Pelvic plexus contributes ganglion cells to the hindgut enteric nervous system

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. © 2006 Wiley‐Liss, Inc.

[1]  I. Shepherd,et al.  Collapsin-1/semaphorin D is a repellent for chick ganglion of Remak axons. , 1999, Developmental biology.

[2]  C. Erickson,et al.  Sacral neural crest cell migration to the gut is dependent upon the migratory environment and not cell-autonomous migratory properties. , 2000, Developmental biology.

[3]  R. Palmiter,et al.  Goosecoid and the organizer. , 1992 .

[4]  D. Newgreen,et al.  A single rostrocaudal colonization of the rodent intestine by enteric neuron precursors is revealed by the expression of Phox2b, Ret, and p75 and by explants grown under the kidney capsule or in organ culture. , 1998, Developmental biology.

[5]  G. Brüning,et al.  The expression pattern of a novel gene encoding brain-fatty acid binding protein correlates with neuronal and glial cell development. , 1994, Development.

[6]  M. Gershon,et al.  Colonization of the avian hindgut by cells derived from the sacral neural crest. , 1990, Developmental biology.

[7]  D. Newgreen,et al.  Differentiation of sympathetic and enteric neurons of the fowl embryo in grafts to the chorio-allantoic membrane , 2004, Cell and Tissue Research.

[8]  N. L. Le Douarin,et al.  The migration of neural crest cells to the wall of the digestive tract in avian embryo. , 1973, Journal of embryology and experimental morphology.

[9]  D. Roberts,et al.  Enteric nervous system patterning in the avian hindgut , 2004, Developmental dynamics : an official publication of the American Association of Anatomists.

[10]  R. Kapur Colonization of the murine hindgut by sacral crest-derived neural precursors: experimental support for an evolutionarily conserved model. , 2000, Developmental biology.

[11]  D. Champeval,et al.  Sacral neural crest cells colonise aganglionic hindgut in vivo but fail to compensate for lack of enteric ganglia. , 2000, Developmental biology.

[12]  A. Goldstein,et al.  Endothelin-3 regulates neural crest cell proliferation and differentiation in the hindgut enteric nervous system. , 2006, Developmental biology.

[13]  D. Roberts,et al.  BMP signaling is necessary for neural crest cell migration and ganglion formation in the enteric nervous system , 2005, Mechanisms of Development.

[14]  C. L. Yntema,et al.  Experiments on the origin and development of the sacral autonomic nerves in the chick embryo , 1955 .

[15]  H. Young,et al.  Acquisition of neuronal and glial markers by neural crest–derived cells in the mouse intestine , 2003, The Journal of comparative neurology.

[16]  A. Magyar,et al.  Peripheral blood fibrocytes contribute to the formation of the avian spleen , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[17]  M. Catala,et al.  Organization and development of the tail bud analyzed with the quail-chick chimaera system , 1995, Mechanisms of Development.

[18]  M. Mann,et al.  Thrombomucin, a Novel Cell Surface Protein that Defines Thrombocytes and Multipotent Hematopoietic Progenitors , 1997, The Journal of cell biology.

[19]  D. Newgreen,et al.  Lumbo‐sacral neural crest contributes to the avian enteric nervous system independently of vagal neural crest , 2000, Developmental dynamics : an official publication of the American Association of Anatomists.

[20]  S. Fraser,et al.  Vital dye labelling demonstrates a sacral neural crest contribution to the enteric nervous system of chick and mouse embryos. , 1991, Development.

[21]  A. Goldstein,et al.  Intestinal coelomic transplants: a novel method for studying enteric nervous system development , 2006, Cell and Tissue Research.

[22]  R. Palmiter,et al.  A transgenic model for studying development of the enteric nervous system in normal and aganglionic mice. , 1992, Development.

[23]  K. Obata,et al.  Pathfinding during spinal tract formation in the chick-quail chimera analysed by species-specific monoclonal antibodies. , 1990, Development.

[24]  D. Newgreen,et al.  The origin and differentiation of enteric neurons of the intestine of the fowl embryo. , 1980, The American journal of anatomy.

[25]  T. Castiella,et al.  Histochemical, Immunohistochemical, and Electron Microscopy Study of the Caudal Portion of the Chicken Intestinal Nerve of Remak , 1998, Neurochemical Research.

[26]  D. Newgreen,et al.  Enteric neural crest‐derived cells: Origin, identification, migration, and differentiation , 2001, The Anatomical record.

[27]  D. Tibboel,et al.  A model for aganglionosis in the chicken embryo. , 1989, Journal of pediatric surgery.

[28]  Viktor Hamburger,et al.  A series of normal stages in the development of the chick embryo , 1992, Journal of morphology.

[29]  A. Burns,et al.  In ovo transplantation of enteric nervous system precursors from vagal to sacral neural crest results in extensive hindgut colonisation. , 2002, Development.

[30]  D. Noden,et al.  Appearance of neurons and glia with respect to the wavefront during colonization of the avian gut by neural crest cells , 2003, Developmental dynamics : an official publication of the American Association of Anatomists.

[31]  A. Burns,et al.  The sacral neural crest contributes neurons and glia to the post-umbilical gut: spatiotemporal analysis of the development of the enteric nervous system. , 1998, Development.

[32]  H. Young,et al.  Phenotypes of neural-crest-derived cells in vagal and sacral pathways , 2005, Cell and Tissue Research.

[33]  A. Burns Migration of neural crest-derived enteric nervous system precursor cells to and within the gastrointestinal tract. , 2005, The International journal of developmental biology.

[34]  M. Browne A study of the sacral autonomic nerves in a chick and a human embryo , 1953, The Anatomical record.

[35]  C. L. Yntema,et al.  The origin of intrinsic ganglia of trunk viscera from vagal neural crest in the chick embryo , 1954, The Journal of comparative neurology.

[36]  A. Burns,et al.  Enteric nervous system development: Analysis of the selective developmental potentialities of vagal and sacral neural crest cells using quail‐chick chimeras , 2001, The Anatomical record.

[37]  M. Teillet Evolution of the lumbo-sacral neural crest in the avian embryo: Origin and differentiation of the ganglionated nerve of Remak studied in interspecific quail-chick chimaerae , 1978, Wilhelm Roux's archives of developmental biology.