Calcium transport into the cells of the sea urchin larva in relation to spicule formation

Vidavsky, Netta; Addadi, Sefi; Schertel, Andreas; BenEzra, David; Shpigel, Muki; Addadi, Lia; Weiner, Steve

doi:10.1073/pnas.1612017113

Cited by 72 publications

(82 citation statements)

References 45 publications

(71 reference statements)

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“…Calcein staining does not distinguish between the different phases of calcium within the skeletogenic cells, but can be used to track the calcium ions. Calcium vesicles are visible in all cells of the embryo, in agreement with previous studies (7, 10). VEGF inhibition does not prevent calcium vesicle accumulation in the SM cells throughout skeletogenesis (arrows in Fig.…”

Section: Introductionsupporting

confidence: 93%

“…When VEGF signaling is inhibited, the apical surface still forms but the lumen is not generated (26). Relatedly, during sea urchin biomineralization, calcium is accumulated through endocytosis (10) and concentrated as amorphous calcium-carbonate in intracellular vesicles that are then secreted into the spicule cord where crystallization occurs (Fig. 1F, (7, 9)), however, the role of VEGF signaling in these processes has not been previously investigated.…”

Section: Introductionmentioning

confidence: 99%

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Possible co-option of a VEGF-driven tubulogenesis program for biomineralization in echinoderms

de-Leon

Gildor

Sher

et al. 2019

Preprint

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12Biomineralization is the process in which living organisms use minerals to form hard 13 structures that protect and support them. Biomineralization is believed to have evolved 14 rapidly and independently in different phyla utilizing existing components used for other 15 purposes. The mechanistic understanding of the regulatory networks that drive 16 biomineralization and their evolution is far from clear. The sea urchin skeletogenesis is an 17 excellent model system for studying both gene regulation and mineral uptake and deposition. 18The sea urchin calcite spicules are formed within a tubular cavity generated by the 19 skeletogenic cells under the control the vascular endothelial growth factor (VEGF) signaling. 20The VEGF pathway controls tubulogenesis and vascularization across metazoans while its 21 regulation of biomineralization was only observed in echinoderms. Despite the critical role of 22 for vascularization and specifically co-opted for biomineralization in the echinoderm phylum. 33 Significance statement 36The sea urchin calcite spicules and vertebrate blood vessels are quite distinct in their function, 37 yet both have a tubular structure and are controlled by the vascular endothelial growth factor 38 (VEGF) pathway. Here we study the downstream program by which VEGF pathway drives 39 sea urchin spiculogenesis and find remarkable similarities to the control of vertebrate 40 vascularization. The similarities are observed both in the upstream gene regulatory network, 41 in the downstream effector genes and the cellular processes that VEGF signaling controls at 42 the site of the calcite spicule formation. We speculate that sea urchin spiculogenesis and 43 vertebrate vascularization diverged from a common ancestral tubulogenesis program that was 44 co-opted for biomineralization in the echinoderm phylum. 45 46 3 47

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Section: Introductionsupporting

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Possible co-option of a VEGF-driven tubulogenesis program for biomineralization in echinoderms

de-Leon

Gildor

Sher

et al. 2019

Preprint

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“…3B). Calcein binds to calcium in all of the calcium phases and therefore marks calcium ions, calcium-carbonate, amorphous and crystallite calciumcarbonate (7,11,12,33).…”

Section: Vegf-vegfr Recognition Is Conserved Between Human and Seamentioning

confidence: 99%

Possible cooption of a VEGF-driven tubulogenesis program for biomineralization in echinoderms

Morgulis

Gildor

Roopin

et al. 2019

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

130

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Biomineralization is the process by which living organisms use minerals to form hard structures that protect and support them. Biomineralization is believed to have evolved rapidly and independently in different phyla utilizing preexisting components. The mechanistic understanding of the regulatory networks that drive biomineralization and their evolution is far from clear. Sea urchin skeletogenesis is an excellent model system for studying both gene regulation and mineral uptake and deposition. The sea urchin calcite spicules are formed within a tubular cavity generated by the skeletogenic cells controlled by vascular endothelial growth factor (VEGF) signaling. The VEGF pathway is essential for biomineralization in echinoderms, while in many other phyla, across metazoans, it controls tubulogenesis and vascularization. Despite the critical role of VEGF signaling in sea urchin spiculogenesis, the downstream program it activates was largely unknown. Here we study the cellular and molecular machinery activated by the VEGF pathway during sea urchin spiculogenesis and reveal multiple parallels to the regulation of vertebrate vascularization. Human VEGF rescues sea urchin VEGF knockdown, vesicle deposition into an internal cavity plays a significant role in both systems, and sea urchin VEGF signaling activates hundreds of genes, including biomineralization and interestingly, vascularization genes. Moreover, five upstream transcription factors and three signaling genes that drive spiculogenesis are homologous to vertebrate factors that control vascularization. Overall, our findings suggest that sea urchin spiculogenesis and vertebrate vascularization diverged from a common ancestral tubulogenesis program, broadly adapted for vascularization and specifically coopted for biomineralization in the echinoderm phylum.

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“…MSP130 proteins are also expressed selectively in biomineralizing tissues in other marine phyla, pointing to a conserved role (Ettensohn, ; Szabó & Ferrier, ). The biochemical functions of MSP130 proteins are not well understood, but these proteins regulate the internalization of calcium, which appears to enter PMCs primarily via endocytosis (see references in Wilt & Ettensohn, ; Ettensohn, ; Vidavsky et al, ; Killian & Wilt, ).…”

Section: The Pmc Gene Regulatory Network Of Sea Urchinsmentioning

confidence: 99%

From genome to anatomy: The architecture and evolution of the skeletogenic gene regulatory network of sea urchins and other echinoderms

Shashikant

Khor

Ettensohn

2018

Genesis

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The skeletogenic gene regulatory network (GRN) of sea urchins and other echinoderms is one of the most intensively studied transcriptional networks in any developing organism. As such, it serves as a pre-eminent model of GRN architecture and evolution. This review summarizes our current understanding of this developmental network. We describe in detail the most comprehensive model of the skeletogenic GRN, one developed for the euechinoid sea urchin Strongylocentrotus purpuratus, including its initial deployment by maternal inputs, its elaboration and stabilization through regulatory gene interactions, and its control of downstream effector genes that directly drive skeletal morphogenesis. We highlight recent comparative studies that have leveraged the euechinoid GRN model to examine the evolution of skeletogenic programs in diverse echinoderms, studies that have revealed both conserved and divergent features of skeletogenesis within the phylum. Lastly, we summarize the major insights that have emerged from analysis of the structure and evolution of the echinoderm skeletogenic GRN and identify key, unresolved questions as a guide for future work.

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Calcium transport into the cells of the sea urchin larva in relation to spicule formation

Cited by 72 publications

References 45 publications

Possible co-option of a VEGF-driven tubulogenesis program for biomineralization in echinoderms

Possible co-option of a VEGF-driven tubulogenesis program for biomineralization in echinoderms

Possible cooption of a VEGF-driven tubulogenesis program for biomineralization in echinoderms

From genome to anatomy: The architecture and evolution of the skeletogenic gene regulatory network of sea urchins and other echinoderms

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