Chondrogenic and gliogenic subpopulations of neural crest play distinct roles during the assembly of epibranchial ganglia.

In vertebrates, the sensory neurons of the epibranchial (EB) ganglia transmit somatosensory signals from the periphery to the CNS. These ganglia are formed during embryogenesis by the convergence and condensation of two distinct populations of precursors: placode-derived neuroblasts and neural crest...

Full description

Bibliographic Details
Main Authors: Maya D Culbertson, Zachary R Lewis, Alexei V Nechiporuk
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3170370?pdf=render
id doaj-41de40abd5df48c698e8e3ab72bea837
record_format Article
spelling doaj-41de40abd5df48c698e8e3ab72bea8372020-11-25T01:41:55ZengPublic Library of Science (PLoS)PLoS ONE1932-62032011-01-0169e2444310.1371/journal.pone.0024443Chondrogenic and gliogenic subpopulations of neural crest play distinct roles during the assembly of epibranchial ganglia.Maya D CulbertsonZachary R LewisAlexei V NechiporukIn vertebrates, the sensory neurons of the epibranchial (EB) ganglia transmit somatosensory signals from the periphery to the CNS. These ganglia are formed during embryogenesis by the convergence and condensation of two distinct populations of precursors: placode-derived neuroblasts and neural crest- (NC) derived glial precursors. In addition to the gliogenic crest, chondrogenic NC migrates into the pharyngeal arches, which lie in close proximity to the EB placodes and ganglia. Here, we examine the respective roles of these two distinct NC-derived populations during development of the EB ganglia using zebrafish morphant and mutants that lack one or both of these NC populations. Our analyses of mutant and morphant zebrafish that exhibit deficiencies in chondrogenic NC at early stages reveal a distinct requirement for this NC subpopulation during early EB ganglion assembly and segmentation. Furthermore, restoration of wildtype chondrogenic NC in one of these mutants, prdm1a, is sufficient to restore ganglion formation, indicating a specific requirement of the chondrogenic NC for EB ganglia assembly. By contrast, analysis of the sox10 mutant, which lacks gliogenic NC, reveals that the initial assembly of ganglia is not affected. However, during later stages of development, EB ganglia are dispersed in the sox10 mutant, suggesting that glia are required to maintain normal EB ganglion morphology. These results highlight novel roles for two subpopulations of NC cells in the formation and maintenance of EB ganglia: chondrogenic NC promotes the early-stage formation of the developing EB ganglia while glial NC is required for the late-stage maintenance of ganglion morphology.http://europepmc.org/articles/PMC3170370?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Maya D Culbertson
Zachary R Lewis
Alexei V Nechiporuk
spellingShingle Maya D Culbertson
Zachary R Lewis
Alexei V Nechiporuk
Chondrogenic and gliogenic subpopulations of neural crest play distinct roles during the assembly of epibranchial ganglia.
PLoS ONE
author_facet Maya D Culbertson
Zachary R Lewis
Alexei V Nechiporuk
author_sort Maya D Culbertson
title Chondrogenic and gliogenic subpopulations of neural crest play distinct roles during the assembly of epibranchial ganglia.
title_short Chondrogenic and gliogenic subpopulations of neural crest play distinct roles during the assembly of epibranchial ganglia.
title_full Chondrogenic and gliogenic subpopulations of neural crest play distinct roles during the assembly of epibranchial ganglia.
title_fullStr Chondrogenic and gliogenic subpopulations of neural crest play distinct roles during the assembly of epibranchial ganglia.
title_full_unstemmed Chondrogenic and gliogenic subpopulations of neural crest play distinct roles during the assembly of epibranchial ganglia.
title_sort chondrogenic and gliogenic subpopulations of neural crest play distinct roles during the assembly of epibranchial ganglia.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2011-01-01
description In vertebrates, the sensory neurons of the epibranchial (EB) ganglia transmit somatosensory signals from the periphery to the CNS. These ganglia are formed during embryogenesis by the convergence and condensation of two distinct populations of precursors: placode-derived neuroblasts and neural crest- (NC) derived glial precursors. In addition to the gliogenic crest, chondrogenic NC migrates into the pharyngeal arches, which lie in close proximity to the EB placodes and ganglia. Here, we examine the respective roles of these two distinct NC-derived populations during development of the EB ganglia using zebrafish morphant and mutants that lack one or both of these NC populations. Our analyses of mutant and morphant zebrafish that exhibit deficiencies in chondrogenic NC at early stages reveal a distinct requirement for this NC subpopulation during early EB ganglion assembly and segmentation. Furthermore, restoration of wildtype chondrogenic NC in one of these mutants, prdm1a, is sufficient to restore ganglion formation, indicating a specific requirement of the chondrogenic NC for EB ganglia assembly. By contrast, analysis of the sox10 mutant, which lacks gliogenic NC, reveals that the initial assembly of ganglia is not affected. However, during later stages of development, EB ganglia are dispersed in the sox10 mutant, suggesting that glia are required to maintain normal EB ganglion morphology. These results highlight novel roles for two subpopulations of NC cells in the formation and maintenance of EB ganglia: chondrogenic NC promotes the early-stage formation of the developing EB ganglia while glial NC is required for the late-stage maintenance of ganglion morphology.
url http://europepmc.org/articles/PMC3170370?pdf=render
work_keys_str_mv AT mayadculbertson chondrogenicandgliogenicsubpopulationsofneuralcrestplaydistinctrolesduringtheassemblyofepibranchialganglia
AT zacharyrlewis chondrogenicandgliogenicsubpopulationsofneuralcrestplaydistinctrolesduringtheassemblyofepibranchialganglia
AT alexeivnechiporuk chondrogenicandgliogenicsubpopulationsofneuralcrestplaydistinctrolesduringtheassemblyofepibranchialganglia
_version_ 1725038931823558656