Proteomic characterization of inhibitory synapses using a novel phluorin-tagged γ-aminobutyric acid receptor, type a (gabaa ), α2 subunit knock-in mouse

Journal of Biological Chemistry

Volumn 291, Issue 23, 2016, Pages 12394-12407

  Nakamura, Yasuko ^a   Morrow, Danielle H ^a   Modgil, Amit ^a   Huyghe, Deborah ^a   Deeb, Tarek Z ^a   Lumb, Michael J ^b   Davies, Paul A ^a   Moss, Stephen J ^a,b  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ANTIGEN-ANTIBODY REACTIONS; BINS; ENZYME ACTIVITY; MAMMALS; MASS SPECTROMETRY;

DOMAIN-CONTAINING PROTEINS; G PROTEIN COUPLED RECEPTORS; GAMMA-AMINOBUTYRIC ACIDS; GREEN FLUORESCENT PROTEIN; METABOTROPIC GLUTAMATE RECEPTORS; POSTSYNAPTIC DENSITIES; PROTEIN PHOSPHORYLATION; RECEPTOR-ASSOCIATED PROTEINS;

PROTEINS;

4 AMINOBUTYRIC ACID A RECEPTOR; COLLYBISTIN; GEPHYRIN; MEMBRANE PROTEIN; PROTEOME; UNCLASSIFIED DRUG; GREEN FLUORESCENT PROTEIN; PHLUORIN;

ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BRAIN NERVE CELL; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEOMICS; SYNAPSE; SYNAPTIC TRANSMISSION; 129 MOUSE; ANIMAL; C57BL MOUSE; ELECTROPHYSIOLOGY; GENETICS; HEK293 CELL LINE; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIAL; MASS SPECTROMETRY; METABOLISM; NERVE CELL; PH; PHYSIOLOGY; PROCEDURES; TRANSGENIC MOUSE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; ELECTROPHYSIOLOGICAL PHENOMENA; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HIPPOCAMPUS; HUMANS; HYDROGEN-ION CONCENTRATION; INHIBITORY POSTSYNAPTIC POTENTIALS; MASS SPECTROMETRY; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; PROTEOME; PROTEOMICS; RECEPTORS, GABA-A; SYNAPSES;

EID: 84974603488     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.724443     Document Type: Article

References (55)

1. Jacob, T. C., Moss, S. J., and Jurd, R. (2008) GABA(A) receptor trafficking and its role in the dynamic modulation of neuronal inhibition. Nat. Rev. Neurosci. 9, 331-343
2. Luscher, B., Fuchs, T., and Kilpatrick, C. L. (2011) GABAA receptor trafficking-mediated plasticity of inhibitory synapses. Neuron 70, 385-409
3. Sieghart, W. (2015) Allosteric modulation of GABAA receptors via multiple drug-binding sites. Adv. Pharmacol. 72, 53-96
4. Rudolph, U., and Möhler, H. (2014) GABAA receptor subtypes: therapeutic potential in Down syndrome, affective disorders, schizophrenia, and autism. Annu. Rev. Pharmacol. Toxicol. 54, 483-507
5. Olsen, R. W., and Sieghart, W. (2008) International Union of Pharmacology. LXX. Subtypes of γ-aminobutyric acid(A) receptors: classification on the basis of subunit composition, pharmacology, and function. Update. Pharmacol. Rev. 60, 243-260
6. Patel, B., Mortensen, M., and Smart, T. G. (2014) Stoichiometry of δ subunit containing GABA(A) receptors. Br. J. Pharmacol. 171, 985-994
7. Verdoorn, T. A., Draguhn, A., Ymer, S., Seeburg, P. H., and Sakmann, B. (1990) Functional properties of recombinant rat GABAA receptors depend upon subunit composition. Neuron 4, 919-928
8. Rudolph, U., and Knoflach, F. (2011) Beyond classical benzodiazepines: novel therapeutic potential of GABAA receptor subtypes. Nat. Rev. Drug Discov. 10, 685-697
9. Feng, W., and Zhang, M. (2009) Organization and dynamics of PDZdomain-related supramodules in the postsynaptic density. Nat. Rev. Neurosci. 10, 87-99
10. Hörtnagl, H., Tasan, R. O., Wieselthaler, A., Kirchmair, E., Sieghart, W., and Sperk, G. (2013) Patterns of mRNA and protein expression for 12 GABAA receptor subunits in the mouse brain. Neuroscience 236, 345-372
11. Brandon, N. J., Jovanovic, J. N., Colledge, M., Kittler, J. T., Brandon, J. M., Scott, J. D., and Moss, S. J. (2003) A-kinase anchoring protein 79/150 facilitates the phosphorylation of GABA(A) receptors by cAMP-dependent protein kinase via selective interaction with receptor β subunits. Mol. Cell Neurosci. 22, 87-97
12. Tretter, V., Jacob, T. C., Mukherjee, J., Fritschy, J. M., Pangalos, M. N., and Moss, S. J. (2008) The clustering of GABA(A) receptor subtypes at inhibitory synapses is facilitated via the direct binding of receptor α2 subunits to gephyrin. J. Neurosci. 28, 1356-1365
13. Shamah, S. M., Lin, M. Z., Goldberg, J. L., Estrach, S., Sahin, M., Hu, L., Bazalakova, M., Neve, R. L., Corfas, G., Debant, A., and Greenberg, M. E. (2001) EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 105, 233-244
14. Jacob, T. C., Michels, G., Silayeva, L., Haydon, J., Succol, F., and Moss, S. J. (2012) Benzodiazepine treatment induces subtype-specific changes in GABA(A) receptor trafficking and decreases synaptic inhibition. Proc. Natl. Acad. Sci. U.S.A. 109, 18595-18600
15. Abramian, A. M., Comenencia-Ortiz, E., Vithlani, M., Tretter, E. V., Sieghart, W., Davies, P. A., and Moss, S. J. (2010) Protein kinase C phosphorylation regulates membrane insertion of GABAA receptor subtypes that mediate tonic inhibition. J. Biol. Chem. 285, 41795-41805
16. Bolte, S., and Cordelières, F. P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213-232
17. Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675
18. Candiano, G., Bruschi, M., Musante, L., Santucci, L., Ghiggeri, G. M., Carnemolla, B., Orecchia, P., Zardi, L., and Righetti, P. G. (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25, 1327-1333
19. Mellacheruvu, D., Wright, Z., Couzens, A. L., Lambert, J. P., St-Denis, N. A., Li, T., Miteva, Y. V., Hauri, S., Sardiu, M. E., Low, T. Y., Halim, V. A., Bagshaw, R. D., Hubner, N. C., Al-Hakim, A., Bouchard, A., et al. (2013) The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat. Methods 10, 730-736
20. Jacob, T. C., Bogdanov, Y. D., Magnus, C., Saliba, R. S., Kittler, J. T., Haydon, P. G., and Moss, S. J. (2005) Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors. J. Neurosci. 25, 10469-10478
21. Connolly, C. N., Wooltorton, J. R., Smart, T. G., and Moss, S. J. (1996) Subcellular localization of γ-aminobutyric acid type A receptors is determined by receptor γ subunits. Proc. Natl. Acad. Sci. U.S.A. 93, 9899-9904
22. Saiepour, L., Fuchs, C., Patrizi, A., Sassoè-Pognetto, M., Harvey, R. J., and Harvey, K. (2010) Complex role of collybistin and gephyrin in GABAA receptor clustering. J. Biol. Chem. 285, 29623-29631
23. Essrich, C., Lorez, M., Benson, J. A., Fritschy, J. M., and Lüscher, B. (1998) Postsynaptic clustering of major GABAA receptor subtypes requires the γ2 subunit and gephyrin. Nat. Neurosci. 1, 563-571
24. Kneussel, M., Brandstätter, J. H., Laube, B., Stahl, S., Müller, U., and Betz, H. (1999) Loss of postsynaptic GABA(A) receptor clustering in gephyrindeficient mice. J. Neurosci. 19, 9289-9297
25. Connolly, C. N., Krishek, B. J., McDonald, B. J., Smart, T. G., and Moss, S. J. (1996) Assembly and cell surface expression of heteromeric and homomeric γ-aminobutyric acid type A receptors. J. Biol. Chem. 271, 89-96
26. Mukherjee, J., Kretschmannova, K., Gouzer, G., Maric, H. M., Ramsden, S., Tretter, V., Harvey, K., Davies, P. A., Triller, A., Schindelin, H., and Moss, S. J. (2011) The residence time of GABA(A)Rs at inhibitory synapses is determined by direct binding of the receptor α1 subunit to gephyrin. J. Neurosci. 31, 14677-14687
27. Hoon, M., Soykan, T., Falkenburger, B., Hammer, M., Patrizi, A., Schmidt, K. F., Sassoè-Pognetto, M., Löwel, S., Moser, T., Taschenberger, H., Brose, N., and Varoqueaux, F. (2011) Neuroligin-4 is localized to glycinergic postsynapses and regulates inhibition in the retina. Proc. Natl. Acad. Sci. U.S.A. 108, 3053-3058
28. Poulopoulos, A., Aramuni, G., Meyer, G., Soykan, T., Hoon, M., Papadopoulos, T., Zhang, M., Paarmann, I., Fuchs, C., Harvey, K., Jedlicka, P., Schwarzacher, S. W., Betz, H., Harvey, R. J., Brose, N., et al. (2009) Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 63, 628-642
29. Meyer, G., Kirsch, J., Betz, H., and Langosch, D. (1995) Identification of a gephyrin binding motif on the glycine receptor β subunit. Neuron 15, 563-572
30. McDonald, B. J., and Moss, S. J. (1997) Conserved phosphorylation of the intracellular domains of GABA(A) receptor β2 and β3 subunits by cAMPdependent protein kinase, cGMP-dependent protein kinase protein kinase C and Ca2+ /calmodulin type II-dependent protein kinase. Neuropharmacology 36, 1377-1385
31. Balasubramanian, S., Teissére, J. A., Raju, D. V., and Hall, R. A. (2004) Hetero-oligomerization between GABAA and GABAB receptors regulates GABAB receptor trafficking. J. Biol. Chem. 279, 18840-18850
32. Sheng, M., and Kim, E. (2011) The postsynaptic organization of synapses. Cold Spring Harb. Perspect. Biol. 3, a005678
33. Schwenk, J., Metz, M., Zolles, G., Turecek, R., Fritzius, T., Bildl, W., Tarusawa, E., Kulik, A., Unger, A., Ivankova, K., Seddik, R., Tiao, J. Y., Rajalu, M., Trojanova, J., Rohde, V., et al. (2010) Native GABA(B) receptors are heteromultimers with a family of auxiliary subunits. Nature 465, 231-235
34. Petroski, M. D., and Deshaies, R. J. (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 6, 9-20
35. Stuppia, G., Rizzo, F., Riboldi, G., Del Bo, R., Nizzardo, M., Simone, C., Comi, G. P., Bresolin, N., and Corti, S. (2015) MFN2-related neuropathies: Clinical features, molecular pathogenesis and therapeutic perspectives. J. Neurol. Sci. 356, 7-18
36. Stenmark, H. (2009) Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10, 513-525
37. Smith, K. R., Muir, J., Rao, Y., Browarski, M., Gruenig, M. C., Sheehan, D. F., Haucke, V., and Kittler, J. T. (2012) Stabilization of GABA(A) receptors at endocytic zones is mediated by an AP2 binding motif within the GABA(A) receptor β3 subunit. J. Neurosci. 32, 2485-2498
38. Wells, C. M., and Jones, G. E. (2010) The emerging importance of group II PAKs. Biochem. J. 425, 465- 473
39. Shi, L., Fu, A. K., and Ip, N. Y. (2010) Multiple roles of the Rho GEF ephexin1 in synapse remodeling. Commun. Integr. Biol. 3, 622-624
40. Besheer, J., and Hodge, C. W. (2005) Pharmacological and anatomical evidence for an interaction between mGluR5- and GABA(A) α1-containing receptors in the discriminative stimulus effects of ethanol. Neuropsychopharmacology 30, 747-757
41. Papadopoulos, T., Korte, M., Eulenburg, V., Kubota, H., Retiounskaia, M., Harvey, R. J., Harvey, K., O'Sullivan, G. A., Laube, B., Hülsmann, S., Geiger, J. R., and Betz, H. (2007) Impaired GABAergic transmission and altered hippocampal synaptic plasticity in collybistin-deficient mice. EMBO J. 26, 3888-3899
42. del Río, J. C., Araujo, F., Ramos, B., Ruano, D., and Vitorica, J. (2001) Prevalence between different α subunits performing the benzodiazepine binding sites in native heterologous GABA(A) receptors containing the α2 subunit. J. Neurochem. 79, 183-191
43. Benke, D., Fakitsas, P., Roggenmoser, C., Michel, C., Rudolph, U., and Mohler, H. (2004) Analysis of the presence and abundance of GABAA receptors containing two different types of α subunits in murine brain using point-mutated α subunits. J. Biol. Chem. 279, 43654-43660
44. Benke, D., Michel, C., and Mohler, H. (1997) GABA(A) receptors containing the α4-subunit: prevalence, distribution, pharmacology, and subunit architecture in situ. J. Neurochem. 69, 806- 814
45. Duggan, M. J., Pollard, S., and Stephenson, F. A. (1991) Immunoaffinity purification of GABAA receptor α-subunit iso-oligomers. Demonstration of receptor populations containing α1 α2, α1 α3, and α2 α3 subunit pairs. J. Biol. Chem. 266, 24778-24784
46. Pollard, S., Thompson, C. L., and Stephenson, F. A. (1995) Quantitative characterization of α6 and α1 α6 subunit-containing native γ-aminobutyric acid A receptors of adult rat cerebellum demonstrates two α subunits per receptor oligomer. J. Biol. Chem. 270, 21285-21290
47. Ju, Y. H., Guzzo, A., Chiu, M. W., Taylor, P., Moran, M. F., Gurd, J. W., MacDonald, J. F., and Orser, B. A. (2009) Distinct properties of murine α5 γ-aminobutyric acid type a receptors revealed by biochemical fractionation and mass spectroscopy. J. Neurosci. Res. 87, 1737-1747
48. Heller, E. A., Zhang, W., Selimi, F., Earnheart, J. C., Œlimak, M. A., Santos-Torres, J., Ibañez-Tallon, I., Aoki, C., Chait, B. T., and Heintz, N. (2012) The biochemical anatomy of cortical inhibitory synapses. PLoS ONE 7, e39572
49. Rudolph, U., and Möhler, H. (2004) Analysis of GABAA receptor function and dissection of the pharmacology of benzodiazepines and general anesthetics through mouse genetics. Annu. Rev. Pharmacol. Toxicol. 44, 475-498
50. Gorrie, G. H., Vallis, Y., Stephenson, A., Whitfield, J., Browning, B., Smart, T. G., and Moss, S. J. (1997) Assembly of GABAA receptors composed of α1 and β2 subunits in both cultured neurons and fibroblasts. J. Neurosci. 17, 6587- 6596
51. Shi, L., Butt, B., Ip, F. C., Dai, Y., Jiang, L., Yung, W. H., Greenberg, M. E., Fu, A. K., and Ip, N. Y. (2010) Ephexin1 is required for structural maturation and neurotransmission at the neuromuscular junction. Neuron 65, 204-216
52. Tada, T., and Sheng, M. (2006) Molecular mechanisms of dendritic spine morphogenesis. Curr. Opin. Neurobiol. 16, 95-101
53. Smith,K. R. Davenport,E. C. Wei,J. Li,X. Pathania,M. Vaccaro,V. Yan,Z. Kittler,J. T.2014GIT1 and βPIX are essential for GABA(A) receptor synaptic stability and inhibitory neurotransmissionCell Rep9298-310
54. Gingras, A. C., Gstaiger, M., Raught, B., and Aebersold, R. (2007) Analysis of protein complexes using mass spectrometry. Nat. Rev. Mol. Cell Biol. 8, 645-654
55. Charych, E. I., Liu, F., Moss, S. J., and Brandon, N. J. (2009) GABA(A) receptors and their associated proteins: implications in the etiology and treatment of schizophrenia and related disorders. Neuropharmacology 57, 481-495