Calcium-vesicles Perform Active Diffusion in the Sea Urchin Embryo During Larval Biomineralization

Overview

Journal PLoS Comput Biol

Specialty Biology

Date 2021 Feb 22

PMID 33617532

Citations 8

Authors

Mark R Winter

Miri Morgulis

Tsvia Gildor

Andrew R Cohen

Smadar Ben-Tabou de-Leon

Affiliations

Soon will be listed here.

Abstract

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 cells 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.

Citing Articles

A mechanosensitive circuit of FAK, ROCK, and ERK controls biomineral growth and morphology in the sea urchin embryo.

Layous M, Gildor T, Nehrer T, Qassem A, Wolfenson H, Ben-Tabou de-Leon S Proc Natl Acad Sci U S A. 2024; 122(1):e2408628121.

PMID: 39739788 PMC: 11725891. DOI: 10.1073/pnas.2408628121.

ROCK and the actomyosin network control biomineral growth and morphology during sea urchin skeletogenesis.

Hijaze E, Gildor T, Seidel R, Layous M, Winter M, Bertinetti L Elife. 2024; 12.

PMID: 38573316 PMC: 10994658. DOI: 10.7554/eLife.89080.

microRNA-1 regulates sea urchin skeletogenesis by directly targeting skeletogenic genes and modulating components of signaling pathways.

Sampilo N, Song J Dev Biol. 2024; 508:123-137.

PMID: 38290645 PMC: 10985635. DOI: 10.1016/j.ydbio.2024.01.010.

Molecular and Cellular Characterization of the TH Pathway in the Sea Urchin .

Cocurullo M, Paganos P, Wood N, Arnone M, Oliveri P Cells. 2023; 12(2).

PMID: 36672206 PMC: 9856734. DOI: 10.3390/cells12020272.

Carbonic anhydrases in development: morphological observations and gene expression profiling in sea urchin embryos exposed to acetazolamide.

Zito F, Bonaventura R, Costa C, Russo R Open Biol. 2023; 13(1):220254.

PMID: 36597694 PMC: 9811153. DOI: 10.1098/rsob.220254.

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