Balaskas, Christos; (1997) Cellular development of the enteric nervous system in the chick embryo. Doctoral thesis (Ph.D), UCL (University College London).

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Abstract

The chemical and structural development of enteric plexuses was studied in the chick from embryonic day 4 to hatching. The enteric ganglia consist of neural crest-derived neuronal and glial cells, which can be distinguished morphologically and immunohistochemically in late developmental stages. At what stage different cell lineages originate from uncommitted precursors remains unknown. While the primordial neurons and glial cells could not be distinguished ultrastructurally from each other until E16, by means of polyclonal antibodies against GFAP and tubulin, distinct populations of neuronal and glial cells were identified from E5 in the duodenal myenteric ganglia. The enteric ganglia display a compact structure with exclusion of blood vessels and collagen, from the earliest stages investigated. A basement membrane, of unknown origin, is recognized ultrastructurally around ganglia and connecting strands from E12. The distribution of laminin, a basement membrane component, was examined by light and electron microscope immunohistochemistry; immunoreactivity was detected inside enteric ganglia, associated with glial cells, from E13 in the duodenum and from E11 in the rectum. The presence of laminin on the entire glial cell surface and probably in the cytoplasm suggests that glial cells are responsible for the production of the laminin-containing periganglionic basement membrane and that laminin is a marker of enteric glia in the chick. In addition, laminin immunolabelled the basement membranes of mesothelium, epithelium, muscle cells and endothelium. An important aspect of the functional maturation of enteric ganglia is the establishment of synapses. Synapse formation was studied by immunohistochemistry and electron microscopy. Synaptic vesicles were detected from E9, when immunoreactivity for the vesicle protein synaptophysin also appeared in ganglionic nerve endings. Because programmed cell death plays a major role in nerve tissue development, the presence of apoptotic cells in enteric ganglia, was studied using the TUNEL method and electron microscopy. The observations suggest that cell death contributes little, if at all, to the morphogenesis of the chick enteric plexuses. In other experiments, the gastrointestinal tract was excised from embryos of E5 to E8 and placed unsegmented in organ culture. The gut not only survived, but also continued to differentiate. The intramural migration of AChE positive ganglion cells into the hindgut, which is aganglionic at E5, proceeded and was completed in vitro, at the same rate as in controls. Separate populations of ganglion cells were identified by means of tubulin and GFAP immunoreactivity, but not ultrastructurally; basement membranes, visible at the ultrastructural level and as laminin immunoreactive structures developed in muscle cells, epithelium and ganglia. Synaptic contacts were established, small synaptic vesicles were visible and synaptophysin immunolabelling was also present. Submucosal ganglia contain fewer cells than myenteric ganglia in the duodenum and therefore, immunolabelling for all the antibodies was consistently less extensive or sometimes even absent. Immunoreactivities appeared in the myenteric ganglia, a day or two earlier than in the submucosal. Similar was the case in the rectum, where ganglia in both plexuses are of comparable size; laminin immunoreactivity, however, appeared earlier and was more extensive in the submucosal than in the myenteric ganglia.

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