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J. Biol. Chem., Vol. 268, Issue 31, 23122-23127, Nov, 1993
J Hartinger and R Jahn
Glutamate, the major excitatory neurotransmitter of the mammalian central
nervous system, is stored in synaptic vesicles and released by exocytosis
upon depolarization of the presynaptic nerve terminal. Synaptic vesicles
possess an active glutamate-specific transporter that is driven by an
electrochemical proton gradient across the vesicle membrane and requires
chloride for maximal activity. In this study, we have characterized the
role of chloride in vesicular glutamate transport using
4,4'-diisothiocyanatostilbene-2,2'-disulfonic acid (DIDS), a potent
inhibitor of anion translocators. DIDS inhibited glutamate uptake with an
IC50 of 0.7 microM or less. In contrast, all energy gradient parameters
(membrane potential, pH gradient, and ATPase activity) required at least
5-fold higher concentration of DIDS for inhibition. Furthermore, high
concentrations of chloride but not of glutamate or other anions prevented
DIDS inhibition of glutamate uptake. In contrast to uptake, glutamate
efflux from glutamate-loaded vesicles was independent of chloride over a
wide concentration range. However, efflux was still susceptible to DIDS
inhibition. DIDS inhibition was prevented by excess chloride. We conclude
that the vesicular glutamate transporter possesses a DIDS-sensitive
chloride binding site on the cytoplasmic side, distinct from the substrate
binding site, which regulates transport activity.
An anion binding site that regulates the glutamate transporter of synaptic vesicles
Howard Hughes Medical Institute, Yale University Medical School, New Haven, Connecticut 06510.
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