Differential plasma membrane distribution of metabotropic glutamate receptors mGluR1α, mGluR2 and mGluR5, relative to neurotransmitter release sites

Journal of Chemical Neuroanatomy

Volumn 13, Issue 4, 1997, Pages 219-241

  Luján, Rafael ^a   Roberts, J David B ^a   Shigemoto, Ryuichi ^b   Ohishi, Hitoshi ^b   Somogyi, Peter ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

Cerebellum; Glutamate; Hippocampus; Immunocytochemistry; Quantitative immunogold; Synaptic junction

Indexed keywords

METABOTROPIC RECEPTOR; RECEPTOR SUBTYPE;

ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CEREBELLUM; DENDRITIC SPINE; FEMALE; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; NERVE FIBER; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PURKINJE CELL; PYRAMIDAL NERVE CELL; RAT; RECEPTOR DENSITY; SYNAPSE;

ANIMALS; BINDING SITES; CELL MEMBRANE; CEREBELLAR CORTEX; FEMALE; IMMUNOHISTOCHEMISTRY; MICE; MICROSCOPY, ELECTRON; NEUROTRANSMITTER AGENTS; PURKINJE CELLS; PYRAMIDAL CELLS; RATS; RATS, WISTAR; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 0030704241     PISSN: 08910618     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-0618(97)00051-3     Document Type: Article

References (98)

1. 2+ signal transduction. J. Biol. Chem. 267:1992;13361-13368.
2. Aniksztejn L., Otani S., Ben-Ari Y. Quisqualate metabotropic receptors modulate NMDA currents and facilitate induction of long-term potentiation through protein kinase C. Eur. J. Neurosci. 4:1992;500-505.
3. Aramori I., Nakanishi S. Signal transduction and pharmacological characteristics of a metabotropic glutamate receptor, mGluR1, in transfected CHO cells. Neuron. 8:1992;757-766.
4. + current by a protein kinase-mediated mechanism. Neurosci. Lett. 112:1990;76-81.
5. Batchelor A.M., Garthwaite J. Frequency detection and temporally dispersed synaptic signal association through a metabotropic glutamate receptor pathway. Nature. 385:1997;74-77.
6. Batchelor A.M., Madge D.J., Garthwaite J. Synaptic activation of metabotropic glutamate receptors in the parallel fibre-Purkinje cell pathway in rat cerebellar slices. Neuroscience. 63:1994;911-915.
7. Baude A., Nusser Z., Roberts J.D.B., Mulvihill E., McIlhinney R.A.J., Somogyi P. The metabotropic glutamate receptor (mGluR1α) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron. 11:1993;771-787.
8. Baude A., Nusser Z., Molnar E., McIlhinney R.A.J., Somogyi P. High-resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and non-synaptic sites in rat hippocampus. Neuroscience. 69:1995;1031-1055.
9. Beaulieu C., Colonnier M. The number of neurons in the different laminae of the binocular and monocular regions of area 17 in the cat. J. Comp. Neurol. 217:1983;337-344.
10. Bischofberger J., Schild D. Glutamate and N-acetylaspartylglutamate block HVA calcium currents in frog olfactory bulb interneurons via an mGluR2/3-like receptor. J. Neurophysiol. 76:1996;2089-2092.
11. Bradley S.R., Levey A.I., Hersch S.M., Conn P.J. Immunocytochemical localization of group III metabotropic glutamate receptors in the hippocampus with subtype-specific antibodies. J. Neurosci. 16:1996;2044-2056.
12. Brakeman P.R., Lanahan A.A., O'Brien R., Roche K., Barnes C.A., Huganir R.L., Worley P.F. Homer: a protein that selectively binds metabotropic glutamate receptors. Nature. 386:1997;284-288.
13. Brandstatter J.H., Koulen P., Kuhn R., van der Putten H., Wassle H. Compartmental localization of a metabotropic glutamate receptor (mGluR7): two different active sites at a retinal synapse. J. Neurosci. 16:1996;4749-4756.
14. Charpak S., Gahwiler B.H., Do K.Q., Knopfel T. Potassium conductances in hippocampal neurons blocked by excitatory amino-acid transmitters. Nature. 347:1990;765-767.
15. Charpak S., Gahwiler B.H. Glutamate mediates a slow synaptic response in hippocampal slice cultures. Proc. R. Soc. London Sci. 243:1991;221-226.
16. Chaudhry F.A., Lehre K.P., Campagne M.V.L., Ottersen O.P., Danbolt N.C., Storm-Mathisen J. Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron. 15:1995;711-720.
17. Clements J.D. Transmitter timecourse in the synaptic cleft: its role in central synaptic function. Trends Neurosci. 19:1996;163-171.
18. 2+-activated nonspecific cationic current in CA1 hippocampal neurons. J. Neurophysiol. 72:1994;1561-1569.
19. Deller T., Adelmann G., Nitsch R., Frotscher M. The alvear pathway of the rat hippocampus. Cell Tissue Res. 286:1996;293-303.
20. Dong H., OÕBrian R.J., Fung E.T., Lanahan A.A., Worley P.F., Huganir R.L. GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature. 386:1997;279-284.
21. Duvoisin R.M., Zhang C., Ramonell K. A novel metabotropic glutamate receptor expressed in the retina and olfactory bulb. J. Neurosci. 15:1995;3075-3083.
22. Eaton S.A., Birse E.F., Wharton B., Sunter D.C., Udvarhelyi P.M., Watkins J.C., Salt T.E. Mediation of thalamic sensory responses in vivo by ACPD-activated excitatory amino acid receptors. Eur. J. Neurosci. 5:1993;186-189.
23. Fitzjohn S.M., Irving A.J., Palmer M.J., Harvey J., Lodge D., Collingridge G.L. Activation of group I mGluRs potentiates NMDA responses in rat hippocampal slices. Neurosci. Lett. 203:1996;211-213.
24. Gerber U., Sim J.A., Gahwiler B.H. Reduction of potassium conductances mediated by metabotropic glutamate receptors in rat CA3 pyramidal cells does not require protein kinase C or protein kinase A. Eur. J. Neurosci. 4:1992;792-797.
25. Gerber, U., Gahwiler, B.H., 1994. Modulation of ionic currents by metabotropic glutamate receptors in the CNS. In: Conn, P.J., Patel, J. (Eds.), The Metabotropic Glutamate Receptors. Humana Press, NJ, pp. 125-146.
26. Gereau R.W., Conn P.J. Roles of specific metabotropic glutamate receptor subtypes in regulation of hippocampal CA1 pyramidal cell excitability. J. Neurophysiol. 74:1995;122-129.
27. Glaum S.R., Miller R.J. Metabotropic glutamate receptors mediate excitatory transmission in the nucleus of the solitary tract. J. Neurosci. 12:1992;2251-2258.
28. Glaum S.R., Slater N.T., Rossi D.J., Miller R.J. Role of metabotropic glutamate (ACPD) receptors at the parallel fiber-Purkinje cell synapse. J. Neurophysiol. 68:1992;1453-1462.
29. Glitsch M., Llano I., Marty A. Glutamate as a candidate retrograde messenger at interneurone-Purkinje cell synapses of rat cerebellum. J. Physiol. (London). 497:1996;531-537.
30. Gomeza J., Joly C., Kuhn R., Knopfel T., Bockaert J., Pin J.-P. The second intracellular loop of metabotropic glutamate receptor 1 cooperates with the other intracellular domains to control grouping to G-proteins. J. Biol. Chem. 271:1996;2199-2205.
31. Grandes P., Mateos J.M., Ruegg D., Kuhn R., Knopfel T. Differential cellular localization of three splice variants of the mGluR1 metabotropic glutamate receptor in rat cerebellum. NeuroReport. 5:1994;2249-2252.
32. + current by metabotropic glutamate and muscarinic receptors in rat CA3 cells: mediation by G-proteins. J. Physiol. 474:1994;27-33.
33. Guerineau N.C., Bossu J.-L., Gahwiler B.H., Gerber U. Activation of a nonselective cationic conductance by metabotropic glutamatergic and muscarinic agonists in CA3 pyramidal neurons of the rat hippocampus. J. Neurosci. 15:1995;4395-4407.
34. Harvey J., Collingridge G.L. Signal transduction pathways involved in the acute potentiation of NMDA responses by (1S,3R)-ACPD in rat hippocampal slices. Br. J. Pharmacol. 109:1993;1085-1090.
35. Hayashi Y., Momiyama A., Takahashi T., Ohishi H., Ogawa-Meguro R., Shigemoto R., Mizuno N., Nakanishi S. Role of a metabotropic glutamate receptor in synaptic modulation in the accessory olfactory bulb. Nature. 366:1993;687-690.
36. Hollmann M., Heinemann S. Cloned glutamate receptors. Ann. Rev. Neurosci. 17:1994;31-108.
37. Joly C., Gomeza J., Brabet I., Curry K., Bockaert J., Pin J.-P. Molecular, functional and pharmacological characterization of the metabotropic glutamate receptor type 5 splice variants: comparison with mGluR1. J. Neurosci. 15:1995;3970-3981.
38. Kharazia V.N., Phend K.D., Rustioni A., Weinberg R.J. EM colocalization of AMPA and NMDA receptor subunits at synapses in rat cerebral cortex. Neurosci. Lett. 210:1996;37-40.
39. Kim E., Cho K.-O., Rothschild A., Sheng M. Heteromultimerization and NMDA receptor-clustering activity of chapsyn-110, a member of the PSD-95 family proteins. Neuron. 17:1996;103-113.
40. Kinoshita A., Ohishi H., Neki A., Nomura S., Shigemoto R., Takada M., Nakanishi S., Mizuno N. Presynaptic localization of a metabotropic glutamate receptor, mGluR8, in the rhinencephalic areas: a light and electron microscope study in the rat. Neurosci. Lett. 207:1996;61-64.
41. Kornau H.-C., Schenker L.T., Kennedy M.B., Seeburg P.H. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science. 269:1995;1737-1740.
42. Landsend A.S., Amiry-Moghaddam M., Matsubara A., Bergersen L., Usami S., Wenthold R.J., Ottersen O.P. Differential localization of delta glutamate receptors in the rat cerebellum: Coexpression with AMPA receptors in parallel fiber-spine synapses and absence from climbing fiber-spine synapses. J. Neurosci. 17:1997;834-842.
43. Lester R.A.J., Jahr C.E. Quisqualate receptor-mediated depression of calcium currents in hippocampal neurons. Neuron. 4:1990;741-749.
44. Linden D.J., Connor J.A. Long-term synaptic depression. Ann. Rev. Neurosci. 18:1995;319-357.
45. Lujan R., Nusser Z., Roberts J.D.B., Shigemoto R., Somogyi P. Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur. J. Neurosci. 8:1996;1488-1500.
46. Martin L.J., Blackstone C.D., Huganir R.L., Price D.L. Cellular localization of a metabotropic glutamate receptor in rat brain. Neuron. 9:1992;259-270.
47. Masu M., Tanabe Y., Tsuchida K., Shigemoto R., Nakanishi S. Sequence and expression of a metabotropic glutamate receptor. Nature. 349:1991;760-765.
48. Masu M., Iwakabe H., Tagawa Y., Miyoshi T., Yamashita M., Fukuda Y., Sasaki H., Hiroi K., Nakamura Y., Shigemoto R., Takada M., Nakamura K., Nakao K., Katsuki M., Nakanishi S. Specific deficit of the ON response in visual transmission by targeted disruption of the mGluR6 gene. Cell. 80:1995;757-765.
49. Matsubara A., Laake J.H., Davanger S., Usami S.I., Ottersen O.P. Organization of AMPA receptor subunits at a glutamate synapse: a quantitative immunogold analysis of hair cell synapses in the rat organ of corti. J. Neurosci. 16:1996;4457-4467.
50. Miles R., Poncer J.-C. Metabotropic glutamate receptors mediate a post-tetanic excitation of guinea-pig hippocampal inhibitory neurones. J. Physiol. 463:1993;461-473.
51. Minakami R., Katsuki F., Sugiyama H. A variant of metabotropic glutamate receptor subtype 5: an evolutionally conserved insertion with no termination codon. Biochem. Biophys. Res. Commun. 194:1993;622-627.
52. Minakami R., Iida K.-I., Hirakawa N., Sugiyama H. The expression of two splice variants of metabotropic glutamate receptor subtype 5 in the rat brain and neuronal cells during development. J. Neurochem. 65:1995;1536-1542.
53. Muller D., Arai A., Lynch G. Factors governing the potentiation of NMDA receptor-mediated responses in hippocampus. Hippocampus. 2:1992;29-38.
54. Naito S., Ueda T. Affinity-purified anti-protein I antibody. J. Biol. Chem. 256:1981;10657-10663.
55. Nakajima Y., Iwakabe H., Akazawa C., Nawa H., Shigemoto R., Mizuno N., Nakanishi S. Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. J. Biol. Chem. 268:1993;11868-11873.
56. Nakanishi S. Metabotropic glutamate receptors: synaptic transmission, modulation, and plasticity. Neuron. 13:1994;1031-1037.
57. Namba T., Sugimoto Y., Negishi M., Irie A., Ushikubi F., Kakizuka A., Ito S., Ichikawa A., Narumiya S. Alternative splicing of C-terminal tail of prostaglandin E receptor subtype EP3 determines G-protein specificity. Nature. 365:1993;166-170.
58. Neki A., Ohishi H., Kaneko T., Shigemoto R., Nakanishi S., Mizuno N. Metabotropic glutamate receptors mGluR2 and mGluR5 are expressed in two non-overlapping populations of Golgi cells in the rat cerebellum. Neuroscience. 75:1996;815-826.
59. Neki A., Ohishi N., Kaneko T., Shigemoto R., Nakanishi S., Mizuno N. Pre- and postsynaptic localization of a metabotropic glutamate receptor, mGluR2, in the rat brain: an immunohistochemical study with a monoclonal antibody. Neurosci. Lett. 202:1996;197-200.
60. Nusser Z., Mulvihill E., Streit P., Somogyi P. Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localisation. Neuroscience. 61:1994;421-427.
61. A receptors on cerebellar granule cells as determined by a quantitative immunogold method. J. Neurosci. 15:1995;2948-2960.
62. Ohishi H., Shigemoto R., Nakanishi S., Mizuno N. Distribution of the messenger RNA for a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat. Neuroscience. 53:1993;1009-1018.
63. Ohishi H., Shigemoto R., Nakanishi S., Mizuno N. Distribution of the mRNA for a metabotropic glutamate receptor (mGluR3) in the rat brain: an in situ hybridization study. J. Comp. Neurol. 335:1993;252-266.
64. Ohishi H., Ogawa-Meguro R., Shigemoto R., Kaneko T., Nakanishi S., Mizuno N. Immunohistochemical localization of metabotropic glutamate receptors, mGluR2 and mGluR3, in rat cerebellar cortex. Neuron. 13:1994;55-66.
65. Ohishi H., Nomura S., Ding Y.-Q., Shigemoto R., Wada E., Kinoshita A., Li J.-L., Neki A., Nakanishi S., Mizuno N. Presynaptic localization of a metabotropic glutamate receptor, mGluR7, in the primary afferent neurons: an immunohistochemical study in the rat. Neurosci. Lett. 202:1995;85-88.
66. Okamoto N., Hori S., Akazawa C., Hayashi Y., Shigemoto R., Mizuno N., Nakanishi S. Molecular characterization of a new metabotropic glutamate receptor mGluR7 coupled to inhibitory cyclic AMP signal transduction. J. Biol. Chem. 269:1994;1231-1236.
67. Peters, A., Palay, S.L., Webster, H., 1991. The Fine Structure of the Nervous System. Oxford University Press, NY.
68. Petralia R.S., Wang Y.- X, Niedzielski A.S., Wenthold R.J. The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neuroscience. 71:1996;949-976.
69. Pickering D.S., Thomsen C., Suzdak P.D., Fletcher E.J., Robitaille R., Salter M.W., MacDonald J.F., Huang X.-P., Hampson D.R. A comparison of two alternatively spliced forms of a metabotropic glutamate receptor coupled to phosphoinositide turnover. J. Neurochem. 6:1993;85-92.
70. Pin J.-P., Waeber C., Prezeau L., Bockaert J., Heinemann S.F. Alternative splicing generates metabotropic glutamate receptors inducing different patterns of calcium release in Xenopus oocytes. Proc. Natl. Acad. Sci. USA. 89:1992;10331-10335.
71. Pin J.-P., Duvoisin R. Neurotransmitter receptors I. The metabotropic glutamate receptors: structure and functions. Neuropharmacology. 34:1995;1-26.
72. Poncer J.-C., Shinozaki H., Miles R. Dual modulation of synaptic inhibition by distinct metabotropic glutamate receptors in the rat hippocampus. J. Physiol. (London). 485:1995;121-134.
73. Prezeau L., Gomeza J., Ahern S., Mary S., Galvez T., Bockaert J., Pin J.-P. Changes in the carboxyl-terminal domain of metabotropic glutamate receptor 1 by alternative splicing generate receptors with differing agonist-independent activity. Mol. Pharm. 49:1996;422-429.
74. Romano C., Sesma M.A., McDonald C.T., O'Malley K., van den Pol A.N., Olney J.W. Distribution of metabotropic glutamate receptor mGluR5 immunoreactivity in rat brain. J. Comp. Neurol. 355:1995;455-469.
75. Romano C., van den Pol A.N., O'Malley K.L. Enhanced early developmental expression of the metabotropic glutamate receptor mGluR5 in rat brain: protein, mRNA splice variants and regional distribution. J. Comp. Neurol. 367:1996;403-412.
76. Sahara Y., Westbrook G.L. Modulation of calcium currents by a metabotropic glutamate receptor involves fast and slow kinetic components in cultured hippocampal neurons. J. Neurosci. 13:1993;3041-3050.
77. Sanchez-Prieto J., Budd D.C., Herrero I., Vazquez E., Nicholls D.G. Presynaptic receptors and the control of glutamate exocytosis. Trends Neurosci. 19:1996;235-239.
78. Sanz J.T., Shigemoto R., Somogyi P. Targeting of interneurons by entorhinal axons in stratum oriens and radiatum of area CA1 in the rat hippocampus. Brain Res. Assoc. Abstr. 13:1996;86.
79. Schoepp D.D., Johnson B.G., Salhoff C.R., Valli M.J., Desai M.A., Burnett J.P., Mayne N.G., Monn J.A. Selective inhibition of forskolin-stimulated cyclic AMP formation in rat hippocampus by a novel mGluR agonist, 2R,4R-4-aminopyrrolidine-2,4-dicarboxylate. Neuropharmacology. 34:1995;843-850.
80. Seeburg P.H. The TINS/TIPS lecture - the molecular biology of mammalian glutamate receptor channels. Trends Neurosci. 16:1993;359-365.
81. Shigemoto R., Nomura S., Ohishi H., Sugihara H., Nakanishi S., Mizuno N. Immunohistochemical localization of a metabotropic glutamate receptor, mGluR5, in the rat brain. Neurosci. Lett. 163:1993;53-57.
82. Shigemoto R., Abe T., Nomura S., Nakanishi S., Hirano T. Antibodies inactivating mGluR1 metabotropic glutamate receptor block long-term depression in cultured Purkinje cells. Neuron. 12:1994;1245-1255.
83. Shigemoto R., Wada E., Ohishi H., Takada M., Mizuno N., Roberts J.D.B., Somogyi P. Differential presynaptic localization of metabotropic glutamate receptor subtypes, mGluR2/3 and mGluR7, in the rat hippocampus. Soc. Neurosci. Abstr. 21:1995;846.
84. Shigemoto R., Kulik A., Roberts J.D.B., Ohishi H., Nusser Z., Kaneko T., Somogyi P. Target-cell-specific concentration of a metabotropic glutamate receptor in the presynaptic active zone. Nature. 381:1996;523-525.
85. Somogyi P., Halasy K., Somogyi J., Storm-Mathisen J., Ottersen O.P. Quantification of immunogold labelling reveals enrichment of glutamate in mossy and parallel fibre terminals in cat cerebellum. Neuroscience. 19:1986;1045-1050.
86. Somogyi P., Eshhar N., Teichberg V.I., Roberts J.D.B. Subcellular localization of a putative kainate receptor in Bergmann Glial cells using a monoclonal antibody in the chick and fish cerebellar cortex. Neuroscience. 35:1990;9-30.
87. Spacek J., Harris K.M. Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J. Neurosci. 17:1997;190-203.
88. Staub C., Vranesic I., Knopfel T. Responses to metabotropic glutamate receptor activation in cerebellar Purkinje cells: induction of an inward current. Eur. J. Neurosci. 4:1992;832-839.
89. Sugimoto Y., Negishi M., Hayashi Y., Namba T., Honda A., Watabe A., Hirata M., Narumiya S., Ichikawa A. Two isoforms of the EP3 receptor with different carboxyl-terminal domains. Identical ligand binding properties and different coupling properties with Gi proteins. J. Biol. Chem. 268:1993;2712-2718.
90. Tanabe Y., Masu M., Ishii T., Shigemoto R., Nakanishi S. A family of metabotropic glutamate receptors. Neuron. 8:1992;169-180.
91. Tanabe Y., Nomura A., Masu M., Shigemoto R., Mizuno N., Nakanishi S. Signal transduction, pharmacological properties, and expression patterns of two rat metabotropic glutamate receptors, mGluR3 and mGluR4. J. Neurosci. 13:1993;1372-1378.
92. van den Pol A.N. Metabotropic glutamate receptor mGluR1 distribution and ultrastructural localization in hypothalamus. J. Comp. Neurol. 349:1994;615-632.
93. van den Pol A.N., Romano C., Ghosh P. Metabotropic glutamate receptor mGluR5 subcellular distribution and developmental expression in hypothalamus. J. Comp. Neurol. 362:1995;134-150.
94. Vidnyanszky Z., Hamori J., Negyessy L., Ruegg D., Knopfel T., Kuhn R., Gorcs T.J. Cellular and subcellular localization of the mGluR5a metabotropic glutamate receptor in rat spinal cord. NeuroReport. 6:1994;209-213.
95. Vidnyanszky Z., Gorcs T.J., Negyessy L., Borostyankoi Z., Kuhn R., Knopfel T., Hamori J. Immunocytochemical visualization of the mGluR1α metabotropic glutamate receptor at synapses of corticothalamic terminals originating from area 17 of the rat. Eur. J. Neurosci. 8:1996;1061-1071.
96. Winsky L., Nakata H., Martin B.M., Jacobowitz D.M. Isolation, partial amino acid sequence, and immunohistochemical localization of a brain-specific calcium-binding protein. Proc. Natl. Acad. Sci. USA. 86:1989;10139-10143.
97. Yamamoto C., Yamashita H., Chujo T. Inhibitory action of glutamic acid on cerebellar interneurones. Nature. 262:1976;786-787.
98. Yokoi M., Kobayashi K., Manabe T., Takahashi T., Sakaguchi I., Katsuura G., Shigemoto R., Ohishi H., Nomura S., Nakamura K., Nakao K., Katsuki M., Nakanishi S. Impairment of hippocampal mossy fiber LTD in mice lacking mGluR2. Science. 273:1996;645-647.