Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Böddeker, Thomas J., Rosowski, Kathryn A., Berchtold, Doris, Emmanouilidis, Leonidas, Han, Yaning, Allain, Frédéric H. T., Style, Robert W., Pelkmans, Lucas, Dufresne, Eric R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
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
_version_ 1784708320326582272
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
work_keys_str_mv AT boddekerthomasj nonspecificadhesiveforcesbetweenfilamentsandmembranelessorganelles
AT rosowskikathryna nonspecificadhesiveforcesbetweenfilamentsandmembranelessorganelles
AT berchtolddoris nonspecificadhesiveforcesbetweenfilamentsandmembranelessorganelles
AT emmanouilidisleonidas nonspecificadhesiveforcesbetweenfilamentsandmembranelessorganelles
AT hanyaning nonspecificadhesiveforcesbetweenfilamentsandmembranelessorganelles
AT allainfredericht nonspecificadhesiveforcesbetweenfilamentsandmembranelessorganelles
AT stylerobertw nonspecificadhesiveforcesbetweenfilamentsandmembranelessorganelles
AT pelkmanslucas nonspecificadhesiveforcesbetweenfilamentsandmembranelessorganelles
AT dufresneericr nonspecificadhesiveforcesbetweenfilamentsandmembranelessorganelles