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Junctions in the central nervous system of the cat

V. The junctional complex of the pia-arachnoid membrane

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Summary

The leptomeningeal tissue of the choroid plexuses and of the brain surfaces have been studied by means of the freeze-etching technique. The pia-arachnoid membrane and the subdural neurothel represent the morphological barrier between the extracerebral tissue and the cerebrospinal compartment. The freeze-etch findings indicate that the arachnoid and neurothelial cells are coupled by extensive zonulae occludentes which seem to represent the structural basis of the barrier mechanism provided by these cell layers. Furthermore, it became evident that gap junctions of considerable structural heterogeneity occur on the pial and arachnoid cells of the interstitial choroidal compartment and of the free brain surfaces. The structural heterogeneity of the nexuses is taken as an indication of the plasticity of the leptomeningeal tissue. The different morphological characteristics of the nexal formations are discussed with respect to their probable functional meaning.

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References

  • Ames, A., Sakanoue, M., Endo S.: Na, K, Ca and Cl concentrations in choroid plexus fluid and cisternal fluid compared with plasma ultrafiltrate. J. Neurophysiol. 27, 672–681 (1964)

    Google Scholar 

  • Andres, K.H.: Über die Feinstruktur der Arachnoidea und Dura mater von Mammalia. Z. Zellforsch. 79, 272–295 (1967)

    Google Scholar 

  • Barr, L., Berger, W., Dewey, M.M.: Electrical transmission at the nexus between smooth muscle cells. J. Gen. Physiol. 51, 347–367 (1968)

    Google Scholar 

  • Brightman, M.W.: The intracerebral movement of proteins injected into blood and cerebrospinal fluid. Progr. Brain Res. 29, 19–40 (1968)

    Google Scholar 

  • Brightman, M.W., Reese, T.S.: Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol. 40, 648–677 (1969)

    Google Scholar 

  • Claude, Ph., Goodenough, D.A.: The ultrastructure of the zonula occludens in tight and leaky epithelia. J. Cell Biol. 55, 46a (1973)

  • Davson, H.: The blood-brain barrier. In: The structure and function of nervous tissue (ed. G.H. Bourne) Vol. IV, p. 321–446. New York-London: Academic Press 1972

    Google Scholar 

  • Davson, H., Segal, M.B.: The effects of some inhibitors and accelerators of sodium transport on the turnover of 22Na in the cerebrospinal fluid and the brain. J. Physiol. 209, 131–153 (1970)

    Google Scholar 

  • Decker, R.S., Friend, D.S.: Assembly of gap junctions during amphibian neurulation. J. Cell Biol. 62, 32–47 (1974)

    Google Scholar 

  • Dempsey, E.W., Wislocki, G.B.: An electron microscope study of the blood-brain barrier in the rat, employing silver nitrate as a vital stain. J. biophys. biochem. Cytol. 1, 245–256 (1955)

    Google Scholar 

  • Dermietzel, R.: Junctions in the central nervous system of the cat. III. Gap junctions and membrane-associated orthogonal particle complexes (MOPC) in astrocytic membranes. Cell Tiss. Res. 149, 121–135 (1974a)

    Google Scholar 

  • Dermietzel, R.: Freeze-etch studies of the membranes of the Pacinian corpuscle. Symposium on Mechanoreception, p. 99–107 (ed. J. Schwartzkopff) Opladen: Westdeutscher Verlag 1974b

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

    Google Scholar 

  • Dermietzel, R., Schünke, D.: A complex junctional system in endothelial and connective tissue cells of the choroid plexus. Amer. J. Anat. 143, 131–136 (1975)

    Google Scholar 

  • Dewey, M.M., Barr, L.: Intercellular connections between smooth muscle cells: the nexus. Science, 137, 670–672 (1962)

    Google Scholar 

  • Diamond, J.M., Wright, E.M.: Biological membranes: The physical basis of ion and non-electrolyte selectivity. Ann. Rev. Physiol. 31, 581–646 (1969)

    Google Scholar 

  • Dohrmann, G.J.: The choroid plexus: a historical review. Brain Res. 18, 197–218 (1970)

    Google Scholar 

  • Dreifuss, J.J., Giradier, L., Forssmann, W.G.: Etude de la propagation de l'exitation dans le ventricle de rat on moyen de solutions hypertoniques. Pflügers Arch. ges. Physiol. 292, 13 (1966)

    Google Scholar 

  • Findlay, J.W.: The choroid plexuses of the lateral ventricles of the brain, their histology, normal and pathological (in relation specially to insanity). Brain, 22, 161–202 (1899)

    Google Scholar 

  • Friend, D.S., Gilula, N.B.: Variations in tight and gap junctions in mammalian tissues. J. Cell Biol. 53, 758–776 (1972)

    Google Scholar 

  • Frömter, E., Diamond, J.: Route of passive ion permeation in epithelia. Nature New Biol. 235, 9–14 (1972)

    Google Scholar 

  • Goldmann, E.: Vitalfärbung am Zentralnervensystem. Beitrag zur Physio-Pathologie des Plexus chorioideus und der Hirnhäute. Abh. kgl. preuß. Akad. Wiss. physik.-med. Kl., Nr. 1, 1–60 (1913)

    Google Scholar 

  • Hand, A.R., Gobel, St.: The structural organization of the septate and gap junctions of hydra. J. Cell Biol. 52, 397–408 (1972)

    Google Scholar 

  • Harvey, S.C., Burr, H.S.: The development of the meninges. Arch. Neurol. Psych. 15, 545–567 (1926)

    Google Scholar 

  • Harvey, S.C., Burr, H.S., van Campenhout, E.: Development of the meninges. Further experiments. Arch. Neurol. Psych. 29, 683–690 (1933)

    Google Scholar 

  • Hüttner, J., Boutet, M., More, R.H.: Gap junctions in arterial endothelium. J. Cell Biol. 57, 247–252 (1973)

    Google Scholar 

  • Huxley, A.F., Stämpfli, R.: Effect of potassium and sodium ions on the electrical activity of the giant axon of the squid. J. Physiol. 112, 496–508 (1951)

    Google Scholar 

  • Johnson, R.G., Preus, D.: Gap junction formation in a reaggregating system: An ultrastructural study. J. Cell Biol. 59, 158a (1973)

  • Imamura, S.: Beiträge zur Histologie des Plexus chorioideus der Menschen. Arb. Neur. Inst. Wien, 7–8, 272 (1900)

    Google Scholar 

  • Krnjevic, K.: Some observations on the perfused frog sciatic nerves. J. Physiol. 123, 338–356 (1954)

    Google Scholar 

  • Lehmann, G., Meesmann, A.: Über das Bestehen eines Donnangleichgewichtes zwischen Blut und Kammerwasser bzw. Liquor cerebrospinalis. Pflügers Arch. ges. Physiol. 205, 210–232 (1924)

    Google Scholar 

  • Lehmann, H.J.: The epineurium as a diffusion barrier. Nature 172, 1045 (1953)

    Google Scholar 

  • Lehmann, H.J.: Über Struktur und Funktion der perineuralen Diffusionsbarrieren. Z. Zellforsch. 46, 232–241 (1957)

    Google Scholar 

  • Loeschcke, H.H.: Über Bestandspotentiale im Gebiet der medulla oblongata. Pflügers Arch. ges. Physiol. 262, 517–531 (1956)

    Google Scholar 

  • Loeschcke, H.H.: DC potentials between CSF and blood. In: Ion homeostasis of the brain, p. 77–96 (eds. Siesjö, B.K., Sørensen, S.C.) Alfred Benzon Symposium III. Munsgaard: Copenhagen 1971

    Google Scholar 

  • Loeschcke, H.H., Sugioka, K.: pH of cerebrospinal fluid in the cisterna magna and on the surface of the choroid plexus of the 4th ventricle, and its effect on ventilation in experimental disturbances of acid base balance. Transients, and steady states. Pflügers Arch. ges. Physiol. 312, 161–188 (1969)

    Google Scholar 

  • Loewenstein, W.R.: Permeability of membrane junctions. Ann. N.Y. Acad. Sci. 137, 441–472 (1966)

    Google Scholar 

  • Maxwell, D.S., Pease, D.C.: The electron microscopy of the choroid plexus. J. biophys. biochem. Cytol. 2, 467–474 (1956)

    Google Scholar 

  • McNutt, N.S., Weinstein, R.S.: The ultrastructure of the nexus. A correlated thin-section and freeze-cleaved study. J. Cell Biol. 47, 666–688 (1970)

    Google Scholar 

  • Moor, H., Mühlethaler, K.: Fine structure in frozen-etched yeast cells. J. Cell Biol. 17, 609–628 (1963)

    Google Scholar 

  • Mottschall, H.J., Loeschcke, H.H.: Das transmeningeale Potential der Katze bei Änderungen des CO2-Druckes und der H+ -Ionenkonzentration. Pflügers Arch. ges. Physiol. 277, 662–670 (1963)

    Google Scholar 

  • Nelson, E., Blinzinger, K., Hager, H.: Electron microscopic observations on subarachnoid and perivascular spaces of the Syrian hamster brain. Neurology 11, 285–295 (1961)

    Google Scholar 

  • Nicely, M.: Measurement of the potential difference across the connective tissue sheath of frog sciatic nerve. Experientia 11, 199 (1955)

    Google Scholar 

  • Nichol, J., Girling, F., Jerrad, W., Claxton, E.B., Burton, A.C.: Fundamental instability of the small blood vessels and critical closing pressures in vascular beds. Amer. J. Physiol. 164, 330–344 (1951)

    Google Scholar 

  • Pappas, G.D., Bennett, M.V.: Specialized junctions involved in electrical transmission between neurons. Ann. N.Y. Acad. Sci. 137, 495–508 (1966)

    Google Scholar 

  • Pease, D.C., Schultz, R.L.: Electron microscopy of rat cranial meninges. Amer. J. Anat. 102, 301–321 (1958)

    Google Scholar 

  • Pinto da Silva, P., Gilula, N.B.: Gap junctions in normal and transformed fibroblasts in culture. Exp. Cell Res. 71, 393–401 (1972)

    Google Scholar 

  • Pitelka, D.R., Hamamoto, S.T., Duafala, J.G., Nemanic, M.K.: Cell contacts in the mouse mammary gland. I. Normal gland in postnatal development and secretory cycle. J. Cell Biol. 56, 707–818 (1973)

    Google Scholar 

  • Pricam, C., Humbert, F., Perrelet, A., Orci, L.: Gap junctions in mesangial and lacis cells. J. Cell Biol. 63, 349–354 (1974)

    Google Scholar 

  • Revel, J.P., Karnovsky, M.J.: Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell Biol. 33, C 7, (1967)

    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 

  • Rhodin, J.A.: An atlas of ultrastructure. Philadelphia: Saunders 1963

    Google Scholar 

  • Robertson, J.D., Bodenheimer, P.S., Stage, D.E.: The ultrastructure of Mauthner cell synapses and nodes in goldfish brains. J. Cell Biol. 19, 159–199 (1963)

    Google Scholar 

  • Schaltenbrand, G.: Plexus und Meningen. In: Handbuch der mikroskopischen Anatomie des Menschen, IV/2, 1–139. Berlin-Göttingen-Heidelberg: Springer 1955

    Google Scholar 

  • Shanthaveerappa, P.R., Bourne, G.H.: A perineural epithelium. J. Cell Biol. 14, 343–346 (1962a)

    Google Scholar 

  • Shanthaveerappa, P.R., Bourne, G.H.: The “perineural epithelium”, a metabolically active, continuous, protoplasmic cell barrier surrounding peripheral nerve fasciculi. J. Anat. 96, 527–537 (1962b)

    Google Scholar 

  • Shanthaveerappa, P.R., Hope, J., Bourne, G.H.: Electron microscopic demonstration of the perineural epithelium in rat peripheral nerve. Acta anat. 52, 193–201 (1963)

    Google Scholar 

  • Shanthaveerappa, P.R., Bourne, G.H.: A sample method for preparation and staining of the whole Pacinian corpuscle. Acta anat. 60, 199–206 (1965)

    Google Scholar 

  • Spatz, H.: Versuche zur Nutzbarmachung der E. Goldmannschen Vitalfarbstoffversuche für die Pathologie des Zentralnervensystems. Allg. Z. Psychiatr. 80, 285–288 (1925)

    Google Scholar 

  • Spatz, H.: Die Bedeutung der vitalen Färbung für die Lehre vom Stoffaustausch zwischen dem Zentralnervensystem und dem übrigen Körper. Arch. Psychiatr. 101, 267–358 (1934)

    Google Scholar 

  • Spurr, A.R.: A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruc. Res. 26, 31–43 (1969)

    Google Scholar 

  • Staehelin, L.A.: Three types of gap junctions interconnecting intestinal epithelial cells visualized by freeze-etching. Proc. Nat. Acad. Sci. 69, 1318–1321 (1972)

    Google Scholar 

  • Staehelin, L.A., Mukherjee, P.M., Williams, A.W.: Freeze-etch appearance of the tight junctions in the epithelium of small and large intestine of mice. Protoplasma 67, 165–184 (1969)

    Google Scholar 

  • Stämpfli, R.: Bau und Funktion isolierter markhaltiger Nervenfasern. Erg. Physiol. 47, 70–165 (1952)

    Google Scholar 

  • Voetmann, E.: On the structure and surface area of the human choroid plexuses. A quantitive anatomical study. Acta anat. 8, Suppl. 10, 1–116 (1949)

    Google Scholar 

  • Waggener, J.D., Beggs, J.: The membrane coverings of neural tissues: an electron microscopy study. J. Neuropathol. 26, 412–426 (1967)

    Google Scholar 

  • Welch, K., Sadler, K.: Electrical potentials of choroid plexus of the rabbit. J. Neurosurg. 22, 344–351 (1965)

    Google Scholar 

  • Wislocki, G.B., Leduc, E.H.: Vital staining of the hematoencephalic barrier by silver nitrate and trypan blue, and cytological comparisons of the neurohypophysis, pineal body, area postrema, intercolumnar tubercle, and supraoptic crest. J. comp. Neurol. 96, 371–414 (1952)

    Google Scholar 

  • Wright, E.M.: Ion transport across the frog posterior choroid plexus. Brain Res. 23, 302–304 (1970)

    Google Scholar 

  • Yee, A.G.: Gap junctions between hepatocytes in regenerating rat liver. J. Cell Biol. 55, 294a (1972) (Abstract).

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  1. Institute of Topographical Anatomy, University Hospital Essen, Germany

    Rolf Dermietzel

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  1. Rolf Dermietzel
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This investigation was supported by the Deutsche Forschungsgemeinschaft SFB 114 (Bionach).

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Dermietzel, R. Junctions in the central nervous system of the cat. Cell Tissue Res. 164, 309–329 (1975). https://doi.org/10.1007/BF00223012

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