 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
Volume 17, Number 19, Issue of October 1, 1997 pp. 7503-7522
Copyright ©1997 Society for NeuroscienceDifferential Presynaptic Localization of Metabotropic Glutamate Receptor Subtypes in the Rat Hippocampus
Received March 28, 1997; revised July 14, 1997; accepted July 16, 1997.
Ryuichi Shigemoto1, Ayae Kinoshita1, Eiki Wada1, Sakashi Nomura3, Hitoshi Ohishi1, Masahiko Takada1, Peter J. Flor4, Akio Neki2, Takaaki Abe2, Shigetada Nakanishi2, and Noboru Mizuno1 Departments of 1 Morphological Brain Science and 2 Biological Sciences,
Faculty of Medicine, and 3 College of Medical Technology, Kyoto University, Kyoto 606, Japan, and 4 Novartis Pharma Inc., Nervous System Research, CH-4002 Basel, Switzerland Neurotransmission in the hippocampus is modulated variously through presynaptic metabotropic glutamate receptors (mGluRs). To establish the precise localization of presynaptic mGluRs in the rat hippocampus, we used subtype-specific antibodies for eight mGluRs (mGluR1-mGluR8) for immunohistochemistry combined with lesioning of the three major hippocampal pathways: the perforant path, mossy fiber, and Schaffer collateral. Immunoreactivity for group II (mGluR2) and group III (mGluR4a, mGluR7a, mGluR7b, and mGluR8) mGluRs was predominantly localized to presynaptic elements, whereas that for group I mGluRs (mGluR1 and mGluR5) was localized to postsynaptic elements. The medial perforant path was strongly immunoreactive for mGluR2 and mGluR7a throughout the hippocampus, and the lateral perforant path was prominently immunoreactive for mGluR8 in the dentate gyrus and CA3 area. The mossy fiber was labeled for mGluR2, mGluR7a, and mGluR7b, whereas the Schaffer collateral was labeled only for mGluR7a. Electron microscopy further revealed the spatial segregation of group II and group III mGluRs within presynaptic elements. Immunolabeling for the group III receptors was predominantly observed in presynaptic active zones of asymmetrical and symmetrical synapses, whereas that for the group II receptor (mGluR2) was found in preterminal rather than terminal portions of axons. Target cell-specific segregation of receptors, first reported for mGluR7a (), was also apparent for the other group III mGluRs, suggesting that transmitter release is differentially regulated by 2-amino-4-phosphonobutyrate-sensitive mGluRs in individual synapses on single axons according to the identity of postsynaptic neurons.
Key words: metabotropic glutamate receptor; hippocampus; perforant path; mossy fiber; Schaffer collateral; axon terminal; preterminal; immunohistochemistry; lesion
This article has been cited by other articles:
K. A. Pelkey and C. J. McBain
Target-cell-dependent plasticity within the mossy fibre-CA3 circuit reveals compartmentalized regulation of presynaptic function at divergent release sites
J. Physiol., March 15, 2008; 586(6): 1495 - 1502.
[Abstract] [Full Text] [PDF]
H. E. Speed and L. E. Dobrunz
Developmental Decrease in Short-Term Facilitation at Schaffer Collateral Synapses in Hippocampus Is mGluR1 Sensitive
J Neurophysiol, February 1, 2008; 99(2): 799 - 813.
[Abstract] [Full Text] [PDF]
A. Kumar and T. C. Foster
Shift in Induction Mechanisms Underlies an Age-Dependent Increase in DHPG-Induced Synaptic Depression at CA3 CA1 Synapses
J Neurophysiol, November 1, 2007; 98(5): 2729 - 2736.
[Abstract] [Full Text] [PDF]
T. Kirschstein, M. Bauer, L. Muller, C. Ruschenschmidt, M. Reitze, A. J. Becker, S. Schoch, and H. Beck
Loss of Metabotropic Glutamate Receptor-Dependent Long-Term Depression via Downregulation of mGluR5 after Status Epilepticus
J. Neurosci., July 18, 2007; 27(29): 7696 - 7704.
[Abstract] [Full Text] [PDF]
I. Marabese, F. Rossi, E. Palazzo, V. de Novellis, K. Starowicz, L. Cristino, D. Vita, L. Gatta, F. Guida, V. Di Marzo, et al.
Periaqueductal Gray Metabotropic Glutamate Receptor Subtype 7 and 8 Mediate Opposite Effects on Amino Acid Release, Rostral Ventromedial Medulla Cell Activities, and Thermal Nociception
J Neurophysiol, July 1, 2007; 98(1): 43 - 53.
[Abstract] [Full Text] [PDF]
P. J. Kammermeier and P. F. Worley
Homer 1a uncouples metabotropic glutamate receptor 5 from postsynaptic effectors
PNAS, April 3, 2007; 104(14): 6055 - 6060.
[Abstract] [Full Text] [PDF]
M. Trevino, C. Vivar, and R. Gutierrez
{beta}/{gamma} Oscillatory Activity in the CA3 Hippocampal Area is Depressed by Aberrant GABAergic Transmission from the Dentate Gyrus after Seizures
J. Neurosci., January 3, 2007; 27(1): 251 - 259.
[Abstract] [Full Text] [PDF]
C. Zhang and G. J. Marek
Group III Metabotropic Glutamate Receptor Agonists Selectively Suppress Excitatory Synaptic Currents in the Rat Prefrontal Cortex Induced by 5-Hydroxytryptamine2A Receptor Activation
J. Pharmacol. Exp. Ther., January 1, 2007; 320(1): 437 - 447.
[Abstract] [Full Text] [PDF]
W. Li and V. Neugebauer
Differential Changes of Group II and Group III mGluR Function in Central Amygdala Neurons in a Model of Arthritic Pain
J Neurophysiol, October 1, 2006; 96(4): 1803 - 1815.
[Abstract] [Full Text] [PDF]
D. A. Rusakov
Ca2+-Dependent Mechanisms of Presynaptic Control at Central Synapses
Neuroscientist, August 1, 2006; 12(4): 317 - 326.
[Abstract] [PDF]
C. M. Santi, G. Ferreira, B. Yang, V.-R. Gazula, A. Butler, A. Wei, L. K. Kaczmarek, and L. Salkoff
Opposite regulation of Slick and Slack K+ channels by neuromodulators.
J. Neurosci., May 10, 2006; 26(19): 5059 - 5068.
[Abstract] [Full Text] [PDF]
B. Capron, C. Sindic, E. Godaux, and L. Ris
The characteristics of LTP induced in hippocampal slices are dependent on slice-recovery conditions
Learn. Mem., May 1, 2006; 13(3): 271 - 277.
[Abstract] [Full Text] [PDF]
A. Kulik, I. Vida, Y. Fukazawa, N. Guetg, Y. Kasugai, C. L. Marker, F. Rigato, B. Bettler, K. Wickman, M. Frotscher, et al.
Compartment-dependent colocalization of Kir3.2-containing K+ channels and GABAB receptors in hippocampal pyramidal cells.
J. Neurosci., April 19, 2006; 26(16): 4289 - 4297.
[Abstract] [Full Text] [PDF]
R. E. Nicholls, X.-l. Zhang, C. P. Bailey, B. R. Conklin, E. R. Kandel, and P. K. Stanton
mGluR2 acts through inhibitory G{alpha} subunits to regulate transmission and long-term plasticity at hippocampal mossy fiber-CA3 synapses
PNAS, April 18, 2006; 103(16): 6380 - 6385.
[Abstract] [Full Text] [PDF]
L. J. Volk, C. A. Daly, and K. M. Huber
Differential Roles for Group 1 mGluR Subtypes in Induction and Expression of Chemically Induced Hippocampal Long-Term Depression
J Neurophysiol, April 1, 2006; 95(4): 2427 - 2438.
[Abstract] [Full Text] [PDF]
Z. Tang, O. E. Far, H. Betz, and A. Scheschonka
Pias1 Interaction and Sumoylation of Metabotropic Glutamate Receptor 8
J. Biol. Chem., November 18, 2005; 280(46): 38153 - 38159.
[Abstract] [Full Text] [PDF]
F. Ferraguti, T. Klausberger, P. Cobden, A. Baude, J. D. B. Roberts, P. Szucs, A. Kinoshita, R. Shigemoto, P. Somogyi, and Y. Dalezios
Metabotropic Glutamate Receptor 8-Expressing Nerve Terminals Target Subsets of GABAergic Neurons in the Hippocampus
J. Neurosci., November 9, 2005; 25(45): 10520 - 10536.
[Abstract] [Full Text] [PDF]
K. L. Brunson, E. Kramar, B. Lin, Y. Chen, L. L. Colgin, T. K. Yanagihara, G. Lynch, and T. Z. Baram
Mechanisms of Late-Onset Cognitive Decline after Early-Life Stress
J. Neurosci., October 12, 2005; 25(41): 9328 - 9338.
[Abstract] [Full Text] [PDF]
Y. Wu, R. Kawakami, Y. Shinohara, M. Fukaya, K. Sakimura, M. Mishina, M. Watanabe, I. Ito, and R. Shigemoto
Target-Cell-Specific Left-Right Asymmetry of NMDA Receptor Content in Schaffer Collateral Synapses in {epsilon}1/NR2A Knock-Out Mice
J. Neurosci., October 5, 2005; 25(40): 9213 - 9226.
[Abstract] [Full Text] [PDF]
M. Trevino and R. Gutierrez
The GABAergic projection of the dentate gyrus to hippocampal area CA3 of the rat: pre- and postsynaptic actions after seizures
J. Physiol., September 15, 2005; 567(3): 939 - 949.
[Abstract] [Full Text] [PDF]
C. Holscher, S. Schmid, P. K.D. Pilz, G. Sansig, H. van der Putten, and C. F. Plappert
Lack of the metabotropic glutamate receptor subtype 7 selectively modulates Theta rhythm and working memory
Learn. Mem., September 1, 2005; 12(5): 450 - 455.
[Abstract] [Full Text] [PDF]
B. Poschel, B. Wroblewska, U. Heinemann, and D. Manahan-Vaughan
The Metabotropic Glutamate Receptor mGluR3 is Critically Required for Hippocampal Long-term Depression and Modulates Long-term Potentiation in the Dentate Gyrus of Freely Moving Rats
Cereb Cortex, September 1, 2005; 15(9): 1414 - 1423.
[Abstract] [Full Text] [PDF]
G. M. Alexander and D. W. Godwin
Presynaptic Inhibition of Corticothalamic Feedback by Metabotropic Glutamate Receptors
J Neurophysiol, July 1, 2005; 94(1): 163 - 175.
[Abstract] [Full Text] [PDF]
J. Guo and S. R. Ikeda
Coupling of Metabotropic Glutamate Receptor 8 to N-Type Ca2+ Channels in Rat Sympathetic Neurons
Mol. Pharmacol., June 1, 2005; 67(6): 1840 - 1851.
[Abstract] [Full Text] [PDF]
J. Skov, S. Nedergaard, and M. Andreasen
New Type of Synaptically Mediated Epileptiform Activity Independent of Known Glutamate and GABA Receptors
J Neurophysiol, April 1, 2005; 93(4): 1845 - 1856.
[Abstract] [Full Text] [PDF]
B. Tu, O. Timofeeva, Y. Jiao, and J. V. Nadler
Spontaneous Release of Neuropeptide Y Tonically Inhibits Recurrent Mossy Fiber Synaptic Transmission in Epileptic Brain
J. Neurosci., February 16, 2005; 25(7): 1718 - 1729.
[Abstract] [Full Text] [PDF]
L. Yang, L. Mao, Q. Tang, S. Samdani, Z. Liu, and J. Q. Wang
A Novel Ca2+-Independent Signaling Pathway to Extracellular Signal-Regulated Protein Kinase by Coactivation of NMDA Receptors and Metabotropic Glutamate Receptor 5 in Neurons
J. Neurosci., December 1, 2004; 24(48): 10846 - 10857.
[Abstract] [Full Text] [PDF]
L. Bogdanik, R. Mohrmann, A. Ramaekers, J. Bockaert, Y. Grau, K. Broadie, and M.-L. Parmentier
The Drosophila Metabotropic Glutamate Receptor DmGluRA Regulates Activity-Dependent Synaptic Facilitation and Fine Synaptic Morphology
J. Neurosci., October 13, 2004; 24(41): 9105 - 9116.
[Abstract] [Full Text] [PDF]
K. J. Bough, D. D. Mott, and R. J. Dingledine
Medial Perforant Path Inhibition Mediated by mGluR7 Is Reduced After Status Epilepticus
J Neurophysiol, September 1, 2004; 92(3): 1549 - 1557.
[Abstract] [Full Text] [PDF]
D. A. Rusakov, A. Wuerz, and D. M. Kullmann
Heterogeneity and Specificity of Presynaptic Ca2+ Current Modulation by mGluRs at Individual Hippocampal Synapses
Cereb Cortex, July 1, 2004; 14(7): 748 - 758.
[Abstract] [Full Text] [PDF]
T. A. Simeone, R. M. Sanchez, and J. M. Rho
Molecular Biology and Ontogeny of Glutamate Receptors in the Mammalian Central Nervous System
J Child Neurol, May 1, 2004; 19(5): 343 - 360.
[Abstract] [PDF]
C. Acuna-Goycolea, Y. Li, and A. N. van den Pol
Group III Metabotropic Glutamate Receptors Maintain Tonic Inhibition of Excitatory Synaptic Input to Hypocretin/Orexin Neurons
J. Neurosci., March 24, 2004; 24(12): 3013 - 3022.
[Abstract] [Full Text] [PDF]
V. Lapointe, F. Morin, S. Ratte, A. Croce, F. Conquet, and J.-C. Lacaille
Synapse-specific mGluR1-dependent long-term potentiation in interneurones regulates mouse hippocampal inhibition
J. Physiol., February 15, 2004; 555(1): 125 - 135.
[Abstract] [Full Text] [PDF]
K. Naie and D. Manahan-Vaughan
Regulation by Metabotropic Glutamate Receptor 5 of LTP in the Dentate Gyrus of Freely Moving Rats: Relevance for Learning and Memory Formation
Cereb Cortex, February 1, 2004; 14(2): 189 - 198.
[Abstract] [Full Text] [PDF]
E. R. Garrido Sanabria, K. M. Wozniak, B. S. Slusher, and A. Keller
GCP II (NAALADase) Inhibition Suppresses Mossy Fiber-CA3 Synaptic Neurotransmission by a Presynaptic Mechanism
J Neurophysiol, January 1, 2004; 91(1): 182 - 193.
[Abstract] [Full Text]
J. J. Lawrence, Z. M. Grinspan, and C. J. McBain
Quantal transmission at mossy fibre targets in the CA3 region of the rat hippocampus
J. Physiol., January 1, 2004; 554(1): 175 - 193.
[Abstract] [Full Text] [PDF]
C. Croci, H. Sticht, J. H. Brandstatter, and R. Enz
Group I Metabotropic Glutamate Receptors Bind to Protein Phosphatase 1C: MAPPING AND MODELING OF INTERACTING SEQUENCES
J. Biol. Chem., December 12, 2003; 278(50): 50682 - 50690.
[Abstract] [Full Text] [PDF]
A. Kulik, I. Vida, R. Lujan, C. A. Haas, G. Lopez-Bendito, R. Shigemoto, and M. Frotscher
Subcellular Localization of Metabotropic GABAB Receptor Subunits GABAB1a/b and GABAB2 in the Rat Hippocampus
J. Neurosci., December 3, 2003; 23(35): 11026 - 11035.
[Abstract] [Full Text] [PDF]
R. Stoop, F. Conquet, B. Zuber, L. L. Voronin, and E. Pralong
Activation of Metabotropic Glutamate 5 and NMDA Receptors Underlies the Induction of Persistent Bursting and Associated Long-Lasting Changes in CA3 Recurrent Connections
J. Neurosci., July 2, 2003; 23(13): 5634 - 5644.
[Abstract] [Full Text] [PDF]
J. Kitano, M. Nishida, Y. Itsukaichi, I. Minami, M. Ogawa, T. Hirano, Y. Mori, and S. Nakanishi
Direct Interaction and Functional Coupling between Metabotropic Glutamate Receptor Subtype 1 and Voltage-sensitive Cav2.1 Ca2+ Channel
J. Biol. Chem., June 27, 2003; 278(27): 25101 - 25108.
[Abstract] [Full Text] [PDF]
C. Millan, E. Castro, M. Torres, R. Shigemoto, and J. Sanchez-Prieto
Co-expression of Metabotropic Glutamate Receptor 7 and N-type Ca2+ Channels in Single Cerebrocortical Nerve Terminals of Adult Rats
J. Biol. Chem., June 20, 2003; 278(26): 23955 - 23962.
[Abstract] [Full Text] [PDF]
L. Feng, P. Molnar, and J. V. Nadler
Short-Term Frequency-Dependent Plasticity at Recurrent Mossy Fiber Synapses of the Epileptic Brain
J. Neurosci., June 15, 2003; 23(12): 5381 - 5390.
[Abstract] [Full Text] [PDF]
H. Romo-Parra, C. Vivar, J. Maqueda, M. A. Morales, and R. Gutierrez
Activity-Dependent Induction of Multitransmitter Signaling Onto Pyramidal Cells and Interneurons of Hippocampal Area CA3
J Neurophysiol, June 1, 2003; 89(6): 3155 - 3167.
[Abstract] [Full Text] [PDF]
R. Kawakami, Y. Shinohara, Y. Kato, H. Sugiyama, R. Shigemoto, and I. Ito
Asymmetrical Allocation of NMDA Receptor {epsilon}2 Subunits in Hippocampal Circuitry
Science, May 9, 2003; 300(5621): 990 - 994.
[Abstract] [Full Text] [PDF]
H. Lavreysen, C. Janssen, F. Bischoff, X. Langlois, J. E. Leysen, and A. S. J. Lesage
[3H]R214127: A Novel High-Affinity Radioligand for the mGlu1 Receptor Reveals a Common Binding Site Shared by Multiple Allosteric Antagonists
Mol. Pharmacol., May 1, 2003; 63(5): 1082 - 1093.
[Abstract] [Full Text] [PDF]
A. Losonczy, P. Somogyi, and Z. Nusser
Reduction of Excitatory Postsynaptic Responses by Persistently Active Metabotropic Glutamate Receptors in the Hippocampus
J Neurophysiol, April 1, 2003; 89(4): 1910 - 1919.
[Abstract] [Full Text] [PDF]
D. L. Taylor, L. T. Diemel, and J. M. Pocock
Activation of Microglial Group III Metabotropic Glutamate Receptors Protects Neurons against Microglial Neurotoxicity
J. Neurosci., March 15, 2003; 23(6): 2150 - 2160.
[Abstract] [Full Text] [PDF]
W.-J. Gao and P. S. Goldman-Rakic
Selective modulation of excitatory and inhibitory microcircuits by dopamine
PNAS, March 4, 2003; 100(5): 2836 - 2841.
[Abstract] [Full Text] [PDF]
C. Millan, R. Lujan, R. Shigemoto, and J. Sanchez-Prieto
Subtype-specific Expression of Group III Metabotropic Glutamate Receptors and Ca2+ Channels in Single Nerve Terminals
J. Biol. Chem., November 27, 2002; 277(49): 47796 - 47803.
[Abstract] [Full Text] [PDF]
P. Benquet, C. E. Gee, and U. Gerber
Two Distinct Signaling Pathways Upregulate NMDA Receptor Responses via Two Distinct Metabotropic Glutamate Receptor Subtypes
J. Neurosci., November 15, 2002; 22(22): 9679 - 9686.
[Abstract] [Full Text] [PDF]
M. Miura, M. Watanabe, S. Offermanns, M. I. Simon, and M. Kano
Group I Metabotropic Glutamate Receptor Signaling via Galpha q/Galpha 11 Secures the Induction of Long-Term Potentiation in the Hippocampal Area CA1
J. Neurosci., October 1, 2002; 22(19): 8379 - 8390.
[Abstract] [Full Text] [PDF]
Y. Dalezios, R. Lujan, R. Shigemoto, J. D. B. Roberts, and P. Somogyi
Enrichment of mGluR7a in the Presynaptic Active Zones of GABAergic and Non-GABAergic Terminals on Interneurons in the Rat Somatosensory Cortex
Cereb Cortex, September 1, 2002; 12(9): 961 - 974.
[Abstract] [Full Text] [PDF]
A. M. Rush, J. Wu, M. J. Rowan, and R. Anwyl
Group I Metabotropic Glutamate Receptor (mGluR)-Dependent Long-Term Depression Mediated via p38 Mitogen-Activated Protein Kinase Is Inhibited by Previous High-Frequency Stimulation and Activation of mGluRs and Protein Kinase C in the Rat Dentate Gyrus In Vitro
J. Neurosci., July 15, 2002; 22(14): 6121 - 6128.
[Abstract] [Full Text] [PDF]
D. R. Ireland and W. C. Abraham
Group I mGluRs Increase Excitability of Hippocampal CA1 Pyramidal Neurons by a PLC-Independent Mechanism
J Neurophysiol, July 1, 2002; 88(1): 107 - 116.
[Abstract] [Full Text] [PDF]
S. M. Rodrigues, E. P. Bauer, C. R. Farb, G. E. Schafe, and J. E. LeDoux
The Group I Metabotropic Glutamate Receptor mGluR5 Is Required for Fear Memory Formation and Long-Term Potentiation in the Lateral Amygdala
J. Neurosci., June 15, 2002; 22(12): 5219 - 5229.
[Abstract] [Full Text] [PDF]
G. Lopez-Bendito, R. Shigemoto, A. Fairen, and R. Lujan
Differential Distribution of Group I Metabotropic Glutamate Receptors during Rat Cortical Development
Cereb Cortex, June 1, 2002; 12(6): 625 - 638.
[Abstract] [Full Text] [PDF]
S. D. Sorensen, T. A. Macek, Z. Cai, J. A. Saugstad, and P. J. Conn
Dissociation of Protein Kinase-Mediated Regulation of Metabotropic Glutamate Receptor 7 (mGluR7) Interactions with Calmodulin and Regulation of mGluR7 Function
Mol. Pharmacol., June 1, 2002; 61(6): 1303 - 1312.
[Abstract] [Full Text] [PDF]
Q. Tong, R. Ouedraogo, and A. L. Kirchgessner
Localization and function of group III metabotropic glutamate receptors in rat pancreatic islets
Am J Physiol Endocrinol Metab, June 1, 2002; 282(6): E1324 - E1333.
