Dynamics of Delta/Notch signaling on endomesoderm segregation in the sea urchin embryo

Croce, Jenifer C.; McClay, David R.

doi:10.1242/dev.044149

Cited by 89 publications

(106 citation statements)

References 29 publications

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“…Because Delta is known to be important for NSM specification, perturbation of Delta signaling from micromeres was tested and the results suggest that FoxN2/3 is activated in NSM independent of Delta signaling. When the Delta signaling pathway was disrupted by dominant-negative notch mRNA or delta MASO injection, the embryos showed the albino phenotype as expected from previous reports using these reagents (Croce and McClay, 2010;Sherwood and McClay, 1999;Sweet et al, 2002). However, foxN2/3 was still expressed in the vegetal plate ( Fig.…”

Section: Gene Regulatory Network Regulation Of Foxn2/3 Expressionsupporting

confidence: 78%

The control offoxN2/3expression in sea urchin embryos and its function in the skeletogenic gene regulatory network

Rho

McClay

2011

Development

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Early development requires well-organized temporal and spatial regulation of transcription factors that are assembled into gene regulatory networks (GRNs). In the sea urchin, an endomesoderm GRN model explains much of the specification in the endoderm and mesoderm prior to gastrulation, yet some GRN connections remain incomplete. Here, we characterize FoxN2/3 in the primary mesenchyme cell (PMC) GRN state. Expression of foxN2/3 mRNA begins in micromeres at the hatched blastula stage and then is lost from micromeres at the mesenchyme blastula stage. foxN2/3 expression then shifts to the non-skeletogenic mesoderm and, later, to the endoderm. Here, we show that Pmar1, Ets1 and Tbr are necessary for activation of foxN2/3 in micromeres. The later endomesoderm expression of foxN2/3 is independent of the earlier expression of foxN2/3 in micromeres and is independent of signals from PMCs. FoxN2/3 is necessary for several steps in the formation of the larval skeleton. Early expression of genes for the skeletal matrix is dependent on FoxN2/3, but only until the mesenchyme blastula stage as foxN2/3 mRNA disappears from PMCs at that time and we assume that the protein is not abnormally long-lived. Knockdown of FoxN2/3 inhibits normal PMC ingression and foxN2/3 morphant PMCs do not organize in the blastocoel and fail to join the PMC syncytium. In addition, without FoxN2/3, the PMCs fail to repress the transfating of other mesodermal cells into the skeletogenic lineage. Thus, FoxN2/3 is necessary for normal ingression, for expression of several skeletal matrix genes, for preventing transfating and for fusion of the PMC syncytium.

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Section: Gene Regulatory Network Regulation Of Foxn2/3 Expressionsupporting

confidence: 78%

The control offoxN2/3expression in sea urchin embryos and its function in the skeletogenic gene regulatory network

Rho

McClay

2011

Development

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“…Several TFs in this set, however, including gcm, foxa, scl and gataC, are restricted to cell types other than PMCs at the mesenchyme blastula stage (Ransick and Davidson, 2006;Croce and McClay, 2010;Flynn et al, 2011) and their identification in our analysis reflected the low level of contamination of the bag preparations with cell types other than PMCs. When we restricted our analysis to the set of 420 DE genes, we identified only 11 TFs (Table 1).…”

Section: Characterization Of De Genesmentioning

confidence: 63%

Genome-wide analysis of the skeletogenic gene regulatory network of sea urchins

Azhari¹,

Shashikant²,

McManus³

et al. 2014

Development

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There was an error published in Development 141, 950-961.Column M of supplementary Table S1 contained an error and has been replaced. The authors apologise to readers for this mistake. ABSTRACT A central challenge of developmental and evolutionary biology is to understand the transformation of genetic information into morphology. Elucidating the connections between genes and anatomy will require model morphogenetic processes that are amenable to detailed analysis of cell/tissue behaviors and to systems-level approaches to gene regulation. The formation of the calcified endoskeleton of the sea urchin embryo is a valuable experimental system for developing such an integrated view of the genomic regulatory control of morphogenesis. A transcriptional gene regulatory network (GRN) that underlies the specification of skeletogenic cells (primary mesenchyme cells, or PMCs) has recently been elucidated. In this study, we carried out a genome-wide analysis of mRNAs encoded by effector genes in the network and uncovered transcriptional inputs into many of these genes. We used RNA-seq to identify >400 transcripts differentially expressed by PMCs during gastrulation, when these cells undergo a striking sequence of behaviors that drives skeletal morphogenesis. Our analysis expanded by almost an order of magnitude the number of known (and candidate) downstream effectors that directly mediate skeletal morphogenesis. We carried out genome-wide analysis of (1) functional targets of Ets1 and Alx1, two pivotal, early transcription factors in the PMC GRN, and (2) functional targets of MAPK signaling, a pathway that plays an essential role in PMC specification. These studies identified transcriptional inputs into >200 PMC effector genes. Our work establishes a framework for understanding the genomic regulatory control of a major morphogenetic process and has important implications for reconstructing the evolution of biomineralization in metazoans. 2542

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“…Examining mesodermal polarity in euechinoids and outgroup echinoderms aids in establishing a timeline of GRN evolution. In euechinoid mesodermal NSM, gcm is directly downstream of Notch signaling and later is restricted before gastrulation to aboral NSM by Not, which is directly downstream of Nodal/SMAD signaling (37,71,93,94). In cidaroids, early expression of gcm likely is not dependent on Delta/Notch (16), and mesodermal polarity is apparent only at 4-6 h after the start of gastrulation (Fig.…”

Section: Divergent Regulatory Linkages In the Evolution Of Echinoid Ementioning

confidence: 94%

“…Abundant comparative evidence exists for other euechinoid taxa as well, including Lytechinus variegatus (Lv) (31)(32)(33)(34)(35)(36)(37) and Paracentrotus lividus (Pl) (38)(39)(40)(41)(42). Data from these indirectdeveloping euechinoids indicate that although these taxa diverged from one another ∼90 mya (9, 43), very little appreciable change to their developmental GRNs has accrued (44)(45)(46).…”

mentioning

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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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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Dynamics of Delta/Notch signaling on endomesoderm segregation in the sea urchin embryo

Cited by 89 publications

References 29 publications

The control offoxN2/3expression in sea urchin embryos and its function in the skeletogenic gene regulatory network

The control offoxN2/3expression in sea urchin embryos and its function in the skeletogenic gene regulatory network

Genome-wide analysis of the skeletogenic gene regulatory network of sea urchins

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

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