An N-methyl-d-aspartate-receptor dependent, late-phase long-term depression in middle-aged mice identifies no GluN2-subunit bias

Neuroscience

Volumn 185, Issue , 2011, Pages 27-38

  Ahmed, T ^a   Sabanov, V ^a   D'Hooge, R ^a   Balschun, D ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Hippocampal cA1 region; In vitro; Long term depression; Synaptic plasticity

Indexed keywords

BRAIN PROTEIN; CALCIUM CHANNEL L TYPE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN GLUN2 SUBUNIT; UNCLASSIFIED DRUG;

AGING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE CONDUCTANCE; CONTROLLED STUDY; FEMALE; HIPPOCAMPAL CA1 REGION; LONG TERM DEPRESSION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR BLOCKING; WHOLE CELL;

AGING; ANIMALS; CALCIUM CHANNEL BLOCKERS; DIAZONIUM COMPOUNDS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; HIPPOCAMPUS; LONG-TERM SYNAPTIC DEPRESSION; MICE; MICE, INBRED C57BL; N-METHYLASPARTATE; NEURONS; NIFEDIPINE; PATCH-CLAMP TECHNIQUES; PYRIDINES; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 79956268764     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.04.006     Document Type: Article

References (91)

1. Abe M., Fukaya M., Yagi T., Mishina M., Watanabe M., Sakimura K. NMDA receptor GluRepsilon/NR2 subunits are essential for postsynaptic localization and protein stability of GluRzeta1/NR1 subunit. J Neurosci 2004, 24:7292-7304.
2. Ahmed T., Frey J.U. Plasticity-specific phosphorylation of CaMKII, MAP-kinases and CREB during late-LTP in rat hippocampal slices in vitro. Neuropharmacology 2005, 49:477-492.
3. Al-Hallaq R.A., Conrads T.P., Veenstra T.D., Wenthold R.J. NMDA di-heteromeric receptor populations and associated proteins in rat hippocampus. J Neurosci 2007, 27:8334-8343.
4. Bai L., Hof P.R., Standaert D.G., Xing Y., Nelson S.E., Young A.B., Magnusson K.R. Changes in the expression of the NR2B subunit during aging in macaque monkeys. Neurobiol Aging 2004, 25:201-208.
5. Balschun D., Wolfer D.P., Gass P., Mantamadiotis T., Welzl H., Schutz G., Frey J.U., Lipp H.P. Does cAMP response element-binding protein have a pivotal role in hippocampal synaptic plasticity and hippocampus-dependent memory?. J Neurosci 2003, 23:6304-6314.
6. Bartlett T.E., Bannister N.J., Collett V.J., Dargan S.L., Massey P.V., Bartolotto Z.A., Fitzjohn S.M., Bashir Z.A., Collingridge G.L., Lodge D. Differential roles of NR2A and NR2B-containing NMDA receptors in LTP and LTD in the CA1 region of two-week old rat hippocampus. Neuropharmacology 2007, 52:60-70.
7. Bashir Z.I., Collingridge G.L. An investigation of depotentiation of long-term potentiation in the CA1 region of the hippocampus. Exp Brain Res 1994, 100:437-443.
8. Bear M.F., Abraham W.C. Long-term depression in hippocampus. Annu Rev Neurosci 1996, 19:437-462.
9. Billard J.M., Rouaud E. Deficit of NMDA receptor activation in CA1 hippocampal area of aged rats is rescued by d-cycloserine. Eur J Neurosci 2007, 8:2260-2268.
10. Bortolotto Z.A., Bashir Z.I., Davies C.H., Collingridge G.L. A molecular switch activated by metabotropic glutamate receptors regulates induction of long-term potentiation. Nature 1994, 368:740-743.
11. Carroll R.C., Zukin R.S. NMDA-receptor trafficking and targeting: implications for synaptic transmission and plasticity. Trends Neurosci 2002, 25:571-577.
12. Clayton D.A., Browning M.D. Deficits in the expression of the NR2B subunit in the hippocampus of aged Fisher 344 rats. Neurobiol Aging 2001, 22:165-168.
13. Collingridge G.L., Olsen R.W., Peters J., Spedding M. A nomenclature for ligand-gated ion channels. Neuropharmacology 2009, 56:2-5.
14. Cooke S.F., Bliss T.V. Plasticity in the human central nervous system. Brain 2006, 129:1659-1667.
15. Costa B.M., Feng B., Tsintsadze T.S., Morley R.M., Irvine M.W., Tsintsadze V., Lozovaya N.A., Jane D.E., Monaghan D.T. N-methyl-d-aspartate (NMDA) receptor NR2 subunit selectivity of a series of novel piperazine-2,3-dicarboxylate derivatives: preferential blockade of extrasynaptic NMDA receptors in the rat hippocampal CA3-CA1 synapse. J Pharmacol Exp Ther 2009, 331:618-626.
16. Cull-Candy S.G., Brickley S., Farrant M. NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 2001, 11:327-335.
17. Cull-Candy S.G., Leszkiewicz D.N. Role of distinct NMDA receptor subtypes at central synapses. Sci STKE 2004, 2004:re16.
18. Dingledine R., Borges K., Bowie D., Traynelis S.F. The glutamate receptor ion channels. Pharmacol Rev 1999, 51:7-61.
19. Dudek S., Bear M.F. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-d-aspartate receptor blockade. Proc Natl Acad Sci USA 1992, 89:4363-4367.
20. Dudek S.M., Bear M.F. Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J Neurosci 1993, 13:2910-2918.
21. Dunah A.W., Yasuda R.P., Wang Y.H., Luo J., Dávila-García M., Gbadegesin M., Vicini S., Wolfe B.B. Regional and ontogenic expression of the NMDA receptor subunit NR2D protein in rat brain using a subunit-specific antibody. J Neurochem 1996, 67:2335-2345.
22. Feng B., Morley R.M.M., Jane D.E., Monaghan D.T. The effect of competitive antagonist chain length on NMDA receptor subunit selectivity. Neuropharmacology 2005, 48:354-359.
23. Fischer G., Mutel V., Trube G., Malherbe P., Kew J.N.C., Mohacsi E., Heitz M.P., Kemp J.A. Ro 25-6981, a highly potent and selective blocker of N-methyl-d-aspartate receptors containing the NR2B subunit. Characterization in vitro. J Pharmacol Exp Ther 1997, 283:1285-1292.
24. Foster T.C. Involvement of hippocampal synaptic plasticity in age-related memory decline. Brain Res Rev 1999, 30:236-249.
25. Foster T.C. Calcium homeostasis and modulation of synaptic plasticity in the aged brain. Aging Cell 2007, 6:319-325.
26. Fox C.J., Russell K.I., Wang Y.T., Christie B.R. Contribution of NR2A and NR2B subunits to bidirectional synaptic plasticity in the hippocampus in vivo. Hippocampus 2006, 16:907-915.
27. Fujii S., Saito K., Miyakawa H., Ito K., Kato H. Reversal of long-term potentiation (depotentiation) induced by tetanus stimulation of the input to CA1 neurons of guinea pig hippocampal slices. Brain Res 1991, 555:112-122.
28. Grilli M., Zappettini S., Zanardi A., Lagomarsino F., Pittaluga A., Zoli M., Marchi M. Exposure to an enriched environment selectively increases the functional response of the pre-synaptic NMDA receptors which modulate noradrenaline release in mouse hippocampus. J Neurochem 2009, 110:1598-1606.
29. Harris A.Z., Pettit D.L. Recruiting extrasynaptic NMDA receptors augments synaptic signaling. J Neurophysiol 2008, 99:524-533.
30. Hatton C.H., Paoletti P. Modulation of triheteromeric NMDA receptors by N-terminal domain ligands. Neuron 2005, 46:261-274.
31. Hrabetova S., Serrano P., Blace N., Tse H.W., Skifter D.A., Jane D.E., Monaghan D.T., Sacktor T.C. Distinct NMDA receptor subpopulations contribute to long term potentiation and long term depression. J Neurosci 2000, 20:RC81.
32. Huber K.M., Roder J.C., Bear M.F. Chemical induction of mGluR5- and protein synthesis-dependent long-term depression in hippocampal area CA1. J Neurophysiol 2001, 86:321-325.
33. Huettner J.E., Bean P.E. Block of N-methyl-d-aspartate-activated current by the anticonvulsant MK-801: selective binding to open channels. Proc Natl Acad Sci U S A 1988, 85:1307-1311.
34. Izumi Y., Zorumski C.F. Nitric oxide and long-term synaptic depression in the rat hippocampus. Neuroreport 1993, 4:1131-1134.
35. Izumi Y., Auberson Y.P., Zorumski C.F. Zinc modulates bidirectional hippocampal plasticity by effects on NMDA receptors. J Neurosci 2006, 26:7181-7188.
36. Kamal A., Biessels G.J., Gispen W.H., Urban I.J. Increasing age reduces expression of long-term depression and dynamic range of transmission plasticity in CA1 field of the rat hippocampus. Neuroscience 1998, 83:707-715.
37. Karavanova I., Vasudevan K., Cheng J., Buonanno A. Novel regional and developmental NMDA receptor expression patterns uncovered in NR2C subunit-beta-galactosidase knock-in mice. Mol Cell Neurosci 2007, 34:468-480.
38. Kemp N., McQueen J., Faulkes S., Bashir Z.I. Different forms of LTD in CA1 region of the hippocampus: a role of age and stimulus protocol. Eur J Neurosci 2000, 12:360-366.
39. Kemp N., Bashir Z.I. Long-term depression: a cascade of induction and expression mechanisms. Prog Neurobiol 2001, 65:339-365.
40. Kerr D.S., Abraham W.C. Cooperative interactions among afferents govern the induction of homosynaptic long-term depression in the hippocampus. Proc Natl Acad Sci U S A 1995, 92:11637-11641.
41. Kim M.J., Dunah A.W., Wang Y.T., Sheng M. Differential roles of NR2A- and NR2B-containing NMDA receptors in Ras-ERK signaling and AMPA receptor trafficking. Neuron 2005, 46:745-760.
42. Kogan J.H., Frankland P.W., Blendy J.A., Coblentz J., Marowitz Z., Schutz G., Silva A.J. Spaced training induces normal long-term memory in CREB mutant mice. Curr Biol 1996, 7:1-11.
43. Köhr G. NMDA receptor function: subunit composition versus spatial distribution. Cell Tissue Res 2006, 326:439-446.
44. Kollen M., Dutar P., Jouvenceau A. The magnitude of hippocampal long term depression depends on the synaptic location of activated NR2-containing N-methyl-d-aspartate receptors. Neuroscience 2008, 154:1308-1317.
45. Krapivinsky G., Krapivinsky L., Manasian Y., Ivanov A., Tyzio R., Pellegrino C., Ben-Ari Y., Clapham D.E. The NMDA receptor is coupled to the ERK pathway by a direct interaction between NR2B and RasGRF1. Neuron 2003, 40:775-784.
46. Larson J., Lynch G. Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events. Science 1986, 232:985-988.
47. Larson J., Wong D., Lynch G. Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 1986, 368:347-350.
48. Lehmann J., Schneider J., McPherson S., Murphy D.E., Bernard P., Tsai C., Bennett D.A., Pastor G., Steel D.J., Boehm C., Cheney D.L., Liebman J.M., Williams M., Wood L. CPP, a selective NMDA type receptor antagonist: characterization in vitro and in vivo. J Pharmacol Exp Ther 1987, 240:737-746.
49. Li R., Dozmorov M., Hellberg F., Tian Y., Jilederos B., Wigstrom H. Characterization of NMDA induced depression in rat hippocampus: involvement of AMPA and NMDA receptors. Neurosci Lett 2004, 357:87-90.
50. Liu L., Wong T.P., Pozza M.F., Lingenhoehl K., Wang Y., Sheng M., Auberson Y.P., Wang Y.T. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 2004, 304:1021-1024.
51. Lodge D., Davies S.N., Jones M.G., Millar J., Manallack D.T., Ornstein P.L., Verberne A.J.M., Young N., Beart P.M. A comparison between the in vivo and in vitro activity of five potent and competitive NMDA antagonists. Br J Pharmacol 1988, 95:957-965.
52. Lozovaya N.A., Grebenyuk S.E., Tsintsadze T.S., Feng B., Monaghan D.T., Krishtal O.A. Extrasynaptic NR2B and NR2D subunits of NMDA receptors shape "superslow" afterburst EPSC in rat hippocampus. J Physiol 2004, 558:451-463.
53. Magnusson K.R. The aging of the NMDA receptor complex. Front Biosci 1998, 3:e70-e80.
54. Martin S.J., Grimwood P.D., Morris R.G.M. Synaptic plasticity and memory. Annu Rev Neurosci 2000, 23:649-711.
55. Massey P.V., Johnson B.E., Moult P.R., Auberson Y.P., Brown M.W., Molnar E., Collingridge G.L., Bashir Z.A. Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J Neurosci 2004, 24:7821-7828.
56. Massey P.V., Bashir Z.I. Long-term depression: multiple forms and implications for brain function. Trends Neurosci 2007, 30:176-184.
57. Milner A.J., Cummings D.M., Spencer J.P., Murphy K.P.S.J. Bi-directional plasticity and age-dependent long-term depression at mouse CA3-CA1 hippocampal synapses. Neurosci Lett 2004, 367:1-5.
58. Mockett B., Coussens C., Abraham W.C. NMDA receptor-mediated metaplasticity during the induction of long-term depression by low-frequency stimulation. Eur J Neurosci 2002, 15:1819-1826.
59. Montgomery J.M., Selcher J., Hanson J.E., Madison D.V. Dynamin-dependent NMDAR endocytosis during LTD and its dependence on synaptic state. BMC Neurosci 2005, 6:48.
60. Monyer H., Burnashev N., Laurie D.J., Sakmann B., Seeburg P.H. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 1994, 12:529-540.
61. Morishita W., Lue W., Smith G.B., Nicoll R.A., Bear M.F., Malenka R.C. Activation of NR2B-containing NMDA receptors is not required for NMDA receptor-dependent long term depression. Neuropharmacology 2007, 52:71-76.
62. Morley R.M., Tse H.W., Feng B., Miller J.C., Monaghan D.T., Jane D.E. Synthesis and pharmacology of N1-substituted piperazine-2,3-dicarboxylic acid derivatives acting as NMDA receptor antagonists. J Med Chem 2005, 48:2627-2637.
63. Mulkey R.M., Malenka R.C. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 1992, 5:967-975.
64. Nicoll R.A., Oliet S.H., Malenka R.C. NMDA receptor-dependent and metabotropic glutamate receptor-dependent forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neurobiol Learn Mem 1998, 70:62-72.
65. Neyton J., Paoletti P. Relating NMDA receptor function to receptor subunit composition: limitations of the pharmacological approach. J Neurosci 2006, 26:1331-1333.
66. Norris C.M., Korol D.L., Foster T.C. Increased susceptibility to induction of long-term depression and long-term potentiation reversal during aging. J Neurosci 1996, 16:5382-5392.
67. Norris C.M., Halpain S., Foster T.C. Reversal of age-related alterations in synaptic plasticity by blockade of L-type Ca2+ channels. J Neurosci 1998, 18:3171-3179.
68. Norris C.M., Halpain S., Foster T.C. Alterations in the balance of protein kinase/phosphatases activities parallel reduced synaptic strength during aging. J Neurophysiol 1998, 80:1567-1570.
69. O'Dell T.J., Kandel E.R. Low-frequency stimulation erases LTP through an NMDA receptor-mediated activation of protein phosphatases. Learn Mem 1994, 1:129-139.
70. Otani S., Connor J.A. Long-term depression of naive synapses in adult hippocampus induced by asynchronous synaptic activity. J Neurophysiol 1995, 73:2596-2601.
71. Paoletti P., Ascher P., Neyton J. High affinity zinc inhibition of NMDAR NR1-NR2A receptor. J Neurosci 1997, 17:5711-5725.
72. Paoletti P., Perin-Durea F., Fayyazuddin A., Le Goff A., Callebaut I., Neyton J. Molecular organisation of zinc binding N-terminal modulatory domain in a NMDA receptor subunit. Neuron 2000, 28:911-925.
73. Paoletti P., Neyton J. NMDA receptor subunits: function and pharmacology. Curr Opin Pharmacol 2007, 7:39-47.
74. Popkirov S.G., Manahan-Vaughan D. Involvement of the metabotropic glutamate receptor mGluR5 in NMDA receptor-dependent, learning-facilitated long-term depression in CA1 synapses. Cereb Cortex 2011, 21:501-509.
75. Rachline J., Perin-Dureau F., Le Goff A., Neyton J., Paoletti P. The micromolar zinc-binding domain on the NMDA receptor subunit NR2B. J Neurosci 2005, 25:308-317.
76. Ryan T.J., Emes R.D., Grant S.G.N., Komiyama N.H. Evolution of NMDA receptor cytoplasmic interaction domains: implications for organisation of synaptic signalling complexes. BMC Neurosci 2008, 9:6.
77. Shankar S., Teyler T.J., Robbins N. Aging differentially alters forms of long-term potentiation in rat hippocampal area CA1. J Neurophysiol 1998, 79:334-341.
78. Sheng M., Cummings J., Roldan L.A., Jan Y.N., Jan L.Y. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 1994, 368:144-147.
79. Staubli U.V., Ji Z.X. The induction of homo- vsheterosynaptic LTD in area CA1 of hippocampal slices from adult rats. Brain Res 1996, 714:169-176.
80. Takai H., Katayama K., Uetsuka K., Nakayama H., Doi K. Distribution of N-methyl-d-aspartate receptors (NMDARs) in the developing rat brain. Exp Mol Pathol 2003, 75:89-94.
81. Traynelis S.F., Burgess M.F., Zheng F., Lyuboslavsky P., Powers J.L. Control of voltage-independent zinc inhibition of NMDA receptors by the NR1 subunit. J Neurosci 1998, 18:6163-6275.
82. von Engelhardt J., Doganci B., Jensen V., Hvalby Ø., Göngrich C., Taylor A., Barkus C., Sanderson D.J., Rawlins J.N., Seeburg P.H., Bannerman D.M., Monyer H. Contribution of hippocampal and extra-hippocampal NR2B-containing NMDA receptors to performance on spatial learning tasks. Neuron 2008, 60:846-860.
83. Wagner J.J., Alger B.E. GABAergic and developmental influences on homosynaptic LTD and depotentiation in rat hippocampus. J Neurosci 1995, 15:1577-1586.
84. Wang D., Cui Z., Zeng Q., Kuang H., Wang L.P., Tsien J.Z., Cao X. Genetic enhancement of memory and long-term potentiation but not CA1 long-term depression in NR2B transgenic rats. PLoS One 2009, 4:e7486.
85. Weitlauf C., Honse Y., Auberson Y.P., Mishina M., Lovinger D.M., Winder D.G. Activation of NR2A-containing NMDA receptors is not obligatory for NMDA receptor-dependent long-term potentiation. J Neurosci 2005, 25:8386-8390.
86. Wenzel A., Villa M., Mohler H., Benke D. Developmental and regional expression of NMDA receptor subtypes containing the NR2D subunit in rat brain. J Neurochem 1996, 66:1240-1248.
87. Wenzel A., Fritschy J.M., Mohler H., Benke D. NMDA receptor heterogeneity during postnatal development of the rat brain: differential expression of the NR2A, NR2B, and NR2C subunit proteins. J Neurochem 1997, 68:469-478.
88. Williams K. Ifenprodil discriminates subtypes of the NMDA receptor: selectivity and mechanisms at recombinant hetromeric receptors. Mol Pharmacol 1993, 44:851-859.
89. Xiao M.Y., Karpefors M., Gustafsson B., Wigstrom H. On the linkage between AMPA and NMDA receptor-mediated EPSPs in homosynaptic long-term depression in the hippocampal CA1 region of young rats. J Neurosci 1995, 15:4496-4506.
90. Yamakura T., Shimoji K. Subunit- and site-specific pharmacology of the NMDA receptor channel. Prog Neurobiol 1999, 59:279-298.
91. Zukin R.S., Bennett M.L.V. Alternatively spliced isoforms of the NMDARI receptor subunit. Trends Neurosci 1995, 18:306-313.