The sea urchin animal pole domain is a Six3-dependent neurogenic patterning center

Wen-ling, Zheng; Yaguchi, Junko; Yaguchi, Shunsuke; Angerer, Robert C.; Angerer, Lynne M.

doi:10.1242/dev.032300

Cited by 105 publications

(139 citation statements)

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“…Among those that were expressed in the anterior neuroectoderm (ANE) was one encoding a zinc finger-containing protein, called Z81 (Materna et al, 2006). Further studies showed that its expression in the ANE depended on Six3, a factor required for neural development (Wei et al, 2009). This gene (Z81; SPU_022242) was initially annotated as zfh-1 (Sodergren et al, 2006) and has subsequently been called Smad Interacting protein, Sip1 or SmadIP (Saudemont et al, 2010) or SpSip1 (Su et al, 2009).…”

Section: Resultsmentioning

confidence: 99%

Zinc finger homeobox is required for the differentiation of serotonergic neurons in the sea urchin embryo

Yaguchi

Angerer

Inaba

et al. 2012

Developmental Biology

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Serotonergic neurons differentiate in the neurogenic animal plate ectoderm of the sea urchin embryo. The regulatory mechanisms that control the specification or differentiation of these neurons in the sea urchin embryo are not yet understood, although, after the genome was sequenced, many genes encoding transcription factors expressed in this region were identified. Here, we report that zinc finger homeobox (zfhx1/z81) is expressed in serotonergic neural precursor cells, using double in situ hybridization screening with a serotonergic neural marker, tryptophan 5-hydroxylase (tph) encoding a serotonin synthase that is required for the differentiation of serotonergic neurons. zfhx1/z81 begins to be expressed at gastrula stage in individual cells in the anterior neuroectoderm, some of which also express delta. zfhx1/z81 expression gradually disappears as neural differentiation begins with tph expression. When the translation of Zfhx1/Z81 is blocked by morpholino injection, embryos express neither tph nor the neural marker synaptotagminB in cells of the animal plate, and serotonergic neurons do not differentiate. In contrast, Zfhx1/Z81 morphants do express fez, another neural precursor marker, which appears to function in the initial phase of specification/differentiation of serotonergic neurons. In addition, zfhx1/z81 is one of the targets suppressed in the animal plate by anti-neural signals such as Nodal as well as Delta-Notch. We conclude that Zfhx1/Z81 functions during the specification of individual anterior neural precursors and promotes the expression of tph and synaptotagminB, required for the differentiation of serotonergic neurons.

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Section: Resultsmentioning

confidence: 99%

Zinc finger homeobox is required for the differentiation of serotonergic neurons in the sea urchin embryo

Yaguchi

Angerer

Inaba

et al. 2012

Developmental Biology

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“…A common feature is the presence of bilaterally displaced serotonin containing neurons (Bisgrove and Burke, 1986;Yaguchi and Katow 2003;Byrne et al 2006). The differentiation of the neurogenic ectoderm appears to be mediated by a core set of metazoan neural transcription factors, including the transcription factors paired-class, achaete-scute, Zic, Six-3 Poustka et al 2007;Wei et al 2009). Wei et al (2009) have identified a large set of animal pole domain regulatory genes that depend upon Six-3 expression and suggest that a gene regulatory network involving Six-3 is necessary for the differentiation of this domain.…”

Section: The Animal Pole Nervous Systemmentioning

confidence: 99%

“…The differentiation of the neurogenic ectoderm appears to be mediated by a core set of metazoan neural transcription factors, including the transcription factors paired-class, achaete-scute, Zic, Six-3 Poustka et al 2007;Wei et al 2009). Wei et al (2009) have identified a large set of animal pole domain regulatory genes that depend upon Six-3 expression and suggest that a gene regulatory network involving Six-3 is necessary for the differentiation of this domain. Neurons associated with the ciliary band also differentiate during late gastrulation (Nakajima et al 2004a).…”

Section: The Animal Pole Nervous Systemmentioning

confidence: 99%

“…2). The location and development of the animal pole component of ambulacrarian nervous systems is similar to the chordate forebrain (Wei et al 2009). While the morphogenesis, segmentation and axial nature of the ambulacral nerve cords are similar to the dorsal nerve cords of chordates.…”

Section: Deuterostome Neural Organizationmentioning

confidence: 99%

“…The similarities in morphogenesis and cellular and tissue organization are really a manifestation of the inherited genetic networks that underlie them (Davidson 2006;Davidson and Erwin 2006). Wei et al (2009) noted that vertebrate forebrain and the animal pole neurons of the sea urchin express a similar suite of transcription factors that appear to be regulated by Six-3. They speculated that a similar gene regulatory networks was involved in the specification of vertebrate forebrain and the animal pole domain of sea urchins.…”

Section: Deuterostome Neural Organizationmentioning

confidence: 99%

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Deuterostome neuroanatomy and the body plan paradox

Burke¹

2011

Evolution &Amp; Development

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The paradox of deuterostome body plans is that genome analyses indicate deuterostomes are a group with strong kinship, yet they are an assemblage with what appear to be distinctly different body plans. The two major deuterostome groups, chordates and ambulacraria, are allied by features of their anatomy that do not include the nervous systems. Here I review data emerging from neuroanatomical studies that indicate echinoderms and hemichordates have two distinct parts to their nervous systems. In this brief perspective, I propose the hypothesis that in the ambulacraria the two parts are separated spatially and temporally over life history stages, whereas in chordates the two parts are united in a single central nervous systems. This view provides a means of including neuroanatomy in a common deuterostome body plan.

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Sea Urchin Embryo: Specification of Cell Fates

Angerer

2012

Encyclopedia of Life Sciences

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Specification of cell fate in sea urchin embryos involves initial asymmetric distribution of maternal molecules that establish posterior and anterior domains of transcription activity. Subsequently, fates of most blastomeres along the anterior–posterior and dorsal–ventral axes of the embryo are patterned by cell–cell interactions involving signalling ligands and cell surface receptors. These signalling pathways regulate the operation of networks of genes encoding transcription factors and additional signals, which guide the terminal differentiation of different cell types. Most of the signalling mechanisms that establish different embryonic territories and some of the transcription factors that specify cell types are highly conserved with those that pattern vertebrate embryos. The relative simplicity of the sea urchin embryo and the existence of tools for rapidly determining gene function provide clear advantages for understanding how early developmental processes work. Key Concepts: Sea urchin embryogenesis employs the two common mechanisms of early fate specification, inheritance of maternal molecules and signalling among cells. The maternally derived initial state, in the absence of all known signals sent among the cells of the embryo, promotes development of anterior neuroectoderm, a region of ectoderm within which nerves develop. Early posterior canonical Wnt signalling activates transcription factors followed by additional signals that convert posterior blastomeres to mesoderm and endoderm and restrict the anterior neuroectoderm fate to the anterior end of the embryo. Patterning of anterior (neuroectoderm) and posterior (endomesoderm) fates requires mutual antagonism between the gene regulatory networks headed by Wnt and Six3, respectively. Nodal signalling is necessary and sufficient for specification of fates along the dorsal–ventral axis, including oral and aboral ectoderm types. Anterior–posterior (AP) and dorsal–ventral (DV) patterning are interconnected and temporally coordinated because early posterior canonical Wnt signalling is required to derepress nodal expression. The components of the major tissue territory gene regulatory networks (GRNs) have been identified by studying embryos lacking signalling through canonical Wnt, Nodal or BMP, and their functional relationships determined by knocking down each of the corresponding proteins in vivo with morpholino oligonucleotides and monitoring effects on expression of other genes. Individual cell types in sea urchin embryos are determined when their fates cannot be changed experimentally; this process requires stable activation of genes necessary for specification of a particular cell type and stable repression of those required for specification of other cell types. The GRN devices that produce stable regulatory states are reinforcing cross‐regulatory and feedback loops among the component transcription factors, which render these states insensitive to signals. The sea urchin embryo has enormous capacity before larval stages to change cell fates upon experimental challenge because the fates of many cells are only gradually specified and can be altered by signals sent from other cells.

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The sea urchin animal pole domain is a Six3-dependent neurogenic patterning center

Cited by 105 publications

References 56 publications

Zinc finger homeobox is required for the differentiation of serotonergic neurons in the sea urchin embryo

Zinc finger homeobox is required for the differentiation of serotonergic neurons in the sea urchin embryo

Deuterostome neuroanatomy and the body plan paradox

Sea Urchin Embryo: Specification of Cell Fates

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