Vimentin Intermediate Filament Rings Deform the Nucleus During the First Steps of Adhesion.

Emmanuel Terriac,Franziska Lautenschläger,Susanne Schütz

doi:10.3389/fcell.2019.00106

Emmanuel Terriac, Franziska Lautenschläger + Show 1 more

Open Access

https://doi.org/10.3389/fcell.2019.00106

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Abstract

During cell spreading, cells undergo many changes to their architecture and their mechanical properties. Vimentin, as an integral part of the cell architecture, and its mechanical stability must adapt to the new state of the cell. This study focuses on the structures formed by vimentin during the first steps of cell adhesion. Very early, ball-like structures, or “knots,” are seen and often vimentin filaments emerge in the shape of rings around the nucleus. Although intermediate filaments are not known to be associated to motor proteins to form contractile systems, these rings can nonetheless strongly deform the cell nucleus. In the first 6 to 12 h of adhesion, these vimentin knots and rings disappear, and the intermediate filament network returns to the state seen before detachment of the cells. As these vimentin structures are very transient in the early steps of cell spreading, they have rarely been described in the literature. However, they can also be seen during mitosis, which is an event that involves partial detachment and re-spreading of the cells. Interestingly, the turnover dynamics of vimentin are reduced in both the knots and rings, compared to vimentin in the lamellipodia. It remains to define how the force is transmitted from the ball-like structures to the rings, and to measure the impact of such strong nuclear deformation on gene expression during cell re-spreading and the rearrangement of the vimentin network.

Highlights

During embryogenesis, as in the more detrimental context of metastasis, cells translocate from their original surrounding or tissue in other tissues (Greenburg and Hay, 1982; Hay, 1995; Davies, 1996; Nieto et al, 2016; Li et al, 2017; Roche, 2018)
Large ball-like structures, or knots, can be seen close to the nuclei. Those structures were accompanied by thin lines of vimentin that span the nuclei, and which were related to nuclear deformation
Our study shows that during cell adhesion and spreading, vimentin intermediate filaments can assemble into ball-like structures, or knots

Summary

Introduction

As in the more detrimental context of metastasis, cells translocate from their original surrounding or tissue in other tissues (Greenburg and Hay, 1982; Hay, 1995; Davies, 1996; Nieto et al, 2016; Li et al, 2017; Roche, 2018) Upon arrival at their new location, the cells need to anchor to their new environment. During these processes, to correctly migrate, cells detach, by at least partial down-regulation of the expression of E-cadherin, among other factors, and upregulation of the expression of mesenchymal markers, like N-cadherin and vimentin (Grunert et al, 2003; Christofori, 2006). In vitro cell migration studies often require full detachment of cultured cells from their

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