Self-organizing actin waves as planar phagocytic cup structures

Abstract

Actin waves that travel on the planar membrane of a substrateattached cell underscore the capability of the actin system to assemble into dynamic structures by the recruitment of proteins from the cytoplasm. The waves have no fixed shape, can reverse their direction of propagation and can fuse or divide. Actin waves separate two phases of the plasma membrane that are distinguished by their lipid composition. The area circumscribed by a wave resembles in its phosphoinositide content the interior of a phagocytic cup, leading us to explore the possibility that actin waves are in-plane phagocytic structures generated without the localized stimulus of an attached particle. Consistent with this view, wave-forming cells were found to exhibit a high propensity for taking up particles. Cells fed rod-shaped particles produced elongated phagocytic cups that displayed a zonal pattern that reflected in detail the actin and lipid pattern of free-running actin waves. Neutrophils and macrophages are known to spread on surfaces decorated with immune complexes, a process that has been interpreted as "frustrated" phagocytosis. We suggest that actin waves enable a phagocyte to scan a surface for particles that might be engulfed.

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

“…1B). These results suggest that F-actin facilitates PIP3 wave nucleation in keeping with earlier observations that actin waves follow local PIP3 accumulation (17). A similar decrease in the nucleation rate was observed for cells treated mildly with PI3-kinase inhibitor LY294002 (Fig.…”

“…Thus, the relationship between complex morphology and geometry of excitability may be of relevance to a wide variety of cell types. Similarities between the PIP3/F-actin waves and the phagocytic cup structure have been noted previously (17). By making use of a mixture of randomness and order, cells may be effectively scanning the surrounding environment as they move and forage in the changing terrain.…”

“…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). Theoretical analysis has also shown that direction sensing could be biased by this spatiotemporal patterning (6,19).…”

Actin and PIP3 waves in giant cells reveal the inherent length scale of an excited state

“…Recent models of actin waves focus on the interactions of small GTPases with the machinery of actin polymerization, consistent with the finding that actin waves in Dictyostelium are coupled to patterns of PIP3 (Asano et al, 2008;Gerisch et al, 2009) and of Ras signaling (Gerisch et al, 2011) on the underlying membrane. In the model analyzed by Mata et al (Mata et al, 2013), the GTPase enhances its own activation by positive feedback, and is inactivated by negative feedback from F-actin.…”

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.…”