 |
Previous Article | Next Article 
The Journal of Neuroscience, January 15, 1999, 19(2):653-663
Kainate Receptor-Mediated Responses in the CA1 Field of Wild-Type
and GluR6-Deficient Mice
Ingrid
Bureau1,
Serge
Bischoff2,
Steve F.
Heinemann3, and
Christophe
Mulle1
1 Centre National de la Recherche Scientifique,
Université Victor Segalen, Bordeaux 33076, France,
2 Novartis, CH-4002, Basel, Switzerland, and
3 Molecular Neurobiology Laboratory, The Salk Institute for
Biological Studies, La Jolla, California 92037
Kainate receptors are abundantly expressed in the hippocampus. Mice
with disruption of kainate receptor subunits allow the genetic
dissection of the role of each kainate receptor subunits in the
synaptic physiology of the hippocampus, as well as in excitotoxic processes. We have compared the action of domoate and kainate on CA1
pyramidal neurons in slices from wild-type and GluR6 / mice. The
difference in the amplitude of inward currents evoked by domoate and
kainate between wild-type and GluR6 / mice demonstrates the presence
of functional kainate receptors in CA1 pyramidal neurons. Block of
domoate-activated inward currents by the AMPA receptor
antagonists
2,3-dihydroxy-6-nitro-7-sulfonyl-benzo(F)quinoxaline (1 µM) and
1-(4-aminophenyl)-3-methylcarbamyl-4-methyl7,8-methylenedioxy-3,4-dihydro-5H-2,3-benzodiazepine) (GYKI 53655) (50 µM) is complete in
GluR6 / mice but only partial in wild-type mice. In the presence of
GYKI 53655, kainate receptor activation dramatically increases the
frequency of spontaneous IPSCs in CA1 pyramidal cells from wild-type,
as well as GluR6 / , mice. This results from the kainate
receptor-mediated activation of a sustained inward current and an
increased action potential firing in afferent GABAergic interneurons of
the CA1 field. These effects are observed in wild-type, as well as
GluR6 / , mice. Kainate receptors also decrease the amplitude of
evoked IPSCs in CA1 pyramidal cells by increasing synaptic failures in
wild-type and GluR6 / mice. These results indicate that in CA1
pyramidal cells, distinct subtypes of kainate receptors mediate several functionally antagonistic effects.
Key words:
kainate receptors; GluR6 knock-out mouse; CA1 pyramidal
cells; CA1 interneurons; NBQX; GYKI 53655
Copyright © 1999 Society for Neuroscience 0270-6474/99/192653-11$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
F. Crepel
Role of Presynaptic Kainate Receptors at Parallel Fiber-Purkinje Cell Synapses in Induction of Cerebellar LTD: Interplay With Climbing Fiber Input
J Neurophysiol,
August 1, 2009;
102(2):
965 - 973.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Miyata and K. Imoto
Contrary roles of kainate receptors in transmitter release at corticothalamic synapses onto thalamic relay and reticular neurons
J. Physiol.,
March 1, 2009;
587(5):
999 - 1012.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Y. Sun, A. F. Bartley, and L. E. Dobrunz
Calcium-Permeable Presynaptic Kainate Receptors Involved in Excitatory Short-Term Facilitation Onto Somatostatin Interneurons During Natural Stimulus Patterns
J Neurophysiol,
February 1, 2009;
101(2):
1043 - 1055.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Oren, W. Nissen, D. M. Kullmann, P. Somogyi, and K. P. Lamsa
Role of Ionotropic Glutamate Receptors in Long-Term Potentiation in Rat Hippocampal CA1 Oriens-Lacunosum Moleculare Interneurons
J. Neurosci.,
January 28, 2009;
29(4):
939 - 950.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Wondolowski and M. Frerking
Subunit-Dependent Postsynaptic Expression of Kainate Receptors on Hippocampal Interneurons in Area CA1
J. Neurosci.,
January 14, 2009;
29(2):
563 - 574.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Xu, Y. Liu, and G.-Y. Zhang
Neuroprotection of GluR5-containing Kainate Receptor Activation against Ischemic Brain Injury through Decreasing Tyrosine Phosphorylation of N-Methyl-D-aspartate Receptors Mediated by Src Kinase
J. Biol. Chem.,
October 24, 2008;
283(43):
29355 - 29366.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. M. Kullmann and K. Lamsa
Roles of distinct glutamate receptors in induction of anti-Hebbian long-term potentiation
J. Physiol.,
March 15, 2008;
586(6):
1481 - 1486.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Tomita, R. K. Byrd, N. Rouach, C. Bellone, A. Venegas, J. L. O'Brien, K. S. Kim, O. Olsen, R. A. Nicoll, and D. S. Bredt
AMPA receptors and stargazin-like transmembrane AMPA receptor-regulatory proteins mediate hippocampal kainate neurotoxicity
PNAS,
November 20, 2007;
104(47):
18784 - 18788.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Crepel and H. Daniel
Developmental Changes in Agonist-Induced Retrograde Signaling at Parallel Fiber Purkinje Cell Synapses: Role of Calcium-Induced Calcium Release
J Neurophysiol,
November 1, 2007;
98(5):
2550 - 2565.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Goldin, J. Epsztein, I. Jorquera, A. Represa, Y. Ben-Ari, V. Crepel, and R. Cossart
Synaptic Kainate Receptors Tune Oriens-Lacunosum Moleculare Interneurons to Operate at Theta Frequency
J. Neurosci.,
September 5, 2007;
27(36):
9560 - 9572.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. S. Pinheiro, D. Perrais, F. Coussen, J. Barhanin, B. Bettler, J. R. Mann, J. O. Malva, S. F. Heinemann, and C. Mulle
GluR7 is an essential subunit of presynaptic kainate autoreceptors at hippocampal mossy fiber synapses
PNAS,
July 17, 2007;
104(29):
12181 - 12186.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Ren, Y. Yoshimura, N. Takada, S. Horibe, and Y. Komatsu
Specialized Inhibitory Synaptic Actions Between Nearby Neocortical Pyramidal Neurons
Science,
May 4, 2007;
316(5825):
758 - 761.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Lang, C. Bohmer, M. Palmada, G. Seebohm, N. Strutz-Seebohm, and V. Vallon
(Patho)physiological Significance of the Serum- and Glucocorticoid-Inducible Kinase Isoforms.
Physiol Rev,
October 1, 2006;
86(4):
1151 - 1178.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L.-R. Shao and F. E. Dudek
Changes in mIPSCs and sIPSCs After Kainate Treatment: Status Epilepticus-Induced Neuronal Loss or Direct Activation of Kainate Receptors?
J Neurophysiol,
August 1, 2006;
96(2):
961 - 962.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X.-M. Liu, D.-S. Pei, Q.-H. Guan, Y.-F. Sun, X.-T. Wang, Q.-X. Zhang, and G.-Y. Zhang
Neuroprotection of Tat-GluR6-9c against Neuronal Death Induced by Kainate in Rat Hippocampus via Nuclear and Non-nuclear Pathways
J. Biol. Chem.,
June 23, 2006;
281(25):
17432 - 17445.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Gebhardt and S. G. Cull-Candy
Influence of agonist concentration on AMPA and kainate channels in CA1 pyramidal cells in rat hippocampal slices
J. Physiol.,
June 1, 2006;
573(2):
371 - 394.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D.-S. Pei, X.-T. Wang, Y. Liu, Y.-F. Sun, Q.-H. Guan, W. Wang, J.-Z. Yan, Y.-Y. Zong, T.-L. Xu, and G.-Y. Zhang
Neuroprotection against ischaemic brain injury by a GluR6-9c peptide containing the TAT protein transduction sequence
Brain,
February 1, 2006;
129(2):
465 - 479.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Qiu, C. W. Pak, and M. C. Curras-Collazo
Sequential Involvement of Distinct Glutamate Receptors in Domoic Acid-Induced Neurotoxicity in Rat Mixed Cortical Cultures: Effect of Multiple Dose/Duration Paradigms, Chronological Age, and Repeated Exposure
Toxicol. Sci.,
January 1, 2006;
89(1):
243 - 256.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Epsztein, A. Represa, I. Jorquera, Y. Ben-Ari, and V. Crepel
Recurrent Mossy Fibers Establish Aberrant Kainate Receptor-Operated Synapses on Granule Cells from Epileptic Rats
J. Neurosci.,
September 7, 2005;
25(36):
8229 - 8239.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L.-J. Wu, M.-G. Zhao, H. Toyoda, S. W. Ko, and M. Zhuo
Kainate Receptor-Mediated Synaptic Transmission in the Adult Anterior Cingulate Cortex
J Neurophysiol,
September 1, 2005;
94(3):
1805 - 1813.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Maingret, S. E Lauri, T. Taira, and J. T. R Isaac
Profound regulation of neonatal CA1 rat hippocampal GABAergic transmission by functionally distinct kainate receptor populations
J. Physiol.,
August 15, 2005;
567(1):
131 - 142.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Jaskolski, E. Normand, C. Mulle, and F. Coussen
Differential Trafficking of GluR7 Kainate Receptor Subunit Splice Variants
J. Biol. Chem.,
June 17, 2005;
280(24):
22968 - 22976.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Strutz-Seebohm, G. Seebohm, E. Shumilina, A. F. Mack, H.-J. Wagner, A. Lampert, F. Grahammer, G. Henke, L. Just, T. Skutella, et al.
Glucocorticoid adrenal steroids and glucocorticoid-inducible kinase isoforms in the regulation of GluR6 expression
J. Physiol.,
June 1, 2005;
565(2):
391 - 401.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Fisahn
Kainate receptors and rhythmic activity in neuronal networks: hippocampal gamma oscillations as a tool
J. Physiol.,
January 1, 2005;
562(1):
65 - 72.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Fisahn, A. Contractor, R. D. Traub, E. H. Buhl, S. F. Heinemann, and C. J. McBain
Distinct Roles for the Kainate Receptor Subunits GluR5 and GluR6 in Kainate-Induced Hippocampal Gamma Oscillations
J. Neurosci.,
October 27, 2004;
24(43):
9658 - 9668.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. K. Christensen, A. V. Paternain, S. Selak, P. K. Ahring, and J. Lerma
A Mosaic of Functional Kainate Receptors in Hippocampal Interneurons
J. Neurosci.,
October 13, 2004;
24(41):
8986 - 8993.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Kang, L. Jiang, W. He, J. Xu, M. Nedergaard, and J. Kang
Presynaptic Inactivation of Action Potentials and Postsynaptic Inhibition of GABAA Currents Contribute to KA-Induced Disinhibition in CA1 Pyramidal Neurons
J Neurophysiol,
August 1, 2004;
92(2):
873 - 882.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Melyan, B. Lancaster, and H. V. Wheal
Metabotropic Regulation of Intrinsic Excitability by Synaptic Activation of Kainate Receptors
J. Neurosci.,
May 12, 2004;
24(19):
4530 - 4534.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D.-h. Youn and M. Randic
Modulation of excitatory synaptic transmission in the spinal substantia gelatinosa of mice deficient in the kainate receptor GluR5 and/or GluR6 subunit
J. Physiol.,
March 15, 2004;
555(3):
683 - 698.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Frerking
When astrocytes signal, kainate receptors respond
PNAS,
March 2, 2004;
101(9):
2649 - 2650.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Q.-s. Liu, Q. Xu, G. Arcuino, J. Kang, and M. Nedergaard
From The Cover: Astrocyte-mediated activation of neuronal kainate receptors
PNAS,
March 2, 2004;
101(9):
3172 - 3177.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. A. Zappone and R. S. Sloviter
Translamellar Disinhibition in the Rat Hippocampal Dentate Gyrus after Seizure-Induced Degeneration of Vulnerable Hilar Neurons
J. Neurosci.,
January 28, 2004;
24(4):
853 - 864.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Morante-Oria, A. Carleton, B. Ortino, E. J. Kremer, A. Fairen, and P.-M. Lledo
Subpallial origin of a population of projecting pioneer neurons during corticogenesis
PNAS,
October 14, 2003;
100(21):
12468 - 12473.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Darstein, R. S. Petralia, G. T. Swanson, R. J. Wenthold, and S. F. Heinemann
Distribution of Kainate Receptor Subunits at Hippocampal Mossy Fiber Synapses
J. Neurosci.,
September 3, 2003;
23(22):
8013 - 8019.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Eder, K. Becker, G. Rammes, A. Schierloh, S. C. Azad, W. Zieglgansberger, and H.-U. Dodt
Distribution and Properties of Functional Postsynaptic Kainate Receptors on Neocortical Layer V Pyramidal Neurons
J. Neurosci.,
July 23, 2003;
23(16):
6660 - 6670.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Carta, O. J. Ariwodola, J. L. Weiner, and C. F. Valenzuela
Alcohol potently inhibits the kainate receptor-dependent excitatory drive of hippocampal interneurons
PNAS,
May 27, 2003;
100(11):
6813 - 6818.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Contractor, A. W. Sailer, M. Darstein, C. Maron, J. Xu, G. T. Swanson, and S. F. Heinemann
Loss of Kainate Receptor-Mediated Heterosynaptic Facilitation of Mossy-Fiber Synapses in KA2-/- Mice
J. Neurosci.,
January 15, 2003;
23(2):
422 - 429.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. L. Crowder, O. J. Ariwodola, and J. L. Weiner
Ethanol Antagonizes Kainate Receptor-Mediated Inhibition of Evoked GABAA Inhibitory Postsynaptic Currents in the Rat Hippocampal CA1 Region
J. Pharmacol. Exp. Ther.,
December 1, 2002;
303(3):
937 - 944.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. A. Kerchner, T. J. Wilding, J. E. Huettner, and M. Zhuo
Kainate Receptor Subunits Underlying Presynaptic Regulation of Transmitter Release in the Dorsal Horn
J. Neurosci.,
September 15, 2002;
22(18):
8010 - 8017.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Coussen, E. Normand, C. Marchal, P. Costet, D. Choquet, M. Lambert, R.-M. Mege, and C. Mulle
Recruitment of the Kainate Receptor Subunit Glutamate Receptor 6 by Cadherin/Catenin Complexes
J. Neurosci.,
August 1, 2002;
22(15):
6426 - 6436.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. L. Crowder and J. L. Weiner
Functional Characterization of Kainate Receptors in the Rat Nucleus Accumbens Core Region
J Neurophysiol,
July 1, 2002;
88(1):
41 - 48.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Khalilov, J. Hirsch, R. Cossart, and Y. Ben-Ari
Paradoxical Anti-Epileptic Effects of a GluR5 Agonist of Kainate Receptors
J Neurophysiol,
July 1, 2002;
88(1):
523 - 527.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Lerma, A. V. Paternain, A. Rodriguez-Moreno, and J. C. Lopez-Garcia
Molecular Physiology of Kainate Receptors
Physiol Rev,
July 1, 2001;
81(3):
971 - 998.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Frerking, D. Schmitz, Q. Zhou, J. Johansen, and R. A. Nicoll
Kainate Receptors Depress Excitatory Synaptic Transmission at CA3{right-arrow}CA1 Synapses in the Hippocampus via a Direct Presynaptic Action
J. Neurosci.,
May 1, 2001;
21(9):
2958 - 2966.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. B. Ali, J. Rossier, J. F. Staiger, and E. Audinat
Kainate Receptors Regulate Unitary IPSCs Elicited in Pyramidal Cells by Fast-Spiking Interneurons in the Neocortex
J. Neurosci.,
May 1, 2001;
21(9):
2992 - 2999.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. J Wilding and J. E Huettner
Functional diversity and developmental changes in rat neuronal kainate receptors
J. Physiol.,
April 15, 2001;
532(2):
411 - 421.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Contractor, G. T. Swanson, A. Sailer, S. O'Gorman, and S. F. Heinemann
Identification of the Kainate Receptor Subunits Underlying Modulation of Excitatory Synaptic Transmission in the CA3 Region of the Hippocampus
J. Neurosci.,
November 15, 2000;
20(22):
8269 - 8278.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Bureau, S. Dieudonne, F. Coussen, and C. Mulle
Kainate receptor-mediated synaptic currents in cerebellar Golgi cells are not shaped by diffusion of glutamate
PNAS,
June 6, 2000;
97(12):
6838 - 6843.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Chergui, A. Bouron, E. Normand, and C. Mulle
Functional GluR6 Kainate Receptors in the Striatum: Indirect Downregulation of Synaptic Transmission
J. Neurosci.,
March 15, 2000;
20(6):
2175 - 2182.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Frerking, C. C. H. Petersen, and R. A. Nicoll
Mechanisms underlying kainate receptor-mediated disinhibition in the hippocampus
PNAS,
October 26, 1999;
96(22):
12917 - 12922.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Cui and M. L. Mayer
Heteromeric Kainate Receptors Formed by the Coassembly of GluR5, GluR6, and GluR7
J. Neurosci.,
October 1, 1999;
19(19):
8281 - 8291.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M.-Y. Min, Z. Melyan, and D. M. Kullmann
Synaptically released glutamate reduces gamma -aminobutyric acid (GABA)ergic inhibition in the hippocampus via kainate receptors
PNAS,
August 17, 1999;
96(17):
9932 - 9937.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|

|