Time scales of membrane fusion revealed by direct imaging of vesicle fusion with high temporal resolution

Haluska, Christopher K.; Riske, Karin A.; Marchi-Artzner, Valérie; Lehn, Jean-Maríe; Lipowsky, Reinhard; Dimova, Rumiana

doi:10.1073/pnas.0602766103

Cited by 234 publications

(206 citation statements)

References 36 publications

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“…2C, ii), is a common intermediate step in the fusion process (9). However, contrary to the usual fusion pathway of pore formation within the hemi-fusion region (9,17,19) tions support an alternative fusion pathway, which has been already suggested by molecular simulations (20,21). The vesicle expels its contents through the pores (Fig.…”

Section: Lateral Expansion Of the Lipid Membranes Is Achieved By Vesiclementioning

confidence: 63%

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 Expansion Of the Lipid Membranes Is Achieved By Vesiclementioning

confidence: 63%

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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“…Both processes, which are involved in cell uptake, secretion, communication, and division for instance, are vital for the survival and proliferation of cells and are driven by various proteins (31)(32)(33). Synthetic models of vesicle fusion have been reported previously in giant liposome and polymeric vesicle systems, often with the aid of various ligands and ions replicating the roles of proteins in biological systems (34)(35)(36)(37)(38)(39). Additionally, vesicle fusion has been modeled with computer simulations for both unilamellar and multilamellar vesicles (40)(41)(42)(43)(44).…”

Section: Resultsmentioning

confidence: 99%

Janus dendrimersomes coassembled from fluorinated, hydrogenated, and hybrid Janus dendrimers as models for cell fusion and fission

Xiao

Sherman

Wilner

et al. 2017

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

203

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A three-component system of Janus dendrimers (JDs) including hydrogenated, fluorinated, and hybrid hydrogenated-fluorinated JDs are reported to coassemble by film hydration at specific ratios into an unprecedented class of supramolecular Janus particles (JPs) denoted Janus dendrimersomes (JDSs). They consist of a dumbbellshaped structure composed of an onion-like hydrogenated vesicle and an onion-like fluorinated vesicle tethered together. The synthesis of dye-tagged analogs of each JD component enabled characterization of JDS architectures with confocal fluorescence microscopy. Additionally, a simple injection method was used to prepare submicron JDSs, which were imaged with cryogenic transmission electron microscopy (cryo-TEM). As reported previously, different ratios of the same three-component system yielded a variety of structures including homogenous onion-like vesicles, core-shell structures, and completely self-sorted hydrogenated and fluorinated vesicles. Taken together with the JDSs reported herein, a self-sorting pathway is revealed as a function of the relative concentration of the hybrid JD, which may serve to stabilize the interface between hydrogenated and fluorinated bilayers. The fission-like pathway suggests the possibility of fusion and fission processes in biological systems that do not require the assistance of proteins but instead may result from alterations in the ratios of membrane composition.Janus particles | onion-like vesicles | self-sorting | fusion mechanism J anus particles (JPs) are nanoscale or microscale objects that exhibit two-faced asymmetry, enabling the presentation of vastly different chemical or physical properties localized at distinct parts of the same structure. They have been prepared as unimolecular systems in the form of dendrimers, dendrimer-like polymers, heterografted polymers, and polyhedral oligomeric silsesquioxanes; as supramolecular assemblies from lipids, block copolymers, and terpolymers and other polymers; as liquid crystals; and as inorganic nanoparticles. JPs have gained increasing attention due to their application in a variety of fields including as emulsion stabilizers, facilitators for the development of novel liquid/liquid and liquid/air interfaces among other interfacial applications, optical nanoprobes, electronic inks, self-propelling beads, targeted stealth drug delivery systems, MRI contrast agents, and theranostics agents, among other biomedical applications (1).Asymmetric molecules such as phospholipids, block copolymers, and Janus dendrimers (JDs) can be thought of as the molecularlevel equivalent of JPs. Phospholipids are the major building block of the bilayers of biological membranes. Synthetic vesicles, which mimic biological membranes, have been prepared from phospholipids and are denoted liposomes. As the result of their instability due to oxidation, phospholipids must be coassembled with cholesterol and polyethylene glycol-conjugated phospholipids to form stable liposomes (2, 3). Furthermore, time-consuming fractionation and extrusio...

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“…Their sizes (in the range of 1–100 µm) make GUVs amenable to direct observation of the membrane behavior under a microscope in real time. The response of GUVs when exposed to various external stimuli such as temperature and osmotic stress,5 magnetic6 and electric fields,7 chemical reactions or pH gradients,8 polymers,9 and detergents10 (not to mention the numerous studies with peptides and proteins) has already been investigated. Experiments with GUVs have thus unequivocally demonstrated the utility of this system for unveiling the material properties of the lipid bilayer.…”

Section: Introductionmentioning

confidence: 99%

Area Increase and Budding in Giant Vesicles Triggered by Light: Behind the Scene

et al. 2018

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Biomembranes are constantly remodeled and in cells, these processes are controlled and modulated by an assortment of membrane proteins. Here, it is shown that such remodeling can also be induced by photoresponsive molecules. The morphological control of giant vesicles in the presence of a water‐soluble ortho‐tetrafluoroazobenzene photoswitch (F‐azo) is demonstrated and it is shown that the shape transformations are based on an increase in membrane area and generation of spontaneous curvature. The vesicles exhibit budding and the buds can be retracted by using light of a different wavelength. In the presence of F‐azo, the membrane area can increase by more than 5% as assessed from vesicle electrodeformation. To elucidate the underlying molecular mechanism and the partitioning of F‐azo in the membrane, molecular dynamics simulations are employed. Comparison with theoretically calculated shapes reveals that the budded shapes are governed by curvature elasticity, that the spontaneous curvature can be decomposed into a local and a nonlocal contribution, and that the local spontaneous curvature is about 1/(2.5 µm). The results show that exo‐ and endocytotic events can be controlled by light and that these photoinduced processes provide an attractive method to change membrane area and morphology.

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Time scales of membrane fusion revealed by direct imaging of vesicle fusion with high temporal resolution

Cited by 234 publications

References 36 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

Janus dendrimersomes coassembled from fluorinated, hydrogenated, and hybrid Janus dendrimers as models for cell fusion and fission

Area Increase and Budding in Giant Vesicles Triggered by Light: Behind the Scene

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