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Adaptive Response of Actin Bundles under Mechanical Stress

Actin is one of the main components of the architecture of cells. Actin filaments form different polymer networks with versatile mechanical properties that depend on their spatial organization and the presence of cross-linkers. Here, we investigate the mechanical properties of actin bundles in the a...

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Autores principales: Rückerl, Florian, Lenz, Martin, Betz, Timo, Manzi, John, Martiel, Jean-Louis, Safouane, Mahassine, Paterski-Boujemaa, Rajaa, Blanchoin, Laurent, Sykes, Cécile
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Biophysical Society 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5611681/
https://www.ncbi.nlm.nih.gov/pubmed/28877490
http://dx.doi.org/10.1016/j.bpj.2017.07.017
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author Rückerl, Florian
Lenz, Martin
Betz, Timo
Manzi, John
Martiel, Jean-Louis
Safouane, Mahassine
Paterski-Boujemaa, Rajaa
Blanchoin, Laurent
Sykes, Cécile
author_facet Rückerl, Florian
Lenz, Martin
Betz, Timo
Manzi, John
Martiel, Jean-Louis
Safouane, Mahassine
Paterski-Boujemaa, Rajaa
Blanchoin, Laurent
Sykes, Cécile
author_sort Rückerl, Florian
collection PubMed
description Actin is one of the main components of the architecture of cells. Actin filaments form different polymer networks with versatile mechanical properties that depend on their spatial organization and the presence of cross-linkers. Here, we investigate the mechanical properties of actin bundles in the absence of cross-linkers. Bundles are polymerized from the surface of mDia1-coated latex beads, and deformed by manipulating both ends through attached beads held by optical tweezers, allowing us to record the applied force. Bundle properties are strikingly different from the ones of a homogeneous isotropic beam. Successive compression and extension leads to a decrease in the buckling force that we attribute to the bundle remaining slightly curved after the first deformation. Furthermore, we find that the bundle is solid, and stiff to bending, along the long axis, whereas it has a liquid and viscous behavior in the transverse direction. Interpretation of the force curves using a Maxwell visco-elastic model allows us to extract the bundle mechanical parameters and confirms that the bundle is composed of weakly coupled filaments. At short times, the bundle behaves as an elastic material, whereas at long times, filaments flow in the longitudinal direction, leading to bundle restructuring. Deviations from the model reveal a complex adaptive rheological behavior of bundles. Indeed, when allowed to anneal between phases of compression and extension, the bundle reinforces. Moreover, we find that the characteristic visco-elastic time is inversely proportional to the compression speed. Actin bundles are therefore not simple force transmitters, but instead, complex mechano-transducers that adjust their mechanics to external stimulation. In cells, where actin bundles are mechanical sensors, this property could contribute to their adaptability.
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spelling pubmed-56116812018-09-05 Adaptive Response of Actin Bundles under Mechanical Stress Rückerl, Florian Lenz, Martin Betz, Timo Manzi, John Martiel, Jean-Louis Safouane, Mahassine Paterski-Boujemaa, Rajaa Blanchoin, Laurent Sykes, Cécile Biophys J Cell Biophysics Actin is one of the main components of the architecture of cells. Actin filaments form different polymer networks with versatile mechanical properties that depend on their spatial organization and the presence of cross-linkers. Here, we investigate the mechanical properties of actin bundles in the absence of cross-linkers. Bundles are polymerized from the surface of mDia1-coated latex beads, and deformed by manipulating both ends through attached beads held by optical tweezers, allowing us to record the applied force. Bundle properties are strikingly different from the ones of a homogeneous isotropic beam. Successive compression and extension leads to a decrease in the buckling force that we attribute to the bundle remaining slightly curved after the first deformation. Furthermore, we find that the bundle is solid, and stiff to bending, along the long axis, whereas it has a liquid and viscous behavior in the transverse direction. Interpretation of the force curves using a Maxwell visco-elastic model allows us to extract the bundle mechanical parameters and confirms that the bundle is composed of weakly coupled filaments. At short times, the bundle behaves as an elastic material, whereas at long times, filaments flow in the longitudinal direction, leading to bundle restructuring. Deviations from the model reveal a complex adaptive rheological behavior of bundles. Indeed, when allowed to anneal between phases of compression and extension, the bundle reinforces. Moreover, we find that the characteristic visco-elastic time is inversely proportional to the compression speed. Actin bundles are therefore not simple force transmitters, but instead, complex mechano-transducers that adjust their mechanics to external stimulation. In cells, where actin bundles are mechanical sensors, this property could contribute to their adaptability. The Biophysical Society 2017-09-05 2017-09-05 /pmc/articles/PMC5611681/ /pubmed/28877490 http://dx.doi.org/10.1016/j.bpj.2017.07.017 Text en © 2017 Biophysical Society. http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Cell Biophysics
Rückerl, Florian
Lenz, Martin
Betz, Timo
Manzi, John
Martiel, Jean-Louis
Safouane, Mahassine
Paterski-Boujemaa, Rajaa
Blanchoin, Laurent
Sykes, Cécile
Adaptive Response of Actin Bundles under Mechanical Stress
title Adaptive Response of Actin Bundles under Mechanical Stress
title_full Adaptive Response of Actin Bundles under Mechanical Stress
title_fullStr Adaptive Response of Actin Bundles under Mechanical Stress
title_full_unstemmed Adaptive Response of Actin Bundles under Mechanical Stress
title_short Adaptive Response of Actin Bundles under Mechanical Stress
title_sort adaptive response of actin bundles under mechanical stress
topic Cell Biophysics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5611681/
https://www.ncbi.nlm.nih.gov/pubmed/28877490
http://dx.doi.org/10.1016/j.bpj.2017.07.017
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