Disentangling the contributions of stress fibres and the unbundled actin meshwork to the anisotropy of cortical tension in response to cell shape

ABSTRACT Many fundamental biological processes, in particular development and morphogenetic movements, involve tissue and cell deformation, as well as the generation of anisotropic mechanical stresses. They are often accompanied by the appearance of oriented contractile actomyosin structures resembling the stress fibres (SF) observed in vitro . Here, we investigate, at the single cell level, how cell shape — by itself — could control the structure and tension of the actomyosin cortex. Using a unique combination of 3D micropatterning, single peripheral SF (PSF) tension measurement, laser ablation and image analysis, we show that cell shape anisotropy, e.g. its 2D aspect ratio, is indeed sufficient to induce anisotropy of the cortical structure and tension. In particular, taking into account the experimentally measured anisotropy of the cortical meshwork, we could quantify cortical tension and decouple the contribution originating from bundled actin (oriented cortical stress fibres, CSF) and the contribution of the unbundled actin meshwork (UAM). We show that the increase of cortical tension anisotropy with the cell’s aspect ratio depends on the CSF alignment and orientation, the contribution of the isotropic mesh being independent of cell shape. Remarkably, while experimental data from single stress fibre measurements and laser ablation were analysed through different theoretical frameworks, namely that of negative pressure in nematics and hole drilling in prestressed materials, we found quantitatively the same composite material behaviour. In sum, we decipher here the very material properties of the actomyosin cortex, and its sensitivity to cell shape which is at the root of many mechanobiological processes, in particular morphogenesis.