Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors

Journal of Neuroscience

Volumn 25, Issue 45, 2005, Pages 10469-10478

  Jacob, Tija C ^a   Bogdanov, Yury D ^b   Magnus, Christopher ^b   Saliba, Richard S ^b   Kittler, Josef T ^a   Haydon, Philip G ^a   Moss, Stephen J ^a,b,c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c 145 Johnson Pavilion ^*  (United States)

Author keywords

GABA; GABA synaptogenesis; GABAA receptor; GABAA receptor trafficking; Gabaergic modulation; Imaging

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; GEPHYRIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BLEACHING; BRAIN NERVE CELL; CELL SURFACE; CONTROLLED STUDY; EMBRYO; FLUORESCENCE; GABAERGIC TRANSMISSION; HIPPOCAMPUS; HUMAN; HUMAN CELL; NERVE ENDING; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR INTRINSIC ACTIVITY; RNA INTERFERENCE; SYNAPSE; SYNAPTIC INHIBITION; SYNAPTOGENESIS;

ANIMALS; BIOTINYLATION; BLOTTING, WESTERN; CARRIER PROTEINS; CLONING, MOLECULAR; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC STIMULATION; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; NEURAL INHIBITION; NEURONS; NONLINEAR DYNAMICS; PATCH-CLAMP TECHNIQUES; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PHOTOBLEACHING; PRESYNAPTIC TERMINALS; PROTEIN SUBUNITS; PYRIDINIUM COMPOUNDS; QUATERNARY AMMONIUM COMPOUNDS; RATS; RECEPTORS, AMPA; RECEPTORS, GABA-A; RNA INTERFERENCE; SYNAPSES; TRANSFECTION; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 27744463295     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2267-05.2005     Document Type: Article

References (42)

1. Amato A, Connolly CN, Moss SJ, Smart TG (1999) Modulation of neuronal and recombinant GABAA receptors by redox reagents. J Physiol (Lond) 517:35-50.
2. Ashby MC, Ibaraki K, Henley JM (2004a) It's green outside: tracking cell surface proteins with pH-sensitive GFP. Trends Neurosci 27:257-261.
3. Ashby MC, De La Rue SA, Ralph GS, Uney J, Collingridge GL, Henley JM (2004b) Removal of AMPA receptors from synapses is preceded by transient endocytosis of extrasynaptic AMPARs. J Neurosci 24:5172-5176.
4. Banker G, Goslin K (1998) Culturing nerve cells, Ed 2. Cambridge, MA: MIT.
5. A receptor cell surface number and subunit stability are regulated by the ubiquitin-like protein Plic-1. Nat Neurosci 4:908-916.
6. Brunig I, Scotti E, Sidler C, Fritschy JM (2002) Intact sorting, targeting, and clustering of gamma-aminobutyric acid A receptor subtypes in hippocampal neurons in vitro. J Comp Neurol 443:43-55.
7. Crestani F, Lorez M, Baer K, Essrich C, Benke D, Laurent JP, Belzung C, Fritschy JM, Luscher B, Mohler H (1999) Decreased GABAA-receptor clustering results in enhanced anxiety and a bias for threat cues. Nat Neurosci 2:833-839.
8. Dahan M, Levi S, Luccardini C, Rostaing P, Riveau B, Triller A (2003) Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science 302:442-445.
9. Danglot L, Triller A, Bessis A (2003) Association of gephyrin with synaptic and extrasynaptic GABAA receptors varies during development in cultured hippocampal neurons. Mol Cell Neurosci 23:264-278.
10. Editorial (2003) Whither RNAi? Nat Cell Biol 5:489-490.
11. Essrich C, Lorez M, Benson JA, Fritschy JM, Luscher B (1998) Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nat Neurosci 1:563-571.
12. Feng G, Tintrup H, Kirsch J, Nichol MC, Kuhse J, Betz H, Sanes JR (1998) Dual requirement for gephyrin in glycine receptor clustering and molybdoenzyme activity. Science 282:1321-1324.
13. Groc L, Heine M, Cognet L, Brickley K, Stephenson FA, Lounis B, Choquet D (2004) Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors. Nat Neurosci 7:695-696.
14. Hannon GJ, Rossi JJ (2004) Unlocking the potential of the human genome with RNA interference. Nature 431:371-378.
15. A receptor phosphorylation, activity, and cell-surface stability. J Neurosci 24:522-530.
16. Kittler JT, Moss SJ (2003) Modulation of GABAA receptor activity by phosphorylation and receptor trafficking: implications for the efficacy of synaptic inhibition. Curr Opin Neurobiol 13:341-347.
17. Kittler JT, Wang J, Connolly CN, Vicini S, Smart TG, Moss SJ (2000a) Analysis of GABAA receptor assembly in mammalian cell lines and hippocampal neurons using gamma 2 subunit green fluorescent protein chimeras. Mol Cell Neurosci 16:440-452.
18. Kittler JT, Delmas P, Jovanovic JN, Brown DA, Smart TG, Moss SJ (2000b) 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.
19. Kittler JT, Thomas P, Tretter V, Bogdanov YD, Haucke V, Smart TG, Moss SJ (2004) Huntingtin-assodated protein l regulates inhibitory synaptic transmission by modulating γ-aminobutyric acid type A receptor membrane trafficking. Proc Natl Acad Sci USA 101:12736-12741.
20. Kneussel M, Betz H (2000a) Receptors, gephyrin and gephyrin-associated proteins: novel insights into the assembly of inhibitory postsynaptic membrane specializations. J Physiol (Lond) 525:1-9.
21. Kneussel M, Betz H (2000b) Clustering of inhibitory neurotransmitter receptors at developing postsynaptic sites: the membrane activation model. Trends Neurosci 23:429-435.
22. A receptor clustering in gephyrin-deficient mice. J Neurosci 19:9289-9297.
23. A receptor subtypes. Mol Cell Neurosci 17:973-982.
24. Lagnado L, Gomis A, Job C (1996) Continuous vesicle cycling in the synaptic terminal of retinal bipolar cells. Neuron 17:957-967.
25. Levi S, Logan SM, Tovar KR, Craig AM (2004) Gephyrin is critical for glycine receptor clustering but not for the formation of functional GABAergic synapses in hippocampal neurons. J Neurosci 24:207-217.
26. Mammen AL, Huganir RL, O'Brien RJ (1997) Redistribution and stabilization of cell surface glutamate receptors during synapse formation. J Neurosci 17:7351-7358.
27. Meier J, Vannier C, Serge A, Triller A, Choquet D (2001) Fast and reversible trapping of surface glycine receptors by gephyrin. Nat Neurosci 4:253-260.
28. Miesenbock G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192-195.
29. Mohrmann R, Lessmann V, Gottmann K (2003) Developmental maturation of synaptic vesicle cycling as a distinctive feature of central glutamatergic synapses. Neuroscience 117:7-18.
30. Moss SJ, Smart TG (2001) Constructing inhibitory synapses. Nat Rev Neurosci 2:240-250.
31. Nuutila J, Lilius EM (2005) Flow cytometric quantitative determination of ingestion by phagocytes needs the distinguishing of overlapping populations of binding and ingesting cells. Cytometry A 65A:93-102.
32. Rathenberg J, Kittler JT, Moss SJ (2004) Palmitoylation regulates the clustering and cell surface stability of GABAA receptors. Mol Cell Neurosci 26:251-257.
33. Schrader N, Kim EY, Winking J, Paulukat J, Schindelin H, Schwarz G (2004) Biochemical characterization of the high affinity binding between the glycine receptor and gephyrin. J Biol Chem 279:18733-18741.
34. Scotti AL, Reuter H (2001) Synaptic and extrasynaptic gamma-aminobutyric acid type A receptor clusters in rat hippocampal cultures during development. Proc Natl Acad Sci USA 98:3489-3494.
35. Sieghart W, Sperk G (2002) Subunit composition, distribution and function of GABAA receptor subtypes. Curr Top Med Chem 2:795-816.
36. Sola M, Kneussel M, Heck IS, Betz H, Weissenhorn W (2001) X-ray crystal structure of the trimeric N-terminal domain of gephyrin. J Biol Chem 276:25294-25301.
37. Sola M, Bavro VN, Timmins J, Franz T, Ricard-Blum S, Schoehn G, Ruigrok RW, Paarmann I, Saiyed T, O'Sullivan GA, Schmitt B, Betz H, Weissenhorn W (2004) Structural basis of dynamic glycine receptor clustering by gephyrin. EMBO J 23:2510-2519.
38. A receptors at inhibitory synapses. Nat Neurosci 8:889-897.
39. Triller A, Choquet D (2003) Synaptic structure and diffusion dynamics of synaptic receptors. Biol Cell 95:465-476.
40. Triller A, Choquet D (2005) Surface trafficking of receptors between synaptic and extrasynaptic membranes: and yet they do move! Trends Neurosci 28:133-139.
41. A receptors and the cytoskeleton. Nature 397:69-72.
42. Xiang S, Nichols J, Rajagopalan KV, Schindelin H (2001) The crystal structure of Escherichia coli MoeA and its relationship to the multifunctional protein gephyrin. Structure (Camb) 9:299-310.