Cardiac neural crest contributes to cardiomyocytes in amniotes and heart regeneration in zebrafish

Abstract
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Abstract

Cardiac neural crest cells contribute to important portions of the cardiovascular system including the aorticopulmonary septum and cardiac ganglion. Using replication incompetent avian retroviruses for precise high-resolution lineage analysis, we uncover a previously undescribed neural crest contribution to cardiomyocytes of the ventricles in Gallus gallus, supported by Wnt1-Cre lineage analysis in Mus musculus. To test the intriguing possibility that neural crest cells contribute to heart repair, we examined Danio rerio adult heart regeneration in the neural crest transgenic line, Tg(-4.9sox10:eGFP). Whereas the adult heart has few sox10+ cells in the apex, sox10 and other neural crest regulatory network genes are upregulated in the regenerating myocardium after resection. The results suggest that neural crest cells contribute to many cardiovascular structures including cardiomyocytes across vertebrates and to the regenerating heart of teleost fish. Thus, understanding molecular mechanisms that control the normal development of the neural crest into cardiomyocytes and reactivation of the neural crest program upon regeneration may open potential therapeutic approaches to repair heart damage in amniotes.

Data availability

All data is available in the main text, the supplementary materials. Databases have been deposited to NCBI (BioProject # PRJNA526570).

The following previously published data sets were used

(2018) Transcriptome profiling of the cardiac neural crest reveals a critical role for MafB.
NCBI BioProject, PRJNA492347.

http://www.ncbi.nlm.nih.gov/bioproject/PRJNA492347
(2018) . From pioneer to repressor: bimodal foxd3 activity dynamically remodels neural crest regulatory landscape in vivo
NCBI Gene Expression Omnibus, GSE106676.

http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE106676

Article and author information

Author details

Weiyi Tang

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:" 0000-0002-1279-1001
Megan L Martik

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

Competing interests
No competing interests declared.
Yuwei 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:" 0000-0001-7753-4869
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 Institutes of Health (NIHR01DE027568)

Marianne E Bronner

National Institutes of Health (NIHRO1HL14058)

Marianne E Bronner

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

Ethics

Animal experimentation: Adult zebrafish were maintained in the Beckman Institute Zebrafish Facility at Caltech, and all animal and embryo work were completed in compliance with California Institute of Technology Institutional Animal Care and Use Committee (IACUC) protocol 1764.

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.