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Clonal analysis and dynamic imaging identify multipotency of individual Gallus gallus caudal hindbrain neural crest cells toward cardiac and enteric fates

Tang, Weiyi and Li, Yuwei and Li, Ang and Bronner, Marianne E. (2021) Clonal analysis and dynamic imaging identify multipotency of individual Gallus gallus caudal hindbrain neural crest cells toward cardiac and enteric fates. Nature Communications, 12 . Art. No. 1894. ISSN 2041-1723. PMCID PMC7994390. doi:10.1038/s41467-021-22146-8. https://resolver.caltech.edu/CaltechAUTHORS:20210325-075837590

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Abstract

Neural crest stem cells arising from caudal hindbrain (often called cardiac and posterior vagal neural crest) migrate long distances to form cell types as diverse as heart muscle and enteric ganglia, abnormalities of which lead to common congenital birth defects. Here, we explore whether individual caudal hindbrain neural crest precursors are multipotent or predetermined toward these particular fates and destinations. To this end, we perform lineage tracing of chick neural crest cells at single-cell resolution using two complementary approaches: retrovirally mediated multiplex clonal analysis and single-cell photoconversion. Both methods show that the majority of these neural crest precursors are multipotent with many clones producing mesenchymal as well as neuronal derivatives. Time-lapse imaging demonstrates that sister cells can migrate in distinct directions, suggesting stochasticity in choice of migration path. Perturbation experiments further identify guidance cues acting on cells in the pharyngeal junction that can influence this choice; loss of CXCR4 signaling results in failure to migrate to the heart but no influence on migration toward the foregut, whereas loss of RET signaling does the opposite. Taken together, the results suggest that environmental influences rather than intrinsic information govern cell fate choice of multipotent caudal hindbrain neural crest cells.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41467-021-22146-8DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7994390PubMed CentralArticle
ORCID:
AuthorORCID
Tang, Weiyi0000-0002-1279-1001
Li, Yuwei0000-0001-7753-4869
Bronner, Marianne E.0000-0003-4274-1862
Additional Information:© The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 11 March 2020; Accepted 22 February 2021; Published 25 March 2021. We thank Dr. Carlos Lois and the Biological Imaging Facility of the Beckman Institute for sharing equipment. This work is supported by NIHRO1HL14058 to M.E.B. Data availability: The authors declare that all data supporting the findings of this study are available within the article and its supplementary information files or from the corresponding author upon reasonable request. Author Contributions: W.T. and M.E.B. conceived the project. W.T. and Y.L designed the experiments. W.T. performed the experiments. Y.L. established single-cell photoconversion and provided help with imaging analysis. A.L. performed quantitative analysis. W.T., Y.L., and M. E.B wrote the manuscript with consultation from A.L. The authors declare no competing interests. Peer review information: Nature Communications thanks David McCauley and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.
Funders:
Funding AgencyGrant Number
NIHRO1HL14058
Subject Keywords:Cell biology; Developmental biology; Stem cells
PubMed Central ID:PMC7994390
DOI:10.1038/s41467-021-22146-8
Record Number:CaltechAUTHORS:20210325-075837590
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210325-075837590
Official Citation:Tang, W., Li, Y., Li, A. et al. Clonal analysis and dynamic imaging identify multipotency of individual Gallus gallus caudal hindbrain neural crest cells toward cardiac and enteric fates. Nat Commun 12, 1894 (2021). https://doi.org/10.1038/s41467-021-22146-8
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:108551
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:25 Mar 2021 17:52
Last Modified:19 Apr 2021 17:22

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