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Actin–microtubule dynamic composite forms responsive active matter with memory

Active cytoskeletal materials in vitro demonstrate self-organizing properties similar to those observed in their counterparts in cells. However, the search to emulate phenomena observed in living matter has fallen short of producing a cytoskeletal network that would be structurally stable yet posses...

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Autores principales: Kučera, Ondřej, Gaillard, Jérémie, Guérin, Christophe, Théry, Manuel, Blanchoin, Laurent
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9351490/
https://www.ncbi.nlm.nih.gov/pubmed/35878035
http://dx.doi.org/10.1073/pnas.2209522119
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author Kučera, Ondřej
Gaillard, Jérémie
Guérin, Christophe
Théry, Manuel
Blanchoin, Laurent
author_facet Kučera, Ondřej
Gaillard, Jérémie
Guérin, Christophe
Théry, Manuel
Blanchoin, Laurent
author_sort Kučera, Ondřej
collection PubMed
description Active cytoskeletal materials in vitro demonstrate self-organizing properties similar to those observed in their counterparts in cells. However, the search to emulate phenomena observed in living matter has fallen short of producing a cytoskeletal network that would be structurally stable yet possess adaptive plasticity. Here, we address this challenge by combining cytoskeletal polymers in a composite where self-assembling microtubules and actin filaments collectively self-organize due to the activity of microtubule-percolating molecular motors. We demonstrate that microtubules spatially organize actin filaments that in turn guide microtubules. The two networks align in an ordered fashion using this feedback loop. In this composite, actin filaments can act as structural memory and, depending on the concentration of the components, microtubules either write this memory or get guided by it. The system is sensitive to external stimuli, suggesting possible autoregulatory behavior in changing mechanochemical environments. We thus establish an artificial active actin–microtubule composite as a system demonstrating architectural stability and plasticity.
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spelling pubmed-93514902023-01-25 Actin–microtubule dynamic composite forms responsive active matter with memory Kučera, Ondřej Gaillard, Jérémie Guérin, Christophe Théry, Manuel Blanchoin, Laurent Proc Natl Acad Sci U S A Physical Sciences Active cytoskeletal materials in vitro demonstrate self-organizing properties similar to those observed in their counterparts in cells. However, the search to emulate phenomena observed in living matter has fallen short of producing a cytoskeletal network that would be structurally stable yet possess adaptive plasticity. Here, we address this challenge by combining cytoskeletal polymers in a composite where self-assembling microtubules and actin filaments collectively self-organize due to the activity of microtubule-percolating molecular motors. We demonstrate that microtubules spatially organize actin filaments that in turn guide microtubules. The two networks align in an ordered fashion using this feedback loop. In this composite, actin filaments can act as structural memory and, depending on the concentration of the components, microtubules either write this memory or get guided by it. The system is sensitive to external stimuli, suggesting possible autoregulatory behavior in changing mechanochemical environments. We thus establish an artificial active actin–microtubule composite as a system demonstrating architectural stability and plasticity. National Academy of Sciences 2022-07-25 2022-08-02 /pmc/articles/PMC9351490/ /pubmed/35878035 http://dx.doi.org/10.1073/pnas.2209522119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Physical Sciences
Kučera, Ondřej
Gaillard, Jérémie
Guérin, Christophe
Théry, Manuel
Blanchoin, Laurent
Actin–microtubule dynamic composite forms responsive active matter with memory
title Actin–microtubule dynamic composite forms responsive active matter with memory
title_full Actin–microtubule dynamic composite forms responsive active matter with memory
title_fullStr Actin–microtubule dynamic composite forms responsive active matter with memory
title_full_unstemmed Actin–microtubule dynamic composite forms responsive active matter with memory
title_short Actin–microtubule dynamic composite forms responsive active matter with memory
title_sort actin–microtubule dynamic composite forms responsive active matter with memory
topic Physical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9351490/
https://www.ncbi.nlm.nih.gov/pubmed/35878035
http://dx.doi.org/10.1073/pnas.2209522119
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