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

Kozak, Eva L.; Miranda-Rodríguez, Jerónimo R.; Borges, Augusto; Dierkes, Kai; Mineo, Alessandro; Pinto-Teixeira, Filipo; Viader Llargués, Oriol; Solon, Jérôme; Chara, Osvaldo; López-Schier, Hernán

doi:http://dx.doi.org/10.1242/dev.200975

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

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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

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.