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Fluid extraction from the left-right organizer uncovers mechanical properties needed for symmetry breaking

2023-07Artigo científico Acesso aberto
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dc.contributor.authorSampaio, Pedro
dc.contributor.authorPestana, Sara
dc.contributor.authorBota, Catarina
dc.contributor.authorGuerrero, Adán
dc.contributor.authorTelley, Ivo A.
dc.contributor.authorSmith, David
dc.contributor.authorLopes, Susana Santos
dc.contributor.institutionNOVA Medical School|Faculdade de Ciências Médicas (NMS|FCM)
dc.contributor.pbleLife Sciences Publications
dc.date.accessioned2023-09-13T22:19:17Z
dc.date.available2023-09-13T22:19:17Z
dc.date.issued2023-07
dc.descriptionFunding Information: This work was mainly supported by the Fundação para a Ciência e Tecnologia (research grant – PTDC/ BEX-BID/1411/2014). Funding Information: PS was funded by a PhD fellowship FCT: SFRH/BD/111611/2015. SP was funded by a PhD fellowship FCT: SFRH/BD/130272/2017 CB was funded by a PhD fellowship FCT: SFRH/BD/141034/2018 IAT was funded by FCT Investigator IF/00082/2013, EU FP7-PEOPLE-2013-CIG (N° 818743) and by the Fundação Calouste Gulbenkian (FCG). AG thanks to CZI Expanding Global Access to Bioimaging and to PAPIIT (IN211821) for funding support. DJS acknowledges support from the Engineering and Physical Sciences Research Council UK via a Healthcare Technologies Challenge Award (EP/N021096/1) and a Turing Fellowship (EP/N510129/1). SL was funded by FCT Investigator IF/00951/2012, by NOVA Medical School and by FCT CEEC-IND 2018. Zebrafish were reared and maintained in the NMS Fish Facility, with the support from the research consortia Congento funded by LISBOA-01–0145-FEDER-022170, microscopy was performed at the IGC Advanced Imaging Facility which is supported by PPBI-POCI-01–0145-FEDER-022122; all co-financed by Lisboa Regional Operational Program (Lisboa2020), under the Portugal 2020 Partnership Agreement, through the European Regional Development Fund (ERDF) and Fundação para a Ciência e Tecnologia under the project. The project LysoCil funded by the European Union Horizon 2020 research and innovation under grant agreement No 811087 supported SL, PS and SP travelling to the FASEB cilia meeting in the USA in 2019, where this work was presented and discussed with peers. We thank Sérgio Dias for reviewing the final version of the manuscript. Publisher Copyright: © Sampaio, Pestana et al.
dc.description.abstractHumans and other vertebrates define body axis left-right asymmetry in the early stages of embryo development. The mechanism behind left-right establishment is not fully understood. Symmetry breaking occurs in a dedicated organ called the left-right organizer (LRO) and involves motile cilia generating fluid-flow therein. However, it has been a matter of debate whether the process of symmetry breaking relies on a chemosensory or a mechanosensory mechanism (Shinohara et al., 2012). Novel tailored manipulations for LRO fluid extraction in living zebrafish embryos allowed us to pinpoint a physiological developmental period for breaking left-right symmetry during development. The shortest critical time-window was narrowed to one hour and characterized by a mild counterclockwise flow. The experimental challenge consisted in emptying the LRO of its fluid, abrogating simultaneously flow force and chemical determinants. Our findings revealed an unprecedented recovery capacity of the embryo to re-fil and re-circulate new LRO fluid. The embryos that later developed laterality problems were found to be those that had lower anterior angular velocity and thus less anteriorposterior heterogeneity. Next, aiming to test the presence of any secreted determinant, we replaced the extracted LRO fluid by a physiological buffer. Despite some transitory flow homogenization, laterality defects were absent unless viscosity was altered, demonstrating that symmetry breaking does not depend on the nature of the fluid content but is rather sensitive to fluid mechanics. Altogether, we conclude that the zebrafish LRO is more sensitive to fluid dynamics for symmetry breaking.en
dc.description.versionpublishersversion
dc.description.versionpublished
dc.format.extent8125697
dc.identifier.doi10.7554/ELIFE.83861
dc.identifier.issn2050-084X
dc.identifier.otherPURE: 71170428
dc.identifier.otherPURE UUID: 51beaa42-316c-45ca-b4cd-84c9ba34a7a1
dc.identifier.otherScopus: 85165500122
dc.identifier.otherPubMed: 37477290
dc.identifier.urihttp://hdl.handle.net/10362/157776
dc.identifier.urlhttps://www.scopus.com/pages/publications/85165500122
dc.language.isoeng
dc.peerreviewedyes
dc.subjectGeneral Neuroscience
dc.subjectGeneral Biochemistry,Genetics and Molecular Biology
dc.subjectGeneral Immunology and Microbiology
dc.titleFluid extraction from the left-right organizer uncovers mechanical properties needed for symmetry breakingen
dc.typejournal article
degois.publication.titleeLife
degois.publication.volume12
dspace.entity.typePublication
rcaap.rightsopenAccess

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