The formation of the cranial ganglia by placodally-derived sensory neuronal precursors

Blentic, Aida; Chambers, David; Skinner, Adam; Begbie, Jo; Graham, Anthony

doi:10.1016/j.mcn.2010.11.010

Cited by 34 publications

(47 citation statements)

References 37 publications

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“…We assessed expression of an additional placode-associated marker, Six4 (25), and found nearly complete overlap between Six1 and Six4-labeled populations (Figure 3, top left). Previous work suggests that placode-derived cranial sensory neurons express Brn3a earlier than neural crest-derived cells (26, 27). We found that nearly all Six1 labeled cells in gCN V express Brn3A at E10.5 (Figure 3, middle left).…”

Section: Resultsmentioning

confidence: 93%

“…Accordingly, we asked whether expression of key transcription factors in cranial sensory populations along the anterior-posterior (A-P) axis was altered systematically at cranial sensory sites in response to FgfR-I or DEAB. We selected 22 transcription factors whose activity has been associated with cranial sensory neuron genesis or differentiation based on expression as well as consequences of loss or gain of function (27, 52-65). …”

Section: Resultsmentioning

confidence: 99%

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A cellular and molecular mosaic establishes growth and differentiation states for cranial sensory neurons

Karpinski

Bryan

Paronett

et al. 2016

Developmental Biology

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We compared apparent origins, cellular diversity and regulation of initial axon growth for differentiating cranial sensory neurons. We assessed the molecular and cellular composition of the developing olfactory and otic placodes, and cranial sensory ganglia to evaluate contributions of ectodermal placode versus neural crest at each site. Special sensory neuron populations—the olfactory and otic placodes—as well as those in vestibulo-acoustic ganglion are entirely populated with cells expressing cranial placode-associated, rather than neural crest-associated markers. The remaining cranial sensory ganglia are a mosaic of cells that express placode-associated as well as neural crest-associated markers. We found two distinct populations of neural crest in the cranial ganglia: the first, as expected, is labeled by Wnt1:Cre mediated recombination. The second is not labeled by Wnt1:Cre recombination, and expresses both Sox10 and FoxD3. These populations—Wnt1:Cre recombined, and Sox10/Foxd3-expressing— are proliferatively distinct from one another. Together, the two neural crest-associated populations are substantially more proliferative than their placode-associated counterparts. Nevertheless, the apparently placodal and crest-associated populations are similarly sensitive to altered signaling that compromises cranial morphogenesis and differentiation. Acute disruption of either Fibroblast growth factor (Fgf) or Retinoic acid (RA) signaling alters axon growth and cell death, but does not preferentially target any of the three distinct populations. Apparently, mosaic derivation and diversity of precursors and early differentiating neurons, modulated uniformly by local signals, supports early cranial sensory neuron differentiation and growth.

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Section: Resultsmentioning

confidence: 93%

Section: Resultsmentioning

confidence: 99%

A cellular and molecular mosaic establishes growth and differentiation states for cranial sensory neurons

Karpinski

Bryan

Paronett

et al. 2016

Developmental Biology

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“…8), additional markers of mature neurons. HuC/D is an RNA binding protein that is only expressed in mature, post-mitotic neurons (Blentic et al, 2011; Smith et al, 2015), whereas NFM is a component of intermediate filaments comprising the axoskeleton of mature neurons that mediates radial projection growth and intracellular transport to axons (Perrot et al, 2008; Smith et al, 2015). We electroporated placodal ectoderm at HH9-10 and collected embryos at HH16-17, when the trigeminal neurons should be morphologically bipolar.…”

Section: Resultsmentioning

confidence: 99%

Annexin A6 controls neuronal membrane dynamics throughout chick cranial sensory gangliogenesis

Shah

Schiffmacher

Taneyhill

2017

Developmental Biology

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Cranial sensory ganglia are components of the peripheral nervous system that possess a significant somatosensory role and include neurons within the trigeminal and epibranchial nerve bundles. Although it is well established that these ganglia arise from interactions between neural crest and neurogenic placode cells, the molecular basis of ganglia assembly is still poorly understood. Members of the Annexin protein superfamily play key roles in sensory nervous system development throughout metazoans. Annexin A6 is expressed in chick trigeminal and epibranchial placode cell-derived neuroblasts and neurons, but its function in cranial ganglia formation has not been elucidated. To this end, we interrogated the role of Annexin A6 using gene perturbation studies in the chick embryo. Our data reveal that placode cell-derived neuroblasts with reduced Annexin A6 levels ingress and migrate normally to the ganglionic anlage, where neural crest cell corridors correctly form around them. Strikingly, while Annexin A6-depleted placode cell-derived neurons still express mature neuronal markers, they fail to form two long processes, which are considered morphological features of mature neurons, and no longer innervate their designated targets due to the absence of this bipolar morphology. Moreover, overexpression of Annexin A6 causes some placode cell-derived neurons to form extra protrusions alongside these bipolar processes. These data demonstrate that the molecular program associated with neuronal maturation is distinct from that orchestrating changes in neuronal morphology, and, importantly, reveal Annexin A6 to be a key membrane scaffolding protein during sensory neuron membrane biogenesis. Collectively, our results provide novel insight into mechanisms underscoring morphological changes within placode cell-derived neurons that are essential for cranial gangliogenesis.

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“…First-order visceral sensory neurons of the geniculate, petrosal, and nodose ganglia are born in epibranchial placodes (5). The placodal cells express Phox2a (the paralogue of Phox2b) and switch on Phox2b as they form the ganglia (6) and become postmitotic (7). In Phox2b null embryos, the cells still form ganglia but lose Dopamine-β-hydroxylase expression at embryonic day (E)9.5 and show attenuated expression of the tyrosine kinase receptor Ret at E10.5 (2).…”

mentioning

confidence: 99%

Homeoprotein Phox2b commands a somatic-to-visceral switch in cranial sensory pathways

D’Autréaux

Coppola

Hirsch

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

110

123

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Taste and most sensory inputs required for the feedback regulation of digestive, respiratory, and cardiovascular organs are conveyed to the central nervous system by so-called "visceral" sensory neurons located in three cranial ganglia (geniculate, petrosal, and nodose) and integrated in the hindbrain by relay sensory neurons located in the nucleus of the solitary tract. Visceral sensory ganglia and the nucleus of the solitary tract all depend for their formation on the pan-visceral homeodomain transcription factor Phox2b, also required in efferent neurons to the viscera. We show here, by genetically tracing Phox2b + cells, that in the absence of the protein, many visceral sensory neurons (first-and second-order) survive. However, they adopt a fate-including molecular signature, cell positions, and axonal projections-akin to that of somatic sensory neurons (first-and second-order), located in the trigeminal, superior, and jugular ganglia and the trigeminal sensory nuclei, that convey touch and pain sensation from the orofacial region. Thus, the cranial sensory pathways, somatic and visceral, are related, and Phox2b serves as a developmental switch from the former to the latter.

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The formation of the cranial ganglia by placodally-derived sensory neuronal precursors

Cited by 34 publications

References 37 publications

A cellular and molecular mosaic establishes growth and differentiation states for cranial sensory neurons

A cellular and molecular mosaic establishes growth and differentiation states for cranial sensory neurons

Annexin A6 controls neuronal membrane dynamics throughout chick cranial sensory gangliogenesis

Homeoprotein Phox2b commands a somatic-to-visceral switch in cranial sensory pathways

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