P2X Receptor Trafficking in Neurons Is Subunit Specific

Journal of Neuroscience

Volumn 22, Issue 12, 2002, Pages 4814-4824

  Bobanovic, Laura K ^a   Royle, Stephen J ^a   Murrell Lagnado, Ruth D ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

ATP; Dynamin; Endocytosis; Heteromer; Ionotropic receptor; P2X; Presynaptic; Recycling; Trafficking

Indexed keywords

ADENOSINE TRIPHOSPHATE; DYNAMIN; IONOTROPIC RECEPTOR; PURINE P2X RECEPTOR; GLUTAMIC ACID; GUANOSINE TRIPHOSPHATASE; PRESYNAPTIC RECEPTOR; PROTEIN SUBUNIT; PURINE P2 RECEPTOR; PURINE P2X2 RECEPTOR; PURINE P2X4 RECEPTOR; PURINE P2X6 RECEPTOR;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENDOSOME; GENE INSERTION; HUMAN; HUMAN CELL; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR BINDING; SYNAPTIC TRANSMISSION; ANIMAL; CELL CULTURE; CELL LINE; CYTOLOGY; DRUG EFFECT; DRUG POTENTIATION; ENDOCYTOSIS; KINETICS; METABOLISM; NERVE CELL; OLFACTORY BULB; PHYSIOLOGY; PROTEIN TRANSPORT; SYNAPSE; WISTAR RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELL LINE; CELL MEMBRANE; CELLS, CULTURED; DYNAMINS; ENDOCYTOSIS; GLUTAMIC ACID; GTP PHOSPHOHYDROLASES; HUMANS; KINETICS; NEURONS; OLFACTORY BULB; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RATS; RATS, WISTAR; RECEPTORS, PRESYNAPTIC; RECEPTORS, PURINERGIC P2; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 0037096435     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-12-04814.2002     Document Type: Article

References (44)

1. 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.
2. Burrone J, Murthy VN (2001) Synaptic plasticity: rush hour traffic in the AMPA lanes. Curr Biol 11:R274-R277.
3. Carroll RC, Beattie EC, Xia HH, Luscher C, Altschuler Y, Nicoll RA, Malenka RC, von Zastrow M (1999) Dynamin-dependent endocytosis of ionotropic glutamate receptors. Proc Natl Acad Sci USA 96:14112-14117.
4. Carroll RC, Beattie EC, von Zastrow M, Malenka RC (2001) Role of AMPA receptor endocytosis in synaptic plasticity. Nat Rev Neurosci 2:315-324.
5. Collo G, North RA, Kawashima E, Merlo-Pich E, Neidhart S, Surprenant A, Buell G (1996) Cloning of P2X5 and P2X6 receptors and the distribution and properties of an extended family of ATP-gated ion channels. J Neurosci 16:2495-2507.
6. Dutton JL, Poronnik P, Li GH, Holding CA, Worthington RA, Vandenberg RJ, Cook DI, Barden JA, Bennett MR (2000) P2X1 receptor membrane redistribution and down-regulation visualized by using receptor-coupled green fluorescent protein chimeras. Neuropharmacology 39:2054-2066.
7. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28:511-525.
8. Ennion SJ, Evans RJ (2001) Agonist-stimulated internalisation of the ligand-gated ion channel P2X(1) in rat vas deferens. FEBS Lett 489:154-158.
9. Evans RJ (1996) Single channel properties of ATP-gated cation channels (P2X receptors) heterologously expressed in Chinese hamster ovary cells. Neurosci Lett 212:212-214.
10. Faddis BT, Hasbani MJ, Goldberg MP (1997) Calpain activation contributes to dendritic remodeling after brief excitotoxic injury in vitro. J Neurosci 17:951-959.
11. Gu JG, MacDermott AB (1997) Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses. Nature 389:749-753.
12. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85-100.
13. Hasbani MJ, Hyrc KL, Faddis BT, Romano C, Goldberg MP (1998) Distinct roles for sodium, chloride, and calcium in excitotoxic dendritic injury and recovery. Exp Neurol 154:241-258.
14. Hugel S, Schlichter R (2000) Presynaptic P2X receptors facilitate inhibitory GABAergic transmission between cultured rat spinal cord dorsal horn neurons. J Neurosci 20:2121-2130.
15. Kanjhan R, Housley GD, Burton LD, Christie DL, Kippenberger A, Thorne PR, Luo L, Ryan AF (1999) Distribution of the P2X2 receptor subunit of the ATP-gated ion channels in the rat central nervous system. J Comp Neurol 407:11-32.
16. Kato F, Shigetomi E (2001) Distinct modulation of evoked and spontaneous EPSCs by purinoceptors in the nucleus tractus solitarii of the rat. J Physiol (Lond) 530:469-486.
17. Khakh BS (2001) Molecular physiology of P2X receptors and ATP signalling at synapses. Nat Rev Neurosci 2:165-174.
18. Khakh BS, Henderson G (1998) ATP receptor-mediated enhancement of fast excitatory neurotransmitter release in the brain. Mol Pharmacol 54:372-378.
19. Khakh BS, Proctor WR, Dunwiddie TV, Labarca C, Lester HA (1999) Allosteric control of gating and kinetics at P2X(4) receptor channels. J Neurosci 19:7289-7299.
20. Khakh BS, Smith WB, Chiu CS, Ju DH, Davidson N, Lester HA (2001a) Activation-dependent changes in receptor distribution and dendritic morphology in hippocampal neurons expressing P2X2-green fluorescent protein receptors. Proc Natl Acad Sci USA 98:5288-5293.
21. Khakh BS, Burnstock G, Kennedy C, King BF, North RA, Seguela P, Voigt M, Humphrey PP (2001b) International union of pharmacology. XXIV Current status of the nomenclature and properties of P2X receptors and their subunits Pharmacol Rev 53:107-118.
22. Kittler JT, Delmas P, Jovanovic JN, Brown DA, Smart TG, Moss SJ (2000) Constitutive endocytosis of GABAA receptors by an association with the adaptin AP2 complex modulates inhibitory synaptic currents in hippocampal neurons. J Neurosci 20:7972-7977.
23. 2+ release signals in NGF-differentiated PC12 cells and hippocampal neurons. Neuron 22:125-137.
24. Kozak M (1987) An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res 15:8125-8148.
25. Lê KT, Villeneuve P, Ramjaun AR, McPherson PS, Beaudet A, Seguela P (1998) Sensory presynaptic and widespread somatodendritic immunolocalization of central ionotropic P2X ATP receptors. Neuroscience 83:177-190.
26. Li GH, Lee EM, Blair D, Holding C, Poronnik P, Cook DI, Barden JA, Bennett MR (2000) The distribution of P2X receptor clusters on individual neurons in sympathetic ganglia and their redistribution on agonist activation. J Biol Chem 275:29107-29112.
27. 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 receptors internalization. Nat Neurosci 3:1282-1290.
28. Lissin DV, Gomperts SN, Carroll RC, Christine CW, Kalman D, Kitamura M, Hardy S, Nicoll RA, Malenka RC, von Zastrow M (1998) Activity differentially regulates the surface expression of synaptic AMPA and NMDA glutamate receptors. Proc Natl Acad Sci USA 95:7097-7102.
29. Man HY, Lin JW, Ju WH, Ahmadian G, Liu LD, Becker LE, Sheng M, Wang YT (2000) Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron 25:649-662.
30. Marsh M, McMahon HT (1999) The structural era of endocytosis. Science 285:215-220.
31. Moss SJ, Smart TG (2001) Constructing inhibitory synapses. Nat Rev Neurosci 2:240-250.
32. Nakatsuka T, Gu JG (2001) ATP P2X receptor-mediated enhancement of glutamate release and evoked EPSCs in dorsal horn neurons of the rat spinal cord. J Neurosci 21:6522-6531.
33. Norenberg W, Illes P (2000) Neuronal P2X receptors: localisation and functional properties. Naunyn Schmiedebergs Arch Pharmacol 362:324-339.
34. Roche KW, Standley S, McCallum J, Dune LC, Ehlers MD, Wenthold RJ (2001) Molecular determinants of NMDA receptor internalization. Nat Neurosci 4:794-802.
35. Rubio ME, Soto F (2001) Distinct Localization of P2X receptors at excitatory postsynaptic specializations. J Neurosci 21:641-653.
36. Sheng M, Lee SH (2001) AMPA receptor trafficking and the control of synaptic transmission. Cell 105:825-828.
37. Shi SH, Hayashi Y, Esteban JA, Malinow R (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105:331-343.
38. Soto F, Garcia-Guzman M, Gomez-Hernandez JM, Hollmann M, Karschin C, Stuhmer W (1996) P2X4: an ATP-activated ionotropic receptor cloned from rat brain. Proc Natl Acad Sci USA 93:3684-3688.
39. Stoop R, Thomas S, Rassendren F, Kawashima E, Buell G, Surprenant A, North RA (1999) Contribution of individual subunits to the multimeric P2X(2) receptor: estimates based on methanethiosulfonate block at T336C. Mol Pharmacol 56:973-981.
40. Torres GE, Egan TM, Voigt MM (1999) Hetero-oligomeric assembly of P2X receptor subunits. Specificities exist with regard to possible partners. J Biol Chem 274:6653-6659.
41. Turrigiano GG (2000) AMPA receptors unbound: Membrane cycling and synaptic plasticity. Neuron 26:5-8.
42. Vulchanova L, Riedl MS, Shuster SJ, Buell G, Surprenant A, North RA, Elde R (1997) Immunohistochemical study of the P2X2 and P2X3 receptor subunits in rat, monkey sensory neurons and their central terminals. Neuropharmacology 36:1229-1242.
43. Wang YT, Linden DJ (2000) Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Neuron 25:635-647.
44. 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.