The Sea Urchin Embryo: A Model for Studying Molecular Mechanisms Involved in Human Diseases and for Testing Bioactive Compounds

β-Catenin is essential for patterning the maternally specified animal-vegetal axis in the sea urchin embryo

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.95.16.9343 ◽

1998 ◽

Vol 95 (16) ◽

pp. 9343-9348 ◽

Cited By ~ 162

Author(s):

Athula H. Wikramanayake ◽

Ling Huang ◽

William H. Klein

Keyword(s):

Sea Urchin ◽

Molecular Mechanisms ◽

Early Embryo ◽

Cell Fates ◽

Cell Stage ◽

Signal Transduction Cascade ◽

Sea Urchin Embryos ◽

Sea Urchin Embryo ◽

Vegetal Pole ◽

Vegetal Cell

In sea urchin embryos, the animal-vegetal axis is specified during oogenesis. After fertilization, this axis is patterned to produce five distinct territories by the 60-cell stage. Territorial specification is thought to occur by a signal transduction cascade that is initiated by the large micromeres located at the vegetal pole. The molecular mechanisms that mediate the specification events along the animal–vegetal axis in sea urchin embryos are largely unknown. Nuclear β-catenin is seen in vegetal cells of the early embryo, suggesting that this protein plays a role in specifying vegetal cell fates. Here, we test this hypothesis and show that β-catenin is necessary for vegetal plate specification and is also sufficient for endoderm formation. In addition, we show that β-catenin has pronounced effects on animal blastomeres and is critical for specification of aboral ectoderm and for ectoderm patterning, presumably via a noncell-autonomous mechanism. These results support a model in which a Wnt-like signal released by vegetal cells patterns the early embryo along the animal–vegetal axis. Our results also reveal similarities between the sea urchin animal–vegetal axis and the vertebrate dorsal–ventral axis, suggesting that these axes share a common evolutionary origin.

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Calcium-vesicles perform active diffusion in the sea urchin embryo during larval biomineralization

PLoS Computational Biology ◽

10.1371/journal.pcbi.1008780 ◽

2021 ◽

Vol 17 (2) ◽

pp. e1008780

Author(s):

Mark R. Winter ◽

Miri Morgulis ◽

Tsvia Gildor ◽

Andrew R. Cohen ◽

Smadar Ben-Tabou de-Leon

Keyword(s):

Sea Urchin ◽

Molecular Mechanisms ◽

Three Dimensional ◽

Growth Factor Receptor ◽

Light Sheet ◽

Physical Support ◽

Light Sheet Microscopy ◽

Mineral Deposition ◽

Sea Urchin Embryo ◽

Diffusion Motion

Biomineralization is the process by which organisms use minerals to harden their tissues and provide them with physical support. Biomineralizing cells concentrate the mineral in vesicles that they secret into a dedicated compartment where crystallization occurs. The dynamics of vesicle motion and the molecular mechanisms that control it, are not well understood. Sea urchin larval skeletogenesis provides an excellent platform for investigating the kinetics of mineral-bearing vesicles. Here we used lattice light-sheet microscopy to study the three-dimensional (3D) dynamics of calcium-bearing vesicles in the cells of normal sea urchin embryos and of embryos where skeletogenesis is blocked through the inhibition of Vascular Endothelial Growth Factor Receptor (VEGFR). We developed computational tools for displaying 3D-volumetric movies and for automatically quantifying vesicle dynamics. Our findings imply that calcium vesicles perform an active diffusion motion in both, calcifying (skeletogenic) and non-calcifying (ectodermal) cells of the embryo. The diffusion coefficient and vesicle speed are larger in the mesenchymal skeletogenic cells compared to the epithelial ectodermal cells. These differences are possibly due to the distinct mechanical properties of the two tissues, demonstrated by the enhanced f-actin accumulation and myosinII activity in the ectodermal cells compared to the skeletogenic cells. Vesicle motion is not directed toward the biomineralization compartment, but the vesicles slow down when they approach it, and probably bind for mineral deposition. VEGFR inhibition leads to an increase of vesicle volume but hardly changes vesicle kinetics and doesn’t affect f-actin accumulation and myosinII activity. Thus, calcium vesicles perform an active diffusion motion in the cell of the sea urchin embryo, with diffusion length and speed that inversely correlate with the strength of the actomyosin network. Overall, our studies provide an unprecedented view of calcium vesicle 3D-dynamics and point toward cytoskeleton remodeling as an important effector of the motion of mineral-bearing vesicles.

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A Peak of H3T3 Phosphorylation Occurs in Synchrony with Mitosis in Sea Urchin Early Embryos

Cells ◽

10.3390/cells9040898 ◽

2020 ◽

Vol 9 (4) ◽

pp. 898 ◽

Cited By ~ 1

Author(s):

Omid Feizbakhsh ◽

Florian Pontheaux ◽

Virginie Glippa ◽

Julia Morales ◽

Sandrine Ruchaud ◽

...

Keyword(s):

Sea Urchin ◽

Cell Cycle Progression ◽

Molecular Mechanisms ◽

Pharmacological Study ◽

Post Translational Modification ◽

Developmental Context ◽

Detection Techniques ◽

Sea Urchin Embryo ◽

Early Embryos ◽

The Impact

The sea urchin embryo provides a valuable system to analyse the molecular mechanisms orchestrating cell cycle progression and mitosis in a developmental context. However, although it is known that the regulation of histone activity by post-translational modification plays an important role during cell division, the dynamics and the impact of these modifications have not been characterised in detail in a developing embryo. Using different immuno-detection techniques, we show that the levels of Histone 3 phosphorylation at Threonine 3 oscillate in synchrony with mitosis in Sphaerechinus granularis early embryos. We present, in addition, the results of a pharmacological study aimed at analysing the role of this key histone post-translational modification during sea urchin early development.

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Exogenous hyalin and sea urchin gastrulation. Part IV: a direct adhesion assay – progress in identifying hyalin's active sites

Zygote ◽

10.1017/s0967199409005498 ◽

2009 ◽

Vol 18 (1) ◽

pp. 17-26 ◽

Cited By ~ 3

Author(s):

Haike Ghazarian ◽

Catherine Coyle-Thompson ◽

William Dalrymple ◽

Virginia Hutchins-Carroll ◽

Stan Metzenberg ◽

...

Keyword(s):

Sea Urchin ◽

Active Sites ◽

Molecular Mechanisms ◽

Sea Urchins ◽

Cellular Interaction ◽

Adhesion Assay ◽

Cellular Interactions ◽

Microplate Assay ◽

Adhesive Interaction ◽

Sea Urchin Embryo

SummaryIn Strongylocentrotus purpuratus the hyalins are a set of three to four rather large glycoproteins (hereafter referred to as ‘hyalin’), which are the major constituents of the hyaline layer, the developing sea urchin embryo's extracellular matrix. Recent research from our laboratories has shown that hyalin is a cell adhesion molecule involved in sea urchin embryo-specific cellular interactions. Other laboratories have shown it to consist of 2–3% carbohydrate and a cloned, sequenced fragment demonstrated repeat domains (HYR) and non-repeat regions. Interest in this molecule has increased because HYR has been identified in organisms as diverse as bacteria, flies, worms, mice and humans, as well as sea urchins. Our laboratories have shown that hyalin appears to mediate a specific cellular interaction that has interested investigators for over a century, archenteron elongation/attachment to the blastocoel roof. We have shown this finding by localizing hyalin on the two components of the cellular interaction and by showing that hyalin and anti-hyalin antibody block the cellular interaction using a quantitative microplate assay. The microplate assay, however, has limitations because it does not directly assess hyalin's effects on the adhesion of the two components of the interaction. Here we have used an elegant direct assay that avoids the limitations, in which we microdissected the two components of the adhesive interaction and tested their re-adhesion to each other, thereby avoiding possible factors in the whole embryos that could confound or confuse results. Using both assays, we found that mild periodate treatment (6 h to 24 h in sodium acetate buffer with 0.2 M sodium periodate at 4 °C in the dark) of hyalin eliminates its ability to block the cellular interaction, suggesting that the carbohydrate component(s) may be involved in hyalin's specific adhesive function. This first step is important in identifying the molecular mechanisms of a well known cellular interaction in the NIH-designated sea urchin embryo model, a system that has led to the discovery of scores of physiological mechanisms, including those involved in human health and disease.

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LvNotch signaling plays a dual role in regulating the position of the ectoderm-endoderm boundary in the sea urchin embryo

Development ◽

10.1242/dev.128.12.2221 ◽

2001 ◽

Vol 128 (12) ◽

pp. 2221-2232 ◽

Cited By ~ 2

Author(s):

David R. Sherwood ◽

David R. McClay

Keyword(s):

Sea Urchin ◽

Molecular Mechanisms ◽

Early Embryo ◽

Notch Receptor ◽

Dominant Negative ◽

Autonomous Function ◽

Sea Urchin Embryo ◽

Dominant Negative Form ◽

A Cell ◽

Negative Form

The molecular mechanisms guiding the positioning of the ectoderm-endoderm boundary along the animal-vegetal axis of the sea urchin embryo remain largely unknown. We report here a role for the sea urchin homolog of the Notch receptor, LvNotch, in mediating the position of this boundary. Overexpression of an activated form of LvNotch throughout the embryo shifts the ectoderm-endoderm boundary more animally along the animal-vegetal axis, whereas expression of a dominant negative form shifts the border vegetally. Mosaic experiments that target activated and dominant negative forms of LvNotch into individual blastomeres of the early embryo, combined with lineage analyses, further reveal that LvNotch signaling mediates the position of this boundary by distinct mechanisms within the animal versus vegetal portions of the embryo. In the animal region of the embryo, LvNotch signaling acts cell autonomously to promote endoderm formation more animally, while in the vegetal portion, LvNotch signaling also promotes the ectoderm-endoderm boundary more animally, but through a cell non-autonomous mechanism. We further demonstrate that vegetal LvNotch signaling controls the localization of nuclear β-catenin at the ectoderm-endoderm boundary. Based on these results, we propose that LvNotch signaling promotes the position of the ectoderm-endoderm boundary more animally via two mechanisms: (1) a cell-autonomous function within the animal region of the embryo, and (2) a cell non-autonomous role in the vegetal region that regulates a signal(s) mediating ectoderm-endoderm position, possibly through the control of nuclear β-catenin at the boundary.

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