Group II mGluR-induced long term depression in the dentate gyrus in vivo is NMDA receptor-independent and does not require protein synthesis

Neuropharmacology

Volumn 49, Issue SUPPL., 2005, Pages 1-12

  Pöschel, Beatrice ^a,b   Manahan Vaughan, Denise ^a,b  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Hippocampus; In vivo; mGlu receptor; Synaptic plasticity

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 4 CARBOXY 3 HYDROXYPHENYLGLYCINE; ANISOMYCIN; CALCIUM; CALCIUM CHANNEL L TYPE; DACTINOMYCIN; MESSENGER RNA; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR 3; METABOTROPIC RECEPTOR AGONIST; N ACETYLASPARTYLGLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NEUROTRANSMITTER RECEPTOR; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL EXPERIMENT; ARTICLE; BRAIN VENTRICLE; CANNULA; CELL FUNCTION; DENTATE GYRUS; ELECTRODE; EVOKED RESPONSE; IMPLANTATION; IN VIVO STUDY; LONG TERM DEPRESSION; MALE; MESSENGER RNA SYNTHESIS; NONHUMAN; PERFORANT NERVE TRACT; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTEIN SYNTHESIS INHIBITION; RAT; SYNAPSE;

2-AMINO-5-PHOSPHONOVALERATE; ANALYSIS OF VARIANCE; ANIMALS; ANISOMYCIN; CALCIUM CHANNEL BLOCKERS; DENTATE GYRUS; DIPEPTIDES; DRUG INTERACTIONS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; FUNCTIONAL LATERALITY; GLYCINE; LONG-TERM DEPRESSION (PHYSIOLOGY); MALE; NEUROPROTECTIVE AGENTS; PROTEIN SYNTHESIS INHIBITORS; RATS; RATS, WISTAR; RECEPTORS, METABOTROPIC GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; TIME FACTORS; VERAPAMIL;

EID: 23644441520     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2005.06.018     Document Type: Article

References (74)

1. T. Abe, H. Sugihara, H. Nawa, R. Shigemoto, N. Mizuno, and S. Nakanishi Molecular characterization of a novel metabotropic glutamate receptor mGluR5 coupled to inositol phosphate/Ca2+ signal transduction J. Biol. Chem. 267 1992 13361 13368
2. R. Anwyl Metabotropic glutamate receptors: electrophysiological properties and role in plasticity Brain Res. Brain Res. Rev. 29 1999 83 120
3. I. Aramori, and S. Nakanishi Signal transduction and pharmacological characteristics of a metabotropic glutamate receptor, mGluR1, in transfected CHO cells Neuron 8 1992 757 765
4. E. Aronica, J.A. Gorter, H. Ijlst-Keizers, A.J. Rozemuller, B. Yankaya, S. Leenstra, and D. Troost Expression and functional role of mGluR3 and mGluR5 in human astrocytes and glioma cells: opposite regulation of glutamate transporter proteins Eur. J. Neurosci. 17 10 2003 2106 2118
5. C.P. Bailey, J.A. Trejos, F.A. Schanne, and P.K. Stanton Pairing elevation of [cyclic GMP] with inhibition of PKA produces long-term depression of glutamate release from isolated rat hippocampal presynaptic terminals Eur. J. Neurosci. 17 2003 903 908
6. T.G. Banke, D. Bowie, H. Lee, R.L. Huganir, A. Schousboe, and S.F. Traynelis Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase J. Neurosci. 20 2000 89 102
7. G. Barrionuevo, F. Schottler, and G. Lynch The effects of repetitive low frequency stimulation on control and "potentiated" synaptic responses in the hippocampus Life Sci. 27 1980 2385 2391
8. R. Bergeron, J.T. Coyle, G. Tsai, and R.W. Greene NAAG reduces NMDA receptor current in CA1 hippocampal pyramidal neurons of acute slices and dissociated neurons Neuropsychopharmacology 30 2005 7 16
9. R.D. Blakely, M.B. Robinson, R.C. Thompson, and J.T. Coyle Hydrolysis of the brain dipeptide N-acetyl-l-aspartyl-l-glutamate: subcellular and regional distribution, ontogeny, and the effect of lesions on N-acetylated-alpha-linked acidic dipeptidase activity J. Neurochem. 50 1988 1200 1209
10. V.Y. Bolshakov, and S.A. Siegelbaum Postsynaptic induction and presynaptic expression of hippocampal long-term depression Science 264 1994 1148 1152
11. K.H. Braunewell, and D. Manahan-Vaughan Long-term depression: a cellular basis for learning? Rev. Neurosci. 12 2 2001 121 140 (Review)
12. A.L. Buller, H.C. Larson, B.E. Schneider, J.A. Beaton, R.A. Morrisett, and D.T. Monaghan The molecular basis of NMDA receptor subtypes: native receptor diversity is predicted by subunit composition J. Neurosci. 14 1994 5471 5484
13. N. Camodeca, N.A. Breakwell, M.J. Rowan, and R. Anwyl Induction of LTD by activation of group I mGluR in the dentate gyrus in vitro Neuropharmacology 38 10 1999 1597 1606
14. R.C. Carroll, D.V. Lissin, M. von Zastrow, R.A. Nicoll, and R.C. Malenka Rapid redistribution of glutamate receptors contributes to long-term depression in hippocampal cultures Nat. Neurosci. 2 1999 454 460
15. P. Chavis, H. Shinozaki, J. Bockaert, and L. Fagni 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 1994 7067 7076
16. B.R. Christie, J.C. Magee, and D. Johnston The role of dendritic action potentials and Ca2+ influx in the induction of homosynaptic long-term depression in hippocampal CA1 pyramidal neurons Learn. Mem. 3 1996 160 169
17. B.R. Christie, L.K. Schexnayder, and D. Johnston Contribution of voltage-gated Ca2+ channels to homosynaptic long-term depression in the CA1 region in vitro J. Neurophysiol. 77 1997 1651 1655
18. P.J. Conn, and J.P. Pin Pharmacology and functions of metabotropic glutamate receptors Annu. Rev. Pharmacol. Toxicol. 37 1997 205 237
19. J.T. Coyle The nagging question of the function of N- acetylaspartylglutamate Neurobiol. Dis. 4 1997 231 238
20. J.A. Cummings, R.M. Mulkey, R.A. Nicoll, and R.C. Malenka Ca2+ signaling requirements for long-term depression in the hippocampus Neuron 16 1996 825 833
21. S.M. Dudek, and M.F. Bear Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-d-aspartate receptor blockade Proc. Natl Acad. Sci. U.S.A. 89 1992 4363 4367
22. M.D. Ehlers Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting Neuron 28 2000 511 525
23. M.D. Ehlers Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system Nat. Neurosci. 6 2003 231 242
24. J.A. Esteban, S.H. Shi, C. Wilson, M. Nuriya, R.L. Huganir, and R. Malinow PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity Nat. Neurosci. Feb 2003 136 143
25. S. Ghose, B. Wroblewska, L. Corsi, D.R. Grayson, A.L. De Blas, S. Vicini, and J.H. Neale N-acetylaspartylglutamate stimulates metabotropic glutamate receptor 3 to regulate expression of the GABA(A) alpha6 subunit in cerebellar granule cells J. Neurochem. 69 1997 2326 2335
26. Y. Hayashi, N. Sekiyama, S. Nakanishi, D.E. Jane, D.C. Sunter, E.F. Birse, P.M. Udvarhelyi, and J.C. Watkins Analysis of agonist and antagonist activities of phenylglycine derivatives for different cloned metabotropic glutamate receptor subtypes J. Neurosci. 14 1994 3370 3377
27. L.Q. Huang, M.J. Rowan, and R. Anwyl mGluR II agonist inhibition of LTP induction, and mGluR II antagonist inhibition of LTD induction, in the dentate gyrus in vitro Neuroreport 8 1997 687 693
28. L. Huang, M.J. Rowan, and R. Anwyl Induction of long-lasting depression by (+)-alpha-methyl-4-carboxyphenylglycine and other group II mGlu receptor ligands in the dentate gyrus of the hippocampus in vitro Eur. J. Pharmacol. 366 1999 151 158
29. L. Huang, J. Killbride, M.J. Rowan, and R. Anwyl Activation of mGluRII induces LTD via activation of protein kinase A and protein kinase C in the dentate gyrus of the hippocampus in vitro Neuropharmacology 38 1999 73 83
30. K.M. Huber, M.S. Kayser, and M.F. Bear Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression Science 288 2000 1254 1257
31. D.E. Jane, N.K. Thomas, H.W. Tse, and J.C. Watkins Potent antagonists at L-AP4- and (1S,3S)-ACPD-sensitive presynaptic metabotropic glutamate receptors in neonatal rat spinal cord Neuropharmacology 35 1996 1029
32. K. Kameyama, H.K. Lee, M.F. Bear, and R.L. Huganir Involvement of a postsynaptic protein kinase A substrate in the expression of homosynaptic long-term depression Neuron 21 1998 1163 1175
33. N. Kemp, and Z.I. Bashir Long-term depression: a cascade of induction and expression mechanisms Prog. Neurobiol. 65 2001 339 365
34. F. Knoflach, and J.A. Kemp Metabotropic glutamate group II receptors activate a G protein-coupled inwardly rectifying K+ current in neurones of the rat cerebellum J. Physiol. 509 1998 347 354
35. A. Kulla, K.G. Reymann, and D. Manahan-Vaughan Time-dependent induction of depotentiation in the dentate gyrus of freely moving rats: involvement of group 2 metabotropic glutamate receptors Eur. J. Neurosci. 11 1999 3864 3872
36. H.K. Lee, K. Kameyama, R.L. Huganir, and M.F. Bear NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus Neuron 21 1998 1151 1162
37. H.K. Lee, M. Barbarosie, K. Kameyama, M.F. Bear, and R.L. Huganir Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity Nature 405 2000 955 959
38. J. Lisman A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory Proc. Natl Acad. Sci. U.S.A. 86 1989 9574 9578
39. L. Liu, T.P. Wong, M.F. Pozza, K. Lingenhoehl, Y. Wang, M. Sheng, Y.P. Auberson, and Y.T. Wang Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity Science 304 2004 1021 1024
40. G. Losi, S. Vicini, and J. Neale NAAG fails to antagonize synaptic and extrasynaptic NMDA receptors in cerebellar granule neurons Neuropharmacology 46 2004 490 496
41. D. Manahan-Vaughan, and K.G. Reymann Regional and developmental profile of modulation of hippocampal synaptic transmission and LTP by AP4-sensitive mGluRs in vivo Neuropharmacology 34 1995 991 1001
42. D. Manahan-Vaughan, and K.G. Reymann 1S,3R-ACPD dose dependently induces a slow onset potentiation in the dentate gyrus in vivo Eur. J. Pharmacol. 294 1995 497 503
43. D. Manahan-Vaughan, and K.G. Reymann Group 1 metabotropic glutamate receptors contribute to slow-onset potentiation in the rat CA1 region in vivo Neuropharmacology 36 1997 1533 1538
44. D. Manahan-Vaughan Group 1 and 2 metabotropic glutamate receptors play differential roles in hippocampal long-term depression and long-term potentiation in freely moving rats J. Neurosci. 17 1997 3303 3311
45. D. Manahan-Vaughan Priming of group 2 metabotropic glutamate receptors facilitates induction of long-term depression in the dentate gyrus of freely moving rats Neuropharmacology 37 1998 1459 1464
46. D. Manahan-Vaughan, K.H. Braunewell, and K.G. Reymann Subtype-specific involvement of metabotropic glutamate receptors in two forms of long-term potentiation in the dentate gyrus of freely moving rats Neuroscience 86 1998 709 721
47. D. Manahan-Vaughan, A. Kulla, and J.U. Frey Requirement of translation but not transcription for the maintenance of long-term depression in the CA1 region of freely moving rats J. Neurosci. 20 2000 8572 8576
48. Naie, K., Manahan-Vaughan, D., 2005. Investigations of the protein synthesis dependency of mGluR-induced long-term depression in the dentate gyrus of freely moving rats. Neuropharmacology, in press. doi:10.1016/j.neuropharm. 2005.06.001
49. Y. Nakajima, H. Iwakabe, C. Akazawa, H. Nawa, R. Shigemoto, N. Mizuno, and S. Nakanishi 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
50. H. Ohishi, R. Shigemoto, S. Nakanishi, and N. Mizuno 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
51. N. Okamoto, S. Hori, C. Akazawa, Y. Hayashi, R. Shigemoto, N. Mizuno, and S. Nakanishi Molecular characterization of a new metabotropic glutamate receptor mGluR7 coupled to inhibitory cyclic AMP signal transduction J. Biol. Chem. 269 1994 1231 1236
52. S.M. O'Mara, M.J. Rowan, and R. Anwyl Metabotropic glutamate receptor-induced homosynaptic long-term depression and depotentiation in the dentate gyrus of the rat hippocampus in vitro Neuropharmacology 34 1995 983 989
53. M.J. Palmer, A.J. Irving, G.R. Seabrook, D.E. Jane, and G.L. Collingridge The group I mGlu receptor agonist DHPG induces a novel form of LTD in the CA1 region of the hippocampus Neuropharmacology 36 1997 1517 1532
54. Pöschel, B., Wroblewska, B., Heinemann, U., Manahan-Vaughan, D. The metabotropic glutamate receptor mGluR3 is critically required for hippocampal long-term depression and modulates long term potentiation in the dentate gyrus of freely moving rats. Cereb. Cortex., in press.
55. 3H]norepinephrine release from rat hippocampal slices J. Pharmacol. Exp. Ther. 266 1993 796 803
56. K.W. Roche, R.J. O'Brien, A.L. Mammen, J. Bernhardt, and R.L. Huganir Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit Neuron 16 1996 1179 1188
57. E.R. Sanabria, K.M. Wozniak, B.S. Slusher, and A. Keller GCP II (NAALADase) inhibition suppresses mossy fiber-CA3 synaptic neurotransmission by a presynaptic mechanism J. Neurophysiol. 91 2004 182 193
58. L. Santschi, M. Reyes-Harde, and P.K. Stanton Chemically induced, activity-independent LTD elicited by simultaneous activation of PKG and inhibition of PKA J. Neurophysiol. 82 1999 1577 1589
59. M. Scanziani, B.H. Gahwiler, and S.M. Thompson Presynaptic inhibition of excitatory synaptic transmission by muscarinic and metabotropic glutamate receptor activation in the hippocampus: are Ca2+ channels involved? Neuropharmacology 34 1995 1549 1557
60. R. Schnabel, I.C. Kilpatrick, and G.L. Collingridge An investigation into signal transduction mechanisms involved in DHPG-induced LTD in the CA1 region of the hippocampus Neuropharmacology 38 1999 1585 1596
61. D. Sharon, D. Vorobiov, and N. Dascal Positive and negative coupling of the metabotropic glutamate receptors to a G protein-activated K+ channel, GIRK, in Xenopus oocytes J. Gen. Physiol. 109 1997 477 490
62. E. Shave, L. Pliss, M.L. Lawrance, T. FitzGibbon, F. Stastny, and V.J. Balcar Regional distribution and pharmacological characteristics of [3H]N-acetyl-aspartyl-glutamate (NAAG) binding sites in rat brain Neurochem. Int. 38 2001 53 62
63. T. Takahashi, I.D. Forsythe, T. Tsujimoto, M. Barnes-Davies, and K. Onodera Presynaptic calcium current modulation by a metabotropic glutamate receptor Science 274 1996 594 597
64. Y. Tanabe, M. Masu, T. Ishii, R. Shigemoto, and S. Nakanishi A family of metabotropic glutamate receptors Neuron 8 1992 169 179
65. Y. Tanabe, A. Nomura, M. Masu, R. Shigemoto, N. Mizuno, and S. Nakanishi Signal transduction, pharmacological properties, and expression patterns of two rat metabotropic glutamate receptors, mGluR3 and mGluR4 J. Neurosci. 13 1993 1372 1378
66. N.K. Thomas, D.E. Jane, H.W. Tse, and J.C. Watkins (S)-a-ethylglutamic acid and (RS)-a-cyclopropyl-4-phosphonophenylglycine as antagonists of L-AP4- and (1S,3S)-ACPD-induced depression of monosynaptic excitation of neonatal rat motoneurones Br. J. Pharmacol. 117 1996 70P
67. B.L. Trommer, Y.B. Liu, and J.F. Pasternak Long-term depression at the medial perforant path-granule cell synapse in developing rat dentate gyrus Brain Res. Dev. Brain Res. 96 1996 97 108
68. H.M. Valivullah, J. Lancaster, P.M. Sweetnam, and J.H. Neale Interactions between N-acetylaspartylglutamate and AMPA, kainate, and NMDA binding sites J. Neurochem. 63 1994 1714 1719
69. Y. Wang, M.J. Rowan, and R. Anwyl Induction of LTD in the dentate gyrus in vitro is NMDA receptor independent, but dependent on Ca2+ influx via low-voltage-activated Ca2+ channels and release of Ca2+ from intracellular stores J. Neurophysiol. 77 1997 812 825
70. A. Wenzel, J.M. Fritschy, H. Mohler, and D. Benke NMDA receptor heterogeneity during postnatal development of the rat brain: differential expression of the NR2A, NR2B, and NR2C subunit proteins J. Neurochem. 68 1997 469 478
71. G.L. Westbrook, M.L. Mayer, M.A. Namboodiri, and J.H. Neale High concentrations of N acetylaspartylglutamate (NAAG) selectively activate NMDA receptors on mouse spinal cord neurons in cell culture J. Neurosci. 6 1986 3385 3392
72. K. Williams Ifenprodil, a novel NMDA receptor antagonist: site and mechanism of action Curr. Drug Targets 2 2001 285 298
73. D.G. Winder, and P.J. Conn Metabotropic glutamate receptor (mGluR)-mediated potentiation of cyclic AMP responses does not require phosphoinositide hydrolysis: mediation by a group II-like mGluR J. Neurochem. 64 1995 592 599
74. S.N. Yang, Y.G. Tang, and R.S. Zucker Selective induction of LTP and LTD by postsynaptic [Ca2+]i elevation J. Neurophysiol. 81 1999 781 787