The biological regulation of sea urchin larval skeletogenesis – From genes to biomineralized tissue

Gildor, Tsvia; Winter, Mark; Layous, Majed; Hijaze, Eman; de-Leon, Smadar Ben-Tabou

doi:10.1016/j.jsb.2021.107797

Cited by 19 publications

(18 citation statements)

References 27 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…[5][6][7][8][9][10][11][12] The larval skeleton of the sea urchin is made of two calcite rods, the spicules, that are engulfed within a tubular spicule cavity, generated by the skeletogenic cells. 5,7,13 During embryogenesis, the skeletogenic cells go through epithelial to mesenchymal transition and enter the blastocoel, fuse through their filopodia and form a pseudopodia cable that links them into a syncytium (Figure 1A). 13,14 The skeletogenic cells organize in a ring with two ventrolateral cell clusters in which the tri-radiate spicules form (Figure 1A, I [17][18][19] ).…”

Section: Introductionmentioning

confidence: 99%

“…5,7,13 During embryogenesis, the skeletogenic cells go through epithelial to mesenchymal transition and enter the blastocoel, fuse through their filopodia and form a pseudopodia cable that links them into a syncytium (Figure 1A). 13,14 The skeletogenic cells organize in a ring with two ventrolateral cell clusters in which the tri-radiate spicules form (Figure 1A, I [17][18][19] ). The spicules elongate within the pseudopodia cable and generate the body, anterolateral and mid-ventral rods (Figure 1A).…”

Section: Introductionmentioning

confidence: 99%

“…Sea urchin larval skeletogenesis is a prominent model for dissecting the genetic regulation of developmental progression 5–12 . The larval skeleton of the sea urchin is made of two calcite rods, the spicules, that are engulfed within a tubular spicule cavity, generated by the skeletogenic cells 5,7,13 . During embryogenesis, the skeletogenic cells go through epithelial to mesenchymal transition and enter the blastocoel, fuse through their filopodia and form a pseudopodia cable that links them into a syncytium (Figure 1A).…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Distinct regulatory states control the elongation of individual skeletal rods in the sea urchin embryo

Tarsis

Gildor

Morgulis

et al. 2022

Developmental Dynamics

Self Cite

View full text Add to dashboard Cite

Background: Understanding how gene regulatory networks (GRNs) control developmental progression is a key to the mechanistic understanding of morphogenesis. The sea urchin larval skeletogenesis provides an excellent platform to tackle this question. In the early stages of sea urchin skeletogenesis, skeletogenic genes are uniformly expressed in the skeletogenic lineage. Yet, during skeletal elongation, skeletogenic genes are expressed in distinct spatial sub-domains. The regulation of differential gene expression during late skeletogenesis is not well understood.Results: Here we reveal the dynamic expression of the skeletogenic regulatory genes that define a specific regulatory state for each pair of skeletal rods, in the sea urchin Paracentrotus lividus. The vascular endothelial growth factor (VEGF) signaling, essential for skeleton formation, specifically controls the migration of cells that form the postoral and distal anterolateral skeletogenic rods. VEGF signaling also controls the expression of regulatory genes in cells

show abstract

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Distinct regulatory states control the elongation of individual skeletal rods in the sea urchin embryo

Tarsis

Gildor

Morgulis

et al. 2022

Developmental Dynamics

Self Cite

View full text Add to dashboard Cite

show abstract

“…The GRN that drives skeletogenesis in the sea urchin embryos was extensively studied in the last two decades, resulting in one of the most comprehensive models of developmental GRN [ 15 , 40 , 59 , 60 , 61 , 62 , 63 ]. The GRN contains about 20 transcription factors that control a sequence of morphogenetic processes, including epithelial to mesenchymal transition, cell migration and cell fusion [ 15 , 40 , 64 , 65 ]. Some of the early transcription factors regulate these early morphogenesis events [ 64 ] but shut down before mineral deposition [ 15 ].…”

Section: Skeletogenesis In Echinoderms and The Grns That Control Itmentioning

confidence: 99%

“…Echinoderm biomineralization occurs within a tubular cavity formed by the skeletogenic cells, and the core GRN that controls this process, shows a strong similarity to the endothelial cell GRNs that control vascularization in vertebrates ( Figure 3 F and Figure 4 E [ 18 , 65 ]). Despite the distinct structural and functional differences between sea urchin skeletons and vertebrates’ blood vessels, an ancestral GRN that controls tube formation could have evolved for these separate usages in the two phyla.…”

Section: Grns That Drive Vascular Tubulogenesis In Vertebratesmentioning

confidence: 99%

The Evolution of Biomineralization through the Co-Option of Organic Scaffold Forming Networks

de-Leon

2022

Cells

Self Cite

View full text Add to dashboard Cite

Biomineralization is the process in which organisms use minerals to generate hard structures like teeth, skeletons and shells. Biomineralization is proposed to have evolved independently in different phyla through the co-option of pre-existing developmental programs. Comparing the gene regulatory networks (GRNs) that drive biomineralization in different species could illuminate the molecular evolution of biomineralization. Skeletogenesis in the sea urchin embryo was extensively studied and the underlying GRN shows high conservation within echinoderms, larval and adult skeletogenesis. The organic scaffold in which the calcite skeletal elements form in echinoderms is a tubular compartment generated by the syncytial skeletogenic cells. This is strictly different than the organic cartilaginous scaffold that vertebrates mineralize with hydroxyapatite to make their bones. Here I compare the GRNs that drive biomineralization and tubulogenesis in echinoderms and in vertebrates. The GRN that drives skeletogenesis in the sea urchin embryo shows little similarity to the GRN that drives bone formation and high resemblance to the GRN that drives vertebrates’ vascular tubulogenesis. On the other hand, vertebrates’ bone-GRNs show high similarity to the GRNs that operate in the cells that generate the cartilage-like tissues of basal chordate and invertebrates that do not produce mineralized tissue. These comparisons suggest that biomineralization in deuterostomes evolved through the phylum specific co-option of GRNs that control distinct organic scaffolds to mineralization.

show abstract

Expression and Transcriptional Targets of TGFβ‐RII in Paracentrotus lividus Larval Skeletogenesis

Goloe,

Gildor,

Ben‐Tabou de‐Leon

2024

Genesis

View full text Add to dashboard Cite

Organisms from the five kingdoms of life use minerals to harden their tissues and make teeth, shells and skeletons, in the process of biomineralization. The sea urchin larval skeleton is an excellent system to study the biological regulation of biomineralization and its evolution. The gene regulatory network (GRN) that controls sea urchin skeletogenesis is known in great details and shows similarity to the GRN that controls vertebrates' vascularization while it is quite distinct from the GRN that drives vertebrates' bone formation. Yet, transforming growth factor beta (TGF‐β) signaling regulates both sea urchin and vertebrates' skeletogenesis. Here, we study the upstream regulation and identify transcriptional targets of TGF‐β in the Mediterranean Sea urchin species, Paracentrotus lividus. TGF‐βRII is transiently active in the skeletogenic cells downstream of vascular endothelial growth factor (VEGF) signaling, in P. lividus. Continuous perturbation of TGF‐βRII activity significantly impairs skeletal elongation and the expression of key skeletogenic genes. Perturbation of TGF‐βRII after skeletal initiation leads to a delay in skeletal elongation and minor changes in gene expression. TGF‐β targets are distinct from its transcriptional targets during vertebrates' bone formation, suggesting that the role of TGF‐β in biomineralization in these two phyla results from convergent evolution.

show abstract

The biological regulation of sea urchin larval skeletogenesis – From genes to biomineralized tissue

Cited by 19 publications

References 27 publications

Distinct regulatory states control the elongation of individual skeletal rods in the sea urchin embryo

Distinct regulatory states control the elongation of individual skeletal rods in the sea urchin embryo

The Evolution of Biomineralization through the Co-Option of Organic Scaffold Forming Networks

Expression and Transcriptional Targets of TGFβ‐RII in Paracentrotus lividus Larval Skeletogenesis

Contact Info

Product

Resources

About