GABA potency at GABA A receptors found in synaptic and extrasynaptic zones

Frontiers in Cellular Neuroscience

Volumn , Issue JANUARY, 2012, Pages

  Mortensen, Martin ^a   Patel, Bijal ^a   Smart, Trevor G ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

GABA; GABA A; Neurons; Receptor; Synaptic and extra synaptic receptors

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA2; 4 AMINOBUTYRIC ACID A RECEPTOR BETA3; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA2;

BINDING AFFINITY; GABAERGIC TRANSMISSION; HUMAN; NERVE CELL EXCITABILITY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR UPREGULATION; REVIEW; SYNAPTIC TRANSMISSION;

EID: 84857010966     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2012.00001     Document Type: Review

References (71)

1. Angelotti, T. P., and MacDonald, R. L. (1993). Assembly of GABAa receptor infunits: c1 (31 and c1 (31 y2S infunits produce unique ion channels with dissimilar single-channel properties. J. Neurosci. 13, 1429-1440.
2. Bedford, F. K., Kittler, J. T., Muller, E., Thomas, P., Uren, J. M., Merlo, D., Wisden, W., Triller, A., Smart, T. G., and Moss, S. J. (2001). GABAa receptor cell surface number and infunit stability are regulated by the ubiquitin-like protein Plic-1. Nat. Neurosci. 4, 908-916.
3. Belelli, D., Harrison, N. L., Maguire, J., MacDonald, R. L., Walker, M. C., and Cope, D. W. (2009). Extrasynaptic GABAa receptors: form, pharmacology, and function. J. Neurosci. 29, 12757-12763.
4. Bencsits, E., Ebert, V., Tretter, V., and Sieghart, W. (1999). A significant part of native y-aminobutyric acid A receptors containing a4 infunits do not contain y or § infunits. J. Biol Chem. 274,19613-19616.
5. Bogdanov, Y., Michels, G., Armstrong-Gold, C., Haydon, P. G., Lindstrom, J., Pangalos, M., and Moss, S. J. (2006). Synaptic GABAA receptors are directly recruited from their extrasynaptic counterparts. EMBO J. 25, 4381-4389.
6. Brickley, S. G., Cull-Candy, S. G., and Farrant, M. (1999). Single-channel properties of synaptic and extrasynaptic GABAA receptors suggest differential targeting of receptor inftypes. J. Neurosci. 19, 2960-2973.
7. araiscos, V. B., Elliott, E. M., You, T., Cheng, V. Y., Belelli, D., Newell, J. G., Jackson, M. F., Lambert, J. J., Rosahl, T. W., Wafford, K. A., MacDonald, J. F., and Orser, B. A. (2004). Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by a5 infunit-containing g-aminobutyric acid type A receptors. Proc. Natl. Acad. Sci. U.S.A. 101, 3662-3667.
8. bert, B., Wafford, K. A., Whiting, P. J., Krogsgaard-Larsen, P., and Kemp, J. A. (1994). Molecular pharmacology of y-aminobutyric acid type A receptor agonists and partial agonists in oocytes injected with different a, 3, and y receptor infunit combinations. Mol. Pharmacol. 46, 957-963.
9. Farrant, M., and Nusser, Z. (2005). Variations on an inhibitory theme: phasic and tonic activation of GABAa receptors. Nat. Rev. Neurosci. 6, 215-229.
10. Farrar, S. J., Whiting, P. J., Bonnert, T. P., and McKernan, R. M. (1999). Stoichiometry of a ligand-gated ion channel determined by fluorescence energy transfer. J. Biol. Chem. 274, 10100-10104.
11. Fritschy, J. M., and Brunig, I. (2003). Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications. Pharmacol. Ther. 98, 299-323.
12. Fritschy, J.-M., and Mohler, H. (1995). GABAa receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major infunits. J. Comp. Neurol. 359, 154-194.
13. Glykys, J., Mann, E. O., and Mody, I. (2008). Which GABAa receptor inf-units are necessary for tonic inhibition in the hippocampus? J. Neurosci. 28, 1421-1426.
14. Glykys, J., Peng, Z., Chandra, D., Homanics, G. E., Houser, C. R., and Mody, I. (2007). A new naturally occurring GABAa receptor infunit partnership with high sensitivity to ethanol. Nat. Neurosci. 10, 40-48.
15. Hadingham, K. L., Wingrove, P. B., Waf-ford, K. A., Bain, C., Kemp, J. A., Palmer, K. J., Wilson, A. W., Wilcox, A. S., Sikela, J. M., Ragan, C. I., and Whiting, P. J. (1993). Role of the? Sinfunit in determining the pharmacology of human y-aminobutyric acid type A receptors. Mol. Pharmacol. 44, 1211-1218.
16. Herd, M. B., Haythornthwaite, A. R., Rosahl, T. W, Wafford, K. A., Homanics, G. E., Lambert, J. J., and Belelli, D. (2008). The expression of GABAa b infunit isoforms in synaptic and extrasynaptic receptor populations of mouse dentate gyrus granule cells. J. Physiol. (Lond) 586, 989-1004.
17. Hutcheon, B., Fritschy, J. M., and Poul-ter, M. O. (2004). Organization of GABA receptor a-infunit clustering in the developing rat neocortex and hippocampus. Eur. J. Neurosci. 19, 2475-2487.
18. Jacob, T. C., Moss, S. J., and Jurd, R. (2008). GABAa receptor trafficking and its role in the dynamic modulation of neuronal inhibition. Nat. Rev. Neurosci. 9, 331-343.
19. echlinger, M., Pelz, R., Tretter, V., Klausberger, T., and Sieghart, W. (1998). Infunit composition and quantitative importance of hetero-oligomeric receptors: GABAa receptors containing a6 infunits. J. Neurosci. 18,2449-2457.
20. Jia, F., Pignataro, L., Schofield, C. M., Yue, M., Harrison, N. L., and Goldstein, P. A. (2005). An extrasynaptic GABAa receptor mediates tonic inhibition in thalamic VB neurons. J. Neurophysiol. 94, 4491-4501.
21. Jones, A., Korpi, E. R., McKernan, R. M., Pelz, R., Nusser, Z., Makela, R., Mellor, J. R., Pollard, S., Bahn, S., Stephenson, F. A., Randall, A. D., Sieghart, W, Somogyi, P., Smith, A. J., and Wisden, W (1997). Ligand-gated ion channel infunit partnerships: GABAa receptor a6 inf-unit gene inactivation inhibits delta infunit expression. J. Neurosci. 17, 1350-1362.
22. Kasugai, Y., Swinny, J. D., Roberts, J. D., Dalezios, Y, Fukazawa, Y., Sieghart, W., Shigemoto, R., and Somogyi, P. (2010). Quantitative localisation of synaptic and extrasynaptic GABAa receptor infunits on hippocampal pyramidal cells by freeze-fracture replica immunolabelling. Eur. J. Neurosci. 32,1868-1888.
23. Keller, C. A., Yuan, X., Panzanelli, P., Martin, M. L., Alldred, M., Sassoe-Pognetto, M., and Luscher, B. (2004). The y2 infunit of GABAa receptors is a infstrate for palmitoy-lation by GODZ. J. Neurosci. 24, 5881-5891.
24. Khan, Z. U., Gutierrez, A., and De Blas, A. L. (1994). The infunit composition of a GABAA/benzodiazepine receptor from rat cerebellum. J. Neu-rochem. 63, 371-374.
25. Kittler, J. T., Thomas, P., Tretter, V., Bogdanov, Y D., Haucke, V., Smart, T. G., and Moss, S. J. (2004). Huntingtin-associated protein 1 regulates inhibitory synaptic transmission by modulating y-aminobutyric acid type A receptor membrane trafficking. Proc. Natl. Acad. Sci. U.S.A. 101, 12736-12741.
26. Klausberger, T., Fuchs, K., Mayer, B., Ehya, N., and Sieghart, W. (2000). GABAa receptor assembly. Identification and structure of y2 sequences forming the inter-infunit contacts with c1 and? Sinfunits. J. Biol. Chem. 275, 8921-8928.
27. Klausberger, T., Sarto, I., Ehya, N., Fuchs, K., Furtmuller, R., Mayer, B., Huck, S., and Sieghart, W (2001). Alternate use of distinct interinfunit contacts controls GABAA receptor assembl and stoichiometry. J. Neurosci. 21 9124-9133.
28. Kneussel, M., Haverkamp, S. Fuhrmann, J. C., Wang, H., Wassle H., Olsen, R. W., and Betz, H. (2000) The gamma-aminobutyric acid typ A receptor (GABAAR)-associate protein GABARAP interacts wit gephyrin but is not involved i receptor anchoring at the synapse Proc. Natl. Acad. Sci. U.S.A. 97 8594-8599.
29. Korpi, E. R., Grunder, G., and Lud dens, H. (2002). Drug interaction at GABAA receptors. Prog. Neurobiol 67, 113-159.
30. Krishek, B. J., Xie, X., Blackstone, C. Huganir, R. L., Moss, S. J., an Smart, T. G. (1994). Regulation o GABAA receptor function by protei kinase C phosphorylation. Neuro 12, 1081-1095.
31. Laurie, D. J., Wisden, W., and Seeburg P. H. (1992). The distribution o thirteen GABAA receptor infuni mRNAs in the rat brain. III. Embry onic and postnatal development. J Neurosci. 12, 4151-4172.
32. Lee, S., Yoon, B. E., Berglund, K., Oh, S J., Park, H., Shin, H. S., Augustine G. J., and Lee, C. J. (2010). Channel mediated tonic GABA release from glia. Science 330, 790-796.
33. Luscher, B., Fuchs, T., and Kilpatrick, C (2011). GABAA receptor trafficking mediated plasticity of inhibitor synapses. Neuron 70, 385-409.
34. Luscher, B., and Keller, C. A. (2004) Regulation of GABAA recepto trafficking, channel activity, an functional plasticity of inhibitor synapses. Pharmacol. Ther. 102 195-221.
35. McKernan, R. M., and Whiting, P J. (1996). Which GABAA-recepto inftypes really occur in the brain Trends. Neurosci. 19, 139-143.
36. Mehta, A. K., and Ticku, M. K (1999).Anupdate on GABAA recep tors. Brain Res. Brain Res. Rev. 29 196-217.
37. Mellor, J. R., Wisden, W., and Ran dall, A. D. (2000). Somato-synapti variation of GABA(A) receptors i cultured murine cerebellar granul cells: investigation of the role of th alpha6 infunit. Neuropharmacolog 39, 1495-1513.
38. Mortensen, M., and Smart, T. G. (2006) Extrasynaptic αβ infunit GABAA receptors on rat hippocampal pyra midal neurons. J. Physiol. (Lond. 577, 841-856.
39. Mortensen, M., and Smart, T. G. (2007) Single-channel recording of ligand gated ion channels. Nat. Protoc. 2 2826-2841.
40. Mortensen, M., Wafford, K. A., Wingrove, P., and Ebert, B. (2003). Pharmacology of GABAa receptors exhibiting different levels of spontaneous activity. Eur. J. Pharmacol. 476, 17-24.
41. Moss, S. J., and Smart, T. G. (2001). Constructing inhibitory synapses. Nat. Rev. Neurosci. 2, 240-250.
42. Moss, S. J., Smart, T. G., Porter, N. M., Nayeem, N., Devine, J., Stephenson, F. A., MacDonald, R. L., and Barnard, E. A. (1990). Cloned GABA receptors are maintained in a stable cell line: allosteric and channel properties. Eur. J. Pharmacol. 189, 77-88.
43. Mozrzymas, J. W, Zarnowska, E. D., Pytel, M., and Mercik, K. (2003). Modulation of GABAa receptors by hydrogen ions reveals synaptic GABA transient and a crucial role of the desensitization process. J. Neurosci. 23, 7981-7992.
44. 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 GABAARs at inhibitory synapses is determined by direct binding of the receptor c1 infunit to gephyrin. J. Neurosci. 31, 14677-14687.
45. Neelands, T. R., Fisher, J. L., Bianchi, M., and MacDonald, R.L. (1999). Spontaneous and y-aminobutyric acid (GABA)-activated GABAa receptor channels formed by s infunit-containing isoforms. Mol. Pharmacol. 55, 168-178.
46. Olsen, R. W, and Sieghart, W. (2008). International Union of Pharmacology. LXX. Inftypes of gamma-aminobutyric acid(A) receptors: classification on the basis of infunit composition, pharmacology, and function. Pharmacol. Rev. 60, 243-260.
47. Pape, J. R., Bertrand, S. S., Lafon, P., Odessa, M. F., Chaigniau, M., Stiles, J. K., and Garret, M. (2009). Expression of GABAa receptor a3-, 9-, and s-infunit mRNAs during rat CNS development and immunolocaliza-tion of the s infunit in developing postnatal spinal cord. Neuroscience 160, 85-96.
48. Peng, Z., Huang, C. S., Stell, B. M., Mody, I., and Houser, C. R. (2004). Altered expression of the d infunit of the GABAa receptor in a mouse model of temporal lobe epilepsy. J. Neurosci. 24, 8629-8639.
49. Pirker, S., Schwarzer, C, Wieselthaler, A., Sieghart, W., and Sperk, G. (2000). GABAa receptors: immunocytochemical distribution of 13 infunits in the adult rat brain. Neuroscience 101, 815-850.
50. Quirk, K., Gillard, N. P., Ragan, C. I., Whiting, P. J., and McKernan, R. M. (1994). Model of infunit composition of g-aminobutyric acidA receptor inftypes expressed in rat cerebellum with respect to their a and g/d infunits. J. Biol. Chem. 269, 16020-16028.
51. Santhakumar, V., Hanchar, H. J., Wall-ner, M., Olsen, R. W., and Otis, T. S. (2006). Contributions of the GABAA receptor α6 infunit to phasic and tonic inhibition revealed by a naturally occurring polymorphism in the α6 gene. J. Neurosci. 26, 3357-3364.
52. Serwanski, D. R., Miralles, C. P., Christie, S. B., Mehta, A. K., Li, X., and De Blas, A. L. (2006). Synaptic and nonsy-naptic localization of GABAA receptors containing the a5 infunit in the rat brain. J. Comp. Neurol. 499, 458-470.
53. Sieghart, W. (1995). Structure and pharmacology of γ-aminobutyric acidA receptor inftypes. Pharmacol. Rev. 47, 181-234.
54. Sieghart, W., and Sperk, G. (2002). Inf-unit composition, distribution and function of GABAA receptor inftypes. Curr. Top. Med. Chem. 2, 795-816.
55. Sigel, E., Baur, R., Trube, G., Mohler, H., and Malherbe, P. (1990). The effect of infunit composition of rat brain GABAA receptors on channel function. Neuron 5, 703-711.
56. Simon, J., Wakimoto, H., Fujita, N., Lalande, M., and Barnard, E. A. (2004). Analysis of the set of GABAA receptor genes in the human genome. J. Biol. Chem. 279, 41422-41435.
57. Sinkkonen, S. T., Hanna, M. C., Kirk-ness, E. F., and Korpi, E. R. (2000). GABAA receptor e and q infunits display unusual structural variation between species and are enriched in the rat locus ceruleus. J. Neurosci. 20, 3588-3595.
58. Sinkkonen, S. T., Vekovischeva, O. Y., Moykkynen, T., Ogris, W., Sieghart, W., Wisden, W., and Korpi, E. R. (2004). Behavioural correlates of an altered balance between synap-tic and extrasynaptic GABAAergic inhibition in a mouse model. Eur. J. Neurosci. 20, 2168-2178.
59. Sperk, G., Schwarzer, C., Tsunashima, K., Fuchs, K., and Sieghart, W. (1997). GABAA receptor inf-units in the rat hippocampus I: immunocytochemical distribution of 13 infunits. Neuroscience 80, 987-1000.
60. Taylor, P. M., Connolly, C. N., Kittler, J. T., Gorrie, G. H., Hosie, A., Smart, T. G., and Moss, S. J. (2000). Identification of residues within GABA(A) receptor alpha infunits that mediate specific assembly with receptor beta infunits. J. Neurosci. 20, 1297-1306.
61. Taylor, P. M., Thomas, P., Gorrie, G. H., Connolly, C. N., Smart, T. G., and Moss, S. J. (1999). Identification of amino acid residues within GABAA receptor β infunits that mediate both homomeric and heteromeric receptor expression. J. Neurosci. 19, 6360-6371.
62. Thomas, P., Mortensen, M., Hosie, A. M., and Smart, T. G. (2005). Dynamic mobility of functional GABAA receptors at inhibitory synapses. Nat. Neurosci. 8, 889-897.
63. Tia, S., Wang, J. F., Kotchabhakdi, N., and Vicini, S. (1996). Developmental changes of inhibitory synap-tic currents in cerebellar granule neurons: role of GABAA receptor α6 infunit. J. Neurosci. 16, 3630-3640.
64. Tretter, V., Jacob, T. C., Mukherjee, J., Fritschy, J. M., Pangalos, M. N., and Moss, S. J. (2008). The clustering of GABAA receptor inftypes at inhibitory synapses is facilitated via the direct binding of receptor α2 infunits to gephyrin. J. Neurosci. 28, 1356-1365.
65. Tretter, V., Kerschner, B., Milenkovic, I., Ramsden, S. L., Ramerstorfer, J., Saiepour, L., Maric, H. M., Moss, S. J., Schindelin, H., Harvey, R. J., Sieghart, W., and Harvey, K. (2011). Molecular basis of the γ-aminobutyric acid a receptor α3 inf-unit interaction with the clustering protein gephyrin. J. Biol. Chem. 286, 37702-37711.
66. Triller, A., and Choquet, D. (2005). Surface trafficking of receptors between synaptic and extrasynaptic membranes: and yet they do move! Trends Neurosci. 28, 133-139.
67. Verdoorn, T. A., Draguhn, A., Ymer, S., Seeburg, P. H., and Sakmann, B. (1990). Functional properties of recombinant rat GABAA receptors depend upon infunit composition. Neuron 4, 919-928.
68. Wang, H. B., Bedford, F. K., Brandon, N. J., Moss, S. J., and Olsen, R. W. (1999). GABAA-receptor-associated protein links GABAA receptors and the cytoskeleton. Nature 397, 69-72.
69. Whiting, P. J., McKernan, R. M., and Wafford, K. A. (1995). Structure and pharmacology of vertebrate GABAA receptor inftypes. Int. Rev. Neuro-biol. 38, 95-138.
70. Wisden, W., Laurie, D. J., Monyer, H., and Seeburg, P. H. (1992). The distribution of 13 GABAA receptor infunit mRNAs in the rat brain. I. Telencephalon, dien-cephalon, mesencephalon. J. Neu-rosci. 12, 1040-1062.
71. Wooltorton, J. R., Moss, S. J., and Smart, T. G. (1997). Pharmacological and physiological characterization of murine homomeric b3 GABAA receptors. Eur. J. Neurosci. 9, 2225-2235.