Fast endocytosis is inhibited by GABA-mediated chloride influx at a presynaptic terminal.
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; tau > 10 s) were significantly slower than those in acutely dissociated terminals (double exponential decay; tau(fast) approximately 1-2 s; tau(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 Ca(2+) buffer. These results suggest a new role for GABA and Cl(-) ions in blocking the trigger for fast endocytosis at this ribbon-type synapse.
Hull
Court
C
The Vollum Institute, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, Portland, OR 97239, USA.
von Gersdorff
Henrique
H
D000818:Animals; D001640:Bicuculline / Q000494:pharmacology; D002118:Calcium / Q000378:metabolism; D002478:Cells, Cultured; D002614:Chelating Agents / Q000494:pharmacology; D002712:Chlorides / Q000378:metabolism*; D004305:Dose-Response Relationship, Drug; D004347:Drug Interactions; D004533:Egtazic Acid / Q000494:pharmacology; D004705:Endocytosis / Q000502:physiology*; D018690:Excitatory Amino Acid Agonists / Q000494:pharmacology; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D018756:GABA Antagonists / Q000494:pharmacology; D006054:Goldfish; D066298:In Vitro Techniques; D007476:Ionophores / Q000494:pharmacology; D008564:Membrane Potentials / Q000187:drug effects / Q000502:physiology; D046529:Microscopy, Electron, Transmission / Q000379:methods; D008959:Models, Neurological; D009433:Neural Inhibition / Q000502:physiology*; D009474:Neurons / Q000166:cytology / Q000502:physiology*; D009761:Nystatin / Q000494:pharmacology; D018408:Patch-Clamp Techniques / Q000379:methods; D010721:Phosphinic Acids / Q000494:pharmacology; D010852:Picrotoxin / Q000494:pharmacology; D017729:Presynaptic Terminals / Q000187:drug effects* / Q000648:ultrastructure; D011725:Pyridines / Q000494:pharmacology; D011810:Quinoxalines / Q000494:pharmacology; D012160:Retina / Q000166:cytology; D013997:Time Factors; D014633:Valine / Q000031:analogs & derivatives* / Q000494:pharmacology; D005680:gamma-Aminobutyric Acid / Q000378:metabolism*
D001640:Bicuculline; D002118:Calcium; D002614:Chelating Agents; D002712:Chlorides; D004533:Egtazic Acid; D018690:Excitatory Amino Acid Agonists; D018691:Excitatory Amino Acid Antagonists; D018756:GABA Antagonists; D007476:Ionophores; D009761:Nystatin; D010721:Phosphinic Acids; D010852:Picrotoxin; D011725:Pyridines; D011810:Quinoxalines; D014633:Valine; D005680:gamma-Aminobutyric Acid; C101879:(1,2,5,6-tetrahydropyridin-4-yl)methylphosphinic acid; C062865:2,3-dioxo-6-nitro-7-sulfamoylbenzo(f)quinoxaline; C056639:2-amino-5-phosphopentanoic acid