Descriptive and experimental analysis of the dispersion of neural crest cells along the dorsolateral path and their entry into ectoderm in the chick embryo

Abstract

We have characterized the dispersion of neural crest cells along the dorsolateral path in the trunk of the chicken embryo and experimentally investigated the control of neural crest cell entry into this path. The distribution of putative neural crest cells was analyzed in plastic sections of embryos that had been incubated for 24 hr in HNK-1 antibody, a procedure that we show successfully labels neural crest cells in the dorsolateral path and ectoderm. In accord with earlier observations, crest cells delay entering the dorsolateral path until a day or more after their counterparts have colonized the ventral path. However, once crest cells enter, they disperse rapidly through the path dorsal to the somite but still delay migrating dorsal to the intersegmental space. During dispersion, crest cells invade the ectoderm at sites associated with local disruptions in the basal lamina which may be caused by crest cells. Finally, deleting the dermamyotome releases an inhibition of neural crest cell migration: crest cells enter the dorsolateral path precociously. We speculate that the epithelial dermatome may transiently produce inhibitory substances and that emerging dermis may provide a long-distance, stimulatory cue.

Long‐distance cue from emerging dermis stimulates neural crest melanoblast migration

“…In normal and sham-operated embryos, the pattern of migration is stereotyped and is uniform across the midline. At stage 19, crest cells have yet to enter this path and remain in the staging areas; at stage 20, the first cells are in the path entryway, dorsal to the medial lip of the dermatome; at stage 21, crest cells have entered but still lie in the most proximal portion of the path (also see Erickson et al, 1992, and reconstructed sham operated embryos in Fig. 4).…”

“…Dermis emerges shortly before neural crest cells enter the dorsal path. At chick and quail hindlimb levels, the epithelial dermatome initiates an epithelial-mesenchymal transition and the first dermal cells begin to disperse between stages 19 and 20, just before neural crest cells enter the path at stage 20 -21, 6 -12 hr later (see also Erickson et al, 1992). Most important, these first dermal cells arise far from the migration staging area containing the melanoblasts.…”

“…Moreover, the melanoblasts are temporally segregated, emerging relatively late into the "migration staging area" circumscribed by the neural tube, ectoderm, and somite. They enter the dorsal path only well after other neural crest cells have finished migrating ventrally into the somite (Weston and Butler, 1966;Serbedzija et al, 1990;Erickson et al, 1992;review: Erickson, 1993). During neural crest cell emergence or during their sojourn in the staging area, they become committed to the melanocyte fate (Erickson and Goins, 1995;Reedy et al, 1998a;Kos et al, 2001;Faraco et al, 2001;Luo et al, 2003) and acquire the special properties that allow them to colonize the dorsal path (Santiago and Erickson, 2002).…”

“…Inhibitory elements within the dorsal path are supplied by the epithelial dermatome (Erickson et al, 1992;Oakley et al, 1994) and include ephrin-B ligands (Koblar et al, 2000;Santiago and Erickson, 2002), chondroitin sulfate, and an uncharacterized substance detected by peanut agglutinin lectin binding (Oakley et al, 1994). Permissive extracellular matrix components such as hyaluronic acid, thrombospondin, collagen, laminin, fibronectin, and basal lamina are also found in trunk paths (reviews, Erickson, 1988;Peris and Perissinotto, 2000) but a diffusible cue has yet to be directly implicated.…”

Significance of the cranial neural crest

“…Those that move furthest ventrally form the sympathetic ganglia, while the remainder cease migration in the anterior sclerotome and form the dorsal root ganglia. The later migrating neural crest cells, however, move dorsolaterally between the dermamyotome and the overlying ectoderm, and these cells will form the melanocytes (Weston and Butler, 1966;Serbedzija et al, 1990;Erickson et al, 1992). In the head, there is also a correlation between the timing of crest migration and the fates the crest cells follow, but it is significantly different.…”