 |
The Journal of Neuroscience, June 15, 2003, 23(12):4831-4841
 Previous Article | Next Article 
Synaptic Activation of Presynaptic Glutamate Transporter Currents in Nerve Terminals
Mary J. Palmer,
Holger Taschenberger,
Court Hull,
Liisa Tremere, and
Henrique von Gersdorff
The Vollum Institute, Oregon Health and Science University, Portland, Oregon 97239
Glutamate uptake by high-affinity transporters is responsible for limiting the activation of postsynaptic receptors and maintaining low levels of ambient glutamate. The reuptake process generates membrane currents, which can be activated by synaptically released glutamate in glial cells and some postsynaptic neurons. However, less is known about presynaptic transporter currents because the small size of synaptic boutons precludes direct recordings. Here, we have recorded from two giant nerve terminals: bipolar cell synaptic terminals in goldfish retina and the calyx of Held in rat auditory brainstem. Exocytosis was evoked by brief depolarizations and measured as an increase in membrane capacitance. In isolated bipolar cell terminals, exocytosis was associated with an anion (NO3- or Cl-) current. The current peaked 2.8 msec after the start of the depolarization and decayed with a mean time constant of 8.5 msec. It was inhibited by the nontransportable glutamate transporter antagonist SC-threo- -benzyloxyaspartate (TBOA) but was insensitive to the GLT1/EAAT2 subtype-selective antagonist dihydrokainate and was affected by extracellular pH buffering. A TBOA-sensitive anion current was also evoked by application of exogenous glutamate to bipolar cell terminals. The large single-channel conductance, derived from noise analysis, and previous immunolocalization studies suggest that synaptically released glutamate activates EAAT5-type transporters in bipolar cell terminals. In contrast, neither exocytosis nor exogenous glutamate evoked a transporter current in the calyx of Held. Glutamate transporter currents with rapid kinetics are therefore identified and characterized in bipolar cell terminals, providing a valuable system for investigating the function and modulation of presynaptic glutamate transporters.
Key words: glutamate transporters; uptake; presynaptic terminal; exocytosis; retinal bipolar cell; synaptic ribbons; calyx of Held; auditory brainstem; EAAT5 anion current
Received Sep. 6, 2002;
revised Feb. 24, 2003;
accepted Feb. 24, 2003.
This article has been cited by other articles:
|
|
|
|
 
S. M. Jones and M. J. Palmer
Activation of the Tonic GABAC Receptor Current in Retinal Bipolar Cell Terminals by Nonvesicular GABA Release
J Neurophysiol,
August 1, 2009;
102(2):
691 - 699.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. H. Mørkve and E. Hartveit
Properties of glycine receptors underlying synaptic currents in presynaptic axon terminals of rod bipolar cells in the rat retina
J. Physiol.,
August 1, 2009;
587(15):
3813 - 3830.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Petit-Jacques and S. A. Bloomfield
Synaptic Regulation of the Light-Dependent Oscillatory Currents in Starburst Amacrine Cells of the Mouse Retina
J Neurophysiol,
August 1, 2008;
100(2):
993 - 1006.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Torres-Salazar and C. Fahlke
Neuronal Glutamate Transporters Vary in Substrate Transport Rate but Not in Unitary Anion Channel Conductance
J. Biol. Chem.,
November 30, 2007;
282(48):
34719 - 34726.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Kam and R. Nicoll
Excitatory Synaptic Transmission Persists Independently of the Glutamate Glutamine Cycle
J. Neurosci.,
August 22, 2007;
27(34):
9192 - 9200.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G.-L. Li, J. Vigh, and H. von Gersdorff
Short-Term Depression at the Reciprocal Synapses between a Retinal Bipolar Cell Terminal and Amacrine Cells
J. Neurosci.,
July 11, 2007;
27(28):
7377 - 7385.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. P. Koch, R. Lane Brown, and H. P. Larsson
The Glutamate-Activated Anion Conductance in Excitatory Amino Acid Transporters Is Gated Independently by the Individual Subunits
J. Neurosci.,
March 14, 2007;
27(11):
2943 - 2947.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. L. Beaudoin, B. G. Borghuis, and J. B. Demb
Cellular Basis for Contrast Gain Control over the Receptive Field Center of Mammalian Retinal Ganglion Cells
J. Neurosci.,
March 7, 2007;
27(10):
2636 - 2645.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Oltedal, S. H. Morkve, M. L. Veruki, and E. Hartveit
Patch-Clamp Investigations and Compartmental Modeling of Rod Bipolar Axon Terminals in an In Vitro Thin-Slice Preparation of the Mammalian Retina
J Neurophysiol,
February 1, 2007;
97(2):
1171 - 1187.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. J. Palmer
Functional segregation of synaptic GABAA and GABAC receptors in goldfish bipolar cell terminals
J. Physiol.,
November 15, 2006;
577(1):
45 - 53.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Wersinger, Y. Schwab, J.-A. Sahel, A. Rendon, D. V. Pow, S. Picaud, and M. J. Roux
The glutamate transporter EAAT5 works as a presynaptic receptor in mouse rod bipolar cells
J. Physiol.,
November 15, 2006;
577(1):
221 - 234.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Hull, K. Studholme, S. Yazulla, and H. von Gersdorff
Diurnal Changes in Exocytosis and the Number of Synaptic Ribbons at Active Zones of an ON-Type Bipolar Cell Terminal
J Neurophysiol,
October 1, 2006;
96(4):
2025 - 2033.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Glowatzki, N. Cheng, H. Hiel, E. Yi, K. Tanaka, G. C. R. Ellis-Davies, J. D. Rothstein, and D. E. Bergles
The glutamate-aspartate transporter GLAST mediates glutamate uptake at inner hair cell afferent synapses in the mammalian cochlea.
J. Neurosci.,
July 19, 2006;
26(29):
7659 - 7664.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Hull, G.-L. Li, and H. von Gersdorff
GABA transporters regulate a standing GABAC receptor-mediated current at a retinal presynaptic terminal.
J. Neurosci.,
June 28, 2006;
26(26):
6979 - 6984.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. J. Palmer
Modulation of Ca2+-activated K+ currents and Ca2+-dependent action potentials by exocytosis in goldfish bipolar cell terminals
J. Physiol.,
May 1, 2006;
572(3):
747 - 762.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Vigh and H. von Gersdorff
Prolonged Reciprocal Signaling via NMDA and GABA Receptors at a Retinal Ribbon Synapse
J. Neurosci.,
December 7, 2005;
25(49):
11412 - 11423.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Taschenberger, V. Scheuss, and E. Neher
Release kinetics, quantal parameters and their modulation during short-term depression at a developing synapse in the rat CNS
J. Physiol.,
October 15, 2005;
568(2):
513 - 537.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Renden, H. Taschenberger, N. Puente, D. A. Rusakov, R. Duvoisin, L.-Y. Wang, K. P. Lehre, and H. von Gersdorff
Glutamate Transporter Studies Reveal the Pruning of Metabotropic Glutamate Receptors and Absence of AMPA Receptor Desensitization at Mature Calyx of Held Synapses
J. Neurosci.,
September 14, 2005;
25(37):
8482 - 8497.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Y. Wong, E. D. Cohen, and J. E. Dowling
Retinal Bipolar Cell Input Mechanisms in Giant Danio. II. Patch-Clamp Analysis of ON Bipolar Cells
J Neurophysiol,
January 1, 2005;
93(1):
94 - 107.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Melzer, A. Biela, and C. Fahlke
Glutamate Modifies Ion Conduction and Voltage-dependent Gating of Excitatory Amino Acid Transporter-associated Anion Channels
J. Biol. Chem.,
December 12, 2003;
278(50):
50112 - 50119.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. J. Palmer, C. Hull, J. Vigh, and H. von Gersdorff
Synaptic Cleft Acidification and Modulation of Short-Term Depression by Exocytosed Protons in Retinal Bipolar Cells
J. Neurosci.,
December 10, 2003;
23(36):
11332 - 11341.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
