Stabilization of GABA A receptors at endocytic zones is mediated by an AP2 binding motif within the GABA Areceptor β3 subunit

Journal of Neuroscience

Volumn 32, Issue 7, 2012, Pages 2485-2498

  Smith, Katharine R ^a   Muir, James ^a   Rao, Yijian ^b   Browarski, Marietta ^a   Gruenig, Marielle C ^b   Sheehan, David F ^a   Haucke, Volker ^b   Kittler, Josef T ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BETA3; ADAPTOR PROTEIN; CLATHRIN; SYNAPSE RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; DENDRITE; EMBRYO; ENDOCYTOSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; EPILEPSY; FEMALE; HIPPOCAMPUS; IMMUNOFLUORESCENCE; INTERNALIZATION; ISCHEMIA; MALE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; RAT; SURFACE PLASMON RESONANCE; SYNAPTIC INHIBITION;

ADAPTOR PROTEIN COMPLEX 2; AMINO ACID MOTIFS; ANIMALS; CELLS, CULTURED; ENDOCYTOSIS; FEMALE; MALE; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN SUBUNITS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A;

EID: 84863403465     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1622-11.2011     Document Type: Article

References (60)

1. Arancibia-Cárcamo IL, Kittler JT (2009) Regulation of GABA(A) receptor membrane trafficking and synaptic localization. Pharmacol Ther 123:17-31.
2. Arancibia-Cárcamo IL, Yuen EY, Muir J, Lumb MJ, Michels G, Saliba RS, Smart TG, Yan Z, Kittler JT, Moss SJ (2009) Ubiquitin-dependent lysosomal targeting of GABA(A) receptors regulates neuronal inhibition. Proc Natl Acad Sci U S A 106:17552-17557.
3. Bannai H, Lévi S, Schweizer C, Inoue T, Launey T, Racine V, Sibarita JB, Mikoshiba K, Triller A (2009) Activity-dependent tuning of inhibitory neurotransmission based on GABAAR diffusion dynamics. Neuron 62:670-682.
4. Bedford FK, Kittler JT, Muller E, Thomas P, Uren JM, Merlo D, Wisden W, Triller A, Smart TG, Moss SJ (2001) GABA(A) receptor cell surface number and subunit stability are regulated by the ubiquitin-like protein Plic-1. Nat Neurosci 4:908-916.
5. Blanpied TA, Scott DB, Ehlers MD (2002) Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron 36:435-449.
6. Bradley CA, Taghibiglou C, Collingridge GL, Wang YT (2008) Mechanisms involved in the reduction of GABAA receptor alpha1-subunit expression caused by the epilepsy mutation A322D in the trafficking-competent receptor. J Biol Chem 283:22043-22050.
7. Brandon NJ, Jovanovic JN, Smart TG, Moss SJ (2002) Receptor for activated C kinase-1 facilitates protein kinase C-dependent phosphorylation and functional modulation of GABAA receptors with the activation of G-protein-coupled receptors. J Neurosci 22:6353-6361.
8. Carroll RC, Beattie EC, Xia H, Lüscher C, Altschuler Y, Nicoll RA, Malenka RC, von Zastrow M (1999) Dynamin-dependent endocytosis of ionotropic glutamate receptors. Proc Natl Acad Sci U S A 96:14112-14117.
9. Chen C, Zhuang X (2008) Epsin 1 is a cargo-specific adaptor for the clathrin-mediated endocytosis of the influenza virus. Proc Natl Acad Sci U S A 105:11790-11795.
10. Chen G, Kittler JT, Moss SJ, Yan Z (2006) Dopamine D3 receptors regulate GABAA receptor function through a phospho-dependent endocytosis mechanism in nucleus accumbens. J Neurosci 26:2513-2521.
11. Chou WH, Wang D, McMahon T, Qi ZH, Song M, Zhang C, Shokat KM, Messing RO (2010) GABAA receptor trafficking is regulated by protein kinase Ce{open} and the N-ethylmaleimide-sensitive factor. J Neurosci 30:13955-13965.
12. Collins BM, McCoy AJ, Kent HM, Evans PR, Owen DJ (2002) Molecular architecture and functional model of the endocytic AP2 complex. Cell 109:523-535.
13. Diviani D, Lattion AL, Abuin L, Staub O, Cotecchia S (2003) The adaptor complex 2 directly interacts with the alpha 1b-adrenergic receptor and plays a role in receptor endocytosis. J Biol Chem 278:19331-19340.
14. Dixon RM, Mellor JR, Hanley JG (2009) PICK1-mediated glutamate receptor subunit 2 (GluR2) trafficking contributes to cell death in oxygen/glucose-deprived hippocampal neurons. J Biol Chem 284:14230-14235.
15. Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Annu Rev Biochem 78:857-902.
16. Dumoulin A, Rostaing P, Bedet C, Lévi S, Isambert MF, Henry JP, Triller A, Gasnier B (1999) Presence of the vesicular inhibitory amino acid transporter in GABAergic and glycinergic synaptic terminal boutons. J Cell Sci 112:811-823.
17. Goodkin HP, Yeh JL, Kapur J (2005) Status epilepticus increases the intracellular accumulation of GABAA receptors. J Neurosci 25:5511-5520.
18. Goto H, Terunuma M, Kanematsu T, Misumi Y, Moss SJ, Hirata M (2005) Direct interaction of N-ethylmaleimide-sensitive factor with GABA(A) receptor beta subunits. Mol Cell Neurosci 30:197-206.
19. Groc L, Choquet D (2006) AMPA and NMDA glutamate receptor trafficking: multiple roads for reaching and leaving the synapse. Cell Tissue Res 326:423-438.
20. Hanley JG, Henley JM (2005) PICK1 is a calcium-sensor for NMDAinduced AMPA receptor trafficking. EMBO J 24:3266-3278.
21. Haucke V, Wenk MR, Chapman ER, Farsad K, De Camilli P (2000) Dual interaction of synaptotagmin with mu2- and alpha-adaptin facilitates clathrin-coated pit nucleation. EMBO J 19:6011-6019.
22. Herring D, Huang R, Singh M, Robinson LC, Dillon GH, Leidenheimer NJ (2003) Constitutive GABAA receptor endocytosis is dynamin-mediated and dependent on a dileucine AP2 adaptin-binding motif within the beta 2 subunit of the receptor. J Biol Chem 278:24046-24052.
23. Jacob TC, Wan Q, Vithlani M, Saliba RS, Succol F, Pangalos MN, Moss SJ (2009) GABA(A) receptor membrane trafficking regulates spine maturity. Proc Natl Acad Sci U S A 106:12500-12505.
24. Jovanovic JN, Thomas P, Kittler JT, Smart TG, Moss SJ (2004) Brainderived neurotrophic factor modulates fast synaptic inhibition by regulating GABAA receptor phosphorylation, activity, and cell-surface stability. J Neurosci 24:522-530.
25. Kastning K, Kukhtina V, Kittler JT, Chen G, Pechstein A, Enders S, Lee SH, Sheng M, Yan Z, Haucke V (2007) Molecular determinants for the interactionbetween AMPA receptors and the clathrin adaptor complex AP-2. Proc Natl Acad Sci U S A 104:2991-2996.
26. Kelley MH, Taguchi N, Ardeshiri A, Kuroiwa M, Hurn PD, Traystman RJ, Herson PS (2008) Ischemic insult to cerebellar Purkinje cells causes diminished GABAA receptor function and allopregnanolone neuroprotection is associated with GABAA receptor stabilization. J Neurochem 107:668-678.
27. 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.
28. Kittler JT, Thomas P, Tretter V, Bogdanov YD, Haucke V, Smart TG, Moss SJ (2004) Huntingtin-associated protein 1 regulates inhibitory synaptic transmission by modulating gamma-aminobutyric acid type A receptor membrane trafficking. Proc Natl Acad Sci U S A 101:12736-12741.
29. Kittler JT, Chen G, Honing S, Bogdanov Y, McAinsh K, Arancibia-Carcamo IL, Jovanovic JN, Pangalos MN, Haucke V, Yan Z, Moss SJ (2005) Phospho-dependent binding of the clathrin AP2 adaptor complex to GABAA receptors regulates the efficacy of inhibitory synaptic transmission. Proc Natl Acad Sci U S A 102:14871-14876.
30. Kittler JT, Chen G, Kukhtina V, Vahedi-Faridi A, Gu Z, Tretter V, Smith KR, McAinsh K, Arancibia-Carcamo IL, Saenger W, Haucke V, Yan Z, Moss SJ (2008) Regulation of synaptic inhibition by phospho-dependent binding of the AP2 complex to a YECL motif in the GABAA receptor gamma2 subunit. Proc Natl Acad Sci U S A 105:3616-3621.
31. Kurotani T, Yamada K, Yoshimura Y, Crair MC, Komatsu Y (2008) Statedependent bidirectional modification of somatic inhibition in neocortical pyramidal cells. Neuron 57:905-916.
32. Laurie DJ, Wisden W, Seeburg PH (1992) The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci 12:4151-4172.
33. 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.
34. Lipton P (1999) Ischemic cell death in brain neurons. Physiol Rev 79: 1431-1568.
35. Liu B, Li L, Zhang Q, Chang N, Wang D, Shan Y, Li L, Wang H, Feng H, Zhang L, Brann DW, Wan Q (2010) Preservation of GABAA receptor function by PTEN inhibition protects against neuronal death in ischemic stroke. Stroke 41:1018-1026.
36. Lo EH, Dalkara T, Moskowitz MA (2003) Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 4:399-415.
37. Macaskill AF, Rinholm JE, Twelvetrees AE, Arancibia-Carcamo IL, Muir J, Fransson A, Aspenstrom P, Attwell D, Kittler JT (2009) Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 61:541-555.
38. Martens H, Weston MC, Boulland JL, Grønborg M, Grosche J, Kacza J, Hoffmann A, Matteoli M, Takamori S, Harkany T, Chaudhry FA, Rosenmund C, Erck C, Jahn R, Härtig W (2008) Unique luminal localization of VGAT-C terminus allows for selective labeling of active cortical GABAergic synapses. J Neurosci 28:13125-13131.
39. Mielke JG, Wang YT (2005) Insulin exerts neuroprotection by counteracting the decrease in cell-surface GABA receptors following oxygen-glucose deprivation in cultured cortical neurons. J Neurochem 92:103-113.
40. Morrell CN, Matsushita K, Lowenstein CJ (2005) A novel inhibitor of N-ethylmaleimide-sensitive factor decreases leukocyte trafficking and peritonitis. J Pharmacol Exp Ther 314:155-161.
41. Muir J, Arancibia-Carcamo IL, MacAskill AF, Smith KR, Griffin LD, Kittler JT (2010) NMDA receptors regulate GABAA receptor lateral mobility and clustering at inhibitory synapses through serine 327 on the gamma2 subunit. Proc Natl Acad Sci U S A 107:16679-16684.
42. Nabi IR, Le PU (2003) Caveolae/raft-dependent endocytosis. J Cell Biol 161:673-77.
43. Naylor DE, Liu H, Wasterlain CG (2005) Trafficking of GABAA receptors, loss of inhibition, and a mechanism for pharmacoresistance in status epilepticus. J Neurosci 25:7724-7733.
44. Owen DJ, Evans PR (1998) A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 282:1327-1332.
45. Petrini EM, Lu J, Cognet L, Lounis B, Ehlers MD, Choquet D (2009) Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron 63:92-105.
46. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16:1197-1207.
47. Schwartz-Bloom RD, Sah R (2001) gamma-Aminobutyric acid(A) neurotransmission and cerebral ischemia. J Neurochem 77:353-371.
48. Scott DB, Michailidis I, Mu Y, Logothetis D, Ehlers MD (2004) Endocytosis and degradative sorting of NMDA receptors by conserved membraneproximal signals. J Neurosci 24:7096-7109.
49. Smith KR, Kittler JT (2010) The cell biology of synaptic inhibition in health and disease. Curr Opin Neurobiol 20:550-556.
50. Smith KR, McAinsh K, Chen G, Arancibia-Carcamo IL, Haucke V, Yan Z, Moss SJ, Kittler JT (2008) Regulation of inhibitory synaptic transmission by a conserved atypical interaction of GABA(A) receptor beta- and gamma-subunits with the clathrin AP2 adaptor. Neuropharmacology 55:844-850.
51. Smith KR, Oliver PL, Lumb MJ, Arancibia-Carcamo IL, Revilla-Sanchez R, Brandon NJ, Moss SJ, Kittler JT (2010) Identification and characterization of a Maf1/Macoco protein complex that interacts with GABA(A) receptors in neurons. Mol Cell Neurosci 44:330-341.
52. Tan HO, Reid CA, Single FN, Davies PJ, Chiu C, Murphy S, Clarke AL, Dibbens L, Krestel H, Mulley JC, Jones MV, Seeburg PH, Sakmann B, Berkovic SF, Sprengel R, Petrou S (2007) Reduced cortical inhibition in a mouse model of familial childhood absence epilepsy. Proc Natl Acad Sci U S A 104:17536-17541.
53. Terunuma M, Xu J, Vithlani M, Sieghart W, Kittler J, Pangalos M, Haydon PG, Coulter DA, Moss SJ (2008) Deficits in phosphorylation of GABAA receptors by intimately associated protein kinase C activity underlie compromised synaptic inhibition during status epilepticus. J Neurosci 28: 376-384.
54. Thévenaz P, Ruttimann UE, Unser M (1998) A pyramid approach to subpixel registration based on intensity. IEEE Trans Image Process 7:27-41.
55. Tretter V, Revilla-Sanchez R, Houston C, Terunuma M, Havekes R, Florian C, Jurd R, Vithlani M, Michels G, Couve A, Sieghart W, Brandon N, Abel T, Smart TG, Moss SJ (2009) Deficits in spatial memory correlate with modified {gamma}-aminobutyric acid type A receptor tyrosine phosphorylation in the hippocampus. Proc Natl Acad Sci U S A 106: 20039-20044.
56. Triller A, Choquet D (2008) New concepts in synaptic biology derived from single-molecule imaging. Neuron 59:359-374.
57. Twelvetrees AE, Yuen EY, Arancibia-Carcamo IL, MacAskill AF, Rostaing P, Lumb MJ, Humbert S, Triller A, Saudou F, Yan Z, Kittler JT (2010) Delivery of GABA(A)Rs to synapses is mediated by HAP1-KIF5 and disrupted by mutant huntingtin. Neuron 65:53- 65.
58. Vonderheit A, Helenius A (2005) Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol 3:e233.
59. Wisden W, Laurie DJ, Monyer H, Seeburg PH (1992) The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J Neurosci 12:1040-1062.
60. Zhan RZ, Nadler JV, Schwartz-Bloom RD (2006) Depressed responses to applied and synaptically-released GABA in CA1 pyramidal cells, but not in CA1 interneurons, after transient forebrain ischemia. J Cereb Blood Flow Metab 26:112-124.