The formation of the superior and jugular ganglia: Insights into the generation of sensory neurons by the neural crest

Thompson, Hannah; Blentic, Aida; Watson, Sheona; Begbie, Jo; Graham, Anthony

doi:10.1002/dvdy.22179

Cited by 15 publications

(15 citation statements)

References 35 publications

(9 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Whole-mount immunofluorescence imaging was performed using anti-Pax2 antibody (Zymed, 1:200) according to standard procedures (Thompson et al, 2010). Embryos were washed thrice in PBSTx (PBS + 1% Triton X-100), blocked with 10% FBS/ PBSTx for 90 min, followed by incubation with the primary antibody diluted in the blocking solution for 3 days.…”

Section: Methodsmentioning

confidence: 99%

Midline-derived Shh regulates mesonephric tubule formation through the paraxial mesoderm

Murashima

Akita

Okazawa

et al. 2014

Developmental Biology

View full text Add to dashboard Cite

During organogenesis, Sonic hedgehog (Shh) possesses dual functions: Shh emanating from midline structures regulates the positioning of bilateral structures at early stages, whereas organ-specific Shh locally regulates organ morphogenesis at later stages. The mesonephros is a transient embryonic kidney in amniote, whereas it becomes definitive adult kidney in some anamniotes. Thus, elucidating the regulation of mesonephros formation has important implications for our understanding of kidney development and evolution. In Shh knockout (KO) mutant mice, the mesonephros was displaced towards the midline and ectopic mesonephric tubules (MTs) were present in the caudal mesonephros. Mesonephros-specific ablation of Shh in Hoxb7-Cre;Shhflox/− and Sall1CreERT2/+;Shhflox/− mice embryos indicated that Shh expressed in the mesonephros was not required for either the development of the mesonephros or the differentiation of the male reproductive tract. Moreover, stage-specific ablation of Shh in ShhCreERT2/flox mice showed that notochord- and/or floor plate-derived Shh were essential for the regulation of the number and position of MTs. Lineage analysis of hedgehog (Hh)-responsive cells, and analysis of gene expression in Shh KO embryos suggested that Shh regulated nephrogenic gene expression indirectly, possibly through effects on the paraxial mesoderm. These data demonstrate the essential role of midline-derived Shh in local tissue morphogenesis and differentiation.

show abstract

Section: Methodsmentioning

confidence: 99%

Midline-derived Shh regulates mesonephric tubule formation through the paraxial mesoderm

Murashima

Akita

Okazawa

et al. 2014

Developmental Biology

View full text Add to dashboard Cite

show abstract

“…Whole-mount antibody staining was carried out as described previously (Thompson et al, 2010). Primary antibodies were: mouse anti-HNK1, 1:200 (Sigma); mouse anti-neurofilament medium chain, 1:5000 (RMO-270, Zymed, Invitrogen); mouse anti-islet 1/2, 1:1000 (a kind gift from Ivo Lieberam, King’s College London, UK); rabbit anti-GFP, 1:500 (Invitrogen).…”

Section: Methodsmentioning

confidence: 99%

“…The CSG can be subdivided into proximal and distal ganglia relating to location on the associated cranial nerve. Neurons of the proximal CSG are generated from NCCs (D’Amico-Martel and Noden, 1983; Thompson et al, 2010). However, in the distal CSG, NCCs mainly generate the non-neuronal components, whereas the majority of neurons originate in ectodermal neurogenic placodes (D’Amico-Martel and Noden, 1983; Harlow et al, 2011; Thompson et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

“…Neurons of the proximal CSG are generated from NCCs (D’Amico-Martel and Noden, 1983; Thompson et al, 2010). However, in the distal CSG, NCCs mainly generate the non-neuronal components, whereas the majority of neurons originate in ectodermal neurogenic placodes (D’Amico-Martel and Noden, 1983; Harlow et al, 2011; Thompson et al, 2010). With the exception of the ophthalmic trigeminal placode, which generates postmitotic neurons, neurogenic placodes produce neuroblasts that delaminate and actively migrate towards the hindbrain (Begbie et al, 2002; Blentic et al, 2011; Graham et al, 2007; McCabe et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Cranial neural crest cells form corridors prefiguring sensory neuroblast migration

et al. 2013

Self Cite

View full text Add to dashboard Cite

The majority of cranial sensory neurons originate in placodes in the surface ectoderm, migrating to form ganglia that connect to the central nervous system (CNS). Interactions between inward-migrating sensory neuroblasts and emigrant cranial neural crest cells (NCCs) play a role in coordinating this process, but how the relationship between these two cell populations is established is not clear. Here, we demonstrate that NCCs generate corridors delineating the path of migratory neuroblasts between the placode and CNS in both chick and mouse. In vitro analysis shows that NCCs are not essential for neuroblast migration, yet act as a superior substrate to mesoderm, suggesting provision of a corridor through a less-permissive mesodermal territory. Early organisation of NCC corridors occurs prior to sensory neurogenesis and can be recapitulated in vitro; however, NCC extension to the placode requires placodal neurogenesis, demonstrating reciprocal interactions. Together, our data indicate that NCC corridors impose physical organisation for precise ganglion formation and connection to the CNS, providing a local environment to enclose migrating neuroblasts and axonal processes as they migrate through a non-neural territory.

show abstract

“…This includes all of those contributing to the epibranchial ganglia: the geniculate, petrosal and nodose, the cells of the vestibuloacoustic ganglion, and many of the neurons of the trigeminal ganglion, and in some vertebrate clades neurons associated with the spiracular/paratympanic organ [4]. Additionally, there are neural crest derived sensory neurons in the head and these will form the proximal ganglia of the IXth and Xth nerves, the Superior and Jugular, as well as contributing to the trigeminal ganglion [1, 3, 5]. Finally, there is one last significant population of sensory neurons in the head which do not lie in a peripheral ganglion but which are situated within the central nervous system (CNS), the cells of the Mesencephalic Trigeminal Nucleus (MTN), (also sometimes abbreviated as MesV), which relay information about the position of the jaw [6, 7].…”

Section: Introductionmentioning

confidence: 99%

The emergence of mesencephalic trigeminal neurons

et al. 2017

Self Cite

View full text Add to dashboard Cite

BackgroundThe cells of the mesencephalic trigeminal nucleus (MTN) are the proprioceptive sensory neurons that innervate the jaw closing muscles. These cells differentiate close to the two key signalling centres that influence the dorsal midbrain, the isthmus, which mediates its effects via FGF and WNT signalling and the roof plate, which is a major source of BMP signalling as well as WNT signalling.MethodsIn this study, we have set out to analyse the importance of FGF, WNT and BMP signalling for the development of the MTN. We have employed pharmacological inhibitors of these pathways in explant cultures as well as utilising the electroporation of inhibitory constructs in vivo in the chick embryo.ResultsWe find that interfering with either FGF or WNT signalling has pronounced effects on MTN development whilst abrogation of BMP signalling has no effect. We show that treatment of explants with either FGF or WNT antagonists results in the generation of fewer MTN neurons and affects MTN axon extension and that inhibition of both these pathways has an additive effect. To complement these studies, we have used in vivo electroporation to inhibit BMP, FGF and WNT signalling within dorsal midbrain cells prior to, and during, their differentiation as MTN neurons. Again, we find that inhibition of BMP signalling has no effect on the development of MTN neurons. We additionally find that cells electroporated with inhibitory constructs for either FGF or WNT signalling can differentiate as MTN neurons suggesting that these pathways are not required cell intrinsically for the emergence of these neurons. Indeed, we also show that explants of dorsal mesencephalon lacking both the isthmus and roof plate can generate MTN neurons. However, we did find that inhibiting FGF or WNT signalling had consequences for MTN differentiation.ConclusionsOur results suggest that the emergence of MTN neurons is an intrinsic property of the dorsal mesencephalon of gnathostomes, and that this population undergoes expansion, and maturation, along with the rest of the dorsal midbrain under the influence of FGF and WNT signalling.

show abstract

The formation of the superior and jugular ganglia: Insights into the generation of sensory neurons by the neural crest

Cited by 15 publications

References 35 publications

Midline-derived Shh regulates mesonephric tubule formation through the paraxial mesoderm

Midline-derived Shh regulates mesonephric tubule formation through the paraxial mesoderm

Cranial neural crest cells form corridors prefiguring sensory neuroblast migration

The emergence of mesencephalic trigeminal neurons

Contact Info

Product

Resources

About