Synaptic NR2A- but not NR2B-containing NMDA receptors increase with blockade of ionotropic glutamate receptors

Frontiers in Molecular Neuroscience

Volumn 2, Issue OCT, 2013, Pages

  von Engelhardt, Jakob ^a   Doganci, Beril ^a   Seeburg, Peter H ^b   Monyer, Hannah ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

Author keywords

APV; Ifenprodil; MK 801; Mouse; NVP AAM077

Indexed keywords

AMPA RECEPTOR; ENHANCED GREEN FLUORESCENT PROTEIN; IFENPRODIL; IONOTROPIC RECEPTOR; LEPIRUDIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; SYNAPSE RECEPTOR; THROMBIN;

ANIMAL CELL; ARTICLE; BRAIN FUNCTION; CELL ACTIVITY; CONTROLLED STUDY; ELECTROPHYSIOLOGICAL PROCEDURES; EXCITOTOXICITY; HIPPOCAMPAL NEURONAL CULTURE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MOUSE; NERVE CELL MEMBRANE CONDUCTANCE; NERVE CELL PLASTICITY; NERVE CONDUCTION; NEUROENDOCRINE SYSTEM; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; QUANTITATIVE ASSAY; RECEPTOR INTRINSIC ACTIVITY; SYNAPTIC POTENTIAL;

EID: 79959832609     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/neuro.02.019.2009     Document Type: Article

References (66)

1. Aniksztejn, L., and Ben-Ari, Y. (1995). Expression of LTP by AMPA and/or NMDA receptors is determined by the extent of NMDA receptors activation during the tetanus. J. Neurophysiol. 74, 2349-2357.
2. Aoki, C., Fujisawa, S., Mahadomrongkul, V., Shah, P. J., Nader, K., and Erisir, A. (2003). NMDA receptor blockade in intact adult cortex increases trafficking of NR2A subunits into spines, postsynaptic densities, and axon terminals. Brain Res. 963, 139-149.
3. Barria, A., and Malinow, R. (2002). Subunitspecific NMDA receptor trafficking to synapses. Neuron 35, 345-353.
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., and Lodge, D. (2007). Differential roles of NR2A and NR2B-containing NMDA receptors in LTP and LTD in the CA1 region of two-week old rat hippocampus. Neuropharmacology. 52, 60-70.
5. Bashir, Z. I., Alford, S., Davies, S. N., Randall, A. D., and Collingridge, G. L. (1991). Long-term potentiation of NMDA receptor-mediated synaptic transmission in the hippocampus. Nature 349, 156-158.
6. Berberich, S., Punnakkal, P., Jensen, V., Pawlak, V., Seeburg, P. H., Hvalby, O., and Kohr, G. (2005). Lack of NMDA receptor subtype selectivity for hippocampal long-term potentiation. J. Neurosci. 25, 6907-6910.
7. Berretta, N., Berton, F., Bianchi, R., Brunelli, M., Capogna, M., and Francesconi, W. (1991). Long-term potentiation of NMDA receptormediated EPSP in guinea-pig hippocampal slices. Eur. J. Neurosci. 3, 850-854.
8. Brewer, G. J., Torricelli, J. R., Evege, E. K., and Price, P. J. (1993). Optimized survival of hippocampal neurons in B27-supplemented neurobasal, a new serum-free medium combination. J. Neurosci. Res. 35, 567-576.
9. Cais, O., Sedlacek, M., Horak, M., Dittert, I., and Vyklicky, L., Jr. (2008). Temperature dependence of NR1/ NR2B NMDA receptor channels. Neuroscience 151, 428-438.
10. Carmignoto, G., and Vicini, S. (1992). Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 258, 1007-1011.
11. Chen, W. S., and Bear, M. F. (2007). Activity-dependent regulation of NR2B translation contributes to metaplasticity in mouse visual cortex. Neuropharmacology 52, 200-214.
12. Clark, K. A., and Collingridge, G. L. (1995). Synaptic potentiation of dual-component excitatory postsynaptic currents in the rat hippocampus. J. Physiol. 482 (Pt 1), 39-52.
13. Clarke, R. J., and Johnson, J. W. (2008). Voltage-dependent gating of NR1/2B NMDA receptors. J. Physiol. 586, 5727-5741.
14. Crump, F. T., Dillman, K. S., and Craig, A. M. (2001). cAMP-dependent protein kinase mediates activityregulated synaptic targeting of NMDA receptors. J. Neurosci. 21, 5079-5088.
15. Cull-Candy, S. G., and Leszkiewicz, D. N. (2004). Role of distinct NMDA receptor subtypes at central synapses. Sci. STKE 2004, re16.
16. Daunt, D. A., Hurt, C., Hein, L., Kallio, J., Feng, F., and Kobilka, B. K. (1997). Subtype-specific intracellular trafficking of alpha2-adrenergic receptors. Mol. Pharmacol. 51, 711-720.
17. Diamond, J. S. (2001). Neuronal glutamate transporters limit activation of NMDA receptors by neurotransmitter spillover on CA1 pyramidal cells. J. Neurosci. 21, 8328-8338.
18. Dunah, A. W., and Standaert, D. G. (2001). Dopamine D1 receptordependent trafficking of striatal NMDA glutamate receptors to the postsynaptic membrane. J. Neurosci. 21, 5546-5558.
19. Fujisawa, S., and Aoki, C. (2003). In vivo blockade of N-methyl-d-aspartate receptors induces rapid trafficking of NR2B subunits away from synapses and out of spines and terminals in adult cortex. Neuroscience 121, 51-63.
20. Fukaya, M., Kato, A., Lovett, C., Tonegawa, S., and Watanabe, M. (2003). Retention of NMDA receptor NR2 subunits in the lumen of endoplasmic reticulum in targeted NR1 knockout mice. Proc. Natl. Acad. Sci. U.S.A. 100, 4855-4860.
21. Groc, L., Choquet, D., Stephenson, F. A., Verrier, D., Manzoni, O. J., and Chavis, P. (2007). NMDA receptor surface trafficking and synaptic subunit composition are developmentally regulated by the extracellular matrix protein Reelin. J. Neurosci. 27, 10165-10175.
22. Groc, L., Heine, M., Cousins, S. L., Stephenson, F. A., Lounis, B., Cognet, L., and Choquet, D. (2006). NMDA receptor surface mobility depends on NR2A-2B subunits. Proc. Natl. Acad. Sci. U.S.A. 103, 18769-18774.
23. Hatton, C. J., and Paoletti, P. (2005). Modulation of triheteromeric NMDA receptors by N-terminal domain ligands. Neuron 46, 261-274.
24. Hein, L., Ishii, K., Coughlin, S. R., and Kobilka, B. K. (1994). Intracellular targeting and trafficking of thrombin receptors. A novel mechanism for resensitization of a G proteincoupled receptor. J. Biol. Chem. 269, 27719-27726.
25. Hestrin, S., Sah, P., and Nicoll, R. A. (1990). Mechanisms generating the time course of dual component excitatory synaptic currents recorded in hippocampal slices. Neuron 5, 247-253.
26. Hollmann, M. (1999). Ionotropic Glutamate Receptors in the CNS. Berlin, Springer.
27. Huh, K. H., and Wenthold, R. J. (1999). Turnover analysis of glutamate receptors identifies a rapidly degraded pool of the N-methyl-D-aspartate receptor subunit, NR1, in cultured cerebellar granule cells. J. Biol. Chem. 274, 151-157.
28. Jonas, P., and Sakmann, B. (1992). Glutamate receptor channels in isolated patches from CA1 and CA3 pyramidal cells of rat hippocampal slices. J. Physiol. 455, 143-171.
29. Konnerth, A., Keller, B. U., Ballanyi, K., and Yaari, Y. (1990). Voltage sensitivity of NMDA-receptor mediated postsynaptic currents. Exp. Brain Res. 81, 209-212.
30. Kutsuwada, T., Kashiwabuchi, N., Mori, H., Sakimura, K., Kushiya, E., Araki, K., Meguro, H., Masaki, H., Kumanishi, T., Arakawa, M., and Mishina, M. (1992). Molecular diversity of the NMDA receptor channel. Nature 358, 36-41.
31. Lan, J. Y., Skeberdis, V. A., Jover, T., Zheng, X., Bennett, M. V., Zukin, R. S. (2001a). Activation of metabotropic glutamate receptor 1 accelerates NMDA receptor trafficking. J. Neurosci. 21, 6058-6068.
32. Lan, J. Y., Skeberdis, V. A., Jover, T., Grooms, S. Y., Lin, Y., Araneda, R. C., Zheng, X., Bennett, M. V., and Zukin, R. S. (2001b). Protein kinase C modulates NMDA receptor trafficking and gating. Nat. Neurosci. 4, 382-390.
33. Lavezzari, G., McCallum, J., Dewey, C. M., and Roche, K. W. (2004). Subunit-specific regulation of NMDA receptor endocytosis. J. Neurosci. 24, 6383-6391.
34. Li, J. H., Wang, Y. H., Wolfe, B. B., Krueger, K. E., Corsi, L., Stocca, G., and Vicini, S. (1998). Developmental changes in localization of NMDA receptor subunits in primary cultures of cortical neurons. Eur. J. Neurosci. 10, 1704-1715.
35. Liao, D., Zhang, X., O'Brien, R., Ehlers, M. D., and Huganir, R. L. (1999). Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons. Nat. Neurosci. 2, 37-43.
36. Liu, L., Wong, T. P., Pozza, M. F., Lingenhoehl, K., Wang, Y., Sheng, M., Auberson, Y. P., and Wang, Y. T. (2004). Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304, 1021-1024.
37. Lozovaya, N. A., Grebenyuk, S. E., Tsintsadze, T., Feng, B., Monaghan, D. T., and Krishtal, O. A. (2004). Extrasynaptic NR2B and NR2D subunits of NMDA receptors shape 'superslow' afterburst EPSC in rat hippocampus. J. Physiol. 558, 451-463.
38. Lu, W. Y., Xiong, Z. G., Lei, S., Orser, B. A., Dudek, E., Browning, M. D., and MacDonald, J. F. (1999). G-proteincoupled receptors act via protein kinase C and Src to regulate NMDA receptors. Nat. Neurosci. 2, 331-338.
39. Luo, J. H., Fu, Z. Y., Losi, G., Kim, B. G., Prybylowski, K., Vissel, B., and Vicini, S. (2002). Functional expression of distinct NMDA channel subunits tagged with green fluorescent protein in hippocampal neurons in culture. Neuropharmacology 42, 306-318.
40. Massey, P. V., Johnson, B. E., Moult, P. R., Auberson, Y. P., Brown, M. W., Molnar, E., Collingridge, G. L., and Bashir, Z. I. (2004). Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J. Neurosci. 24, 7821-7828.
41. Monyer, H., Burnashev, N., Laurie, D. J., Sakmann, B., and Seeburg, P. H. (1994). Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12, 529-540.
42. Morishita, W., Lu, W., Smith, G. B., Nicoll, R. A., Bear, M. F., and Malenka, R. C. (2007). Activation of NR2B-containing NMDA receptors is not required for NMDA receptordependent long-term depression. Neuropharmacology. 52, 71-76.
43. Nong, Y., Huang, Y. Q., Ju, W., Kalia, L. V., Ahmadian, G., Wang, Y. T., and Salter, M. W. (2003). Glycine binding primes NMDA receptor internalization. Nature 422, 302-307.
44. Nowak, G. (2002). Pharmacology of recombinant hirudin. Semin. Thromb. Hemost. 28, 415-424.
45. Paoletti, P., and Neyton, J. (2007). NMDA receptor subunits: function and pharmacology. Curr. Opin. Pharmacol. 7, 39-47.
46. Passafaro, M., Piech, V., and Sheng, M. (2001). Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat. Neurosci. 4, 917-926.
47. Patneau, D. K., and Mayer, M. L. (1990). Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-d-aspartate and quisqualate receptors. J. Neurosci. 10, 2385-2399.
48. Prybylowski, K., Fu, Z., Losi, G., Hawkins, L. M., Luo, J., Chang, K., Wenthold, R. J., and Vicini, S. (2002). Relationship between availability of NMDA receptor subunits and their expression at the synapse. J. Neurosci. 22, 8902-8910.
49. Quinlan, E. M., Philpot, B. D., Huganir, R. L., and Bear, M. F. (1999). Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat. Neurosci. 2, 352-357.
50. Rao, A., and Craig, A. M. (1997). Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons. Neuron 19, 801-812.
51. Roche, K. W., Standley, S., McCallum, J., Dune Ly, C., Ehlers, M. D., and Wenthold, R. J. (2001). Molecular determinants of NMDA receptor internalization. Nat. Neurosci. 4, 794-802.
52. Rumbaugh, G., Prybylowski, K., Wang, J. F., and Vicini, S. (2000). Exon 5 and spermine regulate deactivation of NMDA receptor subtypes. J. Neurophysiol. 83, 1300-1306.
53. Scott, D. B., Michailidis, I., Mu, Y., Logothetis, D., and Ehlers, M. D. (2004). Endocytosis and degradative sorting of NMDA receptors by conserved membrane-proximal signals. J. Neurosci. 24, 7096-7109.
54. Sheng, M., Cummings, J., Roldan, L. A., Jan, Y. N., and Jan, L. Y. (1994). Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368, 144-147.
55. Skeberdis, V. A., Chevaleyre, V., Lau, C. G., Goldberg, J. H., Pettit, D. L., Suadicani, S. O., Lin, Y., Bennett, M. V., Yuste, R., Castillo, P. E., and Zukin, R. S. (2006). Protein kinase A regulates calcium permeability of NMDA receptors. Nat. Neurosci. 9, 501-510.
56. Skeberdis, V. A., Lan, J., Zheng, X., Zukin, R. S., and Bennett, M. V. (2001). Insulin promotes rapid delivery of N-methyl-d-aspartate receptors to the cell surface by exocytosis. Proc. Natl. Acad. Sci. U.S.A. 98, 3561-3566.
57. Stephenson, F. A. (2001). Subunit characterization of NMDA receptors. Curr. Drug Targets 2, 233-239.
58. Tang, Y. P., Shimizu, E., Dube, G. R., Rampon, C., Kerchner, G. A., Zhuo, M., Liu, G., and Tsien, J. Z. (1999). Genetic enhancement of learning and memory in mice. Nature 401, 63-69.
59. Tovar, K. R., and Westbrook, G. L. (2002). Mobile NMDA receptors at hippocampal synapses. Neuron 34, 255-264.
60. Vissel, B., Krupp, J. J., Heinemann, S. F., and Westbrook, G. L. (2001). A use-dependent tyrosine dephosphorylation of NMDA receptors is independent of ion flux. Nat. Neurosci. 4, 587-596.
61. Washbourne, P., Liu, X. B., Jones, E. G., and McAllister, A. K. (2004). Cycling of NMDA receptors during trafficking in neurons before synapse formation. J. Neurosci. 24, 8253-8264.
62. Watt, A. J., Sjostrom, P. J., Hausser, M., Nelson, S. B., and Turrigiano, G. G. (2004). A proportional but slower NMDA potentiation follows AMPA potentiation in LTP. Nat. Neurosci. 7, 518-524.
63. Weitlauf, C., Honse, Y., Auberson, Y. P., Mishina, M., Lovinger, D. M., and Winder, D. G. (2005). Activation of NR2A-containing NMDA receptors is not obligatory for NMDA receptordependent long-term potentiation. J. Neurosci. 25, 8386-8390.
64. Wenthold, R. J., Prybylowski, K., Standley, S., Sans, N., and Petralia, R. S. (2003). Trafficking of NMDA receptors. Annu. Rev. Pharmacol. Toxicol. 43, 335-358.
65. Williams, K. (1993). Ifenprodil discriminates subtypes of the N-methyl-d-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol. Pharmacol. 44, 851-859.
66. Zhao, J., Peng, Y., Xu, Z., Chen, R. Q., Gu, Q. H., Chen, Z., and Lu, W. (2008). Synaptic metaplasticity through NMDA receptor lateral diffusion. J. Neurosci. 28, 3060-3070.