Lipid raft localization of GABAA receptor and Na+, K+-ATPase in discrete microdomain clusters in rat cerebellar granule cells

Neurochemistry International

Volumn 46, Issue 6, 2005, Pages 489-499

  Dalskov, Stine Mathilde ^a   Immerdal, Lissi ^a   Niels Christiansen, Lise Lotte ^a   Hansen, Gert H ^a   Schousboe, Arne ^b   Danielsen, E Michael ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Cerebellar; Cholesterol; GABAA receptor

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ANKYRIN; ANKYRIN G; BIOLOGICAL MARKER; CHOLESTEROL; CYTOSKELETON PROTEIN; DETERGENT; GANGLIOSIDE GM1; GEPHYRIN; ICE; MEMBRANE PROTEIN; METHYL BETA CYCLODEXTRIN; POLYOXYETHYLENE OLEYL ETHER; SCAFFOLD PROTEIN; TRITON X 100; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL FRACTIONATION; CELL SURFACE; CEREBELLUM; CLUSTER ANALYSIS; COLD; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; EXTRACTION; FLUORESCENCE MICROSCOPY; GRANULE CELL; IMMUNOGOLD ELECTRON MICROSCOPY; MICROENVIRONMENT; NONHUMAN; OBSERVATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SOLUBILITY;

EID: 14844303926     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2004.11.010     Document Type: Article

References (63)

1. R.G. Anderson The caveolae membrane system Annu. Rev. Biochem. 67 1998 199 225
2. R.G. Anderson, and K. Jacobson A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains Science 296 2002 1821 1825
3. M. Bagnat, S. Keranen, A. Shevchenko, A. Shevchenko, and K. Simons Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast Proc. Natl. Acad. Sci. USA 97 2000 3254 3259
4. Y. Balslev, and G.H. Hansen Preparation and use of recombinant protein G-gold complexes as markers in double labelling immunocytochemistry Histochem. J. 21 1989 449 454
5. E.M. Barnes Jr. Intracellular trafficking of GABA(A) receptors Life Sci. 66 2000 1063 1070
6. A. Becher, J.H. White, and R.A. McIlhinney 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 2001 787 795
7. A. Braccia, M. Villani, L. Immerdal, L.L. Niels-Christiansen, B.T. Nystrom, G.H. Hansen, and E.M. Danielsen Microvillar membrane Microdomains exist at physiological temperature - Role of galectin-4 as lipid raft stabilizer revealed by "superrafts" J. Biol. Chem. 278 2003 15679 15684
8. N. Brandon, J. Jovanovic, and S. Moss Multiple roles of protein kinases in the modulation of gamma-aminobutyric acid(A) receptor function and cell surface expression Pharmacol. Ther. 94 2002 113 122
9. N.J. Brandon, P. Delmas, J.T. Kittler, B.J. McDonald, W. Sieghart, D.A. Brown, T.G. Smart, and S.J. Moss GABAA receptor phosphorylation and functional modulation in cortical neurons by a protein kinase C-dependent pathway J. Biol. Chem. 275 2000 38856 38862
10. D.A. Brown, and E. London Functions of lipid rafts in biological membranes Annu. Rev. Cell Dev. Biol. 14 1998 111 136
11. D.A. Brown, and J.K. Rose Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface Cell 68 1992 533 544
12. J.L. Bruses, N. Chauvet, and U. Rutishauser Membrane lipid rafts are necessary for the maintenance of the (alpha)7 nicotinic acetylcholine receptor in somatic spines of ciliary neurons J. Neurosci. 21 2001 504 512
13. D.R. Burt Reducing GABA receptors Life Sci. 73 2003 1741 1758
14. B.X. Carlson, L. Elster, and A. Schousboe Pharmacological and functional implications of developmentally-regulated changes in GABA(A) receptor subunit expression in the cerebellum Eur. J. Pharmacol. 352 1998 1 14
15. D. Corbeil, K. Roper, C.A. Fargeas, A. Joester, and W.B. Huttner Prominin: a story of cholesterol, plasma membrane protrusions and human pathology Traffic 2 2001 82 91
16. L. Danglot, A. Triller, and A. Bessis Association of gephyrin with synaptic and extrasynaptic GABAA receptors varies during development in cultured hippocampal neurons Mol. Cell Neurosci. 23 2003 264 278
17. E.M. Danielsen Involvement of detergent-insoluble complexes in the intracellular transport of intestinal brush border enzymes Biochemistry 34 1995 1596 1605
18. E.M. Danielsen, and G.H. Hansen Lipid rafts in epithelial brush borders: atypical membrane microdomains with specialized functions Biochim. Biophys. Acta 1617 2003 1 9
19. J. Drejer, and A. Schousboe Selection of a pure cerebellar granule cell culture by kainate treatment Neurochem. Res. 14 1989 751 754
20. P. Drevot, C. Langlet, X.J. Guo, A.M. Bernard, O. Colard, J.P. Chauvin, R. Lasserre, and H.T. He TCR signal initiation machinery is pre-assembled and activated in a subset of membrane rafts EMBO J. 21 2002 1899 1908
21. M. Edidin The state of lipid rafts: from model membranes to cells Annu. Rev. Biophys. Biomol. Struct. 2003
22. L. Elster, G.H. Hansen, B. Belhage, J.M. Fritschy, H. Mohler, and A. Schousboe Differential distribution of GABAA receptor subunits in soma and processes of cerebellar granule cells: effects of maturation and a GABA agonist Int. J. Dev. Neurosci. 13 1995 417 428
23. F. Fischer, M. Kneussel, H. Tintrup, S. Haverkamp, T. Rauen, H. Betz, and H. Wassle Reduced synaptic clustering of GABA and glycine receptors in the retina of the gephyrin null mutant mouse J. Comp. Neurol. 427 2000 634 648
24. J.M. Fritschy, and I. Brunig Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications Pharmacol. Ther. 98 2003 299 323
25. G.H. Hansen, B. Belhage, and A. Schousboe Effect of a GABA agonist on the expression and distribution of GABAA receptors in the plasma membrane of cultured cerebellar granule cells: an immunocytochemical study Neurosci. Lett. 124 1991 162 165
26. G.H. Hansen, B. Belhage, A. Schousboe, and E. Meier Temporal development of GABA agonist induced alterations in ultrastructure and GABA receptor expression in cultured cerebellar granule cells Int. J. Dev. Neurosci. 5 1987 263 269
27. G.H. Hansen, E. Hosli, B. Belhage, A. Schousboe, and L. Hosli Light and electron microscopic localization of GABAA-receptors on cultured cerebellar granule cells and astrocytes using immunohistochemical techniques Neurochem. Res. 16 1991 341 346
28. G.H. Hansen, L.L. Niels-Christiansen, L. Immerdal, W. Hunziker, A.J. Kenny, and E.M. Danielsen Transcytosis of immunoglobulin A in the mouse enterocyte occurs through glycolipid raft- and rab17-containing compartments Gastroenterology 116 1999 610 622
29. G.H. Hansen, L.L. Niels-Christiansen, E. Thorsen, L. Immerdal, and E.M. Danielsen Cholesterol depletion of enterocytes. Effect on the Golgi complex and apical membrane trafficking J. Biol. Chem. 275 2000 5136 5142
30. T. Harder, P. Scheiffele, P. Verkade, and K. Simons Lipid domain structure of the plasma membrane revealed by patching of membrane components J. Cell Biol. 141 1998 929 942
31. H. Hering, C.C. Lin, and M. Sheng Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability J. Neurosci. 23 2003 3262 3271
32. K. Holm, K. Weclewicz, R. Hewson, and M. Suomalainen Human immunodeficiency virus type 1 assembly and lipid rafts: Pr55(gag) associates with membrane domains that are largely resistant to Brij98 but sensitive to Triton X-100 J. Virol. 77 2003 4805 4817
33. N.M. Hooper Detergent-insoluble glycosphingolipid/cholesterol-rich membrane domains, lipid rafts and caveolae (review) Mol. Membr. Biol. 16 1999 145 156
34. S.M. Jenkins, and V. Bennett Developing nodes of Ranvier are defined by ankyrin-G clustering and are independent of paranodal axoglial adhesion Proc. Natl. Acad. Sci. USA 99 2002 2303 2308
35. K. Kannenberg, R. Baur, and E. Sigel Proteins associated with alpha 1-subunit-containing GABAA receptors from bovine brain J. Neurochem. 68 1997 1352 1360
36. J.T. Kittler, and S.J. Moss Modulation of GABAA receptor activity by phosphorylation and receptor trafficking: implications for the efficacy of synaptic inhibition Curr. Opin. Neurobiol. 13 2003 341 347
37. M. Kneussel Dynamic regulation of GABA(A) receptors at synaptic sites. Brain Res. Brain Res. Rev. 39 2002 74 83
38. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
39. M.D. Ledesma, K. Simons, and C.G. Dotti Neuronal polarity: essential role of protein-lipid complexes in axonal sorting Proc. Natl. Acad. Sci. USA 95 1998 3966 3971
40. R.L. Macdonald, and R.W. Olsen GABAA receptor channels Annu. Rev. Neurosci. 17 1994 569 602
41. S. Maekawa, S. Iino, and S. Miyata Molecular characterization of the detergent-insoluble cholesterol-rich membrane microdomain (raft) of the central nervous system Biochim. Biophys. Acta 1610 2003 261 270
42. J.R. Martens, K. O'Connell, and M. Tamkun Targeting of ion channels to membrane microdomains: localization of K(V) channels to lipid rafts Trends Pharmacol. Sci. 25 2004 16 21
43. P. Munoz, M.D. Navarro, E. Pavon, J. Salmeron, F. Malavasi, J. Sancho, and M. Zubiaur CD38 signaling in T cells is initiated within a subset of membrane rafts containing Lck and CD3-zeta subunit of the T cell antigen receptor J. Biol. Chem. 2003
44. S. Munro Lipid rafts. Elusive or illusive? Cell 115 2003 377 388
45. +)ATPase and implications for the organization of membrane domains in polarized cells Nature 328 1987 533 536
46. E.T. Parkin, A.J. Turner, and N.M. Hooper Amyloid precursor protein, although partially detergent-insoluble in mouse cerebral cortex, behaves as an atypical lipid raft protein Biochem. J. 344 Pt 1 1999 23 30
47. R.G. Parton, and A.A. Richards Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms Traffic 4 2003 724 738
48. F. Pfeiffer, D. Graham, and H. Betz Purification by affinity chromatography of the glycine receptor of rat spinal cord J. Biol. Chem. 257 1982 9389 9393
49. J.L. Salzer Clustering sodium channels at the node of Ranvier: close encounters of the axon-glia kind Neuron 18 1997 843 846
50. J.L. Salzer Polarized domains of myelinated axons Neuron 40 2003 297 318
51. B. Schmitt, P. Knaus, C.M. Becker, and H. Betz The Mr 93,000 polypeptide of the postsynaptic glycine receptor complex is a peripheral membrane protein Biochemistry 26 1987 805 811
52. A. Schon, and E. Freire Thermodynamics of intersubunit interactions in cholera toxin upon binding to the oligosaccharide portion of its cell surface receptor, ganglioside GM1 Biochemistry 28 1989 5019 5024
53. A. Schousboe Pharmacologic and therapeutic aspects of the developmentally regulated expression of GABA(A) and GABA(B) receptors: cerebellar granule cells as a model system Neurochem. Int. 34 1999 373 377
54. M. Sensenbrenner, K. Maderspach, L. Latzkovits, and G.G. Jaros Neuronal cells from chick embryo cerebral hemispheres cultivated on polylysine-coated surfaces Dev. Neurosci. 1 1978 90 101
55. H. Shogomori, and A.H. Futerman Cholera toxin is found in detergent-insoluble rafts/domains at the cell surface of hippocampal neurons but is internalized via a raft-independent mechanism J. Biol. Chem. 276 2001 9182 9188
56. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572
57. K. Simons, and E. Ikonen How cells handle cholesterol Science 290 2000 1721 1726
58. K. Simons, and D. Toomre Lipid rafts and signal transduction Nat. Rev. Mol. Cell Biol. 1 2000 31 39
59. S.T. Sinkkonen, B. Luscher, H. Luddens, and E.R. Korpi Autoradiographic imaging of altered synaptic alphabetagamma2 and extrasynaptic alphabeta GABAA receptors in a genetic mouse model of anxiety Neurochem. Int. 44 2004 539 547
60. +-ATPase: structure, function, and interactions with drugs Adv. Neurol. 44 1986 681 693
61. B. Studler, J.M. Fritschy, and I. Brunig GABAergic and glutamatergic terminals differentially influence the organization of GABAergic synapses in rat cerebellar granule cells in vitro Neuroscience 114 2002 123 133
62. T. Suzuki, J. Ito, H. Takagi, F. Saitoh, H. Nawa, and H. Shimizu Biochemical evidence for localization of AMPA-type glutamate receptor subunits in the dendritic raft. Brain Res. Mol. Brain Res. 89 2001 20 28
63. P.J. Whiting The GABAA receptor gene family: new opportunities for drug development Curr. Opin. Drug Discov. Devel. 6 2003 648 657