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J. Biol. Chem., Vol. 267, Issue 22, 15412-15418, Aug, 1992
JS Tabb, PE Kish, R Van Dyke and T Ueda
Glutamate, the major excitatory neurotransmitter in the mammalian central
nervous system, is transported into bovine synaptic vesicles in a manner
that is ATP dependent and requires a vesicular electrochemical proton
gradient. We studied the electrical and chemical elements of this driving
force and evaluated the effects of chloride on transport. Increasing
concentrations of Cl- were found to increase the steady- state
ATP-dependent vesicular pH gradient (delta pH) and were found to
concomitantly decrease the vesicular membrane potential (delta psi). Low
millimolar chloride concentrations, which cause 3-6-fold stimulation of
vesicular glutamate uptake, caused small but measurable increases in delta
pH and decreases in delta psi, when compared to control vesicles in the
absence of chloride. Nigericin in potassium buffers was used to alter the
relative proportions of delta pH and delta psi. Compared to controls, at
all chloride concentrations tested, nigericin virtually abolished delta pH
and increased the vesicle interior positive delta psi. Concomitantly,
nigericin increased ATP- dependent glutamate uptake in 0-1 mM chloride but
decreased glutamate uptake in 4 mM (45%), 20 mM (80%), and 140 mM (75%) Cl-
(where delta pH in the absence of nigericin was large). These findings
suggest that either delta psi, delta pH, or a combination can drive
glutamate uptake, but to different degrees. In the presence of 4 mM Cl-,
where uptake is optimal, both delta psi and delta pH contribute to the
driving force for uptake. When the extravesicular pH was increased from 7.4
to 8.0, more Cl- was required to stimulate vesicular glutamate uptake. In
the absence of Cl-, as extravesicular pH was lowered to 6.8, uptake was
over 3-fold greater than it was at pH 7.4. As extravesicular pH was reduced
from 8.0 toward 6.8, less Cl- was required for maximal stimulation.
Decreasing the extravesicular pH from 8.0 to 6.8 in the absence of Cl-
significantly increased glutamate uptake activity, even though
proton-pumping ATPase activity actually decreased about 45% under identical
conditions. In the absence of chloride, nigericin increased glutamate
uptake at all the pH values tested except pH 8.0. Glutamate uptake at pH
6.8 in the presence of nigericin was over 6-fold greater than uptake at pH
7.4 in the absence of nigericin. We conclude from these experiments that
optimal ATP-dependent glutamate uptake requires a large delta psi and a
small delta pH.(ABSTRACT TRUNCATED AT 400 WORDS)
Glutamate transport into synaptic vesicles. Roles of membrane potential, pH gradient, and intravesicular pH
Mental Health Research Institute, University of Michigan, Ann Arbor 48109.
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