Triple Function of Synaptotagmin 7 Ensures Efficiency of High-Frequency Transmission at Central GABAergic Synapses

被引:51
作者
Chen, Chong [1 ]
Satterfield, Rachel [2 ]
Young, Samuel M., Jr. [2 ,3 ]
Jonas, Peter [1 ]
机构
[1] IST Austria, Am Campus 1, A-3400 Klosterneuburg, Austria
[2] Max Planck Florida Inst Neurosci, Res Grp Mol Mech Synapt Funct, Jupiter, FL 33458 USA
[3] Univ Iowa, Iowa Neurosci, Dept Otolaryngol, Dept Anat & Cell Biol,Aging Mind Brain Initiat, Iowa City, IA 52242 USA
基金
奥地利科学基金会; 欧洲研究理事会;
关键词
PRINCIPAL NEURON SYNAPSE; TRANSMITTER RELEASE; CA2+ SENSOR; NEUROTRANSMITTER RELEASE; GABA RELEASE; EXOCYTOSIS; FACILITATION; INHIBITION; BEHAVIOR; OUTPUT;
D O I
10.1016/j.celrep.2017.10.122
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Synaptotagmin 7 (Syt7) is thought to be a Ca2+ sensor that mediates asynchronous transmitter release and facilitation at synapses. However, Syt7 is strongly expressed in fast-spiking, parvalbumin-expressing GABAergic interneurons, and the output synapses of these neurons produce only minimal asynchronous release and show depression rather than facilitation. To resolve this apparent contradiction, we examined the effects of genetic elimination of Syt7 on synaptic transmission at the GABAergic basket cell (BC)-Purkinje cell (PC) synapse in cerebellum. Our results indicate that at the BC-PC synapse, Syt7 contributes to asynchronous release, pool replenishment, and facilitation. In combination, these three effects ensure efficient transmitter release during high-frequency activity and guarantee frequency independence of inhibition. Our results identify a distinct function of Syt7: ensuring the efficiency of high-frequency inhibitory synaptic transmission.
引用
收藏
页码:2082 / 2089
页数:8
相关论文
共 45 条
[1]   Nanodomain coupling explains Ca2+ independence of transmitter release time course at a fast central synapse [J].
Arai, Itaru ;
Jonas, Peter .
ELIFE, 2014, 3
[2]   Synaptotagmin-1 and-7 Are Redundantly Essential for Maintaining the Capacity of the Readily-Releasable Pool of Synaptic Vesicles [J].
Bacaj, Taulant ;
Wu, Dick ;
Burre, Jacqueline ;
Malenka, Robert C. ;
Liu, Xinran ;
Suedhof, Thomas C. .
PLOS BIOLOGY, 2015, 13 (10)
[3]   Synaptotagmin-1 and Synaptotagmin-7 Trigger Synchronous and Asynchronous Phases of Neurotransmitter Release [J].
Bacaj, Taulant ;
Wu, Dick ;
Yang, Xiaofei ;
Morishita, Wade ;
Zhou, Peng ;
Xu, Wei ;
Malenka, Robert C. ;
Suedhof, Thomas C. .
NEURON, 2013, 80 (04) :947-959
[4]   Frequency-Independent Synaptic Transmission Supports a Linear Vestibular Behavior [J].
Bagnall, Martha W. ;
McElvain, Lauren E. ;
Faulstich, Michael ;
du Lac, Sascha .
NEURON, 2008, 60 (02) :343-352
[5]   Nanodomain coupling between Ca2+ channels and Ca2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse [J].
Bucurenciu, Iancu ;
Kulik, Akos ;
Schwaller, Beat ;
Frotscher, Michael ;
Jonas, Peter .
NEURON, 2008, 57 (04) :536-545
[6]   Impaired membrane resealing and autoimmune myositis in synaptotagmin VII-deficient mice [J].
Chakrabarti, S ;
Kobayashi, KS ;
Flavell, RA ;
Marks, CB ;
Miyake, K ;
Liston, DR ;
Fowler, KT ;
Gorelick, FS ;
Andrews, NW .
JOURNAL OF CELL BIOLOGY, 2003, 162 (04) :543-549
[7]   Synaptotagmin:: A Ca2+ sensor that triggers exocytosis? [J].
Chapman, ER .
NATURE REVIEWS MOLECULAR CELL BIOLOGY, 2002, 3 (07) :498-508
[8]   Synaptotagmins: That's Why So Many [J].
Chen, Chong ;
Jonas, Peter .
NEURON, 2017, 94 (04) :694-696
[9]   Synaptotagmin 2 Is the Fast Ca2+ Sensor at a Central Inhibitory Synapse [J].
Chen, Chong ;
Arai, Itaru ;
Satterfield, Rachel ;
Young, Samuel M., Jr. ;
Jonas, Peter .
CELL REPORTS, 2017, 18 (03) :723-736
[10]   Fast, Temperature-Sensitive and Clathrin-Independent Endocytosis at Central Synapses [J].
Delvendahl, Igor ;
Vyleta, Nicholas P. ;
von Gersdorff, Henrique ;
Hallermann, Stefan .
NEURON, 2016, 90 (03) :492-498