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Structural connections between dense core vesicles in the central nervous system of Anodonta cygnea L. (mollusca, eulamellibranchia)

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Summary

Electron microscopy of the cerebro-visceral connectives of Anodonta cygnea shows numerous long rows of dense core vesicles within the smaller axons of the connectives. These vesicles are often linked together by bridges of electron-dense material reinforced by one or more “arms”. The use of the tilting stage on the electron microscope, which allows the bridges to be examined from different angles, confirms the presence of these vesicular connections.

Sub-cellular fractionation of the cerebro-visceral connectives was carried out to study the nature of these bridged dense core vesicles. In the negatively stained vesicle fraction two or more dense core vesicles are joined in a row by connections similar to the vesicular bridges of the intact connective. In the fixed vesicle fraction, many of the dense core vesicles are connected by bridges but long rows of bridged vesicles are not seen.

The functional significance of the vesicular bridges is discussed. Preliminary findings of this work have been reported previously (McLaughlin and Howes, 1973).

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References

  • Banks, P., Mayor, D., Tomlinson, D.R.: Further evidence for the involvement of microtubules in the intra-axonal movement of noradrenaline storage granules. J. Physiol. (Lond.) 219, 755–761 (1971)

    Google Scholar 

  • Bargmann, W., Knoop, A.: Elektronenmikroskopische Beobachtungen an der Neurohypophyse. Z. Zellforsch. 46, 242–251 (1957)

    Google Scholar 

  • Bern, H.A.: The properties of neurosecretory cells. Gen. comp. Endocr., Suppl. 1, 117–132 (1962)

    Google Scholar 

  • Dahlström, A.: Synthesis, transport and life-span of amine storage granules in sympathetic adrenergic neurons. In: Cellular dynamics of the neuron, vol. 8 (ed. S. Barondes), p. 153–174. New York: Academic Press 1969

    Google Scholar 

  • Euler, U.S. von: Adrenergic neurotransmission, Ciba Found. Study Group No. 33, p. 116. London: Churchill 1968

    Google Scholar 

  • Gerschenfeld, H.M.: Observations on the ultrastructure of synapses in some pulmonate molluscs. Z. Zellforsch. 60, 258–275 (1963)

    Google Scholar 

  • Gerschenfeld, H.M., Tramezzani, J.H., DeRobertis, E.: Ultrastructure and function of neurohypophysis of the toad. Endocrinology 66, 741–762 (1960)

    Google Scholar 

  • Gray, E.G.: Problems of interpreting the fine structure of vertebrate and invertebrate synapses. Int. Rev. Gen. Exp. Zool. 2, 139–170 (1966)

    Google Scholar 

  • Grimstone, A.V., Cleveland, L.R.: The fine structure and function of the contractile axostyles of certain flagellates. J. Cell Biol. 24, 387–400 (1965)

    Google Scholar 

  • Gupta, B.L., Mellon, D., Treherne, J.E.: The organization of the central nervous connectives in Anodonta cygnea (Linnaeus) (Mollusca: Eulamellibranchia). Tissue and Cell 1, 1–30 (1969)

    Google Scholar 

  • Hepler, P.K., Jackson, W.T.: Microtubules and early stages of cellplate formation in the endosperm of Haemanthus katherinee Baker. J. Cell Biol. 38, 437–446 (1968)

    Google Scholar 

  • Hepler, P.K., McIntosh, J.R., Cleland, S.: Intermicrotubule bridges in mitotic spindle apparatus. J. Cell Biol. 45, 438–444 (1970)

    Google Scholar 

  • Heslop, J.P., Howes, E.A.: Temperature and inhibitor effects on fast axonal transport in a molluscan nerve. J. Neurochem. 19, 1709–1716 (1972)

    Google Scholar 

  • Hiripi, L.: Catecholamines in the different tissues of fresh water mussel (Anodonta cygnea L., Pelecypoda) analysed by thin-layer chromatographic and fluorimetric methods. Annal. Biol. Tihany 39, 13–20 (1972)

    Google Scholar 

  • Horne, R.W., Whittaker, V.P.: The use of the negative staining method for the electron microscopic study of subcellular particles from animal tissues. Z. Zellforsch. 58, 1–16 (1962)

    Google Scholar 

  • Huxley, H.E.: The double array of filaments in cross-striated muscles. J. biophys. biochem. Cytol. 3, 631–648 (1957)

    Google Scholar 

  • Klein, R.L., Thureson-Klein, Å.: An electron microscopic study of noradrenaline storage vesicles isolated from bovine splenic nerve trunk. J. Ultrastruct. Res. 34, 473–491 (1971)

    Google Scholar 

  • Maser, M.D., Powell III, T.E., Philpott, C.W.: Relationships amongst pH, osmolarity, and concentration of fixative solutions. Stain Technol. 42, 175–182 (1967)

    Google Scholar 

  • McIntosh, J.R., Porter, K.R.: Microtubules in the spermatids of the domestic fowl. J. Cell Biol. 35, 153–173 (1967)

    Google Scholar 

  • McLaughlin, B.J., Howes, E.A.: Structural connexions between dense core vesicles. Nature (Lond.) 241, 189–190 (1973)

    Google Scholar 

  • Munn, E.A.: On the structure of mitochondria and the value of ammonium molybdate as a negative stain for osmotically sensitive structures. J. Ultrastruct. Res. 25, 362–380 (1968)

    Google Scholar 

  • Palay, S.L.: The fine structure of the neurohypophysis. In: Progress in neurobiology. II. Ultrastructure and cellular chemistry of neural tissue (eds. S. Korey, J.U. Nurnberger), p. 31–49. New York: Hoeber-Harper 1957

    Google Scholar 

  • Palay, S.L.: The fine structure of secretory neurons in the preoptic nucleus of the goldfish (Carassius auratus). Anat. Rec. 138, 417–425 (1960)

    Google Scholar 

  • Potts, W.T.W.: The inorganic composition of the blood of Mytilus edulis and Anodonta cygnea. J. exp. Biol. 31, 376–385 (1954)

    Google Scholar 

  • Reynolds, E.S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963)

    Google Scholar 

  • Salánki, J., Hiripi, L.: Increase of serotonin in the adductors of Anodonta cygnea L. (Pelecypoda) relaxed by nerve stimulation and in relation to the periodic activity. Comp. Biochem. Physiol. 32, 629–636 (1970)

    Google Scholar 

  • Sandborn, E.B.: Electron microscopy of the neuron membrane systems and filaments. Comp. J. Physiol. Pharmac. 44, 329–338 (1966)

    Google Scholar 

  • Satelle, D.B., Lane, N.J.: Architecture of gastropod central nervous tissues in relation to ionic movements. Tissue and Cell 4, 253–270 (1972)

    Google Scholar 

  • Scharrer, E., Brown, S.: The fine structure of neurosecretory cells of the earthworm Lumbricus terrestris L. Anat. Rec. 139, 271 (1961)

    Google Scholar 

  • Smith, D.S.: On the significance of cross-bridges between microtubules and synaptic vesicles. Phil. Trans. B 261, 395–405 (1971)

    Google Scholar 

  • Smith, D.S., Järlfors, U., Beránek, R.: The organization of synaptic axoplasm in the Lamprey (Petromyzon marinus) central nervous system. J. Cell Biol. 46, 199–219 (1970)

    Google Scholar 

  • Tranzer, J.P.: A new amine storing compartment in adrenergic axons. Nature (Lond.) 237, 57–58 (1972)

    Google Scholar 

  • Venable, J.H., Coggeshall, R.: A simplified lead citrate stain for use in electron microscopy. J. Cell Biol. 25, 407–408 (1965)

    Google Scholar 

  • Westrum, L.E.: A combination staining technique for electron microscopy. J. Micro. 4, 275–278 (1965)

    Google Scholar 

  • Whittaker, V.P.: Some properties of synaptic membranes isolated from the central nervous system. Ann. N.Y. Acad. Sci. 137, 982–998 (1966)

    Google Scholar 

  • Wilson, H.J.: Arms and bridges on microtubules in the mitotic apparatus. J. Cell Biol. 40, 954–959 (1969)

    Google Scholar 

  • Zs-Nagy, I.: Histochemical and electron-microscopic studies on the relation between dopamine and dense core vesicles in the neurons of Anodonta cygnea L. In: Symposium on Neurobiology of Invertebrates (ed. J. Salánki), pp. 69–84. Budapest: Plenum Press 1967

    Google Scholar 

  • Zs-Nagy, I., S.-Rozsa, K., Salánki, J.: Subcellular localization of 5-hydroxytryptamine in the central nervous system of lamellibranchiates. J. Neurochem. 12, 245–251 (1965)

    Google Scholar 

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Acknowledgements. We would like to thank Brij Gupta for assistance in stereo-electron microscopy and John Heslop for helpful discussion and review of the manuscript. One of us (B.J.M.) was recipient of a post-doctoral grant from the Underwood Fund.

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McLaughlin, B.J., Howes, E.A. Structural connections between dense core vesicles in the central nervous system of Anodonta cygnea L. (mollusca, eulamellibranchia). Z.Zellforsch 144, 75–88 (1973). https://doi.org/10.1007/BF00306687

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