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Proliferation and differentiation of intestinal epithelial cells during development of Barbus conchonius (Teleostei, Cyprinidae)


The processes of proliferation, cell division and differentiation of intestinal epithelial cells have been studied during development of the fish, Barbus conchonius. On the 3rd day, nearly all cells of the presumptive gut proliferate. Once the intestinal epithelium begins to differentiate, a decreasing percentage of proliferative cells can be found. On the 7th day, when intestinal folds start to develop, the proliferative cells become restricted to the future basal parts of the folds.

Ultrastructural examination of 3H-thymidine-labeled cells and mitotic cells of 6-day-old larvae shows that functional enterocytes are proliferative. The same feature is suggested for older fish. Proliferating undifferentiated “dark” cells, characterized by many free ribosomes and a few organelles, are also present in the intestinal epithelium of larval fish; they are considered to be stem cells, mainly for goblet cells. Proliferating goblet cells and enteroendocrine cells were not observed. The latter cell type is scarce and has a long turnover time.

A common feature of all these dividing cells is the presence of isolated spherical to cylindrical lamellar structures which may have lost contact with the cell membrane during prophase; they probably regain this contact by fusion with the cell membrane at the end of mitosis.

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  1. Andrew A (1974) Further evidence that enterochromaffin cells are not derived from the neural crest. J Embryol Exp Morphol 31:589–598

  2. Bjerknes M, Cheng H (1981) The stem-cell zone of the small intestinal epithelium. III: Evidence from columnar, enteroendocrine and mucous cells in the adult mouse. Am J Anat 160:77–91

  3. Cheng H, Leblond CP (1974a) Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. I: Columnar cell. Am J Anat 141:461–480

  4. Cheng H, Leblond CP (1974b) Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. V. Unitarian theory of the origin of the four epithelial cell types. Am J Anat 141:537–562

  5. Dongen JM van, Visser WJ, Daems WTh, Galjaard H (1976) The relation between cell proliferation and ultrastructural development in rat intestinal epithelium. Cell Tissue Res 174:183–200

  6. Doyle DG (1980) The origin of nuclear bodies: a study of the undifferentiated epithelial cells of the equine small intestine. Am J Anat 157:61–70

  7. Fontaine J, Le Douarin NM (1977) Analysis of endoderm formation in the avian blastoderm by the use of quail-chick chimaeras. The problem of the neurectodermal origin of the cells of the APUD series. J Embryol Exp Morphol 41:209–222

  8. Fujimoto S, Hattori T, Kimoto K, Yamashita S, Fujita S, Kawai K (1980) Tritiated thymidine autoradiographic study on origin and renewal of gastrin cells in antral area of hamsters. Gastroenterology 79:785–791

  9. Fujita T, Kobayashi S (1977) Structure and function of gut endocrine cells. In: Bourne GH, Danielli JF (eds) International review of cytology. Supplement 6, Academic Press New York pp 187–233

  10. Gas N, Noaillac-Depeyre J (1974) Renouvellement de l'épithélium intestinal de la carpe (Cyprinus carpio L.) influence de la saison. CR Acad Sc (Paris) Sér D 279:1085–1088

  11. Gauthier GF, Landis SC (1972) The relationship of ultrastructural and cytochemical features to absorptive activity in the goldfish intestine. Anat Rec 172:675–702

  12. Hermos JA, Mathan M, Trier JS (1971) DNA-synthesis and proliferation by villous epithelial cells in fetal rats. J Cell Biol 50:266–258

  13. Hyodo-Taguchi Y (1970) Effect of X-irradiation on DNA-synthesis and cell proliferation in the intestinal epithelial cells of goldfish at different temperatures with special reference to recovery process. Radiat Res 41:568–578

  14. Iwai T (1969) Fine structure of gut epithelial cells of larval and juvenile carp during absorption of fat and protein. Arch Histol Jpn 30:183–189

  15. Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137a-138a

  16. Lamers CHJ, Rombout JHWM, Timmermans LPM (1981) An experimental study on neural crest migration in Barbus conchonius (Cyprinidae, Teleostei) with special reference to the origin of the enteroendocrine cells. J Embryol Exp Morphol 62:309–323

  17. Lehy TCR, Willems GMD (1976) Population kinetics of antral gastrin cells in the mouse. Gastroenterology 71:614–619

  18. Marshall JA, Dixon KE (1978) Cell proliferation in the intestinal epithelium of Xenopus laevis tadpoles. J Exp Zool 203:31–40

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

  20. Noaillac-Depeyre J, Gas N (1973) Mise en évidence d'une zone adaptée au transport des ions dans l'intestine de carp commune (Cyprinus carpio L). CR Hebd Seance Acad Sci (Paris) 276:773–776

  21. Noaillac-Depeyre J, Gas N (1976) Electron microscopic study on gut epithelium of the tench (Tinca tinca L.) with respect to its absorptive functions. Tissue Cell 8:511–530

  22. Noaillac-Depeyre J, Gas N (1984) Etude cytophysiologique de l'épithélium intestinal du poisson-chat (Ameiurus nebulosus L.). Can J Zool (in press)

  23. Pearse AGE (1973) Cell migration and the alimentary system: Endocrine contributions of the neural crest to the gut and its derivatives. General review. Digestion 8:372–385

  24. Pearse AGE (1979) The endocrine division of the nervous system: a concept and its verification. In: Szelke McIntyre (eds) Molecular endocrinology. Elsevier, Amsterdam, pp 3–18

  25. Rombout JHWM (1977) Enteroendocrine cells in the digestive tract of Barbus conchonius (Teleostei, Cyprinidae). Cell Tissue Res 185:435–450

  26. Rombout JHWM, Lamers CHJ, Hanstede JG (1978) Enteroendocrine APUD cells in the digestive tract of larval Barbus conchonius (Teleostei, Cyprinidae). J Embryol Exp Morphol 47:121–135

  27. Shcherbina MA, Trofimova LN, Kazlauskene OP (1976) The activity of protease and the resorption intensity of protein with the introduction of different quantities of fat into the food of the carp, Cyprinus carpio. J Ichthyol 16:632–636

  28. Stroband HWJ, Dabrowski KR (1979) Morphological and physiological aspects of the digestive system and feeding in fresh-water fish larvae. In: Fontaine M. (ed) Nutrition des Poissons CNRS, pp 355–376

  29. Stroband HWJ, Debets FMH (1978) The ultrastructure and renewal of the intestinal epithelium of the juvenile grasscarp, Ctenopharyngodon idella (Val). Cell Tissue Res 187:181–200

  30. Stroband HWJ, Kroon AG (1981) The development of the stomach in Clarias lazera and the intestinal absorption of protein macromolecules. Cell Tissue Res 215:397–415

  31. Stroband HWJ, Veen FH van der (1981) Localization of protein absorption during transport of food in the intestine of the grass carp, Ctenopharyngodon idella (Val). J Exp Zool 218:149–156

  32. Stroband HWJ, Meer H vd, Timmermans LPM (1979) Regional function differentiation in the gut of the grasscarp, Ctenopharyngodon idella (Val), as determined by the alkaline phosphatase activity and the absorption of peroxidase in the intestinal epithelium. Histochemistry 64:235–249

  33. Trier JS, Moxey PC (1980) Epithelial cell proliferation in the intestine of the winter flounder, Pseudopleuronectes americanus. Cell Tissue Res 206:379–385

  34. Tsubouchi S (1981) Kinetic analysis of epithelial cell migration in the mouse descending colon. Am J Anat 161:239–246

  35. Tsubouchi S, Leblond CP (1979) Migration and turnover of enteroendocrine and caveolated cells in the epithelium of the descending colon as shown by radio-autography after continuous infusion of 3H-thymidine into mice. Am J Anat 156:431–452

  36. Vries IG de, Bosman FT (1982) Simultaneous detection of DNA-replication and hormone production using a combination of autoradiography and immunocytochemistry. J Histochem Cytochem 30:584

  37. Yamamoto T (1966) An electron microscope study of the columnar epithelial cell in the intestine of fresh water teleosts: goldfish (Carassius auratus) and rainbow trout (Salmo irideus) Z Zellforsch 72:66–87

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Correspondence to Dr. J. H. W. M. Rombout.

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Rombout, J.H.W.M., Stroband, H.W.J. & Taverne-Thiele, J.J. Proliferation and differentiation of intestinal epithelial cells during development of Barbus conchonius (Teleostei, Cyprinidae). Cell Tissue Res. 236, 207–216 (1984).

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Key words

  • Development
  • Enterocytes
  • Fish
  • Mitosis
  • Ultrastructure