A C-Terminal Determinant of GluR6 Kainate Receptor Trafficking

Journal of Neuroscience

Volumn 24, Issue 3, 2004, Pages 679-691

  Yan, Sheng ^a   Sanders, James M ^a   Xu, Jian ^b   Zhu, Yongling ^b   Contractor, Anis ^b,c   Swanson, Geoffrey T ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Endoplasmic reticulum; Glutamate receptor; Immunofluorescence; Kainate receptor; Patch clamp; Trafficking

Indexed keywords

ALANINE; AMPA RECEPTOR; GLUTAMATE RECEPTOR 6; GREEN FLUORESCENT PROTEIN; KAINIC ACID RECEPTOR; PROTEIN SUBUNIT;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CULTURE; CELL STRAIN COS7; CHIMERA; CONTROLLED STUDY; CYTOPLASM; ELECTROPHYSIOLOGY; EMBRYO; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN TRANSPORT; SITE DIRECTED MUTAGENESIS; SYNAPSE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE; COS CELLS; FLUORESCENT ANTIBODY TECHNIQUE; GLUTAMIC ACID; GREEN FLUORESCENT PROTEINS; HUMANS; KIDNEY; KINETICS; LUMINESCENT PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PATCH-CLAMP TECHNIQUES; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RECEPTORS, KAINIC ACID; RECOMBINANT FUSION PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSFECTION;

EID: 0842284000     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4985-03.2004     Document Type: Article

References (45)

1. Bowie D, Garcia EP, Marshall J, Traynelis SF, Lange GD (2003) Allosteric regulation and spatial distribution of kainate receptors bound to ancillary proteins. J Physiol (Lond) 547:373-385.
2. 2+ channels in hippocampal mossy fiber synaptic transmission and long-term potentiation. Neuron 12:261-269.
3. Coleman SK, Cai C, Mottershead DG, Haapalahti JP, Keinanen K (2003) Surface expression of GluR-D AMPA receptor is dependent on an interaction between its C-terminal domain and a 4.1 protein. J Neurosci 23:798-806.
4. Collingridge GL, Isaac JT (2003) Functional roles of protein interactions with AMPA and kainate receptors. Neurosci Res 47:3-15.
5. Contractor A, Swanson GT, Sailer A, O'Gorman S, Heinemann SF (2000) Identification of the kainate receptor subunits underlying modulation of excitatory synaptic transmission in the CA3 region of the hippocampus. J Neurosci 20:8269-8278.
6. Cosson P, Letourneur F (1994) Coatomer interaction with di-lysine endoplasmic reticulum retention motifs. Science 263:1629-1631.
7. Coussen F, Normand E, Marchal C, Costet P, Choquet D, Lambert M, Mege RM, Mulle C (2002) Recruitment of the kainate receptor subunit glutamate receptor 6 by cadherin/catenin complexes. J Neurosci 22:6426-6436.
8. Darstein M, Petralia RS, Swanson GT, Wenthold RJ, Heinemann SF (2003) Distribution of kainate receptor subunits at hippocampal mossy fiber synapses. J Neurosci 23:8013-8019.
9. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7-62.
10. El-Husseini AE, Craven SE, Brock SC, Bredt DS (2001) Polarized targeting of peripheral membrane proteins in neurons. J Biol Chem 276:44984-44992.
11. Falquet L, Pagni M, Bucher P, Hulo N, Sigrist CJ, Hofmann K, Bairoch A (2002) The PROSITE database, its status in 2002. Nucleic Acids Res 30:235-238.
12. Garcia EP, Mehta S, Blair LA, Wells DG, Shang J, Fukushima T, Fallon JR, Garner CC, Marshall J (1998) SAP90 binds and clusters kainate receptors causing incomplete desensitization. Neuron 21:727-739.
13. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287:2262-2267.
14. Herb A, Burnashev N, Werner P, Sakmann B, Wisden W, Seeburg PH (1992) The KA-2 subunit of excitatory amino acid receptors shows widespread expression in brain and forms ion channels with distantly related subunits. Neuron 8:775-785.
15. Hirbec H, Francis JC, Lauri SE, Braithwaite SP, Coussen F, Mulle C, Dev KK, Couthino V, Meyer G, Isaac JT, Collingridge GL, Henley JM (2003) Rapid and differential regulation of AMPA and kainate receptors at hippocampal mossy fibre synapses by PICK1 and GRIP. Neuron 37:625-638.
16. Hollmann M, Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17:31-108.
17. Kamiya H, Ozawa S (2000) Kainate receptor-mediated presynaptic inhibition at the mouse hippocampal mossy fibre synapse. J Physiol (Lond) 523:653-665.
18. Keller BU, Hollmann M, Heinemann S, Konnerth A (1992) Calcium influx through subunits GluR1/GluR3 of kainate/AMPA receptor channels is regulated by cAMP dependent protein kinase. EMBO J 11:891-896.
19. Ma D, Zerangue N, Raab-Graham K, Fried SR, Jan YN, Jan LY (2002) Diverse trafficking patterns due to multiple traffic motifs in G protein-activated inwardly rectifying potassium channels from brain and heart. Neuron 33:715-729.
20. Madden DR (2002) The structure and function of glutamate receptor ion channels. Nat Rev Neurosci 3:91-101.
21. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
22. Margeta-Mitrovic M, Jan YN, Jan LY (2000) A trafficking checkpoint controls GABA(B) receptor heterodimerization. Neuron 27:97-106.
23. Murthy VN, Sejnowski TJ, Stevens CF (1997) Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 18:599-612.
24. Nishimune A, Isaac JT, Molnar E, Noel J, Nash SR, Tagaya M, Collingridge GL, Nakanishi S, Henley JM (1998) NSF binding to GluR2 regulates synaptic transmission. Neuron 21:87-97.
25. 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.
26. Pagano A, Rovelli G, Mosbacher J, Lohmann T, Duthey B, Stauffer D, Ristig D, Schuler V, Meigel I, Lampert C, Stein T, Prezeau L, Blahos J, Pin J, Froestl W, Kuhn R, Heid J, Kaupmann K, Bettler B (2001) C-terminal interaction is essential for surface trafficking but not for heteromeric assembly of GABA(b) receptors. J Neurosci 21:1189-1202.
27. Pickering DS, Taverna FA, Salter MW, Hampson DR (1995) Palmitoylation of the GluR6 kainate receptor. Proc Natl Acad Sci USA 92:12090-12094.
28. Ren Z, Riley NJ, Garcia EP, Sanders JM, Swanson GT, Marshall J (2003) Multiple trafficking signals regulate kainate receptor KA2 subunit surface expression. J Neurosci 23:6608-6616.
29. Resh MD (1999) Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim Biophys Acta 1451:1-16.
30. Schiffer HH, Swanson GT, Heinemann SF (1997) Rat GluR7 and a carboxy-terminal splice variant, GluR7b, are functional kainate receptor subunits with a low sensitivity to glutamate. Neuron 19:1141-1146.
31. Schmitz D, Frerking M, Nicoll RA (2000) Synaptic activation of presynaptic kainate receptors on hippocampal mossy fiber synapses. Neuron 27:327-338.
32. 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.
33. Shen L, Liang F, Walensky LD, Huganir RL (2000) Regulation of AMPA receptor GluR1 subunit surface expression by a 4.1N-linked actin cytoskeletal association. J Neurosci 20:7932-7940.
34. Shi S, Hayashi Y, Esteban JA, Malinow R (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105:331-343.
35. Sommer B, Burnashev N, Verdoorn TA, Keinänen K, Sakmann B, Seeburg PH (1992) A glutamate receptor channel with high affinity for domoate and kainate. EMBO J 11:1651-1656.
36. Song I, Kamboj S, Xia J, Dong H, Liao D, Huganir RL (1998) Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors. Neuron 21:393-400.
37. Standley S, Roche KW, McCallum J, Sans N, Wenthold RJ (2000) PDZ domain suppression ofan ER retention signal in NMDA receptor NR1 splice variants. Neuron 28:887-898.
38. Swanson GT, Heinemann SF (1998) Heterogeneity of homomeric GluR5 kainate receptor desensitization expressed in HEK293 cells. J Physiol (Lond) 513:639-646.
39. Traynelis SF, Wahl P (1997) Control ofrat GluR6 glutamate receptor open probability by protein kinase A and calcineurin. J Physiol (Lond) 503:513-531.
40. Venkatesan S, Petrovic A, Locati M, Kim YO, Weissman D, Murphy PM (2001) A membrane-proximal basic domain and cysteine cluster in the C-terminal tail of CCR5 constitute a bipartite motifcritical for cell surface expression. J Biol Chem 276:40133-40145.
41. Vignes M, Collingridge GL (1997) The synaptic activation of kainate receptors. Nature 388:179-182.
42. Xia H, von Zastrow M, Malenka RC (2002) A novel anterograde trafficking signal present in the N-terminal extracellular domain of ionotropic glutamate receptors. J Biol Chem 277:47765-47769.
43. Xia Z, Dudek H, Miranti CK, Greenberg ME (1996) Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J Neurosci 16:5425-5436.
44. Yaffe MB, Leparc GG, Lai J, Obata T, Volinia S, Cantley LC (2001) A motif-based profile scanning approach for genome-wide prediction of signaling pathways. Nat Biotechnol 19:348-353.
45. Zerangue N, Schwappach B, Jan YN, Jan LY (1999) A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels. Neuron 22:537-548.