Propagating waves separate two states of actin organization in living cells

Abstract

Propagating actin waves are dynamic supramolecular structures formed by the self-assembly of proteins within living cells. They are built from actin filaments together with single-headed myosin, the Arp23 complex, and coronin in a defined three-dimensional order. The function of these waves in structuring the cell cortex is studied on the substrate-attached surface of Dictyostelium cells by the use of total internal reflection fluorescence (TIRF) microscopy. Actin waves separate two areas of the cell cortex from each other, which are distinguished by the arrangement of actin filaments. The Arp23 complex dominates in the area enclosed by a wave, where it has the capacity of building dendritic structures, while the proteins prevailing in the external area, cortexillin I and myosin-II, bundle actin filaments and arrange them in antiparallel direction. Wave propagation is accompanied by transitions in the state of actin with a preferential period of 5 min. Wave generation is preceded by local fluctuations in actin assembly, some of the nuclei of polymerized actin emanating from clathrin-coated structures, others emerging independently. The dynamics of phase transitions has been analyzed to provide a basis for modeling the nonlinear interactions that produce spatio-temporal patterns in the actin system of living cells.

Dynamic Localization of the Actin-Bundling Protein Cortexillin I during Cell Migration

“…The negative effect of cortexillins on the translocation of the Arp2/3 complex to the cortex is consistent with the findings of studies of propagating F-actin waves at the bottom of the cell (Schroth-Diez et al, 2009). Actin waves are formed at the substrate-attached surface in migrating Dictyostelium cells, particularly on strongly adhesive substrates (Heinrich et al, 2008).…”

“…Actin waves separate two F-actin binding proteins, the Arp2/3 complex and cortexillins. The Arp2/3 complex is exclusively localized in the internal region of the F-actin waves, whereas cortexillins are localized at the external regions of the waves (Schroth-Diez et al, 2009). Taken together, our results suggest that cortexillins might play a role in restricting the Arp2/3 complex in the internal region of the F-actin waves.…”

The Mammalian Actin-Binding Protein 1 Is Critical for Spreading and Intraluminal Crawling of Neutrophils under Flow Conditions

“…2B, Supplemental Video 1). Such propagating waves have been described previously for actin and other actin-associated proteins such as myosin-IB, the Arp2/3 complex, and coronin in Dictyostelium, and for hematopoietic protein 1 (Hem-1) in dHL-60 cells (53)(54)(55)(56). Therefore, we studied whether mAbp1 may link the b 2 integrin function to the actin cytoskeleton.…”

Phase geometries of two-dimensional excitable waves govern self-organized morphodynamics of amoeboid cells

“…S2 B and C and Movie S1B). When these waves reach the border it promotes membrane extensions (16) (Fig. S1 C and D).…”

“…In both randomly moving Dictyostelium (12-15) and mammalian cells (7), transient local syntheses of PIP3 and F-actin propagate as waves at the substrate-attached cytosolic side of the membrane. Because the phosphatidylinositol wave induces a largescale protrusion when reaching the cell edge, it dictates timing and direction of large-scale membrane deformation (16). The localized patterns of signaling molecules and cytoskeleton that form the propagating waves resemble the phagocytic cup structure (17), and it has been proposed that the cells are scanning the glass surface for particle intake (18).…”