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Tensile force-induced cytoskeletal remodeling: Mechanics before chemistry
Understanding cellular remodeling in response to mechanical stimuli is a critical step in elucidating mechanical activation of biochemical signaling pathways. Experimental evidence indicates that external stress-induced subcellular adaptation is accomplished through dynamic cytoskeletal reorganizati...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7326277/ https://www.ncbi.nlm.nih.gov/pubmed/32520928 http://dx.doi.org/10.1371/journal.pcbi.1007693 |
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author | Li, Xiaona Ni, Qin He, Xiuxiu Kong, Jun Lim, Soon-Mi Papoian, Garegin A. Trzeciakowski, Jerome P. Trache, Andreea Jiang, Yi |
author_facet | Li, Xiaona Ni, Qin He, Xiuxiu Kong, Jun Lim, Soon-Mi Papoian, Garegin A. Trzeciakowski, Jerome P. Trache, Andreea Jiang, Yi |
author_sort | Li, Xiaona |
collection | PubMed |
description | Understanding cellular remodeling in response to mechanical stimuli is a critical step in elucidating mechanical activation of biochemical signaling pathways. Experimental evidence indicates that external stress-induced subcellular adaptation is accomplished through dynamic cytoskeletal reorganization. To study the interactions between subcellular structures involved in transducing mechanical signals, we combined experimental data and computational simulations to evaluate real-time mechanical adaptation of the actin cytoskeletal network. Actin cytoskeleton was imaged at the same time as an external tensile force was applied to live vascular smooth muscle cells using a fibronectin-functionalized atomic force microscope probe. Moreover, we performed computational simulations of active cytoskeletal networks under an external tensile force. The experimental data and simulation results suggest that mechanical structural adaptation occurs before chemical adaptation during filament bundle formation: actin filaments first align in the direction of the external force by initializing anisotropic filament orientations, then the chemical evolution of the network follows the anisotropic structures to further develop the bundle-like geometry. Our findings present an alternative two-step explanation for the formation of actin bundles due to mechanical stimulation and provide new insights into the mechanism of mechanotransduction. |
format | Online Article Text |
id | pubmed-7326277 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-73262772020-07-10 Tensile force-induced cytoskeletal remodeling: Mechanics before chemistry Li, Xiaona Ni, Qin He, Xiuxiu Kong, Jun Lim, Soon-Mi Papoian, Garegin A. Trzeciakowski, Jerome P. Trache, Andreea Jiang, Yi PLoS Comput Biol Research Article Understanding cellular remodeling in response to mechanical stimuli is a critical step in elucidating mechanical activation of biochemical signaling pathways. Experimental evidence indicates that external stress-induced subcellular adaptation is accomplished through dynamic cytoskeletal reorganization. To study the interactions between subcellular structures involved in transducing mechanical signals, we combined experimental data and computational simulations to evaluate real-time mechanical adaptation of the actin cytoskeletal network. Actin cytoskeleton was imaged at the same time as an external tensile force was applied to live vascular smooth muscle cells using a fibronectin-functionalized atomic force microscope probe. Moreover, we performed computational simulations of active cytoskeletal networks under an external tensile force. The experimental data and simulation results suggest that mechanical structural adaptation occurs before chemical adaptation during filament bundle formation: actin filaments first align in the direction of the external force by initializing anisotropic filament orientations, then the chemical evolution of the network follows the anisotropic structures to further develop the bundle-like geometry. Our findings present an alternative two-step explanation for the formation of actin bundles due to mechanical stimulation and provide new insights into the mechanism of mechanotransduction. Public Library of Science 2020-06-10 /pmc/articles/PMC7326277/ /pubmed/32520928 http://dx.doi.org/10.1371/journal.pcbi.1007693 Text en © 2020 Li et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Li, Xiaona Ni, Qin He, Xiuxiu Kong, Jun Lim, Soon-Mi Papoian, Garegin A. Trzeciakowski, Jerome P. Trache, Andreea Jiang, Yi Tensile force-induced cytoskeletal remodeling: Mechanics before chemistry |
title | Tensile force-induced cytoskeletal remodeling: Mechanics before chemistry |
title_full | Tensile force-induced cytoskeletal remodeling: Mechanics before chemistry |
title_fullStr | Tensile force-induced cytoskeletal remodeling: Mechanics before chemistry |
title_full_unstemmed | Tensile force-induced cytoskeletal remodeling: Mechanics before chemistry |
title_short | Tensile force-induced cytoskeletal remodeling: Mechanics before chemistry |
title_sort | tensile force-induced cytoskeletal remodeling: mechanics before chemistry |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7326277/ https://www.ncbi.nlm.nih.gov/pubmed/32520928 http://dx.doi.org/10.1371/journal.pcbi.1007693 |
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