Calponin-homology domain mediated bending of membrane-associated actin filaments
Actin filaments are central to numerous biological processes in all domains of life. Driven by the interplay with molecular motors, actin binding and actin modulating proteins, the actin cytoskeleton exhibits a variety of geometries. This includes structures with a curved geometry such as axon-stabi...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-07-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/61078 |
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| author | Saravanan Palani Sayantika Ghosh Esther Ivorra-Molla Scott Clarke Andrejus Suchenko Mohan K Balasubramanian Darius Vasco Köster |
| author_facet | Saravanan Palani Sayantika Ghosh Esther Ivorra-Molla Scott Clarke Andrejus Suchenko Mohan K Balasubramanian Darius Vasco Köster |
| author_sort | Saravanan Palani |
| collection | DOAJ |
| description | Actin filaments are central to numerous biological processes in all domains of life. Driven by the interplay with molecular motors, actin binding and actin modulating proteins, the actin cytoskeleton exhibits a variety of geometries. This includes structures with a curved geometry such as axon-stabilizing actin rings, actin cages around mitochondria and the cytokinetic actomyosin ring, which are generally assumed to be formed by short linear filaments held together by actin cross-linkers. However, whether individual actin filaments in these structures could be curved and how they may assume a curved geometry remains unknown. Here, we show that ‘curly’, a region from the IQGAP family of proteins from three different organisms, comprising the actin-binding calponin-homology domain and a C-terminal unstructured domain, stabilizes individual actin filaments in a curved geometry when anchored to lipid membranes. Although F-actin is semi-flexible with a persistence length of ~10 μm, binding of mobile curly within lipid membranes generates actin filament arcs and full rings of high curvature with radii below 1 μm. Higher rates of fully formed actin rings are observed in the presence of the actin-binding coiled-coil protein tropomyosin and when actin is directly polymerized on lipid membranes decorated with curly. Strikingly, curly induced actin filament rings contract upon the addition of muscle myosin II filaments and expression of curly in mammalian cells leads to highly curved actin structures in the cytoskeleton. Taken together, our work identifies a new mechanism to generate highly curved actin filaments, which opens a range of possibilities to control actin filament geometries, that can be used, for example, in designing synthetic cytoskeletal structures. |
| first_indexed | 2024-12-10T04:10:44Z |
| format | Article |
| id | doaj.art-78426e233fe0474a809657362a0bda25 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-12-10T04:10:44Z |
| publishDate | 2021-07-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-78426e233fe0474a809657362a0bda252022-12-22T02:02:45ZengeLife Sciences Publications LtdeLife2050-084X2021-07-011010.7554/eLife.61078Calponin-homology domain mediated bending of membrane-associated actin filamentsSaravanan Palani0https://orcid.org/0000-0002-1893-6777Sayantika Ghosh1https://orcid.org/0000-0003-1399-1168Esther Ivorra-Molla2Scott Clarke3Andrejus Suchenko4Mohan K Balasubramanian5https://orcid.org/0000-0002-1292-8602Darius Vasco Köster6https://orcid.org/0000-0001-8530-5476Centre for Mechanochemical Cell Biology and Warwick Medical School, Division of Biomedical Sciences, Coventry, United Kingdom; Department of Biochemistry, Division of Biological Sciences, Indian Institute of Science, Bangalore, IndiaCentre for Mechanochemical Cell Biology and Warwick Medical School, Division of Biomedical Sciences, Coventry, United KingdomCentre for Mechanochemical Cell Biology and Warwick Medical School, Division of Biomedical Sciences, Coventry, United KingdomCentre for Mechanochemical Cell Biology and Warwick Medical School, Division of Biomedical Sciences, Coventry, United KingdomCentre for Mechanochemical Cell Biology and Warwick Medical School, Division of Biomedical Sciences, Coventry, United KingdomCentre for Mechanochemical Cell Biology and Warwick Medical School, Division of Biomedical Sciences, Coventry, United KingdomCentre for Mechanochemical Cell Biology and Warwick Medical School, Division of Biomedical Sciences, Coventry, United KingdomActin filaments are central to numerous biological processes in all domains of life. Driven by the interplay with molecular motors, actin binding and actin modulating proteins, the actin cytoskeleton exhibits a variety of geometries. This includes structures with a curved geometry such as axon-stabilizing actin rings, actin cages around mitochondria and the cytokinetic actomyosin ring, which are generally assumed to be formed by short linear filaments held together by actin cross-linkers. However, whether individual actin filaments in these structures could be curved and how they may assume a curved geometry remains unknown. Here, we show that ‘curly’, a region from the IQGAP family of proteins from three different organisms, comprising the actin-binding calponin-homology domain and a C-terminal unstructured domain, stabilizes individual actin filaments in a curved geometry when anchored to lipid membranes. Although F-actin is semi-flexible with a persistence length of ~10 μm, binding of mobile curly within lipid membranes generates actin filament arcs and full rings of high curvature with radii below 1 μm. Higher rates of fully formed actin rings are observed in the presence of the actin-binding coiled-coil protein tropomyosin and when actin is directly polymerized on lipid membranes decorated with curly. Strikingly, curly induced actin filament rings contract upon the addition of muscle myosin II filaments and expression of curly in mammalian cells leads to highly curved actin structures in the cytoskeleton. Taken together, our work identifies a new mechanism to generate highly curved actin filaments, which opens a range of possibilities to control actin filament geometries, that can be used, for example, in designing synthetic cytoskeletal structures.https://elifesciences.org/articles/61078actinIQGAPcytoskeletonin vitro |
| spellingShingle | Saravanan Palani Sayantika Ghosh Esther Ivorra-Molla Scott Clarke Andrejus Suchenko Mohan K Balasubramanian Darius Vasco Köster Calponin-homology domain mediated bending of membrane-associated actin filaments eLife actin IQGAP cytoskeleton in vitro |
| title | Calponin-homology domain mediated bending of membrane-associated actin filaments |
| title_full | Calponin-homology domain mediated bending of membrane-associated actin filaments |
| title_fullStr | Calponin-homology domain mediated bending of membrane-associated actin filaments |
| title_full_unstemmed | Calponin-homology domain mediated bending of membrane-associated actin filaments |
| title_short | Calponin-homology domain mediated bending of membrane-associated actin filaments |
| title_sort | calponin homology domain mediated bending of membrane associated actin filaments |
| topic | actin IQGAP cytoskeleton in vitro |
| url | https://elifesciences.org/articles/61078 |
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