Summary
Exocytosis was studied in acetylcholine-stimulated bovine adrenal medulla. During a pre-exocytotic stage, chromaffin granules are found in juxtaposition to the plasma membrane and separated from it by an electron dense space 25–27 Å in width. Freeze-fracture studies show this stage to be characterized by connections between the granules and the plasma membrane. These connections are apparently cytoplasmic but bridge both membranes; they are presumably proteinaceous, but their exact nature remains to be elucidated. Later stages of exocytosis were also studied by the freeze-fracture technique; a typical feature is the lack of intramembrane particles around the fusion site. Both connections and membrane particle movement are discussed in terms of recent biochemical findings.
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Ash, J.F., Louvard, D., Singer, S.J.: Antibody-induced linkages of plasma membrane proteins to intracellular actomyosin-containing filaments in cultured fibroblasts. Proc. Natl. Acad. Sci. (Wash.) 74, 5584–5588 (1977)
Aunis, D., Serck-Hanssen, G., Helle, K.B.: Dopamine-β-hydroxylase in perfusates of stimulated bovine adrenals. Isolation and characterization of the released enzyme. Gen. Pharmacol. 9, 37–43 (1978)
Branton, D., Bullivant, S., Gilula, N.B., Karnovsky, M.J., Moor, H., Mühlethaler, K., Northcote, D.H., Packer, L., Satir, B., Satir, P., Speth, V., Staehelin, L.A., Steere, R.L., Weinstein, R.S.: Freeze-etching nomenclature. Science 190, 54–56 (1975)
Bray, D.: Membrane movements and microfilaments. Nature 273, 265–266 (1978)
Chi, E.Y., Lagunoff, D., Koehler, J.K.: Freeze-fracture study of mast cell secretion. Proc. Natl. Acad. Sci. (Wash.) 73, 2823–2827 (1976)
Crandall, M.A., Brock, T.D.: Molecular aspects of specific cell contact. Science 161, 473–475 (1968)
Creutz, C.E.: Isolation, characterization and localization of bovine adrenal medullary myosin. Cell Tissue Res. 178, 17–38 (1977)
Creutz, C.E., Pazoles, C.J., Pollard, H.B.: Identification and characterization of an adrenal medullary protein (synexin) that causes calcium-dependent aggregation of isolated chromaffin granules. J. Biol. Chem. 253, 2858–2866 (1978)
Diner, O.: L'expulsion des granules de la médullo-surrénale chez le hamster. C.R. Acad. Sci (Paris) Ser. D 265, 616–619 (1967)
Douglas, W.W.: Involvement of calcium in exocytosis and the exocytosis-vesiculation sequence. Biochem. Soc. Symp. 39, 1–28 (1974)
Eagles, P.A.M., Johnson, L.N., van Horn, C.: The distribution of concanavalin A receptor sites on the membrane of chromaffin granules. J. Cell Sci. 19, 33–54 (1975)
Eagles, P.A.M., Johnson, L.N., van Horn, C., Bullivant, S.: Freeze-fracture of adrenal chromaffin granules. Neurosci. 2, 153–158 (1977)
Flanagan, J., Koch, G.L.E.: Cross-linked surface Ig attaches actin. Nature 273, 278–281 (1978)
Gagnon, C., Viveros, O.H., Diliberto, Jr, E.J., Axelrod, J.: Enzymatic methylation of carboxyl groups of chromaffm granule membrane proteins. J. Biol. Chem. 253, 3778–3781 (1978)
Grynszpan-Winograd, O.: Morphological aspects of exocytosis in the adrenal medulla. Philos. Trans. R. Soc. (Lond.) B 261, 291–292 (1971)
Helle, K.B., Serck-Hanssen, G.: The adrenal medulla: a model for studies of hormonal and neuronal storage and release mechanisms. Mol. Cell Biochem. 6, 127–146 (1975)
Hesketh, J.E., Aunis, D., Pescheloche, M., Mandel, P.: Subcellular distribution of myosin (K +, EDTA)-ATPase activity in bovine adrenal medulla. FEBS Lett. 80, 324–328 (1977)
Hesketh, J.E., Aunis, D., Mandel, P., Devilliers, G.: Biochemical and morphological studies of bovine adrenal medullary myosin. Biol. Cell 33, 199–208 (1978)
Jockush, B.M., Burger, M.M., Da Prada, M., Richards, J.G., Chaponnier, C., Gabbiani, G.: α-actinin attached to membranes of secretory vesicles. Nature 270, 628–629 (1977)
Koch, G.L.E., Smith, M.J.: An association between actin and the major histocompatibility antigen H-2. Nature 273, 274–278 (1978)
Korn, E.D.: Biochemistry of actomyosin-dependent cell motility (a review). Proc. Natl. Acad. Sci. (Wash.) 75, 588–599 (1978)
Lawson, D., Raff, M.C., Gomperts, B., Fewtrell, C., Gilula, N.B.: Molecular events during membrane fusion. A study of exocytosis in rat peritoneal mast cells. J. Cell Biol. 72, 242–259 (1977)
Meyer, D.I., Burger, M.M.: The chromaffin granule surface localization of carbohydrate on the cytoplasmic surface of an intracellular organelle. Biochim. Biophys. Acta 443, 428–436 (1976)
Nagasawa, J.: Exocytosis: the common release mechanism. In: Paraneurons. New concept on neuroendocrine relatives (S. Kobayashi, T. Chiba, eds.), pp. 31–47. Arch. Histol. Jpn., Vol. 40, supp. (1977)
Orci, L., Perrelet, A., Friend, D.S.: Freeze-fracture of membrane fusion during exocytosis in pancreatic B-cells. J. Cell Biol. 75, 23–30 (1977)
Rosen, S.D., Simpson, D.L., Rose, J.E., Barondes, S.H.: Carbohydrate-binding proteins from Polysphondylium pallidum implicated in intercellular adhesion. Nature 252, 148–151 (1974)
Satir, B., Schooley, L., Satir, P.: Membrane fusion in a model system. J. Cell Biol. 56, 173–176 (1973)
Shotton, D.: Freeze-fracture view of membrane fusion. Nature 272, 16–17 (1978)
Smith, U., Smith, D.S., Winkler, H., Ryan, J.W.: Exocytosis in the adrenal medulla demonstrated by freeze-etching. Science 179, 79–82 (1972)
Theodosis, D.T., Dreifuss, J.J., Orci, L.: A freeze-fracture study of membrane events during neurohypophysal secretion. J. Cell Biol. 78, 542–553 (1978)
Toh, B.H., Hard, G.C.: Actin co-caps with concanavalin A receptors. Nature 269, 695–697 (1977)
Trifaro, J.M.: Contractile proteins in tissues originating in the neural crest. Neurosci. 3, 1–24 (1978)
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Aunis, D., Hesketh, J.E. & Devilliers, G. Freeze-fracture study of the chromaffin cell during exocytosis: Evidence for connections between the plasma membrane and secretory granules and for movements of plasma membrane-associated particles. Cell Tissue Res. 197, 433–441 (1979). https://doi.org/10.1007/BF00233568
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DOI: https://doi.org/10.1007/BF00233568