Cofilin-mediated actin filament network flexibility facilitates 2D to 3D actomyosin shape change
The organization of actin filaments (F-actin) into crosslinked networks determines the transmission of mechanical stresses within the cytoskeleton and subsequent changes in cell and tissue shape. Principally mediated by proteins such as α-actinin, F-actin crosslinking increases both network connecti...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2024-03-01
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| Series: | European Journal of Cell Biology |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S0171933523000948 |
| _version_ | 1797345966253146112 |
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| author | Zachary Gao Sun Vikrant Yadav Sorosh Amiri Wenxiang Cao Enrique M. De La Cruz Michael Murrell |
| author_facet | Zachary Gao Sun Vikrant Yadav Sorosh Amiri Wenxiang Cao Enrique M. De La Cruz Michael Murrell |
| author_sort | Zachary Gao Sun |
| collection | DOAJ |
| description | The organization of actin filaments (F-actin) into crosslinked networks determines the transmission of mechanical stresses within the cytoskeleton and subsequent changes in cell and tissue shape. Principally mediated by proteins such as α-actinin, F-actin crosslinking increases both network connectivity and rigidity, thereby facilitating stress transmission at low crosslinking yet attenuating transmission at high crosslinker concentration. Here, we engineer a two-dimensional model of the actomyosin cytoskeleton, in which myosin-induced mechanical stresses are controlled by light. We alter the extent of F-actin crosslinking by the introduction of oligomerized cofilin. At pH 6.5, F-actin severing by cofilin is weak, but cofilin bundles and crosslinks filaments. Given its effect of lowering the F-actin bending stiffness, cofilin- crosslinked networks are significantly more flexible and softer in bending than networks crosslinked by α-actinin. Thus, upon local activation of myosin-induced contractile stress, the network bends out-of-plane in contrast to the in-plane compression as observed with networks crosslinked by α-actinin. Here, we demonstrate that local effects on filament mechanics by cofilin introduces novel large-scale network material properties that enable the sculpting of complex shapes in the cell cytoskeleton. |
| first_indexed | 2024-03-08T11:26:24Z |
| format | Article |
| id | doaj.art-07517b2f4f854a6bb922ac8321294967 |
| institution | Directory Open Access Journal |
| issn | 0171-9335 |
| language | English |
| last_indexed | 2024-03-08T11:26:24Z |
| publishDate | 2024-03-01 |
| publisher | Elsevier |
| record_format | Article |
| series | European Journal of Cell Biology |
| spelling | doaj.art-07517b2f4f854a6bb922ac83212949672024-01-26T05:31:36ZengElsevierEuropean Journal of Cell Biology0171-93352024-03-011031151379Cofilin-mediated actin filament network flexibility facilitates 2D to 3D actomyosin shape changeZachary Gao Sun0Vikrant Yadav1Sorosh Amiri2Wenxiang Cao3Enrique M. De La Cruz4Michael Murrell5Systems Biology Institute, Yale University, West Haven, CT 06516, USA; Department of Physics, Yale University, 217 Prospect Street, New Haven, CT 06511, USA; Integrated Graduate Program in Physical and Engineering Biology, Yale University, New Haven, CT 06520, USASystems Biology Institute, Yale University, West Haven, CT 06516, USA; Department of Biomedical Engineering, Yale University, New Haven, CT 06511, USASystems Biology Institute, Yale University, West Haven, CT 06516, USA; Department of Mechanical Engineering and Material Science, Yale University, New Haven, CT 06511, USADepartment of Molecular Biology & Biophysics, Yale University, New Haven, CT 06511, USADepartment of Molecular Biology & Biophysics, Yale University, New Haven, CT 06511, USASystems Biology Institute, Yale University, West Haven, CT 06516, USA; Department of Biomedical Engineering, Yale University, New Haven, CT 06511, USA; Department of Physics, Yale University, 217 Prospect Street, New Haven, CT 06511, USA; Integrated Graduate Program in Physical and Engineering Biology, Yale University, New Haven, CT 06520, USA; Corresponding author at: Systems Biology Institute, Yale University, West Haven, CT 06516, USA.The organization of actin filaments (F-actin) into crosslinked networks determines the transmission of mechanical stresses within the cytoskeleton and subsequent changes in cell and tissue shape. Principally mediated by proteins such as α-actinin, F-actin crosslinking increases both network connectivity and rigidity, thereby facilitating stress transmission at low crosslinking yet attenuating transmission at high crosslinker concentration. Here, we engineer a two-dimensional model of the actomyosin cytoskeleton, in which myosin-induced mechanical stresses are controlled by light. We alter the extent of F-actin crosslinking by the introduction of oligomerized cofilin. At pH 6.5, F-actin severing by cofilin is weak, but cofilin bundles and crosslinks filaments. Given its effect of lowering the F-actin bending stiffness, cofilin- crosslinked networks are significantly more flexible and softer in bending than networks crosslinked by α-actinin. Thus, upon local activation of myosin-induced contractile stress, the network bends out-of-plane in contrast to the in-plane compression as observed with networks crosslinked by α-actinin. Here, we demonstrate that local effects on filament mechanics by cofilin introduces novel large-scale network material properties that enable the sculpting of complex shapes in the cell cytoskeleton.http://www.sciencedirect.com/science/article/pii/S0171933523000948CytoskeletonActinCofilinα-actininCrosslinkersActive Matter |
| spellingShingle | Zachary Gao Sun Vikrant Yadav Sorosh Amiri Wenxiang Cao Enrique M. De La Cruz Michael Murrell Cofilin-mediated actin filament network flexibility facilitates 2D to 3D actomyosin shape change European Journal of Cell Biology Cytoskeleton Actin Cofilin α-actinin Crosslinkers Active Matter |
| title | Cofilin-mediated actin filament network flexibility facilitates 2D to 3D actomyosin shape change |
| title_full | Cofilin-mediated actin filament network flexibility facilitates 2D to 3D actomyosin shape change |
| title_fullStr | Cofilin-mediated actin filament network flexibility facilitates 2D to 3D actomyosin shape change |
| title_full_unstemmed | Cofilin-mediated actin filament network flexibility facilitates 2D to 3D actomyosin shape change |
| title_short | Cofilin-mediated actin filament network flexibility facilitates 2D to 3D actomyosin shape change |
| title_sort | cofilin mediated actin filament network flexibility facilitates 2d to 3d actomyosin shape change |
| topic | Cytoskeleton Actin Cofilin α-actinin Crosslinkers Active Matter |
| url | http://www.sciencedirect.com/science/article/pii/S0171933523000948 |
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