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Expression of Sympathetic Nervous System Genes in Lamprey Suggests Their Recruitment for Specification of a New Vertebrate Feature

Häming, Daniela and Simões-Costa, Marcos and Uy, Benjamin and Valencia, Jonathan and Sauka-Spengler, Tatjana and Bronner-Fraser, Marianne (2011) Expression of Sympathetic Nervous System Genes in Lamprey Suggests Their Recruitment for Specification of a New Vertebrate Feature. PLoS ONE, 6 (10). Art. No. e26543. ISSN 1932-6203. PMCID PMC3203141. https://resolver.caltech.edu/CaltechAUTHORS:20111209-084941847

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Abstract

The sea lamprey is a basal, jawless vertebrate that possesses many neural crest derivatives, but lacks jaws and sympathetic ganglia. This raises the possibility that the factors involved in sympathetic neuron differentiation were either a gnathostome innovation or already present in lamprey, but serving different purposes. To distinguish between these possibilities, we isolated lamprey homologues of transcription factors associated with peripheral ganglion formation and examined their deployment in lamprey embryos. We further performed DiI labeling of the neural tube combined with neuronal markers to test if neural crest-derived cells migrate to and differentiate in sites colonized by sympathetic ganglia in jawed vertebrates. Consistent with previous anatomical data in adults, our results in lamprey embryos reveal that neural crest cells fail to migrate ventrally to form sympathetic ganglia, though they do form dorsal root ganglia adjacent to the neural tube. Interestingly, however, paralogs of the battery of transcription factors that mediate sympathetic neuron differentiation (dHand, Ascl1 and Phox2b) are present in the lamprey genome and expressed in various sites in the embryo, but fail to overlap in any ganglionic structures. This raises the intriguing possibility that they may have been recruited during gnathostome evolution to a new function in a neural crest derivative.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1371/journal.pone.0026543 DOIArticle
http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0026543PublisherArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3203141/PubMed CentralArticle
ORCID:
AuthorORCID
Bronner-Fraser, Marianne0000-0003-4274-1862
Additional Information:© 2011 Häming et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received April 29, 2011; Accepted September 28, 2011; Published October 27, 2011. Editor: Ferenc Mueller, University of Birmingham, United Kingdom. Funding: This work was supported by the National Institutes of Health (Grant #R01 DE017911). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Author Contributions: Conceived and designed the experiments: MSC TSS MBF. Performed the experiments: DH MSC BU JV MBF. Analyzed the data: DH MSC TSS MBF. Wrote the paper: DH MSC MBF.
Funders:
Funding AgencyGrant Number
NIHR01 DE017911
Issue or Number:10
PubMed Central ID:PMC3203141
Record Number:CaltechAUTHORS:20111209-084941847
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20111209-084941847
Official Citation:Häming D, Simoes-Costa M, Uy B, Valencia J, Sauka-Spengler T, et al. (2011) Expression of Sympathetic Nervous System Genes in Lamprey Suggests Their Recruitment for Specification of a New Vertebrate Feature. PLoS ONE 6(10): e26543. doi:10.1371/journal.pone.0026543
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:28383
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:14 Dec 2011 16:56
Last Modified:03 Oct 2019 03:31

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