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Non-specific adhesive forces between filaments and membraneless organelles
Many membraneless organelles are liquid-like domains that form inside the active, viscoelastic environment of living cells through phase separation. To investigate the potential coupling of phase separation with the cytoskeleton, we quantify the structural correlations of membraneless organelles (st...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Nature Publishing Group UK
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9106579/ https://www.ncbi.nlm.nih.gov/pubmed/35582428 http://dx.doi.org/10.1038/s41567-022-01537-8 |
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author | Böddeker, Thomas J. Rosowski, Kathryn A. Berchtold, Doris Emmanouilidis, Leonidas Han, Yaning Allain, Frédéric H. T. Style, Robert W. Pelkmans, Lucas Dufresne, Eric R. |
author_facet | Böddeker, Thomas J. Rosowski, Kathryn A. Berchtold, Doris Emmanouilidis, Leonidas Han, Yaning Allain, Frédéric H. T. Style, Robert W. Pelkmans, Lucas Dufresne, Eric R. |
author_sort | Böddeker, Thomas J. |
collection | PubMed |
description | Many membraneless organelles are liquid-like domains that form inside the active, viscoelastic environment of living cells through phase separation. To investigate the potential coupling of phase separation with the cytoskeleton, we quantify the structural correlations of membraneless organelles (stress granules) and cytoskeletal filaments (microtubules) in a human-derived epithelial cell line. We find that microtubule networks are substantially denser in the vicinity of stress granules. When microtubules are depolymerized, the sub-units localize near the surface of the stress granules. We interpret these data using a thermodynamic model of partitioning of particles to the surface and bulk of the droplets. In this framework, our data are consistent with a weak (≲k(B)T) affinity of the microtubule sub-units for stress granule interfaces. As microtubules polymerize, their interfacial affinity increases, providing sufficient adhesion to deform droplets and/or the network. Our work suggests that proteins and other objects in the cell have a non-specific affinity for droplet interfaces that increases with the contact area and becomes most apparent when they have no preference for the interior of a droplet over the rest of the cytoplasm. We validate this basic physical phenomenon in vitro through the interaction of a simple protein–RNA condensate with microtubules. |
format | Online Article Text |
id | pubmed-9106579 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-91065792022-05-15 Non-specific adhesive forces between filaments and membraneless organelles Böddeker, Thomas J. Rosowski, Kathryn A. Berchtold, Doris Emmanouilidis, Leonidas Han, Yaning Allain, Frédéric H. T. Style, Robert W. Pelkmans, Lucas Dufresne, Eric R. Nat Phys Article Many membraneless organelles are liquid-like domains that form inside the active, viscoelastic environment of living cells through phase separation. To investigate the potential coupling of phase separation with the cytoskeleton, we quantify the structural correlations of membraneless organelles (stress granules) and cytoskeletal filaments (microtubules) in a human-derived epithelial cell line. We find that microtubule networks are substantially denser in the vicinity of stress granules. When microtubules are depolymerized, the sub-units localize near the surface of the stress granules. We interpret these data using a thermodynamic model of partitioning of particles to the surface and bulk of the droplets. In this framework, our data are consistent with a weak (≲k(B)T) affinity of the microtubule sub-units for stress granule interfaces. As microtubules polymerize, their interfacial affinity increases, providing sufficient adhesion to deform droplets and/or the network. Our work suggests that proteins and other objects in the cell have a non-specific affinity for droplet interfaces that increases with the contact area and becomes most apparent when they have no preference for the interior of a droplet over the rest of the cytoplasm. We validate this basic physical phenomenon in vitro through the interaction of a simple protein–RNA condensate with microtubules. Nature Publishing Group UK 2022-03-24 2022 /pmc/articles/PMC9106579/ /pubmed/35582428 http://dx.doi.org/10.1038/s41567-022-01537-8 Text en © The Author(s) 2022, corrected publication 2022 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 Böddeker, Thomas J. Rosowski, Kathryn A. Berchtold, Doris Emmanouilidis, Leonidas Han, Yaning Allain, Frédéric H. T. Style, Robert W. Pelkmans, Lucas Dufresne, Eric R. Non-specific adhesive forces between filaments and membraneless organelles |
title | Non-specific adhesive forces between filaments and membraneless organelles |
title_full | Non-specific adhesive forces between filaments and membraneless organelles |
title_fullStr | Non-specific adhesive forces between filaments and membraneless organelles |
title_full_unstemmed | Non-specific adhesive forces between filaments and membraneless organelles |
title_short | Non-specific adhesive forces between filaments and membraneless organelles |
title_sort | non-specific adhesive forces between filaments and membraneless organelles |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9106579/ https://www.ncbi.nlm.nih.gov/pubmed/35582428 http://dx.doi.org/10.1038/s41567-022-01537-8 |
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