Control of actin polymerization via the coincidence of phosphoinositides and high membrane curvature

Daste, Frédéric; Walrant, Astrid; Holst, Mikkel R.; Gadsby, Jonathan R; Mason, Julia; Lee, Jieun; Brook, D. F.; Mettlen, Marcel; Larsson, Elin; Lee, Steven Frank; Lundmark, Richard; Gallop, Jennifer L.

doi:10.1083/jcb.201704061

Cited by 84 publications

(98 citation statements)

References 56 publications

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“…However, on a smaller (sub-micron) length scale, branched actin networks deform many cellular membranes as part of organelle and vesicle biogenesis and function (Rottner et al, 2017) . The relationship between cellular membrane curvature and local actin assembly for each of these "local" membrane-deformation processes remains relatively unexplored (Daste et al, 2017) .…”

Section: Introduction (890 Words)mentioning

confidence: 99%

Principles of self-organization and load adaptation by the actin cytoskeleton during clathrin-mediated endocytosis

Akamatsu

Vasan

Serwas

et al. 2019

Preprint

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words)Force generation due to actin assembly is a fundamental aspect of membrane sculpting for many essential processes. In this work, we use a multiscale computational model constrained by experimental measurements to show that a minimal branched actin network is sufficient to internalize endocytic pits against physiological membrane tension. A parameter sweep identified the number of Arp2/3 complexes as particularly important for robust internalization, which prompted the development of a molecule-counting method in live mammalian cells. Using this method, we found that ~200 Arp2/3 complexes assemble at sites of clathrin-mediated endocytosis in human cells. Our simulations also revealed that actin networks self-organize in a radial branched array with barbed filament ends oriented to grow toward the base of the pit, and that the distribution of linker proteins around the endocytic pit is critical for this organization. Surprisingly, our model predicted that long actin filaments bend from their attachment sites in the coat to the base of the pit and store elastic energy that can be harnessed to drive endocytosis. This prediction was validated using cryo-electron tomography on cells, which revealed the presence of bent actin filaments along the endocytic site. Furthermore, we predict that under elevated membrane tension, the self-organized actin network directs more growing filaments toward the base of the pit, increasing actin nucleation and bending for increased force production. Thus, our study reveals that spatially constrained actin filament assembly utilizes an adaptive mechanism that enables endocytosis under varying physical constraints.

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Section: Introduction (890 Words)mentioning

confidence: 99%

Principles of self-organization and load adaptation by the actin cytoskeleton during clathrin-mediated endocytosis

Akamatsu

Vasan

Serwas

et al. 2019

Preprint

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“…In a recent study, Mettlen et al showed that membrane curvature induced by using liposomes with various sizes, combined with PI(4,5)P 2 , and PI(3)P signalling are needed to trigger actin polarization. 52 Some actin assemblies induced by membrane curvature on the sparse arrays (see Supplementary MovieS15) resembles actin comets induced in a cell-free assay for the role of phosphoinositide in actin polymerization. 52 The role of nanopillar surface chemistry also remains to be investigated.…”

Section: Discussionmentioning

confidence: 96%

“…52 Some actin assemblies induced by membrane curvature on the sparse arrays (see Supplementary MovieS15) resembles actin comets induced in a cell-free assay for the role of phosphoinositide in actin polymerization. 52 The role of nanopillar surface chemistry also remains to be investigated. Although geometry was attributed the leading role in reduced neuronal migration on nanopillars (Si, SiO 2 and Pt were tested), 26 it cannot be ruled out that the surface chemistry of SU-8 could play a role in the strong membrane interactions observed, and should be investigated further.…”

Section: Discussionmentioning

confidence: 96%

Influence of nanopillar arrays on fibroblast motility, adhesion and migration mechanisms

Beckwith

Ullmann

Vinje

et al. 2019

Preprint

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Surfaces decorated with high aspect ratio nanostructures are a promising tool to study cellular processes and design novel devices to control cellular behaviour, perform intracellular sensing or deliver effector molecules to cells in culture. However, little is known about the dynamics of cellular phenomenon such as adhesion, spreading and migration on such surfaces. In particular, how these are influenced by the surface properties. In this work, we investigate fibroblast behaviour on regular arrays of 1 micrometer high, polymer nanopillars with varying pillar to pillar distance (array pitch).NIH-3T3 fibroblasts spread on all arrays, and on contact with the substrate engulf nanopillars independently of the array pitch. As the cells start to spread, different behaviour is observed. On dense arrays which have the pitch equal or below 1 micrometer, cells are suspended on top of the nanopillars, making only sporadic contact with the glass support. Cells stay attached to the glass support and fully engulf nanopillars during spreading and migration on the sparse arrays which are characterized by a pitch of 2 micrometers and above. These alternate states have a profound effect on cell migration rates, which are strongly reduced on nanopillar sparse arrays. Dynamic actin puncta colocalize with nanopillars during cell spreading and migration. Strong membrane association with engulfed nanopillars might explain the reduced migration rates on sparse arrays. This work reveals several interesting phenomenon of dynamical cell behaviour on nanopillar arrays, and provides important perspectives on design and applications of high aspect ratio nanostructures.

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“…Likewise, CIP4, Fer, and PSTPIP display increased binding affinity to PI(4,5) P 2 , [64] while several BAR proteins involved in fast endophilinmediated endocytosis require PI(3,4)P2. [66,67] Curiously, in some cases, the electrostatic interplay between proteins and lipids is so strong that even phosphoinositide clustering was observed upon protein binding. [66,67] Curiously, in some cases, the electrostatic interplay between proteins and lipids is so strong that even phosphoinositide clustering was observed upon protein binding.…”

Section: Electrostatic Protein-lipid Interactionsmentioning

confidence: 99%

Receptor‐Free Signaling at Curved Cellular Membranes

Ebrahimkutty

Galic

2019

BioEssays

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Plasma membranes are subject to continuous deformations. Strikingly, some of these transient membrane undulations yield membrane-associated signaling hubs that differ in composition and function, depending on membrane geometry and the availability of co-factors. Here, recent advancements on this ubiquitous type of receptor-independent signaling are reviewed, with a special focus on emerging concepts and technical challenges associated with studying these elusive signaling sites.

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Control of actin polymerization via the coincidence of phosphoinositides and high membrane curvature

Cited by 84 publications

References 56 publications

Principles of self-organization and load adaptation by the actin cytoskeleton during clathrin-mediated endocytosis

Principles of self-organization and load adaptation by the actin cytoskeleton during clathrin-mediated endocytosis

Influence of nanopillar arrays on fibroblast motility, adhesion and migration mechanisms

Receptor‐Free Signaling at Curved Cellular Membranes

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