Abstract
Most epithelia are unable to develop in the absence of their surroundings mesenchyme, and the latter influences such fundamental events in epithelial development as cell proliferation, branching morphogenesis and functional differentiation (reviews in Grobstein, 1955; Wessells, 1977; Bernfield and Banerjee, 1978; Hay, 1981, 1984; Cunha et al., 1983; Bernfield et al., 1984). Already the earliest stages of neural development, i.e., the formation of the neural plate in the dorsal ectoderm of the gastrula, are induced by the underlying mesoderm (reviews in Spemann, 1938; Jacobson, 1984). In the spinal cord this neural induction is followed by a series of tissue interactions between neural plate and neural tube on the one hand and the adjacent chorda dorsalis and the somites on the other hand which result in the characteristic shape of the developing spinal cord (see van Straaten and Drukker, this volume). Little is known about similar influences on the development of the brain, yet the mesenchymal partner in such tissue interactions would be the meninges, and the occurrence and significance of a postulated mesenchymal-epithelial interaction during brain development can be assessed if the meningeal cells are eliminated in different stages of CNS ontogeny. In this article we will summarize the evidence collected in our laboratories over the last few years on the influences of meningeal cells on brain development, which we have obtained utilizing a pharmocological method for the selective destruction of meningeal cells. These findings show that in addition to secreting as yet unidentified, probably diffusible molecules stimulating cell proliferation (see Gensburger et al., and Pehlemann et al. this volume), the meningeal cells stabilize the external surface of the cerebellum and hippocampus by producing components of both the interstitial matrix and the basal lamina and thus form the foundation of the radial glial scaffold presenr in these regions which, is involved in establishing the pattern of folia and laminae by guiding neuronal migration.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Alitalo, K. (1980) Production of both interstitial and basement membrane procollagens by fibroblastic Wi 38 cells from human embryonic lung. Biochem. Biophys. Res. Commun. 93: 873–880.
Allen, C., J. Sievers, M. Berry, and S. Jenner (1981) Experimental studies on cerebellar foliation. II. A morphometric analysis of cerebellar fissuration defects and growth retardation after neonatal treatment with 6-OHDA in the rat. J. Comp. Neurol. 202: 771–784.
Bernfield, M.R., and S.D. Banerjee (1978) The basal lamina in epithelial-mesenchymal morphogenetic interactions. In Biology and Chemistry of Basement Membranes, N.A. Kefalides, ed., pp. 137–148. Academic Press, New York. Bernfield, M.R., S.D. Banerjee, J.E. Koda, and A.C. Rapraeger (1984) Remodeling of the basement membrane as a mechanism of morphogenetic tissue interaction. In The role of extracellular matrix in development, R. Trelstad, ed., pp. 545–572. Alan R.Liss, New York.
Boke, R., and J. Sievers (1986) Effects of the noradrenergic neurotoxic DSP4 on the development of the locus coeruleus and the cerebellum. In preparation.
Bönisch, H. (1980) Extraneuronal transport of catecholamines. Pharmacology. 21: 93–108.
Braak, H. (1974) On the intermediate cells of Lugaro within the cerebellar cortex of man. Cell Tissue Res. 149: 399–411.
Cunha, G.R., L.W.K. Chung, J.M. Shannon, O. Taguchi, and H. Fujii (1983) Hormone- induced morphogenesis and growth: Role of mesenchymal-epithelial interactions. Ree. Prog. Hormone Res. 39: 559–398.
Grobstein, C. (1955) Tissue interaction in the morphogenesis of mouse embryonic rudiments in vitro. In Aspects of Synthesis and Order in Growth, D. Rudnick, et., pp. 233–256. Princeton University Press, Princeton.
Grobstein, C., and J. Cohen (1965) Collagenase: Effect on the morphosgenesis of embry¬onic salivary epithelium in vitro. Science 150: 626–628.
Gude, S., J. Burmester, J. Sievers, and F.W. Pehlemann (1986) Meningeal cells synthesize components of both the interstitial matrix and the basal lamina at the surface of the brain. In preparation.
Hartmann, D., J. Sievers, and F.W. Pehlemann (1986a) Die Zerstörung der Meningeal- zellen über dem medialen cerebralen Cortex neugeborener Hamster verhindert die Bildung des infrapyramidalen Blattes des Gyrus dentatus. Anat. Anz.161: 136.
Hartmann, D., J. Sievers, and F.W. Pehlemann (1986b) Die Entwicklung des Gyrus dentatus nach Zerstörung der Meningealzellen: Analyse der Zellwanderung und des Gliagerüstes. Anat. Anz (Erg.-H.), in press.
Hausmann, B., and J. Sievers (1985) Cerebellar external granule cells are attached to the basal lamina from the onset of migration up to the end of their proliferative activity. J. Comp. Neurol. 241: 50–62.
Hay, E.D. (1981) Collagen and embryonic development. In Cell Biology of Extracellular Matrix, E.D. Hay, ed., pp. 379–409. Plenum, New York.
Hay, E.D. (1984) Cell-matrix interaction in the embryo: Cell shape, cell surface, cell skeletons, and their role in differentiation. In The Role of Extracellular Matrix in Development, R. Trelstad, ed., pp. 1–31. Alan R. Liss, New York.
Iversen, L.L. (1975) Uptake processes for biogenic amines. In Handbook of Psychophar- macology, L.L. Iversen, S.D. Iversen, and S.H. Snyder, eds., pp. 96–117, vol. J. Plenum, New York.
Jacobson, M. (1984) Cell lineage analysis of neural induction: Origins of cells forming the induced nervous system. Dev. Biol. 102: 122–129.
Jonsson, G. (1980) Chemical neurotoxins as denervation tools in neurobiology. Ann. Rev. Neurosci. 3: 169–187.
Jonsson, G., H. Hallmann, and E. Sundström (1982) Effects of the noradrenaline neurotoxin DSP4 on the postnatal development of central noradrenaline neurons in the rat. Neuroscience 7: 2895–2907.
Kaplan, G.P., B.K. Hartmann, and C.R. Creveling (1979) Immunhistochemical demonstration of catechol-O-methyltransferase in mammalian brain. Brain Res. 167: 41–52.
Kaplan, G.P., B.K. Hartmann, and C.R. Creveling (1981) Localization of catechol-O- methyltransferase in the leptomeninges, choroid plexus and ciliary epithelium: Implications for the separation of central and peripheral catechols. Brain Res. 204: 353–360.
von Knebel Doeberitz, Ch., J. Sievers, M. Sadler, F.-W. Pehlemann, M. Berry, and P. Halliwell (1986) Destruction of meningeal cells over the newborn hamster cerebellum with 6-hydroxydopamine prevents foliation and lamination in the rostral cerebellum. Neuroscience 17: 409–426.
Kühl, U., R. Timpl, and K. v.d. Mark (1982) Synthesis of type IV collagen and laminin in cultures of skeletal muscle cells and their assembly on the surface of myotubes. Dev. Biol. 93: 344–354.
Kühl, U., M. Öchalan, R. Timpl, R. Mayne, E. Hay, and K. v.d. Mark (1984) Role of muscle fibroblasts in the deposition of type IV collagen in the basal lamina of myotubes. Differentiation 28: 164–172.
Lidov, H.G.W., and M.E. Molliver (1982) The structure of cerebral cortex in the rat following prenatal administration of 6-hydroxydopamine. Dev. Brain Res. 3: 81–108.
Pehlemann, F.W., J. Sie vers, and M. Berry (1985) Meningeal cells are involved in folia¬tion, lamination and neurogenesis of the cerebellum: Evidence from 6-hydroxy- dopamine-induced destruction of meningeal cells. Dev. Biol. 110: 136–146.
Pehlemann, F.W., and J. Sievers (1986) Die Transplantation fetaler Meningealzellen auf das Kleinhirn neugeborener Ratten verringert das Auftreten 6-OHDA-induzierter Veränderungen der Schichtenbildung. Anat. Anz. 161: 154–155.
Rakic, P. (1971) Neuron-glia relationship during granule cell migration in developing cerebellar cortex: A Golgi and electron microscopic study in Macacus rhesus. J. Comp. Neurol. 141: 283–312.
Rakic, P. (1982) The role of neuronal-glial cell interaction during brain development. In Neuronal-glial Cell I interrelationships, T.A. Sears, ed., pp. 25–38. Springer, Heidelberg and New York.
Sanderson, R.D., J.M. Fitch, T.R. Linsenmayer, and R. Mayne (1986) Fibroblasts promote the formation of a continuous basal lamina during myogenesis in vitro. J. Cell Biol. 102: 740–747.
Sievers, 3., H.P. Klemm, S. Jenner, H.G. Baumgarten, and M. Berry (1980) Neuronal and extraneuronal effects of intracisternally administered 6-hydroxydopamine on the developing rat brain. J. Neurochem. 34: 765–771.
Sievers, J., U. Mangold, M. Berry, C. Allen, and H.G. Schlossberger (1981) Experimental studies on cerebellar foliation. I. A qualitative morphological analysis of cerebellar fissuration defects after neonatal treatment with 6-OHDA in the rat. J. Comp. Neurol. 203: 751–769.
Sievers, H., J. Sievers, H.G. Baumgarten, N. König, and H.G. Schlossberger (1983a) Distribution of tritium label in the neonate rat brain following intracisternal or subcutaneous administration of -OHDA. An autoradiographic study. Brain Res. 275: 23–45.
Sievers, J., U. Mangold, and M. Berry (1983b) 6-OHDA-induced ecotopia of external granule cells in the subarachnoid space covering the cerbellum. Genesis and topography. Cell Tissue Res. 230: 309–336.
Sievers, J., F.-W. Pehlemann, H.G. Baumgarten, and M. Berry (1985) Selective destruction of meningeal cells by 6-hydroxydopamine: A tool to study meningeal-neuroepithelial interaction in brain development. Dev. Biol. 110: 127–135.
Sievers, J., F.-W. Pehlemann, and M. Berry (1986a) Influences of meningeal cells on brain development: Findings and hypothesis. Naturwissenschaften 73: 8 8–194.
Sievers, J., Ch. von Knebel Doeberitz, F.W. Pehlemann, and M. Berry (1986b) Meningeal cells influence cerebellar development over a critical period. Anat. Embryol., in press,.
Spemann, H. (1938) Experimentelle Beiträge zu einer Theorie der Entwicklung. Springer, Berlin.
Spooner, B.R., and J.M. Faubion (1980) Collagen involvement in branching morphogenesis of embryonic lung and salivary gland. Dev. Biol. 77: 84–102.
Wessells, N.K. (1977) Tissue Interactions and Development. Benjamin, New York.
Wessells, N.K., and J.A. Cohen (1968) Effects of collagenase on developing epithelia in vitro: Lung, ureteric bud, and pancreas. Dev. Biol. 18: 294–309.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1987 Springer-Verlag Berlin Heidelberg
About this paper
Cite this paper
Sievers, J., Hartmann, D., Gude, S., Pehlemann, F.W., Berry, M. (1987). Influences of Meningeal Cells on the Development of the Brain. In: Wolff, J.R., Sievers, J., Berry, M. (eds) Mesenchymal-Epithelial Interactions in Neural Development. NATO ASI Series, vol 5. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-71837-3_15
Download citation
DOI: https://doi.org/10.1007/978-3-642-71837-3_15
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-71839-7
Online ISBN: 978-3-642-71837-3
eBook Packages: Springer Book Archive