Gene regulatory control in the sea urchin aboral ectoderm: Spatial initiation, signaling inputs, and cell fate lockdown

de-Leon, Smadar Ben-Tabou; Su, Yi-Hsien; Lin, Kuan-Ting; Li, Enhu; Davidson, Eric H.

doi:10.1016/j.ydbio.2012.11.013

Cited by 64 publications

(65 citation statements)

References 45 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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“…Resolution of their expression patterns to the oral side again depends on repression. Many genes of the aboral ectoderm require a positive boost from Bmp signals emitted from the oral ectoderm, as confirmed at the cis-regulatory level (12). Because of the extensive feedbacks within the aboral ectoderm GRN, Bmp MASO essentially down-regulates the whole of this GRN.…”

Section: Grn Interactions Controlling the Apical Domain/oral Ectodermmentioning

confidence: 90%

“…The major territories remaining to be considered at this level are the oral and aboral ectoderm and the neurogenic ciliated band and apical domains, as well as the later oral and aboral mesoderm. Major progress on the GRN linkages within all these regions except the apical domain has recently been attained (8)(9)(10)(11)(12)(13). Regulatory state patterns within them are organized in an essentially orthogonal manner with respect to both the animal/ vegetal axis and the oral/aboral axis of the embryo.…”

mentioning

confidence: 99%

Encoding regulatory state boundaries in the pregastrular oral ectoderm of the sea urchin embryo

Cui

Peter

et al. 2014

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

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By gastrulation the ectodermal territories of the sea urchin embryo have developed an unexpectedly complex spatial pattern of sharply bounded regulatory states, organized orthogonally with respect to the animal/vegetal and oral/aboral axes of the embryo. Although much is known of the gene regulatory network (GRN) linkages that generate these regulatory states, the principles by which the boundaries between them are positioned and maintained have remained undiscovered. Here we determine the encoded genomic logic responsible for the boundaries of the oral aspect of the embryo that separate endoderm from ectoderm and ectoderm from neurogenic apical plate and that delineate the several further subdivisions into which the oral ectoderm per se is partitioned. Comprehensive regulatory state maps, including all spatially expressed oral ectoderm regulatory genes, were established. The circuitry at each boundary deploys specific repressors of regulatory states across the boundary, identified in this work, plus activation by broadly expressed positive regulators. These network linkages are integrated with previously established interactions on the oral/aboral axis to generate a GRN model encompassing the 2D organization of the regulatory state pattern in the pregastrular oral ectoderm of the embryo.regulatory state boundaries | pattern formation | repression circuitry B y the onset of gastrulation, bilaterian embryos consist of a complex mosaic of sharply bounded regulatory state domains, where "regulatory state" refers to the sum of specifically expressed mRNAs encoding DNA sequence-recognizing transcription factors in each nucleus. The regulatory state domains or territories are organized spatially in respect to the two major axes of the embryo, and they constitute informational specifications that determine the subsequent embryonic fates and functions of the cells descendant from these domains. Although in different modes of pregastrular embryogenesis regional specification functions are accomplished in somewhat different ways (1, 2), the end result is always the same: subdivision of the embryo into (transient) spatial regulatory states. These progressively specified regulatory states, and the boundaries between them, are the output of networks of genomically ordained interactions among regulatory genes. Gene regulatory networks (GRNs) encompass the heritable code for the embryonic development of each species. At present, the best known, experimentally determined, large-scale GRN drives the specification of endoderm and mesoderm in the embryo of the sea urchin Strongylocentrotus purpuratus up to gastrulation (3-6). This GRN model encompasses about half of the embryo, covers 30 h of development (18 h in the nonskeletogenic mesoderm), and all or almost all relevant regionally expressed regulatory genes. A recent study (7) shows that the endomesoderm GRN model contains sufficient regulatory relationships to generate a computational automaton that successfully predicts almost all spatial and temporal regulatory gene expre...

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“…Being hbox12 expression achieved in the reducing environment specifically associated to the dorsal side of the early embryo, a likely candidate involved in the activation of hbox12 transcription could be HIF1α. This hypothesis deserves further investigation, being supported by recent studies showing that the HIF1α transcription activator is stabilized in a reducing environment [83,84], and by the fact that knock-down of HIF1α function strongly reduces the expression of dorsal-specific markers in the very early sea urchin embryo [85].…”

Section: Conclusion and Future Perspectivesmentioning

confidence: 83%

Symmetry Breaking and Establishment of Dorsal/Ventral Polarity in the Early Sea Urchin Embryo

Cavalieri

Spinelli

2015

Symmetry

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Abstract:The mechanisms imposing the Dorsal/Ventral (DV) polarity of the early sea urchin embryo consist of a combination of inherited maternal information and inductive interactions among blastomeres. Old and recent studies suggest that a key molecular landmark of DV polarization is the expression of nodal on the future ventral side, in apparent contrast with other metazoan embryos, where nodal is expressed dorsally. A subtle maternally-inherited redox anisotropy, plus some maternal factors such as SoxB1, Univin, and p38-MAPK have been identified as inputs driving the spatially asymmetric transcription of nodal. However, all the mentioned factors are broadly distributed in the embryo as early as nodal transcription occurs, suggesting that repression of the gene in non-ventral territories depends upon negative regulators. Among these, the Hbox12 homeodomain-containing repressor is expressed by prospective dorsal cells, where it acts as a dorsal-specific negative modulator of the p38-MAPK activity. This review provides an overview of the molecular mechanisms governing the establishment of DV polarity in sea urchins, focusing on events taking place in the early embryo. Altogether, these findings provide a framework for future studies aimed to unravel the inceptive mechanisms involved in the DV symmetry breaking.

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Gene regulatory control in the sea urchin aboral ectoderm: Spatial initiation, signaling inputs, and cell fate lockdown

Cited by 64 publications

References 45 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

Encoding regulatory state boundaries in the pregastrular oral ectoderm of the sea urchin embryo

Symmetry Breaking and Establishment of Dorsal/Ventral Polarity in the Early Sea Urchin Embryo

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