Characterization of the trunk neural crest in the bamboo shark, Chiloscyllium punctatum
Abstract
The neural crest is a population of mesenchymal cells that after migrating from the neural tube gives rise to structure and cell types: the jaw, part of the peripheral ganglia, and melanocytes. Although much is known about neural crest development in jawed vertebrates, a clear picture of trunk neural crest development for elasmobranchs is yet to be developed. Here we present a detailed study of trunk neural crest development in the bamboo shark, Chiloscyllium punctatum. Vital labeling with dioctadecyl tetramethylindocarbocyanine perchlorate (DiI) and in situ hybridization using cloned Sox8 and Sox9 probes demonstrated that trunk neural crest cells follow a pattern similar to the migratory paths already described in zebrafish and amphibians. We found shark trunk neural crest along the rostral side of the somites, the ventromedial pathway, the branchial arches, the gut, the sensory ganglia, and the nerves. Interestingly, C. punctatum Sox8 and Sox9 sequences aligned with vertebrate SoxE genes, but appeared to be more ancient than the corresponding vertebrate paralogs. The expression of these two SoxE genes in trunk neural crest cells, especially Sox9, matched the Sox10 migratory patterns observed in teleosts. Also of interest, we observed DiI cells and Sox9 labeling along the lateral line, suggesting that in C. punctatum, glial cells in the lateral line are likely of neural crest origin. Although this has been observed in other vertebrates, we are the first to show that the pattern is present in cartilaginous fishes. These findings demonstrate that trunk neural crest cell development in C. punctatum follows the same highly conserved migratory pattern observed in jawed vertebrates.
Additional Information
© 2013 Wiley Periodicals, Inc. Received November 12, 2012; Revised April 15, 2013; Accepted for publication April 25, 2013. Article first published online: 25 Jul. 2013. The first three authors contributed equally to this work. Grant sponsor: National Institute of Neurological Disorders and Stroke, National Institutes of Health; Grant numbers: 2R15NS060099-02A1 and 5SC3GM096904-02 (to M.E.dB.); Grant sponsor: National Institutes of Health; Grant number: GM 2 T34 GM008959 (to M.E. Zavala for support for M.J.). We give special thanks to Chris Plante and Michelle Malme from the Long Beach Aquarium for providing us the shark embryos; to John Reiss for his helpful comments; and to Kent Coleman for his valuable revisions to this manuscript. Role of Authors: All authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. MJ: performed in situ hybridizations; MR: performed DiI injections; TC: performed DNA/protein analyses, designed phylogenetic figures, performed bioinformatics analysis, and revised the manuscript; LR: performed SEM; SS: performed sectioning; DM and MJ: performed Sox8 and Sox9 cloning; RM: oversaw bioinformatics analysis; MEdB: wrote the manuscript, and performed Sox8 and Sox9 cloning and DiI injections.Attached Files
Accepted Version - nihms-471855.pdf
Supplemental Material - cne23351-sup-0001-suppinfo.docx
Supplemental Material - cne23351-sup-0002-suppinfo.docx
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Additional details
- PMCID
- PMC3729875
- Eprint ID
- 41040
- Resolver ID
- CaltechAUTHORS:20130830-143744531
- National Institute of Neurological Disorders and Stroke (NINDS)
- 2R15NS060099-02A1
- NIH
- 5SC3GM096904-02
- NIH
- GM 2 T34 GM008959
- NIH Predoctoral Fellowship
- Created
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2013-09-11Created from EPrint's datestamp field
- Updated
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2021-11-10Created from EPrint's last_modified field