Patterning of the Dorsal-Ventral Axis in Echinoderms: Insights into the Evolution of the BMP-Chordin Signaling Network

Lapraz, François; Besnardeau, Lydia; Lepage, Thierry

doi:10.1371/journal.pbio.1000248

Cited by 193 publications

(303 citation statements)

References 82 publications

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“…In euechinoids, Bmp2/4 ligand is directly downstream of Nodal and is translocated across the embryo to the aboral side, where it stimulates aboral ectoderm (AE) regulatory genes, such as irxa, msx, and tbx2/3 (38,58,59). In Et, tbx2/3 exhibits spatial distribution complementary to OE genes in lateral AE (Fig.…”

Section: Resultsmentioning

confidence: 99%

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Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

Erkenbrack

2016

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

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Developmental gene regulatory networks (GRNs) are assemblages of gene regulatory interactions that direct ontogeny of animal body plans. Studies of GRNs operating in the early development of euechinoid sea urchins have revealed that little appreciable change has occurred since their divergence ∼90 million years ago (mya). These observations suggest that strong conservation of GRN architecture was maintained in early development of the sea urchin lineage. Testing whether this holds for all sea urchins necessitates comparative analyses of echinoid taxa that diverged deeper in geological time. Recent studies highlighted extensive divergence of skeletogenic mesoderm specification in the sister clade of euechinoids, the cidaroids, suggesting that comparative analyses of cidaroid GRN architecture may confer a greater understanding of the evolutionary dynamics of developmental GRNs. Here I report spatiotemporal patterning of 55 regulatory genes and perturbation analyses of key regulatory genes involved in euechinoid oral-aboral patterning of nonskeletogenic mesodermal and ectodermal domains in early development of the cidaroid Eucidaris tribuloides. These results indicate that developmental GRNs directing mesodermal and ectodermal specification have undergone marked alterations since the divergence of cidaroids and euechinoids. Notably, statistical and clustering analyses of echinoid temporal gene expression datasets indicate that regulation of mesodermal genes has diverged more markedly than regulation of ectodermal genes. Although research on indirectdeveloping euechinoid sea urchins suggests strong conservation of GRN circuitry during early embryogenesis, this study indicates that since the divergence of cidaroids and euechinoids, developmental GRNs have undergone significant, cell typebiased alterations.gene regulatory network | echinoderms | sea urchin embryogenesis | embryonic axis specification | echinoids

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Section: Resultsmentioning

confidence: 99%

“…In euechinoids, msx and tbx2/3 are downstream of Bmp2/4 ligand, which diffuses from OE to AE (58,59,74). Treatment of Pl embryos with SB431542 inhibitor completely and specifically extinguishes both msx and tbx2/3 in AE, although the latter is still expressed in SM (40).…”

Section: Nodal Signaling Is a Highly Conserved Mechanism Patterning Ementioning

confidence: 99%

Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

Erkenbrack

2016

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

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“…6A-F). The nuclear pSmad1/5/8 signal was confirmed to be in the AE, which is opposite of Sp-Chordin expression in the OE (Bradham et al, 2009;Lapraz et al, 2009;Su et al, 2009) (Fig. 6D-I).…”

Section: Nuclearization Of Psmad1/5/8 In the Central Aboral Ectodermmentioning

confidence: 87%

“…Therefore, it is believed that BMP proteins diffuse from the oral to the aboral ectoderm and their effect in the OE is antagonized by the BMP antagonist Chordin, which is also expressed in the OE (Bradham et al, 2009;Lapraz et al, 2009;Su et al, 2009). Recently, Lapraz et al confirmed in the sea urchin Paracentrotus lividus that phosphorylation and nuclearization of Smad1/5/8 (pSmad1/5/8), the BMP signaling transcription factor, occurs in the AE of the blastula embryos and that Chordin restricts effective BMP signaling in the AE (Lapraz et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

The dynamic gene expression patterns of transcription factors constituting the sea urchin aboral ectoderm gene regulatory network

Chen

Luo

2010

Developmental Dynamics

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The temporal and spatial expression patterns of regulatory genes are required for building a gene regulatory network (GRN). The current ectoderm GRN model for the sea urchin embryo includes pregastrular specification functions in the oral (OE) and aboral ectoderm (AE). Unlike the OE, which is resolved into several subdomains, the AE is considered a simpler territory due to the lack of detailed gene expression studies in this territory. Here, we perform temporal and spatial gene expression studies on the eight transcription factor genes constituting the AE GRN. Based on the differential gene expression patterns, we conclude that the AE contains at least three subdomains at the mesenchyme blastula stage. We also performed immunostaining for pSmad1/5/8 to monitor the activation of the BMP signaling pathway. The dynamic changes in the expression patterns of these transcription factor genes and the nuclearization of pSmad1/5/8 may provide a foundation for resolving the AE GRN. Developmental Dynamics 240:250-260,

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“…1). During embryogenesis, the anterior neuroectoderm is localized to the animal pole by controlled canonical Wnt-dependent processes (3,4), and the ciliary band is positioned by TGF-β signaling through nodal and bone morphogenetic protein pathways (5)(6)(7)(8). However, the mechanisms regulating development of pharyngeal neurons have not been explored.…”

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confidence: 99%

Direct development of neurons within foregut endoderm of sea urchin embryos

Wen-ling

Angerer

2011

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

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Although it is well established that neural cells are ectodermal derivatives in bilaterian animals, here we report the surprising discovery that some of the pharyngeal neurons of sea urchin embryos develop de novo from the endoderm. The appearance of these neurons is independent of mouth formation, in which the stomodeal ectoderm joins the foregut. The neurons do not derive from migration of ectoderm cells to the foregut, as shown by lineage tracing with the photoactivatable protein KikGR. Their specification and development depend on expression of Nkx3-2, which in turn depends on Six3, both of which are expressed in the foregut lineage. SoxB1, which is closely related to the vertebrate Sox factors that support a neural precursor state, is also expressed in the foregut throughout gastrulation, suggesting that this region of the fully formed archenteron retains an unexpected pluripotency. Together, these results lead to the unexpected conclusion that, within a cell lineage already specified to be endoderm by a well-established gene regulatory network [Peter IS, Davidson EH (2010) Dev Biol 340:188-199], there also operates a Six3/Nkx3-2-dependent pathway required for the de novo specification of some of the neurons in the pharynx. As a result, neuroendoderm precursors form in the foregut aided by retention of a SoxB1-dependent pluripotent state.cell fate specification | embryonic development | neurogenesis | enteric nerve

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Patterning of the Dorsal-Ventral Axis in Echinoderms: Insights into the Evolution of the BMP-Chordin Signaling Network

Abstract: Deciphering the process of dorsal-ventral patterning in the sea urchin reveals an extreme case of BMP translocation and an unusual configuration of the BMP-Chordin axis in echinoderms.

Cited by 193 publications

References 82 publications

Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

The dynamic gene expression patterns of transcription factors constituting the sea urchin aboral ectoderm gene regulatory network

Direct development of neurons within foregut endoderm of sea urchin embryos

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