Division and migration of satellite glia in the embryonic rat superior cervical ganglion

A. K. Hall, S. C. Landis

While distinct precursors committed to a neuronal or glial cell fate are generated from neural crest cells early in peripheral gangliogenesis, little is known about the subsequent generation and maturation of young satellite glia from restricted glial precursor cells. To examine the division and migration of glial precursor cells and their satellite cell progeny, morphological, immunocytochemical and culture techniques were applied to the developing rat superior cervical ganglion. At embryonic day (E)18.5, numerous clusters of nonneuronal cells appeared transiently in the ganglion. Individual cells with a similar morphology were present in E16.5 ganglia, and are likely to represent the precursor cells which generate these clusters. The clustered cells were distinguishable from neighbouring neurons as well as from endothelial cells and fibroblasts. Morphologically similar cells were present in nerve bundles at E18.5 and surrounding principal neurons and nerve bundles in the adult ganglion. Double-label studies of the E18.5 ganglion with tyrosine hydroxylase to identify noradrenergic neurons and propidium iodide counterstaining to visualize all cell nuclei revealed that the cells in clusters stained with propidium iodide but lacked tyrosine hydroxylase immunoreactivity. To determine if cell clusters arose from division, bromodeoxy-uridine, a thymidine analogue, was administered to pregnant mothers between E16.5-E18.5, and ganglionic cells examined at E18.5 both in vivo and in vitro. Numerous non-neuronal cells divided during this period in situ and composed portions of clusters. When dissociated, superior cervical ganglion satellite glia reacted with an NGF-receptor antibody (MAb 217c) and possessed a flattened shape, in contrast to bipolar Schwann cells. Over half of the 217c-immunoreactive glia at E18.5 had incorporated bromodeoxyuridine during E16.5-18.5 in vivo. At birth, non-neuronal cells were no longer grouped in clusters, but were associated with neuronal cell bodies and processes. These findings suggest that, between E16.5-E18.5, glial precursors divide rapidly to form clusters, and that, after the peak of neurogenesis, daughter cells migrate within the ganglion to associate with nerve cell bodies and processes where proliferation continues at a slower rate. Distinct cellular and molecular interactions are likely to trigger the initial rapid division of glial precursors, initiate their migration and association with neuron cell bodies, and control their subsequent slower division.