Cells Dev 2022 Jun 01;170:203791. doi: 10.1016/j.cdev.2022.203791.

Mechanical strain breaks planar symmetry in embryonic epithelia via polarized microtubules.

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Mechanical strain can act as a global cue to orient the core planar cell polarity pathway (Fz-PCP) in developing epithelia, but how strain directs a Fz-PCP vector is not known. Here we use live cell imaging of apical microtubules (MTs) and components of the Fz-PCP pathway to analyze epithelial cells in Xenopus embryos as they respond to anisotropic mechanical strain and form a Fz-PCP axis. We find that a Fz-PCP axis can be detected approximately 40 min after the application of strain. By contrast, the density and length of apical MTs increases rapidly (5-10 min) in response to strain, independently of Fz-PCP. These early-forming apical MTs are planar polarized: they align to the strain axis and display a marked bias in plus-end orientation that invariably points towards the cell edge opposite the direction of strain application. We show that these MTs can promote the vectorial transport of Dvl3-GFP containing vesicles along the apical surface in a directed manner, perhaps explaining why PCP signaling fails when MTs are disrupted. Finally, we provide evidence that the Fz-PCP axis feeds back after an hour to stabilize oriented apical MTs. These results provide insights into how mechanical strain acts as a developmental cue within the appropriate time frame and with the appropriate vector to promote planar axis formation.

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Species referenced: Xenopus laevis
Genes referenced: dvl3