{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,9]],"date-time":"2026-06-09T08:17:14Z","timestamp":1780993034238,"version":"3.54.1"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1008780","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,3,4]],"date-time":"2021-03-04T00:00:00Z","timestamp":1614816000000}}],"reference-count":80,"publisher":"Public Library of Science (PLoS)","issue":"2","license":[{"start":{"date-parts":[[2021,2,22]],"date-time":"2021-02-22T00:00:00Z","timestamp":1613952000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003977","name":"Israel Science Foundation","doi-asserted-by":"publisher","award":["41\/14"],"award-info":[{"award-number":["41\/14"]}],"id":[{"id":"10.13039\/501100003977","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003977","name":"Israel Science Foundation","doi-asserted-by":"crossref","award":["211\/20"],"award-info":[{"award-number":["211\/20"]}],"id":[{"id":"10.13039\/501100003977","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Zuckerman post-doctoral fellowship"},{"name":"ISEF doctoral fellowship"}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>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\u2019t 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.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1008780","type":"journal-article","created":{"date-parts":[[2021,2,22]],"date-time":"2021-02-22T13:37:01Z","timestamp":1614001021000},"page":"e1008780","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":26,"title":["Calcium-vesicles perform active diffusion in the sea urchin embryo during larval biomineralization"],"prefix":"10.1371","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1180-1957","authenticated-orcid":true,"given":"Mark R.","family":"Winter","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Miri","family":"Morgulis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tsvia","family":"Gildor","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7707-5970","authenticated-orcid":true,"given":"Andrew R.","family":"Cohen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9497-4938","authenticated-orcid":true,"given":"Smadar","family":"Ben-Tabou de-Leon","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,2,22]]},"reference":[{"key":"pcbi.1008780.ref001","doi-asserted-by":"crossref","DOI":"10.1093\/oso\/9780195049770.001.0001","volume-title":"On Biomineralization.","author":"HA Lowenstam","year":"1989"},{"key":"pcbi.1008780.ref002","doi-asserted-by":"crossref","first-page":"e1905554","DOI":"10.1002\/adma.201905554","article-title":"Viewpoint: Homeostasis as Inspiration-Toward Interactive Materials","author":"MM Lerch","year":"2020","journal-title":"Adv Mater"},{"issue":"18","key":"pcbi.1008780.ref003","doi-asserted-by":"crossref","first-page":"e1702170","DOI":"10.1002\/smll.201702170","article-title":"Bioinspired Universal Flexible Elastomer-Based Microchannels.","volume":"14","author":"F Wu","year":"2018","journal-title":"Small"},{"issue":"4","key":"pcbi.1008780.ref004","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1089\/soro.2017.0002","article-title":"A Biologically Inspired, Functionally Graded End Effector for Soft Robotics Applications.","volume":"4","author":"K Kumar","year":"2017","journal-title":"Soft Robot."},{"issue":"3","key":"pcbi.1008780.ref005","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1590\/S0100-879X2010007500008","article-title":"Proteoliposomes as matrix vesicles\u2019 biomimetics to study the initiation of skeletal mineralization","volume":"43","author":"AM Simao","year":"2010","journal-title":"Braz J Med Biol Res"},{"issue":"8","key":"pcbi.1008780.ref006","doi-asserted-by":"crossref","first-page":"129629","DOI":"10.1016\/j.bbagen.2020.129629","article-title":"Matrix vesicle biomimetics harboring Annexin A5 and alkaline phosphatase bind to the native collagen matrix produced by mineralizing vascular smooth muscle cells","author":"M Bolean","year":"2020","journal-title":"Biochim Biophys Acta Gen Subj"},{"issue":"68","key":"pcbi.1008780.ref007","first-page":"1","article-title":"Biomineralization Forming Process and Bio-inspired Nanomaterials for Biomedical Application: A Review.","volume":"9","author":"Y Chen","year":"2019","journal-title":"Minerals."},{"issue":"2\u20134","key":"pcbi.1008780.ref008","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1159\/000324245","article-title":"Evolutionary origins of animal skeletal biomineralization.","volume":"194","author":"DJ Murdock","year":"2011","journal-title":"Cells Tissues Organs"},{"key":"pcbi.1008780.ref009","doi-asserted-by":"crossref","first-page":"329","DOI":"10.2113\/0540329","article-title":"Biomineralization and Evolutionary History.","volume":"54","author":"AH Knoll","year":"2003","journal-title":"Reviews in Mineralogy and Geochemistry."},{"issue":"6247","key":"pcbi.1008780.ref010","doi-asserted-by":"crossref","first-page":"aaa6760","DOI":"10.1126\/science.aaa6760","article-title":"CRYSTAL GROWTH. 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The distribution of microtubules","volume":"41","author":"JR Gibbins","year":"1969","journal-title":"J Cell Biol"},{"issue":"1","key":"pcbi.1008780.ref021","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1006\/jsbi.1998.4081","article-title":"Cellular control over spicule formation in sea urchin embryos: A structural approach","volume":"125","author":"E Beniash","year":"1999","journal-title":"J Struct Biol"},{"issue":"16","key":"pcbi.1008780.ref022","doi-asserted-by":"crossref","first-page":"6088","DOI":"10.1073\/pnas.1118085109","article-title":"Phase transitions in biogenic amorphous calcium carbonate","volume":"109","author":"YU Gong","year":"2012","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1008780.ref023","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1146\/annurev.biophys.35.040405.102002","article-title":"Gene regulation: Gene control network in development","volume":"36","author":"SBT De-Leon","year":"2007","journal-title":"Annual Review of 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reports."},{"issue":"9","key":"pcbi.1008780.ref037","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1016\/j.tcb.2009.04.004","article-title":"Intracellular transport by active diffusion","volume":"19","author":"CP Brangwynne","year":"2009","journal-title":"Trends Cell Biol"},{"issue":"4","key":"pcbi.1008780.ref038","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1038\/ncb3131","article-title":"Active diffusion positions the nucleus in mouse oocytes","volume":"17","author":"M Almonacid","year":"2015","journal-title":"Nat Cell Biol"},{"issue":"1","key":"pcbi.1008780.ref039","doi-asserted-by":"crossref","first-page":"1520","DOI":"10.1038\/s41467-017-01414-6","article-title":"Active diffusion and advection in Drosophila oocytes result from the interplay of actin and microtubules.","volume":"8","author":"M Drechsler","year":"2017","journal-title":"Nat Commun."},{"issue":"3","key":"pcbi.1008780.ref040","doi-asserted-by":"crossref","DOI":"10.1083\/jcb.201908195","article-title":"Active diffusion in oocytes nonspecifically centers large objects during prophase I and meiosis I","volume":"219","author":"A Colin","year":"2020","journal-title":"J Cell Biol"},{"issue":"4","key":"pcbi.1008780.ref041","doi-asserted-by":"crossref","first-page":"950","DOI":"10.1242\/dev.105585","article-title":"Genome-wide analysis of the skeletogenic gene regulatory network of sea urchins","volume":"141","author":"K Rafiq","year":"2014","journal-title":"Development"},{"issue":"20","key":"pcbi.1008780.ref042","doi-asserted-by":"crossref","first-page":"4214","DOI":"10.1242\/dev.100479","article-title":"Growth factor-mediated mesodermal cell guidance and skeletogenesis during sea urchin gastrulation","volume":"140","author":"A Adomako-Ankomah","year":"2013","journal-title":"Development"},{"issue":"12","key":"pcbi.1008780.ref043","doi-asserted-by":"crossref","first-page":"2293","DOI":"10.1242\/dev.005108","article-title":"Localized VEGF signaling from ectoderm to mesenchyme cells controls morphogenesis of the sea urchin embryo skeleton","volume":"134","author":"L Duloquin","year":"2007","journal-title":"Development"},{"issue":"2","key":"pcbi.1008780.ref044","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.gep.2014.10.002","article-title":"Signal-dependent regulation of the sea urchin skeletogenic gene regulatory network","volume":"16","author":"Z Sun","year":"2014","journal-title":"Gene Expr Patterns"},{"issue":"43","key":"pcbi.1008780.ref045","doi-asserted-by":"crossref","first-page":"17908","DOI":"10.1021\/ja309024b","article-title":"Recombinant sea urchin vascular endothelial growth factor directs single-crystal growth and branching in vitro","volume":"134","author":"RT Knapp","year":"2012","journal-title":"J Am Chem Soc"},{"issue":"6","key":"pcbi.1008780.ref046","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1016\/j.cell.2011.08.039","article-title":"Basic and therapeutic aspects of angiogenesis","volume":"146","author":"M Potente","year":"2011","journal-title":"Cell"},{"issue":"6208","key":"pcbi.1008780.ref047","doi-asserted-by":"crossref","first-page":"1257998","DOI":"10.1126\/science.1257998","article-title":"Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution","volume":"346","author":"BC Chen","year":"2014","journal-title":"Science"},{"issue":"7","key":"pcbi.1008780.ref048","doi-asserted-by":"crossref","first-page":"690","DOI":"10.1038\/nmeth.2075","article-title":"Icy: an open bioimage informatics platform for extended reproducible research.","volume":"9","author":"F de Chaumont","year":"2012","journal-title":"Nat Methods"},{"issue":"9","key":"pcbi.1008780.ref049","doi-asserted-by":"crossref","first-page":"951","DOI":"10.1038\/nmeth.3036","article-title":"Fast, accurate reconstruction of cell lineages from large-scale fluorescence microscopy data","volume":"11","author":"F Amat","year":"2014","journal-title":"Nat Methods"},{"key":"pcbi.1008780.ref050","first-page":"368","article-title":"CellProfiler Tracer: exploring and validating high-throughput, time-lapse microscopy image data","volume":"16","author":"MA Bray","year":"2015","journal-title":"BMC Bioinformatics"},{"issue":"3","key":"pcbi.1008780.ref051","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1038\/nmeth.2808","article-title":"Objective comparison of particle tracking methods.","volume":"11","author":"N Chenouard","year":"2014","journal-title":"Nat Methods."},{"issue":"4","key":"pcbi.1008780.ref052","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1016\/j.stemcr.2015.08.002","article-title":"Computational Image Analysis Reveals Intrinsic Multigenerational Differences between Anterior and Posterior Cerebral Cortex Neural Progenitor Cells.","volume":"5","author":"MR Winter","year":"2015","journal-title":"Stem cell reports"},{"issue":"22","key":"pcbi.1008780.ref053","doi-asserted-by":"crossref","first-page":"3530","DOI":"10.1093\/bioinformatics\/btw406","article-title":"LEVER: software tools for segmentation, tracking and lineaging of proliferating cells","volume":"32","author":"M Winter","year":"2016","journal-title":"Bioinformatics"},{"key":"pcbi.1008780.ref054","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.biocel.2016.10.002","article-title":"Light sheet microscopes: Novel imaging toolbox for visualizing life\u2019s processes","volume":"80","author":"JM Heddleston","year":"2016","journal-title":"Int J Biochem Cell Biol"},{"issue":"10","key":"pcbi.1008780.ref055","doi-asserted-by":"crossref","first-page":"982","DOI":"10.1002\/jemt.20838","article-title":"AFM measurement of the stiffness of layers of agarose gel patterned with polylysine","volume":"73","author":"M Salerno","year":"2010","journal-title":"Microsc Res Tech"},{"issue":"1","key":"pcbi.1008780.ref056","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1006\/dbio.2000.9696","article-title":"Cell-substrate interactions during sea urchin gastrulation: migrating primary mesenchyme cells interact with and align extracellular matrix fibers that contain ECM3, a molecule with NG2-like and multiple calcium-binding domains","volume":"222","author":"PG Hodor","year":"2000","journal-title":"Dev Biol"},{"issue":"1","key":"pcbi.1008780.ref057","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1504\/IJCBDD.2012.045950","article-title":"Axonal transport analysis using Multitemporal Association Tracking","volume":"5","author":"MR Winter","year":"2012","journal-title":"Int J Comput Biol Drug 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A"},{"issue":"1","key":"pcbi.1008780.ref061","doi-asserted-by":"crossref","first-page":"e88","DOI":"10.1002\/cpcb.88","article-title":"Practical Considerations in Particle and Object Tracking and Analysis.","volume":"83","author":"J Aaron","year":"2019","journal-title":"Curr Protoc Cell Biol"},{"issue":"46","key":"pcbi.1008780.ref062","doi-asserted-by":"crossref","first-page":"32158","DOI":"10.1074\/jbc.M109.047381","article-title":"Single vesicle millisecond fusion kinetics reveals number of SNARE complexes optimal for fast SNARE-mediated membrane fusion","volume":"284","author":"MK Domanska","year":"2009","journal-title":"J Biol Chem"},{"issue":"2","key":"pcbi.1008780.ref063","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1038\/ncb3288","article-title":"Orchestrated content release from Drosophila glue-protein vesicles by a contractile actomyosin network","volume":"18","author":"T Rousso","year":"2016","journal-title":"Nat Cell 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