Deciphering and modelling the TGF-β signalling interplays specifying the dorsal-ventral axis of the sea urchin embryo

During sea urchin development, secretion of Nodal and BMP2/4 ligands and their antagonists Lefty and Chordin from a ventral organizer region specifies the ventral and dorsal territories. This process relies on a complex interplay between the Nodal and BMP pathways through numerous regulatory circuits. To decipher the interplay between these pathways, we used a combination of treatments with recombinant Nodal and BMP2/4 proteins and a computational modelling approach. We assembled a logical model focusing on cell responses to signalling inputs along the dorsal-ventral axis, which was extended to cover ligand diffusion and enable multicellular simulations. Our model simulations accurately recapitulate gene expression in wild type embryos, accounting for the specification of ventral ectoderm, ciliary band and dorsal ectoderm. Our model simulations further recapitulate various morphant phenotypes, reveals a dominance of the BMP pathway over the Nodal pathway, and stresses the crucial impact of the rate of Smad activation in D/V patterning. These results emphasise the key role of the mutual antagonism between the Nodal and BMP2/4 pathways in driving early dorsal-ventral patterning of the sea urchin embryo.

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Deciphering and modelling the TGF-β signalling interplays specifying the dorsal-ventral axis of the sea urchin embryo

10.1101/2020.02.26.966556 ◽

2020 ◽

Author(s):

Swann Floc’hlay ◽

Maria Dolores Molina ◽

Céline Hernandez ◽

Emmanuel Haillot ◽

Morgane Thomas-Chollier ◽

...

Keyword(s):

Sea Urchin ◽

Organizer Region ◽

Computational Modelling ◽

Model Simulations ◽

Mutual Antagonism ◽

Regulatory Circuits ◽

Sea Urchin Embryo ◽

Bmp Pathway ◽

Summary Statement ◽

Ligand Diffusion

AbstractDuring sea urchin development, secretion of Nodal and BMP2/4 ligands and their antagonists Lefty and Chordin from a ventral organizer region specifies the ventral and dorsal territories. This process relies on a complex interplay between the Nodal and BMP pathways through numerous regulatory circuits. To decipher the interplay between these pathways, we used a combination of treatments with recombinant Nodal and BMP2/4 proteins and a computational modelling approach. We assembled a logical model focusing on cell responses to signalling inputs along the dorsal-ventral axis, which was extended to cover ligand diffusion and enable multicellular simulations. Our model simulations accurately recapitulate gene expression in wild type embryos, accounting for the specification of ventral ectoderm, ciliary band and dorsal ectoderm. Our model simulations further recapitulate various morphant phenotypes, reveals a dominance of the BMP pathway over the Nodal pathway, and stresses the crucial impact of the rate of Smad activation in D/V patterning. These results emphasise the key role of the mutual antagonism between the Nodal and BMP2/4 pathways in driving early dorsal-ventral patterning of the sea urchin embryo.Summary StatementWe propose a predictive computational model of the regulatory network controlling the dorsal-ventral axis specification in sea urchin embryos, and highlight key features of Nodal and BMP antagonism.

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Autonomous and non-autonomous differentiation of ectoderm in different sea urchin species

Development ◽

10.1242/dev.121.5.1497 ◽

1995 ◽

Vol 121 (5) ◽

pp. 1497-1505 ◽

Cited By ~ 7

Author(s):

A.H. Wikramanayake ◽

B.P. Brandhorst ◽

W.H. Klein

Keyword(s):

Sea Urchin ◽

Strongylocentrotus Purpuratus ◽

Protein A ◽

Cellular Interactions ◽

V Protein ◽

Lytechinus Pictus ◽

Sea Urchin Embryo ◽

Oral Ectoderm ◽

Temporal And Spatial

During early embryogenesis, the highly regulative sea urchin embryo relies extensively on cell-cell interactions for cellular specification. Here, the role of cellular interactions in the temporal and spatial expression of markers for oral and aboral ectoderm in Strongylocentrotus purpuratus and Lytechinus pictus was investigated. When pairs of mesomeres or animal caps, which are fated to give rise to ectoderm, were isolated and cultured they developed into ciliated embryoids that were morphologically polarized. In animal explants from S. purpuratus, the aboral ectoderm-specific Spec1 gene was activated at the same time as in control embryos and at relatively high levels. The Spec1 protein was restricted to the squamous epithelial cells in the embryoids suggesting that an oral-aboral axis formed and aboral ectoderm differentiation occurred correctly. However, the Ecto V protein, a marker for oral ectoderm differentiation, was detected throughout the embryoid and no stomodeum or ciliary band formed. These results indicated that animal explants from S. purpuratus were autonomous in their ability to form an oral-aboral axis and to differentiate aboral ectoderm, but other aspects of ectoderm differentiation require interaction with vegetal blastomeres. In contrast to S. purpuratus, aboral ectoderm-specific genes were not expressed in animal explants from L. pictus even though the resulting embryoids were morphologically very similar to those of S. purpuratus. Recombination of the explants with vegetal blastomeres or exposure to the vegetalizing agent LiCl restored activity of aboral ectoderm-specific genes, suggesting the requirement of a vegetal induction for differentiation of aboral ectoderm cells.(ABSTRACT TRUNCATED AT 250 WORDS)

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Specification of endoderm and mesoderm in the sea urchin

Zygote ◽

10.1017/s0967199400130199 ◽

1999 ◽

Vol 8 (S1) ◽

pp. S41-S41 ◽

Cited By ~ 2

Author(s):

David R. McClay

Keyword(s):

Sea Urchin ◽

Wnt Pathway ◽

Special Significance ◽

Nuclear Entry ◽

Cell Stage ◽

Animal Pole ◽

Secondary Axis ◽

Sea Urchin Embryo ◽

Vegetal Pole

It has long been recognized that micromeres have special significance in early specification events in the sea urchin embryo. Micromeres have the ability to induce a secondary axis if transferred to the animal pole at the 16-cell stage of sea urchin embryos (Hörstadius, 1939). Without micromeres an isolated animal hemisphere develops into an ectodermal ball called a dauer blastula. Addition of micromeres to an animal half rescues a normal pluteus larva, including endoderm (Hörstadius, 1939). Despite these well-known experiments, however, neither the molecular basis of that induction nor the endogenous inductive role of micromeres in development was known. In recent experiments we learned that if one eliminates micromeres from the vegetal pole at the 16-cell stage the resulting embryo makes no secondary mesenchyme. Earlier it had been found that β-catenin is crucial for specification events that lead to mesoderm and endoderm (Wikra-manayake et al., 1998; Emily-Fenouil et al., 1998; Logan et al., 1999). We noticed that at the 16-cell stage β-catenin enters the nuclei of micromeres, then enters the nuclei of macromeres at the 32-cell stage (Logan et al., 1999). Since nuclear entry of β-catenin is known to be important for its signalling function in the Wnt pathway, we asked whether β-catenin functions in the micromere induction pathway.

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Lim1-related homeobox gene (HpLim1) expressed in sea urchin embryo

Zygote ◽

10.1017/s0967199400130394 ◽

1999 ◽

Vol 8 (S1) ◽

pp. S71-S72

Author(s):

Keiko Mitsunaga-Nakatsubo ◽

Takahiko Kawasaki ◽

Koichi Takeda ◽

Koji Akasaka ◽

Hiraku Shimada

Keyword(s):

Sea Urchin ◽

Expression Patterns ◽

Homeobox Gene ◽

Mesoderm Induction ◽

Over Expression ◽

Lim Domains ◽

Sea Urchin Embryo ◽

Cell Type Specific ◽

Islet 1

A characteristic cysteine-rich motif, LIM domain, was first detected in three different transcription factors: lin-11, Islet-1 and mec-3. A feature shared by these genes is the presence of two LIM domains linked to a DNA-binding homeodomain (Sánchez-García et al., 1994). LIM homeodomain (LHX) proteins have been reported to be implicated in a variety of developmental processes (Dawid et al., 1998).Expression patterns of LHX genes have been analysed in a wide variety of organisms and reported to be cell-type specific (Dawid et al., 1998). In vertebrates, they are expressed in organiser equivalent regions at the gastrula stage, suggesting their involvement in mesoderm induction (Taira et al., 1992; Barnes et al., 1994; Toyama et al., 1995). Hrlim, an ascidian Lim3, zygotically expresses in the endoderm lineage before gastrulation, suggesting that it is involved in the endoderm determination (Wada et al., 1995).Here, cDNA cloning of the Lim1-related homeobox gene (HpLim1) of the sea urchin, Hemicentrotus pulcherrimus, is described together with the spatially as well as temporally regulated expression of HpLim1 during sea urchin development. A possible role of HpLiml in sea urchin development is also discussed based on its spatial pattern of expression and on the result of an over-expression study.

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Role of the extracellular matrix in tissue-specific gene expression in the sea urchin embryo

Molecular Reproduction and Development ◽

10.1002/mrd.1080290303 ◽

1991 ◽

Vol 29 (3) ◽

pp. 220-226 ◽

Cited By ~ 24

Author(s):

Steve Benson ◽

Robert Rawson ◽

Christopher Killian ◽

Fred Wilt

Keyword(s):

Gene Expression ◽

Extracellular Matrix ◽

Sea Urchin ◽

Specific Gene ◽

Tissue Specific ◽

Tissue Specific Gene ◽

Specific Gene Expression ◽

Sea Urchin Embryo

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A biphasic role of non-canonical Wnt16 signaling during early anterior-posterior patterning and morphogenesis of the sea urchin embryo

Development ◽

10.1242/dev.168799 ◽

2019 ◽

Vol 146 (24) ◽

pp. dev168799 ◽

Cited By ~ 1

Author(s):

Marina Martínez-Bartolomé ◽

Ryan C. Range

Keyword(s):

Sea Urchin ◽

Sea Urchin Embryo ◽

Anterior Posterior

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A precise regulation of presenilin expression is required for the sea urchin early development

Journal of Cell Science ◽

10.1242/jcs.258382 ◽

2021 ◽

Author(s):

Odile Bronchain ◽

Laetitia Philippe-Caraty ◽

Vincent Anquetil ◽

Brigitte Ciapa

Keyword(s):

Sea Urchin ◽

Crucial Role ◽

Senile Plaques ◽

Ciliated Cells ◽

Cellular Functions ◽

Aβ Peptides ◽

Multiple Substrates ◽

Sea Urchin Embryo ◽

Secretase Activity

Presenilins or PSENs homologues are widely expressed across eukaryotes. Two PSEN are expressed in humans where they play a crucial role in Alzheimer's disease (AD). Each PSEN can be part of the γ-secretase complex that has multiple substrates such as Notch or the amyloid precursor protein (AβPP) which gives the Aβ peptides composing the senile plaques during AD. PSENs also interact with various proteins independently of their γ-secretase activity. They can then be involved in numerous cellular functions, which makes their role in a given cell and/or organism complex to decipher. We settled the sea urchin embryo as a new model to study the role of PSEN. PSEN is present in unduplicated form and highly similar to that of humans. Our results suggest that its expression must be precisely tuned to control the course of the first mitotic cycles and the associated Cai transients, gastrulation execution and, probably in association with ciliated cells, the establishment of the pluteus. We suggest that it would be relevant to study the role of PSEN within the GRN deciphered in the sea urchin.

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