Dynamic patterns of actin assembly in cell motility and chemotaxis

Günther Gerisch1, Till Bretschneider1, Annette Müller-Taubenberger1, Kurt Anderson2, and Stefan Diez2
1 Max-Planck-Institut für Biochemie, D-82152 Martinsried, Germany.
2 Max-Planck-Institut für molekulare Zellbiologie und Genetik, D-01307 Dresden, Germany.
Actin networks are continuously reorganized in cells that rapidly change their shape. Applying total internal reflection fluorescence (TIRF) microscopy at acquisition rates of 10 to 20 Hz, we measured an average growth rate of 3 μm x sec-1 for filamentous actin structures throughout the entire substrate-attached cortex of Dictyostelium cells. New filaments often proceed along pre-existing ones, resulting in bundle formation concurrent with filament growth. In cells that orientate in a gradient of chemoattractant, prominent actin assemblies enriched in the Arp2/3 complex are inserted into the network, primarily at the base of filopods that point into the direction of the gradient. The Arp2/3 complex promotes actin nucleation and branching of the filaments. This complex is inhibited by coronin, a WD40-repeat protein. Accordingly, coronin is recruited to a zone behind the leading edge or to other sites where actin assembly ceases. Arp2/3 and coronin are also involved in the formation of propagating actin waves. These are dynamic assemblies of polymerized actin that are formed on a planar area of the cell membrane remote from a leading edge. Our data reveal two types of dynamic patterns that are generated by the control systems of actin polymerization and depolymerization: a network of bundled actin filaments in the cell cortex and, superimposed on that network, patches and waves formed by the filament branching activity of the Arp2/3 complex. We propose that high turnover rates of actin filaments confer plasticity to the cell cortex that is required for fast changes in cell shape, and that autonomous activation of the Arp2/3 complex is a prerequisite for rapid accommodation to external stimuli.