Summary
The hypothesis that the retrieval of membranes of neurohypophysial neurosecretory granules (NSG) and small electron-lucent microvesicles occurs by different routes was tested by incubating neurohypophysial neurosecretosomes with colloidal gold particles of various sizes. Neurosecretosomes derived from normal Long Evans rats and incubated in media of normal ionic composition endocytosed a few small (<25 nm) gold particles into 40–50 nm electron-lucent microvesicles. After depolarisation, more small gold particles were found in microvesicles, and small and large (>25 nm) gold particles in vacuoles. Oxytocin-containing neurosecretosomes derived from Brattleboro rats, which contain 160 nm-diameter NSG, endocytosed gold particles in a pattern indistinguishable from that of neurosecretosomes from Long Evans rats. However, neurosecretosomes derived from defective vasopressin neurones of Brattleboro rats, which contain microvesicles, small vacuoles, and a few 100 nm dense-cored vesicles, but not 160 nm NSG, endocytosed only small colloidal gold particles. Early after depolarisation the gold particles were present only in microvesicles, but later some could be found in vacuoles and lysosome-like structures. Immunogold cytochemistry using a polyclonal antiserum raised against microvesicle-rich neurosecretosomes derived from Brattleboro rats labelled microvesicles in the posterior pituitary strongly, NSG weakly, and vacuoles to a variable extent. These data together indicate that, after exocytosis, the membranes of NSG are recaptured as large vacuoles. Microvesicles are exocytosed and endocytosed separately.
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References
Alonso G, Assenmacher I (1979) The smooth endoplasmic reticulum in neurohypophysial axons of the rat: possible involvement in transport, storage and release of neurosecretory material. Cell Tissue Res 199:414–429
Barnes PRJ, Dyball REJ (1990) Rapid refilling of neurosecretory terminals with secretory granules after an acute stimulus to the isolated neural lobe of the rat. Cell Tissue Res 260:211–213
Beesley JE (1989) Colloidal gold: a new perspective for cytochemical marking. Royal microscopical society handbook 17. Oxford University Press, Oxford
Ben Barak Y, Russell JT, Whitnall MH, Ozato K, Gainer H (1985) Neurophysin in the hypothalamoneurohypophysial system. I. Production and characterization of monoclonal antibodies. J Neurosci 5:81–97
Brimble MJ, Dyball REJ, Forsling ML (1978) Oxytocin release following osmotic activation of oxytocin neurones in the paraventricular and supraoptic nuclei. J Physiol 278:69–78
Broadwell RD, Cataldo AM, Balin BJ (1984) Further studies of the secretory process in hypothalamo-neurohypophysial neurons: an analysis using immunocytochemistry, wheat germ agglutinin-peroxidase, and native peroxidase. J Comp Neurol 228:155–167
Browning MD, Huang C-K, Greengard P (1987) Similarities between protein IIIa and protein IIIb, two prominent synaptic vesicle-associated phosphoproteins. J Neurosci 7:847–853
Buma J, Nieuwenhuys R (1987) Ultrastructural demonstration of oxytocin and vasopressin release sites in the neural lobe and median eminence of the rat by tannic acid and immunogold methods. Neurosci Lett 74:151–157
Castel M (1974) In vivo uptake of tracers by neurosecretory axon terminals in normal and dehydrated mice. Gen Comp Endocrinol 22:336–337
Castel M, Dellmann HD (1981) Cytochemistry of neurosecretory cells reveals different compartments for axonal transport. In: Farner DS, Lederis K (eds) Neurosecretion: molecules, cells, systems. Plenum, New York, pp 468–470
Castel M, Morris JF (1988) The neurophysin-containing innervation of the forebrain of the mouse. Neuroscience 24:937–966
Cazalis M, Dayanithi G, Nordmann JJ (1987a) Requirements for hormone release from permeabilized nerve endings isolated from the rat neurohypophysis. J Physiol 390:71–91
Cazalis M, Dayanithi G, Nordmann JJ (1987b) Hormone release from isolated nerve endings of the rat neurohypophysis. J Physiol 390:55–70
Dellman H-D, Sikora KC, Castel M (1981) Fine structure of the rat supraoptic nucleus and neural lobe during pre-and postnatal development. In: Farner DS, Lederis K (eds) Neurosecretion: molecules, cells, systems. Plenum, New York, pp 177–186
Diederen KHB, Dorland M, Jansen WF, Vullings HGB (1985) Endocytosis in adipokinetic hormone (AKH)-producing cells of the migratory locust Locusta migratoria. Cell Biol Int Rep 9:525
Douglas WW, Nagasawa J, Schulz RA (1971) Coated microvesicles in neurosecretory terminals of posterior pituitary glands shed their coats to become smooth “synaptic” vesicles. Nature 232:340–341
Harlow E, Lane D (1988) Antibodies a laboratory manual, 1st edn. Cold Spring Harbour Laboratory, Cold Spring Harbor, NY, p 651
Heuser JE, Reese TS (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 57:315–344
Lescure H, Nordmann JJ (1980) Neurosecretory granule release and endocytosis during prolonged stimulation of the rat neurohypophysis in vitro. Neuroscience 5:651–659
Lowe AW, Madeddu L, Kelly RB (1988) Endocrine secretory granules and neuronal synaptic vesicles have three integral membrane proteins in common. J Cell Biol 106:51–59
Martin R (1968) Fine structure of the neurosecretory system of the vena cava in octopus. Brain Res 8:201–205
Mason WT, Hatton GI, Ho YW, Chapman C, Robinson ICAF (1986) Central release of oxytocin, vasopressin and neurophysin by magnocellular neurone depolarisation: evidence in slices of guinea pig and rat hypothalamus. Neuroendocrinology 42:311–322
Morris JF (1976) Distribution of neurosecretory granules among the anatomical compartments of the neurosecretory processes of the pituitary gland: a quantitative ultrastructural approach to hormone storage in the neural lobe. J Endocrinol 68:225–234
Morris JF, Nordmann JJ (1976) Membrane retrieval at neurosecretory axon endings. Nature 261:723–725
Morris JF, Nordmann JJ (1980) Membrane recapture after hormone release from nerve endings in the neural lobe of the rat pituitary gland. Neuroscience 5:639–649
Morris JF, Nordmann JJ (1982) Membrane retrieval by vacuoles after exocytosis in the neural lobe of Brattleboro rats. Neuroscience 7:1631–1639
Morris JF, Pow DV (1988) Capturing and quantifying the exocytotic event. J Exp Biol 139:81–103
Morris JF, Nordmann JJ, Shaw FD (1982) Granules, microvesicles, and vacuoles. Their roles in the functional compartments of the neural lobe. In: Farner DS, Lederis K (eds) Neurosecretion: molecules, cells, systems. Plenum, New York, pp 187–196
Morris JF, Pow DV, Shaw FD (1988) Release of neuropeptides from magnocellular neurones: does anatomical compartmentation have a functional significance? In: Pickering BT, Wakerley JB, Summerlee AJS (eds) Neurosecretion. Cellular aspects of the production and release of neuropeptides. Plenum, London, pp 113–122
Morris JF, Pow DV, Shaw FD (1989) Strategies for the ultrastructural study of peptide-containing neurons. In: Fink G, Harmar AJ (eds) Neuropeptides: a methodology. Wiley, Chichester, pp 83–124
Nagasawa J, Douglas WW, Schultz RA (1971) Micropinocytotic origin of coated and smooth microvesicles (“synaptic vesicles”) in neurosecretory terminals of posterior pituitary glands demonstrated by incorporation of horseradish peroxidase. Nature 232:341–342
Navone F, Jahn R, Di Gioia G, Stukenbrok H, Greengard P, De Camilli P (1986) Protein p38: an integral membrane protein specific for small vesicles of neurons and neuroendocrine cells. J Cell Biol 103:2511–2527
Navone F, Di Gioia G, Jahn R, Browning M, Greengard P, De Camilli P (1989) Microvesicles of the neurohypophysis are biochemically related to small synaptic vesicles of presynaptic nerve terminals. J Cell Biol 109:3425–3433
Nordmann JJ (1983) Stimulus-secretion coupling. In: Cross BA, Leng G (eds) The neurohypophysis: structure, function and control. Prog Brain Res 60:281–304
Nordmann JJ, Chevallier J (1980) On the role of microvesicles in buffering Ca2+ in the neurohypophysis. Nature 287:54–56
Nordmann JJ, Dayanithi G (1988) Release of neuropeptides does not only occur at nerve terminals. Biosci Rep 8:471–483
Nordmann JJ, Morris JF (1976) Membrane retrieval at neurosecretory axon endings. Nature 261:723–725
Nordmann JJ, Morris JF (1980) Depletion of neurosecretory granules and membrane retrieval in the sinus gland of the crab. Cell Tissue Res 205:31–42
Nordmann JJ, Dreifuss JJ, Baker PF, Ravazzola M, Malaisse-Lagae F, Orci L (1974) Secretion-dependent uptake of extracullular fluid by the rat neurohypophysis. Nature 250:155–157
Nordmann JJ, Dayanithi G, Cazalis M, Kretz-Zaepfel M, Colin DA (1988) Isolated neurohypophysial nerve endings, a promising tool to study the mechanism of stimulus-secretion coupling. In: Pickering BT, Wakerley JB, Sumerlee AJS (eds) Neurosecretion. Cellular aspects of the production and release of neuropeptides. Plenum, London, pp 147–155
Obata K, Kojima N, Nishiye H, Inoue H, Shirao T, Fujita SC, Uchizono K (1987) Four synaptic vesicle-specific proteins: identification by monoclonal antibodies and distribution in the nervous tissue and the adrenal medulla. Brain Res 404:169–179
Obendorf D, Schwarzenbrunner U, Fischer-Colbrie R, Laslop A, Winkler H (1988) In adrenal medulla synaptophysin (protein p38) is present in chromaffin granules and in a special vesicle population. J Neurochem 51:1573–1580
Palay SL (1955) An electron microscope study of the neurohypophysis in normal, hydrated and dehydrated rats. Anat Rec 121:348
Pow DV, Clark A (1990) Localisation of peptide hormones by light and electron microscopy. In: Fiddle K, Hutton JC (eds) Peptide hormone secretion: a practical approach. Oxford University Press, IRL Press Practical Handbooks Series, Oxford, pp 189–210
Pow DV, Morris JF (1989) Dendrites of hypothalamic magnocellular neurons release neurohypophysial peptides by exocytosis. Neuroscience 32:435–439
Pow DV, Morris JF (1990) Exocytotic release of oxytocin and vasopressin from dendrites in the rat supraoptic nucleus. J Neuroendocrinol [Suppl] 1:50–52
Raisman G (1973) Electron microscopic studies of the development of new neuroheamal contacts in the median eminence of the rat after hypophysectomy. Brain Res 55:245–261
Rutherford DT, Nastuck WL, Gennaro JF (1976) Reversible depletion of synaptic vesicles in K+ depolarized neuromuscular junction. J Cell Biol 70:375A
Shaw FD, Morris JF (1980) Calcium localization in the rat neurohypophysis. Nature 287:56–58
Theodosis DT, Dreifuss JJ, Harris MC, Orci L (1976) Secretion related uptake of horseradish peroxidase in neurohypophysial axons. J Cell Biol 70:294–303
Theodosis DT, Dreifuss JJ, Orci L (1977) Two classes of microvesicles in the neurohypophysis. Brain Res 123:159–163
thoenen H, Barde Y-A (1980) Physiology of nerve growth factor. Physiol Rev 60:1284–1335
Thomas L, Hartung K, Langosch D, Rehm H, Bamberg E, Franke WW, Betz H (1988) Identification of synaptophysin as a hexameric channel protein of the synaptic vesicle membrane. Science 242:1050–1053
Toescu EC, Morris JF (1990) Morphometric analysis of nerve endings isolated from bovine and rat neurohypophysis. J Anat 173:1–17
Trimble WS, Scheller RH (1988) Molecular biology of synaptic vesicle-associated proteins. Trends Neurosci 11:241–242
Valtorta F, Jahn R, Fesce R, Greengard P, Ceccarelli B (1988a) Synaptophysin (p38) at the frog neuromuscular junction: its incorporation into the axolemma and recycling after intense quantal secretion. J Cell Biol 107:2717–2727
Valtorta F, Villa A, Jahn R, De Camilli P, Greengard P, Ceccarelli B (1988b) Localization of synapsin I at the frog neuromuscular junction. Neuroscience 24:593–603
Valtorta F, Fesce R, Grohovaz F, Haimann C, Hurlbut WP, Iezzi N, Torri Tarelli F, Villa A, Ceccarelli B (1990) Neurotransmitter release and synaptic vesicle recycling. Neuroscience 35:477–489
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Pow, D.V., Morris, J.F. Membrane routing during exocytosis and endocytosis in neuroendocrine neurones and endocrine cells: use of colloidal gold particles and immunocytochemical discrimination of membrane compartments. Cell Tissue Res 264, 299–316 (1991). https://doi.org/10.1007/BF00313967
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DOI: https://doi.org/10.1007/BF00313967