Fascin-induced bundling protects actin filaments from disassembly by cofilin

Actin filament turnover plays a central role in shaping actin networks, yet the feedback mechanism between network architecture and filament assembly dynamics remains unclear. The activity of ADF/cofilin, the main protein family responsible for filament disassembly, has been mainly studied at the si...

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Bibliographic Details
Published in:The Journal of cell biology 2024-06, Vol.223 (6), p.1
Main Authors: Chikireddy, Jahnavi, Lengagne, Léana, Le Borgne, Rémi, Durieu, Catherine, Wioland, Hugo, Romet-Lemonne, Guillaume, Jégou, Antoine
Format: Article
Language:English
Subjects:
Actin
Actin Cytoskeleton
Actin Depolymerizing Factors
Actins
Animals
Biochemistry
Biophysics
Bundling
Carrier Proteins
Clusters
Cofilin
Crosslinking
Cytoskeleton
Dismantling
Filaments
Helicity
Humans
Life Sciences
Microfilament Proteins
Proteins
Regulatory proteins
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Summary:Actin filament turnover plays a central role in shaping actin networks, yet the feedback mechanism between network architecture and filament assembly dynamics remains unclear. The activity of ADF/cofilin, the main protein family responsible for filament disassembly, has been mainly studied at the single filament level. This study unveils that fascin, by crosslinking filaments into bundles, strongly slows down filament disassembly by cofilin. We show that this is due to a markedly slower initiation of the first cofilin clusters, which occurs up to 100-fold slower on large bundles compared with single filaments. In contrast, severing at cofilin cluster boundaries is unaffected by fascin bundling. After the formation of an initial cofilin cluster on a filament within a bundle, we observed the local removal of fascin. Notably, the formation of cofilin clusters on adjacent filaments is highly enhanced, locally. We propose that this interfilament cooperativity arises from the local propagation of the cofilin-induced change in helicity from one filament to the other filaments of the bundle. Overall, taking into account all the above reactions, we reveal that fascin crosslinking slows down the disassembly of actin filaments by cofilin. These findings highlight the important role played by crosslinkers in tuning actin network turnover by modulating the activity of other regulatory proteins.
ISSN:0021-9525
1540-8140
1540-8140
DOI:10.1083/jcb.202312106