Hippocampal synaptic metaplasticity requires the activation of NR2B-containing NMDA receptors

Brain Research Bulletin

Volumn 84, Issue 2, 2011, Pages 137-143

  Yang, Qian ^a   Liao, Zhen Hua ^a   Xiao, Yi Xin ^a   Lin, Qing Shu ^a   Zhu, Yi Sheng ^a   Li, Sheng Tian ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Hippocampus; Long term potentiation; Metaplasticity; NMDA receptor; NR2B subunit

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B;

ANIMAL TISSUE; ARTICLE; BRAIN COMMISSURE; CONTROLLED STUDY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; NEURONAL PLASTICITY; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 79451469153     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2010.12.009     Document Type: Article

References (47)

1. Abraham W.C., Bear M.F. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 1996, 19:126-130.
2. Abraham W.C., Mason-Parker S.E., Bear M.F., Webb S., Tate W.P. Heterosynaptic metaplasticity in the hippocampus in vivo: a BCM-like modifiable threshold for LTP. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:10924-10929.
3. Barria A., Malinow R. NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 2005, 48:289-301.
4. Bartlett T.E., Bannister N.J., Collett V.J., Dargan S.L., Massey P.V., Bortolotto Z.A., Fitzjohn S.M., Bashir Z.I., 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.
5. Bayer K.U., LeBel E., McDonald G.L., O'Leary H., Schulman H., De Koninck P. Transition from reversible to persistent binding of CaMKII to postsynaptic sites and NR2B. J. Neurosci. 2006, 26:1164-1174.
6. Bear M.F. Mechanism for a sliding synaptic modification threshold. Neuron 1995, 15:1-4.
7. Berberich S., Punnakkal P., Jensen V., Pawlak V., Seeburg P.H., Hvalby O., Kohr G. Lack of NMDA receptor subtype selectivity for hippocampal long-term potentiation. J. Neurosci. 2005, 25:6907-6910.
8. Bienenstock E.L., Cooper L.N., Munro P.W. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J. Neurosci. 1982, 2:32-48.
9. Buller A.L., Larson H.C., Schneider B.E., Beaton J.A., Morrisett R.A., Monaghan D.T. The molecular basis of NMDA receptor subtypes: native receptor diversity is predicted by subunit composition. J. Neurosci. 1994, 14:5471-5484.
10. Chatterton J.E., Awobuluyi M., Premkumar L.S., Takahashi H., Talantova M., Shin Y., Cui J., Tu S., Sevarino K.A., Nakanishi N., Tong G., Lipton S.A., Zhang D. Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 2002, 415:793-798.
11. Chazot P.L., Stephenson F.A. Molecular dissection of native mammalian forebrain NMDA receptors containing the NR1 C2 exon: direct demonstration of NMDA receptors comprising NR1, NR2A, and NR2B subunits within the same complex. J. Neurochem. 1997, 69:2138-2144.
12. Christie B.R., Stellwagen D., Abraham W.C. Reduction of the threshold for long-term potentiation by prior theta-frequency synaptic activity. Hippocampus 1995, 5:52-59.
13. Cull-Candy S.G., Leszkiewicz D.N. Role of distinct NMDA receptor subtypes at central synapses. Sci. STKE 2004, 2004:re16.
14. Deisseroth K., Bito H., Schulman H., Tsien R.W. Synaptic plasticity: a molecular mechanism for metaplasticity. Curr. Biol. 1995, 5:1334-1338.
15. Didier M., Xu M., Berman S.A., Bursztajn S. Differential expression and co-assembly of NMDA zeta 1 and epsilon subunits in the mouse cerebellum during postnatal development. Neuroreport 1995, 6:2255-2259.
16. Fox C.J., Russell K.I., Wang Y.T., Christie B.R. Contribution of NR2A and NR2B NMDA subunits to bidirectional synaptic plasticity in the hippocampus in vivo. Hippocampus 2006, 16:907-915.
17. Giese K.P., Fedorov N.B., Filipkowski R.K., Silva A.J. Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science 1998, 279:870-873.
18. Hashimoto Y., Schworer C.M., Colbran R.J., Soderling T.R. Autophosphorylation of Ca2+/calmodulin-dependent protein kinase. II. Effects on total and Ca2+-independent activities and kinetic parameters. J. Biol. Chem. 1987, 262:8051-8055.
19. Holland L.L., Wagner J.J. Primed facilitation of homosynaptic long-term depression and depotentiation in rat hippocampus. J. Neurosci. 1998, 18:887-894.
20. Huang Y.Y., Colino A., Selig D.K., Malenka R.C. The influence of prior synaptic activity on the induction of long-term potentiation. Science 1992, 255:730-733.
21. Ishii T., Moriyoshi K., Sugihara H., Sakurada K., Kadotani H., Yokoi M., Akazawa C., Shigemoto R., Mizuno N., Masu M., et al. Molecular characterization of the family of the N-methyl-d-aspartate receptor subunits. J. Biol. Chem. 1993, 268:2836-2843.
22. Izumi Y., Auberson Y.P., Zorumski C.F. Zinc modulates bidirectional hippocampal plasticity by effects on NMDA receptors. J. Neurosci. 2006, 26:7181-7188.
23. Kohr G., Jensen V., Koester H.J., Mihaljevic A.L., Utvik J.K., Kvello A., Ottersen O.P., Seeburg P.H., Sprengel R., Hvalby O. Intracellular domains of NMDA receptor subtypes are determinants for long-term potentiation induction. J. Neurosci. 2003, 23:10791-10799.
24. Leonard A.S., Lim I.A., Hemsworth D.E., Horne M.C., Hell J.W. Calcium/calmodulin-dependent protein kinase II is associated with the N-methyl-d-aspartate receptor. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:3239-3244.
25. Li S.T., Kato K., Tomizawa K., Matsushita M., Moriwaki A., Matsui H., Mikoshiba K. Calcineurin plays different roles in group II metabotropic glutamate receptor- and NMDA receptor-dependent long-term depression. J. Neurosci. 2002, 22:5034-5041.
26. Lisman J., Schulman H., Cline H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat. Rev. Neurosci. 2002, 3:175-190.
27. 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.
28. de Armentia M.Lopez, Sah P. Development and subunit composition of synaptic NMDA receptors in the amygdala: NR2B synapses in the adult central amygdala. J. Neurosci. 2003, 23:6876-6883.
29. Luo J., Wang Y., Yasuda R.P., Dunah A.W., Wolfe B.B. The majority of N-methyl-d-aspartate receptor complexes in adult rat cerebral cortex contain at least three different subunits (NR1/NR2A/NR2B). Mol. Pharmacol. 1997, 51:79-86.
30. Malenka R.C., Nicoll R.A. NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci. 1993, 16:521-527.
31. Malinow R., Schulman H., Tsien R.W. Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 1989, 245:862-866.
32. Massey P.V., Johnson B.E., Moult P.R., Auberson Y.P., Brown M.W., Molnar E., Collingridge G.L., Bashir Z.I. Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J. Neurosci. 2004, 24:7821-7828.
33. Masu M., Nakajima Y., Moriyoshi K., Ishii T., Akazawa C., Nakanashi S. Molecular characterization of NMDA and metabotropic glutamate receptors. Ann. N.Y. Acad. Sci. 1993, 707:153-164.
34. Morris R.G., Anderson E., Lynch G.S., Baudry M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-d-aspartate receptor antagonist, AP5. Nature 1986, 319:774-776.
35. Muller D., Joly M., Lynch G. Contributions of quisqualate and NMDA receptors to the induction and expression of LTP. Science 1988, 242:1694-1697.
36. Neyton J., Paoletti P. Relating NMDA receptor function to receptor subunit composition: limitations of the pharmacological approach. J. Neurosci. 2006, 26:1331-1333.
37. 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.
38. Perez-Otano I., Schulteis C.T., Contractor A., Lipton S.A., Trimmer J.S., Sucher N.J., Heinemann S.F. Assembly with the NR1 subunit is required for surface expression of NR3A-containing NMDA receptors. J. Neurosci. 2001, 21:1228-1237.
39. Portera-Cailliau C., Price D.L., Martin L.J. N-Methyl-d-aspartate receptor proteins NR2A and NR2B are differentially distributed in the developing rat central nervous system as revealed by subunit-specific antibodies. J. Neurochem. 1996, 66:692-700.
40. 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.
41. Strack S., Colbran R.J. Autophosphorylation-dependent targeting of calcium/calmodulin-dependent protein kinase II by the NR2B subunit of the N-methyl-d-aspartate receptor. J. Biol. Chem. 1998, 273:20689-20692.
42. Strack S., McNeill R.B., Colbran R.J. Mechanism and regulation of calcium/calmodulin-dependent protein kinase II targeting to the NR2B subunit of the N-methyl-d-aspartate receptor. J. Biol. Chem. 2000, 275:23798-23806.
43. Tang Y.P., Shimizu E., Dube G.R., Rampon C., Kerchner G.A., Zhuo M., Liu G., Tsien J.Z. Genetic enhancement of learning and memory in mice. Nature 1999, 401:63-69.
44. Wang H., Wagner J.J. Priming-induced shift in synaptic plasticity in the rat hippocampus. J. Neurophysiol. 1999, 82:2024-2028.
45. Woo N.H., Nguyen P.V. Silent metaplasticity of the late phase of long-term potentiation requires protein phosphatases. Learn. Mem. 2002, 9:202-213.
46. Zhang L., Kirschstein T., Sommersberg B., Merkens M., Manahan-Vaughan D., Elgersma Y., Beck H. Hippocampal synaptic metaplasticity requires inhibitory autophosphorylation of Ca2+/calmodulin-dependent kinase II. J. Neurosci. 2005, 25:7697-7707.
47. Zhao M.G., Toyoda H., Lee Y.S., Wu L.J., Ko S.W., Zhang X.H., Jia Y., Shum F., Xu H., Li B.M., Kaang B.K., Zhuo M. Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 2005, 47:859-872.