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

Green, Stephen A. and Uy, Benjamin R. and Bronner, Marianne E. (2017) Ancient evolutionary origin of vertebrate enteric neurons from trunk-derived neural crest. Nature, 544 (7648). pp. 88-91. ISSN 0028-0836. PMCID PMC5383518. https://resolver.caltech.edu/CaltechAUTHORS:20170124-161810111

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Abstract

The enteric nervous system of jawed vertebrates arises primarily from vagal neural crest cells that migrate to the foregut and subsequently colonize and innervate the entire gastrointestinal tract. Here we examine development of the enteric nervous system in the basal jawless vertebrate the sea lamprey (Petromyzon marinus) to gain insight into its evolutionary origin. Surprisingly, we find no evidence for the existence of a vagally derived enteric neural crest population in the lamprey. Rather, labelling with the lipophilic dye DiI shows that late-migrating cells, originating from the trunk neural tube and associated with nerve fibres, differentiate into neurons within the gut wall and typhlosole. We propose that these trunk-derived neural crest cells may be homologous to Schwann cell precursors, recently shown in mammalian embryos to populate post-embryonic parasympathetic ganglia, including enteric ganglia. Our results suggest that neural-crest-derived Schwann cell precursors made an important contribution to the ancient enteric nervous system of early jawless vertebrates, a role that was largely subsumed by vagal neural crest cells in early gnathostomes.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://dx.doi.org/10.1038/nature21679DOIArticle
http://rdcu.be/qhfvPublisherFree ReadCube access
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5383518PubMed CentralArticle
ORCID:
AuthorORCID
Uy, Benjamin R.0000-0003-0438-880X
Bronner, Marianne E.0000-0003-4274-1862
Additional Information:© 2017 Macmillan Publishers Limited. received 23 February 2016; accepted 31 January 2017. Published online 20 March 2017. We thank C. Baker, M. Piacentino, and L. Kerosuo for discussion, and M. Martik, M. Simoes-Costa, and R. Uribe for their comments on this manuscript. These authors contributed equally to this work: Stephen A. Green & Benjamin R. Uy. Author Contributions: The project was conceived by M.E.B., and analyses were designed by S.A.G. and M.E.B. Descriptive analyses of enteric neurons were performed by S.A.G. Cranial DiI labelling was performed by B.R.U., M.E.B., and S.A.G. Trunk DiI labelling was performed by B.R.U., S.A.G. and M.E.B. Surgeries were performed, imaged and analysed by S.A.G. and B.R.U. Schematics were drawn by S.A.G. The manuscript was written by M.E.B., S.A.G. and B.R.U. Data availability: The datasets generated during and/or analysed during the current study are available from the corresponding author upon reasonable request. The authors declare no competing financial interests.
Issue or Number:7648
PubMed Central ID:PMC5383518
Record Number:CaltechAUTHORS:20170124-161810111
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20170124-161810111
Official Citation:Ancient evolutionary origin of vertebrate enteric neurons from trunk-derived neural crest Stephen A. Green, Benjamin R. Uy & Marianne E. Bronner Nature 544, 88–91 (06 April 2017) doi:10.1038/nature21679
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:73681
Collection:CaltechAUTHORS
Deposited By: Katherine Johnson
Deposited On:20 Mar 2017 23:00
Last Modified:03 Oct 2019 16:30

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