Quantitative videomicroscopy reveals latent control of cell-pair rotations in vivo

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• dc.contributor.author Kozak, Eva L.
• dc.contributor.author Miranda-Rodríguez, Jerónimo R.
• dc.contributor.author Borges, Augusto
• dc.contributor.author Dierkes, Kai
• dc.contributor.author Mineo, Alessandro
• dc.contributor.author Pinto-Teixeira, Filipo
• dc.contributor.author Viader Llargués, Oriol
• dc.contributor.author Solon, Jérôme
• dc.contributor.author Chara, Osvaldo
• dc.contributor.author López-Schier, Hernán
• dc.date.accessioned 2023-06-20T06:24:49Z
• dc.date.available 2023-06-20T06:24:49Z
• dc.date.issued 2023
• dc.description.abstract Collective cell rotations are widely used during animal organogenesis. Theoretical and in vitro studies have conceptualized rotating cells as identical rigid-point objects that stochastically break symmetry to move monotonously and perpetually within an inert environment. However, it is unclear whether this notion can be extrapolated to a natural context, where rotations are ephemeral and heterogeneous cellular cohorts interact with an active epithelium. In zebrafish neuromasts, nascent sibling hair cells invert positions by rotating ≤180° around their geometric center after acquiring different identities via Notch1a-mediated asymmetric repression of Emx2. Here, we show that this multicellular rotation is a three-phasic movement that progresses via coherent homotypic coupling and heterotypic junction remodeling. We found no correlation between rotations and epithelium-wide cellular flow or anisotropic resistive forces. Moreover, the Notch/Emx2 status of the cell dyad does not determine asymmetric interactions with the surrounding epithelium. Aided by computer modeling, we suggest that initial stochastic inhomogeneities generate a metastable state that poises cells to move and spontaneous intercellular coordination of the resulting instabilities enables persistently directional rotations, whereas Notch1a-determined symmetry breaking buffers rotational noise.
• dc.description.sponsorship J.R.M.-R. was funded by the European Union's Horizon 2020 research and innovation program under the HORIZON EUROPE Marie Sklodowska-Curie Actions grant agreement 840834. A.B. and O.C. were funded by Fondo para la Investigación Científica y Tecnológica (grants PICT-2017-2307 and PICT-2019-2019-03828 granted to O.C.). O.C. was funded by the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and by the School of Biosciences, University of Nottingham. H.L.-S. was funded by the Helmholtz-Gemeinschaft and the New York University Abu Dhabi. Open access funding provided by New York University Abu Dhabi. Deposited in PMC for immediate release.
• dc.format.mimetype application/pdf
• dc.identifier.citation Kozak EL, Miranda-Rodríguez JR, Borges A, Dierkes K, Mineo A, Pinto-Teixeira F, Viader-Llargués O, Solon J, Chara O, López-Schier H. Quantitative videomicroscopy reveals latent control of cell-pair rotations in vivo. Development. 2023 May 1;150(9):dev200975. DOI: 10.1242/dev.200975
• dc.identifier.doi http://dx.doi.org/10.1242/dev.200975
• dc.identifier.issn 0950-1991
• dc.identifier.uri http://hdl.handle.net/10230/57260
• dc.language.iso eng
• dc.publisher Company of Biologists
• dc.relation.ispartof Development. 2023 May 1;150(9):dev200975
• dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/840834
• dc.rights © 2023. Published by The Company of Biologists Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
• dc.rights.accessRights info:eu-repo/semantics/openAccess
• dc.rights.uri http://creativecommons.org/licenses/by/4.0
• dc.subject.keyword Multicellular rotations
• dc.subject.keyword Patterning
• dc.subject.keyword Regeneration
• dc.subject.keyword Symmetry breaking
• dc.subject.keyword Zebrafish
• dc.title Quantitative videomicroscopy reveals latent control of cell-pair rotations in vivo
• dc.type info:eu-repo/semantics/article
• dc.type.version info:eu-repo/semantics/publishedVersion