Receptor-mediated suppression of potassium currents requires colocalization within lipid rafts

Molecular Pharmacology

Volumn 76, Issue 6, 2009, Pages 1279-1289

  Oldfield, Susan ^a   Hancock, Jane ^a   Mason, Angharad ^a   Hobson, Sally A ^a   Wynick, David ^a   Kelly, Eamonn ^a   Randall, Andrew D ^a   Marrion, Neil V ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; METHYL BETA CYCLODEXTRIN; MUSCARINIC M1 RECEPTOR; MUSCARINIC M3 RECEPTOR; POTASSIUM CHANNEL KCNQ2; POTASSIUM CHANNEL KCNQ3;

ARTICLE; CALCIUM CELL LEVEL; CELL STRAIN HEK293; HUMAN; LIPID MEMBRANE; LIPID RAFT; NONHUMAN; NUCLEOTIDE SEQUENCE; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SPINAL CORD NERVE CELL; SPINAL GANGLION;

ANIMALS; BLOTTING, WESTERN; CALCIUM; CARBACHOL; CELL LINE; CHOLINERGIC AGENTS; GANGLIA, SPINAL; HUMANS; KCNQ2 POTASSIUM CHANNEL; KCNQ3 POTASSIUM CHANNEL; MEMBRANE MICRODOMAINS; MEMBRANE POTENTIALS; MICE; MUSCARINE; OXOTREMORINE; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS; RECEPTOR, MUSCARINIC M1; RECEPTOR, MUSCARINIC M3; RECEPTORS, MUSCARINIC;

EID: 73149093009     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.109.058008     Document Type: Article

References (45)

1. Allen JA, Halverson-Tamboli RA, and Rasenick MM (2007) Lipid raft microdomains and neurotransmitter signalling. Nat Rev Neurosci 8:128-140.
2. Ancellin N, Preisser L, Le Maout S, Barbado M, Créminon C, Corman B, and Morel A (1999) Homologous and heterologous phosphorylation of the vasopressin V1a receptor. Cell Signal 11:743-751.
3. 2+ current and M current in rat sympathetic neurons. Proc Natl Acad Sci U S A 89:9544-9548.
4. + current in a vertebrate neurone. Nature 283:673-676.
5. Calaghan S, Kozera L, and White E (2008) Compartmentalisation of cAMP-dependent signalling by caveolae in the adult cardiac myocyte. J Mol Cell Cardiol 45:88-92.
6. Chamberlain LH (2004) Detergents as tools for the purification and classification of lipid rafts. FEBS Lett 559:1-5.
7. Cooper EC, Aldape KD, Abosch A, Barbaro NM, Berger MS, Peacock WS, Jan YN, and Jan LY (2000) Colocalization and coassembly of two human brain M-type potassium channel subunits that are mutated in epilepsy. Proc Natl Acad Sci U S A 97:4914-4919.
8. Davies A, Douglas L, Hendrich J, Wratten J, Tran Van Minh A, Foucault I, Koch D, Pratt WS, Saibil HR, and Dolphin AC (2006) The calcium channel alpha2delta-2 subunit partitions with CaV2.1 into lipid rafts in cerebellum: implications for localization and function. J Neurosci 26:8748-8757.
9. Dunlop J, Lock T, Jow B, Sitzia F, Grauer S, Jow F, Kramer A, Bowlby MR, Randall A, Kowal D, et al. (2009) Old and new pharmacology: positive allosteric modulation of the α7 nicotinic acetylcholine receptor by the 5-hydroxytryptamine(2B/C) receptor antagonist SB-206553 (3,5-dihydro-5-methyl- N-3-pyridinylbenzo[1,2-b:4,5-b′]di pyrrole-1(2H)-carboxamide). J Pharmacol Exp Ther 328:766-776.
10. Fontana DJ, Inouye GT, and Johnson RM (1994) Linopirdine (DuP 996) improves performance in several tests of learning and memory by modulation of cholinergic neurotransmission. Pharmacol Biochem Behav 49:1075-1082.
11. Holmes FE, Mahoney S, King VR, Bacon A, Kerr NC, Pachnis V, Curtis R, Priestley JV, and Wynick D (2000) Targeted disruption of the galanin gene reduces the number of sensory neurons and their regenerative capacity. Proc Natl Acad Sci U S A 97:11563-11568.
12. Hur EM, Park YS, Lee BD, Jang IH, Kim HS, Kim TD, Suh PG, Ryu SH, and Kim KT (2004) Sensitization of epidermal growth factor-induced signaling by bradykinin is mediated by c-Src. Implications for a role of lipid microdomains. J Biol Chem 279:5852-5860.
13. + channels. J Gen Physiol 133:347-359.
14. 2-adrenoceptors. J Pharmacol Exp Ther. doi: 10.1124/ jpet.109.153619.
15. Klopfenstein DR, Tomishige M, Stuurman N, and Vale RD (2002) Role of phosphatidylinositol(4,5)bisphosphate organization in membrane transport by the Unc104 kinesin motor. Cell 109:347-358.
16. Langmead CJ, Austin NE, Branch CL, Brown JT, Buchanan KA, Davies CH, Forbes IT, Fry VA, Hagan JJ, Herdon HJ, et al. (2008) Characterization of a CNS penetrant, selective M1 muscarinic receptor agonist, 77-LH-28-1. Br J Pharmacol 154:1104-1115.
17. + channel open probability by phosphatidylinositol 4,5-bisphosphate. J Neurosci 25:9825-9835.
18. Marrion NV, Smart TG, Marsh SJ, and Brown DA (1989) Muscarinic suppression of the M-current in the rat sympathetic ganglion is mediated by receptors of the M1-subtype. Br J Pharmacol 98:557-573.
19. Marrion NV (1997) Control of M-current. Annu Rev Physiol 59:483-504.
20. Martens JR, Navarro-Polanco R, Coppock EA, Nishiyama A, Parshley L, Grobaski TD, and Tamkun MM (2000) Differential targeting of Shaker-like potassium channels to lipid rafts. J Biol Chem 275:7443-7446.
21. + channels to distinct lipid raft populations. Targeting of Kv1.5 to caveolae. J Biol Chem 276:8409-8414.
22. Miceli F, Soldovieri MV, Martire M, and Taglialatela M (2008) Molecular pharmacology and therapeutic potential of neuronal Kv7-modulating drugs. Curr Opin Pharmacol 8:65-74.
23. Mundell SJ and Benovic JL (2000) Selective regulation of endogenous G protein-coupled receptors by arrestins in HEK293 cells. J Biol Chem 275:12900-12908.
24. Munro S (2003) Lipid rafts: elusive or illusive? Cell 115:377-388.
25. Passmore GM, Selyanko AA, Mistry M, Al-Qatari M, Marsh SJ, Matthews EA, Dickenson AH, Brown TA, Burbidge SA, Main M, et al. (2003) KCNQ/M currents in sensory neurons: significance for pain therapy. J Neurosci 23:7227-7236.
26. Pepeu G and Giovannini MG (2009) Cholinesterase inhibitors and beyond. Curr Alzheimer Res 6:86-96.
27. Pike LJ and Casey L (1996) Localization and turnover of phosphatidylinositol 4,5-bisphosphate in caveolin-enriched membrane domains. J Biol Chem 271:26453-26456.
28. Prole DL, Lima PA, and Marrion NV (2003) Mechanisms underlying modulation of neuronal KCNQ2/KCNQ3 potassium channels by extracellular protons. J Gen Physiol 122:775-793.
29. Raber J, Huang Y, and Ashford JW (2004) ApoE genotype accounts for the vast majority of AD risk and AD pathology. Neurobiol Aging 25:641-650.
30. Riddell DR, Zhou H, Atchison K, Warwick HK, Atkinson PJ, Jefferson J, Xu L, Aschmies S, Kirksey Y, Hu Y, et al. (2008) Impact of apolipoprotein E (ApoE) polymorphism on brain ApoE levels. J Neurosci 28:11445-11453.
31. 2 signaling in lipid domains: a critical re-evaluation. EMBO J 24:1664-1673.
32. Saeki K, Fukuyama S, Ayada T, Nakaya M, Aki D, Takaesu G, Hanada T, Matsumura Y, Kobayashi T, Nakagawa R, et al. (2009) A major lipid raft protein raftlin modulates T cell receptor signaling and enhances th17-mediated autoimmune responses. J Immunol 182:5929-5937.
33. Selyanko AA, Hadley JK, Wood IC, Abogadie FC, Jentsch TJ, and Brown DA (2000) Inhibition of KCNQ1-4 potassium channels expressed in mammalian cells via M1 muscarinic acetylcholine receptors. J Physiol 522:349-355.
34. Sheets ED, Holowka D, and Baird B (1999a) Membrane organization in immunoglobulin E receptor signaling. Curr Opin Chem Biol 3:95-99.
35. Sheets ED, Holowka D, and Baird B (1999b) Critical role for cholesterol in Lynmediated tyrosine phosphorylation of FcepsilonRI and their association with detergent-resistant membranes. J Cell Biol 145:877-887.
36. Silva WI, Maldonado HM, Lisanti MP, Devellis J, Chompré G, Mayol N, Ortiz M, Velázquez G, Maldonado A, and Montalvo J (1999) Identification of caveolae and caveolin in C6 glioma cells. Int J Dev Neurosci 17:705-714.
37. Simons K and Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1:31-39.
38. Sjögren B, Csöregh L, and Svenningsson P (2008) Cholesterol reduction attenuates 5-HT1A receptor-mediated signaling in human primary neuronal cultures. Naunyn Schmiedebergs Arch Pharmacol 378:441-446.
39. Suh BC and Hille B (2002) Recovery from muscarinic modulation of M current channels requires phosphatidylinositol 4,5-bisphosphate synthesis. Neuron 35: 507-520.
40. 2 is a necessary cofactor for ion channel function: how and why? Annu Rev Biophys 37:175-195.
41. 2+ elevation in cultured rat dorsal root ganglia cells. Naunyn Schmiedebergs Arch Pharmacol 375:293-301.
42. Tillman TS and Cascio M (2003) Effects of membrane lipids on ion channel structure and function. Cell Biochem Biophys 38:161-190.
43. Wang HS, Pan Z, Shi W, Brown BS, Wymore RS, Cohen IS, Dixon JE, and McKinnon D (1998) KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science 282:1890-1893.
44. Wang D, Wang W, Duan Y, Sun Y, Wang Y, and Huang P (2008) Functional coupling of Gs and CFTR is independent of their association with lipid rafts in epithelial cells. Pflugers Arch 456:929-938.
45. Zhang H, Craciun LC, Mirshahi T, Rohács T, Lopes CM, Jin T, and Logothetis DE (2003) PIP(2) activates KCNQ channels, and its hydrolysis underlies receptor-mediated inhibition of M currents. Neuron 37:963-975.