Co-expression of Foxa.a, Foxd and Fgf9/16/20 defines a transient mesendoderm regulatory state in ascidian embryos

Hudson, C. S.; Sirour, Cathy; Yasuo, Hitoyoshi

doi:10.7554/elife.14692

Cited by 39 publications

(39 citation statements)

References 73 publications

(119 reference statements)

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“…a expression begins at the 8-cell stage, and our data did not indicate downregulation of Foxa . a at the 32-cell stage (Fig 2A), which is consistent with a recent study [16]. Nkx2-1 was normally expressed in the vegetal blastomeres designated A7.1, A7.2, A7.5, B7.1, and B7.2 at the 64-cell stage (Fig 3D), whereas it was not expressed in Foxd morphants (Fig 3E), as recently shown at the early gastrula stage [16].…”

Section: Resultssupporting

confidence: 93%

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Differential gene expression along the animal-vegetal axis in the ascidian embryo is maintained by a dual functional protein Foxd

et al. 2017

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In many animal embryos, a specific gene expression pattern is established along the animal-vegetal axis soon after zygotic transcription begins. In the embryo of the ascidian Ciona intestinalis, soon after the division that separates animal and vegetal hemispheres into distinct blastomeres, maternal Gata.a and β-catenin activate specific genes in the animal and vegetal blastomeres, respectively. On the basis of these initial distinct gene expression patterns, gene regulatory networks promote animal cells to become ectodermal tissues and vegetal cells to become endomesodermal tissues and a part of the nerve cord. In the vegetal hemisphere, β-catenin directly activates Foxd, an essential transcription factor gene for specifying endomesodermal fates. In the present study, we found that Foxd also represses the expression of genes that are activated specifically in the animal hemisphere, including Dmrt1, Prdm1-r.a (Bz1), Prdm1-r.b (Bz2), and Otx. A reporter assay showed that Dmrt1 expression was directly repressed by Foxd, and a chromatin immunoprecipitation assay showed that Foxd was bound to the upstream regions of Dmrt1, Prdm1-r.a, Prdm1-r.b, and Otx. Thus, Foxd has a dual function of activating specific gene expression in the vegetal hemisphere and of repressing the expression of genes that are normally expressed in the animal hemisphere. This dual function stabilizes the initial patterning along the animal-vegetal axis by β-catenin and Gata.a.

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Section: Resultssupporting

confidence: 93%

“…On the other hand, Fgf9/16/20 is not downregulated at the 32-cell stage [16, 17], which was also consistent with the RNA-seq result at the 32-cell stage (Fig 2A). Indeed, Fgf9/16/20 was not downregulated at the 16-cell stage in Foxd morphants (S1D and S1E Fig).…”

Section: Resultssupporting

confidence: 85%

Differential gene expression along the animal-vegetal axis in the ascidian embryo is maintained by a dual functional protein Foxd

et al. 2017

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“…Similarly, Foxa.a is activated in the endomesoderm precursors of the 16-cell embryo (Imai et al, 2004), and is required for correct Zic-r.b expression in NN and aMM cells (Fig. S4E) (Hudson et al, 2016). The mechanism of nβ-catenin-mediated transcriptional repression described in the present and previous (Oda- Ishii et al, 2016) studies is different from other mechanisms described in Caenorhabditis elegans and Drosophila melanogaster (Bertrand, 2016;Blauwkamp et al, 2008;Murgan et al, 2015).…”

Section: Discussioncontrasting

confidence: 52%

Antagonism between β-catenin and Gata.a sequentially segregates the germ layers of ascidian embryos

et al. 2016

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Many animal embryos use nuclear β-catenin (nβ-catenin) during the segregation of endomesoderm (or endoderm) from ectoderm. This mechanism is thus likely to be evolutionarily ancient. In the ascidian embryo, nβ-catenin reiteratively drives binary fate decisions between ectoderm and endomesoderm at the 16-cell stage, and then between endoderm and margin (mesoderm and caudal neural) at the 32-cell stage. At the 16-cell stage, nβ-catenin activates endomesoderm genes in the vegetal hemisphere. At the same time, nβ-catenin suppresses the DNA-binding activity of a maternal transcription factor, Gata.a, through a physical interaction, and Gata.a thereby activates its target genes only in the ectodermal lineage. In the present study, we found that this antagonism between nβ-catenin and Gata.a also operates during the binary fate switch at the 32-cell stage. Namely, in marginal cells where nβ-catenin is absent, Gata.a directly activates its target, Zic-r.b (ZicL), to specify the marginal cell lineages. Thus, the antagonistic action between nβ-catenin and Gata.a is involved in two consecutive stages of germ layer segregation in ascidian embryos.

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“…However, we could not rule out the possibility that signaling molecules secreted from surrounding cells regulate Snail expression. Given that Fgf9/16/20 begins to be zygotically expressed in vegetal cells, except B5.2 cells, of 16-cell embryos (Bertrand et al, 2003;Imai et al, 2002a) and activates genes encoding transcription factors and signaling molecules in 32-cell embryos (Bertrand et al, 2003;Hudson et al, 2016;Ikeda et al, 2013;Ikeda and Satou, 2017;Imai et al, 2002b), we next examined Snail expression in Fgf9/16/20 morphants and embryos treated with U0126, which is a specific inhibitor of the MAP kinase kinase, MEK. Snail expression did not change in most of the Fgf9/16/20 morphants (81%; Fig.…”

Section: The Mapk Pathway Is Activated Differently In the Posterior Bmentioning

confidence: 99%

Distinct regulation of Snail in two muscle lineages of the ascidian embryo achieves temporal coordination of muscle development

2018

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The transcriptional repressor Snail is required for proper differentiation of the tail muscle of ascidian tadpole larvae. Two muscle lineages (B5.1 and B6.4) contribute to the anterior tail muscle cells, and are consecutively separated from a transcriptionally quiescent germ cell lineage at the 16- and 32-cell stages. Concomitantly, cells of these lineages begin to express () at the 16- and 32-cell stages, respectively. Meanwhile, expression begins in these two lineages simultaneously at the 32-cell stage. Here, we show that expression is regulated differently between these two lineages. In the B5.1 lineage, was activated through, which is activated by maternal factors, including Zic-r.a. In the B6.4 lineage, the MAPK pathway was cell-autonomously activated by a constitutively active form of Raf, enabling Zic-r.a to activate independently of As a result, begins to be expressed at the 32-cell stage simultaneously in these two lineages. Such shortcuts might be required for coordinating developmental programs in embryos in which cells become separated progressively from stem cells, including germline cells.

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Co-expression of Foxa.a, Foxd and Fgf9/16/20 defines a transient mesendoderm regulatory state in ascidian embryos

Cited by 39 publications

References 73 publications

Differential gene expression along the animal-vegetal axis in the ascidian embryo is maintained by a dual functional protein Foxd

Differential gene expression along the animal-vegetal axis in the ascidian embryo is maintained by a dual functional protein Foxd

Antagonism between β-catenin and Gata.a sequentially segregates the germ layers of ascidian embryos

Distinct regulation of Snail in two muscle lineages of the ascidian embryo achieves temporal coordination of muscle development

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