Membrane Curvature in Synaptic Vesicle Fusion and Beyond

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Membrane Curvature in Synaptic Vesicle Fusion and Beyond Harvey T. McMahon, Michael M. Kozlov, Sascha Martens  Cell  Volume 140, Issue 5, Pages 601-605 (March 2010) DOI: 10.1016/j.cell.2010.02.017 Copyright © 2010 Elsevier Inc. Terms and Conditions

Figure 1 Models of Membrane Bending and Fusion (A) An amphipathic helix, such as found in epsin or endophilin, is shown to insert into the most rigid part of a membrane leaflet to a depth approaching the lipid glycerol backbones. The adjacent hydrocarbon chains tilt and splay to fill the resulting void and drive the generation of local curvature. The picture illustrates the insertion of helix-0 from epsin-1 (PDB: 1h0a) (Ford et al., 2002), and the lipid and structure are to scale. (B) Membrane-inserting C2 domains, illustrated by the synaptotagmin-1 C2B domain (PDB: 1uow), occupy a similar position in the membrane to amphipathic helices but are more bulky than a four-turn helix (taking into account the complete volume) and because of this are likely to be more effective at generating curvature. (C) Response of the surrounding lipids to a wedge-like hydrophobic insertion (amphipathic helix or C2 domain). Lipid tilting could result in an increased membrane curvature that is quickly dissipated on either side of the insertion. (D) Two insertions, when tethered close to each other, could result in high curvature between the wedges. High curvature in this region is not stabilized by insertions and because of this would likely give rise to local instability and transient “hydrophobic-defects,” where the hydrophobic phase of the membrane is exposed. (E) Propagation of an insertion in a circular direction (as in the SNARE organization of vesicle fusion) would result in a region of high curvature that we refer to as the “end cap.” (F) Propagation of insertions in a longitudinal direction would result in a ridge of high curvature, and if also propagated in a circular direction could create a membrane tubule. (G) Propagation of insertions in both circular and longitudinal directions would create membrane tubules. Tubules created by insertions of synaptotamin-1 C2AB domains (see panel) and Doc2b C2AB domains have end caps with diameters of 17 nm (Martens et al., 2007; Groffen et al., 2010). (H) Theoretical calculation of the dependence of energy released by formation of the hemifusion stalk on the curvature of the end cap. Models are drawn in CCP4-MG freely available from http://www.ysbl.york.ac.uk/∼ccp4mg/. Cell 2010 140, 601-605DOI: (10.1016/j.cell.2010.02.017) Copyright © 2010 Elsevier Inc. Terms and Conditions

Figure 2 Membrane Buckling by C2 Domains as a Trigger for Fusion As the vesicle approaches the membrane in this model, the vesicular SNARE component binds to its SNARE counterparts on the target membrane, resulting in the formation of a complex that pulls the two membranes into close apposition (steps A and B). The C2 domains of synaptotagmin bind to the SNARE complex, potentially helping to complete their zippering into a continuous helix. The C2 domains also insert into the target membrane in a Ca2+-dependent manner, resulting in membrane buckling and an unstable membrane region optimally localized for fusion (jagged membrane in step C). As the fusion pore opens, the C2 domains would still be localized to the neck, where they might promote the early stages of fusion pore opening (step D). Cell 2010 140, 601-605DOI: (10.1016/j.cell.2010.02.017) Copyright © 2010 Elsevier Inc. Terms and Conditions