Summary
Astrocytic membranes contacting the basal lamina are found to be less affected by filipin than subjacent lateral membranes. An abrupt change in density of lesions induced by filipin creates a border between subpial and lateral membranes at the glia limitans. This means that orthogonal array-crowded membranes may contain relatively less cholesterol than other astrocytic membrane domains. Another possible explanation for filipin resistance is also considered in relation to aggregated intramembrane particles of orthogonal arrays and/or membrane-associated filamentous elements including the basal lamina. The polygonal particle junction between astrocytic processes located just below the subpial membrane is strongly resistant to the action of filipin. Both membrane-associated enzymes, i.e. alkaline phosphatase (AlkPase) and Na+,K+-ATPase are commonly detected only in perivascular astrocytic membranes, and not in subpial membranes, suggesting a regional differentiation in function of astrocytic membranes. There are variations in the reactive deposits particularly of those for Na+,K+-ATPase. It is apparent that the distribution polarity of orthogonal arrays is not connected with that of either AlkPase or Na+,K+-ATPase. Judging from the relative resistance to filipin, however, astrocytes throughout the C.N.S., having domains specialized with orthogonal arrays, may possess a unique stabilizing mechanism for their own membranes contacting the basal lamina.
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.
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.
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.
Bordi, C. &Perrelet, A. (1978) Orthogonal arrays of particles in plasma membranes of the gastric parietal cell.Anatomical Record 192, 297–304.
Branton, D. (1971) Freeze-etching studies of membrane structure.Philosophical Transactions of the Royal Society B 261, 133–18.
Broderson, S. H., Patton, D. L. &Stahl, W. L. (1978) Fine structural localization of potassium-stimulatedp-nitrophenyl phosphatase activity in dendrites of the cerebral cortex.Journal of Cell Biology 78, R13–7.
Brown, D., Montesano, R. &Orci, L. (1982) Patterns of filipin-sterol complex distribution in intact erythrocytes and intramembrane particle-aggregated ghost membranes.Journal of Histochemistry and Cytochemistry 30, 702–6.
de Kruijff, B., Gerritsen, W. J., Oerlemans, A., Demel, R. A. &van Deenen, L. L. M. (1974) Polyene antibiotic-sterol interaction in membranes ofAcholeplasma Laidlawii cells and lecithin liposomes. I. Specificity of the membranes permeability changes induced by the polyene antibiotics.Biochimica et Biophysica Acta 339, 30–43.
Demel, R. A. &de Kruijff, B. (1976) The function of sterols in membranes.Biochimica et Biophysica Acta 457, 109–32.
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.
Elias, P. M., Friend, D. S. &Goerke, J. (1979) Membrane sterol heterogeneity. Freeze-fracture detection with saponins and filipin.Journal of Histochemistry and Cytochemistry 27, 1247–60.
Ellisman, M. H. &Levinson, S. R. (1982) Immunocytochemical localization of sodium channel distribution in the excitable membranes ofElectrophorus electricus.Proceedings of the National Academy of Sciences USA 79, 6707–11.
Ernst, S. A. (1972) Transport adenosine triphosphatase cytochemistry. II. Cytochemical localization of ouabain-sensitive, potassium dependent phosphatase activity in the secretory epithelium of the avian salt gland.Journal of Histochemistry and Cytochemistry 20, 23–38.
Ernst, S. A. (1975) Transport ATPase cytochemistry: Ultrastructural localization of potassium-dependent and potassium-independent phosphatase activities in rat kidney cortex.Journal of Cell Biology 66, 586–608.
Ernst, S. A. &Hootman, S. R. (1981) Microscopical methods for the localization of Na+, K+-ATPase.Histochemical Journal 13, 397–418.
Feltkamp, C. A. &Van Der Waerden, A. W. M. (1982) Membrane-associated proteins affect the formation of filipin-cholesterol complexes in viral membranes.Experimental Cell Research 140, 289–97.
Friend, D. S. &Bearer, E. L. (1981) β-Hydroxysterol distribution as determined by freeze-fracture cytochemistry.Histochemical Journal 13, 535–46.
Gotow, T. &Hashimoto, P. H. (1979) Fine structure of ependyma and intercellular junctions in the area postrema of the rat.Cell and Tissue Research 201, 207–25.
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.
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.
Gotow, T. &Hashimoto, P. H. (1983a) Regional difference in filipin affection in plasma membranes of epithelial cells and surrounding free cells in the choroid plexus.Cell and Tissue Research 230, 689–94.
Gotow, T. &Hashimoto, P. H. (1983b) Filipin resistance in intermediate junction membranes of guinea pig ependyma: possible relationship to filamentous underlying.Journal of Ultrastructure Research 84, 83–93.
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.
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.
Henderson, D., Eibl, H. &Weder, K. (1979) Structure and biochemistry of gap junctions from rat liver.Journal of Molecular Biology 132, 193–218.
Hertz, L. (1978) An intense potassium uptake into astrocytes, its further enhancement by high concentrations of potassium, and its possible involvement in potassium homeostasis at the cellular level.Brain Research 145, 202–8.
Hirano, A. (1981) Astrocytes. InA Guide to Neuropathology, pp. 204–24. New York, Tokyo: Igaku-Shoin.
Hugon, J. &Borgers, M. (1966) A direct lead method for the electron microscopic visualization of alkaline phosphatase activity.Journal of Histochemistry and Cytochemistry 14, 429–31.
Kimelberg, H. K. (1983) Primary astrocyte cultures-a key to astrocyte function.Cellular and Molecular Neurobiology 3, 1–16.
Koefoed-Johnsen, U. &Ussing, H. H. (1958) The nature of the frog skin potential.Acta physiologica scandinavica 42, 298–308.
Landis, D. M. D. &Reese, T. S. (1974) Arrays of particles in freeze-fractured astrocytic membranes.Journal of Cell Biology 60, 316–20.
Landis, D. M. D. &Reese, T. S. (1981a) Astrocyte membrane structure: change after circulatory arrest.Journal of Cell Biology 88, 660–3.
Landis, D. M. D. &Reese, T. S. (1981b) Membrane structure in mammalian astrocytes: a review of freeze-fracture studies on adult, developing, reactive and cultured astrocytes.Journal of Experimental Biology 95, 35–48.
Landis, D. M. D. &Reese, T. S. (1982) Regional organization of astrocytic membranes in cerebellar cortex.Neuroscience 7, 937–50.
Mayahara, H., Hirano, H., Saito, T. &Ogawa, K. (1967) The new lead citrate method for the ultracytochemical demonstration of activity of non-specific alkaline phosphatase (orthophoshoric monoester phosphohydrolase).Histochemie 11, 88–96.
Medzihradsky, F., Nandhasri, P. S., Idoyaga-Vargas, V. &Sellinger, O. Z. (1971) A comparison of the ATPase activity of the glial cell fraction and the neuronal perikaryal fraction isolated in bulk from rat cerebral cortex.Journal of Neurochemistry 18, 1599–603.
Milhorat, T. H., Davis, D. A. &Hammock, M. K. (1975) Localization of ouabin-sensitive Na-K-ATPase in frog, rabbit and rat choroid plexus.Brain Research 99, 170–4.
Montesano, R. (1979) Inhomogenous distribution of filipin-sterol complexes in the ciliary membrane of rat tracheal epithelium.American Journal of Anatomy 156, 139–45.
Montesano, R., Perrelet, A., Vassalli, P. &Orci, L. (1979) Absence of filipin-sterol complexes from large coated pits on the surface of cultured cell.Proceedings of the National Academy of Sciences USA 76, 6391–5.
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.
Nakajima, Y. &Bridgman, P. C. (1981) Absence of filipin-sterol complexes from the membranes of active zone and acetylcholine receptor aggregates at frog neuromuscular junctions.Journal of Cell Biology 88, 453–8.
Pinto Da Silva, P. &Nicolson, G. L. (1974) Freeze-etch localization of concanavalin A receptors to the membrane intercalated particles of human erythrocyte ghost membranes.Biochimica et Biophysica Acta 363, 311–9.
Popot, J.-L., Demel, R. A., Sobel, A., van Deenen, L. L. M. &Changeux, J.-P. (1978) Interaction of acetylcholine (nicotinic) receptor protein fromTorpedo marmorata electric organ with monolayers of pure lipids.European Journal of Biochemistry 85, 27–42.
Privat, A. (1977) The ependyma and subependymal layer of the young rat: a new contribution with freeze-fracture.Neuroscience 2, 447–57.
Robenek, H., Jung, W. &Gebhard, R. (1982) The topography of filipin-cholesterol complexes in the plasma membrane of cultured hepatocytes and their relation to cell junction formation.Journal of Ultrastructure Research 78, 95–106.
Robinson, J. M. &Karnovsky, M. J. (1983) Ultrastructural localization of several phosphatases with cerium.Journal of Histochemistry and Cytochemistry 31, 1197–208.
Schwartz, M., Ernst, S. A., Siegel, G. J. &Agranoff, B. W. (1981) Immunocytochemical localization of (Na+, K+)-ATPase in the goldfish optic nerve.Journal of Neurochemistry 36, 107–15.
Severs, N. J., Warren, R. C. &Barnes, S. H. (1981) Analysis of membrane structure in the transitional epithelium of rat urinary bladder. 3. Localization of cholesterol using filipin and digitonin.Journal of Ultrastructure Research 77, 160–88.
Skerrow, C. J. &Motoltsy, A. G. (1974) Chemical characterization of isolated epidermal desmosomes.Journal of Cell Biology 63, 524–30.
Stahl, W. L. &Broderson, S. H. (1976) Localization of Na+, K+-ATPase in brain.Federation Proceedings 6, 1260–5.
Sugimura, K. &Mizutani, A. (1979) Histochemical and cytochemical studies of alkaline phosphatase activity in the synapses of rat brain.Histochemistry 61, 123–9.
Wood, J. G., Jean, D. H., Whitaker, J. N., McLAughlin, B. J. &Albers, R. W. (1977) Immunocytochemical localization of the sodium, potassium activated ATPase in knifefish brain.Journal of Neurocytology 6, 571–81.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Gotow, T. Cytochemical characteristics of astrocytic plasma membranes specialized with numerous orthogonal arrays. J Neurocytol 13, 431–448 (1984). https://doi.org/10.1007/BF01148333
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01148333