Formation of an Endophilin-Ca2+ Channel Complex Is Critical for Clathrin-Mediated Synaptic Vesicle Endocytosis

Chen, Yuan; Deng, Lin; Maeno-Hikichi, Yuka; Lai, Meizan; Chang, Shaohua; Chen, Gong; Zhang, Ji Fang

doi:10.1016/s0092-8674(03)00726-8

Cited by 108 publications

(123 citation statements)

References 55 publications

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“…The dynamin-binding BAR-SH3 domain protein endophilin has been postulated to interact with presynaptic Ca 2+ channels 86 , potentially linking Ca 2+ influx to exocytic-endocytic activity. Many dynamin-associated SH3 domain proteins, including intersectin 62 and ABP1, also interact with -and regulate -components of the actin cytoskeleton and of the CAZ (FIG.…”

Section: Super-resolution Light Microscopic Techniquesmentioning

confidence: 99%

Protein scaffolds in the coupling of synaptic exocytosis and endocytosis

2011

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Communication between nerve cells largely occurs at chemical synapses -specialized sites of cell-cell contact where electrical signals trigger the exocytic release of neurotransmitter, which in turn activates postsynaptic receptor channels. The efficacy with which such chemical signals are transmitted is crucial for the functioning of the nervous system. Modulation of neurotransmission enables nerve cells to respond to a vast range of stimulus patterns. Synaptic activity can also be tremendously diverse; from the fast synapses of the hippocampus, to slow neuropeptide-containing synapses. Indeed, some signalling pathways are active in the absence of stimulation, such as those involved in the processing of sensory information, which transmit tonically at high rates of up to 100 Hz or more 1,2 .Intriguing questions arise from these facts, including how high rates of neurotransmission can be maintained over long periods of time, and what limits the ability of a given synapse to release neurotransmitter during sustained periods of activity. Recent data indicate that in many synapses, exocytosis of neurotransmitter is coupled to endocytosis, and that synapses have evolved a specialized apparatus of scaffolding proteins to comply with these demands. Such scaffolds aid the temporal and spatial coupling of exocytosis and endocytosis, and are crucial for maintaining rapid neurotransmission during sustained activity 3 .Exocytosis of neurotransmitter is triggered by stimulusinduced calcium influx into the nerve terminal 4,5 and the subsequent fusion of synaptic vesicles with the presynaptic plasma membrane at specialized regions called active zones (BOX 1). Exocytosed synaptic vesicle membrane proteins and lipids in turn are recycled at the endocytic or periactive zone (BOX 1) that surrounds the release site, to restore functional synaptic vesicle pools for reuse and to ensure long-term functionality of the synapse 6-8 (FIG. 1). Depending on the type of synapse and the stimulation frequency, several modes of endocytosis with different time constants -for example, fast and slow endocytosisseem to operate 7,9,10 . Clathrin-mediated endocytosis arguably represents the main pathway of synaptic vesicle endocytosis 6,8,11 , although other modes -for example, fast kiss-and-run exocytosis and endocytosis -could operate in parallel.Although the machineries for exocytic membrane fusion 12,13 and for endocytic retrieval of synaptic vesicle membranes have been studied separately in some detail 6,14 , comparatively little is known about the coupling between exocytosis and endocytosis. Here we synthesize recent data from physiological, morphological and biochemical studies in several model systems into hypothetical models for scaffold-based mechanisms underlying exocytic-endocytic coupling.The synaptic vesicle cycle Synaptic vesicle pools. Some defining features of chemical synapses are the presence of one or several clusters of synaptic vesicles in the presynaptic nerve terminal, and ultrastructural specializations at the pre-and postsy...

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Section: Super-resolution Light Microscopic Techniquesmentioning

confidence: 99%

Protein scaffolds in the coupling of synaptic exocytosis and endocytosis

2011

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“…13,14,16,19,20 However, it is extremely difficult to routinely transfect single autaptic neurons because of the low efficiency associated with previous Ca 2+ -phosphate transfection method. Since our improved protocol has dramatically increased the transfection efficiency, transfection of single autaptic neurons has become routine in our lab.…”

Section: Single Neuron Transfection In Low-density Microisland Culturementioning

confidence: 99%

“…The effectiveness of this improved Ca 2+ -phosphate transfection method has been demonstrated in our recent study of endophilin-calcium channel interactions. 19 …”

Section: Introductionmentioning

confidence: 99%

High Ca2+-phosphate transfection efficiency enables single neuron gene analysis

2004

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“…and Ca 2+ binds to endophilin II directly and regulates endophilin-Ca 2+ channel complexes [23] . Endophilin II has two different modes at different Ca 2+ concentrations.…”

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confidence: 99%

“…When the Ca 2+ level increases (>1 μmol/L), the endophilin II SH3 domain may have an intramolecular interaction with its embedded PRD domain. In this situation, endophilin II changes to a closed mode and is no longer available for either Ca 2+ channels or dynamin, which leads to its Ca 2+ -dependence [23] . However, whether the other two isoforms of endophilin have similar characteristics in Ca 2+ -dependent binding with Ca 2+ channel proteins and whether these three isoforms have distinct interactions with dynamin I in clathrin-mediated endocytosis remain unknown.…”

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confidence: 99%

Endophilin isoforms have distinct characteristics in interactions with N-type Ca2+ channels and dynamin I

Tian¹,

Zhang²,

Fan

et al. 2012

Neurosci. Bull.

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Objective Formation of the endophilin II-Ca 2+ channel complex is Ca 2+ -dependent in clathrin-mediated endocytosis. However, little is known about whether the other two endophilin isoforms have the same features. The present study aimed to investigate the characteristics of the interactions of all three isoforms with Ca 2+ channels and dynamin I. Methods N-type Ca 2+ channel C-terminal fragments (NCFs) synthesized with a 3 H-leucine-labeled kit, were incubated with endophilin-GST fusion proteins, followed by pull-down assay. Results were counted on a scintillation counter. In addition, the different endophilin isoforms were each co-transfected with dynamin I into 293T cells, followed by flow cytometry and co-immunoprecipitation assay. Immunostaining was performed and an image analysis program was used to evaluate the overlap coefficient of cells expressing endophilin and dynamin I. Results All three isoforms interacted with NCF. Endophilins I and II demonstrated clear Ca 2+ -dependent interactions with NCF, whereas endophilin III did not. Co-immunoprecipitation showed that, compared to endophilin I/II, the interaction between endophilin III and dynamin I was significantly increased. Similar results were obtained from flow cytometry. Furthermore, endophilin III had a higher overlap coefficient with dynamin I in co-transfected 293T cells. Conclusion Endophilin isoforms have distinct characteristics in interactions with NCF and dynamin I. Endophilin III binding to NCF is Ca 2+ -independent, implying that it plays a different role in clathrin-mediated endocytosis.

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Formation of an Endophilin-Ca2+ Channel Complex Is Critical for Clathrin-Mediated Synaptic Vesicle Endocytosis

Cited by 108 publications

References 55 publications

Protein scaffolds in the coupling of synaptic exocytosis and endocytosis

Protein scaffolds in the coupling of synaptic exocytosis and endocytosis

High Ca2+-phosphate transfection efficiency enables single neuron gene analysis

Endophilin isoforms have distinct characteristics in interactions with N-type Ca2+ channels and dynamin I

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