Skip to main content
SpringerLink
Log in

Function of coated membranes and multivesicular bodies during membrane regulation in stimulated exocrine pancreas cells

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Stimulation of secretion by pilocarpine results in a 70% loss of zymogen granules from pancreatic acinar cell during the first hr after injection of the drug. In previous work (Geuze and Poort, 1973), we found that the amount of membrane stored in the surface of the microvilli and of the numerous infoldings present in highly stimulated cells, increases during the first 2 hr and then decreases again during the 3rd hr after stimulation, concurrently with maximal endocytosis of sorbitol-[su14C].

Further observations on the fine structure of stimulated cells at various time intervals after injection of pilocarpine showed that during the first hr numerous smooth vesicles and multivesicular bodies (mvb's) appear in the apical cytoplasm, while the number of coated vesicles and their relative total volume increase significantly 3 hr after stimulation.

By infusion of ferritin in the pancreatic duct system in vivo and application of cytochemical techniques (osmium impregnation, electron microscope autoradiography and acid phosphatase cytochemistry) it could be established that after stimulated exocytotic secretion, redundant apical cell membrane is withdrawn by at least two routes: 1) During the initial rapid increase of the amount of apical cell membrane, withdrawal is accomplished by interiorization of luminal invaginations into smooth endocytotic vesicles, which in turn give rise to mvb's by infolding and subsequent fission of their limiting membrane. 2) Once the bulk of stored secretion granules has been discharged, endocytotic coated vesicles become gradually more prominent as carriers for redundant cell membrane. The contents of endocytotic structures ultimately become incorporated in residual bodies, suggesting lysosomal degradation of cell membrane prior to eventual reutilization.

Coated vesicles also originate by pinching off from mature Golgi cisternae and condensing vacuoles. A possible function of the coated membranes in the concentration of exportable protein within forming secretory granules is discussed.

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

  • Abrahams, S. J., Joltzman, E.: Secretion and endocytosis in insulin-stimulated rat adrenal medulla cells. J. Cell Biol. 56, 540–558 (1973)

    Google Scholar 

  • Amsterdam, A., Ohad, I., Schramm, M.: Dynamic changes in the ultrastructure of the acinar cell of the rat parotid gland during the secretory cycle. J. Cell Biol. 41, 753–773 (1969)

    Google Scholar 

  • Arstila, A. U., Jauregui, H. O., Chang, J., Trump, B. F.: Studies on cellular autophagocytosis. Lab. Invest. 24, 162–177 (1971)

    Google Scholar 

  • Cardell, R. R., Jr., Badenhausen, S., Porter, K. R.: Intestinal triglyceride absorption in the rat. J. Cell Biol. 34, 123–155 (1967)

    Google Scholar 

  • Douglas, W. W., Nagasawa, J.: Membrane vesiculation at sites of exocytosis in the neurohypophysis, adenohypophysis and adrenal medulla: a device for membrane conservation. J. Physiol. (Lond.) 218, 948 (1971)

    Google Scholar 

  • Farquhar, M. G., Bainton, D. F., Baggiolini, M., de Duve, C.: Cytochemical localization of acid phosphatase activity in granule fractions from rabbit polymorphonuclear leukocytes. J. Cell Biol. 54, 141–156 (1972)

    Google Scholar 

  • Farquhar, M. G., Palade, G. E.: Functional evidence for the existence of a third cell type in the renal glomerulus. J. Cell Biol. 13, 55–87 (1962)

    Google Scholar 

  • Friend, D. S.: Cytochemical staining of multivesicular body and Golgi vesicles. J. Cell Biol. 41, 269–279 (1969)

    Google Scholar 

  • Friend, D. S., Farquhar, M. G.: Functions of coated vesicles during protein absorption in the rat vas deferens. J. Cell Biol. 35, 357–376 (1967)

    Google Scholar 

  • Geuze, J. J., Poort, C.: Cell membrane resorption in the rat exocrine pancreas cell after in vivo stimulation of the secretion, as studied by in vitro incubation with extracellular space markers. J. Cell Biol. 57, 159–174 (1973)

    Google Scholar 

  • Gomori, G.: In: Microscopic Histochemistry, Principles and Practice. University of Chicago Press, p. 189 (1952)

  • Grynszpan-Winograd, O.: Morphological aspects of exocytosis in the adrenal medulla. Phil. Trans. Soc. Roy. Lond. Ser. B, Biol. Sci. 261, 291–292 (1971)

    Google Scholar 

  • Hand, A. R..: The fine structure of von Ebner's gland of the rat. J. Cell Biol. 44, 340–353 (1970)

    Google Scholar 

  • Hand, A. R..: Morphology and cytochemistry of the Golgi apparatus of rat salivary gland acinar cells. Am. J. Anat. 130, 141–157 (1971)

    Google Scholar 

  • Hermodson, L. H.: Changes in the ultrastructure of the exocrine pancreas of the cat after stimulation of secretin and pancreozymin. In: Electron Microscopy, New York, Academic Press, Inc., yy-11 (1962)

    Google Scholar 

  • Heuser, J., Reese, T. S..: Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57, 315–344 (1973)

    Google Scholar 

  • Hirsch, J. G., Fedorko, M. E., Cohn, Z. A.: Vesicle fusion and formation at the surface of pinocytotic vacuoles in macrophages. J. Cell Biol. 38, 629–632 (1968)

    Google Scholar 

  • Holtzman, E.: Stimulation-dependent alterations in peroxidase uptake at lobster neuromuscular junctions. Science 173, 733–736 (1971)

    Google Scholar 

  • Ichikawa, A.: Fine structural changes in response to hormonal stimulation of the perfused canine pancreas. J. Cell Biol. 24, 369–385 (1965)

    Google Scholar 

  • Jamieson, J. D., Palade, G. E.: Intracellular transport of secretory proteins in the pancreatic exocrine cell, I. J. Cell Biol. 34, 577–596 (1967)

    Google Scholar 

  • Jamieson, J. D., Palade, G. E.: Condensing vacuole conversion and zymogen granule discharge in pancreatic exocrine cells: metabolic studies. J. Cell Biol. 48, 503–522 (1971)

    Google Scholar 

  • Jamieson, J. D., Palade, G. E..: Synthesis, intracellular transport, and discharge of secretory proteins in stimulated pancreatic exocrine cells. J. Cell Biol. 50, 135–158 (1971)

    Google Scholar 

  • Kanaseki, T., Radota, K.: The “vesicle in the basket”. J. Cell Biol. 42, 202–220 (1969)

    Google Scholar 

  • Kilarski, W., Jasinski, A.: The formation of multivesicular bodies from the nuclear envelope. J. Cell Biol. 45, 205–211 (1970)

    Google Scholar 

  • Kopriwa, B. M.: A semiautomatic instrument for the radioautographic coating technique. J. Histochem. Cytochem. 14, 923 (1966)

    Google Scholar 

  • Kramer, M. F., Geuze, J. J.: Redundant cell membrane regulation in the exocrine pancreas cells after pilocarpine stimulation of the secretion in vivo. In: Advances in Cytopharmacology, vol. 2, p. 87–97. New York: Raven Press (1974)

    Google Scholar 

  • Lettré, H., Paweletz, N.: Probleme der elektronenmikroskopischen Autoradiographie. Naturwissenschaften 53, 268 (1966)

    Google Scholar 

  • Locke, M., Collins, J. V.: Protein uptake in multivesicular bodies in the molt-intermolt cycle of an insect. Science 155, 467–469 (1967)

    Google Scholar 

  • Locke, M., Collins, J. V.: Protein uptake into multivesicular bodies and storage granules in the fat body of an insect. J. Cell Biol. 36, 453–483 (1968)

    Google Scholar 

  • Masur, S. K., Holtzman, E., Schwartz, I. L., Walter, R.: Correlation between pinocytosis and hydroosmosis induced by neurohypophyseal hormones and mediated by adenosine 3′, 5′-cyclic monophosphate. J. Cell Biol. 49, 582–594 (1971)

    Google Scholar 

  • Masur, S. K., Holtzman, E., Walter, R.: Hormone-stimulated exocytosis in the toad urinary bladder. J. Cell Biol. 52, 211–219 (1972)

    Google Scholar 

  • Mata, L. R., Ferreira, J.F.D.: Transport of exogenous peroxidase to Golgi cisternae in the hamster seminal vesicle. J. Microscopie 17, 103–106 (1973)

    Google Scholar 

  • Matter, A., Orci, L., Forssmann, W. G., Rouiller, Ch.: The stereological analysis of the fine structure of the “micropinocytosis vermiformis” in Kupffer cells of the rat. J. Ultrastruct. Res. 23, 272–279 (1968)

    Google Scholar 

  • Maul, G. C., Brumbaugh, J. A.: On the possible function of coated vesicles in melanogenesis of the regenerating fowl feather. J. Cell Biol. 48, 41–48 (1971)

    Google Scholar 

  • Merker, H. J.: Über das Vorkommen multivesiculärer Einschlußkörper im Vaginalepithel der Ratte. Z. Zellforsch. 68, 618–630 (1965)

    Google Scholar 

  • Nevalainen, T. J.: Effects of pilocarpine stimulation on rat pancreatic acinar cells. Acta path. microbiol. scand. A, Suppl. 210 (1970)

  • Nicander, L.: A study of multivesicular bodies in the epididymis. J. Ultrastruct. Res. 14, 424–425 (1969)

    Google Scholar 

  • Novikoff, A. B.: Lysosomes in the physiology and pathology of cells: contributions of staining methods. Ciba Found. Symp. Lysosomes 36 (1963)

  • Okano, Y., Nakamura, T.: Electron microscopic observations on exocrine pancreas cells in mice following the injection of pilocarpine. J. Electron Micr. (Tokyo) 14, 242–243 (1965)

    Google Scholar 

  • Palade, G. E.: In: Subcellular particles, T. Hayashi, ed., 64. New York: The Ronald Press Company 1959

  • Palade, G. E., Bruns, R. R.: Structural modulations of plasmalemmal vesicles. J. Cell Biol. 37, 633–649 (1968)

    Google Scholar 

  • Rosenbluth, J., Wissig, S. L.: The distribution of exogenous ferritin in toad spinal ganglia and the mechanism of its uptake by neurons. J. Cell Biol. 23, 307–325 (1964)

    Google Scholar 

  • Roth, T. F., Porter, K. R.: Specialized sites on the cell surface for protein uptake. In: Electron microscopy: Fifth International Congress for Electron Microscopy, Philadelphia, 1962, S. S. Breese, Jr. ed., vol. 2, p. 144. New York: Academic Press Inc. 1962

    Google Scholar 

  • Shirama, T., Cohen, A. S.: The association of hemidesmosome-like plaque and dense coating with the pinocytotic uptake of a heterologous fibrillar protein (amyloid) by macrophages. J. Ultrastruct. Res. 33, 587–597 (1970)

    Google Scholar 

  • Simionescu, N., Simionescu, M., Palade, G. E.: Permeability of muscle capillaries to exogenous myoglobin. J. Cell Biol. 57, 424–452 (1973)

    Google Scholar 

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

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Centre for Electron Microscopy, Medical Faculty, State University of Utrecht, Utrecht, The Netherlands

    J. J. Geuze & M. F. Kramer

Authors
  1. J. J. Geuze
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. F. Kramer
    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

Geuze, J.J., Kramer, M.F. Function of coated membranes and multivesicular bodies during membrane regulation in stimulated exocrine pancreas cells. Cell Tissue Res. 156, 1–20 (1974). https://doi.org/10.1007/BF00220098

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00220098

Key words

Search

Navigation