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Journal of Neuroscience, Vol 11, 3928-3942, Copyright © 1991 by Society for Neuroscience
Changes in the distribution of extracellular matrix components accompany early morphogenetic events of mammalian cortical development
AM Sheppard, SK Hamilton and AL Pearlman
Department of Cell Biology, Washington University School of Medicine, St. Louis, Missouri 63110.
As a step in defining the molecular environment for development of the
mammalian cerebral cortex, we have used immunohistochemistry to analyze the
distribution and remodeling of three major extracellular matrix (ECM)
components, fibronectin, chondroitin sulfate proteoglycan (CSPG), and
tenascin, during embryonic and early postnatal stages in the mouse.
Fibronectin and CSPG are distributed throughout the proliferative zone that
initially comprises the thin wall of the telencephalic vesicle, but their
distribution changes as newly generated cells form the preplate just
beneath the pia. Immunolabeling for CSPG becomes most prominent in the
preplate, and fibronectin becomes restricted to that layer. Just after this
change occurs, processes of preplate neurons, visualized with antibodies to
neurofilaments, become evident within the matrix-rich preplate zone. The
association of fibronectin and CSPG with preplate cells persists as
cortical plate neurons divide the preplate; both ECM components are now
most prominent in the marginal zone and subplate, the layers above and
below the cortical plate that are preplate derived. Within the preplate and
its derivatives, immunolabeling of fibronectin is punctate and closely
associated with radial glial processes, while labeling of CSPG is more
intense and diffuse. Labeling of fibronectin and CSPG declines rapidly as
the cortical plate begins to differentiate into cortex; labeling for
tenascin first appears at this stage in the most mature layers, the
marginal zone and subplate, then gradually becomes widespread throughout
all of cortex and subcortical white matter. In early postnatal life,
tenascin is eliminated from the hollows of the vibrissal barrels in the
somatosensory region; it then declines rapidly throughout cortex. The
association of both fibronectin and CSPG with preplate cells and the
distribution of fibronectin along radial glia during early cortical
development suggest that one or both of these transient cell types might
produce specific ECM components or induce their local deposition. The
spatial and temporal distribution of fibronectin and CSPG suggests a role
in defining a destination for migrating neurons that form the cortical
plate and in delineating the pathway for early axonal extension. In
contrast, the relatively late appearance of tenascin correlates best with
the formation of astrocytes and their processes rather than with the
establishment of cortical layers or major axonal pathways. These events are
well underway before labeling of tenascin is evident.
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