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Synaptotagmin-7 places dense-core vesicles at the cell membrane to promote Munc13-2- and Ca2+-dependent priming

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Imig,  Cordelia       
Molecular neurobiology, Max Planck Institute of Experimental Medicine, Max Planck Society;

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Wojcik,  Sonja M.
Molecular neurobiology, Max Planck Institute of Experimental Medicine, Max Planck Society;

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Brose,  Nils       
Molecular neurobiology, Max Planck Institute of Experimental Medicine, Max Planck Society;

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Cooper,  Benjamin H.
Molecular neurobiology, Max Planck Institute of Experimental Medicine, Max Planck Society;

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Citation

Tawfik, B., Martins, J. S., Houy, S., Imig, C., Pinheiro, P. S., Wojcik, S. M., et al. (2021). Synaptotagmin-7 places dense-core vesicles at the cell membrane to promote Munc13-2- and Ca2+-dependent priming. eLife, 10: e64527. doi:10.7554/eLife.64527.


Cite as: https://hdl.handle.net/21.11116/0000-000F-5A4A-A
Abstract
Synaptotagmins confer calcium-dependence to the exocytosis of secretory vesicles, but how coexpressed synaptotagmins interact remains unclear. We find that synaptotagmin-1 and synaptotagmin-7 when present alone act as standalone fast and slow Ca2+-sensors for vesicle fusion in mouse chromaffin cells. When present together, synaptotagmin-1 and synaptotagmin-7 are found in largely non-overlapping clusters on dense-core vesicles. Synaptotagmin-7 stimulates Ca2+-dependent vesicle priming and inhibits depriming, and it promotes ubMunc13-2- and phorbolester-dependent priming, especially at low resting calcium concentrations. The priming effect of synaptotagmin-7 increases the number of vesicles fusing via synaptotagmin-1, while negatively affecting their fusion speed, indicating both synergistic and competitive interactions between synaptotagmins. Synaptotagmin-7 places vesicles in close membrane apposition (<6 nm); without it, vesicles accumulate out of reach of the fusion complex (20–40 nm). We suggest that a synaptotagmin-7-dependent movement toward the membrane is involved in Munc13-2/phorbolester/Ca2+-dependent priming as a prelude to fast and slow exocytosis triggering.