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

Abstract

We have investigated the factors controlling both the morphological transformation of glial processes into endfeet 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 fissural 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.

Postnatal Development of the Central Nervous System: Anomalies in the Formation of Cerebellum Fissures

“…Several reports have implicated the pial basement membrane as an important player in brain development; in fact, abnormal brain development has been observed after chemical ablation of meningeal cells (Sievers et al, 1994) and after the targeted deletion of basement membrane constituents (Arikawa-Hirasawa et al, 1999;Costell et al, 1999) or deletion of receptors for basement membrane proteins (Graus-Porta et al, 2001). Damages to the pial basement membrane result in changes in radial glial cell morphology.…”

MICAL flavoprotein monooxygenases: Expression during neural development and following spinal cord injuries in the rat

“…Similarly, expression of MICAL-1, -2, and -3 is upregulated in meningeal fibroblasts that occupy the core of spinal cord scar tissue. Fibrotic scar tissue formed by meningeal fibroblasts seals off CNS tissue from the non-CNS environment following CNS injury (Abnet et al, 1991;Sievers et al, 1994). In addition, meningeal fibroblasts express several axon growth inhibitory molecules, including all Sema3s, and they are believed to constitute a non-permissive substrate for regenerative axon growth De Winter et al, 2002b;Hirsch and Bahr, 1999;Morgenstern et al, 2002;Niclou et al, 2003;Noble et al, 1984;Pasterkamp et al, 1999).…”

GPR56 Regulates Pial Basement Membrane Integrity and Cortical Lamination

“…Meningeal fibroblasts contribute to the BM by secreting and organizing the majority of basal lamina constituents (Sievers et al, 1994). The sites of ECM protein synthesis and BM assembly are spatially distinct, suggesting cell-directed mechanisms that can specify the sites of ECM assembly.…”

“…Meningeal fibroblasts contribute to the BM by secreting the majority of basal lamina constituents, including laminin, collage IV, nidogen, and the heparan sulfate proteoglycan (Sievers et al, 1994). Defective pial BM is thought to be the primary cause of cobblestone lissencephaly (Olson and Walsh, 2002).…”