Ancient evolutionary origin of vertebrate enteric neurons from trunk-derived neural crest

Abstract

The enteric nervous system (ENS) of jawed vertebrates arises primarily from vagal neural crest cells that migrate to the foregut and subsequently colonize and innervate the entire gastrointestinal tract. To gain insight into its evolutionary origin, we examined ENS development in the basal jawless vertebrate, the sea lamprey. Surprisingly, we found no evidence for the existence of a vagally-derived enteric neural crest population in the lamprey. Rather, DiI labeling showed that late-migrating cells, originating from the trunk neural tube and associated with nerve fibers, differentiated into neurons within the gut wall and typhlosole. We propose that these trunk-derived neural crest cells are homologous to Schwann cell precursors (SCPs), recently shown in mammalian embryos to populate post-embryonic parasympathetic ganglia1,2, including enteric ganglia3. Our results suggest that neural crest-derived SCPs made an important contribution to the ancient ENS of early jawless vertebrates, a role that was largely subsumed by vagal neural crest cells in early gnathostomes.

Multipotent peripheral glial cells generate neuroendocrine cells of the adrenal medulla

“…This idea agrees with results by Green et al, showing a marked change through evolution in the contribution of SCPs as progenitors during formation of the enteric nervous system (38). Thus, it is possible that SCPs represent an evolutionary substrate cell type essential for the advancement of neuroendocrine system in the vertebrate lineage.…”

A genome-wide assessment of the ancestral neural crest gene regulatory network

“…Interestingly, the neural crest GRN of lamprey differs from that of zebrafish in that it lacks the neural crest sub-programme involved in the specification of the enteric nervous system (ENS). This is consistent with studies showing that the lamprey may lack vagal neural crest and that the lamprey ENS may have much later onset and possibly different cell of origin 51 . Analysis of co-expression clusters using WGCNA increases the resolution of the putative lamprey neural crest GRN 29 and suggests links between early specification factors and their downstream effectors.…”

Regulatory Logic Underlying Diversification of the Neural Crest

“…Other features unique to jawed vertebrates include ondontoblasts that produce dentine, sympathetic neurons, and vagal-derived enteric neural crest [104,105]. While there are astonishing similarities between the early specification neural crest GRNs of jawed and jawless vertebrates [106], tracing regulatory differences between jawed and jawless vertebrates may have lead to formation of new cells types, thus correlating with the divergence of these cell fates.…”