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Cited by 183Neuroscience and Neuropharmacology ResearchATP Synthase and ATPases ResearchCellular transport and secretion

Glutamate transport into synaptic vesicles. Roles of membrane potential, pH gradient, and intravesicular pH

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Tabb, J.S., Kish, P.E., Van Dyke, R, Ueda, T·1992·Journal of Biological Chemistry
DOI 10.1016/s0021-9258(19)49549-5
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Abstract

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)

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  • Glutamate is an anion at neutral pH, and its loading into vesicles produces charge and proton changes opposite to vMAT and VAChT.

    “Glutamate is an anion at neutral pH, and loading of glutamate into vesicles produces a change in charge and H+ opposite to vMAT and VAChT.20”

    From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [20]

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Authors
Tabb, J. S., Kish, P. E., Van Dyke, R., & Ueda, T.
Affiliations
University of Michigan (US)
ORCID
Venue
Journal of Biological Chemistry
Publisher
Elsevier BV
Published
1992-08
Volume
267
Issue
22
Pages
15412-15418
ISSN
0021-9258 (ISSN-L)
DOI
10.1016/s0021-9258(19)49549-5
OpenAlex
W1490043608
Cited by
182
References
28
Citations by year
2026: 1 · 2025: 3 · 2024: 1 · 2023: 2 · 2022: 4 · 2021: 3 · 2020: 6 · 2019: 3 · 2018: 5 · 2017: 2 · 2016: 6 · 2015: 6 · 2014: 6 · 2013: 5 · 2012: 7
FWCI
3.12
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Biological Chemistry (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health (5t32mh015794-24)
  • National Institute of Mental Health (MH 15794-12)
  • National Institute of Neurological Disorders and Stroke (R01NS026884, NS 26884)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › ATP Synthase and ATPases Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Keywords
glutamate uptake, synaptic vesicles, vesicular glutamate transporter, intravesicular pH, chloride, ATP-dependent transport, proton-pumping ATPase, nigericin, vesicular acidification, vesicle fusion, vesicle exocytosis, vesicle recycling
MeSH terms
Adenosine Triphosphate, Animals, Biological Transport, Cattle, Cerebral Cortex, Chlorides, Glutamates, Hydrogen-Ion Concentration, Membrane Potentials, Methylamines, Nigericin, Synaptic Vesicles, Glutamic Acid

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