Development of the monoaminergic innervation of the avian gut: transient and permanent expression of phenotypic markers.
Specific cellular accumulation of [3H]5-hydroxytryptamine ([3H]5-HT) occurs during development of the avian gut. This accumulation is transient in extraganglionic mesenchymal cells (TES cells) but is a permanent characteristic of enteric serotonergic neurons (ESN). Species-specific differences were found in the location of TES cells and ESN. In chicks TES cells surrounded myenteric ganglia and ESN were restricted to the myenteric plexus. In quails TES cells surrounded submucosal ganglia and [3H]5-HT-labeled submucosal as well as myenteric neurons. [3H]Norepinephrine accumulated only in noradrenergic terminals and not in TES cells or ESN. The origins of TES cells and ESN were studied in chimeras, in which neuraxis from appropriate or inappropriate axial levels was grafted from quail to chick. Both types of chimeric bowel contained TES cells and ESN. Most TES cells in chimeras were chick in origin and distributed as in chicks (around myenteric ganglia); however, some TES cells and all ESN were quail cells. To test whether crest cells are required for development of TES cells and ESN, aneuronal chick hindgut was explanted and grown alone, or with quail neuraxis, as chorioallantoic membrane (CAM) grafts. TES cells appeared in CAM grafts whether or not crest cells were present; however ESN only appeared in explants when quail neuraxis was included. In addition, an ectopic [3H]5-HT-labeled chromaffin-like cell, also of quail origin, was found in enteric plexuses in these combined explants of crest and gut. Most TES cells, therefore, are neither derived from nor dependent on the presence of crest cells in the gut wall. Since even an inappropriate axial level of crest was found to produce ESN when it was experimentally induced to colonize the bowel the enteric microenvironment probably plays a critical role in serotonergic neural development. The species-specific location of TES cells and ESN is consistent with the hypothesis that TES cells constitute an important component of this microenvironment.
D000818:Animals; D002642:Chick Embryo; D002678:Chimera; D003370:Coturnix / Q000196:embryology; D005724:Ganglia / Q000196:embryology / Q000502:physiology; D007422:Intestines / Q000196:embryology / Q000294:innervation*; D008854:Microscopy, Electron; D009197:Myenteric Plexus / Q000196:embryology*; D009432:Neural Crest / Q000502:physiology*; D009638:Norepinephrine / Q000502:physiology; D012701:Serotonin / Q000502:physiology*
D012701:Serotonin; D009638:Norepinephrine