Curving Cells Inside and Out: Roles of BAR Domain Proteins in Membrane Shaping and Its Cellular Implications

Šimunović, Mijo; Evergren, Emma; Callan-Jones, Andrew; Bassereau, Patricia

doi:10.1146/annurev-cellbio-100617-060558

Cited by 121 publications

(126 citation statements)

References 116 publications

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“…Membrane remodeling in living organisms is implicated in a large number of cellular processes and controls various key cellular functions . Two main mechanisms of membrane remodeling are amphipathic helix insertion and scaffolding . Amphipathic helices are thought to deform the membrane by a wedging mechanism whereby hydrophobic residue insertion into the membrane provides an asymmetric stress to the membrane bilayer, leading to its deformation .…”

Section: Introductionmentioning

confidence: 99%

Mechanisms of negative membrane curvature sensing and generation by ESCRT III subunit Snf7

2020

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Certain proteins have the propensity to bind to negatively curved membranes and generate negative membrane curvature. The mechanism of action of these proteins is much less studied and understood than those that sense and generate positive curvature. In this work, we use implicit membrane modeling to explore the mechanism of an important negative curvature sensing and generating protein: the main ESCRT III subunit Snf7. We find that Snf7 monomers alone can sense negative curvature and that curvature sensitivity increases for dimers and trimers. We have observed spontaneous bending of Snf7 oligomers into circular structures with preferred radius of~20 nm. The preferred curvature of Snf7 filaments is further confirmed by the simulations of preformed spirals on a cylindrical membrane surface. Snf7 filaments cannot bind with the same interface to flat and curved membranes. We find that even when a filament has the preferred radius, it is always less stable on the flat membrane surface than on the interior cylindrical membrane surface. This provides an additional energy for membrane bending which has not been considered in the spiral spring model. Furthermore, the rings on the cylindrical spirals are bridged together by helix 4 and hence are extra stabilized compared to the spirals on the flat membrane surface. K E Y W O R D Scomputer simulation, ESCRT III, lipid bilayer, membrane curvature sensing and generation, Snf7

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Section: Introductionmentioning

confidence: 99%

Mechanisms of negative membrane curvature sensing and generation by ESCRT III subunit Snf7

2020

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“…The Bin/Amphiphysin/Rvs (BAR) domain superfamily regulates membrane shape in a range of cellular processes ranging from endocytosis to filopodia formation. (1)(2)(3)(4) Across the superfamily, full-length BAR proteins may have actin-binding domains, specific lipid targeting domains, or terminal amphipathic helices that are key to the proper function and localization of BAR proteins. (5) Notably, BAR domains share a consistent dimeric structure of bundled, kinked helices, and net positive charge.…”

Section: Introductionmentioning

confidence: 99%

Membrane-mediated forces can stabilize tubular assemblies of I-Bar proteins

Jarin

Pak

Bassereau

et al. 2020

Preprint

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Collective action by Inverse-BAR (I-BAR) domains drive micron-scale membrane remodeling. The macroscopic curvature sensing and generation behavior of I-BAR domains is well characterized, and computational models have suggested various mechanisms on simplified membrane systems, but there remain missing connections between the complex environment of the cell and the models proposed thus far. Here, we show a connection between the role of protein curvature and lipid clustering in the stabilization of large membrane deformations. We find lipid clustering provides a directional membrane-mediated interaction between membrane-bound I-BAR domains. Lipid clusters stabilize I-BAR domain aggregates that would not arise through membrane fluctuation-based or curvature-based interactions. Inside of membrane protrusions, lipid cluster-mediated interaction draws long side-by-side aggregates together resulting in more cylindrical protrusions as opposed to bulbous, irregularly shaped protrusions. Statement of SignificanceMembrane remodeling occurs throughout the cell and is crucial to proper cellular function. In the cellular environment, I-BAR proteins are responsible for sensing membrane curvature and initiating the formation of protrusions outward from the cell. Additionally, there is a large body of evidence that I-BAR domains are sufficient to reshape the membrane on scales much larger than any single domain. The mechanism by which I-BAR domains can remodel the membrane is uncertain. However, experiments show that membrane composition and most notably negativelycharge lipids like PIP2 play a role in the onset of tubulation. Using coarse-grained models, we show that I-BAR domains can cluster negatively charge lipids and clustered PIP2-like membrane structures facilitate a directional membrane-mediated interaction between I-BAR domains.

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“…At the larger membrane coverages x blue = 0.04 of convex particles in the morphologies 4 to 7 of Fig. 4, a tubular protrusion is formed at one end of the closed membrane by bound concave particles, while the remaining membrane is covered by lines of convex and concave 13,12,14,9,14,13,15,11,13,11,10,12,10,11, and 12 k B T . The overall number of bound and unbound concave particles is 392, 392, 392, 380, 380, 380, 380, 360, 360, 320, 320, 320, 240, 240, and 240 in these simulations.…”

Section: Particles With Arc Angles Of 90 • and Morementioning

confidence: 93%

“…The membrane and particles are enclosed in a cubic simulation box of volume V box 1.26 · 10 5 a 3 m . To verify convergence, we divide the last 10 7 MC steps per vertex of a simulation into ten intervals of 10 6 steps and calculate the reduced volume v of the The morphologies result from simulations with an initially spherical membrane and the adhesion energy per particle segment U = 10, 13,11,10,13,12,12,9,10,12,11,13,10,11,13,12, and 11 k B T . The overall number of bound and unbound concave particles is 392, 392, 380, 360, 360, 360, 320, 240, 240, 240, 240, 240, 160, 160, 160, 160, and 80 in these simulations.…”

Section: Simulationsmentioning

confidence: 99%

Membrane morphologies induced by mixtures of arc-shaped particles with opposite curvature

2021

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Biological membranes are shaped by various proteins that either generate inward or outward membrane curvature. In this article, we investigate the membrane morphologies induced by mixtures of arc-shaped particles with coarse-grained modeling and simulations. The particles bind to the membranes either with their inward, concave side or their outward, convex side and, thus, generate membrane curvature of opposite sign. We find that small fractions of convex-binding particles can stabilize three-way junctions of membrane tubules, as suggested for the protein lunapark in the endoplasmic reticulum of cells. For comparable fractions of concave-binding and convex-binding particles, we observe lines of particles of the same type, and diverse membrane morphologies with grooves and bulges induced by these particle lines. The alignment and segregation of the particles is driven by indirect, membrane-mediated interactions.

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Curving Cells Inside and Out: Roles of BAR Domain Proteins in Membrane Shaping and Its Cellular Implications

Cited by 121 publications

References 116 publications

Mechanisms of negative membrane curvature sensing and generation by ESCRT III subunit Snf7

Mechanisms of negative membrane curvature sensing and generation by ESCRT III subunit Snf7

Membrane-mediated forces can stabilize tubular assemblies of I-Bar proteins

Membrane morphologies induced by mixtures of arc-shaped particles with opposite curvature

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