Single-cell profiling coupled with lineage analysis reveals vagal and sacral neural crest contributions to the developing enteric nervous system

Abstract
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Abstract

During development, much of the enteric nervous system (ENS) arises from the vagal neural crest that emerges from the caudal hindbrain and colonizes the entire gastrointestinal tract. However, a second ENS contribution comes from the sacral neural crest that arises in the caudal neural tube and populates the post-umbilical gut. By coupling single cell transcriptomics with axial-level specific lineage tracing in avian embryos, we compared the contributions of embryonic vagal and sacral neural crest cells to the chick ENS and the associated peripheral ganglia (Nerve of Remak and pelvic plexuses). At embryonic day (E) 10, the two neural crest populations form overlapping subsets of neuronal and glia cell types. Surprisingly, the post-umbilical vagal neural crest much more closely resembles the sacral neural crest than the pre-umbilical vagal neural crest. However, some differences in cluster types were noted between vagal and sacral derived cells. Notably, RNA trajectory analysis suggests that the vagal neural crest maintains a neuronal/glial progenitor pool whereas this cluster is depleted in the E10 sacral neural crest which instead has numerous enteric glia. The present findings reveal sacral neural crest contributions to the hindgut and associated peripheral ganglia and highlight the potential influence of the local environment and/or developmental timing in differentiation of neural crest-derived cells in the developing ENS.

Data availability

Sequencing data has been deposited to GEO, accession number GSE242228

The following data sets were generated

1. Jacobs-Li J
2. Tang W
3. Li C
4. Bronner ME
(2023) Single-cell profiling coupled with lineage analysis reveals vagal and sacral neural crest contributions to the developing enteric nervous system
NCBI Gene Expression Omnibus, GSE242228.

http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE242228

Article and author information

Author details

Jessica Jacobs-Li

Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0003-1339-3555
Weiyi Tang

Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States

Competing interests
No competing interests declared.
Can Li

Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States

Competing interests
No competing interests declared.
Marianne E Bronner

Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States

For correspondence
mbronner@caltech.edu

Competing interests
Marianne E Bronner, Senior editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0003-4274-1862

Funding

National Institute of Diabetes and Digestive and Kidney Diseases (R01DK13348)

Marianne E Bronner

Eunice Kennedy Shriver National Institute of Child Health and Human Development (F31HD11128)

Jessica Jacobs-Li

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.