Skip to main content
Log in

Meningeal cells organize the superficial glia limitans of the cerebellum and produce components of both the interstitial matrix and the basement membrane

  • Published:
Journal of Neurocytology

Summary

We have investigated the factors controlling both the morphological transformation of glial processes into end feet and the deposition of extracellular matrix molecules into the overlying basement membrane by destroying meningeal cells over the hamster cerebellum by 6-hydroxydopamine administration on the day of birth. We report that within 24 h of destruction of meningeal cells, the concentrations of fibrillary collagens types I, III and IV in the glia limitans externa and the associated basement membrane molecules laminin, collagen type IV, and fibronectin are greatly diminished, resulting in the development of focal gaps in the basement membrane. The immunohistochemical integrity of the basement membrane is restored within 3 days over those surfaces of the folial apices where meningeal cells reappear. Likewise, the fibrillary collagens of the associated interstitial matrix are re-established in the same amounts as in controls. However, meningeal cells remain permanently absent from fissures and all extracellular matrix molecules tested disappear from rostral cerebellar folia covered by the anterior medullary velum. Moreover, the glial endfeet make up the superficial glia limitans only on folial apices, while they disappear from the fissurai surfaces. In primary cultures, meningeal cells produce the fibrillary collagens type I, III, and VI, and the matrix molecules fibronectin and laminin, collagen type IV, nidogen, and heparansulphate proteoglycan. These findings indicate that meningeal cells (i) produce molecular components of both the interstitial matrix and the basement membrane, and (ii) are involved in the morphological transformation of glial fibres into the endfeet which constitute the superficial glia limitans.

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

  • Alitalo, K. (1980) Production of both interstitial and basement membrane procollagens by fibroblastic Wi 38 cells from human embryonic lung.Biochemical and Biophysical Research Communication 93, 873–80.

    Google Scholar 

  • Altman, J. &Bayer, S. A. (1978) Prenatal development of the cerebellar system in the rat. I. Cytogenesis and histogenesis of the deep nuclei and the cortex of the cerebellum.Journal of Comparative Neurology 179, 23–48.

    Google Scholar 

  • Bernfield, M. R., Banerjee, S. D., Koda, J. E. &Rapraeger, A. C. (1984) Remodelling of the basement membrane as a mechanism of morphogenetic tissue interaction. InThe Role of Extracellular Matrix in Development (edited byTrelstad, R.) pp. 545–72. New York: Alan R. Liss.

    Google Scholar 

  • Bernstein, J. J., Getz, R., Jefferson, M. &Velemenz, M. (1985) Astrocytes secrete basal lamina after hemisection of rat spinal cord.Brain Research 327, 135–41.

    Google Scholar 

  • Cameron, R. S. &Rakic, P. (1991) Glial cell lineage in the cerebral cortex: A review and synthesis.Glia 4, 124–37.

    Google Scholar 

  • Del Cerro, M., Walker, J. R., Stoughton, R. L. &Cosgrove, J. W. (1976) Displaced neural elements within the cerebellar fissures of normal and experimental albino rats.Anatomical Record 184, 389 (abstract).

    Google Scholar 

  • Griffin, W., Eriksson, M., Del Cerro, M., Woodward, D. &Stamper, N. (1980) Naturally occurring alterations of cortical layers surrounding the fissura prima of rat cerebellum.Journal of Comparative Neurology 192, 109–18.

    Google Scholar 

  • Gude, S., Burmester, J., Pehlemann, F. W. &Sievers, J. (1987a) Meningeal cells produce constituents of the interstitial matrix and the basal lamina at the cerebellar surface. InNew Frontiers in Brain Research (edited byElsner, N. &Creutzfeldt, O.) p. 233. Stuttgart: Thieme.

    Google Scholar 

  • Gude, S., Burmester, J., Pehlemann, F. W. &Sievers, J. (1987b) Meningealzellen bilden Bestandteile der Interstitialmatrix und der Basalmembran.Anatomische Anzeiger 163, 154 (Abstract).

    Google Scholar 

  • Hartmann, D., Sievers, J., Pehlmann, F. W. &Berry, M. (1992) Destruction of meningeal cells over medial cerebral hemisphere of newborn hamsters prevents the formation of the infrapyramidal blade of the dentate gyrus.Journal of Comparative Neurology 320, 33–61.

    Google Scholar 

  • Hausmann, B. &Sievers, J. (1985) Cerebellar external granule cells are attached to the basal lamina from the onset of migration up to the end of their proliferative activity.Journal of Comparative Neurology 241, 50–62.

    Google Scholar 

  • Hausmann, B., Mangold, U., Sievers, J. &Berry, M. (1985) Derivation of cerebellar Golgi neurons from the external granular layer. Evidence from explantation of external granule cells in vivo.Journal of Comparative Neurology 232, 511–23.

    Google Scholar 

  • Hausmann, B., Hartmann, D. &Sievers, J. (1987) Secondary neuroepithelial stem cells of the cerebellum and the dentate gyrus are attached to the basal lamina during their migration and proliferation. InMesenchymal-Epithelial Interactions in Neural Development (edited byWolff, J. R., Sievers, J. &Berry, M.) pp. 279–92. Berlin: Springer.

    Google Scholar 

  • V. Knebel Doeberitz, Ch., Sievers, J., Sadler, M., Pehlemann, F. W., Berry, M. &Haliwell, P. (1986) Destruction of meningeal cells over the newborn hamster cerebellum with 6-hydroxydopamine prevents foliation and lamination in the rostral cerebellum.Neuroscience 17, 409–26.

    Google Scholar 

  • Krüger, S., Sievers, J., Hansen, C., Sadler, M. &Berry, M. (1986) Three morphologically distinct types of interface develop between adult host and fetal brain transplants: implications for scar formation in the adult central nervous system.Journal of Comparative Neurology 249, 103–16.

    Google Scholar 

  • Kühl, U., Timpl, R. &Von Der Mark, K. (1982) Synthesis of type IV collagen and laminin in cultures of skeletal muscle cells and their assembly on the surface of myotubes.Developmental Biology 93, 344–54.

    Google Scholar 

  • Kühl, U., Oechalan, M., Timpl, R., Mayne, R., Hay, E. &Von Der Mark, K. (1984) Role of muscle fibroblasts in the deposition of type IV collagen in the basal lamina of myotubes.Differentiation 28, 164–72.

    Google Scholar 

  • Liesi, P. (1985) Laminin-immunoreactive glia distinguish regenerative adult CNS systems from nonregenerative ones.EMBO Journal 4, 2505–11.

    Google Scholar 

  • Liesi, P., Dahl, D. &Vaheri, A. (1983) Laminin is produced by early rat astrocytes in primary culture.Journal of Cell Biology 96, 920–4.

    Google Scholar 

  • Liesi, P., Dahl, D. &Vaheri, A. (1984) Neurons cultured from developing rat brain attach and spread preferentially on laminin.Journal of Neuroscience Research 11, 241–51.

    Google Scholar 

  • Liesi, P., Kirkwood, T. &Vaheri, A. (1986) Fibronectin is expressed by astrocytes cultured from embryonic and early postnatal rat brain.Experimental Cell Research 163, 175–85.

    Google Scholar 

  • Pehlemann, F. W., Sievers, J. &Berry, M. (1985) Meningeal cells are involved in foliation, lamination and neurogenesis of the cerebellum: Evidence from 6-OHDA-induced destruction of meningeal cells.Developmental Biology 110, 136–46.

    Google Scholar 

  • Price, J. &Hynes, D. D. (1985) Astrocytes in culture synthesize and secrete a variant form of fibronectin.Journal of Neuroscience 5, 2205–11.

    Google Scholar 

  • Rakic, P. (1971a) Guidance of neurons migrating to the fetal monkey neocortex.Brain Research 33, 471–6.

    Google Scholar 

  • Rakic, P. (1971b) Neuron-glia relationship during granule cell migrating in developing cerebellar cortex. A Golgi and electron microscopic study in Macacus rhesus.Journal of Comparative Neurology 141, 283–312.

    Google Scholar 

  • Rickmann, M. &Wolfe, J. R. (1985) Prenatal gliogenesis in the neopallium of the rat.Advances in Anatomy, Embryology and Cell Biology 93, 1–104.

    Google Scholar 

  • Rutka, J. T., Giblin, J., Dougherty, D. V., McCulloch, J. R., De Armond, S. J. &Rosenblum, M. L. (1986a) An ultrastructural and immunocytochemical analysis of leptomeningeal and meningioma cultures.Journal of Neuropathology and Experimental Neurology 45, 285–303.

    Google Scholar 

  • Rutka, J. T., Kleppe-Hoifodt, H., Emma, D. A., Giblin, J. R., Dougherty, D. V., McCulloch, J. R., De Armond, S. J. &Rosenblum, M. L. (1986b) Characterization of normal human brain cultures: Evidence for the out-growth of leptomeningeal cells.Laboratory Investigation 55, 71–85.

    Google Scholar 

  • Sanderson, R. D., Fitch, J. M., Linsenmayer, T. R. &Mayne, R. (1986) Fibroblasts promote the formation of a continuous basal lamina during myogenesis in vitro.Journal of Cell Biology 102, 740–47.

    Google Scholar 

  • Sauer, F. C. (1935) Mitosis in the neural tube.Journal of Comparative Neurology 62, 377–405.

    Google Scholar 

  • Seymour, R. M. &Berry, M. (1974) Scanning and transmission electron microscope studies of interkinetic nuclear migration in the cerebral vesicles of the rat.Journal of Comparative Neurology 160, 105–26.

    Google Scholar 

  • Sievers, J., Mangold, U., Berry, M., Allen, C. &Schlossberger, H. G. (1981) Experimental studies on cerebellar foliation. I. A qualitative morphological analysis of cerebellar foliation defects after neonatal treatment with 6-OHDA in the rat.Journal of Comparative Neurology 203, 751–69.

    Google Scholar 

  • Sievers, J., Mangold, U. &Berry, M. (1983) 6-OHDA-induced ectopia of external granule cells in the subarachnoid space covering the cerebellum. Genesis and topography.Cell and Tissue Research 230, 309–36.

    Google Scholar 

  • Sievers, J., Pehlemann, F. W., Baumgarten, H. G. &Berry, M. (1985) Selective destruction of meningeal cells by 6-hydroxydopamine (6-OHDA) as a tool to study meningeal-neuroepithelium interaction in brain development.Developmental Biology 110, 127–35.

    Google Scholar 

  • Sievers, J., Pehlemann, F. W., &Berry, M. (1986a) Influences of meningeal cells on brain development: findings and hypothesis.Naturwissenschaften 73, 188–94.

    Google Scholar 

  • Sievers, J., V. Knebel Doeberitz, Ch., Pehlemann, F. W. &Berry, M. (1986b) Meningeal cells influence cerebellar development over a critical period.Anatomy and Embryology 175, 91–100.

    Google Scholar 

  • Sievers, J., Hartmann, D., Gude, S., Pehlemann, F. W. &Berry, M. (1987) Influences of meningeal cells on the development of the brain. InMesenchymal-Epithelial Interactions in Neural Development (edited byWolff, J. R., Sievers, J. &Berry, M.) pp. 171–88. Berlin: Springer.

    Google Scholar 

  • Sievers, J., Hartmann, D., Pehlemann, F. W. &Berry, M. (1992) Development of astroglial cells in the proliferative matrices, the granule cell layer, and the hippocampal fissure of the hamster dentate gyrus.Journal of Comparative Neurology 320, 1–32.

    Google Scholar 

  • Sievers, J., Pehlemann, F. W., Gude, S., Hartmann, D. &Berry, M. (1994a) The development of the radial glial scaffold of the cerebellar cortex is related to the presence of GFAP-positive cells in the external granular layer.Journal of Neurocytology 23, 97–115.

    Google Scholar 

  • Sievers, J., Pehlemann, F. W., Gude, S. &Berry, M. (1994b) A time course study of the alterations in the development of the hamster cerebellar cortex after destruction of the overlying meningeal cells with 6-hydroxydopamine on the day of birth.Journal of Neurocytology 23, 117–134

    Google Scholar 

  • Trelstad, R. (1984)The role of extracellular matrix in development. New York: Alan R. Liss.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sievers, J., Pehlemann, F.W., Gude, S. et al. Meningeal cells organize the superficial glia limitans of the cerebellum and produce components of both the interstitial matrix and the basement membrane. J Neurocytol 23, 135–149 (1994). https://doi.org/10.1007/BF01183867

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01183867

Keywords

Navigation