Endocytosis and degradative sorting of NMDA receptors by conserved membrane-proximal signals

Journal of Neuroscience

Volumn 24, Issue 32, 2004, Pages 7096-7109

  Scott, Derek B ^a   Michailidis, Ioannis ^b   Mu, Yuanyue ^a   Logothetis, Diomedes ^b   Ehlers, Michael D ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Endocytosis; Excitatory synaptic transmission; Intracellular trafficking; Late endosome; NMDA receptor; Synaptic plasticity

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN SUBUNIT;

ANIMAL CELL; ARTICLE; ENDOCYTOSIS; ENDOSOME; INTERNALIZATION; INTRACELLULAR TRANSPORT; LEARNING; MEMORY; NERVE CELL PLASTICITY; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC EFFICACY; SYNAPTIC TRANSMISSION;

AMINO ACID MOTIFS; ANIMALS; CERCOPITHECUS AETHIOPS; CONSERVED SEQUENCE; COS CELLS; ENDOCYTOSIS; ENDOSOMES; FEMALE; HUMANS; PATCH-CLAMP TECHNIQUES; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RECEPTORS, N-METHYL-D-ASPARTATE; XENOPUS LAEVIS;

EID: 4143131141     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0780-04.2004     Document Type: Article

References (76)

1. Abraham WC, Bear MF (1996) Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19:126-130.
2. Barria A, Malinow R (2002) Subunit-specific NMDA receptor trafficking to synapses. Neuron 35:345-353.
3. Bayer KU, De Koninck P, Leonard AS, Hell JW, Schulman H (2001) Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature 411:801-805.
4. Beattie EC, Carroll RC, Yu X, Morishita W, Yasuda H, von Zastrow M, Malenka RC (2000) Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat Neurosci 3:1291-1300.
5. Bolshakov VY, Siegelbaum SA (1994) Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science 264:1148-1152.
6. Bonifacino JS, Traub LM (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72:395-447.
7. Bredt DS, Nicoll RA (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40:361-379.
8. Bresler T, Shapira M, Boeckers T, Dresbach T, Futter M, Garner CC, Rosenblum K, Gundelfinger ED, Ziv NE (2004) Postsynaptic density assembly is fundamentally different from presynaptic active zone assembly. J Neurosci 24:1507-1520.
9. Bucci C, Thomsen P, Nicoziani P, McCarthy J, van Deurs B (2000) Rab7: a key to lysosome biogenesis. Mol Biol Cell 11:467-480.
10. Cao TT, Deacon HW, Reczek D, Bretscher A, von Zastrow M (1999) A kinase-regulated PDZ-domain interaction controls endocytic sorting of the beta2-adrenergic receptor. Nature 401:286-290.
11. Carroll RC, Zukin RS (2002) NMDA-receptor trafficking and targeting: implications for synaptic transmission and plasticity. Trends Neurosci 25:571-577.
12. Carroll RC, Beattie EC, von Zastrow M, Malenka RC (2001) Role of AMPA receptor endocytosis in synaptic plasticity. Nat Rev Neurosci 2:315-324.
13. Chavrier P, Parton RG, Hauri HP, Simons K, Zerial M (1990) Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62:317-329.
14. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28:511-525.
15. Ehlers MD, Zhang S, Bernhadt JP, Huganir RL (1996) Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell 84:745-755.
16. Friedman HV, Bresler T, Garner CC, Ziv NE (2000) Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27:57-69.
17. Goda Y, Davis GW (2003) Mechanisms of synapse assembly and disassembly. Neuron 40:243-264.
18. Grosshans DR, Clayton DA, Coultrap SJ, Browning MD (2002) LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult rat CA1. Nat Neurosci 5:27-33.
19. Heynen AJ, Quinlan EM, Bae DC, Bear MF (2000) Bidirectional, activity-dependent regulation of glutamate receptors in the adult hippocampus in vivo. Neuron 28:527-536.
20. Hicke L, Dunn R (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 19:141-172.
21. Kneussel M (2002) Dynamic regulation of GABA(A) receptors at synaptic sites. Brain Res Brain Res Rev 39:74-83.
22. Kohr G, Jensen V, Koester HJ, Mihaljevic AL, Utvik JK, Kvello A, Ottersen OP, Seeburg PH, Sprengel R, Hvalby O (2003) Intracellular domains of NMDA receptor subtypes are determinants for long-term potentiation induction. J Neurosci 23:10791-10799.
23. Krapivinsky G, Krapivinsky L, Manasian Y, Ivanov A, Tyzio R, Pellegrino C, Ben-Ari Y, Clapham DE, Medina I (2003) The NMDA receptor is coupled to the ERK pathway by a direct interaction between NR2B and Ras-GRF1. Neuron 40:775-784.
24. 2+-dependent inactivation of NMDA receptors. J Neurosci 19:1165-1178.
25. Lavezzari G, McCallum J, Lee R, Roche KW (2003) 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 45:729-737.
26. Lee SH, Liu L, Wang YT, Sheng M (2002) Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor trafficking and hippocampal LTD. Neuron 36:661-674.
27. Legendre P, Rosenmund C, Westbrook GL (1993) Inactivation of NMDA channels in cultured hippocampal neurons by intracellular calcium. J Neurosci 13:674-684.
28. Leonard AS, Bayer KU, Merrill MA, Lim IA, Shea MA, Schulman H, Hell JW (2002) Regulation of calcium/calmodulin-dependent protein kinase II docking to N-methyl-D-aspartate receptors by calcium/calmodulin and alpha-actinin. J Biol Chem 277:48441-48448.
29. Li B, Chen N, Luo T, Otsu Y, MurphyTH, Raymond LA (2002) Differential regulation of synaptic and extra-synaptic NMDA receptors. Nat Neurosci 5:833-834.
30. Liao D, Zhang X, O'Brien R, Ehlers MD, Huganir RL (1999) Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons. Nat Neurosci 2:37-43.
31. Lin JW, Ju W, Foster K, Lee SH, Ahmadian G, Wyszynski M, Wang YT, Sheng M (2000) Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization. Nat Neurosci 3:1282-1290.
32. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
33. Maxfield FR, McGraw TE (2004) Endocytic recycling. Nat Rev Mol Cell Biol 5:121-132.
34. McIlhinney RA, Le Bourdelles B, Molnar E, Tricaud N, Streit P, Whiting PJ (1998) Assembly intracellular targeting and cell surface expression of the human N-methyl-D-aspartate receptor subunits NR1a and NR2A in transfected cells. Neuropharmacology 37:1355-1367.
35. Mellman I (1996) Endocytosis and molecular sorting. Annu Rev Cell Dev Biol 12:575-625.
36. Meresse S, Gorvel JP, Chavrier P (1995) The rab7 GTPase resides on a vesicular compartment connected to lysosomes. J Cell Sci 108:3349-3358.
37. Montgomery JM, Madison DV (2002) State-dependent heterogeneity in synaptic depression between pyramidal cell pairs. Neuron 33:765-777.
38. Mori H, Manabe T, Watanabe M, Satoh Y, Suzuki N, Toki S, Nakamura K, Yagi T, Kushiya E, Takahashi T, Inoue Y, Sakimura K, Mishina M (1998) Role of the carboxy-terminal region of the GluR epsilon2 subunit in synaptic localization of the NMDA receptor channel. Neuron 21:571-580.
39. Mu Y, Otsuka T, Horton AC, Scott DB, Ehlers MD (2003) Activity-dependent mRNA splicing controls ER export and synaptic delivery of NMDA receptors. Neuron 40:581-594.
40. Mukherjee S, Ghosh RN, Maxfield FR (1997) Endocytosis. Physiol Rev 77:759-803.
41. Nong Y, Huang YQ, Ju W, Kalia LV, Ahmadian G, Wang YT, Salter MW (2003) Glycine binding primes NMDA receptor internalization. Nature 422:302-307.
42. Okabe S, Miwa A, Okado H (1999) Alternative splicing of the C-terminal domain regulates cell surface expression of the NMDA receptor NR1 subunit. J Neurosci 19:7781-7792.
43. Oliet SH, Malenka RC, Nicoll RA (1997) Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron 18:969-982.
44. Philpot BD, Sekhar AK, Shouval HZ, Bear MF (2001) Visual experience and deprivation bidirectionally modify the composition and function of NMDA receptors in visual cortex. Neuron 29:157-169.
45. Philpot BD, Espinosa JS, Bear MF (2003) Evidence for altered NMDA receptor function as a basis for metaplasticity in visual cortex. J Neurosci 23:5583-5588.
46. Prybylowski K, Fu Z, Losi G, Hawkins LM, Luo J, Chang K, Wenthold RJ, Vicini S (2002) Relationship between availability of NMDA receptor subunits and their expression at the synapse. J Neurosci 22:8902-8910.
47. Quinlan EM, Philpot BD, Huganir RL, Bear MF (1999) Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat Neurosci 2:352-357.
48. Rao A, Craig AM (1997) Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons. Neuron 19:801-812.
49. Roche KW, Standley S, McCallum J, Dune Ly C, Ehlers MD, Wenthold RJ (2001) Molecular determinants of NMDA receptor internalization. Nat Neurosci 4:794-802.
50. Rosenmund C, Westbrook GL (1993a) Calcium-induced actin depolymerization reduces NMDA channel activity. Neuron 10:805-814.
51. 2+ and ATP. J Physiol (Lond) 470:705-729.
52. Scott DB, Blanpied TA, Swanson GT, Zhang C, Ehlers MD (2001) An NMDA receptor ER retention signal regulated by phosphorylation and alternative splicing. J Neurosci 21:3063-3072.
53. Scott DB, Blanpied TA, Ehlers MD (2003) Coordinated PKA and PKC phosphorylation suppresses RXR-mediated ER retention and regulates the surface delivery of NMDA receptors. Neuropharmacology 45:755-767.
54. Snyder EM, Philpot BD, Huber KM, Dong X, Fallon JR, Bear MF (2001) Internalization of ionotropic glutamate receptors in response to mGluR activation. Nat Neurosci 4:1079-1085.
55. Sonnichsen B, De Renzis S, Nielsen E, Rietdorf J, Zerial M (2000) Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol 149:901-914.
56. Sprengel R, Suchanek B, Amico C, Brusa R, Burnashev N, Rozov A, Hvalby O, Jensen V, Paulsen O, Andersen P, Kim JJ, Thompson RF, Sun W, Webster LC, Grant SG, Eilers J, Konnerth A, Li J, McNamara JO, Seeburg PH (1998) Importance of the intracellular domain of NR2 subunits for NMDA receptor function in vivo. Cell 92:279-289.
57. Standley S, Roche KW, McCallum J, Sans N, Wenthold RJ (2000) PDZ domain suppression of an ER retention signal in NMDA receptor NR1 splice variants. Neuron 28:887-898.
58. Steigerwald F, Schulz TW, Schenker LT, Kennedy MB, Seeburg PH, Kohr G (2000) C-Terminal truncation of NR2A subunits impairs synaptic but not extrasynaptic localization of NMDA receptors. J Neurosci 20:4573-4581.
59. Tan PK, Waites C, Liu Y, Krantz DE, Edwards RH (1998) A leucine-based motif mediates the endocytosis of vesicular monoamine and acetylcholine transporters. J Biol Chem 273:17351-17360.
60. Tjelle TE, Brech A, Juvet LK, Griffiths G, Berg T (1996) Isolation and characterization of early endosomes, late endosomes and terminal lysosomes: their role in protein degradation. J Cell Sci 109:2905-2914.
61. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:892-896.
62. Vissel B, Krupp JJ, Heinemann SF, Westbrook GL (2001) A use-dependent tyrosine dephosphorylation of NMDA receptors is independent of ion flux. Nat Neurosci 4:587-596.
63. Vitelli R, Santillo M, Lattero D, Chiariello M, Bifulco M, Bruni CB, Bucci C (1997) Role of the small GTPase Rab7 in the late endocytic pathway. J Biol Chem 272:4391-4397.
64. von Zastrow M, Svingos A, Haberstock-Debic H, Evans C (2003) Regulated endocytosis of opioid receptors: cellular mechanisms and proposed roles in physiological adaptation to opiate drugs. Curr Opin Neurobiol 13:348-353.
65. 2+] and is prevented by ATP in rat spinal dorsal horn neurons. Neurosci Lett 157:183-186.
66. Washbourne P, Bennett JE, McAllister AK (2002) Rapid recruitment of NMDA receptor transport packets to nascent synapses. Nat Neurosci 5:751-759.
67. Watt AJ, van Rossum MC, MacLeod KM, Nelson SB, Turrigiano GG (2000) Activity coregulates quantal AMPA and NMDA currents at neocortical synapses. Neuron 26:659-670.
68. Wenthold RJ, Prybylowski K, Standley S, Sans N, Petralia RS (2003) Trafficking of NMDA receptors. Annu Rev Pharmacol Toxicol 43:335-358.
69. Westphal RS, Tavalin SJ, Lin JW, Alto NM, Fraser ID, Langeberg LK, Sheng M, Scott JD (1999) Regulation of NMDA receptors by an associated phosphatase-kinase signaling complex. Science 285:93-96.
70. Wiley HS, Burke PM (2001) Regulation of receptor tyrosine kinase signaling by endocytic trafficking. Traffic 2:12-18.
71. Wyszynski M, Lin J, Rao A, Nigh E, Beggs AH, Craig AM, Sheng M (1997) Competitive binding of alpha-actinin and calmodulin to the NMDA receptor. Nature 385:439-442.
72. Xia H, Hornby ZD, Malenka RC (2001) An ER retention signal explains differences in surface expression of NMDA and AMPA receptor subunits. Neuropharmacology 41:714-723.
73. Xu J, Paquet M, Lau AG, Wood JD, Ross CA, Hall RA (2001) beta 1-adrenergic receptor association with the synaptic scaffolding protein membrane-associated guanylate kinase inverted-2 (MAGI-2). Differential regulation of receptor internalization by MAGI-2 and PSD-95. J Biol Chem 276:41310-41317.
74. Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2:107-117.
75. Zhang S, Ehlers MD, Bernhardt JP, Su CT, Huganir RL (1998) Calmodulin mediates calcium-dependent inactivation of N-methyl-D-aspartate receptors. Neuron 21:443-453.
76. Zukin RS, Bennett MV (1995) Alternatively spliced isoforms of the NMDARI receptor subunit. Trends Neurosci 18:306-313.