Pelvic plexus contributes ganglion cells to the hindgut enteric nervous system

Abstract

The hindgut enteric nervous system (ENS) contains cells originating from vagal and sacral neural crest. In avians, the sacral crest gives rise to the nerve of Remak (NoR) and pelvic plexus. Whereas the NoR has been suggested to serve as the source of sacral crest-derived cells to the gut, the contribution of the pelvic ganglia is unknown. The purpose of this study was to test the hypothesis that the pelvic ganglia contribute ganglion cells to the hindgut ENS. We observed that the quail pelvic plexus develops from neural crest-derived cells that aggregate around the cloaca at embryonic day 5. Using chick-quail tissue recombinations, we found that hindgut grafts did not contain enteric ganglia unless the pelvic plexus was included. Neurofibers extended from the NoR into the intestine, but no ganglion cell contribution from the NoR was identified. These results demonstrate that the pelvic plexus, and not the NoR, serves as the staging area for sacral crest-derived cells to enter the avian hindgut, confirming the evolutionary conservation of this important embryologic process. Developmental Dynamics 236:73-83, 2007.

Dual origin of enteric neurons in vagal Schwann cell precursors and the sympathetic neural crest

“…5). Given that thoracic crest will produce enteric neurons when transposed rostrally (32) and, more generally, that neural crest cells are not specified before migration (33,34), the restriction of the dual sympatho-enteric fate to the cervical and sacral levels of the trunk crest is likely to stem, less from cell-intrinsic fate restriction than from topological factors, such as the continuity of the peri-aortic and foregut mesenchymes at one end, and the contiguity of the pelvic ganglion-a "staging site" for the enteric sacral crest (30,35)-to the rectum at the other end.…”

Analysis of the Sacral Neural Crest Cell Contribution to the Hindgut Enteric Nervous System in the Mouse Embryo

“…29,33 In quail-chick chimeric grafting studies, sacral NCCs were found within nerve fiber tracts derived from the nerve of Remak that penetrated the wall of the colorectum at the level of the myenteric plexus. 5,8,34 Therefore, the migration of sacral NCCs in the hindgut is likely to be under the guidance of nerve fibers extending from pelvic ganglia. In contrast, the formation of neuronal processes always lags behind the migration front of vagal NCCs in the hindgut (Young et al 35 ; our unpublished observations).…”

Sonic hedgehog controls enteric nervous system development by patterning the extracellular matrix

“…For Shh immunostaining, guts were fixed in Histochoice (EMS). Cryosections and wholemounts were stained using the primary antibodies listed in Table S1 as described (Nagy et al, 2007). Fluorescent secondary antibodies included Alexa Fluor 594 (goat anti-mouse IgG, IgM and IgG1), Alexa Fluor 488 goat anti-mouse IgG2a, and Alexa Fluor 546 goat anti-rabbit IgG (all Molecular Probes; 1:1000).…”

“…In the developing hindgut, vagal crest-derived cells join neural crest cells originating from the sacral level of the neural tube to form the ENS (Burns and Le Douarin, 1998;Nagy et al, 2007Nagy et al, , 2012. The ENS consists of two ganglionated plexuses, myenteric and submucosal, which are composed of multiple types of neurons and glia arranged as concentric rings and are responsible for regulating the function of the gut, including peristalsis.…”