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The relation between cell proliferation, differentiation and ultrastructural development in rat intestinal epithelium

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Summary

The ultrastructural development of the principal cells in rat small intestine was studied by morphometric analyses in relation to the exact cell position along crypt and villus. From the bottom to the tip of the crypt, a gradual increase occurred in absolute size of the total cell, the cytoplasm, the terminal web and of nearly all cell organelles. Also, the relative size of the cytoplasm, mitochondria, microvilli and endoplasmic reticulum increased during crypt cell differentiation. No sudden changes in ultrastructure were observed in the so-called “critical decision zone”, normally located halfway up the crypt where the proliferative activity ceases. At the crypt-villous junction a 1.4–3 fold increase in cell size, cytoplasm, terminal web and of most organelles was noted. Expansion of the proliferative cell compartment over the total length of the crypt as occurs during recovery after a low X-irradiation dose (72 h after 400 R) does not affect the normal development of cellular ultrastructure. These findings are discussed in relation to biochemical and cell kinetic data.

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References

  • Bennet, G.: Migration of glycoproteins from Golgi apparatus to cell coat in the columnar cells of the duodenal epithelium. J. Cell Biol. 45, 668–673 (1970)

    Google Scholar 

  • Both, N.J. de, Dongen, J.M. van, Hofwegen, B. van, Keulemans, J., Visser, W.J., Galjaard, H.: The influence of various cell kinetic conditions on functional differentiation in the small intestine of the rat. A study of enzymes bound to subcellular organelles. Develop. Biol. 38, 119–137 (1974a)

    Google Scholar 

  • Both, N.J. de, Plaisier, H.: The influence of changing cell kinetics on functional differentiation in the small intestine of the rat. J. Histochem. Cytochem. 22, 352–360 (1974b)

    Google Scholar 

  • Brown, A.L.: Microvilli of the human jejunal epithelial cell. J. Cell Biol. 12, 623–627 (1962)

    Google Scholar 

  • Bruyn, W.C. de, McGee-Russel, S.M.: Bridging a gap in pathology and histology. J. roy. micr. Soc. 85, B 1, 77–90 (1966)

    Google Scholar 

  • Cairnie, A.B., Lamerton, L.F., Steel, G.G.: Cell proliferation studies in the intestinal epithelium of the rat. I. Determination of the kinetic parameters. Exp. Cell Res. 39, 528–538 (1965)

    Google Scholar 

  • Cheng, H., Leblond, C.P.: Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. Amer. J. Anat. 141, 461–561 (1974)

    Google Scholar 

  • Clarke, R.M.: The effect of growth and of fasting on the number of villi and crypts in the small intestine of the albino rat. J. Anat. (Lond.) 112, 27–33 (1972)

    Google Scholar 

  • Eder, M.: Zur Darstellung von Wachstum und Differenzierung nach gleichzeitiger Autoradiographie mit 3H-Thymidine und histochemische Enzymreaktionen. Naturwissenschaften 14, 339–340 (1964)

    Google Scholar 

  • Fortin-Magana, R., Hurwitz, R., Herbst, J.J., Kretchmer, N.: Intestinal enzymes: Indicators of proliferation and differentiation in the jejunum. Science 167, 1627–1628 (1970)

    Google Scholar 

  • Galjaard, H., Bootsma, D.: The regulation of cell proliferation and differentiation in intestinal epithelium. II. A quantitative histochemical and autoradiographic study after low doses of X-irradiation. Exp. Cell Res. 58, 79–92 (1969)

    Google Scholar 

  • Galjaard, H., Buys, J., Duuren, M. van, Giesen, J.: A quantitative histochemical study of intestinal mucosa after X-irradiation. J. Histochem. Cytochem. 18, 291–301 (1970)

    Google Scholar 

  • Galjaard, H., Meer-Flieggen, W. van der, Both, N.J. de: Cell differentiation in gut epithelium. In: Cell differentiation (ed. by D. Viza and H. Harris), pp. 322–328. Copenhagen: Munksgaard 1972

    Google Scholar 

  • Ginsel, L.A., Daems, W.Th., Emeiss, J.J., Vio, P.M.A., Gemund, J.J. van: Fine structure and silverstaining patterns of lysosome-like bodies in absorptive cells of the small intestine in normal children and children with a lysosomal storage disease. Virchows Arch. Abt. B 13, 119–144 (1973)

    Google Scholar 

  • Gonzalez-Licea, A.: Polarization of mitochondria in the absorptive cells of the small intestine of suckling rats. Lab. Invest. 23, 163–167 (1970)

    Google Scholar 

  • Iemhoff, W.G.J., Hülsmann, W.C.: Development of mitochondrial enzyme activities in rat small intestinal epithelium. Europ. J. Biochem. 23, 429–434 (1971)

    Google Scholar 

  • Imondi, A.R., Balis, M.E., Lipkin, M.: Changes in enzyme levels accompanying differentiation of intestinal epithelial cells. Exp. Cell Res. 58, 323–330 (1969)

    Google Scholar 

  • Jasper, D.K., Bronk, J.R.: Studies on the physiological and structural characteristics of rat intestinal mucosa. Mitochondrial structural changes during amino acid absorption. J. Cell Biol. 38, 277–291 (1968)

    Google Scholar 

  • Jervis, H.R.: Enzymes in the mucosa of the small intestine of the rat, the guinea pig, and the rabbit. J. Histochem. Cytochem. 11, 692–699 (1963)

    Google Scholar 

  • Jeynes, B.J., Altmann, G.G.: A region of mitochondrial division in the epithelium of the small intestine of the rat. Anat. Rec. 182, 289–296 (1975)

    Google Scholar 

  • Jonge, H.R. de: Biochemical investigations on rat small intestinal epithelium. Thesis. Rotterdam: Bronder Offset B.V. (1975)

    Google Scholar 

  • Josephson, R.L., Altmann, G.G.: Variation in the silver-staining of the Golgi complex along the epithelium of the intestinal villi in adult rat. Anat. Rec. 173, 221–224 (1972)

    Google Scholar 

  • Lesher, S.: Compensatory reactions in intestinal crypt cells after 300 Roentgens of cobalt-60 gamma irradiation. Radiat. Res. 32, 510–519 (1967)

    Google Scholar 

  • Lipkin, M.: Proliferation and differentiation of gastrointestinal cells. Physiol. Rev. 53, 891–915 (1973)

    Google Scholar 

  • Loehry, C.A., Creamer, B.: Three-dimensional structure of the human small intestinal mucosa in health and disease. Gut 10, 6–12 (1969)

    Google Scholar 

  • Moog, F., Grey, R.D.: Spatial and temporal differentiation of alkaline phosphatase on the intestinal villi of the mouse. J. Cell Biol. 32, 1–6 (1967)

    Google Scholar 

  • Nordström, C., Dahlqvist, A., Josefsson, L.: Quantitative determination of enzymes in different parts of the villi and crypts of rat small intestine. J. Histochem. Cytochem. 15, 713–721 (1968)

    Google Scholar 

  • Osborne, J.W., Prasad, K.N., Zimmerman, G.R.: Changes in rat intestine after X-irradiation of exteriorized short segments of ileum. Radiat. Res. 43, 131–142 (1970)

    Google Scholar 

  • Padykula, H.A.: Recent functional interpretaions of intestinal morphology. Fed. Proc. 21, 873–879 (1962)

    Google Scholar 

  • Padykula, H.A., Strauss, E.W., Ladman, A.J., Gardner, F.H.: A morphologic and histochemical analysis of the human jejunal epithelium in nontropical sprue. Gastroenterology 40, 735–765 (1961)

    Google Scholar 

  • Palay, S.L., Karlin, L.J.: An electronmicroscopic study of the intestinal villus. I. The fasting animal. J. biophys. biochem. Cytol. 5, 363–372 (1959a)

    Google Scholar 

  • Palay, S.L., Karlin, L.J.: An electronmicroscopic study of the intestinal villus. II. The pathway of fat absorption. J. biophys. biochem. Cytol. 5, 373–384 (1959b)

    Google Scholar 

  • Porter., K.R.: Independence of fat absorption and pinocytosis. Fed. Proc. 28, 35–40 (1969)

    Google Scholar 

  • Riecken, E.O., Dowling, H.R.: Intestinal adaptation. Stuttgart: Schattauer Verlag 1974

    Google Scholar 

  • Rijke, R.P.C., Plaisier, H., Hoogeveen, A.T., Lamerton, L.F., Galjaard, H.: The effect of continuous irradiation on cell proliferation and maturation in small intestinal epithelium. Cell Tiss. Kinet. 8, 441–453 (1975)

    Google Scholar 

  • Rubin, W., Ross, L.L., Sleisenger, M.H., Weser, E.: An electron microscopic study of adult celiac disease. Lab. Invest. 15, 1720–1747 (1966)

    Google Scholar 

  • Taylor, A.B., Adamstone, F.B.: Ultrastructural changes in epithelial cells of crypts and villi of jejunum of the rat. Anat. Rec. 148, 334 (1964)

    Google Scholar 

  • Toner, P.G.: Cytology of intestinal epithelial cells. Int. Rev. Cytol. 24, 233–343 (1968)

    Google Scholar 

  • Trier, J.S.: Studies on small intestinal crypt epithelium. I. The fine structure of the crypt epithelium of the proximal small intestine of fasting humans. J. Cell Biol. 18, 599–620 (1963)

    Google Scholar 

  • Trier, J.S.: Structure of the mucosa of the small intestine as it relates to intestinal function. Fed. Proc. 26, 1391–1404 (1967)

    Google Scholar 

  • Trier, J.S., Rubin, E.C.: Electron microscopy of the small intestine. A review. Gastroenterology 49, 574–603 (1965)

    Google Scholar 

  • Venable, J.H., Coggeshall, R.: A simplified lead citrate stain for use in electron microscopy. J. Cell Biol. 25, 407–408 (1965)

    Google Scholar 

  • Wachsmuth, E.D., Torhorst, A.: Possible precursors of aminopeptidase and alkaline phosphatase in the proximal tubules of kidney and the crypts of small intestine of mice. Histochemistry 38, 43–56 (1974)

    Google Scholar 

  • Webster, H.L., Harrison, D.D.: Enzymic activities during the transformation of crypt to columnar intestinal cells. Exp. Cell Res. 56, 245–253 (1969)

    Google Scholar 

  • Weibel, E.R.: Stereological principles for morphometry in electron microscopic cytology. Int. Rev. Cytol. 26, 235–302 (1969)

    Google Scholar 

  • Williams, R.B., Toal, J.N., White, J., Carpenter, H.M.: Effect of total-body X radiation from nearthreshold to tissue lethal doses on small-bowel epithelium of the rat. I. Changes in morphology and rate of cell division in relation to time and dose. J. nat. Cancer Inst. 21, 17–61 (1958)

    Google Scholar 

  • Zetterquist, H.: The ultrastructural organization of the columnar absorbing cells of the mouse jejunum. Stockholm: Aktiebolaget Godvil 1956

    Google Scholar 

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van Dongen, J.M., Visser, W.J., Daems, W.T. et al. The relation between cell proliferation, differentiation and ultrastructural development in rat intestinal epithelium. Cell Tissue Res. 174, 183–199 (1976). https://doi.org/10.1007/BF00222158

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