The Cnidarian and the Canon: the role of Wnt/β‐catenin signaling in the evolution of metazoan embryos

Primus, Alex; Freeman, G. L.

doi:10.1002/bies.20031

Cited by 19 publications

(10 citation statements)

References 12 publications

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“…In Podocoryne, maternal RNAs coding for Brachyury [29] and for the homeobox transcription factor Cnox4-Pc [36] are localised around the animal pole of the egg, and could potentially participate in directing gastrulation and/or other aspects of oral fate [37]. It will be instructive to test the maternal function of these molecules, and of the variety of Wnt pathway regulators present in cnidarians [18].…”

Section: Discussionmentioning

confidence: 99%

Two Oppositely Localised Frizzled RNAs as Axis Determinants in a Cnidarian Embryo

2007

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In phylogenetically diverse animals, including the basally diverging cnidarians, “determinants” localised within the egg are responsible for directing development of the embryonic body plan. Many such determinants are known to regulate the Wnt signalling pathway, leading to regionalised stabilisation of the transcriptional coregulator β-catenin; however, the only strong molecular candidate for a Wnt-activating determinant identified to date is the ligand Wnt11 in Xenopus. We have identified embryonic “oral–aboral” axis determinants in the cnidarian Clytia hemisphaerica in the form of RNAs encoding two Frizzled family Wnt receptors, localised at opposite poles of the egg. Morpholino-mediated inhibition of translation showed that CheFz1, localised at the animal pole, activates the canonical Wnt pathway, promotes oral fates including gastrulation, and may also mediate global polarity in the ectoderm. CheFz3, whose RNA is localised at the egg vegetal cortex, was found to oppose CheFz1 function and to define an aboral territory. Active downregulation mechanisms maintained the reciprocal localisation domains of the two RNAs during early development. Importantly, ectopic expression of either CheFz1 or CheFz3 was able to redirect axis development. These findings identify Frizzled RNAs as axis determinants in Clytia, and have implications for the evolution of embryonic patterning mechanisms, notably that diverse Wnt pathway regulators have been adopted to initiate asymmetric Wnt pathway activation.

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Section: Discussionmentioning

confidence: 99%

Two Oppositely Localised Frizzled RNAs as Axis Determinants in a Cnidarian Embryo

2007

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“…Conversely, in ascidian, sea urchin or nemertean, in which a clear function of b-catenin in endomesoderm specification has been demonstrated, there is no obvious function for late blastoporal Wnts in patterning the anteroposterior axis of the embryo. In cnidarian embryos in which both germ layer formation and axis patterning are under the control of the Wnt pathway (Momose and Houliston, 2007;Wikramanayake et al, 2003), the mechanistic relationships between the two processes are unclear (Primus and Freeman, 2004;Primus and Freeman, 2005). It is rather thought that endoderm specification is a consequence of embryonic polarity establishment, which would be directly controlled by Wnt (Momose and Houliston, 2007).…”

Section: Introductionmentioning

confidence: 99%

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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“…The Wnt/b-catenin pathway is a signaling cascade that is highly conserved among metazoans (Cadigan and Nusse, 1997;Primus and Freeman, 2004). This pathway is used throughout animal development to control a variety of cell fate decisions (Cadigan and Nusse, 1997;Logan and Nusse, 2004).…”

Section: Introductionmentioning

confidence: 99%

C-terminal-binding protein directly activates and represses Wnt transcriptional targets in Drosophila

Fang¹,

Li²,

Blauwkamp³

et al. 2006

EMBO J

155

238

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Regulation of Wnt transcriptional targets is thought to occur by a transcriptional switch. In the absence of Wnt signaling, sequence‐specific DNA‐binding proteins of the TCF family repress Wnt target genes. Upon Wnt stimulation, stabilized β‐catenin binds to TCFs, converting them into transcriptional activators. C‐terminal‐binding protein (CtBP) is a transcriptional corepressor that has been reported to inhibit Wnt signaling by binding to TCFs or by preventing β‐catenin from binding to TCF. Here, we show that CtBP is also required for the activation of some Wnt targets in Drosophila. CtBP is recruited to Wnt‐regulated enhancers in a Wnt‐dependent manner, where it augments Armadillo (the fly β‐catenin) transcriptional activation. We also found that CtBP is required for repression of a subset of Wnt targets in the absence of Wnt stimulation, but in a manner distinct from previously reported mechanisms. CtBP binds to Wnt‐regulated enhancers in a TCF‐independent manner and represses target genes in parallel with TCF. Our data indicate dual roles for CtBP as a gene‐specific activator and repressor of Wnt target gene transcription.

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The Cnidarian and the Canon: the role of Wnt/β‐catenin signaling in the evolution of metazoan embryos

Cited by 19 publications

References 12 publications

Two Oppositely Localised Frizzled RNAs as Axis Determinants in a Cnidarian Embryo

Two Oppositely Localised Frizzled RNAs as Axis Determinants in a Cnidarian Embryo

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

C-terminal-binding protein directly activates and represses Wnt transcriptional targets in Drosophila

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