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Extensile to contractile transition in active microtubule–actin composites generates layered asters with programmable lifetimes

We study a reconstituted composite system consisting of an active microtubule network interdigitated with a passive network of entangled F-actin filaments. Increasing the concentration of filamentous actin controls the emergent dynamics, inducing a transition from turbulent-like flows to bulk contra...

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Detalles Bibliográficos
Autores principales: Berezney, John, Goode, Bruce L., Fraden, Seth, Dogic, Zvonimir
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8812548/
https://www.ncbi.nlm.nih.gov/pubmed/35086931
http://dx.doi.org/10.1073/pnas.2115895119
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author Berezney, John
Goode, Bruce L.
Fraden, Seth
Dogic, Zvonimir
author_facet Berezney, John
Goode, Bruce L.
Fraden, Seth
Dogic, Zvonimir
author_sort Berezney, John
collection PubMed
description We study a reconstituted composite system consisting of an active microtubule network interdigitated with a passive network of entangled F-actin filaments. Increasing the concentration of filamentous actin controls the emergent dynamics, inducing a transition from turbulent-like flows to bulk contractions. At intermediate concentrations, where the active stresses change their symmetry from anisotropic extensile to isotropic contracting, the composite separates into layered asters that coexist with the background turbulent fluid. Contracted onion-like asters have a radially extending microtubule-rich cortex that envelops alternating layers of microtubules and F-actin. These self-regulating structures undergo internal reorganization, which appears to minimize the surface area and maintain the ordered layering, even when undergoing aster merging events. Finally, the layered asters are metastable structures. Their lifetime, which ranges from minutes to hours, is encoded in the material properties of the composite. These results challenge the current models of active matter. They demonstrate self-organized dynamical states and patterns evocative of those observed in the cytoskeleton do not require precise biochemical regulation, but can arise from purely mechanical interactions of actively driven filamentous materials.
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spelling pubmed-88125482022-02-16 Extensile to contractile transition in active microtubule–actin composites generates layered asters with programmable lifetimes Berezney, John Goode, Bruce L. Fraden, Seth Dogic, Zvonimir Proc Natl Acad Sci U S A Physical Sciences We study a reconstituted composite system consisting of an active microtubule network interdigitated with a passive network of entangled F-actin filaments. Increasing the concentration of filamentous actin controls the emergent dynamics, inducing a transition from turbulent-like flows to bulk contractions. At intermediate concentrations, where the active stresses change their symmetry from anisotropic extensile to isotropic contracting, the composite separates into layered asters that coexist with the background turbulent fluid. Contracted onion-like asters have a radially extending microtubule-rich cortex that envelops alternating layers of microtubules and F-actin. These self-regulating structures undergo internal reorganization, which appears to minimize the surface area and maintain the ordered layering, even when undergoing aster merging events. Finally, the layered asters are metastable structures. Their lifetime, which ranges from minutes to hours, is encoded in the material properties of the composite. These results challenge the current models of active matter. They demonstrate self-organized dynamical states and patterns evocative of those observed in the cytoskeleton do not require precise biochemical regulation, but can arise from purely mechanical interactions of actively driven filamentous materials. National Academy of Sciences 2022-01-27 2022-02-01 /pmc/articles/PMC8812548/ /pubmed/35086931 http://dx.doi.org/10.1073/pnas.2115895119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access 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
Berezney, John
Goode, Bruce L.
Fraden, Seth
Dogic, Zvonimir
Extensile to contractile transition in active microtubule–actin composites generates layered asters with programmable lifetimes
title Extensile to contractile transition in active microtubule–actin composites generates layered asters with programmable lifetimes
title_full Extensile to contractile transition in active microtubule–actin composites generates layered asters with programmable lifetimes
title_fullStr Extensile to contractile transition in active microtubule–actin composites generates layered asters with programmable lifetimes
title_full_unstemmed Extensile to contractile transition in active microtubule–actin composites generates layered asters with programmable lifetimes
title_short Extensile to contractile transition in active microtubule–actin composites generates layered asters with programmable lifetimes
title_sort extensile to contractile transition in active microtubule–actin composites generates layered asters with programmable lifetimes
topic Physical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8812548/
https://www.ncbi.nlm.nih.gov/pubmed/35086931
http://dx.doi.org/10.1073/pnas.2115895119
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