Skip to main content
SpringerLink
Log in

Plasma membrane organization of astrocytes in elasmobranchs with special reference to the brain barrier system

  • Published:
Journal of Neurocytology

Summary

The structural machinery contributing to the blood-brain barrier in elasmobranchs has been examined mainly using freeze-fracture techniques. Capillary endothelial cells, which show local aggregations of pinocytotic vesicles and infrequent fenestrations, are connected by poorly developed tight junctions. Astrocytic processes investing the capillary are linked by well-developed tight junctions between lateral membranes immediately beneath the perivascular space. The tight junctions consist of continuous strands of multiple layers coursing circumferentially around the astrocytic processes parallel to one another as well as to the perivascular space. The presence of intramembrane particles (IMPs) within E-face grooves may result in discontinuities in IMP rows on the P-face. Thus, in compensation for the capillary endothelium, perivascular astrocytes constitute the morphological site of the blood-brain barrier in elasmobranchs. Continuous strands of tight junctions are also detected between astrocytic processes forming the glia limitans at the brain surface. These may act as a barrier between meningeal connective tissue and brain parenchyma. Astrocytic membranes have numerous IMPs of 8–9 run in diameter on their P-faces. These IMPs are uniformly distributed so that astrocytic membranes are easily distinguished from neuronal membranes even in the neuropil. Ependymal cells also have numerous IMPs in all their membrane domains. Orthogonal arrays are not detected in either astrocytic or ependymal plasma membranes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anders, J. J., Blessing, P. M. &Brightman, M. W. (1983) Freeze-fracture analysis of plasma membranes of isolated astrocytes from rat brain.Brain Research 278, 81–91.

    PubMed  Google Scholar 

  • Anders, J. J. &Brightman, M. W. (1979) Assemblies of particles in the cell membranes of developing, mature and reactive astrocytes.Journal of Neurocytology 8, 777–95.

    PubMed  Google Scholar 

  • Anders, J. J. &Brightman, M. W. (1982) Particle assemblies in astrocytic plasma membranes are rearranged by various agentsin vitro and cold injuryin vivo.Journal of Neurocytology 11, 1009–29.

    PubMed  Google Scholar 

  • Bodenheimer, T. S. &Brightman, M. W. (1968) A blood-brain barrier to peroxidase in capillaries surrounded by perivascular spaces.American journal of Anatomy 122, 249–68.

    PubMed  Google Scholar 

  • Brightman, M. W. &Reese, T. S. (1969) Junctions between intimately apposed cell membranes in the vertebrate brain.Journal of Cell Biology 40, 648–77.

    PubMed  Google Scholar 

  • Brightman, M. W., Reese, T. S., Olsson, Y. &Klatzo, I. (1971) Morphologic aspects of the blood-brain barrier to peroxidase in elasmobranchs.Progress in Neuropathology 1, 146–61.

    Google Scholar 

  • Bundgaard, M. (1982) Brain barrier systems in the lamprey. I. Ultrastructure and permeability of cerebral blood vessels.Brain Research 240, 55–64.

    PubMed  Google Scholar 

  • Bundgaard, M. &Cserr, H. (1981) A glial blood-brain barrier in elasmobranchs.Brain Research 266, 61–73.

    Google Scholar 

  • Bundgaard, M., Cserr, H. &Murray, M. (1979) Impermeability of hagfish cerebral capillaries to horseradish peroxidase.Cell and Tissue Research 198, 65–77.

    PubMed  Google Scholar 

  • Cserr, H. F., Fenstermacher, J. D. &Rall, D. P. (1978) Comparative aspects of brain barrier systems for nonelectrolytes.American Journal of Physiology 234, R52–60.

    PubMed  Google Scholar 

  • Dermietzel, R. (1974) Junctions in the central nervous system of the cat. III. Gap junctions and membrane-associated orthogonal particle complexes (MOPC) in astrocytic membranes.Cell and Tissue Research 149, 121–35.

    PubMed  Google Scholar 

  • Dermietzel, R. (1975) Junctions in the central nervous system of the cat. IV. Interendothelial junctions of cerebral blood vessels from selected areas of the brain.Cell and Tissue Research 164, 45–62.

    PubMed  Google Scholar 

  • Gotow, T. (1984) Cytochemical characteristics of astrocytic plasma membranes specialized with numerous orthogonal arrays.Journal of Neurocytology 13 (in press).

  • Gotow, T. &Hashimoto, P. H. (1982a) Intercellular junctions between specialized ependymal cells in the subcommissural organ of the rat.Journal of Neurocytology 11, 363–79.

    PubMed  Google Scholar 

  • Gotow, T. &Hashimoto, P. H. (1982b) Fine structural studies on ependymal paracellular and capillary transcellular permeability in the subcommissural organ of the guinea-pig.Journal of Neurocytology 11, 447–62.

    PubMed  Google Scholar 

  • Hashimoto, P. H. &Hama, K. (1968) An electron microscope study on protein uptake into brain regions devoid of the blood-brain barrier.Medical Journal of Osaka University 18, 331–46.

    PubMed  Google Scholar 

  • Hashimoto, P. H. (1972) Intracellular channels as a route for protein passage in the capillary endothelium of the shark brain.American Journal of Anatomy 134, 41–58.

    PubMed  Google Scholar 

  • Hatton, J. D. &Ellisman, M. H. (1981) The distribution of orthogonal arrays and their relationship to intercellular junctions in neuroglia of the freeze-fractured hypothalamo-neurohypophysial system.Cell and Tissue Research 215, 309–23.

    PubMed  Google Scholar 

  • Hatton, J. D. &Ellisman, M. H. (1982) The distribution of orthogonal arrays in the freeze-fractured rat median eminence.Journal of Neurocytology 11, 335–49.

    PubMed  Google Scholar 

  • Kenny, T. P. &Shivers, R. R. (1974) The blood-brain barrier in a reptile,Anolis carolinesis.Tissue and Cell 6, 319–33.

    PubMed  Google Scholar 

  • Klatzo, I. &Stein Wall, O. (1965) Observation on cerebrospinal fluid pathways and behaviour of the blood-brain barrier in sharks.Acta Neuropathologica 5, 161–75.

    PubMed  Google Scholar 

  • Korte, G. E. &Rosenbluth, J. (1981) Ependymal astrocytes in the frog cerebellum.Anatomical Record 199, 267–79.

    PubMed  Google Scholar 

  • Landis, D. M. D. &Reese, T. S. (1974) Arrays of particles in freeze-fractured astrocytic membranes.Journal of Cell Biology 60, 316–20.

    PubMed  Google Scholar 

  • Landis, D. M. D. &Reese, T. S. (1982) Regional organization of astrocytic membranes in cerebellar cortex.Neuroscience 7, 937–50.

    PubMed  Google Scholar 

  • Long, D. M., Bodenheimer, T. S., Hartmann, J. F. &Klatzo, I. (1968) Ultrastructural features of the shark brain.American Journal of Anatomy 122, 209–36.

    PubMed  Google Scholar 

  • Martínez-Palomo, A. &Erlij, D. (1975) Structure of tight junctions in epithelia with different permeability.Proceedings of the National Academy of Sciences USA 72, 4487–91.

    Google Scholar 

  • Massa, P. T. &Mugnaini, E. (1982) Cell junctions and intramembrane particles of astrocytes and oligodendrocytes: a freeze-fracture study.Neuroscience 7, 523–38.

    PubMed  Google Scholar 

  • Miragall, F. (1983) Evidence for orthogonal arrays of particles in the plasma membranes of olfactory and vomeronasal sensory neurons of vertebrates.Journal of Neurocytology 12, 567–76.

    PubMed  Google Scholar 

  • Møllgård, K., Malinowska, D. H. &Saunders, N. R. (1976) Lack of correlation between tight junction morphology and permeability properties in developing choroid plexus.Nature 264, 293–4.

    PubMed  Google Scholar 

  • Nabeshima, S., Reese, T. S., Landis, D. M. D. &Brightman, M. W. (1975) Junction in the meninges and marginal glia.Journal of Comparative Neurology 164, 127–70.

    PubMed  Google Scholar 

  • Nakai, Y., Kudo, J. &Hashimoto, A. (1980) Specific cell membrane differentiation in the tanycytes and glial cells of the organum vasculosum of the lamina terminalis in dog.Journal of Electron Microscopy 29, 144–50.

    PubMed  Google Scholar 

  • Pannese, E., Luciano, L., Iurato, S. &Reale, A. (1977) Intercellular junctions and other membrane specializations in developing spinal ganglia; a freeze-fracture study.Journal of Ultrastructure Research 60, 169–80.

    PubMed  Google Scholar 

  • Privat, A. (1977) The ependyma and subependymal layer of the young rat: a new contribution with freeze-fracture.Neuroscience 2, 447–57.

    PubMed  Google Scholar 

  • Reese, T. S. &Karnovsky, M. J. (1967) Fine structural localization of a blood-brain barrier to exogenous peroxidase.Journal of Cell Biology 34, 207–17.

    PubMed  Google Scholar 

  • Usukura, J. &Yamada, E. (1978) Observation on the cytolemma of the olfactory receptor cell in the newt. I. Freeze replica analysis.Cell and Tissue Research 188, 83–98.

    PubMed  Google Scholar 

  • Van Deurs, B. (1979) Cell junctions in the endothelia and connective tissue of the rat choroid plexus.Anatomical Record 195, 73–94.

    PubMed  Google Scholar 

  • Van Deurs, B. (1980) Structural aspects of brain barriers, with special reference to the permeability of cerebral endothelium and choridal epithelium.International Review of Cytology 65, 117–91.

    PubMed  Google Scholar 

  • Wolburg, H., Kastner, R. &Kurz-Isler, G. (1983) Lack of orthogonal particle assemblies and presence of tight junctions in astrocytes of the goldfish (Carassius auratus). A freeze-fracture study.Cell and Tissue Research 234, 389–402.

    PubMed  Google Scholar 

  • Wujek, J. R. &Reier, P. J. (1984)Journal of Comparative Neurology 222, 607–19.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, Osaka University Medical School, Nakanoshima, Kitaku, 530, Osaka, Japan

    Takahiro Gotow & Paulo H. Hashimoto

Authors
  1. Takahiro Gotow
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paulo H. Hashimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gotow, T., Hashimoto, P.H. Plasma membrane organization of astrocytes in elasmobranchs with special reference to the brain barrier system. J Neurocytol 13, 727–742 (1984). https://doi.org/10.1007/BF01148491

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01148491

Keywords

Search

Navigation