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The material properties of a bacterial-derived biomolecular condensate tune biological function in natural and synthetic systems

Intracellular phase separation is emerging as a universal principle for organizing biochemical reactions in time and space. It remains incompletely resolved how biological function is encoded in these assemblies and whether this depends on their material state. The conserved intrinsically disordered...

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Autores principales: Lasker, Keren, Boeynaems, Steven, Lam, Vinson, Scholl, Daniel, Stainton, Emma, Briner, Adam, Jacquemyn, Maarten, Daelemans, Dirk, Deniz, Ashok, Villa, Elizabeth, Holehouse, Alex S., Gitler, Aaron D., Shapiro, Lucy
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9512792/
https://www.ncbi.nlm.nih.gov/pubmed/36163138
http://dx.doi.org/10.1038/s41467-022-33221-z
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author Lasker, Keren
Boeynaems, Steven
Lam, Vinson
Scholl, Daniel
Stainton, Emma
Briner, Adam
Jacquemyn, Maarten
Daelemans, Dirk
Deniz, Ashok
Villa, Elizabeth
Holehouse, Alex S.
Gitler, Aaron D.
Shapiro, Lucy
author_facet Lasker, Keren
Boeynaems, Steven
Lam, Vinson
Scholl, Daniel
Stainton, Emma
Briner, Adam
Jacquemyn, Maarten
Daelemans, Dirk
Deniz, Ashok
Villa, Elizabeth
Holehouse, Alex S.
Gitler, Aaron D.
Shapiro, Lucy
author_sort Lasker, Keren
collection PubMed
description Intracellular phase separation is emerging as a universal principle for organizing biochemical reactions in time and space. It remains incompletely resolved how biological function is encoded in these assemblies and whether this depends on their material state. The conserved intrinsically disordered protein PopZ forms condensates at the poles of the bacterium Caulobacter crescentus, which in turn orchestrate cell-cycle regulating signaling cascades. Here we show that the material properties of these condensates are determined by a balance between attractive and repulsive forces mediated by a helical oligomerization domain and an expanded disordered region, respectively. A series of PopZ mutants disrupting this balance results in condensates that span the material properties spectrum, from liquid to solid. A narrow range of condensate material properties supports proper cell division, linking emergent properties to organismal fitness. We use these insights to repurpose PopZ as a modular platform for generating tunable synthetic condensates in human cells.
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spelling pubmed-95127922022-09-28 The material properties of a bacterial-derived biomolecular condensate tune biological function in natural and synthetic systems Lasker, Keren Boeynaems, Steven Lam, Vinson Scholl, Daniel Stainton, Emma Briner, Adam Jacquemyn, Maarten Daelemans, Dirk Deniz, Ashok Villa, Elizabeth Holehouse, Alex S. Gitler, Aaron D. Shapiro, Lucy Nat Commun Article Intracellular phase separation is emerging as a universal principle for organizing biochemical reactions in time and space. It remains incompletely resolved how biological function is encoded in these assemblies and whether this depends on their material state. The conserved intrinsically disordered protein PopZ forms condensates at the poles of the bacterium Caulobacter crescentus, which in turn orchestrate cell-cycle regulating signaling cascades. Here we show that the material properties of these condensates are determined by a balance between attractive and repulsive forces mediated by a helical oligomerization domain and an expanded disordered region, respectively. A series of PopZ mutants disrupting this balance results in condensates that span the material properties spectrum, from liquid to solid. A narrow range of condensate material properties supports proper cell division, linking emergent properties to organismal fitness. We use these insights to repurpose PopZ as a modular platform for generating tunable synthetic condensates in human cells. Nature Publishing Group UK 2022-09-26 /pmc/articles/PMC9512792/ /pubmed/36163138 http://dx.doi.org/10.1038/s41467-022-33221-z Text en © The Author(s) 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
Lasker, Keren
Boeynaems, Steven
Lam, Vinson
Scholl, Daniel
Stainton, Emma
Briner, Adam
Jacquemyn, Maarten
Daelemans, Dirk
Deniz, Ashok
Villa, Elizabeth
Holehouse, Alex S.
Gitler, Aaron D.
Shapiro, Lucy
The material properties of a bacterial-derived biomolecular condensate tune biological function in natural and synthetic systems
title The material properties of a bacterial-derived biomolecular condensate tune biological function in natural and synthetic systems
title_full The material properties of a bacterial-derived biomolecular condensate tune biological function in natural and synthetic systems
title_fullStr The material properties of a bacterial-derived biomolecular condensate tune biological function in natural and synthetic systems
title_full_unstemmed The material properties of a bacterial-derived biomolecular condensate tune biological function in natural and synthetic systems
title_short The material properties of a bacterial-derived biomolecular condensate tune biological function in natural and synthetic systems
title_sort material properties of a bacterial-derived biomolecular condensate tune biological function in natural and synthetic systems
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9512792/
https://www.ncbi.nlm.nih.gov/pubmed/36163138
http://dx.doi.org/10.1038/s41467-022-33221-z
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