Metabotropic glutamate receptor agonist-induced hyperpolarizations in rat basolateral amygdala neurons: Receptor characterization and ion channels

Journal of Neurophysiology

Volumn 76, Issue 5, 1996, Pages 3059-3069

  Holmes, Keith H ^a   Keele, N Bradley ^a   Arvanov, Viktor L ^a   Shinnick Gallagher, Patricia ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 AMINO 1,3 CYCLOPENTANEDICARBOXYLIC ACID; 2 (CARBOXYCYCLOPROPYL)GLYCINE; 4 CARBOXYPHENYLGLYCINE; ALPHA METHYL 4 CARBOXYPHENYLGLYCINE; IBOTENIC ACID; METABOTROPIC RECEPTOR; POTASSIUM CHANNEL; QUISQUALIC ACID;

AMYGDALOID NUCLEUS; ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; BRAIN SLICE; CHANNEL GATING; CONTROLLED STUDY; HYPERPOLARIZATION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0029911059     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.76.5.3059     Document Type: Article

References (75)

1. ABE, T., SUGIHARA, H., NAWA, H., SHIGEMOTO, R., MIZUNO, N., AND NAKANISHI, S. Molecular characterization of a novel metabotropic glutamate receptor mGLUR5 coupled to inositol phosphate/Ca signal transduction. J. Biol. Chem. 267: 13361-13368, 1992.
2. BAUDE, A., NUSSER, Z., ROBERTS, J. D. B., MULVIHILL, E., MCILHINNEY, R. A. J., AND SOMOGYI, P. The metabotropic glutamate receptor (mGluR1α) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11: 771-787, 1993.
3. BLATZ, A. L. AND MAGLEBY, K. L. Single apamin-blocked Ca-activated K channels of small conductance in cultured rat skeletal muscle. Nature Lond. 323: 718-720, 1986.
4. BOLSHAKOV, Y. V., GAPON, S. A., AND MAGAZANIK, L. G. Different types of glutamate receptors in isolated and identified neurones of the mollusc Planobarius corneus. J. Physiol. Lond. 439: 15-65, 1991.
5. BOSS, V. AND BOATEN, A. S. An L-cysteine sulfinic acid-sensitive metabotropic receptor mediates increased cAMP accumulation in hippocampal slices. Neurosci. Lett. 184: 1-4, 1995.
6. BOSS, V., NUTT, K. M., AND CONN, P. J. L-Cysteine sulfinic acid as an endogenous agonist of a novel metabotropic receptor coupled to stimulation of phospholipase D activity. J. Pharmacol. Exp. Ther. 45: 1177-1182, 1994.
7. BRABET, I., MARY, S., BOCKAERT, J., AND PIN, J.-P. Phenylglycine derivatives discriminate between mGluR1- and mGluR5-mediated responses. Neuropharmacology 34: 895-903, 1995.
8. CARTMELL, J., CURTIS, A. R., KEMP, J. A., KENDALL, D. A., AND ALEXANDER, S. P. H. Subtypes of metabotropic excitatory amino acid receptor distinguished by stereoisomers of the rigid glutamate analogue, 1-aminocyclopentane-1,3-dicarboxylate. Neurosci. Lett. 153: 107-110, 1993.
9. COLLINGRIDGE, G. L. AND LESTER, R. A. J. Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacol. Rev. 40: 143-210, 1989.
10. DAVIES, C. H., LARKE, V. R. J., JANE, D. E., AND COLLINGRIDGE, G. L. Pharmacology of postsynaptic metabotropic glutamate receptors in rat hippocampal CA1 pyramidal neurones. Br. J. Pharmacol. 11: 1859-1869, 1995.
11. + channel by stimulation of glutamate phosphoinositide-coupled receptors in cultured cerebellar granule cells. Eur. J. Neurosci. 3: 778-789, 1991.
12. FLEISCHER, S. AND INVI, M. Biochemistry and biophysics of excitation-contraction coupling. Annu. Rev. Biophys. Biophys. Chem. 18: 333-364, 1989.
13. FRANCIOLINI, F. Calcium and voltage dependence of single Ca-activated K channels from cultured hippocampal neurons or rat. Biochim. Biophys. Acta 943: 419-427, 1988.
14. GALLAGHER, J. P., ZHENG, F., AND SHINNICK-GALLAGHER, P. Long-lasting modulation of synaptic transmission by metabotropic glutamate receptors. In: Metabotropic Glutamate Receptors, edited by P. J. Conn and J. Patel. Totowa, NJ: Humana, 1994, p. 173-194.
15. GEREAU, R. W. AND CONN, P. J. Roles of specific metabotropic glutamate receptor subtypes in regulation of hippocampal CA1 pyramidal cell excitability. J. Neurophysiol. 74: 122-129, 1995.
16. GLAUM, S. R. AND MILLER, R. J. Inhibition of phosphoprotein phosphatases blocks metabotropic receptor effects in the rat nucleus tractus solitarii. J. Pharmacol. Exp. Ther. 45: 1221-1226, 1994.
17. GLAUM, S. R., SLATER, N. T., ROSSI, D. J., AND MILLER, R. J. Role of metabotropic glutamate (ACPD) receptors at the parallel fiber-Purkinje cell synapse. J. Neurophysiol. 68: 1453-1462, 1992.
18. GUÉRINEAU, N. C., Bossu, J.-L., GÄHWILER, B. H., AND GERBER, U. Activation of a non-selective cationic conductance by metabotropic glutamatergic and muscarinic agonists in CA3 pyramidal neurons of the rat hippocampus. J. Neurosci. 15: 4395-4407, 1995.
19. HAYASHI, Y., SEKIYAMA, N., NAKANISHI, S., JANE, D. E., SUNTER, D. C., BIRSE, E. F., UDVARHELYI, P. M., AND WATKINS, J. C. Analysis of agonist and antagonist activities of phenylglycine derivatives for different cloned metabotropic glutamate receptor subtypes. J. Neurosci. 14: 3370-3377, 1994.
20. HAYASHI, Y., TANABE, Y., ARAMORI, I., MASU, M., SHIMAMOTO, K., OHFUNE, Y., AND NAKANISHI, S. Agonist analysis of 2-(carboxycyclopropyl)glycine isomers for cloned metabotropic glutamate receptor subtypes expressed in chinese hamster ovary cells. Br. J. Pharmacol. 107: 539-543, 1992.
21. HOLMES, K. H., ARVANOV, V. L., KEELE, N. B., AND SHINNICK-GALLACHER, P. Kindling eliminates the mGluR agonist-induced hyperpolarization observed in basolateral amygdala neurons. Soc. Neurosci. Abstr. 20: 410, 1994.
22. HOLMES, K. H., KEELE, N. B., AND SHINNICK-GALLAGHER, P. Loss of mGluR-mediated hyperpolarizations and increase in mGluR depolarizations in basolateral amygdala neurons in kindling-induced epilepsy. J. Neurophysiol. 76: 2808-2812, 1996.
23. HOLMES, K. H., RAINNIE, D. G., AND SHINNICK-GALLAGHER, P. Metabotropic glutamate receptor activation by (1S,3R)-ACPD or 4C3HPG elicits membrane hyperpolarization and depolarization in basolateral amygdala (BLA) neurones. Soc. Neurosci. Abstr. 19: 296, 1993.
24. HOUAMED, K. M., KUIJPER, J. L., GILBERT, T. L., HALDEMAN, B. A., O'HARA, P. J., MULVIHILL, E. R., ALMERS, W., AND HAGEN, S. F. Cloning, expression, and gene structure of a G protein-coupled glutamate receptor from rat brain. Science Wash. DC 252: 1318-1321, 1991.
25. INOUE, T., MIYAKAWA, H., ITO, K., MIKOSHIBA, K., AND KATO, H. A hyperpolarizing response induced by glutamate in mouse cerebellar Purkinje cells. Neurosci. Res. 15: 265-271, 1992.
26. ISHIDA, M., AKAGI, H., SHIMAMOTO, K., OHFUNE, Y., AND SHINOZAKI, H. A potent metabotropic glutamate receptor agonist: electrophysiological actions of a conformationally restricted glutamate analogue in the rat spinal cord and Xenopus oocytes. Brain Res. 537: 311-314, 1990.
27. JANE, D. E., JONES, P. L. S. J., POOK, P. C.-K., TSE, H.-W., AND WATKINS, J. C. Actions of two new antagonists showing selectivity for different sub-types of metabotropic glutamate receptor in the neonatal rat spinal cord. Br. J. Pharmacol. 112: 809-816, 1994.
28. JOLY, C., GOMEZA, J., BRABET, I., CURRY, K., BOCKAERT, J., AND PIN, J.-P. Molecular functional and pharmacological characterization of the metabotropic glutamate receptor type 5 splice variants: comparison with mGluR1. J. Neurosci. 15: 3970-3981, 1995.
29. KATZ, P. S. AND LEVITAN, I. B. Quisqualate and ACPD are agonists for a glutamate-activated current in identified Aplysia neurons. J. Neurophysiol. 69: 143-150, 1993.
30. KEHOE, J. S. Glutamate activates a K conductance increase in Aplysia neurons that appears to be independent of G proteins. Neuron 13: 691-702, 1994.
31. KINZIE, J. M., SAUGSTAD, J. A., WESTBROOK, G. L., AND SEGERSON, T. P. Distribution of metabotropic glutamate receptor 7 messenger RNA in the developing and adult rat brain. Neuroscience 69: 167-176, 1995.
32. KRISTENSEN, P., SUZDAK, P. D., AND THOMSEN, C. Expression pattern and pharmacology of the rat type IV metabotropic glutamate receptor. Neurosci. Lett. 155: 159-162, 1993.
33. LATORRE, R. AND MILLER, C. Conduction and selectivity in potassium channels. J. Membr. Biol. 71: 11-30, 1983.
34. LATORRE, R., OBERHAUSER, A., LABARACA, P., AND ALVAREZ, O. Varieties of calcium-activated potassium channels. Annu. Rev. Physiol. 51: 385-399, 1989.
35. MARTIN, L. J., BLACKSTONE, C. D., HUGANIR, R. L., AND PRICE, D. L. Cellular localization of a metabotropic glutamate receptor in rat brain. Neuron 9: 259-270, 1992.
36. MARTY, A. Ca-dependent K channels with large unitary conductance. Trends Neurosci. 6: 262-265, 1983.
37. MASU, M., TANABE, Y., TSUCHIDA, K., SHIGEMOTO, R., AND NAKANISHI, S. Sequence and expression of a metabotropic glutamate receptor. Nature Lond. 349: 760-765, 1991.
38. MCGREW, S. G., WOLLEBEN, C., SIEGL, P., AND FLEISCHER, S. Positive cooperativity of ryanodine binding to the calcium release channel of sarcoplasmic reticulum from heart and skeletal muscle. Biochemistry 28: 1686-1691, 1989.
39. NAKAJIMA, Y., IWAKABE, H., AKAZAWA, C., NAWA, H., SHIGEMOTO, R., MIZUNO, N., AND NAKANISHI, S. Molecular characterization of a novel retinal metabotropic glutamate receptor mGLUR6 with a high selectivity for L-2-amino-4-phosphonobutyrate. J. Biol. Chem. 268: 11868-11873, 1993.
40. NAKANISHI, S. Molecular diversity of glutamate receptors and implications for brain function. Science Wash. DC 258: 597-603, 1992.
41. OHISHI, H., AKAZAWA, C., SHIGEMOTO, R., NAKANISHI, S., AND MIZUNO, N. 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, 1995.
42. OHISHI, H., SHIGEMOTO, R., NAKANISHI, S., AND MIZUNO, N. Distribution of the messenger RNA for a metabotropic glutamate receptor, mGluR2, in !he central nervous system of the rat. Neuroscience 53: 1009-1018, 1993a.
43. OHISHI, H., SHIGEMOTO, R., NAKANISHI, S., AND 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: 252-266, 1993b.
44. ONOZUKA, M., WATANABE, K., NAGATA, K., AND IMAI, S. Involvement of a Ca/calmodulin-dependent protein kinase II-associated mechanism in the induction of an outward potassium current by quisqualate. Brain Res. 650: 336-340, 1994.
45. PALMER, E., MONAGHAN, D. T., AND COTMAN, C. W. Trans-ACPD, a selective agonist of the phosphoinositide-coupled excitatory amino acid receptor. Eur. J. Pharmacol. 166: 585-587, 1989.
46. PAXINOS, G. AND WATSON, C. The Rat Brain in Stereotaxic Co-Ordinates. New York: Academic, 1986.
47. +-currents in bullfrog sympathetic ganglion cells. Proc. Natl. Acad. Sci. USA 82: 3040-3044, 1985.
48. PICKERING, D. S., THOMSEN, C., SUZDAK, P. D., FLETCHER, E. J., ROBITAILLE, R., SALTER, M. W., MACDONALD, J. F., HUANG, X., AND HAMPSON, P. R. A comparison of two alternatively spliced forms of a metabotropic glutamate receptor coupled to phosphoinositides turnover. J. Neurochem. 61: 85-92, 1993.
49. PIN, J.-P. AND DUVOISIN, R. Review: neurotransmitter receptors. I. The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34: 1-26, 1995.
50. PORTER, R. H. AND ROBERTS, P. J. Glutamate metabotropic receptor activation in neonatal rat cerebral cortex by sulphur-containing excitatory amino acids. Neurosci. Lett. 154: 78-80, 1993.
51. RAINNIE, D. G., ASPRODINI, E. K., AND SHINNICK-GALLAGHER, P. Intracellular recordings from morphologically identified neurons of the basolateral amygdala. J. Neurophysiol. 69: 1350-1362, 1993.
52. RAINNIE, D. G., HOLMES, K. H., AND SHINNICK-GALLAGHER, P. Activation of postsynaptic metabotropic glutamate receptors by Trans-ACPD hyperpolarizes neurons of the basolateral amygdala. J. Neurosci. 14: 7208-7220, 1994.
53. REINHART, P. H., CHUNG, S., MARTIN, B. L., BRAUTIGAN, D. L., AND LEVITAN, I. W. Modulation of calcium-activated potassium channels from rat brain by protein kinase A and phosphatase 2A. J. Neurosci. 11: 1627-1635, 1991.
54. ROBERTS, P. J. Review: pharmacological tools for the investigation of metabotropic glutamate receptors (mGluRs): phenylglycine derivatives and other selective antagonists - an update. Neuropharmacology 34: 813-819, 1995.
55. ROMANO, C., SESMA, M. A., MCDONALD, C. T., O'MALLEY, K., VANDENPOL, A. N., AND OLNEY, J. W. Distribution of metabotropic glutamate receptor mGluR5 immunoreactivity in rat brain. J. Comp. Neurol. 355: 455-469, 1995.
56. SCHOEPP, D. D., JOHNSON, B. G., SOLHOFF, C. R., WRIGHT, R. A., GOLDSWORTHY, J. S., AND BAKER, S. R. Second-messenger responses in brain slices to elucidate novel glutamate receptors. J. Neurosci. Methods 59: 105-110, 1995.
57. SHIGEMOTO, R., NAKANISHI, S., AND MIZUNO, N. 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, 1992.
58. SHINNICK-GALLAGHER, P., ARVANOV, V. L., STEINSLAND, O., AND HOLMES, K. H. mGluR agonist-induced hyperpolarizations in basolateral amygdala neurons: receptor characterization and ion channels. Soc. Neurosci. Abstr. 20: 640, 1994.
59. SHIRASAKI, T., HARATA, H., AND AKAIKE, N. Metabotropic glutamate response in acutely dissociated hippocampal CA1 pyramidal neurones of the rat. J. Physiol. Lond. 475: 439-453, 1994.
60. STAUB, C., VRANESIC, I., AND KNÖPFEL, T. Responses to metabotropic glutamate receptor activation in cerebellar Purkinje cells: induction of on inward current. Eur. J. Neurosci. 4: 832-839, 1992.
61. TANABE, Y., MASU, M., ISHII, T., SHIGEMOTO, R., AND NAKANISHI, S. A family of metabotropic glutamate receptors. Neuron 8: 169-179, 1992.
62. TANABE, Y., NOMURA, A., MASU, M., SHIGEMOTO, R., MEZUNO N., AND NAKANISHI, S. Signal transduction, pharmacological properties, and expression patterns of two rat at metabotropic glutamate receptors, mGluR3 and mGluR4. J. Neurosci. 13: 1372-1378, 1993.
63. TAUBE, J. S. AND SCHWARTZKROIN, P. A. Hyperpolarizing responses to application of glutamate in hippocampal CA1 pyramidal neurons. Neurosci. Lett. 78: 85-90, 1987.
64. THOMSEN, C., BOEL, E., AND SUZDAK, P. Actions of phenylglycine analogs at subtypes of the metabotropic glutamate receptor family. Eur. J. Pharmacol. 267: 77-84, 1994.
65. TSENG-CRANK, J., FOSTER, C. D., KRAUSE, J. D., MERTZ, R., GODINOT, N., DICHIARA, T. J., AND REINHART, P. H. Cloning, expression, and distribution of functionally distinct Ca-activated K channel isoforms from human brain. Neuron 13: 1315-1330, 1994.
66. VIGNES, M., CLARKE, V. R. J., DAVIES, C. H., CHAMBERS, A., JANE, D. E., WATKINS, J. C., AND COLLINGRIDGE, G. L. Pharmacological evidence for an involvement of group II and group III mGluRs in the presynaptic regulation of excitatory synaptic responses in the CA1 region of rat hippocampal slices. Neuropharmacology 34: 973-982, 1995.
67. VRANESIC, I., STAUB, C., AND KNOPFEL, T. Activation of metabotropic glutamate receptors induces an outward current which is potentiated by methylxanthines in rat cerebellar Purkinje cells. Neurosci. Res. 16: 209-215, 1993.
68. WANN, K. T. AND RICHARDS, C. D. Properties of single calcium-activated potassium channels of large conductance in rat hippocampal neurons in culture. Eur. J. Neurosci. 6: 607-617, 1994.
69. WATANABE, K. AND ONOZUKA, M. Glutamate elicits an outward K current which is normally suppressed by a Ca/calmodulin-dependent protein kinase II. Brain Res. 654: 352-356, 1994.
70. WATKINS, J. C. AND COLLINGRIDGE, G. L. Phenylglycine derivatives as antagonists of metabotropic receptors. Trends Pharmacol. Sci. 14: 333-342, 1994.
71. WINDER D. G., AND CONN, P. J. Activation of metabotropic glutamate receptors in the hippocampus increases cyclic AMP accumulation. J. Neurochem. 59: 375-378, 1992.
72. WINDER, D. G. AND CONN, P. J. Activation of metabotropic glutamate receptors increases cAMP accumulation in hippocampus by potentiating responses to endogenous adenosine. J. Neurosci. 13: 38-44, 1993.
73. YOSHIDA, A., ODA, M., AND IKEMOTO, Y. Kinetics of the Ca-activated K channel in rat hippocampal neurons. Jpn. J. Physiol. 41: 297-315, 1991.
74. ZHENG, F. AND GALLAGHER J. P. Pharmacologically distinct, pertussis toxin-resistant inward currents evoked by metabotropic glutamate receptor (mGluR) agonists in dorsolateral septal nucleus (DLSN) neurons. J. Neurosci. 15: 504-510, 1995.
75. ZHENG, F., HASUO, H., AND GALLAGHER, J. P. 1S,3S-ACPD preferring inward current is mediated by a novel excitatory amino acid receptor. Neuropharmacology 34: 905-917, 1995.