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Dynamic Mechanochemical feedback between curved membranes and BAR protein self-organization

Roux, Anabel-Lise Le; Tozzi, Caterina; Walani, Nikhil; Quiroga, Xarxa; Zalvidea, Dobryna; Trepat, Xavier; Staykova, Margarita; Arroyo, Marino; Roca-Cusachs, Pere

Dynamic Mechanochemical feedback between curved membranes and BAR protein self-organization Thumbnail


Authors

Anabel-Lise Le Roux

Caterina Tozzi

Nikhil Walani

Xarxa Quiroga

Dobryna Zalvidea

Xavier Trepat

Marino Arroyo

Pere Roca-Cusachs



Abstract

In many physiological situations, BAR proteins reshape membranes with pre-existing curvature (templates), contributing to essential cellular processes. However, the mechanism and the biological implications of this reshaping process remain unclear. Here we show, both experimentally and through modelling, that BAR proteins reshape low curvature membrane templates through a mechanochemical phase transition. This phenomenon depends on initial template shape and involves the co-existence and progressive transition between distinct local states in terms of molecular organization (protein arrangement and density) and membrane shape (template size and spherical versus cylindrical curvature). Further, we demonstrate in cells that this phenomenon enables a mechanotransduction mode, in which cellular stretch leads to the mechanical formation of membrane templates, which are then reshaped into tubules by BAR proteins. Our results demonstrate the interplay between membrane mechanics and BAR protein molecular organization, integrating curvature sensing and generation in a comprehensive framework with implications for cell mechanical responses.

Citation

Roux, A. L., Tozzi, C., Walani, N., Quiroga, X., Zalvidea, D., Trepat, X., …Roca-Cusachs, P. (2021). Dynamic Mechanochemical feedback between curved membranes and BAR protein self-organization. Nature Communications, 12, Article 6550. https://doi.org/10.1038/s41467-021-26591-3

Journal Article Type Article
Acceptance Date Oct 11, 2021
Online Publication Date Nov 12, 2021
Publication Date 2021
Deposit Date Nov 2, 2021
Publicly Available Date Jan 31, 2022
Journal Nature Communications
Publisher Nature Research
Peer Reviewed Peer Reviewed
Volume 12
Article Number 6550
DOI https://doi.org/10.1038/s41467-021-26591-3
Public URL https://durham-repository.worktribe.com/output/1226861
Related Public URLs https://doi.org/10.1101/2020.09.23.310169

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http://creativecommons.org/licenses/by/4.0/

Copyright Statement
This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.






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