Summary
Secretory granules have been observed to swell during the process of exocytosis. Swelling is an indication of osmotic stress. The probable role of osmotic pressure in facilitating membrane fusion makes it necessary to determine whether granule membrane ‘swelling’ can occur prior to its fusion with the plasma membrane (pore formation) in the process of exocytosis. By subjecting adjacent thin and semi-thin sections of an activated granule to ultrastructural examination for membrane enlargement, and to metachromatic staining for verification of pore formation it is concluded that the perigranular membrane can indeed enlarge prior to pore formation. However, the degree of membrane enlargement can far exceed the limit of 2–3% stretching allowed under normal osmotic stress for a membrane bilayer. Such an extensive membrane enlargement, which takes place in the mechanism of exocytosis, cannot be achieved without being accompanied by the insertion of additional membrane.
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ANDERSON, P., SLORACH, S. A. & UVNAS, B. (1973) Sequential exocytosis of storage granules during antigen-induced histamine release from sensitized rat mast cellsin vitro An electron microscopic study.Acta Physiol. Scand. 88, 359–72.
ANDERSON, P., ROHLICH, P., SLORACH, S. A. & UVNAS, B. (1974) Morphology and storage properties of rat mast cell granules isolated by different methods.Acta Physiol. Scand. 91, 145–53.
BERGERON, J. A. & SINGER, M. (1958) Metachromasy: an experimental and theoretical reevaluation.J. Biophys. Biochem. Cytol. 4, 433–57.
BILINSKI, M., PLATTNER, H. & MATT, H. (1981) Secretory protein decondensation as a distinct, Ca2+-mediated event during the final steps of exocytosis inParamecium cells.J. Cell Biol. 88, 179–88.
BLASCHKO, H., FIREMARK, H., SMITH, A. D. & WINKLER, H. (1967) Lipids of the adrenal medulla: lysolecithin, a characteristic constituent of chromaffin granules.Biochem. J. 104, 545–9.
BLOOM, G. D. & HAEGERMARK, O. (1965) A study on morphological changes and histamine release induced by compound 48/80 in rat peritoneal mast cells.Expl. Cell Res. 40, 637–54.
BLOOM, G. D. & HAEGERMARK, O. (1967) Studies on morphological changes and histamine release induced by bee venom,n-decylamine and hypotonic solution in rat peritoneal mast cells.Acta Physiol. Scand. 71, 257–69.
BLOOM, G. D. & CHAKRAVARTY, N. (1970) Time course of anaphylactic histamine release and morphological changes in rat peritoneal mast cells.Acta Physiol. Scand. 78, 410–19.
CAULFIELD, J. P., LEWIS, R. A., HEIN, A. & AUSTEN, K. F. (1980) Secretion in dissociated human pulmonary mast cells.J. Cell Biol. 85, 299–311.
CHI, E. Y., LAGUNOFF, D. & KOEHLER, J. K. (1976) Freeze-fracture study of mast cell secretion.Proc. Natl. Acad. Sci. USA 73, 2823–7.
CHOCK, S. P. & CHOCK, E. S. (1985) A two-stage fusion model for secretion.Fed. Proc. 44 (4), 1324.
CHOCK, S. P. & SCHMAUDER-CHOCK, E. A. (1985) Evidence ofde novo membrane generation in the mechanism of mast cell secretory granule activation.Biochem. Biophys. Res. Commun. 132, 134–9.
CHOCK, S. P. & SCHMAUDER-CHOCK, E. A. (1987) The mast cell granules: a phospholipid source for prostaglandin synthesis. InProstaglandin and Lipid Metabolism in Radiation Injury. (edited by WALDEN, T. L. and HUGHES, H. N.). New York: Plenum (in press).
COHEN, F. S., AKABAS, M. H. & FINKELSTEIN, A. (1982) Osmotic swelling of phospholipid vesicles causes them to fuse with a planar phospholipid bilayer membrane.Science 217, 458–60.
CONTE, F. P., MELVILLE, G. S. & UPTON, A. C. (1956) Effects of graded whole-body X-irradiation on mast cells in the rat mesentery.Amer. J. Physiol. 187, 160–2.
CURRAN, M. & BRODWICK, M. S. (1985) Mast cell exocytosis and the gel-swell of granules.Biophys. J. 47, 172a.
EISEN, V. D. & WILSON, C. W. M. (1957) The effects of beta-irradiation on skin histamine and vascular responses in the rat.J. Physiol. 136, 122–130.
FINKELSTEIN, A., ZIMMERBERG, J. & COHEN, F. S. (1986) Osmotic swelling of vesicles: its role in the fusion of vesicles with planar phospholipid bilayer membranes and its possible role in exocytosis.Ann. Rev. Physiol. 48, 163–74.
HELLE, K. B. (1968) The chromogranin of the adrenal medulla: a high-density lipoprotein.Biochem. J. 109, 43–4.
HENRIQUEZ, A. S., BLOCH, K. J., KENYON, K. R., BAIRD, R. S., HANNINEN, L. A. & ALLANSMITH, M. R. (1983) Ultrastructure of mast cells in rat ocular tissue undergoing anaphylaxis.Arch. Ophthalmol. 101, 1439–46.
HOLSTEIN, T. & TARDENT, P. (1984) An ultra-high speed analysis of exocytosis: nematocyst discharge.Science 223, 830–33.
HOLZ, R. W. (1986) The role of osmotic forces in exocytosis from adrenal chromaffin cells.Annu. Rev. Physiol. 48, 175–89.
KAGAYAMA, M. & DOUGLAS, W. W. (1974) Electron microscopic evidence of calcium induced exocytosis in mast cells treated with 48/80 or the ionophores A23187 and X-537A.J. Cell Biol. 62, 519–26.
KWOK, R. & EVANS, E. (1981) Thermoelasticity of large lecithin bilayer membrane vesicles.Biophys. J. 35, 637–52.
LAGUNOFF, D., PHILLIPS, M. T., ISERI, O. H. & BENDITT, E. P. (1964) Isolation and preliminary characterization of rat mast cell granules.Lab. Invest. 13, 1331–44.
LAWSON, D., RAFF, M. C., GOMPERTS, B., FEWTRELL, C. & GILULA, N. B. (1977) Molecular events during membrane fusion: a study of exocytosis in rat peritoneal mast cells.J. Cell Biol. 72, 242–59.
MARCUS, A. J., ULLMAN, H. L. & SAFIER, L. B. (1969) Lipid composition of subcellular particles of human blood platelets.J. Lipid Res. 10, 108–14.
PADAWER, J. (1970) The reaction of rat mast cells to polylysine.J. Cell Biol. 47, 352–72.
ROHLICH, P., ANDERSON, P. & UVNAS, B. (1971) Electron microscope observations on compound 48/80-induced degranulation in rat mast cells.J. Cell Biol. 51, 465–83.
SCHMAUDER-CHOCK, E. A. & CHOCK, S. P. (1985)De novo membrane generation: implication of hydration forces in the mechanism of histamine release. InArmed Forces Radiobiology Research Institute Annual Research Report, 1985, pp. 21–3. Bethesda: AFRRI.
SIMSON, J. A. V., HALL, B. J. & SPICER, S. S. (1973) Histochemical evidence for lipoidal material in secretory granules of rat salivary glands.Histochem. J. 5, 239–54.
THON, I. L. & UVNAS, B. (1967) Degranulation and histamine release: two consecutive steps in the response of rat mast cells to compound 48/80.Acta Physiol. Scand. 71, 303–15.
UVNAS, B. (1982) Mast cell granules, inThe Secretory Granules (edited by POISNER, A. M. and TRIFARO, J. M.) pp. 357–84. Amsterdam: Elsevier Biomedical.
ZIMMERBERG, J. & WHITAKER, M. (1985) Irreversible swelling of secretory granules during exocytosis caused by calcium.Nature 315, 581–4.
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Schmauder-Chock, E.A., Chock, S.P. Mechanism of secretory granule exocytosis: Can granule enlargement precede pore formation?. Histochem J 19, 413–418 (1987). https://doi.org/10.1007/BF01675751
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DOI: https://doi.org/10.1007/BF01675751