Synapsin condensation controls synaptic vesicle sequestering and dynamics

Christian Hoffmann, Jakob Rentsch, Taka A. Tsunoyama, Akshita Chhabra, Gerard Aguilar Perez, Rajdeep Chowdhury, Franziska Trnka, Aleksandr A. Korobeinikov, Ali H. Shaib, Marcelo Ganzella, Gregory Giannone, Silvio O. Rizzoli, Akihiro Kusumi, Helge Ewers and Dragomir Milovanovic ()
Additional contact information
Christian Hoffmann: German Center for Neurodegenerative Diseases (DZNE)
Jakob Rentsch: Freie Universität Berlin
Taka A. Tsunoyama: Okinawa Institute of Science and Technology Graduate University (OIST); Onna-son
Akshita Chhabra: German Center for Neurodegenerative Diseases (DZNE)
Gerard Aguilar Perez: German Center for Neurodegenerative Diseases (DZNE)
Rajdeep Chowdhury: Germany; Excellence Cluster Multiscale Bioimaging
Franziska Trnka: German Center for Neurodegenerative Diseases (DZNE)
Aleksandr A. Korobeinikov: German Center for Neurodegenerative Diseases (DZNE)
Ali H. Shaib: Germany; Excellence Cluster Multiscale Bioimaging
Marcelo Ganzella: Max Planck Institute for Multidisciplinary Sciences
Gregory Giannone: University of Bordeaux, UMR 5297
Silvio O. Rizzoli: Germany; Excellence Cluster Multiscale Bioimaging
Akihiro Kusumi: Okinawa Institute of Science and Technology Graduate University (OIST); Onna-son
Helge Ewers: Freie Universität Berlin
Dragomir Milovanovic: German Center for Neurodegenerative Diseases (DZNE)

Nature Communications, 2023, vol. 14, issue 1, 1-13

Abstract: Abstract Neuronal transmission relies on the regulated secretion of neurotransmitters, which are packed in synaptic vesicles (SVs). Hundreds of SVs accumulate at synaptic boutons. Despite being held together, SVs are highly mobile, so that they can be recruited to the plasma membrane for their rapid release during neuronal activity. However, how such confinement of SVs corroborates with their motility remains unclear. To bridge this gap, we employ ultrafast single-molecule tracking (SMT) in the reconstituted system of native SVs and in living neurons. SVs and synapsin 1, the most highly abundant synaptic protein, form condensates with liquid-like properties. In these condensates, synapsin 1 movement is slowed in both at short (i.e., 60-nm) and long (i.e., several hundred-nm) ranges, suggesting that the SV-synapsin 1 interaction raises the overall packing of the condensate. Furthermore, two-color SMT and super-resolution imaging in living axons demonstrate that synapsin 1 drives the accumulation of SVs in boutons. Even the short intrinsically-disordered fragment of synapsin 1 was sufficient to restore the native SV motility pattern in synapsin triple knock-out animals. Thus, synapsin 1 condensation is sufficient to guarantee reliable confinement and motility of SVs, allowing for the formation of mesoscale domains of SVs at synapses in vivo.

Date: 2023
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DOI: 10.1038/s41467-023-42372-6

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