Abstract
Interphase microtubule organization is critical for cell function and tissue architecture. In general, physical mechanisms are sufficient to drive microtubule organization in single cells, whereas cells within tissues are thought to utilize signalling mechanisms. By improving the imaging and quantitation of microtubule alignment within developing Drosophila embryos, here we demonstrate that microtubule alignment underneath the apical surface of epithelial cells follows cell shape. During development, epidermal cell elongation and microtubule alignment occur simultaneously, but by perturbing cell shape, we discover that microtubule organization responds to cell shape, rather than the converse. A simple set of microtubule behaviour rules is sufficient for a computer model to mimic the observed responses to changes in cell surface geometry. Moreover, we show that microtubules colliding with cell boundaries zip-up or depolymerize in an angle-dependent manner, as predicted by the model. Finally, we show microtubule alignment responds to cell shape in diverse epithelia.
Highlights
Interphase microtubule organization is critical for cell function and tissue architecture
Our experimental perturbations of cell elongation had a greater impact on MT organization than perturbations of MTs had on cell shape
This prediction is further supported by our finding that one of the key aspects of MT behaviour suggested to be required for MT self-organization by our in silico model, namely angle-dependent outcomes of MT collisions with cell boundaries, could be documented in Drosophila embryonic epidermal cells
Summary
Interphase microtubule organization is critical for cell function and tissue architecture. We describe improvements in our ability to quantify MT alignment, by using 3D Structured Illumination Microscopy (3D-SIM) to generate high-resolution images of the MTs, and combining this with automated image analysis to quantify MT organization relative to cell shape This analysis showed that even within a multicellular tissue MT alignment correlated well with cell shape, suggesting that a PCP mechanism may not be necessary. By analysing EB1-green fluorescent protein (GFP) trajectories and collisions with the cell membrane, we were able to confirm the angle-dependence of MT–cell boundary collisions (zipping-up versus catastrophes), a mechanism predicted to contribute to MT alignment by the computer model This demonstrates that the organization of MT arrays within epithelial layers of Drosophila can be largely explained by the response of growing MTs to the geometric constraints of the cell
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