 |
Previous Article | Next Article 
Volume 17, Number 2,
Issue of January 15, 1997
pp. 834-842
Copyright ©1997 Society for Neuroscience
Differential Localization of Glutamate Receptors in the Rat
Cerebellum: Coexpression with AMPA Receptors in Parallel
Fiber-Spine Synapses and Absence from Climbing Fiber-Spine
Synapses
Received Sept. 3, 1996; revised Oct. 23, 1996; accepted Nov. 5, 1996.
Alf Sommer Landsend1,
Mahmood Amiry-Moghaddam1,
Atsushi Matsubara2,
Linda Bergersen1,
Shin-ichi Usami2,
Robert J. Wenthold3, and
Ole P. Ottersen1
1 Department of Anatomy, Institute of Basic Medical
Sciences, University of Oslo, N-0317 Oslo, Norway,
2 Department of Otorhinolaryngology, Hirosaki University
School of Medicine, Hirosaki 036, Japan, and 3 Laboratory
of Neurochemistry, National Institute on Deafness and Other
Communication Disorders, National Institutes of Health, Bethesda,
Maryland 20892
The 2 glutamate receptors are prominently expressed in Purkinje
cells and are thought to play a key role in the induction of cerebellar
long-term depression. The synaptic and subsynaptic localization of receptors in rat cerebellar cortex was investigated with sensitive and
high-resolution immunogold procedures. After postembedding incubation
with an antibody raised to a C-terminal peptide of 2, high gold
particle densities occurred in all parallel fiber synapses with
Purkinje cell dendritic spines, whereas other synapses were
consistently devoid of labeling. Among the types of immunonegative
synapse were climbing fiber synapses with spines and parallel fiber
synapses with dendritic stems of interneurons. At the parallel
fiber-spine synapse, gold particles signaling receptors were
restricted to the postsynaptic specialization. By the use of double
labeling with two different gold particle sizes, it was shown that and AMPA GluR2/3 receptors were colocalized along the entire extent of
the postsynaptic specialization without forming separate domains. The
distribution of gold particles representing receptors was
consistent with a cytoplasmic localization of the C terminus and an
absence of a significant presynaptic pool of receptor molecules. The
present data suggest that the 2 receptors are targeted selectively
to a subset of Purkinje cell spines and that they are coexpressed with
ionotropic receptors in the postsynaptic specialization. This
arrangement could allow for a direct interaction between the two
classes of receptor.
Key words:
immunogold;
glutamate receptor;
freeze substitution;
colocalization;
synapse;
cerebellum
This article has been cited by other articles:

|
 |

|
 |
 
W. Kakegawa, T. Miyazaki, K. Kohda, K. Matsuda, K. Emi, J. Motohashi, M. Watanabe, and M. Yuzaki
The N-Terminal Domain of GluD2 (GluR{delta}2) Recruits Presynaptic Terminals and Regulates Synaptogenesis in the Cerebellum In Vivo
J. Neurosci.,
May 6, 2009;
29(18):
5738 - 5748.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. B. Hansen, P. Naur, N. L. Kurtkaya, A. S. Kristensen, M. Gajhede, J. S. Kastrup, and S. F. Traynelis
Modulation of the Dimer Interface at Ionotropic Glutamate-Like Receptor {delta}2 by D-Serine and Extracellular Calcium
J. Neurosci.,
January 28, 2009;
29(4):
907 - 917.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Kano, K. Hashimoto, and T. Tabata
Type-1 metabotropic glutamate receptor in cerebellar Purkinje cells: a key molecule responsible for long-term depression, endocannabinoid signalling and synapse elimination
Phil Trans R Soc B,
June 27, 2008;
363(1500):
2173 - 2186.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Kakegawa, T. Miyazaki, K. Emi, K. Matsuda, K. Kohda, J. Motohashi, M. Mishina, S. Kawahara, M. Watanabe, and M. Yuzaki
Differential Regulation of Synaptic Plasticity and Cerebellar Motor Learning by the C-Terminal PDZ-Binding Motif of GluR{delta}2
J. Neurosci.,
February 6, 2008;
28(6):
1460 - 1468.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Uemura, S. Kakizawa, M. Yamasaki, K. Sakimura, M. Watanabe, M. Iino, and M. Mishina
Regulation of Long-Term Depression and Climbing Fiber Territory by Glutamate Receptor {delta}2 at Parallel Fiber Synapses through its C-Terminal Domain in Cerebellar Purkinje Cells
J. Neurosci.,
October 31, 2007;
27(44):
12096 - 12108.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Kakegawa, K. Kohda, and M. Yuzaki
The {delta}2 'ionotropic' glutamate receptor functions as a non-ionotropic receptor to control cerebellar synaptic plasticity
J. Physiol.,
October 1, 2007;
584(1):
89 - 96.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. K. Osswald, A. Galan, and D. Bowie
Light triggers expression of philanthotoxin-insensitive Ca2+-permeable AMPA receptors in the developing rat retina
J. Physiol.,
July 1, 2007;
582(1):
95 - 111.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Masugi-Tokita, E. Tarusawa, M. Watanabe, E. Molnar, K. Fujimoto, and R. Shigemoto
Number and Density of AMPA Receptors in Individual Synapses in the Rat Cerebellum as Revealed by SDS-Digested Freeze-Fracture Replica Labeling
J. Neurosci.,
February 21, 2007;
27(8):
2135 - 2144.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Bao, Z. Pang, M. A. Morgan, J. Parris, Y. Rong, L. Li, and J. I. Morgan
Cbln1 Is Essential for Interaction-Dependent Secretion of Cbln3
Mol. Cell. Biol.,
December 15, 2006;
26(24):
9327 - 9337.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Matsuda, K. Matsuda, and M. Yuzaki
A New Motif Necessary and Sufficient for Stable Localization of the {delta}2 Glutamate Receptors at Postsynaptic Spines
J. Biol. Chem.,
June 23, 2006;
281(25):
17501 - 17509.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Yawata, H. Tsuchida, M. Kengaku, and T. Hirano
Membrane-proximal region of glutamate receptor delta2 subunit is critical for long-term depression and interaction with protein interacting with C kinase 1 in a cerebellar Purkinje neuron.
J. Neurosci.,
April 5, 2006;
26(14):
3626 - 3633.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Cubelos, C. Gimenez, and F. Zafra
Localization of the GLYT1 Glycine Transporter at Glutamatergic Synapses in the Rat Brain
Cereb Cortex,
April 1, 2005;
15(4):
448 - 459.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Takeuchi, T. Miyazaki, M. Watanabe, H. Mori, K. Sakimura, and M. Mishina
Control of Synaptic Connection by Glutamate Receptor {delta}2 in the Adult Cerebellum
J. Neurosci.,
February 23, 2005;
25(8):
2146 - 2156.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Miyazaki, K. Hashimoto, H.-S. Shin, M. Kano, and M. Watanabe
P/Q-Type Ca2+ Channel {alpha}1A Regulates Synaptic Competition on Developing Cerebellar Purkinje Cells
J. Neurosci.,
February 18, 2004;
24(7):
1734 - 1743.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Evinger and J. S. Perlmutter
Blind men and blinking elephants
Neurology,
June 10, 2003;
60(11):
1732 - 1733.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Cesa, L. Morando, and P. Strata
Glutamate Receptor delta 2 Subunit in Activity-Dependent Heterologous Synaptic Competition
J. Neurosci.,
March 15, 2003;
23(6):
2363 - 2370.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Sekerkova, P. A. Loomis, B. Changyaleket, L. Zheng, R. Eytan, B. Chen, E. Mugnaini, and J. R. Bartles
Novel Espin Actin-Bundling Proteins Are Localized to Purkinje Cell Dendritic Spines and Bind the Src Homology 3 Adapter Protein Insulin Receptor Substrate p53
J. Neurosci.,
February 15, 2003;
23(4):
1310 - 1319.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Ichikawa, T. Miyazaki, M. Kano, T. Hashikawa, H. Tatsumi, K. Sakimura, M. Mishina, Y. Inoue, and M. Watanabe
Distal Extension of Climbing Fiber Territory and Multiple Innervation Caused by Aberrant Wiring to Adjacent Spiny Branchlets in Cerebellar Purkinje Cells Lacking Glutamate Receptor delta 2
J. Neurosci.,
October 1, 2002;
22(19):
8487 - 8503.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Mi, X. Tang, R. Sutter, D. Xu, P. Worley, and R. J. O'Brien
Differing Mechanisms for Glutamate Receptor Aggregation on Dendritic Spines and Shafts in Cultured Hippocampal Neurons
J. Neurosci.,
September 1, 2002;
22(17):
7606 - 7616.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. R. Carter, C. Chen, P. M. Schwartz, and R. A. Segal
Brain-Derived Neurotrophic Factor Modulates Cerebellar Plasticity and Synaptic Ultrastructure
J. Neurosci.,
February 15, 2002;
22(4):
1316 - 1327.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Miyagi, T. Yamashita, M. Fukaya, T. Sonoda, T. Okuno, K. Yamada, M. Watanabe, Y. Nagashima, I. Aoki, K. Okuda, et al.
Delphilin: a Novel PDZ and Formin Homology Domain-Containing Protein that Synaptically Colocalizes and Interacts with Glutamate Receptor delta 2 Subunit
J. Neurosci.,
February 1, 2002;
22(3):
803 - 814.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Hashimoto, R. Ichikawa, H. Takechi, Y. Inoue, A. Aiba, K. Sakimura, M. Mishina, T. Hashikawa, A. Konnerth, M. Watanabe, et al.
Roles of Glutamate Receptor delta 2 Subunit (GluRdelta 2) and Metabotropic Glutamate Receptor Subtype 1 (mGluR1) in Climbing Fiber Synapse Elimination during Postnatal Cerebellar Development
J. Neurosci.,
December 15, 2001;
21(24):
9701 - 9712.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. K. Ghosh, S. Haverkamp, and H. Wassle
Glutamate Receptors in the Rod Pathway of the Mammalian Retina
J. Neurosci.,
November 1, 2001;
21(21):
8636 - 8647.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Morando, R. Cesa, R. Rasetti, R. Harvey, and P. Strata
Role of glutamate delta -2 receptors in activity-dependent competition between heterologous afferent fibers
PNAS,
August 1, 2001;
(2001)
171098398.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Ito
Cerebellar Long-Term Depression: Characterization, Signal Transduction, and Functional Roles
Physiol Rev,
July 1, 2001;
81(3):
1143 - 1195.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. J. Brockie, D. M. Madsen, Y. Zheng, J. Mellem, and A. V. Maricq
Differential Expression of Glutamate Receptor Subunits in the Nervous System of Caenorhabditis elegans and Their Regulation by the Homeodomain Protein UNC-42
J. Neurosci.,
March 1, 2001;
21(5):
1510 - 1522.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. E. Rubio and F. Soto
Distinct Localization of P2X Receptors at Excitatory Postsynaptic Specializations
J. Neurosci.,
January 15, 2001;
21(2):
641 - 653.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Opitz, S. Y. Grooms, M. V. L. Bennett, and R. S. Zukin
Remodeling of alpha -amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit composition in hippocampal neurons after global ischemia
PNAS,
November 21, 2000;
97(24):
13360 - 13365.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. P. Wollmuth, T. Kuner, C. Jatzke, P. H. Seeburg, N. Heintz, and J. Zuo
The Lurcher Mutation Identifies delta 2 as an AMPA/Kainate Receptor-Like Channel That Is Potentiated by Ca2+
J. Neurosci.,
August 15, 2000;
20(16):
5973 - 5980.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. L. Pettit and G. J. Augustine
Distribution of Functional Glutamate and GABA Receptors on Hippocampal Pyramidal Cells and Interneurons
J Neurophysiol,
July 1, 2000;
84(1):
28 - 38.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Toth and C. J McBain
Target-specific expression of pre- and postsynaptic mechanisms
J. Physiol.,
May 15, 2000;
525(1):
41 - 51.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Sassoe-Pognetto and O. P. Ottersen
Organization of Ionotropic Glutamate Receptors at Dendrodendritic Synapses in the Rat Olfactory Bulb
J. Neurosci.,
March 15, 2000;
20(6):
2192 - 2201.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. W. Roche, J. C. Tu, R. S. Petralia, B. Xiao, R. J. Wenthold, and P. F. Worley
Homer 1b Regulates the Trafficking of Group I Metabotropic Glutamate Receptors
J. Biol. Chem.,
September 3, 1999;
274(36):
25953 - 25957.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. R. Howe
REVIEW {blacksquare} : How Glutamate Receptors Are Built
Neuroscientist,
September 1, 1999;
5(5):
311 - 323.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Yazawa, A. Ikeda, R. Kaji, K. Terada, T. Nagamine, K.-i. Toma, T. Kubori, J. Kimura, and H. Shibasaki1
Abnormal cortical processing of voluntary muscle relaxation in patients with focal hand dystonia studied by movement-related potentials
Brain,
July 1, 1999;
122(7):
1357 - 1366.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. E. Rubio and R. J. Wenthold
Differential Distribution of Intracellular Glutamate Receptors in Dendrites
J. Neurosci.,
July 1, 1999;
19(13):
5549 - 5562.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. W. Roche, C. D. Ly, R. S. Petralia, Y.-X. Wang, A. W. McGee, D. S. Bredt, and R. J. Wenthold
Postsynaptic Density-93 Interacts with the delta 2 Glutamate Receptor Subunit at Parallel Fiber Synapses
J. Neurosci.,
May 15, 1999;
19(10):
3926 - 3934.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. L. Doughty, A. Lohof, F. Selimi, N. Delhaye-Bouchaud, and J. Mariani
Afferent-Target Cell Interactions in the Cerebellum: Negative Effect of Granule Cells on Purkinje Cell Development in Lurcher Mice
J. Neurosci.,
May 1, 1999;
19(9):
3448 - 3456.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K.-H. Huh and R. J. Wenthold
Turnover Analysis of Glutamate Receptors Identifies a Rapidly Degraded Pool of the N-Methyl-D-aspartate Receptor Subunit, NR1, in Cultured Cerebellar Granule Cells
J. Biol. Chem.,
January 1, 1999;
274(1):
151 - 157.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H.-M. Zhao, R. J. Wenthold, and R. S. Petralia
Glutamate Receptor Targeting to Synaptic Populations on Purkinje Cells Is Developmentally Regulated
J. Neurosci.,
July 15, 1998;
18(14):
5517 - 5528.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Nusser, W. Sieghart, and P. Somogyi
Segregation of Different GABAA Receptors to Synaptic and Extrasynaptic Membranes of Cerebellar Granule Cells
J. Neurosci.,
March 1, 1998;
18(5):
1693 - 1703.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y.-X. Wang, R. J. Wenthold, O. P. Ottersen, and R. S. Petralia
Endbulb Synapses in the Anteroventral Cochlear Nucleus Express a Specific Subset of AMPA-Type Glutamate Receptor Subunits
J. Neurosci.,
February 1, 1998;
18(3):
1148 - 1160.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Yang, C. Iadecola, and F. M. Faraci
Activation of Cerebellar Climbing Fibers Increases Cerebellar Blood Flow : Role of Glutamate Receptors, Nitric Oxide, and cGMP • Editorial Comment: Role of Glutamate Receptors, Nitric Oxide, and cGMP
Stroke,
February 1, 1998;
29(2):
499 - 508.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Kurihara, K. Hashimoto, M. Kano, C. Takayama, K. Sakimura, M. Mishina, Y. Inoue, and M. Watanabe
Impaired Parallel Fiberright-arrowPurkinje Cell Synapse Stabilization during Cerebellar Development of Mutant Mice Lacking the Glutamate Receptor delta 2 Subunit
J. Neurosci.,
December 15, 1997;
17(24):
9613 - 9623.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. H. Brandstatter, P. Koulen, and H. Wassle
Selective Synaptic Distribution of Kainate Receptor Subunits in the Two Plexiform Layers of the Rat Retina
J. Neurosci.,
December 1, 1997;
17(23):
9298 - 9307.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Safieddine and R. J. Wenthold
The Glutamate Receptor Subunit delta 1 Is Highly Expressed in Hair Cells of the Auditory and Vestibular Systems
J. Neurosci.,
October 1, 1997;
17(19):
7523 - 7531.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Morando, R. Cesa, R. Rasetti, R. Harvey, and P. Strata
Role of glutamate delta -2 receptors in activity-dependent competition between heterologous afferent fibers
PNAS,
August 14, 2001;
98(17):
9954 - 9959.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|

|