Cell-scale dynamic recycling and cortical flow of the actin–myosin cytoskeleton for rapid cell migration

Yumura, Shigehiko; Itoh, Go; Kikuta, Yumi; Kikuchi, Tsuneaki; Kitanishi-Yumura, Toshiko; Tsujioka, Masatsune

doi:10.1242/bio.20122899

Cited by 36 publications

(45 citation statements)

References 64 publications

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“…Previously we used GFP‐ABD120K for the estimation of the turnover of actin filaments and proved that the turnover of GFP‐ABD120K reflects the turnover of actin filaments (Yumura et al . ). In the case of dividing dlpA null cells, the half‐time of fluorescence recovery was 0.88 ± 0.17 s ( n = 15), whereas it was 1.1 ± 0.23 s ( n = 18) in wild‐type cells (Fig.…”

Section: Resultsmentioning

confidence: 97%

Dynamin contributes to cytokinesis by stabilizing actin filaments in the contractile ring

et al. 2013

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Dynamin has been proposed to play an important role in cytokinesis, although the nature of its contribution has remained unclear. Dictyostelium discoideum has five dynamin-like proteins: DymA, DymB, DlpA, DlpB and DlpC. Cells mutant for dymA, dlpA or dlpB presented defects in cytokinesis that resulted in multinucleation when the cells were cultured in suspension. However, the cells could divide normally when attached to the substratum; this latter process depends on traction-mediated cytokinesis B. A dynamin GTPase inhibitor also blocked cytokinesis in suspension, suggesting an important role for dynamin in cytokinesis A, which requires a contractile ring powered by myosin II. Myosin II did not properly localize to the cleavage furrow in dynamin mutant cells, and the furrow shape was distorted. DymA and DlpA were associated with actin filaments at the furrow. Fluorescence recovery after photobleaching and a DNase I binding assay showed that actin filaments in the contractile ring were significantly fragmented in mutant cells. Dynamin is therefore involved in the stabilization of actin filaments in the furrow, which, in turn, maintain proper myosin II organization. We conclude that the lack of these dynamins disrupts proper actomyosin organization and thereby disables cytokinesis A.

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Section: Resultsmentioning

confidence: 97%

Dynamin contributes to cytokinesis by stabilizing actin filaments in the contractile ring

et al. 2013

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“…During inflammation, neutrophils extrude pseudopods (also called lamellipods) that are essential in crawling on the endothelium and eventually extravasating into the extracellular space. Pseudopods are organelle-less extensions that grow and retract due to the polymerization of actin filaments; once extruded, they remain stiff 7,11,33 . Four percent of leukocytes freshly-harvested from human whole blood exhibited pseudopod projections 6 .…”

Section: Introductionmentioning

confidence: 99%

Effect of Pseudopod Extensions on Neutrophil Hemodynamic Transport Near a Wall

2015

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During inflammation, circulating neutrophils roll on, and eventually tether to, the endothelial lining of blood vessels, allowing them to exit the bloodstream and enter the surrounding tissue to target pathogens. This process is mediated by the selectin family of adhesion proteins expressed by endothelial cells. Interestingly, only 10% of activated, migrating neutrophils transmigrate into the extravascular space; the other 90% detach from the wall and rejoin the blood flow. Neutrophils extrude pseudopods during the adhesion cascade; however, the transport behavior of this unique cell geometry has not been previously addressed. In this study, a three-dimensional computational model was applied to neutrophils with pseudopodial extensions to study the effect of cell shape on the hydrodynamic transport of neutrophils. The collision time, contact area, contact force, and collision frequency were analyzed as a function of pseudopod length. It was found that neutrophils experience more frequent collisions compared to prolate spheroids of equal volume and length. Longer pseudopods and lower shear rates increase the collision time integral contact area, a predictor of binding potential. Our results indicate that contact between the neutrophil and the vessel wall was found to be focused predominantly on the pseudopod tip.

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“…A number of myosin motors are also associated with the juxtamembranous actin cortex, of which nonmuscle myosin II is the major component in remodeling the cortex and creating actin flows (4,23,25,26,31,32). Based on our observations that Significance This manuscript addresses the role of active processes in the spatial organization and dynamics of cell surface components.…”

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confidence: 95%

“…The membrane models mentioned above have by-and-large neglected this active nature of the actin cortex where actin filaments are being continuously polymerized and depolymerized (18)(19)(20)(21), in addition to being persistently acted upon by a variety of myosin motors (22)(23)(24) that consume ATP and exert contractile stresses on cortical actin filaments, continually remodeling the architecture of the cortex (4,21,25). These active processes in turn can generate tangential stresses and currents on the cell surface, which could drive the dynamics and local composition of membrane components at different scales (22,(26)(27)(28)(29).…”

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Actomyosin dynamics drive local membrane component organization in an in vitro active composite layer

Köster

Husain

Iljazi

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

147

152

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The surface of a living cell provides a platform for receptor signaling, protein sorting, transport, and endocytosis, whose regulation requires the local control of membrane organization. Previous work has revealed a role for dynamic actomyosin in membrane protein and lipid organization, suggesting that the cell surface behaves as an active composite composed of a fluid bilayer and a thin film of active actomyosin. We reconstitute an analogous system in vitro that consists of a fluid lipid bilayer coupled via membrane-associated actinbinding proteins to dynamic actin filaments and myosin motors. Upon complete consumption of ATP, this system settles into distinct phases of actin organization, namely bundled filaments, linked apolar asters, and a lattice of polar asters. These depend on actin concentration, filament length, and actin/myosin ratio. During formation of the polar aster phase, advection of the self-organizing actomyosin network drives transient clustering of actin-associated membrane components. Regeneration of ATP supports a constitutively remodeling actomyosin state, which in turn drives active fluctuations of coupled membrane components, resembling those observed at the cell surface. In a multicomponent membrane bilayer, this remodeling actomyosin layer contributes to changes in the extent and dynamics of phasesegregating domains. These results show how local membrane composition can be driven by active processes arising from actomyosin, highlighting the fundamental basis of the active composite model of the cell surface, and indicate its relevance to the study of membrane organization.T he cell surface mediates interactions between the cell and the outside world by serving as the site for signal transduction. It also facilitates the uptake and release of cargo and supports adhesion to substrates. These diverse roles require that the cell surface components involved in each function are spatially and temporally organized into domains spanning a few nanometers (nanoclusters) to several micrometers (microdomains). The cell surface itself may be considered as a fluid-lipid bilayer wherein proteins are embedded (1). In the living cell, this multicomponent system is supported by an actin cortex, composed of a branched network of actin and a collection of filaments (2-4).Current models of membrane organization fall into three categories: those invoking lipid-lipid and lipid-protein interactions in the plasma membrane [e.g., the fluid mosaic model (1, 5) and the lipid raft hypothesis (6)], or those that appeal to the membrane-associated actin cortex (e.g., the picket fence model) (7), or a combination of these (8, 9). Although these models based on thermodynamic equilibrium principles have successfully explained the organization and dynamics of a range of membrane components and molecules, there is a growing class of phenomena that appears inconsistent with chemical and thermal equilibrium, which might warrant a different explanation. These include aspects of the organization and dynamics of outer leaflet...

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Cell-scale dynamic recycling and cortical flow of the actin–myosin cytoskeleton for rapid cell migration

Cited by 36 publications

References 64 publications

Dynamin contributes to cytokinesis by stabilizing actin filaments in the contractile ring

Dynamin contributes to cytokinesis by stabilizing actin filaments in the contractile ring

Effect of Pseudopod Extensions on Neutrophil Hemodynamic Transport Near a Wall

Actomyosin dynamics drive local membrane component organization in an in vitro active composite layer

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