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The glial cells of the cerebral ganglia of Helix pomatia L. (Gastropoda, Pulmonata)

II. Uptake of ferritin and 3H-Glutamate

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Summary

  1. 1.

    With Helix pomatia intracerebral injections of ferritin were carried out (maximal incubation time: 45 min). First, the marker spreads with time via the extracellular space throughout the cerebral ganglia and, secondly, is transported out of the ganglia. Electron microscopical studies showed that all glial cell types take up great amounts of ferritin by endocytosis. The plasmatic glial cells at the periphery incorporate more of the marker than the filamentous glial cells in the centre. No uptake of ferritin by neurons or axons was observed. In vitro studies proved that ferritin can penetrate from the connective tissue capsule into the ganglia only after disruption of the neural lamella and damaging of the peripheral glial processes.

  2. 2.

    3H-glutamate, a putative transmitter of the CNS of Helix pomatia, was injected into the hemocoel of active snails (incubation times: 15min, l h, 6h, 3d). Light microscopical evaluation of radioautographs showed that great quantities of the tracer penetrate into the ganglia. The bulk of it is taken up by glial cells, whereas the neurons exhibit only small amounts of the tracer.

The studies with ferritin as well as those with 3H-glutamate indicate that the glial cells of the cerebral ganglia of Helix pomatia act as a “hemolymph-neuron barrier”. A dominant role of the plasmatic glial cells according to these processes is discussed.

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References

  • Abbott, N.J.: Absence of blood-brain barrier in a crustacean, Carcinus maenas L. Nature (Lond.) 225, 291–293 (1970)

    Google Scholar 

  • Abbott, N.J.: The organization of the cerebral ganglion in the shore crab, Carcinus maenas. II. The relation of intracerebral blood vessels to other brain elements. Z. Zellforsch. 120, 401–419 (1971)

    Google Scholar 

  • Abbott, N.J.: Access of ferritin to the interstitial space of Carcinus brain from intracerebral blood vessels. Tissue & Cell 4, 99–104 (1972)

    Google Scholar 

  • Baecker, R.: Die Micromorphologie von Helix pomatia und einigen anderen Stylommatophoren. Ergebn. Anat. Entwickl.-Gesch. 29, 449–585 (1932)

    Google Scholar 

  • Barber, V.C., Graziadei, P.: The fine structure of cephalopod blood vessels. II. The vessels of the nervous system. Z. Zellforsch. 77, 147–161 (1967)

    Google Scholar 

  • Becker, N.H., Hirano, A., Zimmermann, H.M.: Observations of the distribution of exogenous peroxidase in the rat cerebrum. J. Neuropath, exp. Neurol. 27, 439–452 (1968)

    Google Scholar 

  • Benjamin, A,M., Quastel, J.H.: Fate of L-glutamate in the brain. J. Neurochem. 23, 457–464 (1974)

    Google Scholar 

  • Berl, S., Clarke, D.D.: Compartmentation of amino acid metabolism. In: Handbook of neurochemistry, Vol. I, Chemical architecture of the nervous system (Lajtha, A., ed.), pp. 447–476. New York: Plenum Press 1969

    Google Scholar 

  • Brightman, M.W.: The distribution within the brain of ferritin injected into cerebrospinal fluid compartments. II. Parenchymal distribution. Amer. J. Anat. 117, 193–220 (1965)

    Google Scholar 

  • Buchholz, K., Kuhlmann, D., Nolle, A.: Aufnahme von Trypanblau und Ferritin in die Blasenzellen des Bindegewebes von Helix pomatia und Cepaea nemoralis (Stylommatophora, Pulmonata). Z. Zellforsch. 113, 203–215 (1971)

    Google Scholar 

  • Campos-Ortega, J.A.: Autoradiographic localization of 3H-γ-ammobutyric acid uptake in the lamina ganglionaris of Musca and Drosophila. Z. Zellforsch. 147, 415–431 (1974)

    Google Scholar 

  • Chalazonitis, N., Chagneux, H., Riche, D.: Transport macromoléculaire glioneuronique par vésiculation à double membrane. C.R. Acad. Sci. (Paris) D227, 1779–1783 (1973)

    Google Scholar 

  • Coggeshall, R.E.: A light and election microscope study of the abdominal ganglion of Aplysia California. J. Neurophysiol. 30, 1263–1287 (1967)

    Google Scholar 

  • Cottrell, G.A., Macon, J., Szczepaniak, A.C.: Glutamic acid mimicking of synaptic inhibition on the giant serotonin containing neuron of the snail. Brit. J. Pharmacol. 45, 684–688 (1972)

    Google Scholar 

  • Dyer, R.F., Cowden, R.R.: Electron microscopy of the esophageal ganglion complex of the gastropod pulmonate Triodopsis divesta. I. Ultrastructure of the epineurium. J. Morph. 139, 125–154 (1973)

    Google Scholar 

  • Ehinger, B.: Glial uptake of taurine in the rabbit retina. Brain Res. 60, 512–516 (1973)

    Google Scholar 

  • Ehinger, B., Falck, B.: Autoradiography of some suspected neurotransmitter substances: gaba, glycine, aspartic acid, glutamic acid, histamine, dopamine and L-dopa. Brain Res. 33, 157–172 (1971)

    Google Scholar 

  • Evans, P.D.: An autoradiographic study of the localization of the uptake of glutamate by the peripheral nerves of the crab, Carcinus maenas L. J. Cell Sci. 14, 351–367 (1974)

    Google Scholar 

  • Fernandez, J.: Electron microscopic study of neuron-neuroglial relationships and the transport of opaque tracers in the nervous system of Helix aspersa. Anat. Rec. 157, 243 (1967)

    Google Scholar 

  • Fernandez, J.: Nervous system of the snail Helix aspersa. II. Fine structure of vascular channels and amoebocytes associated with ganglionic sheath. Z. Zellforsch. 118, 512–524 (1971)

    Google Scholar 

  • Gerschenfeld, H.M.: Chemical transmission in invertebrate central nervous systems and neuromuscular junctions. Physiol. Rev. 53, 1–119 (1973)

    Google Scholar 

  • Gerschenfeld, H.M., Lasansky, A.: Action of glutamic acid and other naturally occurring aminoacids on snail central neurons, J. Neuropharmacol. 3, 301–314 (1964)

    Google Scholar 

  • Gray, E.G.: Electron microscopy of glio-vascular organization of the brain of Octopus. Phil. Trans. B 255, 13–32 (1969)

    Google Scholar 

  • Hebb, C.: CNS at the cellular level: identity of transmitter agents. Ann. Rev. Physiol. 32, 165–192 (1970)

    Google Scholar 

  • Henn, F.A., Goldstein, M.N., Hamberger, A.: Uptake of the neurotransmitter candidate glutamate by glia. Nature (Lond.) 249, 663–664 (1974)

    Google Scholar 

  • Henn, F.A., Hamberger, A.: Glial cell function: Uptake of transmitter substances. Proc. nat. Acad. Sci. (Wash.) 68, 2686–2690 (1971)

    Google Scholar 

  • Hösli, E., Ljungdahl, Å., Hökfelt, T., Hösli, L.: Spinal cord tissue cultures — a model for autoradiographic studies on uptake of putative neurotransmitters as glycine or GABA. Experientia (Basel) 28, 1342–1344(1972)

    Google Scholar 

  • Holtzman, E., Freeman, A.R., Kashner, L.A.: A cytochemical and electron microscope study of channels in the Schwann cells surrounding lobster giant axons. J. Cell Biol. 44, 438–445 (1970)

    Google Scholar 

  • Kerkut, G.A., Cottrell, G.A.: Aminoacids in the blood and nervous system of Helix aspersa. Comp. Biochem. Physiol. 5, 227–230 (1962)

    Google Scholar 

  • Kerkut, G.A., Ralph, K., Walker, R.J., Woodruff, G., Woods, R.: Excitation in the molluscan central nervous system. In: Excitatory synaptic mechanisms. Ed. Anderson, P., Jansen, J.K.S., pp. 105–117. Oslo: Universitetsforlaget 1970

    Google Scholar 

  • Klemm, H.: Das Perineurium als Diffusionsbarriere gegenüber Peroxidase bei epiund endoneuraler Applikation. Z. Zellforsch. 108, 431–446 (1970)

    Google Scholar 

  • Kristensson, K., Strömberg, E., Elofsson, R., Olsson, Y.: Distribution of protein tracers in the nervous system of the crayfish (Astacus astacus L.) following systemic and local application. J. Neurocytol. 1, 35–48 (1972)

    Google Scholar 

  • Kuhlmann, D.: Einbau von H3-Thymidin in Zellen und Gewebe von Helix pomatia L. (Gastropoda, Pulmonata). Experientia (Basel) 27, 690–691 (1971)

    Google Scholar 

  • Lane, N.J.: Fine structure of an lepidopteran nervous system and its accessibility to peroxidase and lanthanum. Z. Zellforsch. 131, 205–222 (1972)

    Google Scholar 

  • Lane, N.J., Leslie, R.A., Swales, L.S.: Insect peripheral nerves: accessibility of neurohaemal regions to lanthanum. J. Cell Sci. 18, 179–197 (1975)

    Google Scholar 

  • Lane, N.J., Treherne, J.E.: Uptake of peroxidase by cockroach central nervous system. Tissue & Cell 2, 413–425 (1970)

    Google Scholar 

  • Lane, N.J., Treherne, J.E.: Accessibility of the central nervous connectives of Anodonta cygnea to a large molecular weight compound. J. Exp. Biol. 56, 493–499 (1972a)

    Google Scholar 

  • Lane, N.J., Treherne, J.E.: Studies on perineurial junctional complexes and the sites of uptake of microperoxidase and lanthanum in the cockroach central nervous system. Tissue & Cell 4, 427–436 (1972b)

    Google Scholar 

  • Ljungdahl, Å., Hökfelt, T.: Autoradiographic uptake patterns of [3H]-GABA and [3H]-glycine in central nervous tissues with special reference to the cat spinal cord. Brain Res. 62, 587–595 (1973)

    Google Scholar 

  • Mirolli, M., Gorman, A.L.F.: The extracellular space of a simple molluscan nervous system and its permeability to potassium. J. Exp. Biol. 58, 423–436 (1973)

    Google Scholar 

  • Nolle, A., Kuhlmann, D.: Einbau von 3H-Uridin in den Schlundring von Helix pomatia L. Naturwissenschaften 11, 281–282 (1966)

    Google Scholar 

  • Nolte, A., Reinecke, M., Kuhlmann, D., Speckmann, E.-J., Schulze, H.: Glial cells of the snail brain. Some remarks on morphology and function. In: “Snail Brain Symposium” (J. Salanki, ed.). Budapest: Akadémiai Kiadó (in press) 1976

    Google Scholar 

  • Oldendorf, W.H.: Brain uptake of radiolabelled amino acids, amines, and hexoses after arterial injection. Amer. J. physiol. 221, 1629–1639 (1971)

    Google Scholar 

  • Orkand, P.M., Kravitz, E.A.: Localization of the sites of γ-aminobutyric acid (GABA) uptake in lobster nerve-muscle preparations. J. Cell Biol. 49, 75–89 (1971)

    Google Scholar 

  • Pelletier, G., Dupont, A., Puviani, R.: Ultrastructural study of the uptake of peroxidase by the rat median eminence, Cell Tiss. Res. 156, 521–532 (1975)

    Google Scholar 

  • Pentreath, V.W., Cottrell, G.A.: The blood supply to the central nervous system of Helix pomatia. Z. Zellforsch. 111, 160–178 (1970)

    Google Scholar 

  • Pentreath, V.W., Cottrell, G.A.: Uptake of serotonin, 5-hydroxytryptophan and tryptophan by giant serotonin-containing neurones and other neurones in the central nervous system of the snail (Helix pomatia). Z. Zellforsch. 143, 21–35 (1973)

    Google Scholar 

  • Reinecke, M.: Die Gliazellen der Cerebralganglien von Helix pomatia L. (Gastropoda: Pulmonata). I. Ultrastructur und Organisation. Zoomorphologie 82, 105–136 (1975)

    Google Scholar 

  • Roberts, P.J., Keen, P.: (14C) glutamate uptake and compartmentation in glia of rat dorsal sensory ganglion. J. Neurochem. 23, 201–209 (1974)

    Google Scholar 

  • Rogers, D.C.: Fine structure of the epineural connective tissue sheath of the subesophageal ganglion of Helix aspera. Z. Zellforsch. 102, 99–112 (1969)

    Google Scholar 

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

    Google Scholar 

  • Salpeter, M.M., Faeder, I.R.: The role of sheath cells in glutamate uptake by insect nerve muscle preparations. Progr. Brain Res. 34, 103–114 (1971)

    Google Scholar 

  • Sandeman, D.C.: The vascular circulation in the brain, optic lobes and thoracic ganglia of the crab Carcinus. Proc. Roy. Soc. B 168, 82–90 (1967)

    Google Scholar 

  • Scharrer, E.: The capillary bed of the central nervous system of certain invertebrates. Biol. Bull. 87, 52–58 (1944)

    Google Scholar 

  • Schloot, W.: Postembryogenese des Schlundrings von Helix pomatia L. (Gastropoda) unter Berücksichtigung der Sekretion der Nervenzellen. Z. Zellforsch. 67, 406–426 (1965)

    Google Scholar 

  • Schon, F., Kelly, J.S.: Autoradiographic localization of 3H-GABA and 3H-glutamate over satellite glial cells. Brain Res. 66, 275–288 (1974)

    Google Scholar 

  • Schubert, D.: The uptake of GABA by clonal nerve and glia. Brain Res. 84, 87–98 (1975)

    Google Scholar 

  • Sellinger, O.Z., Petiet, P.D.: Horseradish peroxidase uptake in vivo by neuronal and glial lysosomes. Exp. Neurol. 38, 370–385 (1973)

    Google Scholar 

  • Selwood, L.: Electron microscopy of the fate of exogenous ferritin in the feline visual cortex. Z. Zellforsch. 107, 6–14 (1970)

    Google Scholar 

  • Selwood, L.: Electron microscopy of endocytotic elements in the cat cerebrum. Acta neuropath. (Berl.) 18, 299–310 (1971)

    Google Scholar 

  • Skaer, H. le B., Lane, N.J.: Junctional complexes, perineurial and glia-axonal relationships and the ensheathing structures of the insect nervous system; a comparative study using conventional and freeze-cleaving techniques. Tissue & Cell 6, 695–718 (1974)

    Google Scholar 

  • Thurston, J.H., Warren, S.K.: Permeability of the blood-brain barrier to monosodium glutamate and effects on the components of the energy reserve in new-born mouse brain. J. Neurochem. 8, 2241–2244 (1971)

    Google Scholar 

  • Treherne, J.E., Moreton, R.B.: The environment and function of invertebrate nerve cells. Int. Rev. Cytol. 28, 45–88 (1970)

    Google Scholar 

  • Treherne, J.E., Pichon, Y.: The insect blood brain barrier. Adv. Insect Physiol. 6, 257–313 (1972)

    Google Scholar 

  • Villegas, G.M., Villegas, R.: Ultrastructural studies of the squid nerve fibers. J. gen. Physiol. 51, 44S-60S (1968)

    Google Scholar 

  • Wolburg-Buchholz, K.: Blasenzellen im Bindegewebe des Schlundrings von Cepaea nemoralis L. (Gastropoda, Stylommatophora). II. Aufnahme und Speicherung von Ferritin. Z. Zellforsch. 130, 262–278 (1972)

    Google Scholar 

  • Wolburg-Buchholz, K., Nolle, A.: Untersuchungen zur Struktur der Basallamelle des Zentralnervensystems von Crepidula fornicata L. (Gastropoda, Prosobranchia). forma et functio 6, 359–372 (1973)

    Google Scholar 

  • Zimmermann, P.: Beziehungen verschiedenartiger Zellkomplexe des normalen und regenerierenden Nervensystems von Lumbricus terrestris L. zum Gefäßsystem. Z. Zellforsch. 106, 423–438 (1970)

    Google Scholar 

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  1. Abteilung für Histophysiologie, Zoologisches Institut, Universität Münster, and Fachbereich Biologie, Universität Konstanz, West Germany

    Manfred Reinecke

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I thank Prof. Dr. Angela Nolte, Universität Münster, for her advice in this study and helpful discussions. I would also like to thank my colleagues for reading the manuscript, in particular Dr. Toni Lindl and Mrs. Grace Chapman, who helped with the English

Part of this work has been supported by a grant of the Deutsche Forschungsgemeinschaft (SFB 138)

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Reinecke, M. The glial cells of the cerebral ganglia of Helix pomatia L. (Gastropoda, Pulmonata). Cell Tissue Res. 169, 361–382 (1976). https://doi.org/10.1007/BF00219608

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