Actin Migration Driven by Directional Assembly and Disassembly of Membrane-Anchored Actin Filaments

Katsuno, Hiroko; Toriyama, Minoru; Hosokawa, Yoichiroh; Mizuno, Kensaku; Ikeda, Kazushi; Sakumura, Yuichi; Inagaki, Naoyuki

doi:10.1016/j.celrep.2015.06.048

Cited by 69 publications

(121 citation statements)

References 74 publications

(172 reference statements)

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“…Actin waves are physiological events generic for a large set of mammalian neurons, e.g., of hippocampal or cortical origin. They have been observed both in dissociated neurons in culture and within brain slices (Katsuno et al, 2015; Flynn et al, 2009). The role of these directional structures in neuronal growth and polarization was already underlined in the first descriptions of this phenomenon in the literature, about two decades ago (Ruthel and Banker, 1998).…”

Section: Introductionmentioning

confidence: 99%

“…Several in-depth studies published in recent years have however provided new insights into the role and characteristics of these propagative structures. First, actin waves seem to propagate using directional actin treadmilling that generates mechanical force (Katsuno et al, 2015). Actin polymerization and depolymerization is accompanied by the presence of several actin-associated proteins, such as Arp3, cofilin, or shootin within the actin wave (Flynn et al, 2009; Toriyama et al, 2006; Tilve et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

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Geometrical Determinants of Neuronal Actin Waves

Tomba

Braïni

Bugnicourt

et al. 2017

Front. Cell. Neurosci.

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Hippocampal neurons produce in their early stages of growth propagative, actin-rich dynamical structures called actin waves. The directional motion of actin waves from the soma to the tip of neuronal extensions has been associated with net forward growth, and ultimately with the specification of neurites into axon and dendrites. Here, geometrical cues are used to control actin wave dynamics by constraining neurons on adhesive stripes of various widths. A key observable, the average time between the production of consecutive actin waves, or mean inter-wave interval (IWI), was identified. It scales with the neurite width, and more precisely with the width of the proximal segment close to the soma. In addition, the IWI is independent of the total number of neurites. These two results suggest a mechanistic model of actin wave production, by which the material conveyed by actin waves is assembled in the soma until it reaches the threshold leading to the initiation and propagation of a new actin wave. Based on these observations, we formulate a predictive theoretical description of actin wave-driven neuronal growth and polarization, which consistently accounts for different sets of experiments.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Geometrical Determinants of Neuronal Actin Waves

Tomba

Braïni

Bugnicourt

et al. 2017

Front. Cell. Neurosci.

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show abstract

“…One striking example of unsteady protrusion is traveling waves at the leading edge. These traveling waves have been observed in diverse cell types [3,5–12] and represent a regular and relatively simple kind of unsteady protrusion event. Thus, elucidating the molecular and mechanical mechanisms that govern traveling wave generation may illuminate general mechanisms that regulate leading edge protrusion.…”

Section: Introductionmentioning

confidence: 99%

Adhesion-Dependent Wave Generation in Crawling Cells

et al. 2017

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Summary Dynamic actin networks are excitable. In migrating cells, feedback loops can amplify stochastic fluctuations in actin dynamics, often resulting in traveling waves of protrusion. The precise contributions of various molecular and mechanical interactions to wave generation have been difficult to disentangle, in part due to complex cellular morphodynamics. Here we use a relatively simple cell type – the fish epithelial keratocyte – to define a set of mechanochemical feedback loops underlying actin network excitability and wave generation. Although keratocytes are normally characterized by the persistent protrusion of a broad leading edge, increasing cell-substrate adhesion strength results in waving protrusion of a short leading edge. We show that protrusion waves are due to fluctuations in actin polymerization rates, and that overexpression of VASP, an actin anti-capping protein that promotes actin polymerization, switches highly-adherent keratocytes from waving to persistent protrusion. Moreover, VASP localizes both to adhesion complexes and the leading edge. Based on these results, we developed a mathematical model for protrusion waves in which local depletion of VASP from the leading edge by adhesions, along with lateral propagation of protrusion due to the branched architecture of the actin network, and negative mechanical feedback from the cell membrane, results in regular protrusion waves. Consistent with our model simulations, we show that VASP localization at the leading edge oscillates, with VASP leading edge enrichment greatest just prior to protrusion initiation. We propose that the mechanochemical feedbacks underlying wave generation in keratocytes may constitute a general module for establishing excitable actin dynamics in other cellular contexts.

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“…This chain attaches itself to the plasma membrane as it crawls, and totes various actin-binding proteins along with it. When the researchers halted the waves, the axon could not grow, indicating they waves are essential for neurons to reach out to other cells (4). Waves are also required to establish the polarity of neurons, with an axon on one side and dendrites on the other, without which they could not transmit signals throughout the brain.…”

Section: Mysterious Movementsmentioning

confidence: 99%

“…And new insights provide clues as to how actin moves in waves to transport itself and how it collects in patches to allow axon branching (4,5).…”

mentioning

confidence: 99%