Role of P/Q-Ca2+ Channels in Metabotropic Glutamate Receptor 2/3-Dependent Presynaptic Long-Term Depression at Nucleus Accumbens Synapses

Journal of Neuroscience

Volumn 22, Issue 11, 2002, Pages 4346-4356

  Robbe, David ^a   Alonso, Gérard ^a   Chaumont, Séverine ^b   Bockaert, Joël ^a   Manzoni, Olivier J ^a  

^a CNRS   (France)

^b INSTITUTE OF HUMAN GENETICS   (France)

Author keywords

Calcium channels; Long term depression; Metabotropic glutamate receptors; mGlu2 3; Mice; Nucleus accumbens; Prelimbic cortex; Presynaptic inhibition

Indexed keywords

CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; CYCLIC AMP DEPENDENT PROTEIN KINASE; EGLUMETAD; GLUTAMIC ACID; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR 3; OMEGA AGATOXIN VIA; PROTEIN KINASE; UNCLASSIFIED DRUG; 2 AMINO 2 (2 CARBOXYCYCLOPROPYL) 3 (XANTHEN 9 YL)PROPIONIC ACID; AMINO ACID; AMINO ACID RECEPTOR BLOCKING AGENT; AMINO ACID RECEPTOR STIMULATING AGENT; BICYCLO COMPOUND; CALCIUM; CALCIUM CHANNEL; CALCIUM CHANNEL BLOCKING AGENT; XANTHENE DERIVATIVE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; DENDRITE; DEPRESSION; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; GLIA; IMMUNOHISTOCHEMISTRY; LIMBIC CORTEX; MOUSE; NERVE CELL PLASTICITY; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEUS ACCUMBENS; PERIKARYON; PRIORITY JOURNAL; SYNAPSE; SYNAPTIC TRANSMISSION; TISSUE PREPARATION; ANIMAL; C57BL MOUSE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; IN VITRO STUDY; MALE; METABOLISM; NERVE CELL INHIBITION; PATCH CLAMP; PHYSIOLOGY; SIGNAL TRANSDUCTION; SYNAPTOSOME;

AMINO ACIDS; ANIMALS; BICYCLO COMPOUNDS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS; CALCIUM CHANNELS, P-TYPE; CALCIUM CHANNELS, Q-TYPE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; MALE; MICE; MICE, INBRED C57BL; NEURAL INHIBITION; NEURONAL PLASTICITY; NUCLEUS ACCUMBENS; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION; XANTHENES;

EID: 0036616837     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-11-04346.2002     Document Type: Article

References (68)

1. Anwyl R (1999) Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Brain Res Rev 29:83-120.
2. Bergles DE, Jahr CE (1998) Glial contribution to glutamate uptake at Schaffer collateral-commissural synapses in the hippocampus. J Neurosci 18:7709-7716.
3. Brandon EP, Zhuo M, Huang YY, Qi M, Gerhold KA, Burton KA, Kandel ER, McKnight GS, Idzerda RL (1995) Hippocampal long-term depression and depotentiation are defective in mice carrying a targeted disruption of the gene encoding the RI beta subunit of cAMP-dependent protein kinase. Proc Natl Acad Sci USA 92:8851-8855.
4. Cartmell J, Schoepp DD (2000) Regulation of neurotransmitter release by metabotropic glutamate receptors. J Neurochem 75:889-907.
5. Cartmell J, Monn JA, Schoepp DD (1999) The metabotropic glutamate 2/3 receptor agonists LY354740 and LY379268 selectively attenuate phencyclidine versus d-amphetamine motor behaviors in rats. J Pharmacol Exp Ther 291:161-170.
6. Cartmell J, Monn JA, Schoepp DD (2000a) Attenuation of specific PCP-evoked behaviors by the potent mGlu2/3 receptor agonist, LY379268 and comparison with the atypical antipsychotic, clozapine. Psychopharmacology 148:423-429.
7. Cartmell J, Monn JA, Schoepp DD (2000b) The mGlu(2/3) receptor agonist LY379268 selectively blocks amphetamine ambulations and rearing. Eur J Pharmacol 400:221-224.
8. Casado M, Dieudonne S, Ascher P (2000) Presynaptic NMDA receptors at the parallel fiber-Purkinje cell synapse. Proc Natl Acad Sci USA 97:11593-11597.
9. Chavis P, Shinozaki H, Bockaert J, Fagni L (1994) The metabotropic glutamate receptor types 2/3 inhibit L-type calcium channels via a pertussis toxin-sensitive G-protein in cultured cerebellar granule cells. J Neurosci 14:7067-7076.
10. 2+ channels involves multiple receptor sub-types in cortical neurons. J Neurosci 16:36-45.
11. Conn PJ, Pin JP (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37:205-237.
12. 2+ channels expressed in Xenopus oocytes. Neurosci Lett 217:13-16.
13. Fundytus ME, Coderre TJ (1997) Attenuation of precipitated morphine withdrawal symptoms by acute i.c.v. administration of a group II mGluR agonist. Br J Pharmacol 121:511-514.
14. Fundytus ME, Ritchie J, Coderre TJ (1997) Attenuation of morphine withdrawal symptoms by subtype-selective metabotropic glutamate receptor antagonists. Br J Pharmacol 120:1015-1020.
15. Glaum SR, Miller RJ (1995) Presynaptic metabotropic glutamate receptors modulate omega-conotoxin-GVIA-insensitive calcium channels in the rat medulla. Neuropharmacology 34:953-964.
16. Helton DR, Tizzano JP, Monn JA, Schoepp DD, Kallman MJ (1997) LY354740: a metabotropic glutamate receptor agonist which ameliorates symptoms of nicotine withdrawal in rats. Neuropharmacology 36:1511-1516.
17. Helton DR, Tizzano JP, Monn JA, Schoepp DD, Kallman MJ (1998) Anxiolytic and side-effect profile of LY354740: a potent, highly selective, orally active agonist for group II metabotropic glutamate receptors. J Pharmacol Exp Ther 284:651-660.
18. Horne AL, Woodruff GN, Kemp JA (1990) Synaptic potentials mediated by excitatory amino acid receptors in the nucleus accumbens of the rat, in vitro. Neuropharmacology 29:917-921.
19. Huang CC, Hsu KS, Gean PW (1996) Isoproterenol potentiates synaptic transmission primarily by enhancing presynaptic calcium influx via P- and/or Q-type calcium channels in the rat amygdala. J Neurosci 16:1026-1033.
20. Huang CC, Wang SJ, Gean PW (1998) Selective enhancement of P-type calcium currents by isoproterenol in the rat amygdala. J Neurosci 18:2276-2282.
21. Huang L, Killbride J, Rowan MJ, Anwyl R (1999) Activation of mGlu-RII induces LTD via activation of protein kinase A and protein-kinase C in the dentate gyrus of the hippocampus in vitro. Neurophatmacology 38:73-83.
22. Huang LQ, Rowan MJ, Anwyl R (1997) mGluR II agonist inhibition of LTP induction, and mGluR II antagonist inhibition of LTD induction, in the dentate gyrus in vitro. NeuroReport 8:687-693.
23. Huang YY, Li XC, Kandel ER (1994) cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 79:69-79.
24. Kahn L, Alonso G, Robbe D, Bockaert J, Manzoni OJ (2001) Group 2 metabotropic glutamate receptors induced long-term depression in mouse striatal slices. Neurosci Lett 316:178-183.
25. 2+ channels by cyclic nucleotides and G-proteins. Life Sci 62:1543-1547.
26. Kobayashi K, Manabe T, Takahashi T (1996) Presynaptic long-term depression at the hippocampal mossy fiber-CA3 synapse. Science 273:648-650.
27. Kombian SB, Malenka RC (1994) Simultaneous LTP of non-NMDA and LTD of NMDA-receptor-mediated responses in the nucleus accumbens. Nature 368:242-246.
28. Lin HC, Wang SJ, Luo MZ, Gean PW (2000) Activation of group II metabotropic glutamate receptors induces long-term depression of synaptic transmission in the rat amygdala. J Neurosci 20:9017-9024.
29. Manzoni O, Prezeau L, Sladeczek F, Bockaert J (1992) Trans-ACPD inhibits cAMP formation via a pertussis toxin-sensitive G-protein. Eur J Pharmacol 225:357-358.
30. Manzoni O, Michel JM, Bockaert J (1997) Metabotropic glutamate receptors in the rat nucleus accumbens. Eur J Neurosci 9:1514-1523.
31. Manzoni O, Pujalte D, Williams J, Bockaert J (1998) Decreased presynaptic sensitivity to adenosine after cocaine withdrawal. J Neurosci 18:7996-8002.
32. Manzoni OJ, Williams JT (1999) Presynaptic regulation of glutamate release in the ventral tegmental area during morphine withdrawal. J Neurosci 19:6629-6636.
33. Martin G, Przewlocki R, Siggins GR (1999) Chronic morphine treatment selectively augments metabotropic glutamate receptor-induced inhibition of N-methyl-D-aspartate receptor-mediated neurotransmission in nucleus accumbens. J Pharmacol Exp Ther 288:30-35.
34. Meir A, Ginsburg S, Butkevich A, Kachalsky SG, Kaiserman I, Ahdut R, Demirgoren S, Rahamimoff R (1999) Ion channels in presynaptic nerve terminals and control of transmitter release. Physiol Rev 79:1019-1088.
35. Miller RJ (1990) Receptor-mediated regulation of calcium channels and neurotransmitter release. FASEB J 4:3291-3299.
36. Mineff E, Valtschanoff J (1999) Metabotropic glutamate receptors 2 and 3 expressed by astrocytes in rat ventrobasal thalamus. Neurosci Lett 270:95-98.
37. Ohishi H, Shigemoto R, Nakanishi S, Mizumo N (1993a) Distribution of the mRNA for a metabotropic glutamate receptors, mGluR2 in the central nervous system of the rat. Neuroscience 53:1009-1018.
38. Ohishi H, Shigemoto R, Nakanishi S, Mizumo N (1993b) Distribution of the mRNA for a metabotropic glutamate receptors, mGluR3 in the rat brain: an in situ hybridization study. J Comp Neurol 335:252-266.
39. Ohishi H, Neki A, Mizumo N (1998) Distribution of a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat and mouse: an immunohistochemical study with a monoclonal antibody. Neurosci Res 30:65-82.
40. Oliet SH, Malenka RC, Nicoll RA (1997) Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron 18:969-982.
41. 3H]LY341495, a highly potent, selective and novel-radio-ligand for labeling Group II metabotropic glutamate receptors. Bioorg Med Chem Lett 8:1919-1922.
42. Otani S, Auclair N, Desce JM, Roisin MP, Crepel F (1999) Dopamine receptors and groups I and II mGluRs cooperate for long-term depression induction in rat prefrontal cortex through converging postsyhaptic activation of MAP kinases. J Neurosci 19:9788-9802.
43. Parnas H, Segel L, Dudel J, Parnas I (2000) Autoreceptors, membrane potential and the regulation of transmitter release. Trends Neurosci 23:60-68.
44. Paxinos G, Franklin KBJ (2001) The mouse brain atlas in stereotaxic coordinates. San Diego: Academic.
45. Pennartz CMA, Ameerun RF, Groenewegen HJ, Lopes da Silva FH (1993) Synaptic plasticity in an vitro slice preparation of the rat nucleus accumbens. Eur J Neurosci 5:107-117.
46. Pennartz CMA, Groenewegen HJ, Lopes da Silva FH (1994) The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioral, electrophysiological and anatomical data. Prog Neurobiol 42:719-761.
47. Petralia RS, Wang YX, Niedzielski AS, Wenthold RJ (1996) The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neuroscience 71:949-976.
48. Pin JP, De Colle C, Bessis AS, Acher F (1999) New perspectives for the development of selective metabotropic glutamate receptor ligands. Eur J Pharmacol 375:277-294.
49. Prézeau L, Manzoni O, Homburger V, Sladeczeck F, Curry K, Bockaert J (1992) Characterization of a metabotropic glutamate receptor: direct negative coupling to adenylate cyclase and involvement of a pertussis toxin-sensitive G protein. Proc Natl Acad Sci USA 89:8040-8044.
50. Qi M, Zhuo M, Skalhegg BS, Brandon EP, Kandel ER, McKnight GS, Idzerda RL (1996) Impaired hippocampal plasticity in mice lacking the Cbeta1 catalytic subunit of cAMP-dependent protein kinase. Proc Natl Acad Sci USA 93:1571-1576.
51. Robbe D, Alonso G, Duchamp F, Bockaert J, Manzoni OJ (2001) Localization and mechanisms of action of cannabinoid receptors at the glutamatergic synapses of the mouse nucleus accumbens. J Neurosci 21:109-116.
52. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kanai Y, Hediger MA, Wang Y, Schielke JP, Welty DF (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16:675-686.
53. 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.
54. Schacter GB, Yang CR, Innis NK, Mogenson GJ (1989) The role of hippocampal-nucleus accumbens pathway in radial-arm maze performance. Brain Res 494:339-349.
55. Schoepp DD, Johnson BG, Wright RA, Salhoff CR, Mayne NG, Wu S, Cockerman SL, Burnett JP, Belegaje R, Bleakman D, Monn JA (1997) LY354740 is a potent and highly selective group II metabotropic glutamate receptor agonist in cells expressing human glutamate receptors. Neuropharmacology 36:1-11.
56. Seamon KB, Daly JW (1986) Forskolin: its biological and chemical properties. Adv Cyclic Nucleotide Protein Phosphorylation Res 20:1-150.
57. Shigemoto R, Nomura S, Ohishi H, Sugihara H, Nakanishi S, Mizumo N (1993) Immunohistochemical localization of a metabotropic glutamate receptor, mGluR5, in the rat brain. Neurosci Lett 163:53-57.
58. Stefani A, Pisani A, Mercuri NB, Calabresi P (1996) The modulation of calcium currents by the activation of mGluRs. Functional implications. Mol Neurobiol 13:81-95.
59. Sudhof TC (2001) The synaptic vesicle cycle revisited. Neuron 28:317-320.
60. Surmeier DJ, Bargas J, Hemmings HC, Nairn AC, Greengard P (1995) Modulation of calcium currents by a D1 dopaminergic protein kinase/ phosphatase cascade in rat neostriatal neurons. Neuron 14:385-397.
61. Tamaru Y, Nomura N, Mizuno N, Shigemoto R (2001) Distribution of metabotropic glutamate receptor mGlu3 in the mouse CNS: differential location relative to pre- and postsynaptic sites. Neuroscience 106:481-503.
62. Thomson AM (2000a) Facilitation, augmentation and potentiation at central synapses. Trends Neurosci 23:305-312.
63. Thomson AM (2000b) Molecular frequency filters at central synapses. Prog Neurobiol 62:159-196.
64. Tzounopoulos T, Janz R, Sudhof TC, Nicoll RA, Malenka RC (1998). A role for cAMP in long-term depression at hippocampal mossy fiber synapses. Neuron 21:837-845.
65. Weisskopf MG, Castillo PE, Zalutsky RA, Nicoll RA (1993) Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science 265:1878-1882.
66. Wu LG, Saggau P (1997) Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci 20:204-212.
67. 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.
68. Zucker RS (1999) Calcium- and activity-dependent synaptic plasticity. Curr Opin Neurobiol 9:305-313.