Two pools of Triton X-100-insoluble GABAA receptors are present in the brain, one associated to lipid rafts and another one to the post-synaptic GABAergic complex

Journal of Neurochemistry

Volumn 102, Issue 4, 2007, Pages 1329-1345

  Li, Xuejing ^b   Serwanski, David R ^b   Miralles, Celia P ^b   Bahr, Ben A ^b   De Blas, Angel L ^a,b  

^a University of Connecticut ^*  (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

aminobutyric acid type A receptor; Detergent resistant membrane; Gephyrin; Hippocampal cultures; Lipid rafts; Post synaptic density

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CHOLESTEROL; GEPHYRIN; LIPID; TRITON X 100;

ALPHA CHAIN; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BETA CHAIN; BRAIN SYNAPTOSOME; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; GABAERGIC TRANSMISSION; HIPPOCAMPUS; LIPID RAFT; MALE; NERVE CELL CULTURE; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; RECEPTOR AFFINITY; RECEPTOR DENSITY; RECEPTOR INTRINSIC ACTIVITY; SEDIMENTATION;

ANIMALS; BRAIN; CELLS, CULTURED; DETERGENTS; EMBRYO; FLUNITRAZEPAM; GABA MODULATORS; GAMMA-AMINOBUTYRIC ACID; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; NEURONS; OCTOXYNOL; RADIOLIGAND ASSAY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; SAPONINS; SUBCELLULAR FRACTIONS; SYNAPTOSOMES;

RATTUS;

EID: 34547520352     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.04635.x     Document Type: Article

References (86)

1. Allison D. W., Chervin A. S., Gelfand V. I. Craig A. M. (2000) Postsynaptic scaffolds of excitatory and inhibitory synapses in hippocampal neurons: maintenance of core components independent of actin filaments and microtubules. J. Neurosci. 20, 4545 4554.
2. Becher A., White J. A. McIlhinney R. A. (2001) The gamma-aminobutyric acid receptor B, but not the metabotropic glutamate receptor type-1, associates with lipid rafts in the rat cerebellum. J. Neurochem. 79, 787 795.
3. Besshoh S., Bawa D., Teves L., Wallace M. C. Gurd J. W. (2005) Increased phosphorylation and redistribution of NMDA receptors between synaptic lipid rafts and post-synaptic densities following transient global ischemia in the rat brain. J. Neurochem. 93, 186 194.
4. Brickley S. G., Cull-Candy S. G. Farrant M. (1999) Single-channel properties of synaptic and extrasynaptic GABAA receptors suggest differential targeting of receptor subtypes. J. Neurosci. 19, 2960 2973.
5. Brown D. A. London E. (1997) Structure of detergent-resistant membrane domains: does phase separation occur in biological membranes? Biochem. Biophys. Res. Commun. 240, 1 7.
6. Brown D. A. London E. (1998) Functional of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14, 111 136.
7. Brown D. A. London E. (2000) Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275, 17221 17224.
8. Brown D. A. Rose J. K. (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533 544.
9. Brunig I., Suter A., Knuesel I., Luscher B. Fritschy J. M. (2002) GABAergic terminals are required for postsynaptic clustering of dystrophin but not of GABA(A) receptors and gephyrin. J. Neurosci. 22, 4805 4813.
10. Bruses J. L., Chauvet N. Rutishauser U. (2001) Membrane lipid rafts are necessary for the maintenance of the (alpha)7 nicotinic acetylcholine receptor in somatic spines of ciliary neurons. J. Neurosci. 21, 504 512.
11. Carlin R. K., Grab D. J., Cohen R. S. Siekevitz P. (1980) Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J. Cell Biol. 86, 831 843.
12. Cerneus D. P., Ueffing E., Posthuma G., Strous G. J. van der Ende A. (1993) Detergent insolubility of alkaline phosphatase during biosynthetic transport and endocytosis. Role of cholesterol. J. Biol. Chem. 268, 3150 3155.
13. Chandra D., Korpi E. R., Miralles C. P., De Blas A. L. Homanics G. E. (2005) GABAA receptor gamma2 subunit knockdown mice have enhanced anxiety-like behavior but unaltered hypnotic response to benzodiazepines. BMC Neurosci. 6, 30.
14. Charych E. I., Yu W., L R. et al. (2004a) A four PDZ domain-containing splice variant form of GRIP1 is localized in GABAergic and glutamatergic synapses in the brain. J. Biol. Chem. 279, 38978 38990.
15. Charych E. I., Yu W., Miralles C. P., Serwanski D. R., Li X., Rubio M. De Blas A. L. (2004b) The brefeldin A-inhibited GDP/GTP exchange factor 2, a protein involved in vesicular trafficking, interacts with the beta subunits of the GABA receptors. J. Neurochem. 90, 173 189.
16. Choquet D. Triller A. (2003) The role of receptor diffusion in the organization of the postsynaptic memebrane. Nat. Rev. Neurosci. 4, 251 265.
17. Christie S. B. De Blas A. L. (2002) α5 Subunit-containing GABAA receptors form clusters at GABAergic synapses in hippocampal cultures. Neuroreport 13, 2355 2358.
18. Christie S. B. De Blas A. L. (2003) GABAergic and glutamatergic axons innervate the axon initial segment and organize GABAA receptor clusters of cultured hippocampal pyramidal cells. J. Comp. Neurol. 456, 361 374.
19. Christie S. B., Li R. W., Miralles C. P. et al. (2002a) Synaptic and extrasynaptic GABA receptor and gephyrin clusters. Prog. Brain Res. 136, 157 180.
20. Christie S. B., Miralles C. P. De Blas A. L. (2002b) GABAergic innervation organizes synaptic and extrasynaptic GABAA receptor clustering in cultured hippocampal neurons. J. Neurosci. 22, 684 697.
21. Christie S. B., Li R-W., Miralles C. P., Yang B-Y. De Blas A. L. (2006) Clustered and non-clustered GABAA receptors in cultured hippocampal neurons. Mol. Cell Neurosci. 31, 1 4.
22. Collin M. O., Husi H., Yu L., Brandon J. M., Anderson C. N., Blackstock W. P., Choudhary J. S. Grant S. G. (2006) Molecular characterization and comparison of the components and multiprotein complexes in the postsynaptic proteome. J. Neurochem. 1 (Suppl. 16 23.
23. Cotman C. W., Banker G., Churchill L. Taylor D. (1974) Isolation of postsynaptic densities from rat brain. J. Cell Biol. 63, 441 455.
24. Craig A. M., Blackstone C. D., Huganir H. L. Banker G. (1994) Selective clustering of glutamate and gamma-aminobutyric acid receptors opposite terminals releasing the corresponding neurotransmitters. Proc. Natl Acad. Sci. USA 91, 12373 12377.
25. Craig A. M., Banker G., Chang W., Mcgrath M. E. Serpinskaya A. S. (1996) Clustering of gephyrin at GABAergic but not glutamatergic synapses in cultured rat hippocampal neurons. J. Neurosci. 16, 3166 3177.
26. Dalskov S. M., Immerdal L., Nisels-Christiansen L. L., Hansen G. H., Schousboe A. Danielsen E. M. (2005) Lipid raft localization of GABAA receptor and Na+, K+-ATPase in discrete microdomain clusters in rat cerebellar granule cells. Neurochem. Int. 46, 489 499.
27. De Blas A. L. Cherwinski H. M. (1983) Detection of antigens on nitrocellular paper immunoblots with monoclonal antibodies. Anal. Biochem. 133, 214 219.
28. De Blas A. L., Vitorica J. Friedrich P. (1988) Localization of the GABAA receptor in the rat brain with a monoclonal antibody to the 57 000 Mr peptide of the GABAA receptor/benzodiazepine receptor/Cl-channel complex. J. Neurosci. 8, 602 614.
29. Essrich C., Lorez M., Benson J. A., Fritschy J. M. Lusher B. (1998) Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nat. Neurosci. 1, 563 571.
30. Farrant M. Nusser Z. (2005) Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat. Rev. Neurosci. 6, 215 229.
31. Feng G., Tintrup H., Kirsch J., Nichol M. C., Kuhse J., Betz H. Sanes J. R. (1998) Dual requirement for gephyrin in glycine receptor clustering and molybdoenzyme activity. Science 282, 1321 1324.
32. Fritschy J. M Brunig I. (2003) Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications. Pharmacol. Ther. 98, 299 323.
33. Fritschy J. M. Mohler H. (1995) GABAA-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J. Comp. Neurol. 359, 154 194.
34. Fritschy J. M., Weinmann O., Wenzel A. Benke D. (1998) Synapse-specific localization of NMDA and GABA(A) receptor subunits revealed by antigen-retrieval immunohistochemistry. J. Comp. Neurol. 390, 194 210.
35. Giustetto M., Kirsch J., Fritschy J. M., Cantino D. Sassoe-Pognotto M. (1998) Localization of the clustering protein gephyrin at GABAergic synapses in the main olfactory bulb of the rat. J. Comp. Neurol. 395, 231 244.
36. Goslin K., Asmussen H. Banker G. (1998) Rat hippocampal neurons in low-density culture, in Culturing Nerve cells (Banker G. Goslin K., eds pp. 339 370. MIT press, Cambridge, MA.
37. Harder T., Scheiffele P., Verkade P. Simons K. (1998) Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141, 929 942.
38. Hering H., Lin Chih-chun. Sheng M. (2003) Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J. Neurosci. 23, 3262 3271.
39. Holowka D., Gosse J. A., Hammond A. T. et al. (2005) Lipid segregation and IgE receptor signaling: a decade of progress. Biochim. Biophys. Acta 1746, 252 259.
40. Homanics G. E., Harrison N. L., Quinlan J. J. et al. (1999) Normal electrophysiological and behavioral responses to ethanol in mice lacking the long splice variant of the gamma2 subunit of the gamma-aminobutyrate type A receptor. Neuropharmacology 38, 253 265.
41. Hunt C. A., Schenker L. J. Kennedy M. B. (1996) PSD-95 is associated with the postsynaptic density and not with the presynaptic membrane at forebrain synapses. J. Neurosci. 16, 1380 1388.
42. Jacob T. C., Bogdanov Y. D., Mgnus. C., Saliba R. S., Kittler J. T., Haydon P. G. Moss S. J. (2005) Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors. J. Neurosci. 25, 10469 10478.
43. Jing S. Q., Spencer T., Miller K., Hopkins C. Trowbridge I. S. (1990) Role of the human transferrin receptor cytoplasmic domain in endocytosis: localization of a specific signal sequence for internalization. J. Cell Biol. 110, 283 294.
44. Jones D. H. Matus A. I. (1974) Isolation of synaptic plasma membrane from brain by combined flotation-sedimentation density gradient centrifugation. Biochim. Biophys. Acta 356, 276 287.
45. Jordan B. A., Fernholz B. D., Boussac M., Xu C., Grigorean G., Ziff E. B. Neubert T. A. (2004) Identification and verification of novel rodent postsynaptic density proteins. Mol. Cell Proteomics 3, 857 871.
46. Kawasaki B. T., Hoffman K. B., Yamamoto R. S. Bahr B. A. (1997) Variants of the receptor/channel clustering molecule gephyrin in brain: distinct distribution patterns, developmental profiles, and proteolytic cleavage by calpain. J. Neurosci. Res. 49, 381 388.
47. Kennedy M. B. (1997) The postsynaptic density at glutamatergic synapses. Trends Neurosci. 20, 264 268.
48. Kneussel M., Brandstatter J. H., Laube B., Stahl S., Muller U. Betz H. (1999) Loss of postsynaptic GABA(A) receptor clustering in gephyrin-deficient mice. J. Neurosci. 19, 9289 9297.
49. Kneussel M., Brandstatter J. H., Gasnier B., Feng G., Sanes J. R. Betz H. (2001) Gephyrin-independent clustering of postsynaptic GABA(A) receptor subtypes. Mol. Cell Neurosci. 17, 973 982.
50. Kullmann D. M., Ruiz A., Rusakov D. M., Scott R., Semyanov A. Walker M. C. (2005) Presynaptic, extrasynaptic and axonal GABAA receptors in the CNS: where and why? Prog. Biophys. Mol. Biol. 87, 33 46.
51. Levi S., Logan S. M., Tovar K. R. Craig A. M. (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.
52. Li R. W., Serwanski D. R., Miralles C. P., Li X., Charych E., Riquelme R., Huganir R. L. De Blas A. L. (2005a) GRIP1 in GABAergic synapses. J. Comp. Neurol. 488, 11 27.
53. Li R. W., Yu W., Christie S., Miralles C. P., Bai J., Loturco J. J. De Blas A. L. (2005b) Disruption of postsynaptic GABA receptor clusters leads to decreased GABAergic innervation of pyramidal neurons. J. Neurochem. 95, 756 770.
54. London E. Brown D. A. (2000) Insolubility of lipid in Triton X-100: physical origin and relationship to sphingolipid/cholesterol membrane domains (rafts). Biochem. Biophys. Acta 1508, 182 195.
55. Luscher B. Keller C. A. (2004) Regulation of GABAA receptor trafficking, channel activity, and functional plasiticity of inhibitory synapses. Pharmacol. Ther. 102, 195 221.
56. Masserini M., Palestini P. Pitto M. (1999) Glycolipid-enriched caveolae and caveolae-like domains in the nervous system. J. Neurochem. 73, 1 11.
57. Matus A., Pehling G., Ackermann M. Maeder J. (1980) Brain postsynaptic densities: the relationship to glial and neuronal filaments. J. Cell Biol. 87, 346 359.
58. Miralles C. P., Li M., Metha A. K., Kahn Z. U. De Blas A. L. (1999) Immunocytochemical localization of the beta(3) subunit of the gamma-aminobutyric acid(A) receptor in the rat brain. J. Comp. Neurol. 413, 535 548.
59. Mody I. (2005) Aspects of the homeostatic plasticity of GABAA receptor-mediated inhibition. J. Physiol. 562, 37 46.
60. Moreno J. I., Piva M. A., Miralles C. P. De Blas A. L. (1994) Immunocytochemical localization of the beta 2 subunit of the gamma-aminobutyric acid(A) receptor in the rat brain. J. Comp. Neurol. 350, 260 271.
61. Mortensen M. Smart T. G. (2006) Extrasynaptic αβ subunit GABAA receptors on hippocampal pyramidal neurons. J. Physiol. (Lond.) 577, 841 856.
62. Moss S. J. Smart T. G. (2001) Constructing inhibitory synapses. Nat. Rev. Neurosci. 2, 240 250.
63. Nusser Z. Mody I. (2002) Selective modulation of tonic and phasic inhibition in dentate gyrus granule cells. J. Neurophysiol. 87, 2626 2628.
64. Nusser Z., Roberts J. D., Baude A., Richards J. G. Somogyi P. (1995) Immunocytochemical localization of the alpha 1 and beta 2/3 subunits of the GABAA receptor in relation to specific GABAergic synapses in the dentate gyrus. Eur. J. Neurosci. 7, 630 646.
65. Nusser Z., Sieghart W. Somogyi P. (1998) Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J. Neurosci. 18, 1693 1703.
66. Owens D. F Kriegstein A. R. (2002) Is there more to GABA than synaptic inhibition? Nat. Rev. Neurosci. 3, 715 727.
67. Peng J., Kim M. J., Cheng D., Duong D. M., Gygi S. P. Sheng M. (2004) Semiquantitative proteomic analysis of rat forebrain postsynaptic density fractions by mass spectrometry. J. Biol. Chem. 279, 21003 21011.
68. Pirker S., Schwarzer C., Wieselthaler A., Sieghart W. Sperk G. (2000) GABA(A) receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101, 815 850.
69. Riquelme R., Miralles C. P. De Blas A. L. (2002) Bergmann glia GABAA Receptors Concentrate on the Glial Processes that Wrap Inhibitory Synapses. J. Neurosci. 22, 10720 10730.
70. Sassoe-Pognetto M., Panzanelli P., Sieghart W. Fritschy J. M. (2000) Colocalization of multiple GABA(A) receptor subtypes with gephyrin at postsynaptic sites. J. Comp. Neurol. 420, 481 498.
71. Schroeder R., London E. Brown D. (1994) Interactions between saturated acyl chains confer detergent resistance on lipid and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior. Proc. Natl Acad. Sci. USA 91, 12130 12134.
72. Schweizer C., Balsiger S., Bluethmann H., Mansuy I. M., Fritschy J. M., Mohler H. Lusher B. (2003) The gamma 2 subunit of GABA(A) receptors is required for maintenance of receptors at mature synapses. Mol. Cell Neurosci. 24, 442 450.
73. Serwanski D. R., Miralles C. P., Christie S. B., Mehta A. K., Li X. De Blas A. L. (2006) Synaptic and non-synaptic localization of GABAA receptors containing the α5 subunit in the rat brain. J. Comp. Neurol. 499, 458 470.
74. Simons K. Toomre D. (2000) Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31 39.
75. Somogyi P., Fritschy J. M., Benke D., Roberts J. D. B. Sieghart W. (1996) The γ2 subunit of the GABAA receptor is concentrated in synaptic junctions containing the α1 and β2/3 subunits in hippocampus, cerebellum and globus pallidus. Neuropharmacol 35, 1425 1444.
76. Sooksawate T. Simmonds M. A. (2001) Influence of membrane cholesterol on modulation of the GABA(A) receptor by neuroactive steroids and other potentiators. Br. J. Pharmacol. 134, 1303 1311.
77. Stell B. M., Brickley S. G., Tang C. Y., Farrant M. Mody I. (2003) Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by delta subunit-containing GABAA receptors. Proc. Natl Acad. Sci. USA 100, 14439 14444.
78. Suzuki T. (2002) Lipid rafts at postsynaptic sites: distribution, function and linkage to postsynaptic density. Neurosci. Res. 44, 1 9.
79. Suzuki T., Ito J., Takagi H., Saitoh F., Nawa H. Shimizu H. (2001) Biochemical evidence for localization of AMPA-type glutamate receptor subunits in the dendritic raft. Brain Res. Mol. Brain Res. 89, 20 28.
80. Thomas P., Mortensen M., Hosie A. A. Smart T. G. (2005) Dynamic mobility of functional GABAA receptors at inhibitory synapses. Nat. Neurosci. 8, 889 897.
81. Van Rijnsoever C., Sidler C. Fritschy J. M. (2005) Internalized GABA-receptor subunits are transferred to a intracellular pool associated with the postsynaptic density. Eur. J. Neurosci. 21, 327 338.
82. Vitorica J., Park D., Chin G. De Blas A. L. (1988) Monoclonal antibodies and conventional antisera to the GABAA receptor/benzodiazepine receptor/Cl- channel complex. J. Neurosci. 8, 615 622.
83. Walikonis R. S., Jensen O. N., Mann M., Provance Jr. D. W., Mercer J. A. Kennedy M. B. (2000) Identification of proteins in the postsynaptic density fraction by mass spectrometry. J. Neurosci. 20, 4069 4080.
84. Wei W., Zhang N., Peng Z., Houser C. R. Mody I. (2003) Perisynaptic localization of delta subunit-containing GABAA receptors and their activation by GABA spillover in the mouse dentate gyrus. J. Neurosci. 23, 10650 10661.
85. Yoshimura Y., Yamauchi Y., Shinkawa T., Taoka M., Donai H., Takahashi N., Isobe T. Yamauchi T. (2004) Molecular constituents of the postsynaptic density fraction revealed by proteomic analysis using multidimensional liquid chromatography-tandem mass spectrometry. J. Neurochem. 88, 759 768.
86. Zhu D., Xiong WC Mei L. (2006) Lipid rafts serve as a signaling platform for nicotinic acetylcholine receptor clustering. J. Neurosci. 26, 4841 4845.