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Quantitative videomicroscopy reveals latent control of cell-pair rotations in vivo.
Development 150:14 (2023)
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.
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Publication type
Article: Journal article
Document type
Scientific Article
Keywords
Multicellular Rotations ; Patterning ; Regeneration ; Symmetry Breaking ; Zebrafish; Gene-expression; Motion; Regeneration; Migration; Drosophila; Establishment; Morphogenesis; Segmentation; Organization; Mechanics
ISSN (print) / ISBN
0950-1991
e-ISSN
1477-9129
Quellenangaben
Volume: 150,
Issue: 9,
Article Number: 14
Publisher
Company of Biologists
Publishing Place
Bidder Building, Station Rd, Histon, Cambridge Cb24 9lf, England
Non-patent literature
Publications
Reviewing status
Peer reviewed
Grants
Marie Curie Actions (MSCA)
Helmholtz-Gemeinschaft
New York University Abu Dhabi
School of Biosciences, University of Nottingham
Consejo Nacional de Investigaciones Cientificas y Tecnicas (CONICET)
Fondo para la Investigacion Cientifica y Tecnologica
European Union
Helmholtz-Gemeinschaft
New York University Abu Dhabi
School of Biosciences, University of Nottingham
Consejo Nacional de Investigaciones Cientificas y Tecnicas (CONICET)
Fondo para la Investigacion Cientifica y Tecnologica
European Union