Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus

Journal of Neuroscience

Volumn 17, Issue 19, 1997, Pages 7503-7522

  Shigemoto, Ryuichi ^a   Kinoshita, Ayae ^a   Wada, Eiki ^a   Nomura, Sakashi ^a   Ohishi, Hitoshi ^a   Takada, Masahiko ^a   Flor, Peter J ^b   Neki, Akio ^a   Abe, Takaaki ^a   Nakanishi, Shigetada ^a   Mizuno, Noboru ^a  

^a KYOTO UNIVERSITY   (Japan)

^b NOVARTIS PHARMA AG   (Switzerland)

Author keywords

Axon terminal; Hippocampus; Immunohistochemistry; Lesion; Metabotropic glutamate receptor; Mossy fiber; Perforant path; Preterminal; Schaffer collateral

Indexed keywords

GLUTAMATE RECEPTOR; METABOTROPIC RECEPTOR; RECEPTOR SUBTYPE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; HIPPOCAMPUS; LEARNING; MALE; MEMORY; MOSSY FIBER; NERVE CELL PLASTICITY; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; RECEPTOR DENSITY;

EID: 0030821474     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.17-19-07503.1997     Document Type: Article

References (93)

1. Aiba A, Chen C, Herrup K, Rosenmund C, Stevens CF, Tonegawa S (1994) Reduced hippocampal long-term potentiation and context-specific deficit in associative learning in mGluR1 mutant mice. Cell 79:365-375.
2. Amaral DG, Witter MP (1995) Hippocampal formation. In: The rat nervous system, second edition (Paxinos G, ed), pp 443-493. San Diego: Academic.
3. Bakst I, Avendano C, Morrison JH, Amaral DG (1986) An experimental analysis of the origins of somatostatin-like immunoreactivity in the dentate gyrus of the rat. J Neurosci 6:1452-1462.
4. Baskys A, Gerlai R, Pekhletski R, Roder J, Hampson DR (1996) Physiological and behavioral studies of mice lacking type 4 mGluRs. Neuropharmacology 35:A2.
5. Baude A, Nusser Z, Roberts JDB, Mulvihill E, McIlhinney RAJ, Somogyi P (1993) The metabotropic glutamate receptor (mGluR1α) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11:771-787.
6. Boulton CL, Irving AJ, Southam E, Potier B, Garthwaite J, Collingridge GL (1994) The nitric oxide-cyclic GMP pathway and synaptic depression in rat hippocampal slices. Eur J Neurosci 6:1528-1535.
7. Bradley SR, Levey AI, Hersch SM, Conn PJ (1996) Immunocytochemical localization of group III metabotropic glutamate receptors in the hippocampus with subtype-specific antibodies. J Neurosci 16:2044-2056.
8. Bramham CR, Torp R, Zhang N, Storm-Mathisen J, Ottersen OP (1990) Distribution of gutamate-like immunoreactivity in excitatory hippocampal pathways: a semiquantitative electron microscopic study in rats. Neuroscience 39:405-417.
9. Buckmaster PS, Wenzel HJ, Kunkel DD, Schwartzkroin PA (1996) Axon arbors and synaptic connections of hippocampal mossy cells in the rat in vivo. J Comp Neurol 366:270-292.
10. Buhl EH, Halasy K, Somogyi P (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368:823-828.
11. Bushell TJ, Jane DE, Tse H-W, Watkins JC, Garthwaite J, Collingridge GL (1996a) Pharmacological antagonism of the actions of group II and III mGluR agonists in the lateral perforant path of rat hippocampal slices. Br J Pharmacol 117:1457-1462.
12. Bushell TJ, Sansig G, Shigemoto R, Flor P, Kuhn R, Knoepfel T, Schroeder M, Collett VL, Collingridge GL, van der Putten H (1996b) An impair- ment of hippocampal synaptic plasticity in mice lacking mGlu7 receptors. Neuropharmacology 35:A6.
13. Coyle JT, Schwarcz R (1976) Lesion of striatal neurones with kainic acid provides a model for Huntington's chorea. Nature 263:244-246,
14. 2+-activatcd nonspecific cationic current in CA1 hippocampal neurons. J Neurophysiol 72:1561-1569.
15. Davies CH, Clarke VRJ, Jane DE, Collingridge GL (1995) Pharmacology of postsynaptic metabotropic glutamate receptors in rat hippocampal CA1 pyramidal neurones. Br J Pharmacol 116:1859-1869.
16. Di Iorio P, Battaglia G, Ciccarelli R, Ballerini P, Giuliani P, Poli A, Nicoletti F, Caciagli F (1996) Interaction between Al adenosine and class II metabotropic glutamate receptors in the regulation of purine and glutamate release from rat hippocampal slices. J Neurochem 67:302-309.
17. Flor PJ, van der Putten H, Rüegg D, Lukic S, Leonhardt T, Bence M, Sansig G, Knöpfel T, Kuhn R (1997) A novel splice variant of a metabotropic glutamate receptor, human mGluRTb. Neuropharmacology 36:153-159.
18. Fotuhi M, Standaert DG, Testa CM, Penney JB, Young AB (1994) Differential expression of metabotropic glutamate receptors in the hippocampus and entorhinal cortex of the rat. Mol Brain Res 21:283-292.
19. Frotscher M, Leranth C (1985) Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study. J Comp Neurol 239:237-246.
20. Gereau RW, Conn PJ (1995a) Multiple presynapttc metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CAL J Neurosci 15:6879-6889.
21. Gereau RW, Conn PJ (1995b) Roles of specific metabotropic glutamate receptor subtypes in regulation of hippocampal CA1 pyramidal cell excitability. J Neurophysiol 74:122-129.
22. Glitsch M, Llano I, Marty A (1996) Glutamate as a candidate retrograde messenger at interneurone-Purkinje cell synapses of rat cerebellum. J Physiol (Lond) 497:531-537.
23. Goldschmidt RB, Steward O (1980) Preferential neurotoxicity of colchicine for granule cells of the dentate gyrus of the adult rat. Proc Natl Acad Sci USA 77:3047-3051.
24. + current by metabotropic glutamate and muscarinic receptors in rat CA3 cells: mediation by G-proteins. J Physiol (Lond) 474:27-33.
25. Guérineau NC, Bossu J-L, Gähwiler BH, Gerber U (1995) Activation of a nonselective cationic conductance by metabotropic glutamatergic and muscarinic agonists in CA3 pyramidal neurons of the rat hippocampus. J Neurosci 15:4395-4407.
26. Han Z-S, Buhl EH, Lörinczi Z, Somogyi P (1993) A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus. Eur J Neurosci 5:395-410.
27. Harvey J, Palmer MJ, Irving AJ, Clarke VRJ, Collingridge GL (1996) NMDA receptor dependence of mGlu-mediated depression of synaptic transmission in the CA1 region of the rat hippocampus. Br J Pharmacol 119:1239-1247.
28. Hayashi Y, Momiyama A, Takahashi T, Ohishi H, Ogawa-Meguro R, Shigemoto R, Mizuno N, Nakanishi S (1993) Role of a metabotropic glutamate receptor in synaptic modulation in the accessory olfactory bulb. Nature 366:687-690.
29. Ikeda SR, Lovinger DM, McCool BA, Lewis DL (1995) Heterologous expression of metabotropic glutamate receptors in adult rat sympathetic neurons: subtype-specific coupling to ion channels. Neuron 14:1029-1038.
30. Johansen PA, Chase LA, Sinor AD, Koerner JF, Johnson RL, Robinson MB (1995) Type 4a metabotropic glutamate receptor: identification of new potent agonists and differentiation from the L-( + )-2-amino-4-phosphonobutanoic acid-sensitive receptor in the lateral perforant pathway in rats. Mol Pharmacol 48:140-149.
31. Kinoshita A, Ohishi H, Neki A, Nomura S, Shigemoto R, Takada M, Nakanishi S, Mizuno N (1996a) Presynaptic localization of a metabotropic glutamate receptor, mGluR8, in the rhinencephalic areas: a light and electron microscope study in the rat. Neurosci Lett 207:61-64.
32. Kinoshita A, Ohishi H, Nomura S, Shigemoto R, Nakanishi S, Mizuno N (1996b) Presynaptic localization of a metabotropic glutamate receptor, mGluR4a, in the cerebellar cortex: a light and electron microscope study in the rat. Neurosci Lett 207:199-202.
33. Kishi K, Stanfield BB, Cowan WM (1980) A quantitative EM autoradiographic study of the commissural and associational connections of the dentate gyrus in the rat. Anat Embryol 160:173-186.
34. Koerner JF, Cotman CW (1981) Micromolar L-2-amino-4-phosphonobutyric acid selectively inhibits perforant path synapses from lateral entorhinal cortex. Brain Res 216:192-198.
35. Lanthorn TH, Ganong AH, Cotman CW (1984) 2-amino-4-phosphonobutyrate selectively blocks mossy fiber-CA3 responses in guinea pig but not rat hippocampus. Brain Res 290:174-178.
36. 1d, a novel splice variant of the human type I metabotropic glutamate receptor. Eur J Pharmacol 296:R1-R3.
37. Leranth C, Frotscher M (1987) Cholinergic innervation of hippocampal GAD- and somatostatin-immunoreactive commissural neurons. J Comp Neurol 261:33-47.
38. Leranth C, Malcolm AJ, Frotscher M (1990) Afferent and efferent synaptic connections of somatostatin-immunoreactive neurons in the rat fascia dentata. J Comp Neurol 295:111-122.
39. Lu Y-M, Jia Z, Janus C, Henderson JT, Gerlai R, Wojtowicz JM, Roder JC (1997) Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 long-term potentiation (LTP) but normal CA3 LTP. J Neurosci 17:5196-5205.
40. Luján R, Nusser Z, Roberts JDB, Shigemoto R, Somogyi P (1996) Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci 8:1488-1500.
41. Macek TA, Winder DG, Gereau RW, Ladd CO, Conn PJ (1996) Differential involvement of group II and group III mGluRs as autoreceptors at lateral and medial perforant path synapses. J Neurophysiol 76:3798-3806.
42. Maglóczky Z, Acsády L, Freund TF (1994) Principal cells are the postsynaptic targets of supramammillary afferents in the hippocampus of the rat. Hippocampus 4:322-334.
43. Manzoni O, Bockaert J (1995) Metabotropic glutamate receptors inhibiting excitatory synapses in the CA1 area of rat hippocampus. Eur J Neurosci 7:2518-2523.
44. Manzoni OJ, Manabe T, Nicoll RA (1994) Release of adenosine by activation of NMDA receptors in the hippocampus. Science 265:2098-2101.
45. Masu M, Tanabe Y, Tsuchida K, Shigemoto R, Nakanishi S (1991) Sequence and expression of a metabotropic glutamate receptor. Nature 349:760-765.
46. Matthews DA, Cotman C, Lynch G (1976) An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. I. Magnitude and time course of degeneration. Brain Res 115:1-21.
47. McGinty JF, Henriksen SJ, Goldstein A, Terenius L, Bloom FE (1983) Dynorphin is contained within hippocampal mossy fibers: immuno-chemical alterations after kainic acid administration and colchicine-induced neurotoxicity. Proc Natl Acad Sci USA 80:589-593.
48. Milner TA, Bacon CE (1989) Ultrastructural localization of somatostatin-like immunoreactivity in the rat dentate gyrus. J Comp Neurol 290:544-560.
49. Minakami R, Katsuki F, Sugiyama H (1993) A variant of metabotropic glutamate receptor subtype 5: an evolutionally conserved insertion with no termination codon. Biochem Biophys Res Commun 194:622-627.
50. Nadler JV, Perry BW, Gentry C, Cotman CW (1980) Degeneration of hippocampal CA3 pyramidal cells induced by intraventricular kainic acid. J Comp Neurol 192:333-359.
51. Nadler JV, Perry BW, Gentry C, Cotman CW (1981) Fate of the hippocampal mossy fiber projection after destruction of its postsynaptic targets with intraventricular kainic acid. J Comp Neurol 196:549-569.
52. Nakajima Y, Iwakabe H, Akazawa C, Nawa H, Shigemoto R, Mizuno N, Nakanishi S (1993) Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. J Biol Chem 268:11868-11873.
53. Nakanishi S, Masu M (1994) Molecular diversity and functions of glutamate receptors. Annu Rev Biophys Biomol Struct 23:319-348.
54. Neki A, Ohishi H, Kaneko T, Shigemoto R, Nakanishi S, Mizuno N (1996) Pre- and postsynaptic localization of a metabotropic glutamate receptor, mGluR2, in the rat brain: an immunohistochemical study with a monoclonal antibody. Neurosci Lett 202:197-200.
55. Nomura A, Shigemoto R, Nakamura Y, Okamoto N, Mizuno N, Nakanishi S (1994) Developmentally regulated postsynaptic localization of a metabotropic glutamate receptor in rat rod bipolar cells. Cell 77:361-369.
56. Nusser Z, Siegharl W, Benke D, Fritschy J-M, Somogyi P (1996) Differ- ential synaptic localization of two major y-aminobutyric acid type A receptor α subunits on hippocampal pyramidal cells. Proc Natl Acad Sci USA 93:11939-11944.
57. Ohishi H, Shigemoto R, Nakanishi S, Mizuno N (1993a) Distribution of the messenger RNA for a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat. Neuroscience 53:1009-1018.
58. Ohishi H, Shigemoto R, Nakanishi S, Mizuno N (1993b) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR3) in the rat brain: an in situ hybridization study. J Comp Neurol 335:252-266.
59. Ohishi H, Ogawa-Meguro R, Shigemoto R, Kaneko T, Nakanishi S, Mizuno N (1994) Immunohistochemical localization of metabotropic glutamate receptors, mGIuR2 and mGluR3, in rat cerebellar cortex. Neuron 13:55-66.
60. Ohishi H, Akazawa C, Shigemoto R, Nakanishi S, Mizuno N (1995a) Distributions of the mRNAs for L-2-amino-4-phosphonobutyrate-sensitive metabotropic glutamate receptors, mGluR4 and mGluR7, in the rat brain. J Comp Neurol 360:555-570.
61. Ohishi H, Nomura S, Ding Y-Q, Shigemoto R, Wada E, Kinoshita A, Li J-L, Neki A, Nakanishi S, Mizuno N (1995b) Presynaptic localization of a metabotropic glutamate receptor, mGluR7, in the primary afferent neurons: an immunohistochemical study in the rat. Neurosci Lett 202:85-88.
62. Okamoto N, Hori S, Akazawa C, Hayashi Y, Shigemoto R, Mizuno N, Nakanishi S (1994) Molecular characterization of a new metabotropic glutamate receptor mGluR7 coupled to inhibitory cyclic AMP signal transduction. J Biol Chem 269:1231-1236.
63. Ouardouz M, Lacaille J-C (1995) Mechanisms of selective long-term potentiation of excitatory synapses in stratum oriens/alveus interneurons of rat hippocampal slices. J Neurophysiol 73:810-819.
64. Pekhletski R, Gerlai R, Overstreet LS, Huang XP, Agopyan N, Slater NT, Abramow-Newerly W, Roder JC, Hampson DR (1996) Impaired cerebellar synaptic plasticity and motor performance in mice lacking the mGluR4 subtype of metabotropic glutamate receptor. J Neurosci 16:6364-6373.
65. Petralia RS, Wang Y-X, Niedzielski AS, Wenthold RJ (1996) The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neuroscience 71:949-976.
66. Pin J-P, Duvoisin R (1995) Neurotransmitter receptors I. The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34:1-26.
67. Pin J-P, Waeber C, Prézeau L, Bockaert J, Heinemann SF (1992) Alternative splicing generates metabotropic glutamate receptors inducing different patterns of calcium release in Xenopus oocytes. Proc Natl Acad Sci USA 89:10331-10335.
68. + channel proteins (GIRK1) are present in the soma and dendrites as well as in nerve terminals of specific neurons in the brain. J Neurosci 16:1990-2001.
69. Poncer J-C, Shinozaki H, Miles R (1995) Dual modulation of synaptic inhibition by distinct metabotropic glutamate receptors in the rat hippocampus. J Physiol (Lond) 485:121-134.
70. Romano C, Yang W-L, O'Malley KL (1996) Metabotropic glutamate receptor 5 is a disulfide-linked dimer. J Biol Chem 271:28612-28616.
71. Sahara Y, Westbrook GL (1993) Modulation of calcium currents by a metabotropic glutamate receptor involves fast and slow kinetic components in cultured hippocampal neurons. J Neurosci 13:3041-3050.
72. 1A subunits of brain calcium channels. J Cell Biol 134:511-528.
73. Saugstad JA, Kinzie JM, Mulvihill ER, Segerson TP, Westbrook GL (1994) Cloning and expression of a new member of the L-2-amino-4-phosphonobutyric acid-sensitive class of metabotropic glutamate receptors. Mol Pharmacol 45:367-372.
74. Saugstad JA, Segerson TP, Westbrook GL (1996) Metabotropic glutamate receptors activate G-protein-coupled inwardly rectifying potassium channels in Xenopus oocytes. J Neurosci 16:5979-5985.
75. 2+ channels involved? Neuropharmacology 34:1549-1557.
76. Scanziani M, Salin PA, Vogt KE, Malenka RC, Nicoll RA (1997) Use- dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385:630-634.
77. Schoepp DD, Goldsworthy J, Johnson BG, Salhoff CR, Baker SR (1994) 3,5-Dihydroxyphenylglycine is a highly selective agonist for phosphoinositide-linked metabotropic glutamate receptors in the rat hippocampus. J Neurochem 63:769-772.
78. + channels detected in vivo. Nature 365:72-75.
79. Shigemoto R, Nakanishi S, Mizuno N (1992) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: an in situ hybridization study in adult and developing rat. J Comp Neurol 322:121-135.
80. Shigemoto R. Nomura S, Ohishi H, Sugihara H, Nakanishi S, Mizuno N (1993) Immunohistochemical localization of a metabotropic glutamate receptor, mGluR5, in the rat brain. Neurosci Lett 163:53-57.
81. Shigemoto R, Abe T, Nomura S, Nakanishi S, Hirano T (1994) Antibodies inactivating mGluR1 metabotropic glutamate receptor block long-term depression in cultured Purkinje cells. Neuron 12:1245-1255.
82. Shigemoto R, Wada E, Ohishi H, Takada M, Mizuno N, Roberts JDB, Somogyi P (1995) Differential presynaptic localization of metabotropic glutamate receptor subtypes, mGluR2/3 and mGluR7, in the rat hippocampus. Soc Neurosci Abstr 21:846.
83. Shigemoto R, Kulik A, Roberts JDB, Ohishi H, Nusser Z, Kaneko T, Somogyi P (1996) Target-cell-specific concentration of a metabotropic glutamate receptor in the presynaptic active zone. Nature 381:523-525.
84. Steward O (1976) Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J Comp Neurol 167:285-314.
85. Steward O, Scoville SA (1976) Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J Comp Neurol 169:347-370.
86. Swanson LW, Wyss JM, Cowan WM (1978) An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J Comp Neurol 181:681-716.
87. Swartz KJ, Bean BP (1992) Inhibition of calcium channels in rat CA3 pyramidal neurons by a metabotropic glutamate receptor. J Neurosci 12:4358-4371.
88. Takahashi T, Forsythe ID, Tsujimoto T, Barnes-Davies M, Onodera K (1996) Presynaptic calcium current modulation by a metabotropic glutamate receptor. Science 274:594-597.
89. Tanabe Y, Masu M, Ishii T, Shigemoto R, Nakanishi S (1992) A family of metabotropic glutamate receptors. Neuron 8:169-179.
90. Thomson C, Pekhletski, Haldeman B, Gilbert TA, O'hara P, Hampson DR (1997) Cloning and characterization of a metabotropic glutamate receptor, mGluR4b. Neuropharmacology 36:21-30.
91. Wouferlood FG, Saldana E, Witter MP (1990) Projection from the nucleus reuniens thalami to the hippocampal region: light and electron microscopic tracing study in the rat with the anterograde tracer Phaseolus vulgaris-leucoagglutinin. J Comp Neurol 296:179-203.
92. Wyss JM (1981) An autoradiographic study of the efferent connections of the entorhinal cortex in the rat. J Comp Neurol 199:495-512.
93. 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 (1996) Impairment of hippocampal mossy fiber LTD in mice lacking mGluR2. Science 273:645-647.