Membrane Buckling Induced by Curved Filaments

Abstract

We present a novel buckling instability relevant to membrane budding in eukaryotic cells. In this mechanism, curved filaments bind to a lipid bilayer without changing its intrinsic curvature. As more and more filaments adsorb, newly added ones are more and more strained, which destabilizes the flat membrane. We perform a linear stability analysis of filament-dressed membranes and find that the buckling threshold is within reasonable in vivo parameter values. We account for the formation of long tubes previously observed in cells and in purified systems. We study strongly deformed dressed membranes and their bifurcation diagram numerically. Our mechanism could be validated by a simple experiment.

Charged Multivesicular Body Protein 2B (CHMP2B) of the Endosomal Sorting Complex Required for Transport-III (ESCRT-III) Polymerizes into Helical Structures Deforming the Plasma Membrane

“…Immunogold labeling indicates that the protein lattice is made of CHMP2B, confirming the immunofluorescence staining of CHMP2B along the entire length of cellular membrane tubes. The CHMP2B protein lattice present in the tubes displays a lateral striation that is produced by helical symmetry; thus, tube formation most likely followed the biophysical principle of membrane buckling as proposed for ESCRT-III polymer assembly (38). The pitch of the helix was determined by cryo-EM to be 32 Å.…”

Structures, Functions, and Dynamics of ESCRT-III/Vps4 Membrane Remodeling and Fission Complexes

“…A series of models have been proposed to explain how ESCRT-III filaments and Vps4 together catalyze membrane remodeling, constriction, and fission (Adell et al 2017, Chiaruttini & Roux 2017, Fabrikant et al 2009, Hanson et al 2008, Henne et al 2013, Johnson et al 2018, Lenz et al 2009, Peel et al 2011, Saksena et al 2009, Schoeneberg et al 2018, Schöneberg et al 2017) (Figure 6). A consensus model has not emerged, however, and different aspects of the divergent models may need to be combined to explain how the ESCRT machinery can remodel membranes across such a variety of spatial scales and membrane geometries.…”

“…In an alternative class of models, membrane extrusion and fission are driven by filament buckling and unbuckling (Chiaruttini & Roux 2017, Chiaruttini et al 2015, Lenz et al 2009, Schoeneberg et al 2018). As illustrated in Figure 6 d , this elegant model envisions that ESCRT-III filaments initially spiral on a flat planar membrane, as is seen in the EM images in Figure 1 b , c .…”

Domes and cones: Adhesion-induced fission of membranes by ESCRT proteins

“…[23] In particular, the assembly of ESCRT-I and II has been proposed to drive bud formation through the induction of negative Gaussian curvature of the membrane, [24, 25] through the generation of lipid domains with a strong line tension at the domain boundary, [24] and through a significant spontaneous curvature arising from the protein coat. [8] Budding of the membrane may also be driven by the buckling of the ESCRT-III Snf7 spiral, [14, 26] or by the cargo itself, as in the case of exocytic engulfment of viral capsids or nanoparticles. [1, 27] Moreover, we note that although we will use the word ‘bud’ for conciseness throughout the paper, the results described here can be applied not only to the fission of small buds, but also to membrane fission during cytokinesis.…”

“…These dynamic processes are presumably governed by the energetics of association and deformation of the different ESCRT components and Vps4. While the elasticity of Snf7 spirals is now fairly well understood through in vitro experiments [14] and theory, [14, 26] it is still unclear how the remaining components interact with each other and with Snf7 in the full in vivo ESCRT assembly. In particular, it is possible that the ATP-dependent activity of Vps4 plays an important role in the growth and deformation of the assembly.…”