|
|
|
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
Development, Vol 125, Issue 21 4335-4347, Copyright © 1998 by Company of Biologists
JOURNAL ARTICLES |
AJ Burns and NM Le Douarin
Institut d'Embryologie Cellulaire et Moleculaire, du CNRS et du College de France, Avenue de la Belle Gabrielle, France. Nicole.
The majority of the enteric nervous system is derived from vagal neural crest cells (NCC), which migrate to the developing gut, proliferate, form plexuses and differentiate into neurons and glia. However, for some time, controversy has existed as to whether cells from the sacral region of the neural crest also contribute to the enteric nervous system. The aim of this study was to investigate the spatiotemporal migration of vagal and sacral NCC within the developing gut and to determine whether the sacral neural crest contributes neurons and glia to the ENS. We utilised quail-chick chimeric grafting in conjunction with antibody labelling to identify graft-derived cells, neurons and glia. We found that vagal NCC migrated ventrally within the embryo and accumulated in the caudal branchial arches before entering the pharyngeal region and colonising the entire length of the gut in a proximodistal direction. During migration, vagal crest cells followed different pathways depending on the region of the gut being colonised. In the pre-umbilical intestine, NCC were evenly distributed throughout the splanchnopleural mesenchyme while, in the post-umbilical intestine, they occurred adjacent to the serosal epithelium. Behind this migration front, NCC became organised into the presumptive Auerbach's and Meissner's plexuses situated on either side of the developing circular muscle layer. The colorectum was found to be colonised in a complex manner. Vagal NCC initially migrated within the submucosa, internal to the circular muscle layer, before migrating outwards, adjacent to blood vessels, towards the myenteric plexus region. In contrast, sacral NCC, which also formed the entire nerve of Remak, were primarily located in the presumptive myenteric plexus region and subsequently migrated inwards towards the submucosal ganglia. Although present throughout the post-umbilical gut, sacral NCC were most numerous in the distal colorectum where they constituted up to 17% of enteric neurons, as identified by double antibody labelling using the quail-cell-specific marker, QCPN and the neuron-specific marker, ANNA-1. Sacral NCC were also immunopositive for the glial-specific antibody, GFAP, thus demonstrating that this region of the neural crest contributes neurons and glia to the enteric nervous system.
This article has been cited by other articles:
|
|
 |
|
  A. J. Barlow, A. S. Wallace, N. Thapar, and A. J. Burns Critical numbers of neural crest cells are required in the pathways from the neural tube to the foregut to ensure complete enteric nervous system formation Development, May 1, 2008; 135(9): 1681 - 1691. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Gao and R. H. Miller Specification of optic nerve oligodendrocyte precursors by retinal ganglion cell axons. J. Neurosci., July 19, 2006; 26(29): 7619 - 7628. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. A. Heanue and V. Pachnis From the Cover: Expression profiling the developing mammalian enteric nervous system identifies marker and candidate Hirschsprung disease genes PNAS, May 2, 2006; 103(18): 6919 - 6924. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. A. Eisenberg, J. B.E. Burch, and L. M. Eisenberg Bone Marrow Cells Transdifferentiate to Cardiomyocytes When Introduced into the Embryonic Heart Stem Cells, May 1, 2006; 24(5): 1236 - 1245. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Pietsch, J.-M. Delalande, B. Jakaitis, J. D. Stensby, S. Dohle, W. S. Talbot, D. W. Raible, and I. T. Shepherd lessen encodes a zebrafish trap100 required for enteric nervous system development Development, February 1, 2006; 133(3): 395 - 406. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Antonellis, W. R. Bennett, T. R. Menheniott, A. B. Prasad, S.-Q. Lee-Lin, NISC Comparative Sequencing Program, E. D. Green, D. Paisley, R. N. Kelsh, W. J. Pavan, et al. Deletion of long-range sequences at Sox10 compromises developmental expression in a mouse model of Waardenburg-Shah (WS4) syndrome Hum. Mol. Genet., January 15, 2006; 15(2): 259 - 271. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 U. Rauch, M. Klotz, S. Maas-Omlor, E. Wink, A. Hansgen, C. Hagl, S. Holland-Cunz, and K.-H. Schafer Expression of Intermediate Filament Proteins and Neuronal Markers in the Human Fetal Gut J. Histochem. Cytochem., January 1, 2006; 54(1): 39 - 46. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Chalazonitis, F. D'Autreaux, U. Guha, T. D. Pham, C. Faure, J. J. Chen, D. Roman, L. Kan, T. P. Rothman, J. A. Kessler, et al. Bone Morphogenetic Protein-2 and -4 Limit the Number of Enteric Neurons But Promote Development of a TrkC-Expressing Neurotrophin-3-Dependent Subset J. Neurosci., April 28, 2004; 24(17): 4266 - 4282. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. T. Shepherd, J. Pietsch, S. Elworthy, R. N. Kelsh, and D. W. Raible Roles for GFR{alpha}1 receptors in zebrafish enteric nervous system development Development, January 1, 2004; 131(1): 241 - 249. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Niederreither, J. Vermot, I. L. Roux, B. Schuhbaur, P. Chambon, and P. Dolle The regional pattern of retinoic acid synthesis by RALDH2 is essential for the development of posterior pharyngeal arches and the enteric nervous system Development, June 1, 2003; 130(11): 2525 - 2534. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. J. Burns, J.-M. M. Delalande, and N. M. Le Douarin In ovo transplantation of enteric nervous system precursors from vagal to sacral neural crest results in extensive hindgut colonisation Development, March 8, 2003; 129(12): 2785 - 2796. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Paratore, C. Eichenberger, U. Suter, and L. Sommer Sox10 haploinsufficiency affects maintenance of progenitor cells in a mouse model of Hirschsprung disease Hum. Mol. Genet., November 15, 2002; 11(24): 3075 - 3085. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. M. Young, B. R. Jones, and S. J. McKeown The Projections of Early Enteric Neurons Are Influenced by the Direction of Neural Crest Cell Migration J. Neurosci., July 15, 2002; 22(14): 6005 - 6018. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M H Sham, V C H Lui, M Fu, B Chen, and P K H Tam SOX10 is abnormally expressed in aganglionic bowel of Hirschsprung's disease infants Gut, August 1, 2001; 49(2): 220 - 226. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H M Young, C J Hearn, and D F Newgreen Embryology and development of the enteric nervous system Gut, December 1, 2000; 47(90004): iv12 - 14. [Full Text] [PDF]
|
|
|
|
 |
|
 M. D. Gershon II. Disorders of enteric neuronal development: insights from transgenic mice Am J Physiol Gastrointest Liver Physiol, August 1, 1999; 277(2): G262 - G267. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. White and D. Anderson In vivo transplantation of mammalian neural crest cells into chick hosts reveals a new autonomic sublineage restriction Development, January 10, 1999; 126(19): 4351 - 4363. [Abstract] [PDF]
|
|
|
|
|
|
J. Wu, J. Chen, T. Rothman, and M. Gershon Inhibition of in vitro enteric neuronal development by endothelin-3: mediation by endothelin B receptors Development, January 3, 1999; 126(6): 1161 - 1173. [Abstract] [PDF]
|
|
