1. Quantitative videomicroscopy reveals latent control of cell-pair rotations in vivo
- Author
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European Commission, Fondo para la Investigación Científica y Tecnológica (Argentina), Consejo Nacional de Investigaciones Científicas y Técnicas (Argentina), University of Nottingham, New York University Abu Dhabi, Miranda-Rodríguez, Jerónimo R. [0000-0002-2775-6719], Borges, Augusto [0000-0003-0773-5352], Dierkes, Kai [0000-0002-9174-3517], Mineo, Alessandro [0000-0002-7047-1313], Solon, Jérôme [0000-0001-9967-9794], Chara, Osvaldo [0000-0002-0868-2507], López-Schier, Hernán [0000-0001-7925-7439], Kozak, Eva L., Miranda-Rodríguez, Jerónimo R., Borges, Augusto, Dierkes, Kai, Mineo, Alessandro, Pinto-Teixeira, Filipe, Viader-Llargués, Oriol, Solon, Jérôme, Chara, Osvaldo, López-Schier, Hernán, European Commission, Fondo para la Investigación Científica y Tecnológica (Argentina), Consejo Nacional de Investigaciones Científicas y Técnicas (Argentina), University of Nottingham, New York University Abu Dhabi, Miranda-Rodríguez, Jerónimo R. [0000-0002-2775-6719], Borges, Augusto [0000-0003-0773-5352], Dierkes, Kai [0000-0002-9174-3517], Mineo, Alessandro [0000-0002-7047-1313], Solon, Jérôme [0000-0001-9967-9794], Chara, Osvaldo [0000-0002-0868-2507], López-Schier, Hernán [0000-0001-7925-7439], Kozak, Eva L., Miranda-Rodríguez, Jerónimo R., Borges, Augusto, Dierkes, Kai, Mineo, Alessandro, Pinto-Teixeira, Filipe, Viader-Llargués, Oriol, Solon, Jérôme, Chara, Osvaldo, and López-Schier, Hernán
- 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.
- Published
- 2023