Colonization of the bowel by neural crest-derived cells re-migrating from foregut backtransplanted to vagal or sacral regions of host embryos.
The enteric nervous system (ENS) in avian embryos is formed by cells that migrate to the bowel from vagal and sacral regions of the neural crest. Experiments were carried out to evaluate the developmental potential of crest-derived cells at the time they colonize the gut. Backtransplantation of E4 quail foregut (or control aneuronal hindgut) was used to determine whether crest-derived cells that have previously colonized the bowel are capable of following defined neural crest migration pathways in host embryos. Vagal and sacral, but not truncal, backgrafts provided donor cells for the host's bowel. These cells were immunostained by the neural crest marker, NC-1, restricted to the ENS, and appeared only when foregut was backgrafted; therefore, they were crest-derived. In order for cells to migrate to the host's bowel, backgrafts evidently had to be located in the vicinity of the neuraxis at the time crest-derived cells exited from them. When vagal grafts moved away from the neuraxis, crest-derived donor cells colonized cephalic ganglia and the vagus nerves near the grafts; however, such cells did not migrate down the vagi to the host's gut. Sacral backgrafts provided crest-derived cells for the bowel only if the donor gut was transplanted prior to the formation of somite 28, at the level of the disappearing primitive streak. Cells from vagal backgrafts were capable of reaching the host's cloaca, but backgrafts placed at a sacral level colonized only the post-umbilical bowel. In addition, donor cells proliferated extensively within the host's gut. Whenever the host's gut was colonized, donor crest-derived cells were also found in non-enteric targets including nerves, cephalic (vagal backgrafts), or sympathetic (sacral backgrafts) ganglia; however, donor cells did not form ectomesenchyme or melanocytes. These data suggest that (i) crest-derived cells that have colonized the bowel remain capable of re-migrating and following defined neural crest migration pathways in host embryos; (ii) remigrating cells must enter these pathways at their start; (iii) the gut stimulates the proliferation of enteric crest-derived cells; (iv) vagal crest-derived cells can follow sacral pathways to reach enteric, Remak's, or sympathetic ganglia; and (v) the migration of crest-derived cells within the gut is determined more by the route they follow to reach the bowel than by their level of origin in the neural crest.
Rothman
T P
TP
Department of Anatomy and Cell Biology, Columbia University, College of Physicians and Surgeons, New York, New York 10032.
Le Douarin
N M
NM
Fontaine-Pérus
J C
JC
Gershon
M D
MD
D000818:Animals; D002454:Cell Differentiation / Q000502:physiology; D002465:Cell Movement / Q000502:physiology; D002642:Chick Embryo; D003370:Coturnix / Q000196:embryology; D017615:Enteric Nervous System / Q000196:embryology*; D007422:Intestines / Q000196:embryology* / Q000294:innervation; D009432:Neural Crest / Q000166:cytology* / Q000502:physiology; D012445:Sacrococcygeal Region / Q000196:embryology; D014630:Vagus Nerve / Q000166:cytology / Q000196:embryology