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

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 model...

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Autores principales: Le Roux, Anabel-Lise, Tozzi, Caterina, Walani, Nikhil, Quiroga, Xarxa, Zalvidea, Dobryna, Trepat, Xavier, Staykova, Margarita, Arroyo, Marino, Roca-Cusachs, Pere
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8589976/
https://www.ncbi.nlm.nih.gov/pubmed/34772909
http://dx.doi.org/10.1038/s41467-021-26591-3
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author Le Roux, Anabel-Lise
Tozzi, Caterina
Walani, Nikhil
Quiroga, Xarxa
Zalvidea, Dobryna
Trepat, Xavier
Staykova, Margarita
Arroyo, Marino
Roca-Cusachs, Pere
author_facet Le Roux, Anabel-Lise
Tozzi, Caterina
Walani, Nikhil
Quiroga, Xarxa
Zalvidea, Dobryna
Trepat, Xavier
Staykova, Margarita
Arroyo, Marino
Roca-Cusachs, Pere
author_sort Le Roux, Anabel-Lise
collection PubMed
description 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.
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spelling pubmed-85899762021-11-15 Dynamic mechanochemical feedback between curved membranes and BAR protein self-organization Le Roux, Anabel-Lise Tozzi, Caterina Walani, Nikhil Quiroga, Xarxa Zalvidea, Dobryna Trepat, Xavier Staykova, Margarita Arroyo, Marino Roca-Cusachs, Pere Nat Commun Article 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. Nature Publishing Group UK 2021-11-12 /pmc/articles/PMC8589976/ /pubmed/34772909 http://dx.doi.org/10.1038/s41467-021-26591-3 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access 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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Le Roux, Anabel-Lise
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
title Dynamic mechanochemical feedback between curved membranes and BAR protein self-organization
title_full Dynamic mechanochemical feedback between curved membranes and BAR protein self-organization
title_fullStr Dynamic mechanochemical feedback between curved membranes and BAR protein self-organization
title_full_unstemmed Dynamic mechanochemical feedback between curved membranes and BAR protein self-organization
title_short Dynamic mechanochemical feedback between curved membranes and BAR protein self-organization
title_sort dynamic mechanochemical feedback between curved membranes and bar protein self-organization
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8589976/
https://www.ncbi.nlm.nih.gov/pubmed/34772909
http://dx.doi.org/10.1038/s41467-021-26591-3
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