Traveling waves in actin dynamics and cell motility - PubMed (original) (raw)

Review

Traveling waves in actin dynamics and cell motility

Jun Allard et al. Curr Opin Cell Biol. 2013 Feb.

Abstract

Much of current understanding of cell motility arose from studying steady treadmilling of actin arrays. Recently, there have been a growing number of observations of a more complex, non-steady, actin behavior, including self-organized waves. It is becoming clear that these waves result from activation and inhibition feedbacks in actin dynamics acting on different scales, but the exact molecular nature of these feedbacks and the respective roles of biomechanics and biochemistry are still unclear. Here, we review recent advances achieved in experimental and theoretical studies of actin waves and discuss mechanisms and physiological significance of wavy protrusions.

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Figures

Figure 1

Figure 1. Experimental observations of actin traveling waves

(A) Waves of YFP-Hem1 on the ventral surface of neutrophils (reproduced from [9] under the CCA License). Time is indicated by color as the wave spreads outward. (B) Rearward waves of alpha-actinin in fibroblasts shown in micrograph (left) and kymograph (right) (reproduced from [14] with permission). Scale bars 2 microns, 30 sec. (C) Wave of protrusion across the keratocyte’s leading edge (provided by E. Barnhart).

Figure 2

Figure 2. Major questions

(A) Mechanisms of waving: (i) T-waves arising from excitability require an initial trigger, typically above a threshold, to initiate a wave (a–b). Once one subcellular region is excited, neighboring regions must be coupled for the wave to propagate (b–c). Many cells exhibit transient wave pulses, after which the region returns to its initial state (c–d). This return is posited to arise because of the depletion of a promoter or replenishment of an inhibitor. (ii) Three possible spatial couplings. (a) Polymerization of actin with a lateral component could transports the excited state. (b) Diffusion of a regulator. (c) Transmission of stress to neighboring regions. The stress could be mediated by the membrane or actin(-myosin) gel. (B) Possible functional roles of waving. (i) Migration in the face of limited resources. Unable to protrude uniformly along the entire leading edge, cells may focus their protrusive machinery to a limited region. If this region is stationary (a), protrusion may result in fingering and translocation of the cell body will not occur. (An alternative is narrowing of the migrating cell.) If the protruding region moves randomly (b), cell coherence could be jeopardized. A sequence of traveling waves (c) results in smooth translocation of the cell body, without affecting cell width. (ii) Avoidance of obstacles. A uniformly protruding leading edge could become stuck upon encountering an obstacle (black circle) if the stalled region (red) has no effective means of communicating with nearby regions of the edge. Waves of protrusion may circumvent this problem since the direction of cell migration is defined locally.

Box figure

Box figure

Biochemical networks (top right) comprised of fast positive and slow negative feedbacks can exhibit qualitatively different behavior (time series, left) depending on parameters, on several timescales. Blue and red curves show behavior of molecular species A and B respectively. Steady state values of A marked by ss. Green arrows are external stimuli which instantaneously increases A and, if above a threshold (dashed lines), may relax to the only steady state, induce transient excitations in excitable systems, switch to a new steady state in bistable systems, or start fluctuating in oscillatory systems. In a region of space where each location exhibits the local dynamics shown on the left, as well as a spatial coupling to neighboring locations, spatiotemporal patterns of pulse wave, spatially uniform periodic oscillations, or wave of invasion emerge (kymographs, right).

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