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Synaptotagmin 2 Is the Fast Ca2+ Sensor at a Central Inhibitory Synapse
Journal article   Open access   Peer reviewed

Synaptotagmin 2 Is the Fast Ca2+ Sensor at a Central Inhibitory Synapse

Chong Chen, Itaru Arai, Rachel Satterfield, Samuel M Young and Peter Jonas
Cell reports (Cambridge), Vol.18(3), pp.723-736
01/17/2017
DOI: 10.1016/j.celrep.2016.12.067
PMCID: PMC5276807
PMID: 28099850
url
https://doi.org/10.1016/j.celrep.2016.12.067View
Published (Version of record) Open Access

Abstract

GABAergic synapses in brain circuits generate inhibitory output signals with submillisecond latency and temporal precision. Whether the molecular identity of the release sensor contributes to these signaling properties remains unclear. Here, we examined the Ca2+ sensor of exocytosis at GABAergic basket cell (BC) to Purkinje cell (PC) synapses in cerebellum. Immunolabeling suggested that BC terminals selectively expressed synaptotagmin 2 (Syt2), whereas synaptotagmin 1 (Syt1) was enriched in excitatory terminals. Genetic elimination of Syt2 reduced action potential-evoked release to ∼10%, identifying Syt2 as the major Ca2+ sensor at BC-PC synapses. Differential adenovirus-mediated rescue revealed that Syt2 triggered release with shorter latency and higher temporal precision and mediated faster vesicle pool replenishment than Syt1. Furthermore, deletion of Syt2 severely reduced and delayed disynaptic inhibition following parallel fiber stimulation. Thus, the selective use of Syt2 as release sensor at BC-PC synapses ensures fast and efficient feedforward inhibition in cerebellar microcircuits. [Display omitted] •Syt2 is the Ca2+ sensor of fast transmitter release at a cerebellar GABAergic synapse•Syt2 triggers transmitter release with faster time course than Syt1•Syt2 ensures faster replenishment of the readily releasable pool than Syt1•Syt2 is essential for fast feedforward inhibition in cerebellar microcircuits Chen et al. identify synaptotagmin 2 as the major Ca2+ sensor of transmitter release at cerebellar inhibitory synapses. Furthermore, they demonstrate that synaptotagmin 2 triggers faster release and ensures faster refilling of the vesicular pool than synaptotagmin 1.
feedforward inhibition transmitter release Ca2+ sensor pool replenishment endocytosis GABAergic synapses exocytosis synaptotagmin cerebellum basket cells

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