Dual Palmitoylation of NR2 Subunits Regulates NMDA Receptor Trafficking

Neuron

Volumn 64, Issue 2, 2009, Pages 213-226

  Hayashi, Takashi ^a   Thomas, Gareth M ^a   Huganir, Richard L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CELLBIO; MOLNEURO; SIGNALING

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PALMITOYLTRANSFERASE; PROTEIN TYROSINE KINASE; TRANSFERASE; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN HEK293; CONTROLLED STUDY; GOLGI COMPLEX; HUMAN; HUMAN CELL; INTERNALIZATION; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN TRANSPORT; RECEPTOR OCCUPANCY;

ANESTHETICS, LOCAL; ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; CYSTEINE; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNOPRECIPITATION; LIPOYLATION; MEMBRANE PROTEINS; MICE; MUTATION; NEURONS; PALMITATES; PROTEIN TRANSPORT; PROTEIN-TYROSINE KINASES; RECEPTORS, N-METHYL-D-ASPARTATE; TETRODOTOXIN; TRANSFECTION; TRITIUM; TYROSINE;

EID: 70350207200     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2009.08.017     Document Type: Article

References (66)

1. Abe M., Fukaya M., Yagi T., Mishina M., Watanabe M., and Sakimura K. NMDA receptor GluRepsilon/NR2 subunits are essential for postsynaptic localization and protein stability of GluRzeta1/NR1 subunit. J. Neurosci. 24 (2004) 7292-7304
2. Alaluf S., Mulvihill E.R., and McIlhinney R.A. The metabotropic glutamate receptor mGluR4, but not mGluR1 alpha, is palmitoylated when expressed in BHK cells. J. Neurochem. 64 (1995) 1548-1555
3. Bijlmakers M.J., and Marsh M. The on-off story of protein palmitoylation. Trends Cell Biol. 13 (2003) 32-42
4. Bizzozero O.A. Chemical analysis of acylation sites and species. Methods Enzymol. 250 (1995) 361-379
5. Carroll R.C., and Zukin R.S. NMDA-receptor trafficking and targeting: implications for synaptic transmission and plasticity. Trends Neurosci. 25 (2002) 571-577
6. Cavara N.A., and Hollmann M. Shuffling the deck anew: how NR3 tweaks NMDA receptor function. Mol. Neurobiol. 38 (2008) 16-26
7. Chien A.J., Carr K.M., Shirokov R.E., Rios E., and Hosey M.M. Identification of palmitoylation sites within the L-type calcium channel beta2a subunit and effects on channel function. J. Biol. Chem. 271 (1996) 26465-26468
8. Collingridge G.L., Isaac J.T., and Wang Y.T. Receptor trafficking and synaptic plasticity. Nat. Rev. Neurosci. 5 (2004) 952-962
9. Constantine-Paton M., Cline H.T., and Debski E. Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annu. Rev. Neurosci. 13 (1990) 129-154
10. Cull-Candy S.G., and Leszkiewicz D.N. Role of distinct NMDA receptor subtypes at central synapses. Sci. STKE 2004 (2004) re16
11. Derkach V.A., Oh M.C., Guire E.S., and Soderling T.R. Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat. Rev. Neurosci. 8 (2007) 101-113
12. Dietrich L.E., Gurezka R., Veit M., and Ungermann C. The SNARE Ykt6 mediates protein palmitoylation during an early stage of homotypic vacuole fusion. EMBO J. 23 (2004) 45-53
13. Dietrich L.E., and Ungermann C. On the mechanism of protein palmitoylation. EMBO Rep. 5 (2004) 1053-1057
14. Dingledine R., Borges K., Bowie D., and Traynelis S.F. The glutamate receptor ion channels. Pharmacol. Rev. 51 (1999) 7-61
15. Drisdel R.C., Alexander J.K., Sayeed A., and Green W.N. Assays of protein palmitoylation. Methods 40 (2006) 127-134
16. Drisdel R.C., Manzana E., and Green W.N. The role of palmitoylation in functional expression of nicotinic alpha7 receptors. J. Neurosci. 24 (2004) 10502-10510
17. El-Husseini A.-D., and Bredt D.S. Protein palmitoylation: a regulator of neuronal development and function. Nat. Rev. Neurosci. 3 (2002) 791-802
18. Fukata M., Fukata Y., Adesnik H., Nicoll R.A., and Bredt D.S. Identification of PSD-95 Palmitoylating Enzymes. Neuron 44 (2004) 987-996
19. Hayashi T., and Huganir R.L. Tyrosine phosphorylation and regulation of the AMPA receptor by SRC family tyrosine kinases. J. Neurosci. 24 (2004) 6152-6160
20. Hayashi T., Rumbaugh G., and Huganir R.L. Differential regulation of AMPA receptor subunit trafficking by palmitoylation of two distinct sites. Neuron 47 (2005) 709-723
21. Hollmann M., and Heinemann S. Cloned glutamate receptors. Annu. Rev. Neurosci. 17 (1994) 31-108
22. Huang K., Yanai A., Kang R., Arstikaitis P., Singaraja R.R., Metzler M., Mullard A., Haigh B., Gauthier-Campbell C., Gutekunst C.A., et al. Huntingtin-interacting protein HIP14 is a palmitoyl transferase involved in palmitoylation and trafficking of multiple neuronal proteins. Neuron 44 (2004) 977-986
23. Kang R., Wan J., Arstikaitis P., Takahashi H., Huang K., Bailey A.O., Thompson J.X., Roth A.F., Drisdel R.C., Mastro R., et al. Neural palmitoyl-proteomics reveals dynamic synaptic palmitoylation. Nature 456 (2008) 904-909
24. Keller C.A., Yuan X., Panzanelli P., Martin M.L., Alldred M., Sassoe-Pognetto M., and Luscher B. The gamma2 subunit of GABA(A) receptors is a substrate for palmitoylation by GODZ. J. Neurosci. 24 (2004) 5881-5891
25. 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. Nat. Neurosci. 4 (2001) 382-390
26. Lau C.G., and Zukin R.S. NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nat. Rev. Neurosci. 8 (2007) 413-426
27. Lavezzari G., McCallum J., Dewey C.M., and Roche K.W. Subunit-specific regulation of NMDA receptor endocytosis. J. Neurosci. 24 (2004) 6383-6391
28. Leonard A.S., and Hell J.W. Cyclic AMP-dependent protein kinase and protein kinase C phosphorylate N-methyl-D-aspartate receptors at different sites. J. Biol. Chem. 272 (1997) 12107-12115
29. Li B., Chen N., Luo T., Otsu Y., Murphy T.H., and Raymond L.A. Differential regulation of synaptic and extra-synaptic NMDA receptors. Nat. Neurosci. 5 (2002) 833-834
30. Lin D.T., Makino Y., Sharma K., Hayashi T., Neve R., Takamiya K., and Huganir R.L. Regulation of AMPA receptor extrasynaptic insertion by 4.1N, phosphorylation and palmitoylation. Nat. Neurosci. 12 (2009) 879-887
31. Lobo S., Greentree W.K., Linder M.E., and Deschenes R.J. Identification of a Ras palmitoyltransferase in Saccharomyces cerevisiae. J. Biol. Chem. 277 (2002) 41268-41273
32. Malinow R., and Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25 (2002) 103-126
33. 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
34. Mori H., and Mishina M. Structure and function of the NMDA receptor channel. Neuropharmacology 34 (1995) 1219-1237
35. 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. J. Biol. Chem. 276 (2001) 693-699
36. Nakazawa T., Komai S., Watabe A.M., Kiyama Y., Fukaya M., Arima-Yoshida F., Horai R., Sudo K., Ebine K., Delawary M., et al. NR2B tyrosine phosphorylation modulates fear learning as well as amygdaloid synaptic plasticity. EMBO J. 25 (2006) 2867-2877
37. Ng G.Y., George S.R., Zastawny R.L., Caron M., Bouvier M., Dennis M., and O'Dowd B.F. Human serotonin1B receptor expression in Sf9 cells: phosphorylation, palmitoylation, and adenylyl cyclase inhibition. Biochemistry 32 (1993) 11727-11733
38. Ng G.Y., Mouillac B., George S.R., Caron M., Dennis M., Bouvier M., and O'Dowd B.F. Desensitization, phosphorylation and palmitoylation of the human dopamine D1 receptor. Eur. J. Pharmacol. 267 (1994) 7-19
39. Ng G.Y., O'Dowd B.F., Caron M., Dennis M., Brann M.R., and George S.R. Phosphorylation and palmitoylation of the human D2L dopamine receptor in Sf9 cells. J. Neurochem. 63 (1994) 1589-1595
40. Ohno Y., Kihara A., Sano T., and Igarashi Y. Intracellular localization and tissue-specific distribution of human and yeast DHHC cysteine-rich domain-containing proteins. Biochim. Biophys. Acta 1761 (2006) 474-483
41. Omkumar R.V., Kiely M.J., Rosenstein A.J., Min K.T., and Kennedy M.B. Identification of a phosphorylation site for calcium/calmodulindependent protein kinase II in the NR2B subunit of the N-methyl-D-aspartate receptor. J. Biol. Chem. 271 (1996) 31670-31678
42. Pickering D.S., Taverna F.A., Salter M.W., and Hampson D.R. Palmitoylation of the GluR6 kainate receptor. Proc. Natl. Acad. Sci. USA 92 (1995) 12090-12094
43. Ponimaskin E.G., Heine M., Joubert L., Sebben M., Bickmeyer U., Richter D.W., and Dumuis A. The 5-hydroxytryptamine(4a) receptor is palmitoylated at two different sites, and acylation is critically involved in regulation of receptor constitutive activity. J. Biol. Chem. 277 (2002) 2534-2546
44. Ponimaskin E.G., Schmidt M.F., Heine M., Bickmeyer U., and Richter D.W. 5-Hydroxytryptamine 4(a) receptor expressed in Sf9 cells is palmitoylated in an agonist-dependent manner. Biochem. J. 353 (2001) 627-634
45. 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
46. Qin N., Platano D., Olcese R., Costantin J.L., Stefani E., and Birnbaumer L. Unique regulatory properties of the type 2a Ca2+ channel beta subunit caused by palmitoylation. Proc. Natl. Acad. Sci. USA 95 (1998) 4690-4695
47. Rathenberg J., Kittler J.T., and Moss S.J. Palmitoylation regulates the clustering and cell surface stability of GABAA receptors. Mol. Cell. Neurosci. 26 (2004) 251-257
48. Resh M.D. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim. Biophys. Acta 1451 (1999) 1-16
49. Roche K.W., Standley S., McCallum J., Dune Ly C., Ehlers M.D., and Wenthold R.J. Molecular determinants of NMDA receptor internalization. Nat. Neurosci. 4 (2001) 794-802
50. Roth A.F., Feng Y., Chen L., and Davis N.G. The yeast DHHC cysteine-rich domain protein Akr1p is a palmitoyl transferase. J. Cell Biol. 159 (2002) 23-28
51. Schmidt J.W., and Catterall W.A. Palmitylation, sulfation, and glycosylation of the alpha subunit of the sodium channel. Role of post-translational modifications in channel assembly. J. Biol. Chem. 262 (1987) 13713-13723
52. 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
53. 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. J. Neurosci. 21 (2001) 3063-3072
54. 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. J. Neurosci. 24 (2004) 7096-7109
55. Seeburg P.H. The TiPS/Trends Neurosci. lecture: the molecular biology of mammalian glutamate receptor channels. Trends Pharmacol. Sci. 14 (1993) 297-303
56. Shepherd J.D., and Huganir R.L. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu. Rev. Cell Dev. Biol. 23 (2007) 613-643
57. Skeberdis V.A., Lan J., Zheng X., Zukin R.S., and Bennett M.V. Insulin promotes rapid delivery of N-methyl-D- aspartate receptors to the cell surface by exocytosis. Proc. Natl. Acad. Sci. USA 98 (2001) 3561-3566
58. Song I., and Huganir R.L. Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci. 25 (2002) 578-588
59. Stephenson F.A. Subunit characterization of NMDA receptors. Curr. Drug Targets 2 (2001) 233-239
60. Swope S.L., Moss S.J., Raymond L.A., and Huganir R.L. Regulation of ligand-gated ion channels by protein phosphorylation. Adv. Second Messenger Phosphoprotein Res. 33 (1999) 49-78
61. Uemura T., Mori H., and Mishina M. Isolation and characterization of Golgi apparatus-specific GODZ with the DHHC zinc finger domain. Biochem. Biophys. Res. Commun. 296 (2002) 492-496
62. 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. Nat. Neurosci. 4 (2001) 587-596
63. Wan J., Roth A.F., Bailey A.O., and Davis N.G. Palmitoylated proteins: purification and identification. Nat. Protoc. 2 (2007) 1573-1584
64. Wenthold R.J., Prybylowski K., Standley S., Sans N., and Petralia R.S. Trafficking of NMDA receptors. Annu. Rev. Pharmacol. Toxicol. 43 (2003) 335-358
65. Wenthold R.J., Sans N., Standley S., Prybylowski K., and Petralia R.S. Early events in the trafficking of N-methyl-D-aspartate (NMDA) receptors. Biochem. Soc. Trans. 31 (2003) 885-888
66. Yaka R., Thornton C., Vagts A.J., Phamluong K., Bonci A., and Ron D. NMDA receptor function is regulated by the inhibitory scaffolding protein, RACK1. Proc. Natl. Acad. Sci. USA 99 (2002) 5710-5715