A SLC4 family bicarbonate transporter is critical for intracellular pH regulation and biomineralization in sea urchin embryos

Hu, Marian Yong-An; Yan, Jia‐Jiun; Petersen, Inga; Himmerkus, Nina; Stumpp, Meike

doi:10.7554/elife.36600

Cited by 41 publications

(65 citation statements)

References 49 publications

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“…Two inorganic carbon transporters (JGI ID 466232, 436956) were differentially expressed at the ambient calcium concentration compared with the limited calcium concentration, suggesting that these solute SLC4 transporters are related to the calcium concentration. In sea urchin embryos, the SLC4 family bicarbonate transporter regulates intracellular pH and biomineralization and is crucial for the production of an elaborate calcitic endoskeleton [64]. The increased SLC4 gene expression seen at the ambient-calcium concentration (10 mM) compared with the limited-calcium concentrations suggests its potential involvement in the calcification process.…”

Section: Discussionmentioning

confidence: 99%

De novo transcriptome profile of coccolithophorid alga Emiliania huxleyi CCMP371 at different calcium concentrations with proteome analysis

et al. 2019

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The haptophyte alga Emiliania huxleyi is the most abundant coccolithophore in the modern ocean and produces elaborate calcite crystals, called coccolith, in a separate intracellular compartment known as the coccolith vesicle. Despite the importance of biomineralization in coccolithophores, the molecular mechanism underlying it remains unclear. Understanding this precise machinery at the molecular level will provide the knowledge needed to enable further manipulation of biomineralization. In our previous study, altering the calcium concentration modified the calcifying ability of E . huxleyi CCMP371. Therefore in this study, we tested E . huxleyi cells acclimated to three different calcium concentrations (0, 0.1, and 10 mM). To understand the whole transcript profile at different calcium concentrations, RNA-sequencing was performed and used for de novo assembly and annotation. The differentially expressed genes (DEGs) among the three different calcium concentrations were analyzed. The functional classification by gene ontology (GO) revealed that ‘intrinsic component of membrane’ was the most enriched of the GO terms at the ambient calcium concentration (10 mM) compared with the limited calcium concentrations (0 and 0.1 mM). Moreover, the DEGs in those comparisons were enriched mainly in ‘secondary metabolites biosynthesis, transport and catabolism’ and ‘signal transduction mechanisms’ in the KOG clusters and ‘processing in endoplasmic reticulum’, and ‘ABC transporters’ in the KEGG pathways. Furthermore, metabolic pathways involved in protein synthesis were enriched among the differentially expressed proteins. The results of this study provide a molecular profile for understanding the expression of transcripts and proteins in E . huxleyi at different calcium concentrations, which will help to identify the detailed mechanism of its calcification.

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Section: Discussionmentioning

confidence: 99%

De novo transcriptome profile of coccolithophorid alga Emiliania huxleyi CCMP371 at different calcium concentrations with proteome analysis

et al. 2019

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“…Additionally, the compensation of induced alkalosis was very weak in oyster mantle epithelial cells in comparison to mammalian cells types (Bourgeois et al 2018 ). This may be because these cells rarely experience such an extracellular alkalosis in the environment (seawater) or hemolymph and similar weak compensations to an ammonia induced alkalosis have also been observed in sea urchin larvae (Stumpp et al 2012 ; Hu et al 2018 ).…”

Section: Discussionmentioning

confidence: 81%

Intracellular pH regulation in mantle epithelial cells of the Pacific oyster, Crassostrea gigas

Ramesh

Melzner

et al. 2020

J Comp Physiol B

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Shell formation and repair occurs under the control of mantle epithelial cells in bivalve molluscs. However, limited information is available on the precise acid–base regulatory machinery present within these cells, which are fundamental to calcification. Here, we isolate mantle epithelial cells from the Pacific oyster, Crassostrea gigas and utilise live cell imaging in combination with the fluorescent dye, BCECF-AM to study intracellular pH (pHi) regulation. To elucidate the involvement of various ion transport mechanisms, modified seawater solutions (low sodium, low bicarbonate) and specific inhibitors for acid–base proteins were used. Diminished pH recovery in the absence of Na+ and under inhibition of sodium/hydrogen exchangers (NHEs) implicate the involvement of a sodium dependent cellular proton extrusion mechanism. In addition, pH recovery was reduced under inhibition of carbonic anhydrases. These data provide the foundation for a better understanding of acid–base regulation underlying the physiology of calcification in bivalves.

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“…Together, these findings indicate that the biological regulation of calcium vesicle content is distinct between the skeletogenic and the ectodermal cells which apparently leads to higher calcium vesicle volume in the skeletogenic biomineralizing cells. There is a multitude of evidence of a specific activation of genes that regulate homeostasis in the skeletogenic cells, e.g., the carbonic anhydrase like-7, Caral7[17, 41], and the bicarbonate transporter, SCL4a10[61]. However, further studies are required to identify the genes responsible for the specific regulation of Ca +2 ions in the vesicles of the skeletogenic cells.…”

Section: Discussionmentioning

confidence: 99%

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

Winter

Morgulis

Gildor

et al. 2020

Preprint

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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 mineral-vesicle motion and the molecular mechanisms that regulate it, are not well understood. Sea urchin larval skeletogenesis provides an excellent platform for the analyses of vesicle kinetics. Here we used calcein labeling and lattice light-sheet microscopy to investigate the three-dimensional (3D) vesicle dynamics in control sea urchin embryos and in Vascular Endothelial Growth Factor Receptor (VEGFR) inhibited embryos, where skeletogenesis is blocked. We developed computational tools for displaying 3D-volumetric movies and for automatically quantifying vesicle dynamics in the different embryonic tissues. Our findings imply that calcium vesicles perform an active diffusion motion in all the cells of the embryo. This mode of diffusion is defined by the mechanical properties of the cells and the dynamic rearrangements of the cytoskeletal network. The diffusion coefficient is larger in the mesenchymal skeletogenic cells compared to the epithelial ectodermal cells, possibly due to the distinct mechanical properties of the two tissues. Vesicle motion is not directed toward the biomineralization compartment, but the vesicles slow down when they approach it, and probably bind for mineral deposition. Under VEGFR inhibition, vesicle volume increases and vesicle speed is reduced but the vesicles continue in their diffusive motion. Overall, our studies provide an unprecedented view of calcium vesicle 3D-dynamics and illuminate possible molecular mechanisms that control vesicle dynamics and deposition.

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A SLC4 family bicarbonate transporter is critical for intracellular pH regulation and biomineralization in sea urchin embryos

Cited by 41 publications

References 49 publications

De novo transcriptome profile of coccolithophorid alga Emiliania huxleyi CCMP371 at different calcium concentrations with proteome analysis

De novo transcriptome profile of coccolithophorid alga Emiliania huxleyi CCMP371 at different calcium concentrations with proteome analysis

Intracellular pH regulation in mantle epithelial cells of the Pacific oyster, Crassostrea gigas

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

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