Building excitable membranes: Lipid rafts and multiple controls on trafficking of electrogenic molecules

Neuroscientist

Volumn 18, Issue 1, 2012, Pages 70-81

  Pristerá, Alessandro ^a   Okuse, Kenji ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

ion pumps; ligand gated ion channels; lipid rafts; trafficking; voltage gated ion channels

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CAVEOLIN 3; GLYCOSYLPHOSPHATIDYLINOSITOL; GREEN FLUORESCENT PROTEIN; ION CHANNEL; LIGAND GATED ION CHANNEL; METHYL BETA CYCLODEXTRIN; MUSCARINIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; POSTSYNAPTIC DENSITY PROTEIN 95; SCAFFOLD PROTEIN; SEROTONIN; SODIUM ION; SPHINGOMYELIN PHOSPHODIESTERASE; TRANSIENT RECEPTOR POTENTIAL CHANNEL; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

AMINO TERMINAL SEQUENCE; CELL MEMBRANE; CYTOSKELETON; ENERGY EXPENDITURE; HUMAN; LIPID RAFT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW;

CELL MEMBRANE; ION CHANNELS; MEMBRANE MICRODOMAINS; NEURONS; PROTEIN TRANSPORT;

EID: 84856454195     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858410393977     Document Type: Review

References (69)

1. Alvarez de la Rosa D, Zhang P, Shao D, White F, Canessa CM. Functional implications of the localization and activity of acid-sensitive channels in rat peripheral nervous system. Proc Natl Acad Sci U S A. 2002 ; 99 (4). 2326-31 (Pubitemid 34169060)
2. Barnes NM, Hales TG, Lummis SC, Peters JA. The 5-HT3 receptor-the relationship between structure and function. Neuropharmacology. 2009 ; 56 (1). 273-84
3. Besshoh S, Bawa D, Teves L, Wallace MC, Gurd JW. 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. 2005 ; 93 (1). 186-94 (Pubitemid 40463528)
4. Besshoh S, Chen S, Brown IR, Gurd JW. Developmental changes in the association of NMDA receptors with lipid rafts. J Neurosci Res. 2007 ; 85 (9). 1876-83 (Pubitemid 47051476)
5. Bruses JL, Chauvet N, Rutishauser U. Membrane lipid rafts are necessary for the maintenance of the (alpha)7 nicotinic acetylcholine receptor in somatic spines of ciliary neurons. J Neurosci. 2001 ; 21 (2). 504-12 (Pubitemid 32107440)
6. Cao YQ. Voltage-gated calcium channels and pain. Pain. 2006 ; 126 (1-3). 5-9
7. Choquet D. Fast AMPAR trafficking for a high-frequency synaptic transmission. Eur J Neurosci. 2010 ; 32 (2). 250-60
8. Dalskov SM, Immerdal L, Niels-Christiansen LL, Hansen GH, Schousboe A, Danielsen EM. Lipid raft localization of GABA A receptor and Na+, K+-ATPase in discrete microdomain clusters in rat cerebellar granule cells. Neurochem Int. 2005 ; 46 (6). 489-99 (Pubitemid 40349597)
9. Davies A, Douglas L, Hendrich J, Wratten J, Tran Van Minh A, Foucault I. The calcium channel alpha2delta-2 subunit partitions with CaV2.1 into lipid rafts in cerebellum: implications for localization and function. J Neurosci. 2006 ; 26 (34). 8748-57 (Pubitemid 44319410)
10. Debanne D, Guerineau NC, Gahwiler BH, Thompson SM. Action-potential propagation gated by an axonal I(A)-like K+ conductance in hippocampus. Nature. 1997 ; 389 (6648). 286-9 (Pubitemid 27406642)
11. Delint-Ramirez I, Fernandez E, Bayes A, Kicsi E, Komiyama NH, Grant SG. In vivo composition of NMDA receptor signaling complexes differs between membrane subdomains and is modulated by PSD-95 and PSD-93. J Neurosci. 2010 ; 30 (24). 8162-70
12. Delint-Ramirez I, Salcedo-Tello P, Bermudez-Rattoni F. Spatial memory formation induces recruitment of NMDA receptor and PSD-95 to synaptic lipid rafts. J Neurochem. 2008 ; 106 (4). 1658-68
13. Delpire E. Cation-chloride cotransporters in neuronal communication. News Physiol Sci. 2000 ; 15: 309-12 (Pubitemid 33205102)
14. Dingledine R, Borges K, Bowie D, Traynelis SF. The glutamate receptor ion channels. Pharmacol Rev. 1999 ; 51 (1). 7-61 (Pubitemid 29113865)
15. Doczi MA, Morielli AD, Damon DH. Kv1. 3 channels in postganglionic sympathetic neurons: expression, function, and modulation. Am J Physiol Regul Integr Comp Physiol. 2008 ; 295 (3). R733-40
16. Eisensamer B, Uhr M, Meyr S, Gimpl G, Deiml T, Rammes G. Antidepressants and antipsychotic drugs colocalize with 5-HT3 receptors in raft-like domains. J Neurosci. 2005 ; 25 (44). 10198-206 (Pubitemid 41636216)
17. Eshcol JO, Harding AM, Hattori T, Costa V, Welsh MJ, Benson CJ. Acid-sensing ion channel 3 (ASIC3) cell surface expression is modulated by PSD-95 within lipid rafts. Am J Physiol Cell Physiol. 2008 ; 295 (3). C732-9
18. Fujimoto T, Kogo H, Ishiguro K, Tauchi K, Nomura R. Caveolin-2 is targeted to lipid droplets, a new "membrane domain" in the cell. J Cell Biol. 2001 ; 152 (5). 1079-85 (Pubitemid 34286082)
19. Gazula VR, Strumbos JG, Mei X, Chen H, Rahner C, Kaczmarek LK. Localization of Kv1.3 channels in presynaptic terminals of brainstem auditory neurons. J Comp Neurol. 2010 ; 518 (16). 3205-20
20. Gutman GA, Chandy KG, Grissmer S, Lazdunski M, McKinnon D, Pardo LA. International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels. Pharmacol Rev. 2005 ; 57 (4). 473-508 (Pubitemid 43036437)
21. Hartmann AM, Blaesse P, Kranz T, Wenz M, Schindler J, Kaila K. Opposite effect of membrane raft perturbation on transport activity of KCC2 and NKCC1. J Neurochem. 2009 ; 111 (2). 321-31
22. Hering H, Lin CC, Sheng M. Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J Neurosci. 2003 ; 23 (8). 3262-71 (Pubitemid 36531967)
23. Hoffman DA, Johnston D. Downregulation of transient K+ channels in dendrites of hippocampal CA1 pyramidal neurons by activation of PKA and PKC. J Neurosci. 1998 ; 18 (10). 3521-8 (Pubitemid 28225660)
24. Hou Q, Huang Y, Amato S, Snyder SH, Huganir RL, Man HY. Regulation of AMPA receptor localization in lipid rafts. Mol Cell Neurosci. 2008 ; 38 (2). 213-23
25. Kessels HW, Malinow R. Synaptic AMPA receptor plasticity and behavior. Neuron. 2009 ; 61 (3). 340-50
26. Kupper J, Prinz AA, Fromherz P. Recombinant Kv1.3 potassium channels stabilize tonic firing of cultured rat hippocampal neurons. Pflugers Arch. 2002 ; 443 (4). 541-7 (Pubitemid 34185058)
27. Lim ST, Antonucci DE, Scannevin RH, Trimmer JS. A novel targeting signal for proximal clustering of the Kv2.1 K+ channel in hippocampal neurons. Neuron. 2000 ; 25 (2). 385-97
28. Liu M, Huang W, Wu D, Priestley JV. TRPV1, but not P2X, requires cholesterol for its function and membrane expression in rat nociceptors. Eur J Neurosci. 2006 ; 24 (1). 1-6 (Pubitemid 44050659)
29. Long SB, Campbell EB, Mackinnon R. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science. 2005 ; 309 (5736). 897-903 (Pubitemid 41099919)
30. Malik-Hall M, Poon WY, Baker MD, Wood JN, Okuse K. Sensory neuron proteins interact with the intracellular domains of sodium channel NaV1.8. Brain Res Mol Brain Res. 2003 ; 110 (2). 298-304 (Pubitemid 36184702)
31. Martens JR, Navarro-Polanco R, Coppock EA, Nishiyama A, Parshley L, Grobaski TD. Differential targeting of Shaker-like potassium channels to lipid rafts. J Biol Chem. 2000 ; 275 (11). 7443-6 (Pubitemid 30159634)
32. Momin A, Wood JN. Sensory neuron voltage-gated sodium channels as analgesic drug targets. Curr Opin Neurobiol. 2008 ; 18 (4). 383-8
33. Morenilla-Palao C, Pertusa M, Meseguer V, Cabedo H, Viana F. Lipid raft segregation modulates TRPM8 channel activity. J Biol Chem. 2009 ; 284 (14). 9215-24
34. North RA. Molecular physiology of P2X receptors. Physiol Rev. 2002 ; 82 (4). 1013-67
35. Nothdurfter C, Tanasic S, Di Benedetto B, Rammes G, Wagner EM, Kirmeier T. Impact of lipid raft integrity on 5-HT3 receptor function and its modulation by antidepressants. Neuropsychopharmacology. 2010 ; 35 (7). 1510-9
36. Ogawa Y, Rasband MN. Proteomic analysis of optic nerve lipid rafts reveals new paranodal proteins. J Neurosci Res. 2009 ; 87 (15). 3502-10
37. Okuse K. Pain signalling pathways: from cytokines to ion channels. Int J Biochem Cell Biol. 2007 ; 39 (3). 490-6 (Pubitemid 46096803)
38. Okuse K, Chaplan SR, McMahon SB, Luo ZD, Calcutt NA, Scott BP, Akopian AN, Wood JN. Regulation of expression of the sensory neuron-specific sodium channel SNS in inflammatory and neuropathic pain. Mol Cell Neurosci. 1997 ; 10 (3-4). 196-207 (Pubitemid 28144510)
39. Okuse K, Malik-Hall M, Baker MD, Poon WY, Kong H, Chao MV, Wood JN. Annexin II light chain regulates sensory neuron-specific sodium channel expression. Nature. 2002 ; 417 (6889). 653-6 (Pubitemid 34614824)
40. Oldfield S, Hancock J, Mason A, Hobson SA, Wynick D, Kelly E. Receptor-mediated suppression of potassium currents requires colocalization within lipid rafts. Mol Pharmacol. 2009 ; 76 (6). 1279-89
41. Pato C, Stetzkowski-Marden F, Gaus K, Recouvreur M, Cartaud A, Cartaud J. Role of lipid rafts in agrin-elicited acetylcholine receptor clustering. Chem Biol Interact. 2008 ; 175 (1-3). 64-7
42. Poliak S, Peles E. The local differentiation of myelinated axons at nodes of Ranvier. Nat Rev Neurosci. 2003 ; 4 (12). 968-80 (Pubitemid 37486673)
43. Poon WY, Malik-Hall M, Wood JN, Okuse K. Identification of binding domains in the sodium channel Na(V)1.8 intracellular N-terminal region and annexin II light chain p11. FEBS Lett. 2004 ; 558 (1-3). 114-8 (Pubitemid 38167420)
44. Roura-Ferrer M, Sole L, Oliveras A, Dahan R, Bielanska J, Villarroel A. Impact of KCNE subunits on KCNQ1 (Kv7.1) channel membrane surface targeting. J Cell Physiol. 2010 ; 225 (3). 692-700
45. Rush AM, Cummins TR, Waxman SG. Multiple sodium channels and their roles in electrogenesis within dorsal root ganglion neurons. J Physiol 579 Pt. 2007 ; 1: 1-14
46. Pristerá A, Okuse K. Association of NaV1.8 with lipid rafts in rat dorsal root ganglia neuron. Presented at the 12th World Congress of Pain (PH340) ; 2008 ; 2008..
47. Pristerá A, Okuse K. Action potential propagation in unmyelinated axons of rat sensory neurons requires association of NaV 1.8 channels with the lipid rafts. Presented at the Society for Neuroscience (820.9/C43) ; 2009 ; 2009..
48. Santha P, Oszlacs O, Dux M, Dobos I, Jancso G. Inhibition of glucosylceramide synthase reversibly decreases the capsaicin-induced activation and TRPV1 expression of cultured dorsal root ganglion neurons. Pain. 2010 ; 150 (1). 103-12
49. Schafer DP, Bansal R, Hedstrom KL, Pfeiffer SE, Rasband MN. Does paranode formation and maintenance require partitioning of neurofascin 155 into lipid rafts?. J Neurosci. 2004 ; 24 (13). 3176-85 (Pubitemid 38451884)
50. Scheiffele P, Roth MG, Simons K. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J. 1997 ; 16 (18). 5501-8 (Pubitemid 27399842)
51. Seno K, Kishimoto M, Abe M, Higuchi Y, Mieda M, Owada Y. Light- and guanosine 5'-3-O-(thio)triphosphate-sensitive localization of a G protein and its effector on detergent-resistant membrane rafts in rod photoreceptor outer segments. J Biol Chem. 2001 ; 276 (24). 20813-6
52. Shao D, Baker MD, Abrahamsen B, Rugiero F, Malik-Hall M, Poon WY. A multi PDZ-domain protein Pdzd2 contributes to functional expression of sensory neuron-specific sodium channel Na(V)1.8. Mol Cell Neurosci. 2009 ; 42 (3). 219-25
53. Simons K, Gerl MJ. Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol. 2010 ; 11 (10). 688-99
54. Simons K, Ikonen E. Functional rafts in cell membranes. Nature. 1997 ; 387 (6633). 569-72 (Pubitemid 27248754)
55. Sole L, Roura-Ferrer M, Perez-Verdaguer M, Oliveras A, Calvo M, Fernandez-Fernandez JM. KCNE4 suppresses Kv1.3 currents by modulating trafficking, surface expression and channel gating. J Cell Sci 122 Pt. 2009 ; 20: 3738-48
56. Stahl WL, Harris WE. Na+,K+-ATPase: structure, function, and interactions with drugs. Adv Neurol. 1986 ; 44: 681-93
57. Susuki K, Baba H, Tohyama K, Kanai K, Kuwabara S, Hirata K. Gangliosides contribute to stability of paranodal junctions and ion channel clusters in myelinated nerve fibers. Glia. 2007 ; 55 (7). 746-57 (Pubitemid 46663027)
58. Suzuki T, Ito J, Takagi H, Saitoh F, Nawa H, Shimizu H. Biochemical evidence for localization of AMPA-type glutamate receptor subunits in the dendritic raft. Brain Res Mol Brain Res. 2001 ; 89 (1-2). 20-8 (Pubitemid 32322731)
59. Swanwick RS, Pristerá A, Okuse K. The trafficking of Na(V)1.8. Neurosci Lett. 2010 ; 486 (2). 78-83
60. Swanwick CC, Shapiro ME, Vicini S, Wenthold RJ. Flotillin-1 promotes formation of glutamatergic synapses in hippocampal neurons. Dev Neurobiol. 2010 ; 70 (13). 875-83
61. Swanwick CC, Shapiro ME, Yi Z, Chang K, Wenthold RJ. NMDA receptors interact with flotillin-1 and -2, lipid raft-associated proteins. FEBS Lett. 2009 ; 583 (8). 1226-30
62. Szoke E, Borzsei R, Toth DM, Lengl O, Helyes Z, Sandor Z. Effect of lipid raft disruption on TRPV1 receptor activation of trigeminal sensory neurons and transfected cell line. Eur J Pharmacol. 2010 ; 628 (1-3). 67-74
63. Vacca F, Amadio S, Sancesario G, Bernardi G, Volonte C. P2X3 receptor localizes into lipid rafts in neuronal cells. J Neurosci Res. 2004 ; 76 (5). 653-61 (Pubitemid 38691788)
64. Watanabe M, Wake H, Moorhouse AJ, Nabekura J. Clustering of neuronal K+-Cl- cotransporters in lipid rafts by tyrosine phosphorylation. J Biol Chem. 2009 ; 284 (41). 27980-8
65. Waxman SG. The neuron as a dynamic electrogenic machine: modulation of sodium-channel expression as a basis for functional plasticity in neurons. Philos Trans R Soc Lond B Biol Sci. 2000 ; 355 (1394). 199-213 (Pubitemid 30144106)
66. Wong W, Schlichter LC. Differential recruitment of Kv1.4 and Kv4.2 to lipid rafts by PSD-95. J Biol Chem. 2004 ; 279 (1). 444-52 (Pubitemid 38044845)
67. Yamada E. The fine structure of the gall bladder epithelium of the mouse. J Biophys Biochem Cytol. 1955 ; 1 (5). 445-58
68. Yarbrough TL, Lu T, Lee HC, Shibata EF. Localization of cardiac sodium channels in caveolin-rich membrane domains: regulation of sodium current amplitude. Circ Res. 2002 ; 90 (4). 443-9 (Pubitemid 34633914)
69. Zhu D, Xiong WC, Mei L. Lipid rafts serve as a signaling platform for nicotinic acetylcholine receptor clustering. J Neurosci. 2006 ; 26 (18). 4841-51 (Pubitemid 44315325)