Skip to main content
Log in

Cell junctions and membrane specializations in the ventricular zone (germinal matrix) of the developing sheep brain: A CSF-brain barrier

  • Published:
Journal of Neurocytology

Summary

Cell junctions in the ventricular zone (germinal matrix) of the embryonic and foetal sheep brain were examined with thin-section and freeze-fracture electron microscopy. Neuroependymal cells in the early ventricular zone (days 19–40 of embryonic development, gestation period 147 days) exhibit a novel arrangement of cell junctions that connect adjacent neuroependymal cells at their lateral cell membranes next to the ventricular system. Small but typical gap junctions were also identified from the earliest stages examined. In serial thin sections and using a goniometer with a tilting device, the cell contacts showed a tight junction-like appearance of close and continuous fusion between neighbouring cell membranes. However, they were not arranged in a belt-like fashion close to the ventricular surface, but spiralled from the ventricular pole of the cells along the lateral cell membrane towards the deeper parts of the ventricular zone. Their freeze fracture appearance was different from that of single-stranded tight junctions in that the dimensions of their ridges and grooves were generally greater and the E-face grooves contained many particles. The junctions were especially prominent where more than two cells made contact. At mid-gestation they were less prominent than earlier and at 125 days gestation the neuroependymal layer was replaced by a mature-looking normal ependymal layer in which individual ependymal cells were connected by zonulae adherentes and large gap junctions; orthogonal arrays were also prominent. The close contact between gap junctions and single-stranded junctions found early in gestation suggests that there may be some developmental relation between these two membrane specializations.

The transient single-strand junctions presumably form the morphological basis for a recently described CSF-brain barrier in the early foetal sheep brain. They may also have some mechanical function in anchoring neighbouring cells together in the region of the developing brain where cells are continuously dividing and migrating.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • 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.

    Google Scholar 

  • Åstrøm, K. E. (1967) On the early development of the isocortex in fetal sheep.Progress in Brain Research 26, 1–59.

    Google Scholar 

  • Brightman, M. W., Prescott, L. &Reese, T. S. (1975) Intercellular junctions of special ependyma.Brain-Endocrine Interaction II. The Ventricular System. 2nd International Symposium, Shizuoka, pp. 146–65. Basel: Karger.

    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.

    Google Scholar 

  • Cavanagh, M. E. &Warren, A. (1985) The distribution of native albumin and foreign albumin injected into lateral ventricles of prenatal and neonatal rat forebrain.Anatomy and Embryology 172, 345–51.

    Google Scholar 

  • Davson, H. (1967)Physiology of the Cerebrospinal Fluid. London: Churchill.

    Google Scholar 

  • Decker, R. S. &Friend, D. S. (1974) Assembly of gap junctions during amphibian neurulation.Journal of Cell Biology 62, 32–47.

    Google Scholar 

  • Duckett, S. (1968) The germinal layer of the growing human brain during early fetal life.Anatomical Record 161, 231–46.

    Google Scholar 

  • Dziegielewska, K. M., Evans, C. A. N., Malinowska, D. H., Møllgård, K., Reynolds, J. M., Reynolds, M. L. &Saunders, N. R. (1979) Studies of the development of brain barrier systems to lipid insoluble molecules in fetal sheep.Journal of Physiology 292, 207–31.

    Google Scholar 

  • Dziegielewska, K. M. &Saunders, N. R. (1987) The development of the blood-brain barrier: proteins in fetal and neonatal CSF, their nature and origins. InHandbook of Human Growth and Biological Development (edited byMeisami, E. &Timiras, P. J.) Boca Raton: CRC Press (in press).

    Google Scholar 

  • Dziegielewska, K. M., Saunders, N. R., Schejter, E. J., Zakut, H., Zevin-Sonkin, D., Zisling, R. &Soreq, H. (1986) Synthesis of plasma proteins in fetal, adult and neoplastic human brain tissue.Developmental Biology 115, 93–104.

    Google Scholar 

  • Dziegielewska, K. M., Saunders, N. R. &Soreq, H. (1985) Messenger ribonucleic acid (mRNA) from developing rat cerebellum directsin vitro synthesis of plasma proteins.Developmental Brain Research 23, 259–67.

    Google Scholar 

  • Farquhar, M. &Palade, G. (1963) Junctional complexes in various epithelia.Journal of Cell Biology 17, 375–412.

    Google Scholar 

  • Felgenhauer, K. (1974) Protein size and cerebrospinal fluid composition.Klinische Wochenschrift 52, 1158–64.

    Google Scholar 

  • Fossan, G., Cavanagh, M. E., Evans, C. A. N., Malinowska, D. H., Møllgård, K., Reynolds, M. L. &Saunders, N. R. (1985) CSF-brain permeability in the immature sheep fetus: a CSF-brain barrier.Developmental Brain Research 18, 113–24.

    Google Scholar 

  • Friend, D. &Gilula, N. (1972) Variations in tight and gap junctions in mammalian tissues.Journal of Cell Biology 53, 758–76.

    Google Scholar 

  • Gros, D., Mocquard, J. P., Challice, C. E. &Schrevel, J. (1978) Formation and growth of gap junctions in mouse myocardium during ontogenesis: a freeze-cleave study.Journal of Cell Science 30, 45–61.

    Google Scholar 

  • Kachar, B. &Pinto DA Silva, P. (1981) Rapid massive assembly of tight junction strands.Science 213, 541–3.

    Google Scholar 

  • Levitt, P., Cooper, M. L. &Rakic, P. (1981) Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: an ultrastructural immunoperoxidase analysis.Journal of Neuroscience 1, 27–39.

    Google Scholar 

  • Madsen, J. K. &Møllgård, K. (1979) The tight epithelium of the Mongolian gerbil subcommissural organ as revealed by freeze-fracturing.Journal of Neurocytology 8, 481–91.

    Google Scholar 

  • Meller, K. (1985) Ultrastructural aspects of the choroid plexus epithelium as revealed by the rapid-freezing and deep-etching techniques.Cell and Tissue Research 239, 189–201.

    Google Scholar 

  • Møllgård, K., Lauritzen, B. &Saunders, N. R. (1979) Double replica technique applied to choroid plexus from early foetal sheep: completeness and complexity of tight junctions.Journal of Neurocytology 8, 139–49.

    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.

    Google Scholar 

  • Møllgård, K. &Saunders, N. R. (1977) A possible transepithelial pathway via endoplasmic reticulum in foetal sheep choroid plexus.Proceedings of the Royal Society of London, Series B 199, 321–6.

    Google Scholar 

  • Møllgård, K. &Saunders, N. R. (1986) The development of the human blood-brain and blood-CSF barriers.Neuropathology and Applied Neurobiology 12, 337–58.

    Google Scholar 

  • Monroe, B. Y. &Holmes, E. M. (1982) The freeze fractured median eminence. I. Development of intercellular junctions in the ependyma of the 3rd ventricle of the rat.Cell and Tissue Research 222, 389–408.

    Google Scholar 

  • Reynolds, M. L. &Møllgård, K. (1985) The distribution of plasma proteins in the neocortex and early allocortex of the developing sheep brain.Anatomy and Embryology 171, 41–60.

    Google Scholar 

  • Saunders, N. R. &Møllgård, K. (1984) Development of the blood-brain barrier.Journal of Developmental Physiology 6, 45–57.

    Google Scholar 

  • Sheridan, J. D. (1968) Electrophysiological evidence for low-resistance intercellular junctions in the early chick embryo.Journal of Cell Biology 37, 650–9.

    Google Scholar 

  • Shoukimas, G. M. &Hinds, J. W. (1978) The development of the cerebral cortex in the embryonic mouse: an electron microscopic serial section analysis.Journal of Comparative Neurology 179, 795–830.

    Google Scholar 

  • Simionescu, M. &Simionescu, N. (1977) Organization of cell junctions in the peritoneal mesothelium.Journal of Cell Biology 74, 98–110.

    Google Scholar 

  • Staehelin, L. A. (1973) Further observations on the fine structure of freeze-cleaved tight junctions.Journal of Cell Science 13, 763–86.

    Google Scholar 

  • Staehelin, L. A. (1974) Structure and function of intercellular junctions.International Review of Cytology 39, 191–283.

    Google Scholar 

  • Stensaas, L. J. &Stensaas, S. S. (1968) An electron microscope study of cells in the matrix and intermediate laminae of the cerebral hemisphere of the 45 mm rabbit embryo.Zeitschrift für Zellforschung und mikroskopische Anatomie 91, 341–65.

    Google Scholar 

  • Tauc, M., Vignon, X. &Bouchaud, C. (1984) Evidence for the effectiveness of the blood-csf barrier in the fetal rat choroid plexus. A freeze-fracture and peroxidase diffusion study.Tissue and Cell 16, 65–74.

    Google Scholar 

  • Tennyson, V. M. &Pappas, G. D. (1962) An electron microscope study of ependymal cells of the fetal, early postnatal and adult rabbit.Zeitschrift für Zellforschung und mikroskopische Anatomie 56, 595–618.

    Google Scholar 

  • Van Deurs, B. &Luft, J. H. (1979) Effects of glutaraldehyde fixation on the structure of tight junctions.Journal of Ultrastructure Research 68, 160–72.

    Google Scholar 

  • Warner, A. E., Guthrie, S. C. &Gilula, N. B. (1984) Antibodies to gap-junctional protein selectively disrupt junctional communication in the early amphibian embryo.Nature 311, 127–31.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Møllgård, K., Balslev, Y., Lauritzen, B. et al. Cell junctions and membrane specializations in the ventricular zone (germinal matrix) of the developing sheep brain: A CSF-brain barrier. J Neurocytol 16, 433–444 (1987). https://doi.org/10.1007/BF01668498

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01668498

Keywords

Navigation