Activity-dependent endocytic sorting of kainate receptors to recycling or degradation pathways

EMBO Journal

Volumn 23, Issue 24, 2004, Pages 4749-4759

  Martin, Stéphane ^a   Henley, Jeremy M ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Endocytosis; Kainate receptors; Receptor recycling; Surface expression

Indexed keywords

CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUTAMATE RECEPTOR 6; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN KINASE C;

ARTICLE; CELL MEMBRANE; ENDOCYTOSIS; ENDOSOME; HIPPOCAMPUS; INTERNALIZATION; LYSOSOME; NERVE CELL; NERVE CELL PLASTICITY; NEUROTRANSMISSION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN TARGETING;

BICUCULLINE; CALCIUM; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENDOCYTOSIS; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; GABA ANTAGONISTS; HIPPOCAMPUS; KAINIC ACID; LYSOSOMES; N-METHYLASPARTATE; NEURONS; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RECEPTORS, KAINIC ACID; TETRODOTOXIN;

HIPPOCAMPUS HIPPOCAMPUS;

EID: 11244305900     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600483     Document Type: Article

References (45)

1. Barry MF, Ziff EB (2002) Receptor trafficking and the plasticity of excitatory synapses. Curr Opin Neurobiol 12: 279-286
2. Beattie EC, Carroll RC, Yu X, Morishita W, Yasuda A, von Zastrow M, Malenka RC (2000) Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat Neurosci 3: 1291-1300
3. Brose N, Rosenmund C (2002) Move over protein kinase C, you've got company: alternative cellular effectors of diacylglycerol and phorbol esters. J Cell Sci 115: 4399-4411
4. Castillo PE, Malenka RC, Nicoll RA (1997) Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 388: 182-188
5. Chittajallu R, Braithwaite SP, Clarke VRJ, Henley JM (1999) Kainate receptors: subunits, synaptic localisation and function. Trends Pharmacol Sci 20: 544-553
6. Cho K, Francis JC, Hirbec H, Dev K, Brown MW, Henley JM, Bashir ZI (2003) Regulation of kainate receptors by protein kinase C and metabotropic glutamate receptors. J Physiol 548: 723-730
7. Colledge M, Snyder EM, Crozier RA, Soderling JA, Jin Y, Langeberg LK, Lu H, Bear MF, Scott JD (2003) Ubiquitination regulates PSD-95 degradation and AMPA receptor surface expression. Neuron 40: 595-607
8. Cossart R, Tyzio R, Dinocourt C, Esclapez M, Hirsch JC, Ben-Ari Y, Bernard C (2001) Presynaptic kainate receptors that enhance the release of GABA on CA1 hippocampal interneurons. Neuron 29: 497-508
9. 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
10. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28: 511-525
11. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, Malinow R (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6: 136-143
12. Fleck MW, Cornell E, Mah SJ (2003) Amino-acid residues involved in glutamate receptor 6 kainate receptor gating and desensitization. J Neurosci 23: 1219-1227
13. Gallyas Jr F, Ball SM, Molnar E (2003) Assembly and cell surface expression of KA-2 subunit-containing kainate receptors. J Neurochem 86: 1414-1427
14. 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
15. Ghetti A, Heinemann SF (2000) NMDA-dependent modulation of hippocampal kainate receptors by calcineurin and Ca(2+)/calmodulin-dependent protein kinase. J Neurosci 20: 2766-2773
16. Hayes DM, Braud S, Hurtado DE, McCallum J, Standley S, Isaac JT, Roche KW (2003) Trafficking and surface expression of the glutamate receptor subunit, KA2. Biochem Biophys Res Commun 310: 8-13
17. Hirbec H, Francis JC, Lauri SE, Braithwaite SP, Coussen F, Mulle C, Dev KK, Coutinho 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
18. Isaac JTR, Mellor J, Hurtado D, Roche K (2004) Kainate receptor trafficking: physiological roles and molecular mechanisms. Pharmacol Therapeutics (in press)
19. Jaskolski F, Coussen F, Nagarajan N, Normand E, Rosenmund C, Mulle C (2004) Subunit composition and alternative splicing regulate membrane delivery of kainate receptors. J Neurosci 24: 2506-2515
20. Kameyama K, Lee HK, Bear MF, Huganir RL (1998) Involvement of a postsynaptic protein kinase A substrate in the expression of homosynaptic long-term depression. Neuron 21: 1163-1175
21. Kidd FL, Isaac JT (1999) Developmental and activity-dependent regulation of kainate receptors at thalamocortical synapses. Nature 400: 569-573
22. Lee HK, Kameyama K, Huganir RL, Bear MF (1998) NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus. Neuron 21: 1151-1162
23. 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
24. Lee SH, Simonetta A, Sheng M (2004) Subunit rules governing the sorting of internalized AMPA receptors in hippocampal neurons. Neuron 43: 221-236
25. Lerma J (2003) Roles and rules of kainate receptors in synaptic transmission. Nat Rev Neurosci 4: 481-495
26. Lerma J, Morales M, Vicente MA, Herreras O (1997) Glutamate receptors of the kainate type and synaptic transmission. Trends Neurosci 20: 9-12
27. Lerma J, Paternain AV, Rodriguez-Moreno A, Lopez-Garcia JC (2001) Molecular physiology of kainate receptors. Physiol Rev 81: 971-998
28. 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
29. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annn Rev Neurosci 25: 103-126
30. Melyan Z, Lancaster B, Wheal HV (2004) Metabotropic regulation of intrinsic excitability by synaptic activation of kainate receptors. J Neurosci 24: 4530-4534
31. Melyan Z, Wheal HV, Lancaster B (2002) Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron 34: 107-114
32. Mulle C, Sailer A, Perez-Otano I, Dickinson-Anson H, Castillo PE, Bureau I, Maron C, Gage FH, Mann JR, Bettler B, Heinemann SF (1998) Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 392: 601-605
33. Mulle C, Sailer A, Swanson GT, Brana C, O'Gorman S, Bettler B, Heinemann SF (2000) Subunit composition of kainate receptors in hippocampal interneurons. Neuron 28: 475-484
34. Noel J, Ralph GS, Pickard L, Williams J, Molnar E, Uney JB, Collingridge GL, Henley JM (1999) Surface expression of AMPA receptors in hippocampal neurons is regulated by an NSF-dependent mechanism. Neuron 23: 365-376
35. Patneau DK, Vyklicky L, Mayer ML (1993) Hippocampal neurons exhibit cyclothiazide-sensitive rapidly desensitizing responses to kainate. J Neurosci 13: 3496-3509
36. Raymond LA, Blackstone CD, Huganir RL (1993) Phosphorylation and modulation of recombinant GluR6 glutamate receptors by cAMP-dependent protein kinase. Nature 361: 637-641
37. Ren Z, Riley NJ, Garcia EP, Sanders JM, Swanson GT, Marshall J (2003a) Multiple trafficking signals regulate kainate receptor KA2 subunit surface expression. J Neurosci 23: 6608-6616
38. Ren Z, Riley NJ, Needleman LA, Sanders JM, Swanson GT, Marshall J (2003b) Cell surface expression of GluR5 kainate receptors is regulated by an endoplasmic reticulum retention signal. J Biol Chem 278: 52700-52709
39. Ruano D, Lambolez B, Rossier J, Paternain AV, Lerma J (1995) Kainate receptor subunits expressed in single cultured hippocampal neurones: molecular and functional variants by RNA editing. Neuron 14: 1009-1017
40. Schmitz D, Mellor J, Frerking M, Nicoll RA (2001) Presynaptic kainate receptors at hippocampal mossy fiber synapses. Proc Natl Acad Sci USA 98: 11003-11008
41. Terashima A, Cotton L, Dev KK, Meyer G, Zaman S, Duprat F, Henley JM, Collingridge GL, Isaac JT (2004) Regulation of synaptic strength and AMPA receptor subunit composition by PICK1. J Neurosci 24: 5381-5390
42. Traynelis SF, Wahl P (1997) Control of rat GluR6 glutamate receptor open probability by protein kinase A and calcineurin. J Physiol 503 (Part 3): 513-531
43. Vignes M, Collingridge GL (1997) The synaptic activation of kainate receptors. Nature 388: 179-182
44. Wang LY, Taverna FA, Huang XP, Macdonald JF, Hampson DR (1993) Phosphorylation and modulation of a kainate receptor (GluR6) by cAMP-dependent protein kinase. Science 259: 1173-1175
45. Yan S, Sanders JM, Xu J, Zhu Y, Contractor A, Swanson GT (2004) A C-terminal determinant of GluR6 kainate receptor trafficking. J Neurosci 24: 679-691