Ezrin enrichment on curved membranes requires a specific conformation or interaction with a curvature-sensitive partner

Tsai, Feng-Ching; Bertin, Aurélie; Bousquet, Hugo; Manzi, John; Senju, Yosuke; Tsai, Meng Chen; Picas, Laura; Miserey-Lenkei, Stéphanie; Lappalainen, Pekka; Lemichez, Emmanuel; Coudrier, Evelyne; Bassereau, Patricia

doi:10.7554/elife.37262

Cited by 62 publications

(72 citation statements)

References 75 publications

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“…Membrane deformations, also referred to as membrane curvature, have been extensively studied in vitro in the context of several membrane binding/remodeling proteins [ 36 ], and the relationship between tension and curvature is well understood for these simplified systems [ 37 , 38 , 39 ]. Interestingly, MCA proteins such as Ezrin can change their membrane tethering abilities depending on interactions with actin and curvature-sensing binding partners [ 40 ]. Thus, it is plausible that differences in the curvature landscape of a cell could affect the propagation of membrane tension by influencing obstacle distribution and binding ( Figure 1 d).…”

Section: To Flow or Not To Flow?mentioning

confidence: 99%

Pay attention to membrane tension: Mechanobiology of the cell surface

Sitarska

Diz-Muñoz

2020

Current Opinion in Cell Biology

150

105

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The cell surface is a mechanobiological unit that encompasses the plasma membrane, its interacting proteins, and the complex underlying cytoskeleton. Recently, attention has been directed to the mechanics of the plasma membrane, and in particular membrane tension, which has been linked to diverse cellular processes such as cell migration and membrane trafficking. However, how tension across the plasma membrane is regulated and propagated is still not completely understood. Here, we review recent efforts to study the interplay between membrane tension and the cytoskeletal machinery and how they control cell form and function. We focus on factors that have been proposed to affect the propagation of membrane tension and as such could determine whether it can act as a global or local regulator of cell behavior. Finally, we discuss the limitations of the available tool kit as new approaches that reveal its dynamics in cells are needed to decipher how membrane tension regulates diverse cellular processes.

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Section: To Flow or Not To Flow?mentioning

confidence: 99%

Pay attention to membrane tension: Mechanobiology of the cell surface

Sitarska

Diz-Muñoz

2020

Current Opinion in Cell Biology

150

105

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“…This suggests that CHMP2B has some affinity for negative Gaussian curvature, but not for negative mean curvature, in contrast with in vivo overexpression conditions 29 . In order to test whether CHMP2B binds as well to positively curved membranes, we incorporated CHMP2B into GUVs and employed the I-BAR protein IRSp53 to form membrane tube invaginations on another set of GUVs 59,60 corresponding to the (iv) geometry ( Fig. 1D).…”

Section: Chmp2bmentioning

confidence: 99%

Human ESCRT-III Polymers Assemble on Positively Curved Membranes and Induce Helical Membrane Tube Formation

Bertin

Franceschi

Mora

et al. 2019

Preprint

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Endosomal sorting complexes required for transport-III (ESCRT-III) are thought to assemble in vivo inside membrane structures with a negative Gaussian curvature. How membrane shape influences ESCRT-III polymerization and conversely how ESCRT-III polymers shape membranes is still unclear. Here, we used human core ESCRT-III proteins, CHMP4B, CHMP2A, CHMP2B and CHMP3 to address this issue in vitro by combining membrane nanotube pulling experiments, cryo-electron microscopy, cryo-electron tomography and highspeed AFM. We show that CHMP4B filaments bind preferentially to flat membranes or to membrane tubes with a positive mean curvature. Both CHMP2B and CHMP2A/CHMP3 assemble on positively curved membrane tubes, the latter winding around the tubes. Although combinations of CHMP4B/CHMP2B and CHMP4B/CHMP2A/CHMP3 are recruited to the neck of pulled membrane tubes, they also reshape large unilamellar vesicles into helical membrane tubes with a pipe surface shape. Sub-tomogram averaging reveals that the filaments assemble parallel to the tube axis with some local perpendicular connections, highlighting the particular mechanical stresses imposed by ESCRT-III to stabilize the corkscrew-like membrane architecture. Our results thus underline the versatile membrane remodeling activity of ESCRT-III that may be a general feature of ESCRT-III required for all or selected cellular membrane remodeling processes.

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“…A role for tension in the formation of ZO-1 cytosolic complexes is also suggested by the observation that integrin stimulation is required for nanotopography-induced epithelia permeability ( 12, 13 ). We also found that ezrin, a cytosolic scaffold protein that links the actin cytoskeleton to cellular membrane receptors ( 24 ), was upregulated in NS-treated cells (fig. S6B).…”

Section: Discussionmentioning

confidence: 64%

Nanotopography enhances dynamic remodeling of tight junction proteins through cytosolic complexes

Huang

Shi

Hansen

et al. 2019

Preprint

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24The epithelial tight junction regulates barrier function and is responsive to extracellular stimuli. Here we 25 demonstrated that contact of synthetic surfaces with defined nanotopography at the apical surface of 26 epithelial monolayers increased paracellular permeability of macromolecules. To monitor changes in tight 27 junction morphology in live cells, we fluorescently tagged the scaffold protein zonula occludens-1 (ZO-28 1) through CRISPR/Cas9-based gene editing. Contact between cells and nanostructured surfaces 29 destabilized junction-associated ZO-1 and promoted its arrangement into highly dynamic non-junctional 30 cytosolic complexes that averaged ~2 µm in diameter. Junction-associated ZO-1 rapidly remodeled, and 31 we also observed the direct transformation of cytosolic complexes into junction-like structures. Claudin-32 family tight junction transmembrane proteins and F-actin also were associated with these ZO-1 containing 33 cytosolic complexes. These data suggest that the cytosolic structures are novel intermediates formed in 34 response to nanotopographic cues that facilitate rapid tight junction remodeling in order to regulate 35 paracellular permeability. 36 37 1B, fig. S1B). FITC-labeled IgG (FITC-IgG) was added to the apical side of the monolayer as a tracer for 87 barrier permeability (Fig. 1A, fig. S1A). We then tracked FITC-IgG that penetrated through epithelial 88 monolayers to the basal side with submicron resolution, using TIRF microscopy that selectively 89 illuminated fluorophores within ~100 nm zone above the basal substrate (Fig. 1A). Acquired TIRF images 90 were quantified as the mean FITC fluorescence intensity at cell-cell borders marked by bulk plasma 91 membrane using Cell Mask Deep Red (fig. S1C). Strikingly, FITC-IgG accumulated in basolateral gaps 92 below cell-cell borders of Caco-2 monolayer after apical contact with nanostructured (NS) films for 1 93 hour at 37 o C (Fig. 1, C and D), while FITC-IgG showed minimal paracellular permeability in non-treated 94 (NT) cells ( fig. S1 D and E). NS film treated cells also showed significantly higher paracellular 95 accumulation of FITC-IgG than cells in contact with control flat (FT) polypropylene films (Fig. 1C-E). 96 These data are consistent with our previous studies, which demonstrate increased paracellular permeability 97 to macromolecules when epithelial cells are in contact with nanotopographic structures (12-14), further 98 indicating the regulation of tight junctions through nanostructure contact. We then immunostained ZO-1 99 in differentially treated cells (fig. S1F) given its important role in tight junction regulation (5-9). We found 100 NS-specific effects on ZO-1 morphology, including induction of a zigzag appearance in the xy focal plane 101 ( Fig.

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Ezrin enrichment on curved membranes requires a specific conformation or interaction with a curvature-sensitive partner

Cited by 62 publications

References 75 publications

Pay attention to membrane tension: Mechanobiology of the cell surface

Pay attention to membrane tension: Mechanobiology of the cell surface

Human ESCRT-III Polymers Assemble on Positively Curved Membranes and Induce Helical Membrane Tube Formation

Nanotopography enhances dynamic remodeling of tight junction proteins through cytosolic complexes

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