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Proc Natl Acad Sci U S A. 2017 Nov 7;114(45):11980-11985. doi: 10.1073/pnas.1710308114. Epub 2017 Oct 24.

Dual origin of enteric neurons in vagal Schwann cell precursors and the sympathetic neural crest.

Author information

1
Institut de Biologie de l'École Normale Supérieure (IBENS), École Normale Supérieure, CNRS, INSERM, PSL Research University, 75005 Paris, France.
2
Stem Cells and Regenerative Medicine, Birth Defects Research Centre, University College London Great Ormond Street Institute of Child Health, WC1N 1EH London, United Kingdom.
3
Laboratory for Neural Differentiation and Regeneration, Graduate School of Medicine, Kobe University, 650-0017 Kobe City, Japan.
4
Max-Delbrück-Center for Molecular Medicine in the Helmholtz-Association, 13125 Berlin, Germany.
5
Department of Clinical Genetics, Erasmus Medical Center, 3015 CE Rotterdam, The Netherlands.
6
Institut de Biologie de l'École Normale Supérieure (IBENS), École Normale Supérieure, CNRS, INSERM, PSL Research University, 75005 Paris, France; jfbrunet@biologie.ens.fr.

Abstract

Most of the enteric nervous system derives from the "vagal" neural crest, lying at the level of somites 1-7, which invades the digestive tract rostro-caudally from the foregut to the hindgut. Little is known about the initial phase of this colonization, which brings enteric precursors into the foregut. Here we show that the "vagal crest" subsumes two populations of enteric precursors with contrasted origins, initial modes of migration, and destinations. Crest cells adjacent to somites 1 and 2 produce Schwann cell precursors that colonize the vagus nerve, which in turn guides them into the esophagus and stomach. Crest cells adjacent to somites 3-7 belong to the crest streams contributing to sympathetic chains: they migrate ventrally, seed the sympathetic chains, and colonize the entire digestive tract thence. Accordingly, enteric ganglia, like sympathetic ones, are atrophic when deprived of signaling through the tyrosine kinase receptor ErbB3, while half of the esophageal ganglia require, like parasympathetic ones, the nerve-associated form of the ErbB3 ligand, Neuregulin-1. These dependencies might bear relevance to Hirschsprung disease, with which alleles of Neuregulin-1 are associated.

KEYWORDS:

Neuregulin1; chicken; enteric nervous system; mouse; neural crest

PMID:
29078343
PMCID:
PMC5692562
DOI:
10.1073/pnas.1710308114
[Indexed for MEDLINE]
Free PMC Article

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