Fast endocytosis is inhibited by GABA-mediated chloride influx at a presynaptic terminal

Court Hull; Henrique Von Gersdorff

doi:10.1016/j.neuron.2004.10.010

Fast endocytosis is inhibited by GABA-mediated chloride influx at a presynaptic terminal

Court Hull
, Henrique Von Gersdorff

Vollum Institute

Research output: Contribution to journal › Article › peer-review

51 Scopus citations

Abstract

Although multiple kinetic components of synaptic vesicle endocytosis have been identified, it has remained unclear whether neurons can differentially modulate these components. Using membrane capacitance measurements from isolated goldfish bipolar cell terminals, we found that the kinetics of endocytosis in retinal slices (single exponential decay; τ > 10 s) were significantly slower than those in acutely dissociated terminals (double exponential decay; τ_fast ≅ 1-2 s; τ_slow > 10 s). Surprisingly, GABA_A and/or GABA_C receptor antagonists restored the fast component of endocytosis to terminals in retinal slices. Blocking GABAergic feedback from reciprocal synapses or removing external Cl^- ions also allowed for fast endocytosis. Elevating internal Cl^- via the patch pipette invariably slowed endocytosis, even in terminals dialyzed with increased Ca²⁺ buffer. These results suggest a new role for GABA and Cl^- ions in blocking the trigger for fast endocytosis at this ribbon-type synapse.

Original language	English (US)
Pages (from-to)	469-482
Number of pages	14
Journal	Neuron
Volume	44
Issue number	3
DOIs	https://doi.org/10.1016/j.neuron.2004.10.010
State	Published - Oct 28 2004

Funding

We thank Steven Yazulla (SUNY at Stony Brook, NY) for generously donating the goldfish bipolar cell electron micrograph. We thank Craig Jahr, Gary Matthews, Mary J. Palmer, and Jozsef Vigh for discussions. This work was supported by a grant from the NEI (H.v.G.) and an NRSA predoctoral fellowship (C.H.).

Funders	Funder number
National Eye Institute and Casey Eye Institute	R01EY014043
National Institute of Neurological Disorders and Stroke	F31NS042506
Israel National Road Safety Authority

ASJC Scopus subject areas

General Neuroscience

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10.1016/j.neuron.2004.10.010

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title = "Fast endocytosis is inhibited by GABA-mediated chloride influx at a presynaptic terminal",

abstract = "Although multiple kinetic components of synaptic vesicle endocytosis have been identified, it has remained unclear whether neurons can differentially modulate these components. Using membrane capacitance measurements from isolated goldfish bipolar cell terminals, we found that the kinetics of endocytosis in retinal slices (single exponential decay; τ > 10 s) were significantly slower than those in acutely dissociated terminals (double exponential decay; τfast ≅ 1-2 s; τslow > 10 s). Surprisingly, GABAA and/or GABAC receptor antagonists restored the fast component of endocytosis to terminals in retinal slices. Blocking GABAergic feedback from reciprocal synapses or removing external Cl- ions also allowed for fast endocytosis. Elevating internal Cl- via the patch pipette invariably slowed endocytosis, even in terminals dialyzed with increased Ca2+ buffer. These results suggest a new role for GABA and Cl- ions in blocking the trigger for fast endocytosis at this ribbon-type synapse.",

author = "Court Hull and \{Von Gersdorff\}, Henrique",

note = "Funding Information: We thank Steven Yazulla (SUNY at Stony Brook, NY) for generously donating the goldfish bipolar cell electron micrograph. We thank Craig Jahr, Gary Matthews, Mary J. Palmer, and Jozsef Vigh for discussions. This work was supported by a grant from the NEI (H.v.G.) and an NRSA predoctoral fellowship (C.H.). ",

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N2 - Although multiple kinetic components of synaptic vesicle endocytosis have been identified, it has remained unclear whether neurons can differentially modulate these components. Using membrane capacitance measurements from isolated goldfish bipolar cell terminals, we found that the kinetics of endocytosis in retinal slices (single exponential decay; τ > 10 s) were significantly slower than those in acutely dissociated terminals (double exponential decay; τfast ≅ 1-2 s; τslow > 10 s). Surprisingly, GABAA and/or GABAC receptor antagonists restored the fast component of endocytosis to terminals in retinal slices. Blocking GABAergic feedback from reciprocal synapses or removing external Cl- ions also allowed for fast endocytosis. Elevating internal Cl- via the patch pipette invariably slowed endocytosis, even in terminals dialyzed with increased Ca2+ buffer. These results suggest a new role for GABA and Cl- ions in blocking the trigger for fast endocytosis at this ribbon-type synapse.

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Fast endocytosis is inhibited by GABA-mediated chloride influx at a presynaptic terminal

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