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Complexin has a dual synaptic function as checkpoint protein in vesicle priming and as a promoter of vesicle fusion

MPS-Authors
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López-Murcia,  Francisco José
Department of Molecular Neurobiology, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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Lin,  Kun-Han
Emeritus Group of Membrane Biophysics, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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Berns,  Manon M. M.
Department of Molecular Neurobiology, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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Ranjan,  Mrinalini
Department of Molecular Neurobiology, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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Lipstein,  Noa
Department of Molecular Neurobiology, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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Neher,  Erwin       
Emeritus Group of Membrane Biophysics, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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Brose,  Nils       
Department of Molecular Neurobiology, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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Reim,  Kerstin
Department of Molecular Neurobiology, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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Taschenberger,  Holger       
Department of Molecular Neurobiology, Max Planck Institute for Multidisciplinary Sciences, Max Planck Society;

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Citation

López-Murcia, F. J., Lin, K.-H., Berns, M. M. M., Ranjan, M., Lipstein, N., Neher, E., et al. (2024). Complexin has a dual synaptic function as checkpoint protein in vesicle priming and as a promoter of vesicle fusion. PNAS, 121(15): e2320505121. doi:10.1073/pnas.2320505121.


Cite as: https://hdl.handle.net/21.11116/0000-000F-5732-7
Abstract
The presynaptic SNARE-complex regulator complexin (Cplx) enhances the fusogenicity of primed synaptic vesicles (SVs). Consequently, Cplx deletion impairs action potential-evoked transmitter release. Conversely, though, Cplx loss enhances spontaneous and delayed asynchronous release at certain synapse types. Using electrophysiology and kinetic modeling, we show that such seemingly contradictory transmitter release phenotypes seen upon Cplx deletion can be explained by an additional of Cplx in the control of SV priming, where its ablation facilitates the generation of a “faulty” SV fusion apparatus. Supporting this notion, a sequential two-step priming scheme, featuring reduced vesicle fusogenicity and increased transition rates into the faulty primed state, reproduces all aberrations of transmitter release modes and short-term synaptic plasticity seen upon Cplx loss. Accordingly, we propose a dual presynaptic function for the SNARE-complex interactor Cplx, one as a “checkpoint” protein that guarantees the proper assembly of the fusion machinery during vesicle priming, and one in boosting vesicle fusogenicity.