A comprehensive survey of wnt and frizzled expression in the sea urchin Paracentrotuslividus

Naeije, Robert; Lhomond, Guy; Schubert, Michael; Croce, Jenifer C.

doi:10.1002/dvg.22754

Cited by 35 publications

(66 citation statements)

References 44 publications

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“…S2 and S3. Similar results have been established in the embryos of a related species of sea urchin, Paracentrotus lividus (21). Because this study focuses on identifying the function of Wnt signaling in the interaction between different cell-fate specification processes, we have represented individual gene-expression patterns abstractly according to their embryonic expression domain (Fig.…”

Section: Resultsmentioning

confidence: 73%

Specific functions of the Wnt signaling system in gene regulatory networks throughout the early sea urchin embryo

Cui

Siriwon

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Wnt signaling affects cell-fate specification processes throughout embryonic development. Here we take advantage of the well-studied gene regulatory networks (GRNs) that control pregastrular sea urchin embryogenesis to reveal the gene regulatory functions of the entire Wnt-signaling system. Five wnt genes, three frizzled genes, two secreted frizzled-related protein 1 genes, and two Dickkopf genes are expressed in dynamic spatial patterns in the pregastrular embryo of Strongylocentrotus purpuratus. We present a comprehensive analysis of these genes in each embryonic domain. Total functions of the Wnt-signaling system in regulatory gene expression throughout the embryo were studied by use of the Porcupine inhibitor C59, which interferes with zygotic Wnt ligand secretion. Morpholino-mediated knockdown of each expressed Wnt ligand demonstrated that individual Wnt ligands are functionally distinct, despite their partially overlapping spatial expression. They target specific embryonic domains and affect particular regulatory genes. The sum of the effects of blocking expression of individual wnt genes is shown to equal C59 effects. Remarkably, zygotic Wnt-signaling inputs are required for only three general aspects of embryonic specification: the broad activation of endodermal GRNs, the regional specification of the immediately adjacent stripe of ectoderm, and the restriction of the apical neurogenic domain. All Wnt signaling in this pregastrular embryo is short range (and/or autocrine). Furthermore, we show that the transcriptional drivers of wnt genes execute important specification functions in the embryonic domains targeted by the ligands, thus connecting the expression and function of wnt genes by encoded crossregulatory interactions within the specific regional GRNs. embryonic interdomain signaling | developmental GRNs | Wnt system regulatory functions | Porcupine T he formation of spatial patterns of gene expression and the development of the body plan are controlled by gene regulatory networks (GRNs). Signaling interactions have a particular role in these networks, in that they provide the means of communication between cell-fate specification processes operating in separate cellular domains. The timing, location, and function of each signaling interaction is determined by GRN linkages that control the expression of signaling ligands and receptors as well as the expression of regulatory genes in response to a combination of signaling inputs and cell fate-specific transcription factors. Cell-fate specification GRNs active during pregastrular development of the sea urchin Strongylocentrotus purpuratus are particularly well understood. During the first 30 h of sea urchin embryogenesis, more than 15 gene-expression domains are formed, and specifically expressed regulatory genes have been identified for each domain. In most cases, the regulatory mechanisms determining their spatial expression patterns have been resolved. Thus, fairly complete GRN models have been constructed for the majority of cell-fate domains in ...

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Section: Resultsmentioning

confidence: 73%

Specific functions of the Wnt signaling system in gene regulatory networks throughout the early sea urchin embryo

Cui

Siriwon

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…Phylogenetic analysis of X. bocki Wnt relatives was performed as explained previously [29], using a maximum-likelihood approach with the program RAxML and 100 bootstrap replications. The alignment of the reference species was provided by Dr J. C. Croce [80] and included the sequences from the species Pl, Lg, Hs and Xt (see below for abbreviations); the other sequences are used in Kusserow et al [81] and were downloaded from the NCBI database, the accession numbers are indicated after the name. Protein families are highlighted in different colours.…”

Section: A Genomics View Of Xenacoelomorpha Neurogenesismentioning

confidence: 99%

Xenacoelomorpha: a case of independent nervous system centralization?

Gavilán

Perea-Atienza

Martı́nez

2016

Phil. Trans. R. Soc. B

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One contribution of 16 to a discussion meeting issue 'Homology and convergence in nervous system evolution'. Centralized nervous systems (NSs) and complex brains are among the most important innovations in the history of life on our planet. In this context, two related questions have been formulated: How did complex NSs arise in evolution, and how many times did this occur? As a step towards finding an answer, we describe the NS of several representatives of the Xenacoelomorpha, a clade whose members show different degrees of NS complexity. This enigmatic clade is composed of three major taxa: acoels, nemertodermatids and xenoturbellids. Interestingly, while the xenoturbellids seem to have a rather 'simple' NS (a nerve net), members of the most derived group of acoel worms clearly have ganglionic brains. This interesting diversity of NS architectures (with different degrees of compaction) provides a unique system with which to address outstanding questions regarding the evolution of brains and centralized NSs. The recent sequencing of xenacoelomorph genomes gives us a privileged vantage point from which to analyse neural evolution, especially through the study of key gene families involved in neurogenesis and NS function, such as G protein-coupled receptors, helixloop-helix transcription factors and Wnts. We finish our manuscript proposing an adaptive scenario for the origin of centralized NSs (brains).

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“…Four Frizzled receptor genes have been identified so far in the Strongylocentrotus purpuratus genome but no information is available about the expression dynamics of these genes during embryogenesis. The expression of these receptors has been deeply investigated in another sea urchin species, Paracentrotus lividus, indicating Fzd9/10 as possible candidate for mediating Wnt10 signaling in the hindgut (Croce et al, 2006;Lhomond et al, 2012;Robert et al, 2014). It would be interesting to study the dynamics of expression of the four Frizzled receptor genes in S. purpuratus in order to identify a possible candidate for the transduction of the Wnt10 signal to the intestinal cells.…”

Section: Conserved Function and Regulation In Intestine Differentmentioning

confidence: 99%

A dynamic regulatory network explains ParaHox gene control of gut patterning in the sea urchin

Annunziata

Arnone

2014

Development

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The anteroposterior patterning of the embryonic gut represents one of the most intriguing biological processes in development. A dynamic control of gene transcription regulation and cell movement is perfectly orchestrated to shape a functional gut in distinct specialized parts. Two ParaHox genes, Xlox and Cdx, play key roles in vertebrate and sea urchin gut patterning through molecular mechanisms that are still mostly unclear. Here, we have combined functional analysis methodologies with high-resolution imaging and RNA-seq to investigate Xlox and Cdx regulation and function. We reveal part of the regulatory machinery responsible for the onset of Xlox and Cdx transcription, uncover a Wnt10 signal that mediates Xlox repression in the intestinal cells, and provide evidence of Xlox-and Cdx-mediated control of stomach and intestine differentiation, respectively. Our findings offer a novel mechanistic explanation of how the control of transcription is linked to cell differentiation and morphogenesis for the development of a perfectly organized biological system such as the sea urchin larval gut.

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A comprehensive survey of wnt and frizzled expression in the sea urchin Paracentrotuslividus

Cited by 35 publications

References 44 publications

Specific functions of the Wnt signaling system in gene regulatory networks throughout the early sea urchin embryo

Specific functions of the Wnt signaling system in gene regulatory networks throughout the early sea urchin embryo

Xenacoelomorpha: a case of independent nervous system centralization?

A dynamic regulatory network explains ParaHox gene control of gut patterning in the sea urchin

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