Microtubule organization is determined by the shape of epithelial cells

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.

The walkoff effect: cargo distribution implies motor type in bidirectional microtubule bundles

“…To validate the predicted roles of kinesins and dyneins in transport on MT networks with mixed directionality we turned to epithelial cells in the Drosophila embryonic epidermis. There, the apical MTs grow from the sites of cell-cell adhesion on the cell boundaries and are restricted to a thin 1 µm layer below the cell apical surface [26,38,60]. To investigate the directions of MT growth, we examined live embryos expressing the GFPtagged End Binding protein 1 (EB1-GFP) at the stage 15 of the embryonic development ( Fig.…”

“…This means that the directionality of MTs networks directly influences the motor transport. Depending on the cell type, MT networks are either unipolar, with all the MTs oriented in the same direction as in the vertebrate axons, or have mixed directionality as in vertebrate dendrites or epithelial cells [36][37][38][39][40][41]. Additionally, MTs form bundles, where several MTs are closely apposed, often connected by specialized cross-linking proteins [42][43][44], and unidirectional bundles facilitate intracellular transport [45,46].…”

Cytoskeletal organization in isolated plant cells under geometry control

“…The cell cytoskeleton is often viewed as a major determinant of cell shape. While the impact of geometry on cytoskeletal organization is well characterized in animal cells (Gomez et al 2016) , (Théry et al 2006;Versaevel et al 2012) ; (Bao et al 2017;Bao et al 2019) and in in vitro systems (Cosentino Lagomarsino et al 2007; Soares e Silva et al 2011;Alvarado et al 2014;Pinot et al 2009) , single cell analysis in planta is lacking. Since plant cells are encased into a stiff wall, strong and persistent geometrical constraints act on cells throughout the plant life, t he importance of cell geometry for organising cytoskeletal filaments in living plant cells needs to be better understood.…”

Plant cortical microtubule dynamics and cell division plane orientation

“…microtubule can not translate or rotate, but can treadmill (Shaw et al, 2003;Vos et al, 2004). Due to this attachment, the dynamics of microtubule is influenced by cell geometry (Gomez et al, 2016), through a geometrical constraint that depends on the cell shape. The imposed physical and geometrical constraints can change: (1) The interaction length (see Sec.…”

“…However, the molecular/physical basis behind the establishment of such order and orientation of the cortical microtubule array remained unclear. The possible known default factors that control the cortical microtubule dynamics are cell shapes (Gomez et al, 2016) and edge-catastrophe (Ambrose et al, 2011). Additional factors that might also be involved are auxin-dependent transcriptionally regulated enhanced face-stability/reduced edge-catastrophe to microtubules.…”