Influence of Meningeal Cells on Cell Proliferation in the Cerebellum
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Meningeal cells participate in the development of the cerebellum both by stabilizing the extracellular matrix of the pial surface and by organizing the radial glial scaffold and the lamination of the cerebellar cortex. In the present study we investigated possible influences of meningeal cells on the development of the dentate gyrus, whose ontogenesis has many similarities to that of the cerebellum. Meningeal cells were selectively destroyed by injecting newborn hamsters with 25 micrograms 6-hydroxydopamine (6-OHDA) into the interhemispheric fissure. Twenty-four hours postinjection (p.i.) the meningeal cells over the medial cerebral hemispheres were completely destroyed. Thirty days p.i. the infrapyramidal blade of the dentate gyrus was almost completely missing, while the suprapyramidal blade was hypertrophied, extending with its medial tip almost up to the medial surface of the cortex. In order to ascertain that this maldevelopment was caused by the destruction of meningeal cells, another group of hamsters was pretreated with normetanephrine (NMN) which inhibits the extraneuronal uptake of 6-OHDA into meningeal cells. In this group the meningeal cells were unaffected by the treatment, and the morphology of the dentate gyrus was normal 30 days p.i. of 6-OHDA plus NMN. When the meningeal cells were destroyed in later stages of development (postnatal days 1-5), alterations of the dentate gyrus could be induced only up to the fourth postnatal day; thereafter, 6-OHDA treatment left it unchanged. This indicates a critical period of meningeal cell influence that coincides with the period of existence of the subpial dentate matrix. Analysis of the time course of the defective development revealed that in the first 5 days p.i. 1) meningeal cells over the medial cerebral hemisphere were destroyed and removed, 2) the pial basement membrane over both the dentate anlage and the diencephalon thinned and ruptured, and the adjacent brain parts fused focally, 3) many cells of the subpial dentate matrix disappeared from their subsurface position, 4) the number of "immature" cells increased in the hilus and the subgranular zone of the suprapyramidal blade, 5) the suprapyramidal blade elongated and thickened considerably, while the infrapyramidal blade did not form. Beyond 5 days p.i. those parts of the pial surface of the dentate anlage that had not fused with the diencephalon were repopulated with meningeal cells. This reappearance of meningeal cells was accompanied by 1) the restitution of the normal morphology of the basement membrane, 2) the reappearance of neuronal and glial cells below the pial surface, and 3) the formation of fragments of the infrapyramidal blade which later developed a normal appearing lamination.(ABSTRACT TRUNCATED AT 400 WORDS)
Meningeal cells participate in the development of the cerebellum both by stabilizing the extracellular matrix of the pial surface and by organizing the radial glial scaffold and the lamination of the cerebellar cortex. In the present study we investigated possible influences of meningeal cells on the development of the dentate gyrus, whose ontogenesis has many similarities to that of the cerebellum. Meningeal cells were selectively destroyed by injecting newborn hamsters with 25 micrograms 6-hydroxydopamine (6-OHDA) into the interhemispheric fissure. Twenty-four hours postinjection (p.i.) the meningeal cells over the medial cerebral hemispheres were completely destroyed. Thirty days p.i. the infrapyramidal blade of the dentate gyrus was almost completely missing, while the suprapyramidal blade was hypertrophied, extending with its medial tip almost up to the medial surface of the cortex. In order to ascertain that this maldevelopment was caused by the destruction of meningeal cells, another group of hamsters was pretreated with normetanephrine (NMN) which inhibits the extraneuronal uptake of 6-OHDA into meningeal cells. In this group the meningeal cells were unaffected by the treatment, and the morphology of the dentate gyrus was normal 30 days p.i. of 6-OHDA plus NMN. When the meningeal cells were destroyed in later stages of development (postnatal days 1-5), alterations of the dentate gyrus could be induced only up to the fourth postnatal day; thereafter, 6-OHDA treatment left it unchanged. This indicates a critical period of meningeal cell influence that coincides with the period of existence of the subpial dentate matrix. Analysis of the time course of the defective development revealed that in the first 5 days p.i. 1) meningeal cells over the medial cerebral hemisphere were destroyed and removed, 2) the pial basement membrane over both the dentate anlage and the diencephalon thinned and ruptured, and the adjacent brain parts fused focally, 3) many cells of the subpial dentate matrix disappeared from their subsurface position, 4) the number of "immature" cells increased in the hilus and the subgranular zone of the suprapyramidal blade, 5) the suprapyramidal blade elongated and thickened considerably, while the infrapyramidal blade did not form. Beyond 5 days p.i. those parts of the pial surface of the dentate anlage that had not fused with the diencephalon were repopulated with meningeal cells. This reappearance of meningeal cells was accompanied by 1) the restitution of the normal morphology of the basement membrane, 2) the reappearance of neuronal and glial cells below the pial surface, and 3) the formation of fragments of the infrapyramidal blade which later developed a normal appearing lamination.(ABSTRACT TRUNCATED AT 400 WORDS)
This study is a chronological analysis of 6-hydroxydopamine-induced alterations in development of the hamster cerebellar cortex. This treatment destroys the overlying meningeal cells, the sequelae of which include (i) a thinning of the external granular layer over the folial apices and a thickening in the region of the prospective fissures, reflecting a retardation of the growth of the cerebellar cortex, accompanied by displacement of the normally superficialmost GFAP-positive external granular layer cells into deeper parts of the external granular layer; (ii) a retardation of multiplication of Golgi epithelial cells which colonize the rostral third of the Purkinje cell layer so that their numbers decrease in the rostralmost folia; (iii) disturbed morphological and biochemical differentiation of the Golgi epithelial cells and their processes, the growing radial Bergmann glial fibres which detach from the pial surface and branch within the external granular layer, causing a failure in endfeet formation at the superficial glia limitans, loss of characteristic radial morphology, with the adoption of a multipolar form, and normal or increased GFAP expression and decreased S-100 expression; (iv) fragmentation of the external granular layer beyond P5 to P7 with loss of the regular lamination and foliation of the cerebellar cortex, characterized by a completely random distribution of fragments of Purkinje cell layer, molecular zone and internal granular layer. We conclude that the destruction of meningeal cells interferes with the establishment and stabilization of both the external granular layer and the secondary radial glial scaffold composed of Golgi epithelial cells, whose proliferation, growth and differentiation is subsequently disturbed. The failure to stabilize the external granular layer and to form a normal secondary radial glial scaffold is, in turn, responsible for the disruption of the regular laminar deposition of the neurons of the cerebellar cortex.
We have used the quail-chick chimera system to reveal the cell migrations and settling pattern involved in the construction of the cerebellum. Three types of orthotopic transplantations were carried out, between quail and chick embryos, at the 12-somite stage: exchanges of (i) the whole metencephalic vesicle, (ii) the lateral half of this vesicle and (iii) the diencephalic plus the mesencephalic vesicles. Histological study of chimeric embryos and young chicks provided the following results: longitudinal morphogenetic movements distort the embryonic neural tube as early as the fifth embryonic day, so that the dorsal limit of the mes-, met- and myelencephalic vesicles are displaced caudad and their ventral limits rostrad. This leads to a participation of mesencephalic vesicular material in the construction of the cerebellum. Cells originating in the mesencephalic vesicle are found in a rostromedial V-shaped region, in all the cerebellar cellular layers, except the external granular layer, the presumptive territory of which is entirely located in the metencephalic vesicle. The chimerism of the rostromedial part of the cerebellum allows the analysis of the origin of the various cerebellar cell types. We find (i) that the Purkinje cells always have the same cellular marker as the ventricular epithelium radially beneath them. This strongly suggests that these cells reach their final localization following strictly radial migrations. (ii) Most of the small cells surrounding the Purkinje neurons and most of the neurons and glial cells of the molecular layer are also of the same type as the ventricular epithelium they surmount, i.e. different from the type of the external granular layer cells. Therefore, they are not derived from the external granular layer and are not of the same origin as the granule cells as previously believed. Unilateral substitutions of the metencephalic vesicle revealed that transverse cell migrations occur across the sagittal plane. They have been observed mainly in the inner and external granular layers, but also, though to a lesser extent, in the molecular layer and in the cell layer located at the level of the Purkinje neurons. These observations show that the position of cerebellar cells is determined by both morphogenetic movements and cell type-specific active radial and tangential migrations. The quail-chick chimera system is thus able to provide new information both on the origin of cerebellar cells and how each cell type assumes its final position.
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