Tenascin protein and mRNA in the avian visual system: distribution and potential contribution to retinotectal development.

The large glycoprotein tenascin is one of the extracellular matrix proteins that is abundant in the developing nervous system. To determine its distribution and possible role in the ontogenty of the avian retinotectal system, the distribution of the protein, the expression of its mRNA, and the effect of the protein on growing retinal neurites in vitro was investigated. Immunocytochemistry demonstrated that relatively little tenascin was present in the optic fiber layer of the retina, the optic nerve and tract. Tenascin, however, was abundant in the stratum opticum of the tectum, the target of retinal axons in the brain. Whereas tenascin protein is found only in discrete portions and layers of the brain, in situ hybridization studies showed that tenascin mRNA was expressed throughout development by radial glial cells at the ventricular surfaces of the brain, distant from the tissue localization of the protein. Injection of antitenascin antiserum into the tectal ventricle disturbed the distribution of the protein in the tectum by binding tenascin closer to its origin at the ventricular border. This suggests that the localization of tenascin in the brain is not restricted to its site of synthesis, but is mediated by tenascin-binding proteins that are expressed in defined areas and layers in the brain. In vitro studies showed that tenascin did not promote neurite outgrowth of retinal axons. On the contrary, the addition of tenascin to retinal explants growing on collagen or on L1 slowed the growth rate of optic axons by as much as 50%. The inhibitory function in vitro suggests that this protein has a modulatory role in axonal growth in vivo. The absence of tenascin from the optic fiber layer of retina, optic nerve, and optic tract and its abundance in the tectum suggest that tenascin may function to slow the rapidly growing optic nerve fibers once they arrive at the tectum. The slowing of optic fiber outgrowth may then facilitate terminal arborization and synapse formation within the tectum. The abundant tenascin in synaptic layers may also serve to stabilize synapses once they have formed.