Membrane tension controls the assembly of curvature-generating proteins

Šimunović, Mijo; Voth, Gregory A.

doi:10.1038/ncomms8219

Cited by 145 publications

(170 citation statements)

References 67 publications

(96 reference statements)

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“…Molecular dynamics simulations support the findings of Baumgart and coworkers (58) showing that a membrane tension in the range of 0.2 mN/m and larger increases the free energy barrier for the formation of tubules from a planar membrane and inhibits polymerization of N-BAR domains (59). Our results as well as those of others are also in line with the notion that exo-and endocytic pathways are regulated by lateral membrane tension in vivo.…”

Section: ϫ4supporting

confidence: 92%

Epsin N-terminal Homology Domain (ENTH) Activity as a Function of Membrane Tension

Gleisner

Kroppen

Fricke

et al. 2016

Journal of Biological Chemistry

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The epsin N-terminal homology domain (ENTH) is a major player in clathrin-mediated endocytosis. To investigate the influence of initial membrane tension on ENTH binding and activity, we established a bilayer system based on adhered giant unilamellar vesicles (GUVs) to be able to control and adjust the membrane tension covering a broad regime. The shape of each individual adhered GUV as well as its adhesion area was monitored by spinning disc confocal laser microscopy. Control of in a range of 0.08-1.02 mN/m was achieved by altering the Mg 2؉ concentration in solution, which changes the surface adhesion energy per unit area of the GUVs. Specific binding of ENTH to phosphatidylinositol 4,5-bisphosphate leads to a substantial increase in adhesion area of the sessile GUV. At low tension (<0.1 mN/m) binding of ENTH can induce tubular structures, whereas at higher membrane tension the ENTH interaction deflates the sessile GUV and thereby increases the adhesion area. The increase in adhesion area is mainly attributed to a decrease in the area compressibility modulus K A . We propose that the insertion of the ENTH helix-0 into the membrane is largely responsible for the observed decrease in K A , which is supported by the observation that the mutant ENTH L6E shows a reduced increase in adhesion area. These results demonstrate that even in the absence of tubule formation, the area compressibility modulus and, as such, the bending rigidity of the membrane is considerably reduced upon ENTH binding. This renders membrane bending and tubule formation energetically less costly.Clathrin-mediated endocytosis is one of the key metabolic pathways for the uptake of macromolecules into eukaryotic cells (1-4). Driven by a chain of remodeling events and an elaborate set of proteins acting in an orchestrated manner, an almost flat patch of plasma membrane is transformed into a closed, cargo-containing vesicle. As plasma membrane shape transformation is associated with significant local bending of the membrane, the process is highly sensitive to lateral membrane tension. Plasma membrane tension originates from two primary sources; that is, hydrostatic pressure across the lipid bilayer and cytoskeleton-membrane adhesion (5). Depending on the cell type, plasma membrane tensions span a range of roughly 0.003-0.45 mN/m (5-8). Even though it had become clear already in the late 1990s that tension plays a role in exoand endocytosis (9, 10), only in recent years has significant evidence been accumulated that membrane tension is of utmost importance for processes that rely on membrane remodeling (11-14). Cells actively maintain and regulate their membrane tension and use it to control exo-and endocytosis (15). In K562 cells it has been reported that endocytosis is completely suppressed under hypoosmotic conditions (16). Generally, high lateral membrane tension suppresses membrane deformation as both stretching the lipid bilayer and opening bonds between the cytoskeleton and the plasma membrane requires a large amount of energy (17).One protein...

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Section: ϫ4supporting

confidence: 92%

Epsin N-terminal Homology Domain (ENTH) Activity as a Function of Membrane Tension

Gleisner

Kroppen

Fricke

et al. 2016

Journal of Biological Chemistry

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“…The protein assembly produces polygonal membrane tubes and polyhedral vesicles at a high protein density [58]. A positive surface tension destabilizes the rod assembly [59] and tubulation [54] whereas it stabilizes the striped structure formed by the two types of rods [46].…”

Section: Introductionmentioning

confidence: 99%

Acceleration and suppression of banana-shaped-protein-induced tubulation by addition of small membrane inclusions of isotropic spontaneous curvatures

Noguchi

2017

Soft Matter

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The membrane tubulation induced by banana-shaped protein rods is investigated by using coarsegrained meshless membrane simulations. It is found that the tubulation is promoted by laterally isotropic membrane inclusions that generate the same sign of spontaneous curvature as the adsorbed protein rods. The inclusions are concentrated in the tubules and reduce the bending energy of the tip of the tubules. On the other hand, the inclusions with an opposite curvature suppress the tubulation by percolated-network formation at a high protein-rod density while they induce a spherical membrane bud at a low rod density. When equal amounts of the two types of inclusions (with positive and negative curvatures) are added, their effects cancel each other for the first short period but later the tubulation is slowly accelerated. A positive surface tension suppresses the tubulation. Out results suggest that the cooperation of scaffolding of BAR (Bin/Amphiphysin/Rvs) domains and isotropic membrane inclusions is important for the tubulation.

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“…Atomic and coarse-grained molecular simulations [40][41][42][43][44][45] have been employed to investigate molecular-scale interactions between BAR proteins and lipids. The scaffold formation [43] and linear assembly [44] of BAR domains have been demonstrated.…”

Section: Introductionmentioning

confidence: 99%

Shape deformation of lipid membranes by banana-shaped protein rods: Comparison with isotropic inclusions and membrane rupture

Noguchi

2016

Phys. Rev. E

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The assembly of curved protein rods on fluid membranes is studied using implicit-solvent meshless membrane simulations. As the rod curvature increases, the rods on a membrane tube assemble along the azimuthal direction first and subsequently along the longitudinal direction. Here, we show that both transition curvatures decrease with increasing rod stiffness. For comparison, curvature-inducing isotropic inclusions are also simulated. When the isotropic inclusions have the same bending rigidity as the other membrane regions, the inclusions are uniformly distributed on the membrane tubes and vesicles even for large spontaneous curvature of the inclusions. However, the isotropic inclusions with much larger bending rigidity induce shape deformation and are concentrated on the region of a preferred curvature. For high rod density, high rod stiffness, and/or low line tension of the membrane edge, the rod assembly induces vesicle rupture, resulting in the formation of a high-genus vesicle. A gradual change in the curvature suppresses this rupture. Hence, large stress, compared to the edge tension, induced by the rod assembly is the key factor determining rupture. For rod curvature with the opposite sign to the vesicle curvature, membrane rupture induces inversion of the membrane, leading to division into multiple vesicles as well as formation of a high-genus vesicle.

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Membrane tension controls the assembly of curvature-generating proteins

Cited by 145 publications

References 67 publications

Epsin N-terminal Homology Domain (ENTH) Activity as a Function of Membrane Tension

Epsin N-terminal Homology Domain (ENTH) Activity as a Function of Membrane Tension

Acceleration and suppression of banana-shaped-protein-induced tubulation by addition of small membrane inclusions of isotropic spontaneous curvatures

Shape deformation of lipid membranes by banana-shaped protein rods: Comparison with isotropic inclusions and membrane rupture

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