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Song, Sang-Ho; Augustine, George J.
Cell reports (Cambridge), 08/2023, Letnik: 42, Številka: 8Journal Article
Synapsins cluster synaptic vesicles (SVs) to provide a reserve pool (RP) of SVs that maintains synaptic transmission during sustained activity. However, it is unclear how synapsins cluster SVs. Here we show that either liquid-liquid phase separation (LLPS) or tetramerization-dependent cross-linking can cluster SVs, depending on whether a synapse is excitatory or inhibitory. Cell-free reconstitution reveals that both mechanisms can cluster SVs, with tetramerization being more effective. At inhibitory synapses, perturbing synapsin-dependent LLPS impairs SV clustering and synchronization of gamma-aminobutyric acid (GABA) release, while preventing synapsin tetramerization does not. At glutamatergic synapses, the opposite is true: synapsin tetramerization enhances clustering of glutamatergic SVs and mobilization of these SVs from the RP, while synapsin LLPS does not. Comparison of inhibitory and excitatory transmission during prolonged synaptic activity reveals that synapsin LLPS serves as a brake to limit GABA release, while synapsin tetramerization enables rapid mobilization of SVs from the RP to sustain glutamate release. Display omitted •Synapsins cluster synaptic vesicles by liquid-liquid phase separation and by tetramerization•Synapsin-dependent liquid-liquid phase separation clusters vesicles at GABAergic synapses•Synapsin tetramerization cross-links vesicles at glutamatergic synapses•These synapsin-dependent processes confer different properties on GABA and glutamate release Song and Augustine examine how synaptic vesicles cluster in presynaptic terminals. They find that different types of synapses employ the same protein in different ways: at inhibitory synapses, synapsin-dependent liquid-liquid phase separation sequesters synaptic vesicles, while synapsin tetramers cross-link synaptic vesicles at glutamatergic synapses.
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