Gelsolin is a six domain protein (82 kDa) which regulates actin assembly by severing, capping, and nucleating filaments. We have performed electron cryomicroscopy of F-actin decorated with G2-6, a gelsolin deletion mutant which lacks the high affinity monomer binding domain that is required for efficient severing. Electron cryomicrographs of F-actin decorated with G2-6 in calcium, but not in EGTA, a condition that exhibits normal severing activity, show dramatic distortions of filaments which appear to correlate with severing activity. A three-dimensional reconstruction of G2-6:F-actin was obtained under conditions which permit severing, but at a lower efficiency. The structure shows that gelsolin bridges two longitudinally-associated monomers when it binds the filament. The F-actin binding site is centered axially at subdomain 3 and radially between subdomains 1 and 3 of the upper actin monomer. Both the distorted appearance of the decorated filaments and the location of the G2-6 density suggest that in order for domain G4 to bind actin and sever the filament, both gelsolin and actin undergo large conformational changes.
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