Migratory neural crest cell αN-catenin impacts chick trigeminal ganglia formation

Wu, Chyong-Yi; Hooper, Rachel M.; Han, Kyeong; Taneyhill, Lisa A.

doi:10.1016/j.ydbio.2014.05.016

Cited by 18 publications

(25 citation statements)

References 32 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Using the above Annexin A6 MO knockdown approach, we electroporated placodal ectoderm at HH9-10 and collected embryos at HH16-17 when trigeminal and epibranchial (here the geniculate) bipolar neurons are forming nerves within the ganglia. To evaluate neuronal and overall ganglion morphology, we performed immunohistochemistry for Tubb3 (Moody et al, 1989; Shiau et al, 2008; Wu et al, 2014), the class III β-tubulin in neurons either in their last stage of, or upon their exit, from the cell cycle (Moody et al, 1989), and examined tissue sections of forming trigeminal and geniculate ganglia (Figs. 3 and 4), and the trigeminal ganglion in lateral, whole-mount views (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…As such, we performed cell proliferation (phospho-histone H3 immunohistochemistry) and cell death (TUNEL) assays (Wu et al, 2014) (Fig. S1).…”

Section: Resultsmentioning

confidence: 99%

“…Sections were mounted using Fluoromount G that contains 4′,6-diamidino-2-phenylindole (DAPI). The TUNEL assay (Roche, TMR red and fluorescein) was performed on de-gelatinized sections to detect apoptotic cells as in (Wu et al, 2014). For all experiments, images were acquired using a Zeiss LSM800 confocal microscope at 40X and 63X magnifications, and data processing was conducted using Adobe Photoshop 9.0.…”

Section: Methodsmentioning

confidence: 99%

“…Measurements of each of the two morphological types of neurons (control MO: bipolar; Annexin A6 MO: short projections) were performed using the Zeiss Zen 2.0 software from Z-stacks generated from at least five serial sections through a minimum of five each control MO- and Annexin A6 MO-electroporated embryos. Results are reported as means +/− standard deviation and standard error of the mean, with statistical significance of data established using an unpaired student’s t test (Schiffmacher et al, 2014) (Wu et al, 2014). …”

Section: Methodsmentioning

confidence: 99%

See 3 more Smart Citations

Annexin A6 controls neuronal membrane dynamics throughout chick cranial sensory gangliogenesis

Shah

Schiffmacher

Taneyhill

2017

Developmental Biology

Self Cite

View full text Add to dashboard Cite

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.

show abstract

Section: Resultsmentioning

confidence: 99%

“…As such, we performed cell proliferation (phospho-histone H3 immunohistochemistry) and cell death (TUNEL) assays (Wu et al, 2014) (Fig. S1).…”

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

See 2 more Smart Citations

Annexin A6 controls neuronal membrane dynamics throughout chick cranial sensory gangliogenesis

Shah

Schiffmacher

Taneyhill

2017

Developmental Biology

Self Cite

View full text Add to dashboard Cite

show abstract

“…Thus, any loss of migratory neural crest populations can impact cranial nerve formation by severing the cellular conduit for nascent axons growing out of the placodal cores of the cranial ganglia. In terms of molecular signals that can orchestrate cranial neural crest cell and placodal interactions, several studies have shown that cell adhesion molecules such as N-cadherin ( Cdh2 ) or αN-catenin ( Ctnna2 ) are important for cranial nerve integration [ 6 , 41 ]. Excessive N-cadherin ( Cdh2 ) expression in Xenopus results in abnormal aggregation and migration of neural crest cells [ 42 ].…”

Section: Discussionmentioning

confidence: 99%

Cranial Nerve Development Requires Co-Ordinated Shh and Canonical Wnt Signaling

et al. 2015

View full text Add to dashboard Cite

Cranial nerves govern sensory and motor information exchange between the brain and tissues of the head and neck. The cranial nerves are derived from two specialized populations of cells, cranial neural crest cells and ectodermal placode cells. Defects in either cell type can result in cranial nerve developmental defects. Although several signaling pathways are known to regulate cranial nerve formation our understanding of how intercellular signaling between neural crest cells and placode cells is coordinated during cranial ganglia morphogenesis is poorly understood. Sonic Hedgehog (Shh) signaling is one key pathway that regulates multiple aspects of craniofacial development, but whether it co-ordinates cranial neural crest cell and placodal cell interactions during cranial ganglia formation remains unclear. In this study we examined a new Patched1 (Ptch1) loss-of-function mouse mutant and characterized the role of Ptch1 in regulating Shh signaling during cranial ganglia development. Ptch1Wig/ Wig mutants exhibit elevated Shh signaling in concert with disorganization of the trigeminal and facial nerves. Importantly, we discovered that enhanced Shh signaling suppressed canonical Wnt signaling in the cranial nerve region. This critically affected the survival and migration of cranial neural crest cells and the development of placodal cells as well as the integration between neural crest and placodes. Collectively, our findings highlight a novel and critical role for Shh signaling in cranial nerve development via the cross regulation of canonical Wnt signaling.

show abstract

Cadherin‐7 mediates proper neural crest cell–placodal neuron interactions during trigeminal ganglion assembly

Taneyhill

2018

Genesis

Self Cite

View full text Add to dashboard Cite

Summary The cranial trigeminal ganglia play a vital role in the peripheral nervous system through their relay of sensory information from the vertebrate head to the brain. These ganglia are generated from the intermixing and coalescence of two distinct cell populations: cranial neural crest cells and placodal neurons. Trigeminal ganglion assembly requires the formation of cadherin-based adherens junctions within the neural crest cell and placodal neuron populations; however, the molecular composition of these adherens junctions is still unknown. Herein, we aimed to define the spatio-temporal expression pattern and function of Cadherin-7 during early chick trigeminal ganglion formation. Our data reveal that Cadherin-7 is expressed exclusively in migratory cranial neural crest cells and is absent from trigeminal neurons. Using molecular perturbation experiments, we demonstrate that modulation of Cadherin-7 in neural crest cells influences trigeminal ganglion assembly, including the organization of neural crest cells and placodal neurons within the ganglionic anlage. Moreover, alterations in Cadherin-7 levels lead to changes in the morphology of trigeminal neurons. Taken together, these findings provide additional insight into the role of cadherin-based adhesion in trigeminal ganglion formation, and, more broadly, the molecular mechanisms that orchestrate the cellular interactions essential for cranial gangliogenesis.

show abstract

Migratory neural crest cell αN-catenin impacts chick trigeminal ganglia formation

Cited by 18 publications

References 32 publications

Annexin A6 controls neuronal membrane dynamics throughout chick cranial sensory gangliogenesis

Annexin A6 controls neuronal membrane dynamics throughout chick cranial sensory gangliogenesis

Cranial Nerve Development Requires Co-Ordinated Shh and Canonical Wnt Signaling

Cadherin‐7 mediates proper neural crest cell–placodal neuron interactions during trigeminal ganglion assembly

Contact Info

Product

Resources

About