Lipid rafts, synaptic transmission and plasticity: Impact in age-related neurodegenerative diseases

Neuropharmacology

Volumn 64, Issue , 2013, Pages 97-107

  Sebastião, Ana M ^a,b   Colino Oliveira, Mariana ^a,b   Assaife Lopes, Natália ^a,b   Dias, Raquel B ^a,b   Ribeiro, Joaquim A ^a,b  

^a INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^b UNIVERSITY OF LISBON   (Portugal)

Author keywords

Ageing; Learning and memory; Lipid rafts; Neurodegenerative disorders; Neuronal communication; Synaptic plasticity

Indexed keywords

AMYLOID PRECURSOR PROTEIN; CAVEOLIN 1; CHOLESTEROL; GLYCOSPHINGOLIPID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER;

AGING; ALZHEIMER DISEASE; CELL COMMUNICATION; CELL MIGRATION; CENTRAL NERVOUS SYSTEM; COGNITIVE DEFECT; CYTOSKELETON; DEGENERATIVE DISEASE; DOPAMINERGIC TRANSMISSION; ENDOCYTOSIS; EXOCYTOSIS; GABAERGIC TRANSMISSION; GLUTAMATERGIC TRANSMISSION; HIPPOCAMPUS; HUMAN; HUNTINGTON CHOREA; LEARNING; LIPID RAFT; MEMORY; MYRISTYLATION; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PALMITOYLATION; PARKINSON DISEASE; PICK PRESENILE DEMENTIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEOMICS; PURINERGIC TRANSMISSION; REVIEW; SEROTONINERGIC TRANSMISSION; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC TRANSMISSION;

AGING; ANIMALS; CENTRAL NERVOUS SYSTEM; HUMANS; MEMBRANE MICRODOMAINS; NEURODEGENERATIVE DISEASES; NEURONAL PLASTICITY; NEURONS; NOOTROPIC AGENTS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84866384152     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.06.053     Document Type: Review

References (155)

1. E.M. Adkins, D.J. Samuvel, J.U. Fog, J. Eriksen, L.D. Jayanthi, C.B. Vaegter, S. Ramamoorthy, and U. Gether Membrane mobility and microdomain association of the dopamine transporter studied with fluorescence correlation spectroscopy and fluorescence recovery after photobleaching Biochemistry 46 2007 10484 10497
2. J.A. Allen, R.A. Halverson-Tamboli, and M.M. Rasenick Lipid raft microdomains and neurotransmitter signalling Nat. Rev. Neurosci. 8 2007 128 140
3. R. Allsopp, U. Lalo, and R. Evans Lipid raft association and cholesterol sensitivity of P2X1-4 receptors for ATP J. Biol. Chem. 285 2010 32770 32777
4. N. Assaife-Lopes, V.C. Sousa, D.B. Pereira, J.A. Ribeiro, M.V. Chao, and A.M. Sebastião Activation of adenosine A2A receptors induces TrkB translocation and increases BDNF-mediated phospho-TrkB localization in lipid rafts: implications for neuromodulation J. Neurosci. 30 2010 8468 8480
5. N. Balasubramanian, D.W. Scott, J.D. Castle, J.E. Casanova, and M.A. Schwartz Arf6 and microtubules in adhesion-dependent trafficking of lipid rafts Nat. Cell Biol. 9 2007 1381 1391
6. F.J. Barrantes Cholesterol effects on nicotinic acetylcholine receptor J. Neurochem. 103 Suppl. 1 2007 72 80
7. 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
8. A. Becher, A. Green, A.O. Ige, A. Wise, J.H. White, and R.A. McIlhinney Ectopically expressed gamma-aminobutyric acid receptor B is functionally down-regulated in isolated lipid raft-enriched membranes Biochem. Biophys. Res. Commun. 321 2004 981 987
9. S. Besshoh, D. Bawa, L. Teves, M.C. Wallace, and J.W. Gurd 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 2005 186 194
10. S. Besshoh, S. Chen, I.R. Brown, and J.W. Gurd Developmental changes in the association of NMDA receptors with lipid rafts J. Neurosci. Res. 85 2007 1876 1883
11. A. Bhatnagar, D. Sheffler, W. Kroeze, B. Compton-Toth, and B. Roth Caveolin-1 interacts with 5-HT2A serotonin receptors and profoundly modulates the signaling of selected Galphaq-coupled protein receptors J. Biol. Chem. 279 2004 34614 34623
12. J.A. Blundon, and S.S. Zakharenko Dissecting the components of long-term potentiation Neuroscientist 14 2008 598 608
13. I. Borbon, J. Totenhage, M.T. Fiorenza, S. Canterini, W. Ke, T. Trouard, and R.P. Erickson Niemann-Pick C1 mice, a model of "Juvenile Alzheimer's disease", with normal gene expression in neurons and fibrillary astrocytes show long term survival and delayed neurodegeneration J. Alzheimers Dis. 2012 (Epub ahead of print)
14. C. Bouillot, A. Prochiantz, G. Rougon, and B. Allinquant Axonal amyloid precursor protein expressed by neurons in vitro is present in a membrane fraction with caveolae-like properties J. Biol. Chem. 271 1996 7640 7644
15. S.G. Brickley, and I. Mody Extrasynaptic GABA(A) receptors: their function in the CNS and implications for disease Neuron 73 2012 23 34
16. D.A. Brown, and E. London Functions of lipid rafts in biological membranes Annu. Rev. Cell Dev. Biol. 14 1998 111 136
17. 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
18. G. Burnstock Historical review: ATP as a neurotransmitter Trends Pharmacol. Sci. 27 2006 166 176
19. M.E. Butchbach, G. Tian, H. Guo, and C.L. Lin Association of excitatory amino acid transporters, especially EAAT2, with cholesterol-rich lipid raft microdomains: importance for excitatory amino acid transporter localization and function J. Biol. Chem. 279 2004 34388 34396
20. W. Chadwick, R. Brenneman, B. Martin, and S. Maudsley Complex and multidimensional lipid raft alterations in a murine model of Alzheimer's disease Int. J. Alzheimers Dis. 2010 10.4061/2010/604792
21. A. Citri, and R.C. Malenka Synaptic plasticity: multiple forms, functions, and mechanisms Neuropsychopharmacology 33 2008 18 41
22. A.A. Cole, A. Dosemeci, and T.S. Reese Co-segregation of AMPA receptors with G(M1) ganglioside in synaptosomal membrane subfractions Biochem. J. 427 2010 535 540
23. M.A. Colicos, and N.I. Syed Neuronal networks and synaptic plasticity: understanding complex system dynamics by interfacing neurons with silicon technologies J. Exp. Biol. 209 2006 2312 2319
24. J.M. Cordy, I. Hussain, C. Dingwall, N.M. Hooper, and A.J. Turner Exclusively targeting beta-secretase to lipid rafts by GPI-anchor addition up-regulates beta-site processing of the amyloid precursor protein Proc. Natl. Acad. Sci. U. S. A. 100 2003 11735 11740
25. A.R. Costenla, M.J. Diógenes, P.M. Canas, R.J. Rodrigues, C. Nogueira, J. Maroco, P.M. Agostinho, J.A. Ribeiro, R.A. Cunha, and A. de Mendonça Enhanced role of adenosine A(2A) receptors in the modulation of LTP in the rat hippocampus upon ageing Eur. J. Neurosci. 34 2011 12 21
26. M.L. Cremona, H.J. Matthies, K. Pau, E. Bowton, N. Speed, B.J. Lute, M. Anderson, N. Sen, S.D. Robertson, R.A. Vaughan, J.E. Rothman, A. Galli, J.A. Javitch, and A. Yamamoto Lotillin-1 is essential for PKC-triggered endocytosis and membrane microdomain localization of DAT Nat. Neurosci. 14 2011 469 477
27. G. D'Arcangelo, D. Grossi, G. De Chiara, M.C. de Stefano, G. Cortese, G. Citro, S. Rufini, V. Tancredi, D. Merlo, and C. Frank Glutamatergic neurotransmission in a mouse model of Niemann-Pick type C disease Brain Res. 1396 2011 11 19
28. S.M. Dalskov, L. Immerdal, L.L. Niels-Christiansen, G.H. Hansen, A. Schousboe, and E.M. Danielsen Lipid raft localization of GABA A receptor and Na+, K+-ATPase in discrete microdomain clusters in rat cerebellar granule cells Neurochem. Int. 46 2005 489 499
29. I. Delint-Ramirez, P. Salcedo-Tello, and F. Bermudez-Rattoni Spatial memory formation induces recruitment of NMDA receptor and PSD-95 to synaptic lipid rafts J. Neurochem. 106 2008 1658 1668
30. R.B. Dias, J.A. Ribeiro, and A.M. Sebastião Enhancement of AMPA currents and GluR1 membrane expression through PKA-coupled adenosine A(2A) receptors Hippocampus 22 2012 276 291
31. J.M. Dietschy, and S.D. Turley Cholesterol metabolism in the brain Curr. Opin. Lipidol. 12 2001 105 112
32. M.J. Diógenes, C.C. Fernandes, A.M. Sebastião, and J.A. Ribeiro Activation of adenosine A2A receptor facilitates brain-derived neurotrophic factor modulation of synaptic transmission in hippocampal slices J. Neurosci. 24 2004 2905 2913
33. M.J. Diógenes, N. Assaife-Lopes, A. Pinto-Duarte, J.A. Ribeiro, and A.M. Sebastião Influence of age on BDNF modulation of hippocampal synaptic transmission: interplay with adenosine A2A receptors Hippocampus 17 2007 577 585
34. M.J. Diógenes, A.R. Costenla, L.V. Lopes, A. Jerónimo- Santos, V.C. Sousa, B.M. Fontinha, J.A. Ribeiro, and A.M. Sebastião Enhancement of LTP in aged rats is dependent on endogenous BDNF Neuropsychopharmacology 36 2011 1823 1836
35. F. Dufour, Q.Y. Liu, P. Gusev, D. Alkon, and M. Atzori Cholesterol-enriched diet affects spatial learning and synaptic function in hippocampal synapses Brain Res. 1103 2006 88 98
36. J.L. Dupree, and A.D. Pomicter Myelin, DIGs, and membrane rafts in the central nervous system Prostaglandins Other Lipid Mediat. 91 2010 118 129
37. N. Fabelo, V. Martin, G. Santpere, R. Marin, L. Torrent, I. Ferrer, and M. Diaz Severe alterations in lipid composition of frontal cortex lipid rafts from Parkinson's disease and incidental Parkinson's disease Mol. Med. 17 2011 1107 1118
38. Q.W. Fan, W. Yu, J.S. Gong, K. Zou, N. Sawamura, T. Senda, K. Yanagisawa, and M. Michikawa Cholesterol-dependent modulation of dendrite outgrowth and microtubule stability in cultured neurons J. Neurochem. 80 2002 178 190
39. C. Fang, L. Deng, C.A. Keller, M. Fukata, Y. Fukata, G. Chen, and B. Luscher GODZ-mediated palmitoylation of GABA(A) receptors is required for normal assembly and function of GABAergic inhibitory synapses J. Neurosci. 26 2006 12758 12768
40. C.C. Fernandes, A. Pinto-Duarte, J.A. Ribeiro, and A.M. Sebastião Postsynaptic action of brain-derived neurotrophic factor attenuates alpha7 nicotinic acetylcholine receptor-mediated responses in hippocampal interneurons J. Neurosci. 28 2008 5611 5618
41. D. Fioravante, and W.G. Regehr Short-term forms of presynaptic plasticity Curr. Opin. Neurobiol. 21 2011 269 274
42. B.M. Fontinha, M.J. Diógenes, J.A. Ribeiro, and A.M. Sebastião Enhancement of long-term potentiation by brain-derived neurotrophic factor requires adenosine A2A receptor activation by endogenous adenosine Neuropharmacology 54 2008 924 933
43. L.J. Foster, C.L. De Hoog, and M. Mann Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors Proc. Natl. Acad. Sci. U. S. A. 100 2003 5813 5818
44. J.D. Foster, S.D. Adkins, J.R. Lever, and R.A. Vaughan Phorbol ester induced trafficking-independent regulation and enhanced phosphorylation of the dopamine transporter associated with membrane rafts and cholesterol J. Neurochem. 105 2008 1683 1699
45. A. Francesconi, R. Kumari, and R.S. Zukin Regulation of group I metabotropic glutamate receptor trafficking and signaling by the caveolar/lipid raft pathway J. Neurosci. 29 2009 3590 3602
46. C. Frank, A.M. Giammarioli, R. Pepponi, C. Fiorentini, and S. Rufini Cholesterol perturbing agents inhibit NMDA-dependent calcium influx in rat hippocampal primary culture FEBS Lett. 566 2004 25 29
47. C. Frank, S. Rufini, V. Tancredi, R. Forcina, D. Grossi, and G. D'Arcangelo Cholesterol depletion inhibits synaptic transmission and synaptic plasticity in rat hippocampus Exp. Neurol. 212 2008 407 414
48. S.B. Gaudreault, J.F. Blain, J.P. Gratton, and J. Poirier A role for caveolin-1 in post-injury reactive neuronal plasticity J. Neurochem. 92 2005 831 839
49. E. Gielen, W. Baron, M. Vandeven, P. Steels, D. Hoekstra, and M. Ameloot Rafts in oligodendrocytes: evidence and structure-function relationship Glia 54 2006 499 512
50. C. Gil, A. Soler-Jover, J. Blasi, and J. Aguilera Synaptic proteins and SNARE complexes are localized in lipid rafts from rat brain synaptosomes Biochem. Biophys. Res. Commun. 329 2005 117 124
51. C. Gómez-Moutón, R. Lacalle, E. Mira, S. Jiménez-Baranda, D. Barber, A. Carrera, A.C. Martínez-, and S. Mañes Dynamic redistribution of raft domains as an organizing platform for signaling during cell chemotaxis J. Cell Biol. 164 2004 759 768
52. P. Gonnord, C. Delarasse, R. Auger, K. Benihoud, M. Prigent, M. Cuif, C. Lamaze, and J. Kanellopoulos Palmitoylation of the P2X7 receptor, an ATP-gated channel, controls its expression and association with lipid rafts FASEB J. 23 2009 795 805
53. A. Gruart, C. Sciarretta, M. Valenzuela-Harrington, J.M. Delgado-Garcia, and L. Minichiello Mutation at the TrkB PLC{gamma}-docking site affects hippocampal LTP and associative learning in conscious mice Learn. Mem. 14 2007 54 62
54. C. Guirland, S. Suzuki, M. Kojima, B. Lu, and J.Q. Zheng Lipid rafts mediate chemotropic guidance of nerve growth cones Neuron 42 2004 51 62
55. M.F. Hanzal-Bayer, and J.F. Hancock Lipid rafts and membrane traffic FEBS Lett. 581 2007 2098 2104
56. G.E. Hardingham, and H. Bading Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders Nat. Rev. Neurosci. 11 2010 682 696
57. B.P. Head, H.H. Patel, Y.M. Tsutsumi, Y. Hu, T. Mejia, R.C. Mora, P.A. Insel, D.M. Roth, J.C. Drummond, and P.M. Patel Caveolin-1 expression is essential for N-methyl-d-aspartate receptor-mediated Src and extracellular signal-regulated kinase 1/2 activation and protection of primary neurons from ischemic cell death FASEB J. 22 2008 828 840
58. B.P. Head, J.N. Peart, M. Panneerselvam, T. Yokoyama, M.L. Pearn, I.R. Niesman, J.A. Bonds, J.M. Schilling, A. Miyanohara, J. Headrick, S.S. Ali, D.M. Roth, P.M. Patel, and H.H. Patel Loss of caveolin-1 accelerates neurodegeneration and aging PLoS One 5 2010 e15697
59. B.P. Head, Y. Hu, J.C. Finley, M.D. Saldana, J.A. Bonds, A. Miyanohara, I.R. Niesman, S.S. Ali, F. Murray, P.A. Insel, D.M. Roth, H.H. Patel, and P.M. Patel Neuron-targeted caveolin-1 protein enhances signaling and promotes arborization of primary neurons J. Biol. Chem. 286 2011 33310 33321
60. 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
61. A.P. Hibbert, B.M. Kramer, F.D. Miller, and D.R. Kaplan The localization, trafficking and retrograde transport of BDNF bound to p75NTR in sympathetic neurons Mol. Cell. Neurosci. 32 2006 387 402
62. H. Hibino, and Y. Kurachi Distinct detergent-resistant membrane microdomains (lipid rafts) respectively harvest K(+) and water transport systems in brain astroglia Eur. J. Neurosci. 26 2007 2539 2555
63. Q. Hou, Y. Huang, S. Amato, S.H. Snyder, R.L. Huganir, and H.Y. Man Regulation of AMPA receptor localization in lipid rafts Mol. Cell. Neurosci. 38 2008 213 223
64. Y.Z. Huang, S. Won, D.W. Ali, Q. Wang, M. Tanowitz, Q.S. Du, K.A. Pelkey, D.J. Yang, W.C. Xiong, M.W. Salter, and L. Mei Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses Neuron 26 2000 443 455
65. M. Jafurulla, S. Tiwari, and A. Chattopadhyay Identification of cholesterol recognition amino acid consensus (CRAC) motif in G-protein coupled receptors Biochem. Biophys. Res. Commun. 404 2011 569 573
66. L. Jiang, J. Fang, D.S. Moore, N.V. Gogichaeva, N.A. Galeva, M.L. Michaelis, and A. Zaidi Age-associated changes in synaptic lipid raft proteins revealed by two-dimensional fluorescence difference gel electrophoresis Neurobiol. Aging 31 2010 2146 2159
67. H. Kamiguchi The region-specific activities of lipid rafts during axon growth and guidance J. Neurochem. 98 2006 330 335
68. M.J. Kang, Y.H. Chung, C.I. Hwang, M. Murata, T. Fujimoto, I.H. Mook-Jung, C.I. Cha, and W.Y. Park Caveolin-1 upregulation in senescent neurons alters amyloid precursor protein processing Exp. Mol. Med. 38 2006 126 133
69. J.M. Karasinska, and M.R. Hayden Cholesterol metabolism in Huntington disease Nat. Rev. Neurol. 7 2011 561 572
70. M.J. Karnovsky, A.M. Kleinfeld, R.L. Hoover, and R.D. Klausner The concept of lipid domains in membranes J. Cell Biol. 94 1982 1 6
71. J.N. Kew, and J.A. Kemp Ionotropic and metabotropic glutamate receptor structure and pharmacology Psychopharmacology 179 2005 4 29
72. M. Ko, K. Zou, H. Minagawa, W. Yu, J.-S. Gong, and K. Yanagisawa Cholesterol-mediated neurite outgrowth is differently regulated between cortical and hippocampal neurons J. Biol. Chem. 280 2005 42759 42765
73. M.M. Kong, A. Hasbi, M. Mattocks, T. Fan, B.F. O'Dowd, and S.R. George Regulation of D1 dopamine receptor trafficking and signaling by caveolin-1 Mol. Pharmacol. 72 2007 1157 1170
74. Z. Korade, and A.K. Kenworthy Lipid rafts, cholesterol, and the brain Neuropharmacology 55 2008 1265 1273
75. A.R. Koudinov, and N.V. Koudinova Essential role for cholesterol in synaptic plasticity and neuronal degeneration FASEB J. 15 2001 1858 1860
76. L. Koyrakh, R. Lujan, J. Colon, C. Karschin, Y. Kurachi, A. Karschin, and K. Wickman Molecular and cellular diversity of neuronal G-protein-gated potassium channels J. Neurosci. 25 2005 11468 11478
77. P. Lajoie, and I.R. Nabi Regulation of raft-dependent endocytosis J. Cell Mol. Med. 11 2007 644 653
78. R.D. Lasley Adenosine receptors and membrane microdomains Biochim. Biophys. Acta 1808 2011 1284 1289
79. F.S. Lee, and M.V. Chao Activation of Trk neurotrophin receptors in the absence of neurotrophins Proc. Natl. Acad. Sci. U. S. A. 98 2001 3555 3560
80. S.J. Lee, U. Liyanage, P.E. Bickel, W. Xia, P.T. Lansbury Jr.; and K.S. Kosik A detergent-insoluble membrane compartment contains A beta in vivo Nat. Med. 4 1998 730 734
81. L. Li, D. Cao, H. Kim, R. Lester, and K. Fukuchi Simvastatin enhances learning and memory independent of amyloid load in mice Ann. Neurol. 60 2006 729 739
82. X. Li, D.R. Serwanski, C.P. Miralles, B.A. Bahr, and A.L. De Blas Two pools of triton X-100-insoluble GABA(A) receptors are present in the brain, one associated to lipid rafts and another one to the post-synaptic GABAergic complex J. Neurochem. 102 2007 1329 1345
83. A. Linetti, A. Fratangeli, E. Taverna, P. Valnegri, M. Francolini, V. Cappello, M. Matteoli, M. Passafaro, and P. Rosa Cholesterol reduction impairs exocytosis of synaptic vesicles J. Cell Sci. 123 2010 595 605
84. Y. Liu, T.P. Wong, M. Aarts, A. Rooyakkers, L. Liu, T.W. Lai, D.C. Wu, J. Lu, M. Tymianski, A.M. Craig, and Y.T. Wang NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo J. Neurosci. 27 2007 2846 2857
85. H.A. Lucero, and P.W. Robbins Lipid rafts-protein association and the regulation of protein activity Arch. Biochem. Biophys. 426 2004 208 224
86. J.H. Lv, L. He, and S.F. Sui Lipid rafts association of synaptotagmin I on synaptic vesicles Biochemistry (Mosc.) 73 2008 283 288
87. L. Ma, Y.Z. Huang, G.M. Pitcher, J.G. Valtschanoff, Y.H. Ma, L.Y. Feng, B. Lu, W.C. Xiong, M.W. Salter, R.J. Weinberg, and L. Mei Ligand-dependent recruitment of the ErbB4 signaling complex into neuronal lipid rafts J. Neurosci. 23 2003 3164 3175
88. J.L. Macdonald, and L.J. Pike A simplified method for the preparation of detergent-free lipid rafts J. Lipid Res. 46 2005 1061 1067
89. F. Magnani, C.G. Tate, S. Wynne, C. Williams, and J. Haase Partitioning of the serotonin transporter into lipid microdomains modulates transport of serotonin J. Biol. Chem. 279 2004 38770 38778
90. R.A. Mans, N. Chowdhury, D. Cao, L.L. McMahon, and L. Li Simvastatin enhances hippocampal long-term potentiation in C57BL/6 mice Neuroscience 166 2010 435 444
91. D. Marques-da-Silva, and C. Gutierrez-Merino L-type voltage-operated calcium channels, N-methyl-d-aspartate receptors and neuronal nitric-oxide synthase form a calcium/redox nano-transducer within lipid rafts Biochem. Biophys. Res. Commun. 420 2012 257 262
92. V. Martin, N. Fabelo, G. Santpere, B. Puig, R. Marin, I. Ferrer, and M. Diaz Lipid alterations in lipid rafts from Alzheimer's disease human brain cortex J. Alzheimers Dis. 19 2010 489 502
93. M. Masserini, P. Palestini, and M. Pitto Glycolipid-enriched caveolae and caveolae-like domains in the nervous system J. Neurochem. 73 1999 1 11
94. D.H. Mauch, K. Nagler, S. Schumacher, C. Goritz, E.C. Muller, A. Otto, and F.W. Pfrieger CNS synaptogenesis promoted by glia-derived cholesterol Science 294 2001 1354 1357
95. S. Meyer dos Santos, C.C. Weber, C. Franke, W.E. Muller, and G.P. Eckert Cholesterol: coupling between membrane microenvironment and ABC transporter activity Biochem. Biophys. Res. Commun. 354 2007 216 221
96. V. Michel, and M. Bakovic Lipid rafts in health and disease Biol. Cell 99 2007 129 140
97. C. Missale, S.R. Nash, S.W. Robinson, M. Jaber, and M.G. Caron Dopamine receptors: from structure to function Physiol. Rev. 78 1998 189 225
98. J. Mojsilovic-Petrovic, G.B. Jeong, A. Crocker, A. Arneja, S. David, D.S. Russell, and R.G. Kalb Protecting motor neurons from toxic insult by antagonism of adenosine A2a and Trk receptors J. Neurosci. 26 2006 9250 9263
99. N.M. Nathanson Synthesis, trafficking, and localization of muscarinic acetylcholine receptors Pharmacol. Ther. 119 2008 33 43
100. D.M. Navaroli, Z.H. Stevens, Z. Uzelac, L. Gabriel, M.J. King, L.M. Lifshitz, H.H. Sitte, and H.E. Melikian The plasma membrane-associated GTPase Rin interacts with the dopamine transporter and is required for protein kinase C-regulated dopamine transporter trafficking J. Neurosci. 31 2011 13758 13770
101. G. Neves, S.F. Cooke, and T.V. Bliss Synaptic plasticity, memory and the hippocampus: a neural network approach to causality Nat. Rev. Neurosci. 9 2008 65 75
102. P. North, and S. Fleischer Alteration of synaptic membrane cholesterol/phospholipid ratio using a lipid transfer protein. Effect on gamma-aminobutyric acid uptake J. Biol. Chem. 258 1983 1242 1253
103. S. Oldfield, J. Hancock, A. Mason, S. Hobson, D. Wynick, E. Kelly, A. Randall, and N. Marrion Receptor-mediated suppression of potassium currents requires colocalization within lipid rafts Mol. Pharmacol. 76 2009 1279 1289
104. J. Oshikawa, Y. Toya, T. Fujita, M. Egawa, J. Kawabe, S. Umemura, and Y. Ishikawa Nicotinic acetylcholine receptor α7 regulates cAMP signal within lipid rafts Am. J. Physiol. Cell. Physiol. 285 2003 C567 C574
105. D.F. Owens, and A.R. Kriegstein Is there more to GABA than synaptic inhibition? Nat. Rev. Neurosci. 3 2002 715 727
106. M.O. Parat The biology of caveolae: achievements and perspectives Int. Rev. Cell Mol. Biol. 273 2009 117 162
107. 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
108. L. Pelkmans, and A. Helenius Endocytosis via caveolae Traffic 3 2002 311 320
109. D.B. Pereira, and M.V. Chao The tyrosine kinase Fyn determines the localization of TrkB receptors in lipid rafts J. Neurosci. 27 2007 4859 4869
110. D.A. Persaud-Sawin, S. Lightcap, and G.J. Harry Isolation of rafts from mouse brain tissue by a detergent-free method J. Lipid Res. 50 2009 759 767
111. L.J. Pike Lipid rafts: bringing order to chaos J. Lipid Res. 44 2003 655 667
112. L.J. Pike Rafts defined: a report on the keystone symposium on lipid rafts and cell function J. Lipid Res. 47 2006 1597 1598
113. L.J. Pike The challenge of lipid rafts J. Lipid Res. 50 2009 S323 S328
114. P.A. Pousinha, M.J. Diógenes, J.A. Ribeiro, and A.M. Sebastião Triggering of BDNF facilitatory action on neuromuscular transmission by adenosine A2A receptors Neurosci. Lett. 404 2006 143 147
115. S. Pryor, G. McCaffrey, L.R. Young, and M.L. Grimes NGF causes TrkA to specifically attract microtubules to lipid rafts PLoS One 7 2012 e35163
116. T.J. Pucadyil, and A. Chattopadhyay Cholesterol modulates ligand binding and G-protein coupling to serotonin(1A) receptors from bovine hippocampus Biochim. Biophys. Acta 1663 2004 188 200
117. J. Rathenberg, J.T. Kittler, and S.J. Moss Palmitoylation regulates the clustering and cell surface stability of GABA(A) receptors Mol. Cell. Neurosci. 26 2004 251 257
118. R. Rajagopal, and M.V. Chao A role for Fyn in Trk receptor transactivation by G-protein-coupled receptor signaling Mol. Cell. Neurosci. 33 2006 36 46
119. U. Renner, K. Glebov, T. Lang, E. Papusheva, S. Balakrishnan, B. Keller, D. Richter, R. Jahn, and E. Ponimaskin Localization of the mouse 5-hydroxytryptamine1a receptor in lipid microdomains depends on its palmitoylation and is involved in receptor-mediated signaling Mol. Pharmacol. 72 2007 502 513
120. M. Renner, D. Choquet, and A. Triller Control of the postsynaptic membrane viscosity J. Neurosci. 29 2009 2926 2937
121. A.F. Schinder, and M. Poo The neurotrophin hypothesis for synaptic plasticity Trends Neurosci. 23 2000 639 645
122. A.M. Sebastião, A. de Mendonça, T. Moreira, and J.A. Ribeiro Activation of synaptic NMDA receptors by action potential-dependent release of transmitter during hypoxia impairs recovery of synaptic transmission on reoxygenation J. Neurosci. 21 2001 8564 8571
123. A.M. Sebastião, and J.A. Ribeiro Tuning and fine-tuning of synapses with adenosine Curr. Neuropharmacol. 7 2009 180 194
124. A.M. Sebastião, N. Assaife-Lopes, M.J. Diógenes, S.H. Vaz, and J.A. Ribeiro Modulation of brain-derived neurotrophic factor (BDNF) actions in the nervous system by adenosine A(2A) receptors and the role of lipid rafts Biochim. Biophys. Acta 1808 2011 1340 1349
125. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572
126. M. Simons, P. Keller, B. De Strooper, K. Beyreuther, C.G. Dotti, and K. Simons Cholesterol depletion inhibits the generation of beta-amyloid in hippocampal neurons Proc. Natl. Acad. Sci. U. S. A. 95 1998 6460 6464
127. K. Simons, and D. Toomre Lipid rafts and signal transduction Nat. Rev. Mol. Cell Biol. 1 2000 31 39
128. K. Simons, and M.J. Gerl Revitalizing membrane rafts: new tools and insights Nat. Rev. Mol. Cell Biol. 11 2010 688 699
129. S.J. Singer, and G.L. Nicolson The fluid mosaic model of the structure of cell membranes Science 175 1972 720 731
130. B. Sjögren, and P. Svenningsson Caveolin-1 affects serotonin binding and cell surface levels of human 5-HT7(a) receptors FEBS Lett. 581 2007 5115 5121
131. B. Sjögren, and P. Svenningsson Depletion of the lipid raft constituents, sphingomyelin and ganglioside, decreases serotonin binding at human 5-HT7(a) receptors in HeLa cells Acta Physiol. 190 2007 47 53
132. B. Sjögren, L. Csöregh, and P. Svenningsson Cholesterol reduction attenuates 5-HT1A receptor-mediated signaling in human primary neuronal cultures Naunyn Schmiedebergs Arch. Pharmacol. 378 2008 441 446
133. E.J. Smart, Y.S. Ying, C. Mineo, and R.G. Anderson A detergent-free method for purifying caveolae membrane from tissue culture cells Proc. Natl. Acad. Sci. U. S. A. 92 1995 10104 10108
134. K.S. Song, S. Li, T. Okamoto, L.A. Quilliam, M. Sargiacomo, and M.P. Lisanti Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae microdomains J. Biol. Chem. 271 1996 9690 9697
135. T.C. Südhof Calcium control of neurotransmitter release Cold Spring Harb. Perspect. Biol. 4 1 2012 Jan 1 a011353
136. S. Suzuki, T. Numakawa, K. Shimazu, H. Koshimizu, T. Hara, H. Hatanaka, L. Mei, B. Lu, and M. Kojima BDNF-induced recruitment of TrkB receptor into neuronal lipid rafts: roles in synaptic modulation J. Cell Biol. 167 2004 1205 1215
137. S. Suzuki, K. Kiyosue, S. Hazama, A. Ogura, M. Kashihara, T. Hara, H. Koshimizu, and M. Kojima Brain-derived neurotrophic factor regulates cholesterol metabolism for synapse development J. Neurosci. 27 2007 6417 6427
138. T. Suzuki Lipid rafts at postsynaptic sites: distribution, function and linkage to postsynaptic density Neurosci. Res. 44 2002 1 9
139. T. Suzuki, J. Zhang, S. Miyazawa, Q. Liu, M.R. Farzan, and W.D. Yao Association of membrane rafts and postsynaptic density: proteomics, biochemical, and ultrastructural analyses J. Neurochem. 119 2011 64 77
140. C.C. Swanwick, M.E. Shapiro, Z. Yi, K. Chang, and R.J. Wenthold NMDA receptors interact with flotillin-1 and -2, lipid raft-associated proteins FEBS Lett. 583 2009 1226 1230
141. Y. Takayasu, K. Takeuchi, R. Kumari, M.V. Bennett, R.S. Zukin, and A. Francesconi Caveolin-1 knockout mice exhibit impaired induction of mGluR-dependent long-term depression at CA3-CA1 synapses Proc. Natl. Acad. Sci. U. S. A. 107 2010 21778 21783
142. E. Taverna, E. Saba, J. Rowe, M. Francolini, F. Clementi, and P. Rosa Role of lipid microdomains in P/Q-type calcium channel (Cav2.1) clustering and function in presynaptic membranes J. Biol. Chem. 279 2004 5127 5134
143. E. Taverna, E. Saba, A. Linetti, R. Longhi, A. Jeromin, M. Righi, F. Clementi, and P. Rosa Localization of synaptic proteins involved in neurosecretion in different membrane microdomains J. Neurochem. 100 2007 664 677
144. L. Trovo, P.P. Van Veldhoven, M.G. Martin, and C.G. Dotti Sphingomyelin upregulation in mature neurons contributes to TrkB activity by Rac1 endocytosis J. Cell Sci. 124 2011 1308 1315
145. B.A. Tsui-Pierchala, M. Encinas, J. Milbrandt, and E.M. Johnson Jr. Lipid rafts in neuronal signaling and function Trends Neurosci. 25 2002 412 417
146. F. Vacca, S. Amadio, G. Sancesario, G. Bernardi, and C. Volonte P2X3 receptor localizes into lipid rafts in neuronal cells J. Neurosci. Res. 76 2004 653 661
147. M. Valenza, V. Leoni, A. Tarditi, C. Mariotti, I. Bjorkhem, S. Di Donato, and E. Cattaneo Progressive dysfunction of the cholesterol biosynthesis pathway in the R6/2 mouse model of Huntington's disease Neurobiol. Dis. 28 2007 133 142
148. J.E. Vance Lipid imbalance in the neurological disorder, Niemann-Pick C disease FEBS Lett. 580 2006 5518 5524
149. P.J. Voulalas, J. Schetz, and A.S. Undieh Differential subcellular distribution of rat brain dopamine receptors and subtype-specific redistribution induced by cocaine Mol. Cell. Neurosci. 46 2011 645 654
150. 2+ wave propagation in glial cells Cell Calcium 41 2007 155 167
151. R. Williamson, A.J. Thompson, M. Abu, A. Hye, A. Usardi, S. Lynham, B.H. Anderton, and D.P. Hanger Isolation of detergent resistant microdomains from cultured neurons: detergent dependent alterations in protein composition BMC Neurosci. 11 2010 120
152. C. Wu, S. Butz, Y. Ying, and R.G. Anderson Tyrosine kinase receptors concentrated in caveolae-like domains from neuronal plasma membrane J. Biol. Chem. 272 1997 3554 3559
153. E. Yamada The fine structure of the renal glomerulus of the mouse J. Biophys. Biochem. Cytol. 1 1955 551 566
154. M. Zervas, K. Dobrenis, and S.U. Walkley Neurons in Niemann-Pick disease type C accumulate gangliosides as well as unesterified cholesterol and undergo dendritic and axonal alterations J. Neuropathol. Exp. Neurol. 60 2001 49 64
155. D. Zhu, W.C. Xiong, and L. Mei Lipid rafts serve as a signaling platform for nicotinic acetylcholine receptor clustering J. Neurosci. 26 2006 4841 4851