Chemically Triggered Ejection of Membrane Tubules Controlled by Intermonolayer Friction

Fournier, Jean‐Baptiste; Khalifat, Nada; Puff, Nicolas; Angelova, Maria

doi:10.1103/physrevlett.102.018102

Cited by 70 publications

(123 citation statements)

References 24 publications

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“…The apparent stability of the tubes may be explained by the higher shear modulus of the supported bilayer, which slows the membrane bending kinetics, and the equilibrated tension at the cessation of the compression. Finally, we note that lipid tubes were previously shown to form in vivo in cells by molecular motors exerting point forces (31) or by the curving of the membrane through molecular (32) and chemical interactions (33). Our observations indicate a unique passive route for tube formations, determined solely by mechanical constraints on the membrane.…”

Section: Lateral Compression Of Confined Lipid Membranes Results In Fmentioning

confidence: 52%

Mechanics of surface area regulation in cells examined with confined lipid membranes

Staykova

Holmes

Read

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

133

141

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Cells are wrapped in inelastic membranes, yet they can sustain large mechanical strains by regulating their area. The area regulation in cells is achieved either by membrane folding or by membrane exo- and endocytosis. These processes involve complex morphological transformations of the cell membrane, i.e., invagination, vesicle fusion, and fission, whose precise mechanisms are still under debate. Here we provide mechanistic insights into the area regulation of cell membranes, based on the previously neglected role of membrane confinement, as well as on the strain-induced membrane tension. Commonly, the membranes of mammalian and plant cells are not isolated, but rather they are adhered to an extracellular matrix, the cytoskeleton, and to other cell membranes. Using a lipid bilayer, coupled to an elastic sheet, we are able to demonstrate that, upon straining, the confined membrane is able to regulate passively its area. In particular, by stretching the elastic support, the bilayer laterally expands without rupture by fusing adhered lipid vesicles; upon compression, lipid tubes grow out of the membrane plane, thus reducing its area. These transformations are reversible, as we show using cycles of expansion and compression, and closely reproduce membrane processes found in cells during area regulation. Moreover, we demonstrate a new mechanism for the formation of lipid tubes in cells, which is driven by the membrane lateral compression and may therefore explain the various membrane tubules observed in shrinking cells.

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Section: Lateral Compression Of Confined Lipid Membranes Results In Fmentioning

confidence: 52%

Mechanics of surface area regulation in cells examined with confined lipid membranes

Staykova

Holmes

Read

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

133

141

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“…One can evaluate the relative importance of these contributions in Eq. 5 using the following bilayer parameters a = 5 nm, d = 1 nm (19), b = 10 9 J·s·m −4 (20)(21)(22) and μ m = 6 × 10 −10 J·s·m −2 (23), from which one finds the dimensionless factors bd 2 =ηa ' 200, ðd=aÞ 2 ' 0:04, and μ m d 2 =2ηa 3 ' 2. It follows from such estimates that the monolayer friction should play the largest role in the effective friction of the protein (Eq.…”

Section: Applied Physical Sciencesmentioning

confidence: 99%

Shape matters in protein mobility within membranes

Quemeneur

Sigurdsson

Renner

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

106

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The lateral mobility of proteins within cell membranes is usually thought to be dependent on their size and modulated by local heterogeneities of the membrane. Experiments using single-particle tracking on reconstituted membranes demonstrate that protein diffusion is significantly influenced by the interplay of membrane curvature, membrane tension, and protein shape. We find that the curvature-coupled voltage-gated potassium channel (KvAP) undergoes a significant increase in protein mobility under tension, whereas the mobility of the curvature-neutral water channel aquaporin 0 (AQP0) is insensitive to it. Such observations are well explained in terms of an effective friction coefficient of the protein induced by the local membrane deformation.Brownian motion | Saffman-Delbrück | internal membrane structure | drag force | micropipette aspiration B rownian motion plays an essential role in biological processes. Since the pioneering experiments of Perrin (1), the observation of diffusing objects has emerged as a mean to extract the rheological properties of the surrounding medium or the probe particle size. The theoretical investigation of diffusion of proteins within membranes has been studied widely going back to P. G. Saffman and M. Delbrück (SD). They investigated the hydrodynamic drag acting on a membrane inclusion when the membrane is described as a 2D fluid sheet of viscosity μ m embedded within a less viscous fluid of viscosity η (2). In this theory, the diffusion coefficient D 0 in the limit of a large viscosity contrast between the membrane and bulk fluid is given by:The length ℓ = μ m =η is the length scale over which flow is generated within the bilayer by the inclusion, k B T is the thermal energy, and γ is Euler's constant. This model predicts a logarithmic dependence of D 0 on the protein radius a p , which has been confirmed for some in vitro experiments on membranes containing transmembrane proteins (see ref.3 and references therein). In contrast, the experiments of Gambin et al. (4) showed significant deviations from the SD theory. A possible origin for the discrepancy observed by Gambin et al. (4) is the significant local membrane deformation due to the interaction between the inclusion and the lipid bilayer (5). Naji et al. suggested in ref. 6 that inclusions experience additional dissipation, either due to internal flows within the membrane or to additional fluid flows produced by the deformed membrane. This work triggered a number of theoretical studies investigating the coupling of inclusion proteins with the membrane that had been pioneered by the Seifert's group (see ref. 7 and references therein). Such studies have systematically gone beyond the SD model by including additional effects (8-12). So far, a thorough verification of these ideas has not been attempted. To investigate the effect of the protein-lipid coupling on the protein mobility, we study its dependence on membrane tension, because this parameter affects the local membrane deformation.In this work, we compare the mobility of t...

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“…They transiently respond for instance to pH gradients by developing tubules and pearled protrusions (Khalifat et al, 2014(Khalifat et al, , 2008Fournier et al, 2009). Furthermore, a myriad of proteins interact with lipid bilayers through curvature, either to generate it or to sense it (McMahon and Gallop, 2005;Zimmerberg and Kozlov, 2006;Sens et al, 2008;Shibata et al, 2009;Antonny, 2011).…”

Section: Introductionmentioning

confidence: 99%

“…When it comes to the interaction of bilayers with proteins, the bilayer architecture is bound to play an important role since proteins can merely scaffold the membrane, shallowly insert into one monolayer, or pierce through the entire bilayer. Elasto-hydrodynamical models capturing the bilayer architecture have been developed under the assumption of linearized perturbations (Seifert and Langer, 1993;Fournier et al, 2009;CallanJones et al, 2016), or in a fully nonlinear albeit axisymmetric setting (Rahimi and Arroyo, 2012). In the present Chapter, we will not focus on this aspect.…”

Section: Introductionmentioning

confidence: 99%

Onsager’s Variational Principle in Soft Matter: Introduction and Application to the Dynamics of Adsorption of Proteins onto Fluid Membranes

Arroyo

Walani

Torres-Sánchez

et al. 2017

CISM International Centre for Mechanical Sciences

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Chemically Triggered Ejection of Membrane Tubules Controlled by Intermonolayer Friction

Cited by 70 publications

References 24 publications

Mechanics of surface area regulation in cells examined with confined lipid membranes

Mechanics of surface area regulation in cells examined with confined lipid membranes

Shape matters in protein mobility within membranes

Onsager’s Variational Principle in Soft Matter: Introduction and Application to the Dynamics of Adsorption of Proteins onto Fluid Membranes

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