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Volume 17, Number 12,
Issue of June 15, 1997
pp. 4672-4687
Copyright ©1997 Society for Neuroscience
Transporters Buffer Synaptically Released Glutamate on a
Submillisecond Time Scale
Received Feb. 4, 1997; revised April 7, 1997; accepted April 8, 1997.
Jeffrey S. Diamond and
Craig E. Jahr
The Vollum Institute, Oregon Health Sciences University,
Portland, Oregon 97201
The role of transporters in clearing free glutamate from the
synaptic cleft was studied in rat CA1 hippocampal neurons cultured on
glial microislands. The time course of free glutamate in the cleft
during a synaptic event was estimated by measuring the extent to which
the rapidly dissociating AMPA receptor antagonist kynurenate (KYN) was
replaced by glutamate during a synaptic response. Dose inhibition of
the AMPA receptor EPSC by KYN was less than predicted by the
equilibrium affinity of the antagonist, and the rise time of AMPA
receptor miniature EPSCs (mEPSCs) was slowed by KYN. Both results
indicated that KYN dissociated from AMPA receptors and was replaced by
synaptically released transmitter. When transporters were blocked by
D,L-threo- -hydroxyaspartic acid
(THA) or Li+, the mEPSC rise time in the presence of
KYN was slowed further, indicating that transporters affect the
glutamate concentration in the first few hundred microseconds of the
synaptic response.
The glutamate transient necessary to cause these effects was determined
by developing a detailed kinetic model of the AMPA receptor. The model
replicated the effects of KYN on the amplitude and rise time of the
synaptic responses when driven by glutamate transients that were
similar to previous estimates (; ).
The effects of THA were replicated by slowing and enlarging the slower
phase of the dual component transient by about 20% or by prolonging
the single component by almost 40%. Because transport is too slow to
account for these effects, it is concluded that transporters buffer
glutamate in the synaptic cleft.
Key words:
glutamate transporters;
AMPA receptor;
kinetic
model;
cultured hippocampal neurons;
buffered diffusion;
miniature
EPSC;
kynurenate;
D,L-threo--hydroxyaspartic acid
(THA)
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Kinetics and Activation of Postsynaptic Kainate Receptors at Thalamocortical Synapses: Role of Glutamate Clearance
J Neurophysiol,
September 1, 2001;
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[Abstract]
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N. Chen, J. Ren, L. A. Raymond, and T. H. Murphy
Changes in Agonist Concentration Dependence That Are a Function of Duration of Exposure Suggest N-Methyl-D-aspartate Receptor Nonsaturation during Synaptic Stimulation
Mol. Pharmacol.,
February 1, 2001;
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[Abstract]
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E. Neher and T. Sakaba
Combining Deconvolution and Noise Analysis for the Estimation of Transmitter Release Rates at the Calyx of Held
J. Neurosci.,
January 15, 2001;
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T. Sakaba and E. Neher
Quantitative Relationship between Transmitter Release and Calcium Current at the Calyx of Held Synapse
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January 15, 2001;
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[Abstract]
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J. Levenson, S. Endo, L. S. Kategaya, R. I. Fernandez, D. G. Brabham, J. Chin, J. H. Byrne, and A. Eskin
Long-term regulation of neuronal high-affinity glutamate and glutamine uptake in Aplysia
PNAS,
October 23, 2000;
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[Abstract]
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J. R. Cottrell, G. R. Dube, C. Egles, and G. Liu
Distribution, Density, and Clustering of Functional Glutamate Receptors Before and After Synaptogenesis in Hippocampal Neurons
J Neurophysiol,
September 1, 2000;
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C. Grewer, N. Watzke, M. Wiessner, and T. Rauen
Glutamate translocation of the neuronal glutamate transporter EAAC1 occurs within milliseconds
PNAS,
August 6, 2000;
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[Abstract]
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S. Eskandari, M. Kreman, M. P. Kavanaugh, E. M. Wright, and G. A. Zampighi
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PNAS,
July 18, 2000;
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[Abstract]
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A. G. Carter and W. G. Regehr
Prolonged Synaptic Currents and Glutamate Spillover at the Parallel Fiber to Stellate Cell Synapse
J. Neurosci.,
June 15, 2000;
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M. L. Beckman and M. W. Quick
The Ups and Downs of Neurotransmitter Transporters
Neuroscientist,
June 1, 2000;
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[Abstract]
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J. S. Diamond and C. E. Jahr
Synaptically Released Glutamate Does Not Overwhelm Transporters on Hippocampal Astrocytes During High-Frequency Stimulation
J Neurophysiol,
May 1, 2000;
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[Abstract]
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M. M. Bolton, A. J. Pittman, and D. C. Lo
Brain-Derived Neurotrophic Factor Differentially Regulates Excitatory and Inhibitory Synaptic Transmission in Hippocampal Cultures
J. Neurosci.,
May 1, 2000;
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T. S. Otis and M. P. Kavanaugh
Isolation of Current Components and Partial Reaction Cycles in the Glial Glutamate Transporter EAAT2
J. Neurosci.,
April 15, 2000;
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P. Jonas
The Time Course of Signaling at Central Glutamatergic Synapses
Physiology,
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M. Grunewald and B. I. Kanner
The Accessibility of a Novel Reentrant Loop of the Glutamate Transporter GLT-1 Is Restricted by Its Substrate
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March 24, 2000;
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T. C. Smith, L.-Y. Wang, and J. R. Howe
Heterogeneous Conductance Levels of Native AMPA Receptors
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March 15, 2000;
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B. Hutcheon, P. Morley, and M. O Poulter
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January 1, 2000;
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S. Duan, C. M. Anderson, B. A. Stein, and R. A. Swanson
Glutamate Induces Rapid Upregulation of Astrocyte Glutamate Transport and Cell-Surface Expression of GLAST
J. Neurosci.,
December 1, 1999;
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S. Mennerick, W. Shen, W. Xu, A. Benz, K. Tanaka, K. Shimamoto, K. E. Isenberg, J. E. Krause, and C. F. Zorumski
Substrate Turnover by Transporters Curtails Synaptic Glutamate Transients
J. Neurosci.,
November 1, 1999;
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L. S. Overstreet, G. A. Kinney, Y.-B. Liu, D. Billups, and N. T. Slater
Glutamate Transporters Contribute to the Time Course of Synaptic Transmission in Cerebellar Granule Cells
J. Neurosci.,
November 1, 1999;
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K. Matsui, N. Hosoi, and M. Tachibana
Active Role of Glutamate Uptake in the Synaptic Transmission from Retinal Nonspiking Neurons
J. Neurosci.,
August 15, 1999;
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R. Ventura and K. M. Harris
Three-Dimensional Relationships between Hippocampal Synapses and Astrocytes
J. Neurosci.,
August 15, 1999;
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J. E. Hanson and Y. Smith
Group I Metabotropic Glutamate Receptors at GABAergic Synapses in Monkeys
J. Neurosci.,
August 1, 1999;
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J. A. Dzubay and C. E. Jahr
The Concentration of Synaptically Released Glutamate Outside of the Climbing Fiber-Purkinje Cell Synaptic Cleft
J. Neurosci.,
July 1, 1999;
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S. Kojima, T. Nakamura, T. Nidaira, K. Nakamura, N. Ooashi, E. Ito, K. Watase, K. Tanaka, K. Wada, Y. Kudo, et al.
Optical Detection of Synaptically Induced Glutamate Transport in Hippocampal Slices
J. Neurosci.,
April 1, 1999;
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Y. Zhang and B. I. Kanner
Two serine residues of the glutamate transporter GLT-1 are crucial for coupling the fluxes of sodium and the neurotransmitter
PNAS,
February 16, 1999;
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[Abstract]
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R. Rao-Mirotznik, G. Buchsbaum, and P. Sterling
Transmitter Concentration at a Three-Dimensional Synapse
J Neurophysiol,
December 1, 1998;
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[Abstract]
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M. V. Jones, Y. Sahara, J. A. Dzubay, and G. L. Westbrook
Defining Affinity with the GABAA Receptor
J. Neurosci.,
November 1, 1998;
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K. P. Lehre and N. C. Danbolt
The Number of Glutamate Transporter Subtype Molecules at Glutamatergic Synapses: Chemical and Stereological Quantification in Young Adult Rat Brain
J. Neurosci.,
November 1, 1998;
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J. I. Wadiche and M. P. Kavanaugh
Macroscopic and Microscopic Properties of a Cloned Glutamate Transporter/Chloride Channel
J. Neurosci.,
October 1, 1998;
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T. S. Otis and C. E. Jahr
Anion Currents and Predicted Glutamate Flux through a Neuronal Glutamate Transporter
J. Neurosci.,
September 15, 1998;
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M. L. Beckman, E. M. Bernstein, and M. W. Quick
Protein Kinase C Regulates the Interaction between a GABA Transporter and Syntaxin 1A
J. Neurosci.,
August 15, 1998;
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