Ablation of various regions within the avian vagal neural crest has differential effects on ganglion formation in the fore‐, mid‐ and hindgut

Abstract

The vagal neural crest adjacent to the first seven somites gives rise to both ganglionic and ectomesenchymal derivatives. Ganglionic derivatives are the neurons and supportive cells of the enteric nervous system (ENS), cardiac, and dorsal root ganglia. Ectomesenchymal derivatives are cells in the cardiac outflow tract and the mesenchymal components of thymus and parathyroids. Ectomesenchymal derivatives are formed by a segment of the vagal neural crest, from the level of the otic vesicle down to the caudal boundary of the third somite, called the cardiac neural crest. We performed neural crest ablations to study regional differences within the avian vagal neural crest with regard to the formation of the ENS. Ablation of the entire vagal neural crest from the mid-otic vesicle down to the seventh somite plus the nodose placode resulted in the absence of ganglia in the midgut (jejunum and ileum) and hindgut (colon). The foregut (esophagus, proventriculus, gizzard, and duodenum) was normally innervated. After ablation of the vagal neural crest adjacent to somites 3-5, ganglia were absent in the hindgut. Ablations of vagal neural crest not including this segment had no effect on the formation of the ENS. We surmise that the innervation of the hindgut in vivo depends specifically on the neural crest adjacent to somites 3-5, whereas innervation of the midgut can be accomplished by all segments within the vagal neural crest. The foregut can also be innervated by a source outside the vagal neural crest.To study intrinsic differences between various vagal neural crest segments regarding ENS formation, we performed chorioallantoic membrane cocultures of segments of quail vagal neural anlage and E4 chicken hindgut. We found that all vagal neural crest segments were able to give rise to enteric ganglia in the hindgut. When the neural crest of somites 6 and 7 was included in the segment, we also found melanocytes in the hindgut, suggesting that this segment is more related to trunk neural crest. Furthermore, we found that the vagal neural anlage from older embryos (>18 somites) showed an increased potential to form enteric ganglia. This suggests that vagal neural crest cells that have been in prolonged contact with the neural tube in vivo, because of either late emigration or delayed migration, have an increased probability to form enteric ganglia.0 1993 Wiley-Liss, Inc.

Mapping the origin of the avian enteric nervous system with a retroviral marker

“…Our data further suggest that somite 5 is the biggest contributor. Although Peters-van der Sanden et al (1993) found the gut was colonized in the absence of crest from somites 3 or 6, our results indicate that crest from these somites make a substantial contribution on the basis of the number of positive cells and the percentage of preparations labeled. The ability of crest cells to compensate for a loss in some of their number is well known (McKee and Ferguson, 1984;Kirby, 1988) and it appears that the crest from somites 4-7 can provide sufficient cells to populate the entire gut after the loss of crest between the otic placode and somite 3.…”

“…Peters-van der Sanden et al (1993) found that crest cells colonized the foregut after ablation of the vagal crest. This indicated a source of crest cells outside of the vagal region which could contribute to the gut, although it is not clear if these non-vagal crest normally occupy the gut or do so to compensate for the loss of the ablated crest.…”

“…Others have mapped the origin of enteric crest cells by first ablating lengths of vagal crest and subsequently examining the treated embryo for the distribution of ganglion cells along the gut (Peters-van der Sanden et al, 1993). When crest between the mid-otic vesicle and somite 7 was extirpated, only the foregut (esophagus to duodenum) contained ganglion cells.…”

Appearance of neurons in the developing chick gut

“…In this regard the source of crest cells from the neuroaxis for the esophagus is not clear. Although the enteric nervous system (Le Douarin and Teillet, 1973) forms from vagal crest precursors emerging between somites 1-7, neurons are found in the esophagus after ablation of the vagal neural crest and nodose placode (Peters-van der Sanden et al, 1993). We have recently found that injection of retrovirus containing the lac2 gene into somites 1-7 labels few esophageal crest-derived cells (Epstein et al, 1994).…”

Controlled levels of canonical Wnt signaling are required for neural crest migration

“…They are induced along the entire length of neuraxis as a bilateral, segmented stripe of cells at the lateral border of the neural plate and nonneural ectoderm (Hall, 2008;Le Douarin and Kalcheim, 1999;Sauka-Spengler and Bronner-Fraser, 2008;Steventon et al, 2005). NC cells are subdivided into cranial (Graham et al, 2004;Cordero et al, 2011), cardiac (Kirby et al, 1983;Keyte and Hutson, 2012), vagal (Kuo and Erickson, 2011;Peters-Van Der Sanden et al, 1993;Burns and Le Douarin, 1998;Yntema and Hammond, 1954), trunk (Bronner-Fraser and Fraser, 1989;Serbedzija et al, 1994) and sacral (Burns and Le Douarin, 1998;Anderson et al, 2006) NC cells due to their diversity along neuraxis ( Fig.1.1A). Upon closure of the neural plate, NC cells undergo epithelial-to-mesenchymal transition (EMT) (Ahlstrom and Erickson, 2009;Alfandari et al, 2010;Berndt et al, 2008 andDuband, 2010) allowing them to delaminate from prospective neural tube and migrate throughout the embryo ( Fig.1.1B).…”