Remodeling of Membrane Shape and Topology by Curvature Elasticity and Membrane Tension

Abstract

Cellular membranes exhibit a fascinating variety of different morphologies, which are continuously remodeled by transformations of membrane shape and topology. This remodeling is essential for important biological processes (cell division, intracellular vesicle trafficking, endocytosis) and can be elucidated in a systematic and quantitative manner using synthetic membrane systems. Here, recent insights obtained from such synthetic systems are reviewed, integrating experimental observations and molecular dynamics simulations with the theory of membrane elasticity. The study starts from the polymorphism of biomembranes as observed for giant vesicles by optical microscopy and small nanovesicles in simulations. This polymorphism reflects the unusual elasticity of fluid membranes and includes the formation of membrane necks or fluid ‘worm holes'. The proliferation of membrane necks generates stable multi‐spherical shapes, which can form tubules and tubular junctions. Membrane necks are also essential for the remodeling of membrane topology via membrane fission and fusion. Neck fission can be induced by fine‐tuning of membrane curvature, which leads to the controlled division of giant vesicles, and by adhesion‐induced membrane tension as observed for small nanovesicles. Challenges for future research include the interplay of curvature elasticity and membrane tension during membrane fusion and the localization of fission and fusion processes within intramembrane domains.

Enhanced Expansion and Reduced Kiss-and-Run Events in Fusion Pores Steered by Synaptotagmin-1 C2B Domains

“…Therefore, once we generated a nucleated fusion pore in the space of ξ n , we have let it evolve freely in the space of ξ e where it could be later controlled, either to be shrunk or enlarged. The general shape of the schematic PMF shown in Figure is in good agreement with other proposed energy landscapes. ,− …”

Enhanced Expansion and Reduced Kiss-and-Run Events in Fusion Pores Steered by Synaptotagmin-1 C2B Domains

“…Therefore, once we generated a nucleated fusion pore in the space of ξ n , we have let it evolve freely in the space of ξ e where it could be later controlled, either to be shrunk or enlarged. The general shape of the schematic PMF shown in Figure is in good agreement with other proposed energy landscapes. ,− …”

Methyl-β-cyclodextrin asymmetrically extracts phospholipid from bilayers, granting tunable control over differential stress in lipid vesicles

“…5d–f ); this finding might relate to the metastability of closed necks in these vesicles. 75 Occurrence of lipid insertion for Q ϕ = 1100 M −3 agrees with our estimate of Q cross ϕ = 1200 ± 109 M −3 (within associated uncertainty) (please see indicated note). 76 The significance of this finding will be emphasized in the Discussion section.…”

Self-organized spatial targeting of contractile actomyosin rings for synthetic cell division

“…3c). 29 Furthermore, consistent with our previous observations and simultaneous to this membrane remodelling effect, the diffusiophoretic transport of actomyosin bundles reorganized the network at the membrane. As a result, membrane compartments changed in size and the 13 oscillations maintained a chaotic mode inducing dynamic blebs in other areas of the vesicle (Fig.…”

Enhanced Expansion and Reduced Kiss-and-Run Events in Fusion Pores Steered by Synaptotagmin-1 C2B Domains

“…Therefore, once we generated a nucleated fusion pore in the space of ξ n , we have let it evolve freely in the space of ξ e where it could be later controlled, either to be shrunk or enlarged. The general shape of the schematic PMF shown in Figure is in good agreement with other proposed energy landscapes. ,− …”

Methyl-β-cyclodextrin asymmetrically extracts phospholipid from bilayers, granting tunable control over differential stress in lipid vesicles

“…5d–f ); this finding might relate to the metastability of closed necks in these vesicles. 75 Occurrence of lipid insertion for Q ϕ = 1100 M −3 agrees with our estimate of Q cross ϕ = 1200 ± 109 M −3 (within associated uncertainty) (please see indicated note). 76 The significance of this finding will be emphasized in the Discussion section.…”

Self-organized spatial targeting of contractile actomyosin rings for synthetic cell division

“…3c). 29 Furthermore, consistent with our previous observations and simultaneous to this membrane remodelling effect, the diffusiophoretic transport of actomyosin bundles reorganized the network at the membrane. As a result, membrane compartments changed in size and the 13 oscillations maintained a chaotic mode inducing dynamic blebs in other areas of the vesicle (Fig.…”

Enhanced Expansion and Reduced Kiss-and-Run Events in Fusion Pores Steered by Synaptotagmin-1 C2B Domains

“…Therefore, once we generated a nucleated fusion pore in the space of ξ n , we have let it evolve freely in the space of ξ e where it could be later controlled, either to be shrunk or enlarged. The general shape of the schematic PMF shown in Figure is in good agreement with other proposed energy landscapes. ,− …”

Methyl-β-cyclodextrin asymmetrically extracts phospholipid from bilayers, granting tunable control over differential stress in lipid vesicles

“…5d–f ); this finding might relate to the metastability of closed necks in these vesicles. 75 Occurrence of lipid insertion for Q ϕ = 1100 M −3 agrees with our estimate of Q cross ϕ = 1200 ± 109 M −3 (within associated uncertainty) (please see indicated note). 76 The significance of this finding will be emphasized in the Discussion section.…”

Self-organized spatial targeting of contractile actomyosin rings for synthetic cell division

“…3c). 29 Furthermore, consistent with our previous observations and simultaneous to this membrane remodelling effect, the diffusiophoretic transport of actomyosin bundles reorganized the network at the membrane. As a result, membrane compartments changed in size and the 13 oscillations maintained a chaotic mode inducing dynamic blebs in other areas of the vesicle (Fig.…”