Formins specify membrane patterns generated by propagating actin waves

Ecke, Mary; Prassler, Jana; Tanribil, Patrick; Müller‐Taubenberger, Annette; Körber, Sarah; Faix, Jan; Gerisch, Günther

doi:10.1091/mbc.e19-08-0460

Cited by 18 publications

(20 citation statements)

References 56 publications

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“…This suggests that VASP generates at least part of the filaments from which Arp2/3 complex nucleates branches. In addition, formin B is localized to the actin waves 110 and may complement VASP in supplying the Arp2/3 complex with mother filaments.…”

Section: The Architecture Of the Actin Cytoskeletonmentioning

confidence: 99%

Three‐dimensional organization of the cytoskeleton: A cryo‐electron tomography perspective

2020

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Traditionally, structures of cytoskeletal components have been studied ex situ, that is, with biochemically purified materials. There are compelling reasons to develop approaches to study them in situ in their native functional context. In recent years, cryo-electron tomography emerged as a powerful method for visualizing the molecular organization of unperturbed cellular landscapes with the potential to attain near-atomic resolution. Here, we review recent works on the cytoskeleton using cryo-electron tomography, demonstrating the power of in situ studies. We also highlight the potential of this method in addressing important questions pertinent to the field of cytoskeletal biomechanics. K E Y W O R D S actin filaments, cryo-electron tomography, in situ architecture, intermediate filaments, microtubules Abbreviations: 3D, three-dimensional; ATP, adenosine triphosphate;

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Section: The Architecture Of the Actin Cytoskeletonmentioning

confidence: 99%

Three‐dimensional organization of the cytoskeleton: A cryo‐electron tomography perspective

2020

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“…Four of them have already been attributed specific cellular functions: ForG in macroendocytosis and ForA, ForE, and ForH in regulation of actin cell cortex mechanics (31), thus leaving ForB as the only remaining candidate. Although a previous study found no detectable null-mutant phenotype (41), more recent evidence suggests ForB to be involved in the propagation of actin waves (42), which resemble frustrated phagocytic cups, pointing towards a potential role of ForB in macroendocytosis.…”

Section: Resultsmentioning

confidence: 89%

“…Notably, the actin system of macrophages and Dictyostelium cells has the capacity to self-organize into waves that propagate on the planar, substrate-attached membrane of a cell (50). In a recent analysis of these actin waves, which resemble 2D-projections of frustrated phagocytic cups (3, 51, 52), active ForB showed a prominent localization to the transition area of the actin wave that is assumed to correspond to the tip of phagocytic cups, while it only weakly associated with the inner territory, which corresponds to the base of phagocytic cups and where active ForG was found (42). Thus, in accordance with the proposed homology between waves and phagocytic cups, ForB would have been expected to be localized more at the protrusive edge of phagocytic cups rather than the base.…”

Section: Discussionmentioning

confidence: 99%

Convergence of Ras- and Rac-regulated formin pathways is pivotal for phagosome formation and particle uptake in Dictyostelium

Körber¹,

Junemann²,

Litschko³

et al. 2022

Preprint

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Macroendocytosis comprising phagocytosis and macropinocytosis are actin-driven processes regulated by small GTPases that depend on the dynamic reorganization of the membrane that protrudes and internalizes extracellular material by cup-shaped structures. To effectively capture, enwrap, and internalize their targets, these cups are arranged into a peripheral ring or ruffle of protruding actin sheets emerging from an actin-rich, non-protrusive zone at its base. Despite extensive knowledge of the mechanism driving actin assembly of the branched network at the protrusive cup edge, which is initiated by the actin-related protein (Arp) 2/3 complex downstream of Rac signaling, our understanding of actin assembly in the base is still incomplete. In the Dictyostelium model system, the Ras-regulated formin ForG was previously shown to specifically contribute to actin assembly at the cup base. Loss of ForG is associated with a strongly impaired macroendocytosis and a 50% reduction of F-actin content at the base of phagocytic cups, in turn indicating the presence of additional factors that specifically contribute to actin formation at the base. Here, we show that ForG synergizes with the Rac-regulated formin ForB to form the bulk of linear filaments at the cup base. Consistently, combined loss of both formins virtually abolishes cup formation and leads to severe defects of macroendocytosis, emphasizing the relevance of converging Ras- and Rac-regulated formin pathways in assembly of linear filaments in the cup base, which apparently provide mechanical support to the entire structure. Remarkably, we finally show that active ForB, unlike ForG, additionally drives phagosome rocketing to aid particle internalization.

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“…Figure 7 shows that Arp2/3 is prevalent in the inner region while bundled filaments are dominant in the outer region, but the dichotomy may not be so clean. Recent work shows that formins, which nucleate and elongate actin filaments, are distributed throughout the inner and outer regions, but the type of formin varies, and the waves disappear when cells are treated with a formin inhibitor [ 83 ]. Figure 8 A shows that formin A is high outside the wave, reduced in the inner region, but high in the wave front and back.…”

Section: Intracellular Actin Waves In the Absence Of Directional Smentioning

confidence: 99%

“…Scale bar 10

m. ( B ) The spatial distribution of formin (green) and Arp2/3 (red) along the wavefront. From Ecke et al [ 83 ].…”

Section: Figurementioning

confidence: 99%

The Roles of Signaling in Cytoskeletal Changes, Random Movement, Direction-Sensing and Polarization of Eukaryotic Cells

Cheng

Félix

Othmer

2020

Cells

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Movement of cells and tissues is essential at various stages during the lifetime of an organism, including morphogenesis in early development, in the immune response to pathogens, and during wound-healing and tissue regeneration. Individual cells are able to move in a variety of microenvironments (MEs) (A glossary of the acronyms used herein is given at the end) by suitably adapting both their shape and how they transmit force to the ME, but how cells translate environmental signals into the forces that shape them and enable them to move is poorly understood. While many of the networks involved in signal detection, transduction and movement have been characterized, how intracellular signals control re-building of the cyctoskeleton to enable movement is not understood. In this review we discuss recent advances in our understanding of signal transduction networks related to direction-sensing and movement, and some of the problems that remain to be solved.

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Formins specify membrane patterns generated by propagating actin waves

Cited by 18 publications

References 56 publications

Three‐dimensional organization of the cytoskeleton: A cryo‐electron tomography perspective

Three‐dimensional organization of the cytoskeleton: A cryo‐electron tomography perspective

Convergence of Ras- and Rac-regulated formin pathways is pivotal for phagosome formation and particle uptake in Dictyostelium

The Roles of Signaling in Cytoskeletal Changes, Random Movement, Direction-Sensing and Polarization of Eukaryotic Cells

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