Sea urchin neural development and the metazoan paradigm of neurogenesis

Burke, Robert D.; Möller, Daniel; Krupke, Oliver A.; Taylor, Valerie Jones

doi:10.1002/dvg.22750

Cited by 41 publications

(38 citation statements)

References 84 publications

(172 reference statements)

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“…Although there are significant differences in the nervous systems created from this early territory among the deuterostomes, the ANE initially arises from a relatively simple, flat neuroepithelium during the early stages of development and many of the cell types that this territory produces are remarkably conserved (Burke et al, 2014;Castro et al, 2015;Cavodeassi, 2013;Garner et al, 2015;Pani et al, 2012;Range, 2014). Based on the spatial and temporal expression of ANE regulatory genes in several species, it appears that the ANE gene regulatory network (GRN) hierarchy is also remarkably conserved among many deuterostome embryos, suggesting that these could be homologous territories (Range, 2014).…”

Section: Introductionmentioning

confidence: 99%

An anterior signaling center patterns and sizes the anterior neuroectoderm of the sea urchin embryo

Range

Wen-ling

2016

Development

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Anterior signaling centers help specify and pattern the early anterior neuroectoderm (ANE) in many deuterostomes. In sea urchin the ANE is restricted to the anterior of the late blastula stage embryo, where it forms a simple neural territory comprising several types of neurons as well as the apical tuft. Here, we show that during early development, the sea urchin ANE territory separates into inner and outer regulatory domains that express the cardinal ANE transcriptional regulators FoxQ2 and Six3, respectively. FoxQ2 drives this patterning process, which is required to eliminate six3 expression from the inner domain and activate the expression of Dkk3 and sFRP1/5, two secreted Wnt modulators. Dkk3 and low expression levels of sFRP1/5 act additively to potentiate the Wnt/JNK signaling pathway governing the positioning of the ANE territory around the anterior pole, whereas high expression levels of sFRP1/5 antagonize Wnt/JNK signaling. sFRP1/5 and Dkk3 levels are rigidly maintained via autorepressive and cross-repressive interactions with Wnt signaling components and additional ANE transcription factors. Together, these data support a model in which FoxQ2 initiates an anterior patterning center that implements correct size and positions of ANE structures. Comparisons of functional and expression studies in sea urchin, hemichordate and chordate embryos reveal striking similarities among deuterostome ANE regulatory networks and the molecular mechanism that positions and defines ANE borders. These data strongly support the idea that the sea urchin embryo uses an ancient anterior patterning system that was present in the common ambulacrarian/chordate ancestor.

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Section: Introductionmentioning

confidence: 99%

An anterior signaling center patterns and sizes the anterior neuroectoderm of the sea urchin embryo

Range

Wen-ling

2016

Development

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“…Simultaneous hybridization with probes for Hnf6 (also known as onecut), which is an APD/ ciliary band marker, and SoxC transcripts showed that SoxCexpressing cells lie adjacent to, or within, the ciliary band and APD ( Fig. 1G-I′, arrowheads), as expected for neural precursors (Burke et al, 2014). Further supporting this identity, cells in both the apical plate and lateral ectoderm that express SoxC also express Delta (Fig.…”

Section: Soxc Function Is Required Downstream Of Six3 For Developmentmentioning

confidence: 57%

“…At the end of embryogenesis the nervous system of the sea urchin early pluteus larva includes an apical ganglion in the apical plate at the anterior (animal) pole, a set of 40-50 peripheral neurons, most of which differentiate in, or adjacent to, the ciliary band, and a few neurons that differentiate in the pharyngeal endoderm Wei et al, 2009;Range et al, 2013;Burke et al, 2014) (Fig. S1).…”

Section: Introductionmentioning

confidence: 99%

“…The apical organ develops within a distinct regulatory domain termed the animal pole domain (APD) , which encompasses 10-15% of the blastula surrounding the anterior pole. The patterns of gene expression in the APD become increasingly complex during later larval development and, in addition to the apical ganglion, it generates the apical tuft of cilia and several different groups of cells identified by expression of specific genes with neurogenic functions in other organisms (Burke et al, 2014); the first of these to appear are 2-6 neurons at the posterior margin within the APD, which express serotonin and tryptophan hydroxylase (Tph), an enzyme in the serotonin biosynthesis pathway. The peripheral neurons send projections along the ciliary band to the apical organ and out into the dorsal ectoderm (Burke et al, 2014); the apical ganglion is thought to have sensory and integrating functions, while the ciliary band neurons are thought to have sensory function, and together they are proposed to coordinate the ciliary beat.…”

Section: Introductionmentioning

confidence: 99%

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Neurogenic gene regulatory pathways in the sea urchin embryo

Wen-ling

Angerer

2015

Development

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During embryogenesis the sea urchin early pluteus larva differentiates 40-50 neurons marked by expression of the panneural marker synaptotagmin B (SynB) that are distributed along the ciliary band, in the apical plate and pharyngeal endoderm, and 4-6 serotonergic neurons that are confined to the apical plate. Development of all neurons has been shown to depend on the function of Six3. Using a combination of molecular screens and tests of gene function by morpholino-mediated knockdown, we identified SoxC and Brn1/2/4, which function sequentially in the neurogenic regulatory pathway and are also required for the differentiation of all neurons. Misexpression of Brn1/2/4 at low dose caused an increase in the number of serotonin-expressing cells and at higher dose converted most of the embryo to a neurogenic epithelial sphere expressing the Hnf6 ciliary band marker. A third factor, Z167, was shown to work downstream of the Six3 and SoxC core factors and to define a branch specific for the differentiation of serotonergic neurons. These results provide a framework for building a gene regulatory network for neurogenesis in the sea urchin embryo.

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“…SoxB genes have been associated with broad neurogenic functions throughout the animal kingdom, from deuterostomes (chordates, echinoderms, hemichordates) (Burke et al, 2014;Reiprich and Wegner, 2014;Taguchi et al, 2002) and protostomes (Ecdysozoa, Lophotrochozoa) (Kerner et al, 2009;Overton et al, 2002) to even earlier diverging animal lineages such as cnidarians (Richards and Rentzsch, 2014). SoxB proteins are required for neuronal commitment broadly throughout the embryonic nervous system during the earliest stages of development, predominantly in proliferating, undifferentiated precursors (Pevny and Placzek, 2005;Pevny and Nicolis, 2010;Reiprich and Wegner, 2014;Sarkar and Hochedlinger, 2013).…”

Section: Discussionmentioning

confidence: 99%

C. elegansSoxB genes are dispensable for embryonic neurogenesis but required for terminal differentiation of specific neuron types

et al. 2015

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Neurogenesis involves deeply conserved patterning molecules, such as the proneural basic helix-loop-helix transcription factors. Sox proteins and specifically members of the SoxB and SoxC groups are another class of conserved transcription factors with an important role in neuronal fate commitment and differentiation in various species. In this study, we examine the expression of all five Sox genes of the nematode C. elegans and analyze the effect of null mutant alleles of all members of the SoxB and SoxC groups on nervous system development. Surprisingly, we find that, unlike in other systems, neither of the two C. elegans SoxB genes sox-2 (SoxB1) and sox-3 (SoxB2), nor the sole C. elegans SoxC gene sem-2, is broadly expressed throughout the embryonic or adult nervous system and that all three genes are mostly dispensable for embryonic neurogenesis. Instead, sox-2 is required to maintain the developmental potential of blast cells that are generated in the embryo but divide only postembryonically to give rise to differentiated neuronal cell types. Moreover, sox-2 and sox-3 have selective roles in the terminal differentiation of specific neuronal cell types. Our findings suggest that the common themes of SoxB gene function across phylogeny lie in specifying developmental potential and, later on, in selectively controlling terminal differentiation programs of specific neuron types, but not in broadly controlling neurogenesis.

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Sea urchin neural development and the metazoan paradigm of neurogenesis

Cited by 41 publications

References 84 publications

An anterior signaling center patterns and sizes the anterior neuroectoderm of the sea urchin embryo

An anterior signaling center patterns and sizes the anterior neuroectoderm of the sea urchin embryo

Neurogenic gene regulatory pathways in the sea urchin embryo

C. elegansSoxB genes are dispensable for embryonic neurogenesis but required for terminal differentiation of specific neuron types

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