Enteric nervous system development: Analysis of the selective developmental potentialities of vagal and sacral neural crest cells using quail-chick chimeras
Aj. Burns et Nm. Le Douarin, Enteric nervous system development: Analysis of the selective developmental potentialities of vagal and sacral neural crest cells using quail-chick chimeras, ANAT REC, 262(1), 2001, pp. 16-28
The majority of the enteric nervous system (ENS) is derived from vagal neur
al crest cells (NCC). For many years, the contribution from a second region
of the neuraxis (the sacral neural crest) to the ENS has been less clear,
with conflicting reports appearing in the literature. To resolve this longs
tanding issue, we documented the spatiotemporal migration and differentiati
on of vagal and sacral-derived NCC within the developing chick embryo using
quail-chick grafting: and antibody labelling. Results showed that vagal NC
C colonised the entire length of the gut in a rostrocaudal direction. The h
indgut, the region of the gastrointestinal tract most frequently affected i
n developmental disorders, was found to be colonised in a complex manner. V
agal NCC initially migrated within the submucosa, interval to the circular
muscle layer, before colonising the myenteric plexus region. In contrast, s
acral NCC, which colonised the hindgut in a caudorostral direction, were pr
imarily located in the myenteric plexus region from where they subsequently
migrated to the submucosa. We also observed that sacral NCC migrated into
the hindgut in significant numbers only after vagal-derived cells had colon
ised the entire length of the gut. This suggested that to participate in EN
S formation, sacral cells may require an interaction with vagal-derived cel
ls, or with factors or signalling molecules released by them or their proge
ny. To investigate this possible inter-relationship, we ablated sections of
vagal neural crest (NC) to prevent the rostrocaudal migration of ENS precu
rsors and, thus, create an aganglionic hindgut model. In the same NC ablate
d animals, quail-chick sacral NC grafts were performed. In the absence of v
agal-derived ganglia, sacral NCC migrated and differentiated in an apparent
ly normal manner. Although the numbers of sacral cells within the hindgut w
as slightly higher in the absence of vagal-derived cells, the increase was
not sufficient to compensate for the lack of enteric ganglia. As vagal NCC
appear to be more invasive than sacral NCC, since they colonise the entire
length of the gut, we investigated the ability of transplanted vagal cells
to colonise the hindgut by grafting the vagal NC into the sacral region. We
found that when transplanted, vagal cells retained their invasive capacity
and migrated into the hindgut in large numbers. Although sacral-derived ce
lls normally contribute a relatively small number of precursors to the post
-umbilical gut, many heterotopic vagal cells were found within the hindgut
enteric plexuses at; much earlier stages of development than normal. Hetero
topic grafting of invasive vagal NCC into the sacral neuraxis may, therefor
e, be a means of rescuing an aganglionic hindgut phenotype. Anat Rec 262:16
-28, 2001. (C) 2001 Wiley-Liss, Inc.