapidly proliferating and forming typical islets. At the same time, fibroblasts possessing well-developed rough endoplasmic reticulum differentiated close to epithelial cells and often made contact with them. These results indicate that the connective tissue originating from the typhlosole plays an important role in adult epithelial development of the anuran small intestine, probably via direct cell-to-cell contacts or some factor(s) synthesized by the fibroblasts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bonneville MA (1963) Fine structural changes in the intestinal epithelium of the bullfrog during metamorphosis. J Cell Biol 18:579–597

    Google Scholar 

  • Dournon C, Chibon P (1974) Influence de la température, de l'âge et des conditions hormonales (thyroxine) sur la prolifération cellulaire chez la jeune larve et pendant la métamorphose du crapaudBufo bufo L. (Amphibien Anoure). Roux's Arch Dev Biol 175:27–47

    Google Scholar 

  • Enami J, Enami S, Koga M (1983) Growth of normal and neoplastic mouse mammary epithelial cells in primary culture: stimulation by conditioned medium from mouse mammary fibroblasts. Gann 74:845–853

    Google Scholar 

  • Fox H (1983) Amphibian metamorphosis. Humana Press, Clifton, pp 119–126

    Google Scholar 

  • Freed J, Mezger-Freed L (1970) Culture methods for anuran cells. In: Prescott DM (ed) Methods in cell physiology, vol 4. Academic Press, New York, pp 19–47

    Google Scholar 

  • Hourdry J, Dauca M (1977) Cytological and cytochemical changes in the intestinal epithelium during anuran metamorphosis. Int Rev Cytol [Suppl] 5:337–385

    Google Scholar 

  • Ishizuya-Oka A, Mizuno T (1984) Intestinal cytodifferentiation in vitro of chick stomach endoderm induced by the duodenal mesenchyme. J Embryol Exp Morphol 82:163–176

    Google Scholar 

  • Ishizuya-Oka A, Shimozawa A (1987a) Development of the connective tissue in the digestive tract of the larval and metamorphosingXenopus laevis. Anat Anz 164:81–93

    Google Scholar 

  • Ishizuya-Oka A, Shimozawa A (1987b) Ultrastructural changes in the intestinal connective tissue ofXenopus laevis during metamorphosis. J Morphol 193:13–22

    Google Scholar 

  • shizuya-Oka A, Shimozawa A (1990) Changes in lectin-binding pattern in the digestive tract ofXenopus laevis during metamorphosis: II. Small intestine. J Morphol 205:9–15

    Google Scholar 

  • Ishizuya-Oka A, Shimozawa A (1991) Induction of metamorphosis by thyroid hormone in anuran small intestine cultured organotypically in vitro. In Vitro Cell Dev Biol 27A:853–857

    Google Scholar 

  • Kerr JFR, Wyllie AII, Currie AR (1972) Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239–257

    Google Scholar 

  • Kinoshita T, Sasaki F, Watanabe K (1986) Regional specificity of anuran larval skin during metamorphosis: Dermal specificity in development and histolysis of recombined skin grafts. Cell Tiss Res 245:297–304

    Google Scholar 

  • Kinoshita T, Takahama H, Sasaki F, Watanabe K (1989) Determination of cell death in the developmental process of anuran larval skin. J Exp Zool 251:37–46

    Google Scholar 

  • Kordylewski L (1983) Light and electron microscopic observations of the development of intestinal musculature inXenopus. Z Mikrosk-anat Forsh 97:719–734

    Google Scholar 

  • Le Douarin N (1964) Étude expérimentale de l'organogènese du tube digestif et du foie chez l'embryon dc Poulet. Bull Biol Fr Belg 98:543–676

    Google Scholar 

  • Lehtonen E, Wartiovaara J, Nordling S, Saxen L (1975) Demonstration of cytoplasmic processes in Millipore filters permitting kidney tube induction. J Embryol Exp Morphol 33:187–203

    Google Scholar 

  • Marsh MN, Trier JS (1974) Morphology and cell proliferation of subepithelial fibroblasts in adult mouse jejunum: I. Structural features. Gastroenterology 67:622–635

    Google Scholar 

  • Marshall JA, Dixon KE (1978) Cell specialization in the epithelium of the small intestine of feedingXenopus laevis tadpoles. J Anat 126:133–144

    Google Scholar 

  • Mathan M, Hermos JA, Trier JS (1972) Structural features of the epitheli-mesenchymal interface of rat duodenal mucosa during development. J Cell Biol 52:577–588

    Google Scholar 

  • McAvoy JW, Dixon KE (1977) Cell proliferation and renewal in the small intestinal epithelium of metamorphosing and adultXenopus laevis. J Exp Zool 202:129–138

    Google Scholar 

  • Nieuwkoop PD, Faber J (1967) Normal table ofXenopus laevis (Daudin). North-Holland, Amsterdam

    Google Scholar 

  • Parker FG, Barnes EN, Kaye GI (1974) The pericryptal fibroblast sheath: IV. Replication, migration, and differentiation of the subepithelial fibroblasts of the crypt and villus of the rabbit jejunum. Gastroenterology 67:607–621

    Google Scholar 

  • Pouyet JC, Hourdry J (1977) Effet de la thyroxine sur la structure des épithéliocytes intestinaux en culture organotypique, chez la larve deDiscoglossus pictus Otth (Amphibien Anoure). Biol Cell 29:123–134

    Google Scholar 

  • Pouyet JC, Hourdry J (1980) Effet de la thyroxine sur la prolifération des épithéliocytes intestinaux en culture organotypique, chez la larve du Crapaud-accoucheur (Alytes obstetricans Laurenti). Biol Cell 38:237–242

    Google Scholar 

  • Rutter WJ, Pictel RL, Harding JD, Chirgwin JM, MacDonald RJ, Przybyla AE (1978) An analysis of pancreatic development: Role of mesenchymal factor and other extracellular factors. In: Papaconstantinou J, Rutter WJ (eds) Molecular control of proliferation and differentiation. Academic Press, New York, pp 205–277

    Google Scholar 

  • Thesleff I, Hurmerinta K (1981) Tissue interactions in tooth development. Differentiation 18:75–88

    Google Scholar 

  • Trowell OA (1959) The culture of mature organs in a synthetic medium. Exp Cell Res 16:118–148

    Google Scholar 

  • Wyllie AH, Kerr JFR, Currie AR (1980) Cell death: The significance of apoptosis. Int Rev Cytol 68:251–306

    Google Scholar 

  • Yasugi S, Mizuno T (1990) Mesenchymal-epithelial interactions in the organogenesis of digestive tract. Zool Sci 7:163–174

    Google Scholar 

  • Yoshizato K (1989) Biochemistry and cell biology of amphibian metamorphosis with a special emphasis on the mechanism of removal of larval organs. Int Rev Cytol 119:97–149

    Google Scholar 

  • Yoshizato K, Kikuyama S, Shioya N (1980) Stimulation of glucose utilization and lactate production in cultured human fibroblasts by thyroid hormone. Biochim Biophys Acta 627:23–29

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ishizuya-Oka, A., Shimozawa, A. Connective tissue is involved in adult epithelial development of the small intestine during anuran metamorphosis in vitro. Roux's Arch Dev Biol 201, 322–329 (1992). https://doi.org/10.1007/BF00592113

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00592113

Key words

Navigation