Neuronal subtype specification in the spinal cord of a protovertebrate

Stolfi, Alberto; Levine, Michael

doi:10.1242/dev.061507

Cited by 65 publications

(84 citation statements)

References 67 publications

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“…For example, we showed that FGF signaling is upstream of vsx2 during zebrafish retinal neurogenesis, as has been demonstrated in mouse RPCs Horsford et al, 2005). Moreover, our data indicate that vsx2 and dmbx1 function in an antagonistic manner in embryonic RPCs, similar to their homologs in Ciona that act to promote different types of motor ganglion interneurons from posterior neural tube progenitor cells (Stolfi and Levine, 2011). However, our findings also reveal novel insight into the regulation of this signaling axis.…”

Section: Discussionsupporting

confidence: 78%

“…As the proposed function for dmbx1 is to promote RPC cell cycle exit and differentiation cell-autonomously, we hypothesized that these two genes might function antagonistically during retinogenesis. Consistent with this notion, it has been reported that Dmbx1 and Vsx2 strongly repress each other during visceral ganglion cell fate specification in Ciona (Stolfi and Levine, 2011). Normally the expression of vsx2 is sharply down-regulated in the central retina at $48 hpf, coincident with the onset of dmbx1 expression (Chang et al, 2006).…”

Section: Dmbx1 Functions Cell Autonomously To Regulate Rpc Behaviorsupporting

confidence: 55%

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Mutual antagonism of the paired-type homeobox genes, vsx2 and dmbx1, regulates retinal progenitor cell cycle exit upstream of ccnd1 expression

Wong

Power

Miles

et al. 2015

Developmental Biology

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Understanding the mechanisms that regulate the transition between the proliferative and a post-mitotic state of retinal progenitor cells (RPCs) is key to advancing our knowledge of retinal growth and maturation. In the present study we determined that during zebrafish embryonic retinal neurogenesis, two paired-type homeobox genes - vsx2 and dmbx1 - function in a mutually antagonistic manner. We demonstrate that vsx2 gene expression requires active Fgf signaling and that this in turn suppresses dmbx1 expression and maintains cells in an undifferentiated, proliferative RPC state. This vsx2-dependent RPC state can be prolonged cell-autonomously by knockdown of dmbx1, or it can be suppressed prematurely by the over-expression of dmbx1, which we show can inhibit vsx2 expression and lead to precocious neuronal differentiation. dmbx1 loss of function also results in altered expression of canonical cell cycle genes, and in particular up-regulation of ccnd1, which correlates with our previous finding of a prolonged RPC cell cycle. By knocking down ccnd1 and dmbx1 simultaneously, we show that RPCs can overcome this phenotype to exit the cell cycle on time and differentiate normally into retinal neurons. Collectively, our data provide novel insight into the mechanism that enables RPCs to exit the cell cycle through a previously unrecognized antagonistic interaction of two paired-type homeobox genes that are central regulators of an Fgf-vsx2-dmbx1-ccnd1 signaling axis.

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Section: Discussionsupporting

confidence: 78%

Section: Dmbx1 Functions Cell Autonomously To Regulate Rpc Behaviorsupporting

confidence: 55%

Mutual antagonism of the paired-type homeobox genes, vsx2 and dmbx1, regulates retinal progenitor cell cycle exit upstream of ccnd1 expression

Wong

Power

Miles

et al. 2015

Developmental Biology

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“…The VAChT- positive MN outside the lineage was not affected by FGF8/17/18>COE::WRPW since it does not express FGF8/17/18 . Electroporation of FGF8/17/18>Ets::WRPW 43 converts the entire A9.30 lineage into cholinergic neurons, as predicted 44 , demonstrating the specificity of the COE::WRPW effect. Scale bar, 50μm.…”

Section: Figuresupporting

confidence: 62%

“…This fragment was cloned upstream of unc-76-tagged Venus (YFP). COE>mCherry and FGF8/17/18>H2B::mCherry have been previously described 44 . HA-tagged COE::WRPW 35 and Ets::WRPW 43 coding sequences were subcloned downstream of FGF8/17/18 driver in place of H2B::mCherry to make FGF8/17/18>COE::WRPW and FGF8/17/18>Ets::WRPW, respectively.…”

Section: Methodsmentioning

confidence: 99%

Coordinated regulation of cholinergic motor neuron traits through a conserved terminal selector gene

et al. 2011

Self Cite

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Cholinergic motor neurons are defined by the co-expression of a battery of genes which encode proteins that act sequentially to synthesize, package and degrade acetylcholine and reuptake its breakdown product, choline. How expression of these critical motor neuron identity determinants is controlled and coordinated is not understood. We show here that in the nematode Caenorhabditis elegans all members of the cholinergic gene battery, as well as many other markers of terminal motor neuron fate, are co-regulated by a shared cis-regulatory signature and a common trans-acting factor, the phylogenetically conserved COE (Collier/Olf/EBF)-type transcription factor UNC-3. UNC-3 initiates and maintains expression of cholinergic fate markers and is sufficient to induce cholinergic fate in other neuron types. UNC-3 furthermore operates in negative feedforward loops to induce the expression of transcription factors that repress individual, UNC-3-induced terminal fate markers resulting in diversification of motor neuron differentiation programs in specific motor neuron subtypes. A chordate ortholog of UNC-3, Ciona intestinalis COE, is also both required and sufficient for inducing a cholinergic fate. Thus, UNC-3 is a terminal selector for cholinergic motor neuron differentiation whose function is conserved across phylogeny.

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“…5B). A/A n 10.57 also displayed a more elongated shape along its anterior-posterior axis than the other perimeter cells (Imai and Meinertzhagen, 2007a;Okada et al, 2002;Stolfi and Levine, 2011). Using these morphological landmarks, we could find the borders between the neck, VG, and caudal NT (Fig.…”

Section: Sensory Vesicle (Sv)mentioning

confidence: 87%

Three-dimensional anatomy of the Ciona intestinalis tailbud embryo at single-cell resolution

Nakamura

Terai

Okubo

et al. 2012

Developmental Biology

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During embryogenesis, chordates pass through a tailbud stage in which the larval tail is formed. Since acquisition of a tadpole-like tail during tailbud stage is one of the key events in the evolution of chordates, understanding the anatomy of the tailbud stage chordate embryo is of special interest. In this study, to understand comprehensively the anatomy of the tailbud embryo at single-cell-level, real microscopic image stacks of the tailbud embryo in Ciona intestinalis were reconstructed into a 3D computer model. This comprehensive 3D model of the ascidian tailbud embryo was based on real images of confocal laser scanning microscope (CLSM) and therefore, cell shape, location and cell arrangement reflect real geometries of the tailbud embryo. We found that the tailbud embryo consists of 1579 cells, including 836 epidermal cells, 228 cells in the central nervous system, 218 mesenchymal cells, four trunk ventral cells, two B/B(⁎)8.11 cells, 36 muscle cells, 40 notochord cells, four primordial germ cells, and 199 endodermal cells. Moreover, we identified for the first time two populations of previously undefined cells (a total of 12 cells) in Ciona: one located in the lateral trunk and the other located under the tail dorsal epidermis. This information provides a first step for understanding how the body plan of the chordate tailbud embryo formed and evolved.

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Neuronal subtype specification in the spinal cord of a protovertebrate

Cited by 65 publications

References 67 publications

Mutual antagonism of the paired-type homeobox genes, vsx2 and dmbx1, regulates retinal progenitor cell cycle exit upstream of ccnd1 expression

Mutual antagonism of the paired-type homeobox genes, vsx2 and dmbx1, regulates retinal progenitor cell cycle exit upstream of ccnd1 expression

Coordinated regulation of cholinergic motor neuron traits through a conserved terminal selector gene

Three-dimensional anatomy of the Ciona intestinalis tailbud embryo at single-cell resolution

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