Nuclear accumulation of β‐catenin and transcription of downstream genes are regulated by zygotic Wnt5α and maternal Dsh in ascidian embryos

Kawai, Nobuyoshi; Iida, Yoshihiro; Kumano, Gaku; Nishida, Hiroki

doi:10.1002/dvdy.21169

Cited by 29 publications

(27 citation statements)

References 60 publications

(49 reference statements)

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“…The regulated stabilisation of bcatenin is required to specify endomesodermal fate and leads to activation of a specific transcriptional regulatory network that is responsible for fate specification and differentiation. A very similar situation has been described in other deuterostomes (other echinoderms and in ascidians that belong to chordates) (Imai et al, 2000;Kawai et al, 2007;Miyawaki et al, 2003). In bilaterians outside of deuterostomes, the function of the Wnt/b-catenin pathway has been deciphered in great detail in the ecdysozoan model systems C. elegans and D. melanogaster, in which it is involved in different aspects of anteroposterior polarity.…”

Section: Introductionsupporting

confidence: 56%

“…The Wnt/b-catenin pathway is activated at the vegetal pole As knockdown of b-catenin leads to animalized embryos in both ascidians and sea urchins (Imai et al, 2000;Kawai et al, 2007;Logan et al, 1999;Wikramanayake et al, 1998), we tested whether this pathway had a similar function in S. kowalevskii. When the Wnt/b-catenin pathway is activated, b-catenin protein becomes stabilized and translocates to the nucleus where it activates transcriptional targets.…”

Section: Research Articlementioning

confidence: 99%

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β-Catenin specifies the endomesoderm and defines the posterior organizer of the hemichordate Saccoglossus kowalevskii

et al. 2011

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SUMMARYThe canonical Wnt/b-catenin pathway is a key regulator of body plan organization and axis formation in metazoans, being involved in germ layer specification, posterior growth and patterning of the anteroposterior axis. Results from animals spanning a wide phylogenetic range suggest that a unifying function of b-catenin in metazoans is to define the posterior/vegetal part of the embryo. Although the specification of vegetal territories (endoderm) by b-catenin has been demonstrated in distantly related animals (cnidarians, a protostome, echinoderms and ascidians), the definition of the posterior part of the embryo is well supported only for vertebrates and planarians. To gain insights into b-catenin functions during deuterostome evolution, we have studied the early development of the direct developing hemichordate Saccoglossus kowalevskii. We show that the zygote is polarized after fertilization along the animal-vegetal axis by cytoplasmic rearrangements resembling the ascidian vegetal contraction. This early asymmetry is translated into nuclear accumulation of b-catenin at the vegetal pole, which is necessary and sufficient to specify endomesoderm. We show that endomesoderm specification is crucial for anteroposterior axis establishment in the ectoderm. The endomesoderm secretes as yet unidentified signals that posteriorize the ectoderm, which would otherwise adopt an anterior fate. Our results point to a conserved function at the base of deuterostomes for b-catenin in germ layer specification and to a causal link in the definition of the posterior part of the embryonic ectoderm by way of activating posteriorizing endomesodermal factors. Consequently, the definition of the vegetal and the posterior regions of the embryo by b-catenin should be distinguished and carefully re-examined.

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Section: Introductionsupporting

confidence: 56%

Section: Research Articlementioning

confidence: 99%

β-Catenin specifies the endomesoderm and defines the posterior organizer of the hemichordate Saccoglossus kowalevskii

et al. 2011

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“…-catenin, in turn, activates a gene regulatory network that leads to specification of the endoderm (Davidson et al, 2002a). It has been suggested that the role of -catenin in specification of the endomesodermal germ layer might reflect an ancestral function because it is conserved in other deuterostomes and in cnidarians (Kawai et al, 2007;Momose and Houliston, 2007;Wikramanayake et al, 2003). In vertebrates, however, TGF signals, not Wnts, appear to be the primary inducers of the endoderm.…”

Section: Nodal Signalling and Endoderm Formationmentioning

confidence: 99%

Nodal and BMP2/4 pattern the mesoderm and endoderm during development of the sea urchin embryo

et al. 2010

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SUMMARYNodal factors play fundamental roles in induction and patterning of the mesoderm and endoderm in vertebrates, but whether this reflects an ancient role or one that evolved recently in vertebrates is not known. Here, we report that in addition to its primary role in patterning the ectoderm, sea urchin Nodal is crucial for patterning of the endoderm and skeletogenic mesoderm through the regulation of the expression of key transcription factors and signalling molecules, including BMP2/4 and FGFA. In addition, we uncovered an essential role for Nodal and BMP2/4 in the formation and patterning of the non-skeletogenic mesoderm. By comparing the effects of misexpressing Nodal or an activated Nodal receptor in clones of cells, we provide evidence that Nodal acts over a long range in the endomesoderm and that its effects on the blastocoelar cell precursors are likely to be direct. The activity of Nodal and BMP2/4 are antagonistic, and although bmp2/4 is transcribed in the ventral ectoderm downstream of Nodal, the BMP2/4 ligand is translocated to the dorsal side, where it activates signalling in the dorsal primary mesenchyme cells, the dorsal endoderm and in pigment cell precursors. Therefore, correct patterning of the endomesoderm depends on a balance between ventralising Nodal signals and dorsalising BMP2/4 signals. These experiments confirm that Nodal is a key regulator of dorsal-ventral polarity in the sea urchin and support the idea that the ventral ectoderm, like the Spemann organiser in vertebrates, is an organising centre that is required for patterning all three germ layers of the embryo.

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“…The knockdown (KD) of pem-1 causes irregular cleavages of the posterior blastomeres because the centrosome-CAB linkage is interrupted, owing to collapse of the microtubule bundles that connect them (Negishi et al, 2007;Prodon et al, 2010). Furthermore, although -catenin normally accumulates in the nucleus of only the vegetal somatic blastomeres, where it regulates the expression of -catenin/TCF-dependent genes during the cleavage stages (Imai et al, 2000;Kawai et al, 2007), pem-1 KD in H. roretzi embryos causes the nuclear accumulation of -catenin in the germline blastomeres, resulting in the ectopic expression of -catenin/TCF-dependent genes, such as FoxA-a, FoxD and FGF9/16/20 (Kumano and Nishida, 2009). Therefore, Pem-1 regulates, directly or indirectly, the position of cleavage planes and -catenin/TCF-dependent transcription.…”

Section: Introductionmentioning

confidence: 99%

Ci-Pem-1 localizes to the nucleus and represses somatic gene transcription in the germline of Ciona intestinalis embryos

Shirae-Kurabayashi¹,

Matsuda²,

Nakamura³

2011

Development

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In many animal embryos, germ-cell formation depends on maternal factors located in the germ plasm. To ensure the development of germ cells, germline progenitors must be prevented from differentiating inappropriately into somatic cells. A common mechanism for this appears to be the active repression of somatic gene transcription. Species-specific germ-plasm components, such as Pgc in Drosophila and PIE-1 in C. elegans, establish germline transcriptional quiescence by inhibiting general transcriptional machineries. In the ascidian Ciona intestinalis, although transcriptional repression in the germline has been proposed, the factors and mechanisms involved have been unknown. We found that the protein products of Ci-pem-1 RNA, which is an ascidian-specific component of the postplasm (the germ plasm equivalent in ascidians), localized to the nucleus of germline blastomeres, as well as to the postplasm. Morpholino oligonucleotide-mediated Ci-pem-1 knockdown resulted in the ectopic expression of several somatic genes that are usually silent in the germline. In the Ci-pem-1 knockdown embryos, the expression of both β-catenin- and GATAa-dependent genes was derepressed in the germline blastomeres, suggesting that Ci-Pem-1 broadly represses germline mRNA transcription. Immunoprecipitation assays showed that Ci-Pem-1 could interact with two C. intestinalis homologs of Groucho, which is a general co-repressor of mRNA transcription. These results suggest that Ci-pem-1 is the C. intestinalis version of a germ-plasm RNA whose protein product represses the transcription of somatic genes during specification of the germ-cell fate, and that this repression may be operated through interactions between Ci-Pem-1 and Groucho co-repressors.

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Nuclear accumulation of β‐catenin and transcription of downstream genes are regulated by zygotic Wnt5α and maternal Dsh in ascidian embryos

Cited by 29 publications

References 60 publications

β-Catenin specifies the endomesoderm and defines the posterior organizer of the hemichordate Saccoglossus kowalevskii

β-Catenin specifies the endomesoderm and defines the posterior organizer of the hemichordate Saccoglossus kowalevskii

Nodal and BMP2/4 pattern the mesoderm and endoderm during development of the sea urchin embryo

Ci-Pem-1 localizes to the nucleus and represses somatic gene transcription in the germline of Ciona intestinalis embryos

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