Architecture dependence of actin filament network disassembly.
Turnover of actin networks in cells requires the fast disassembly of aging actin structures. While ADF/cofilin and Aip1 have been identified as central players, how their activities are modulated by the architecture of the networks remains unknown. Using our ability to reconstitute a diverse array of cellular actin organizations, we found that ADF/cofilin binding and ADF/cofilin-mediated disassembly both depend on actin geometrical organization. ADF/cofilin decorates strongly and stabilizes actin cables, whereas its weaker interaction to Arp2/3 complex networks is correlated with their dismantling and their reorganization into stable architectures. Cooperation of ADF/cofilin with Aip1 is necessary to trigger the full disassembly of all actin filament networks. Additional experiments performed at the single-molecule level indicate that this cooperation is optimal above a threshold of 23 molecules of ADF/cofilin bound as clusters along an actin filament. Our results indicate that although ADF/cofilin is able to dismantle selectively branched networks through severing and debranching, stochastic disassembly of actin filaments by ADF/cofilin and Aip1 represents an efficient alternative pathway for the full disassembly of all actin networks. Our data support a model in which the binding of ADF/cofilin is required to trigger a structural change of the actin filaments, as a prerequisite for their disassembly by Aip1.
Physics of the Cytoskeleton and Morphogenesis Group, Institut de Recherches en Technologies et Sciences pour le Vivant, Laboratoire de Physiologie Cellulaire et Végétale, CNRS/CEA/INRA/UJF, Grenoble 38054, France.
Laurène
L
Gressin
Physics of the Cytoskeleton and Morphogenesis Group, Institut de Recherches en Technologies et Sciences pour le Vivant, Laboratoire de Physiologie Cellulaire et Végétale, CNRS/CEA/INRA/UJF, Grenoble 38054, France.
Audrey
A
Guillotin
Physics of the Cytoskeleton and Morphogenesis Group, Institut de Recherches en Technologies et Sciences pour le Vivant, Laboratoire de Physiologie Cellulaire et Végétale, CNRS/CEA/INRA/UJF, Grenoble 38054, France.
Christophe
C
Guérin
Physics of the Cytoskeleton and Morphogenesis Group, Institut de Recherches en Technologies et Sciences pour le Vivant, Laboratoire de Physiologie Cellulaire et Végétale, CNRS/CEA/INRA/UJF, Grenoble 38054, France. Electronic address: laurent.blanchoin@cea.fr.
Laurent
L
Blanchoin
Physics of the Cytoskeleton and Morphogenesis Group, Institut de Recherches en Technologies et Sciences pour le Vivant, Laboratoire de Physiologie Cellulaire et Végétale, CNRS/CEA/INRA/UJF, Grenoble 38054, France. Electronic address: alphee.michelot@cea.fr.
Alphée
A
Michelot
D008841:Actin Cytoskeleton / Q000378:metabolism*; D051339:Actin Depolymerizing Factors / Q000378:metabolism*; D000199:Actins / Q000378:metabolism*; D000818:Animals; D008840:Microfilament Proteins / Q000378:metabolism*; D011817:Rabbits; D015003:Yeasts
D051339:Actin Depolymerizing Factors; D000199:Actins; D008840:Microfilament Proteins; C115237:actin interacting protein 1