Regulation of NMDA receptors by phosphorylation

Neuropharmacology

Volumn 53, Issue 3, 2007, Pages 362-368

  Chen, Bo Shiun ^a   Roche, Katherine W ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Glutamate; Kinase; NMDA receptors; Phosphorylation

Indexed keywords

AMPA RECEPTOR; CALCIUM ION; CASEIN KINASE II; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; CYCLIN DEPENDENT KINASE 5; GLUTAMATE RECEPTOR; GLUTAMIC ACID; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; KAINIC ACID RECEPTOR; MAGNESIUM ION; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN 14 3 3; PROTEIN KINASE B; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; RECEPTOR SUBUNIT;

ALZHEIMER DISEASE; BRAIN; ENZYME SUBSTRATE; HUMAN; MENTAL DISEASE; NEUROLOGIC DISEASE; NEUROTRANSMISSION; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SCHIZOPHRENIA; SYNAPSE;

ANIMALS; GENE EXPRESSION; PHOSPHORYLATION; PROTEIN TRANSPORT; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 34547664721     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2007.05.018     Document Type: Review

References (87)

1. Barria A., and Malinow R. NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48 (2005) 289-301
2. Binshtok A.M., Fleidervish I.A., Sprengel R., and Gutnick M.J. NMDA receptors in layer 4 spiny stellate cells of the mouse barrel cortex contain the NR2C subunit. The Journal of Neuroscience 26 (2006) 708-715
3. 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., and Zhang D. Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 415 (2002) 793-798
4. Chen L., and Huang L.Y. Protein kinase C reduces Mg2+ block of NMDA-receptor channels as a mechanism of modulation. Nature 356 (1992) 521-523
5. Chung H.J., Huang Y.H., Lau L.F., and Huganir R.L. Regulation of the NMDA receptor complex and trafficking by activity-dependent phosphorylation of the NR2B subunit PDZ ligand. The Journal of Neuroscience 24 (2004) 10248-10259
6. Chen, B.S., Isaac, J.T., Roche, K.W., 2005. PKB Phosphorylation of the NMDA receptor subunit NR2C and binding to 14-3-3ε. Society for Neuroscience 35th Annual Meeting, Abstract 844.9.
7. Chen B.S., Braud S., Badger II J.D., Isaac J.T., and Roche K.W. Regulation of NR1/NR2C N-methyl-D-aspartate (NMDA) receptors by phosphorylation. The Journal of biological chemistry 281 (2006) 16583-16590
8. Ciabarra A.M., Sullivan J.M., Gahn L.G., Pecht G., Heinemann S., and Sevarino K.A. Cloning and characterization of chi-1: a developmentally regulated member of a novel class of the ionotropic glutamate receptor family. The Journal of Neuroscience 15 (1995) 6498-6508
9. Cohen N.A., Brenman J.E., Snyder S.H., and Bredt D.S. Binding of the inward rectifier K+ channel Kir 2.3 to PSD-95 is regulated by protein kinase A phosphorylation. Neuron 17 (1996) 759-767
10. Crump F.T., Dillman K.S., and Craig A.M. cAMP-dependent protein kinase mediates activity-regulated synaptic targeting of NMDA receptors. The Journal of Neuroscience 21 (2001) 5079-5088
11. Cull-Candy S., Brickley S., and Farrant M. NMDA receptor subunits: diversity, development and disease. Current Opinion in Neurobiology 11 (2001) 327-335
12. Cull-Candy, S.G., Leszkiewicz, D.N., 2004. Role of distinct NMDA receptor subtypes at central synapses. Science's STKE 2004, re16.
13. Dingledine R., Borges K., Bowie D., and Traynelis S.F. The glutamate receptor ion channels. Pharmacological Reviews 51 (1999) 7-61
14. Dunah A.W., Yasuda R.P., and Wolfe B.B. Developmental regulation of tyrosine phosphorylation of the NR2D NMDA glutamate receptor subunit in rat central nervous system. Journal of Neurochemistry 71 (1998) 1926-1934
15. Ehlers M.D., Zhang S., Bernhadt J.P., and Huganir R.L. Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell 84 (1996) 745-755
16. Ehlers M.D., Fung E.T., O'Brien R.J., and Huganir R.L. Splice variant-specific interaction of the NMDA receptor subunit NR1 with neuronal intermediate filaments. The Journal of Neuroscience 18 (1998) 720-730
17. Ellis P.D., Bissoon N., and Gurd J.W. Synaptic protein tyrosine kinase: partial characterization and identification of endogenous substrates. Journal of Neurochemistry 51 (1988) 611-620
18. Erreger K., Chen P.E., Wyllie D.J., and Traynelis S.F. Glutamate receptor gating. Critical Reviews in Neurobiology 16 (2004) 187-224
19. Fong D.K., Rao A., Crump F.T., and Craig A.M. Rapid synaptic remodeling by protein kinase C: reciprocal translocation of NMDA receptors and calcium/calmodulin-dependent kinase II. The Journal of Neuroscience 22 (2002) 2153-2164
20. Furukawa H., and Gouaux E. Mechanisms of activation, inhibition and specificity: crystal structures of the NMDA receptor NR1 ligand-binding core. The EMBO Journal 22 (2003) 2873-2885
21. Furukawa H., Singh S.K., Mancusso R., and Gouaux E. Subunit arrangement and function in NMDA receptors. Nature 438 (2005) 185-192
22. Gardoni F., Bellone C., Cattabeni F., and Di Luca M. Protein kinase C activation modulates alpha-calmodulin kinase II binding to NR2A subunit of N-methyl-d-aspartate receptor complex. The Journal of Biological Chemistry 276 (2001) 7609-7613
23. Grant E.R., Guttmann R.P., Seifert K.M., and Lynch D.R. A region of the rat N-methyl-d-aspartate receptor 2A subunit that is sufficient for potentiation by phorbol esters. Neuroscience Letters 310 (2001) 9-12
24. Groc L., Heine M., Cousins S.L., Stephenson F.A., Lounis B., Cognet L., and Choquet D. NMDA receptor surface mobility depends on NR2A-2B subunits. Proceedings of the National Academy of Sciences of the United States of America 103 (2006) 18769-18774
25. Hollmann M., and Heinemann S. Cloned glutamate receptors. Annual Review of Neuroscience 17 (1994) 31-108
26. Jones M.L., and Leonard J.P. PKC site mutations reveal differential modulation by insulin of NMDA receptors containing NR2A or NR2B subunits. Journal of Neurochemistry 92 (2005) 1431-1438
27. Karadottir R., Cavelier P., Bergersen L.H., and Attwell D. NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438 (2005) 1162-1166
28. Kim M.J., Dunah A.W., Wang Y.T., and Sheng M. Differential roles of NR2A- and NR2B-containing NMDA receptors in Ras-ERK signaling and AMPA receptor trafficking. Neuron 46 (2005) 745-760
29. Kohr G., and Seeburg P.H. Subtype-specific regulation of recombinant NMDA receptor-channels by protein tyrosine kinases of the src family. The Journal of Physiology 492 Pt 2 (1996) 445-452
30. Krupp J.J., Vissel B., Thomas C.G., Heinemann S.F., and Westbrook G.L. Calcineurin acts via the C-terminus of NR2A to modulate desensitization of NMDA receptors. Neuropharmacology 42 (2002) 593-602
31. 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. Protein kinase C modulates NMDA receptor trafficking and gating. Nature Neuroscience 4 (2001) 382-390
32. Lau L.F., and Huganir R.L. Differential tyrosine phosphorylation of N-methyl-d-aspartate receptor subunits. The Journal of Biological Chemistry 270 (1995) 20036-20041
33. Lavezzari G., McCallum J., Lee R., and Roche K.W. Differential binding of the AP-2 adaptor complex and PSD-95 to the C-terminus of the NMDA receptor subunit NR2B regulates surface expression. Neuropharmacology 45 (2003) 729-737
34. Lavezzari G., McCallum J., Dewey C.M., and Roche K.W. Subunit-specific regulation of NMDA receptor endocytosis. The Journal of Neuroscience 24 (2004) 6383-6391
35. Lee H.K. Synaptic plasticity and phosphorylation. Pharmacology & Therapeutics 112 (2006) 810-832
36. Li B.S., Sun M.K., Zhang L., Takahashi S., Ma W., Vinade L., Kulkarni A.B., Brady R.O., and Pant H.C. Regulation of NMDA receptors by cyclin-dependent kinase-5. Proceedings of the National Academy of Sciences of the United States of America 98 (2001) 12742-12747
37. Li B., Chen N., Luo T., Otsu Y., Murphy T.H., and Raymond L.A. Differential regulation of synaptic and extra-synaptic NMDA receptors. Nature Neuroscience 5 (2002) 833-834
38. Liao G.Y., Wagner D.A., Hsu M.H., and Leonard J.P. Evidence for direct protein kinase-C mediated modulation of N-methyl-d-aspartate receptor current. Molecular Pharmacology 59 (2001) 960-964
39. Lin J.W., Wyszynski M., Madhavan R., Sealock R., Kim J.U., and Sheng M. Yotiao, a novel protein of neuromuscular junction and brain that interacts with specific splice variants of NMDA receptor subunit NR1. The Journal of Neuroscience 18 (1998) 2017-2027
40. Liu X.Y., Chu X.P., Mao L.M., Wang M., Lan H.X., Li M.H., Zhang G.C., Parelkar N.K., Fibuch E.E., Haines M., Neve K.A., Liu F., Xiong Z.G., and Wang J.Q. Modulation of D2R-NR2B interactions in response to cocaine. Neuron 52 (2006) 897-909
41. Lu W.Y., Xiong Z.G., Lei S., Orser B.A., Dudek E., Browning M.D., and MacDonald J.F. G-protein-coupled receptors act via protein kinase C and Src to regulate NMDA receptors. Nature Neuroscience 2 (1999) 331-338
42. Mammen A.L., Kamboj S., and Huganir R.L. Protein phosphorylation of ligand-gated ion channels. Methods in Enzymology 294 (1999) 353-370
43. Markram H., and Segal M. Activation of protein kinase C suppresses responses to NMDA in rat CA1 hippocampal neurones. The Journal of Physiology 457 (1992) 491-501
44. Micu I., Jiang Q., Coderre E., Ridsdale A., Zhang L., Woulfe J., Yin X., Trapp B.D., McRory J.E., Rehak R., Zamponi G.W., Wang W., and Stys P.K. NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 439 (2006) 988-992
45. Monyer H., Burnashev N., Laurie D.J., Sakmann B., and Seeburg P.H. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12 (1994) 529-540
46. Moon I.S., Apperson M.L., and Kennedy M.B. The major tyrosine-phosphorylated protein in the postsynaptic density fraction is N-methyl-d-aspartate receptor subunit 2B. Proceedings of the National Academy of Sciences of the United States of America 91 (1994) 3954-3958
47. Mu Y., Otsuka T., Horton A.C., Scott D.B., and Ehlers M.D. Activity-dependent mRNA splicing controls ER export and synaptic delivery of NMDA receptors. Neuron 40 (2003) 581-594
48. Nakazawa T., Komai S., Tezuka T., Hisatsune C., Umemori H., Semba K., Mishina M., Manabe T., and Yamamoto T. Characterization of Fyn-mediated tyrosine phosphorylation sites on GluR epsilon 2 (NR2B) subunit of the N-methyl-d-aspartate receptor. The Journal of Biological Chemistry 276 (2001) 693-699
49. O'Kelly I., Butler M.H., Zilberberg N., and Goldstein S.A. Forward transport. 14-3-3 binding overcomes retention in endoplasmic reticulum by dibasic signals. Cell 111 (2002) 577-588
50. Okabe S., Miwa A., and Okado H. Alternative splicing of the C-terminal domain regulates cell surface expression of the NMDA receptor NR1 subunit. The Journal of Neuroscience 19 (1999) 7781-7792
51. Omkumar R.V., Kiely M.J., Rosenstein A.J., Min K.T., and Kennedy M.B. Identification of a phosphorylation site for calcium/calmodulin-dependent protein kinase II in the NR2B subunit of the N-methyl-d-aspartate receptor. The Journal of Biological Chemistry 271 (1996) 31670-31678
52. Prybylowski K., Chang K., Sans N., Kan L., Vicini S., and Wenthold R.J. The synaptic localization of NR2B-containing NMDA receptors is controlled by interactions with PDZ proteins and AP-2. Neuron 47 (2005) 845-857
53. Raman I.M., Tong G., and Jahr C.E. Beta-adrenergic regulation of synaptic NMDA receptors by cAMP-dependent protein kinase. Neuron 16 (1996) 415-421
54. Roche K.W., Standley S., McCallum J., Dune Ly C., Ehlers M.D., and Wenthold R.J. Molecular determinants of NMDA receptor internalization. Nature Neuroscience 4 (2001) 794-802
55. Roche K.W., Tingley W.G., and Huganir R.L. Glutamate receptor phosphorylation and synaptic plasticity. Current Opinion in Neurobiology 4 (1994) 383-388
56. Rumbaugh G., Prybylowski K., Wang J.F., and Vicini S. Exon 5 and spermine regulate deactivation of NMDA receptor subtypes. The Journal of Neurophysiology 83 (2000) 1300-1306
57. Salter M.G., and Fern R. NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 438 (2005) 1167-1171
58. Salter M.W., and Kalia L.V. Src kinases: a hub for NMDA receptor regulation. Nature Reviews 5 (2004) 317-328
59. Sanchez-Perez A.M., and Felipo V. Serines 890 and 896 of the NMDA receptor subunit NR1 are differentially phosphorylated by protein kinase C isoforms. Neurochemistry International 47 (2005) 84-91
60. Scott D.B., Blanpied T.A., Swanson G.T., Zhang C., and Ehlers M.D. An NMDA receptor ER retention signal regulated by phosphorylation and alternative splicing. The Journal of Neuroscience 21 (2001) 3063-3072
61. Scott D.B., Blanpied T.A., and Ehlers M.D. Coordinated PKA and PKC phosphorylation suppresses RXR-mediated ER retention and regulates the surface delivery of NMDA receptors. Neuropharmacology 45 (2003) 755-767
62. Scott D.B., Michailidis I., Mu Y., Logothetis D., and Ehlers M.D. Endocytosis and degradative sorting of NMDA receptors by conserved membrane-proximal signals. The Journal of Neuroscience 24 (2004) 7096-7109
63. Sigel E., Baur R., and Malherbe P. Protein kinase C transiently activated heteromeric N-methyl-d-aspartate receptor channels independent of the phosphorylatable C-terminal splice domain and of consensus phosphorylation sites. The Journal of Biological Chemistry 269 (1994) 8204-8208
64. 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. Protein kinase A regulates calcium permeability of NMDA receptors. Nature Neuroscience 9 (2006) 501-510
65. Snyder E.M., Nong Y., Almeida C.G., Paul S., Moran T., Choi E.Y., Nairn A.C., Salter M.W., Lombroso P.J., Gouras G.K., and Greengard P. Regulation of NMDA receptor trafficking by amyloid-beta. Nature Neuroscience 8 (2005) 1051-1058
66. Standley S., Roche K.W., McCallum J., Sans N., and Wenthold R.J. PDZ domain suppression of an ER retention signal in NMDA receptor NR1 splice variants. Neuron 28 (2000) 887-898
67. Steigerwald F., Schulz T.W., Schenker L.T., Kennedy M.B., Seeburg P.H., and Kohr G. C-Terminal truncation of NR2A subunits impairs synaptic but not extrasynaptic localization of NMDA receptors. The Journal of Neuroscience 20 (2000) 4573-4581
68. Stocca G., and Vicini S. Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons. The Journal of Physiology 507 Pt 1 (1998) 13-24
69. Strack S., and Colbran R.J. Autophosphorylation-dependent targeting of calcium/ calmodulin-dependent protein kinase II by the NR2B subunit of the N-methyl-d-aspartate receptor. The Journal of Biological Chemistry 273 (1998) 20689-20692
70. Strack S., McNeill R.B., and 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. The Journal of Biological Chemistry 275 (2000) 23798-23806
71. Sucher N.J., Akbarian S., Chi C.L., Leclerc C.L., Awobuluyi M., Deitcher D.L., Wu M.K., Yuan J.P., Jones E.G., and Lipton S.A. Developmental and regional expression pattern of a novel NMDA receptor-like subunit (NMDAR-L) in the rodent brain. The Journal of Neuroscience 15 (1995) 6509-6520
72. Takasu M.A., Dalva M.B., Zigmond R.E., and Greenberg M.E. Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 295 (2002) 491-495
73. Thomas C.G., Miller A.J., and Westbrook G.L. Synaptic and extrasynaptic NMDA receptor NR2 subunits in cultured hippocampal neurons. Journal of Neurophysiology 95 (2006) 1727-1734
74. Tingley W.G., Roche K.W., Thompson A.K., and Huganir R.L. Regulation of NMDA receptor phosphorylation by alternative splicing of the C-terminal domain. Nature 364 (1993) 70-73
75. Tingley W.G., Ehlers M.D., Kameyama K., Doherty C., Ptak J.B., Riley C.T., and Huganir R.L. Characterization of protein kinase A and protein kinase C phosphorylation of the N-methyl-d-aspartate receptor NR1 subunit using phosphorylation site-specific antibodies. The Journal of Biological Chemistry 272 (1997) 5157-5166
76. Tovar K.R., and Westbrook G.L. The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. The Journal of Neuroscience 19 (1999) 4180-4188
77. Traynelis S.F., Hartley M., and Heinemann S.F. Control of proton sensitivity of the NMDA receptor by RNA splicing and polyamines. Science (New York, NY) 268 (1995) 873-876
78. Traynelis S.F., Burgess M.F., Zheng F., Lyuboslavsky P., and Powers J.L. Control of voltage-independent zinc inhibition of NMDA receptors by the NR1 subunit. The Journal of Neuroscience 18 (1998) 6163-6175
79. Vissel B., Krupp J.J., Heinemann S.F., and Westbrook G.L. A use-dependent tyrosine dephosphorylation of NMDA receptors is independent of ion flux. Nature Neuroscience 4 (2001) 587-596
80. Wang Y.T., and Salter M.W. Regulation of NMDA receptors by tyrosine kinases and phosphatases. Nature 369 (1994) 233-235
81. Wang Y.T., Yu X.M., and Salter M.W. Ca(2+)-independent reduction of N-methyl-D-aspartate channel activity by protein tyrosine phosphatase. Proceedings of the National Academy of Sciences of the United States of America 93 (1996) 1721-1725
82. Wang J., Liu S., Fu Y., Wang J.H., and Lu Y. Cdk5 activation induces hippocampal CA1 cell death by directly phosphorylating NMDA receptors. Nature Neuroscience 6 (2003) 1039-1047
83. Waxman E.A., and Lynch D.R. N-methyl-D-aspartate receptor subtypes: multiple roles in excitotoxicity and neurological disease. The Neuroscientist 11 (2005) 37-49
84. Yang M., and Leonard J.P. Identification of mouse NMDA receptor subunit NR2A C-terminal tyrosine sites phosphorylated by coexpression with v-Src. The Journal of Neurochemistry 77 (2001) 580-588
85. Yuan H., Michelsen K., and Schwappach B. 14-3-3 dimers probe the assembly status of multimeric membrane proteins. Current Biology 13 (2003) 638-646
86. Zheng F., Gingrich M.B., Traynelis S.F., and Conn P.J. Tyrosine kinase potentiates NMDA receptor currents by reducing tonic zinc inhibition. Nature Neuroscience 1 (1998) 185-191
87. Zheng X., Zhang L., Wang A.P., Bennett M.V., and Zukin R.S. Protein kinase C potentiation of N-methyl-d-aspartate receptor activity is not mediated by phosphorylation of N-methyl-d-aspartate receptor subunits. Proceedings of the National Academy of Sciences of the United States of America 96 (1999) 15262-15267