Skip to main content
SpringerLink
Log in

Transport of radiolabelled glycoprotein to cell surface and lysosome-like bodies of absorptive cells in cultured small-intestinal tissue from normal subjects and patients with a lysosomal storage disease

  • Published:
Virchows Archiv B

Summary

The transport of3H-fucose-and3H-glucosamine-labelled glycoproteins in the absorptive cells of cultured human small-intestinal tissue was investigated with light-and electron-microscopical autoradiography. The findings showed that these glycoproteins were completed in the Golgi apparatus and transported in small vesicular structures to the apical cytoplasm of these cells. Since this material arrived in the cell coat on the microvilli and in the lysosome-like bodies simultaneously, a crinophagic function of these organelles in the regulation of the transport or secretion of cell-coat material was supported. In the absorptive cells of patients with fucosidosis or Hunter’s type of lysosomal storage disease, a similar transport of cell-coat material to the lysosome-like bodies and a congenital defect of a lysosomal hydrolase normally involved in the degradation of cell-coat material, can explain the accumulation of this material in the dense bodies.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bachmann, L., Salpeter, M.M.: Autoradiography with the electron microscope. Lab. Invest.14, 1041–1053 (1965)

    PubMed  CAS  Google Scholar 

  • Bekesi, J.G., Winzler, R.J.: The metabolism of plasma glycoproteins. Studies on the incorporation of L-fucose-l-14C into tissue and serum in the normal rat. J. Biol. Chem.242, 3873–3879 (1967)

    PubMed  CAS  Google Scholar 

  • Bennett, G.: A comparison of radioautographic reactions in rat tissues at various times after injection of3H-glucose,3H-galactose, and3H-mannose, Anat. Rec.157, 212 (1967)

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bennett, G., LeBlond, C.P.: Formation of cell coat material for the whole surface of columnar cells in the rat small intestine as visualized by radiography with L-fucose3H. J. Cell Biol.46, 409–416(1970)

    Article  PubMed  CAS  Google Scholar 

  • Bennett, G., LeBlond, C.P.: Passage of fucose-3H label from the Golgi apparatus into dense and multivesicular bodies in the duodenal columnar cells and hepatocytes of the rat. J. Cell Biol.51, 875–881 (1971)

    Article  PubMed  CAS  Google Scholar 

  • Bennett, G., LeBlond, C.P., Haddad, A.: Migration of glycoprotein from the Golgi apparatus to the surface of various cell types as shown by radioautography after labeled fucose injections into rats. J. Cell Biol.60, 258–284 (1974)

    Article  PubMed  CAS  Google Scholar 

  • Browning, T.M., Trier, J.S.: Organ culture of mucosal biopsies of human small intestine. J. Clin. Invest.48, 1423–1432 (1969)

    Article  PubMed  CAS  Google Scholar 

  • Coffey, J.W., Miller, O.N., Sellinger, O.Z.: The metabolism of L-fucose in the rat. J. Biol. Chem.239, 011 (1964)

    Google Scholar 

  • Daems, W.Th., Gemund, J.J. van Vio, P.M.A., Willighagen, R.G.J., Den Tandt, W.R.: The use of intestinal suction biopsy material for the study of lysosomal storage diseases. In: Lysosomal storage diseases, Hers, H.G., Hoof, F. van (eds.), pp. 575–598. New York: Academic Press 1973

    Google Scholar 

  • Farquhar, M.G.: Lysosome function in regulation secretion: disposal of secretory granules in cells of the anterior pituitary gland. In: Lysosomes in biology and pathology, Dingle, J.T., Fell, H.B. (eds.), vol. II, p. 462. Amsterdam: North-Holland Publ. Comp. 1969

    Google Scholar 

  • Forstner, G.G.: l-14C-glucosamine incorporation by subcellular fractions of small intestinal mucosa. J. Biol. Chem.245, 3584–3592 (1970)

    PubMed  CAS  Google Scholar 

  • Ginsel, L.A., Daems, W.Th., Emeis, J.J., Vio, P.M.A., Gemund, J.J. van: Fine structure and silver-staining 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. Zellpath.13, 119–144(1973)

    CAS  Google Scholar 

  • Ginsel, L.A., Debets, W.F., Daems, W.Th.: The effect of colchicine on the distribution of apical vesicles and tubules in absorptive cells of cultured human intestine. In: Microtubules and microtubule inhibitors, Borgers, M., Brabander, M. de (eds.), pp. 187–198. Amsterdam: North-Holland Publ. Comp. 1975

    Google Scholar 

  • Ginsel, L.A., Onderwater, J.J.M., Daems, W.Th.: The transport of3H-fucose labelled glycoprotein in the absorptive cells of cultured human small intestine. In: Electron microscopy 1976. Proc. 6th Europ. Congress Jerusalem, September 14–20, 1976. Vol. II, Biological sciences, Y. Ben-Shaul (ed.), pp. 292–294. Jerusalem: Tal Intern. Publ. Comp. 1976a

    Google Scholar 

  • Ginsel, L.A., Onderwater, J.J.M., Daems, W.Th.: The transport of radiolabelled glycoprotein in absorptive cells of cultured small-intestinal tissue from normal children and children with a lysosomal storage disease. Ultramicroscopy2, 126 (1976b)

    Google Scholar 

  • Ginsel, L.A., Want, J.J.L. van der, Daems, W.Th.: Qualitative and quantitative preservation of the fine structure of absorptive cells in cultured biopsies of human small-intestine. Cell Tiss. Res.181, 143–162 (1977)

    Article  CAS  Google Scholar 

  • Ginsel, L.A., Cambier, P.H., Daems, W.Th.: Fucosidosis and I-cell disease: a fine-structural and silver-staining study of abnormal inclusion bodies in small-intestinal cells. Virchows Arch. B Cell Path.27, 99–117 (1978)

    CAS  Google Scholar 

  • Ginsel, L.A., Onderwater, J. J.M., Daems, W.Th.: The effect of colchicine on the intracellular transport of 3H-fucose labelled glycoproteins in absorptive cells of cultured human small intestine (1979a). (To be published)

  • Ginsel, L.A., Onderwater, J.J.M., Daems, W.Th.: The resolution of a gold latensification-elon ascorbic acid developer for Ilford L4 emulsion (1979b). (To be published)

  • Ginsel, L.A., Jutte, C., Daems, W.Th.: A preliminary study on endocytosis in the absorptive cells of cultured human small intestine. (1979 c). (To be published)

  • Goldstein, A., Koenig, H.: Biosynthesis of lysosomal glycoproteins in rat kidney. Life Sci.11, 511–523 (1972)

    Article  Google Scholar 

  • Hauri, H.P., Kedinger, M., Haffen, K., Freiburghaus, A., Grenier, J.F., Hadorn, B.: Biosynthesis of brushborder glycoproteins by human small intestinal mucosa in organ culture. Biochim. Biophys. Acta467, 327–339 (1977)

    Article  PubMed  CAS  Google Scholar 

  • Hsu, L.H., Tappel, A.L.: Lysosomal enzymes of rat intestinal mucosa. J. Cell Biol.23, 233–240 (1964)

    Article  PubMed  CAS  Google Scholar 

  • Hsu, L.H., Tappel, A.L.: Lysosomal enzymes and mucopolysaccharides in the gastro-intestinal tract of the rat and pig. Biochim. Biophys. Acta (Amst.)101, 83–89 (1965)

    CAS  Google Scholar 

  • Hugon, J., Borgers, M.: Fine structural localization of acid and alkaline phosphatase activities in the absorbing cells of the duodenum of rodents. Histochemie12, 42–53 (1968)

    Article  PubMed  CAS  Google Scholar 

  • Isselbacher, K.J.: The intestinal cell surface: some properties of normal undifferentiated, and malignant cells. Ann. Int. Med.81, 681–686 (1974)

    PubMed  CAS  Google Scholar 

  • Ito, S.: Radioactive labelling of the surface coat on enteric microvilli. Anat. Rec.151, 489 (abstr.) (1965)

    Google Scholar 

  • Ito, S.: Structure and function of the glycocalyx. Fed. Proc.28, 12–25 (1969)

    PubMed  CAS  Google Scholar 

  • Ito, S.: Form and function of the glycocalyx on the free cell surfaces. Phil. Trans. R. Soc. Lond. B.268, 55–66 (1974)

    Article  Google Scholar 

  • James, W.P.T., Alpers, D.H., Gerber, J.E.: The turnover of disaccharidases and brushborder proteins in rat intestine. Biochim. Biophys. Acta230, 194–203 (1971)

    PubMed  CAS  Google Scholar 

  • Jersild, R.A., Crawford, R.W.: The distribution and mobility of anionic sites on the brushborder of intestinal absorptive cells. Am. J. Anat.152, 287–306 (1978)

    Article  PubMed  Google Scholar 

  • Kim, Y.S., Perdomo, J., Nordberg, J.: Glycoprotein biosynthesis in small intestinal mucosa. I. A study of glycosyltransferases in microsomal subfractions. J. Biol. Chem.246, 5466–5476 (1971)

    PubMed  CAS  Google Scholar 

  • Kim, Y.S., Perdomo, J.M.: Membrane glycoproteins of the small intestine. Chemical composition of membrane glycoproteins. Biochim. Biophys. Acta339, 111–125 (1974)

    Google Scholar 

  • Louisot, P., Frot-Coutaz, J., Bertagnolie, G., Got, R., Colobert, L.: The incorporation of 1-14C-Dglucosamine into subcellular fractions of rat intestinal mucosa. Biochem. Biophys. Res. Commun.28, 385–389 (1967)

    Article  PubMed  CAS  Google Scholar 

  • MacDermott, R.P., Donaldson, R.M., Trier, J.S.: Glycoprotein synthesis and secretion by mucosal biopsies of rabbit colon and human rectum. J. Clin. Invest.54, 545–554 (1974)

    Article  PubMed  CAS  Google Scholar 

  • Michaels, E., LeBlond, C.P.: Transport of glycoprotein from Golgi apparatus to cell surface by means of “carrier” vesicles, as shown by radioautography of mouse colonic epithelium after injection of3H-fucose. J. Microsc. Biol. Cell.25, 243–248 (1976)

    Google Scholar 

  • Neutra, M., LeBlond, C.P.: Radioautographic comparison of the uptake of galactose-3H and glucose-H3 in the Golgi region of various cells secreting glycoprotein or mucopolysaccharides. J. Cell Biol.30, 137 (1966)

    Article  PubMed  CAS  Google Scholar 

  • Rambourg, A., Bennett, G., Kopriwa, B., LeBlond, C.P.: Détection radioautographique des glycoprotéines de l’epithélium intestinal du rat après injèction de fucose-3H. J. Microsc.11, 163–168 (1971)

    CAS  Google Scholar 

  • Ryser, H.J.P.: Uptake of protein by mammalian cells: An underdeveloped area. Sci.159, 390–396 (1968)

    Article  CAS  Google Scholar 

  • Spiro, R.: Glycoproteins: Their biochemistry, biology and role in human disease. Biochem. Biophys. Res. Comm.46, 1270–1277 (1972)

    Article  Google Scholar 

  • Vrensen, G.F.J.M.: Some new aspects of efficiency of electron microscopic autoradiography with tritium. J. Histochem. Cytochem.18, 278–290 (1970)

    PubMed  CAS  Google Scholar 

  • Weiser, M.M.: Intestinal epithelial cell surface membrane glycoprotein synthesis. I. An indicator of cellular differentiation. J. Biol. Chem.248, 2536–2541 (1973)

    PubMed  CAS  Google Scholar 

  • Williams, M.A.: The assessment of electron microscopic autoradiographs. In: Advances in optical and electron microscopy, Barer, R. and Coslett, V.E. (eds.), pp. 219–272. London: Academic Press 1969

    Google Scholar 

  • Williams, M.A.: Electron microscopic autoradiography: Its application to protein biosynthesis. In: Techniques in protein biosynthesis, Campbell, P.N., Sargent, J.R. (eds), pp. 125–191. London: Academic Press 1973

    Google Scholar 

  • Wisse, E., Tates, A.D.: A gold latensification-elon ascorbic acid developer for Ilford L4 emulsion. In: Electronmicroscopy, 4th European Region. Conf. on electron microscopy, Rome, Italy (Bocciarelli, D.S., ed.) Vol. II, pp. 465–466, 1968

  • Wollman, S.H.: Secretion of thyroid hormons. In: Lysosomes in biology and pathology, Dingle, J.T., Fell, H.D. (eds.), Vol. II, p. 483, Amsterdam: North-Holland Publ. Comp. 1969

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory for Electron Microscopy, University of Leiden, Rijnsburgerweg 10, Leiden, The Netherlands

    L. A. Ginsel, J. J. M. Onderwater & W. Th. Daems

Authors
  1. L. A. Ginsel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. J. M. Onderwater
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. W. Th. Daems
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ginsel, L.A., Onderwater, J.J.M. & Daems, W.T. Transport of radiolabelled glycoprotein to cell surface and lysosome-like bodies of absorptive cells in cultured small-intestinal tissue from normal subjects and patients with a lysosomal storage disease. Virchows Arch. B Cell Path. 30, 245–273 (1979). https://doi.org/10.1007/BF02889106

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02889106

Key words

Search

Navigation