Gating the pore of potassium leak channels

European Biophysics Journal

Volumn 39, Issue 1, 2009, Pages 61-73

  Cohen, Asi ^a   Ben Abu, Yuval ^a   Zilberberg, Noam ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Activation gate; C type inactivation; Gating; KCNK0; TREK 1; Two pore domain potassium channels

Indexed keywords

MEMBRANE PROTEIN; PHORBOL 13 ACETATE 12 MYRISTATE; POTASSIUM CHANNEL; PROTEIN KINASE C ACTIVATOR; PROTEIN KINASE INHIBITOR; STAUROSPORINE; ZINC;

CHANNEL GATING; CONFORMATIONAL TRANSITION; ION CONDUCTANCE; MEMBRANE CONDUCTANCE; MEMBRANE ELECTROPHYSIOLOGY; MEMBRANE POTENTIAL; NONHUMAN; PROTEIN CONFORMATION; PROTEIN STRUCTURE; REVIEW;

ANIMALS; HUMANS; HYDROGEN-ION CONCENTRATION; ION CHANNEL GATING; POTASSIUM CHANNELS, TANDEM PORE DOMAIN;

EID: 70450279016     PISSN: 01757571     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00249-009-0457-6     Document Type: Review

References (99)

1. + channel involved in polymodal pain perception EMBO J 25 2368 2376 10.1038/sj.emboj.7601116 10.1038/sj.emboj.7601116 16675954 (Pubitemid 44012220)
2. Armstrong CM (2003) Voltage-gated K channels. Sci STKE 2003:re10. doi: 10.1126/stke.2003.188.re10
3. PH Backx E Marban 1993 Background potassium current active during the plateau of the action potential in guinea pig ventricular myocytes Circ Res 72 890 900 8443875
4. O Barel SA Shalev R Ofir A Cohen J Zlotogora Z Shorer G Mazor G Finer S Khateeb N Zilberberg OS Birk 2008 Maternally inherited Birk Barel mental retardation dysmorphism syndrome caused by a mutation in the genomically imprinted potassium channel KCNK9 Am J Hum Genet 83 193 199 10.1016/j.ajhg.2008. 07.010 10.1016/j.ajhg.2008.07.010 18678320
5. +: a tale of two inactivation mechanisms Neuron 15 951 960 10.1016/0896-6273(95)90185-X 10.1016/0896-6273(95)90185-X 7576643
6. + channel Science 271 653 656 10.1126/science.271.5249.653 10.1126/science.271.5249.653 8571129
7. + channel gates underlies distinct roles in electrical signaling Nat Struct Mol Biol 16 71 79 10.1038/nsmb.1525 10.1038/nsmb.1525 19098918
8. F Bezanilla CM Armstrong 1972 Negative conductance caused by entry of sodium and cesium ions into the potassium channels of squid axons J Gen Physiol 60 588 608 10.1085/jgp.60.5.588 10.1085/jgp.60.5.588 4644327
9. D Bockenhauer N Zilberberg SA Goldstein 2001 KCNK2: reversible conversion of a hippocampal potassium leak into a voltage-dependent channel Nat Neurosci 4 486 491 11319556
10. SG Brickley MI Aller C Sandu EL Veale FG Alder H Sambi A Mathie W Wisden 2007 TASK-3 two-pore domain potassium channels enable sustained high-frequency firing in cerebellar granule neurons J Neurosci 27 9329 9340 10.1523/JNEUROSCI.1427-07.2007 10.1523/JNEUROSCI.1427-07.2007 17728447 (Pubitemid 47358198)
11. KJ Buckler BA Williams E Honore 2000 An oxygen-, acid- and anaesthetic-sensitive TASK-like background potassium channel in rat arterial chemoreceptor cells J Physiol 525 135 142 10.1111/j.1469-7793.2000.00135.x 10.1111/j.1469-7793.2000.00135.x 10811732
12. + channel TREK-1 EMBO J 24 44 53 10.1038/sj.emboj.7600494 10.1038/sj.emboj.7600494 15577940 (Pubitemid 40188462)
13. 2 and other membrane phospholipids Pflugers Arch 455 97 103 10.1007/s00424-007-0250-2 10.1007/s00424-007-0250-2 17384962 (Pubitemid 47403975)
14. X Chen EM Talley N Patel A Gomis WE McIntire B Dong F Viana JC Garrison DA Bayliss 2006 Inhibition of a background potassium channel by Gq protein alpha-subunits Proc Natl Acad Sci USA 103 3422 3427 10.1073/pnas.0507710103 10.1073/pnas.0507710103 16492788 (Pubitemid 43346484)
15. M Chesler 2003 Regulation and modulation of pH in the brain Physiol Rev 83 1183 1221 14506304
16. S Choe 2002 Potassium channel structures Nat Rev Neurosci 3 115 121 10.1038/nrn727 10.1038/nrn727 11836519 (Pubitemid 135706580)
17. + channels Proc Natl Acad Sci USA 88 5092 5095 10.1073/pnas.88.12.5092 10.1073/pnas.88.12.5092 2052588
18. CE Clarke EL Veale PJ Green HJ Meadows A Mathie 2004 Selective block of the human 2-P domain potassium channel, TASK-3, and the native leak potassium current, IKSO, by zinc J Physiol 560 51 62 10.1113/jphysiol.2004.070292 10.1113/jphysiol.2004.070292 15284350 (Pubitemid 39406016)
19. + channels J Physiol 573 291 304 10.1113/jphysiol.2006.108332 10.1113/jphysiol.2006.108332 16556651 (Pubitemid 43871049)
20. CE Clarke EL Veale K Wyse JI Vandenberg A Mathie 2008 The M1P1 loop of TASK3 K2P channels apposes the selectivity filter and influences channel function J Biol Chem 283 16985 16992 10.1074/jbc.M801368200 10.1074/jbc. M801368200 18417474
21. + channels is regulated by extracellular charges Biophys J 87 2407 2418 10.1529/biophysj.103.039073 10.1529/biophysj.103. 039073 15454439 (Pubitemid 41071339)
22. A Cohen N Zilberberg 2006 Fluctuations in Xenopus oocytes protein phosphorylation levels during two-electrode voltage clamp measurements J Neurosci Methods 153 62 70 10.1016/j.jneumeth.2005.10.005 10.1016/j.jneumeth. 2005.10.005 16293314
23. 2P2.1 channel gating: facilitation of C-type gating by protonation of extracellular histidine residues J Biol Chem 283 19448 19455 10.1074/jbc.M801273200 10.1074/jbc.M801273200 18474599
24. 2P2.1 channel Mol Cell Neurosci 40 382 389 10.1016/j.mcn.2008.12.004 10.1016/j.mcn.2008.12.004 19130888
25. JF Cordero-Morales LG Cuello Y Zhao V Jogini DM Cortes B Roux E Perozo 2006 Molecular determinants of gating at the potassium-channel selectivity filter Nat Struct Mol Biol 13 311 318 10.1038/nsmb1069 10.1038/nsmb1069 16532009 (Pubitemid 43873501)
26. JF Cordero-Morales V Jogini A Lewis V Vasquez DM Cortes B Roux E Perozo 2007 Molecular driving forces determining potassium channel slow inactivation Nat Struct Mol Biol 14 1062 1069 10.1038/nsmb1309 10.1038/nsmb1309 17922012 (Pubitemid 350060332)
27. A Dedman R Sharif-Naeini JH Folgering F Duprat A Patel E Honore 2009 The mechano-gated K(2P) channel TREK-1 Eur Biophys J 38 293 303 10.1007/s00249-008- 0318-8 10.1007/s00249-008-0318-8 18369610
28. JW Deitmer CR Rose 1996 pH regulation and proton signalling by glial cells Prog Neurobiol 48 73 103 10.1016/0301-0082(95)00039-9 10.1016/0301- 0082(95)00039-9 8737439 (Pubitemid 26126312)
29. F Doring H Scholz RP Kuhnlein A Karschin E Wischmeyer 2006 Novel Drosophila two-pore domain K channels: rescue of channel function by heteromeric assembly Eur J Neurosci 24 2264 2274 10.1111/j.1460-9568.2006.05102.x 10.1111/j.1460-9568.2006.05102.x 17074048 (Pubitemid 44622347)
30. + conduction and selectivity Science 280 69 77 10.1126/science.280. 5360.69 10.1126/science.280.5360.69 9525859 (Pubitemid 28169082)
31. + channel to sense external pH variations near physiological pH EMBO J 16 5464 5471 10.1093/emboj/16.17.5464 10.1093/emboj/16.17.5464 9312005 (Pubitemid 27380153)
32. + channels TREK-1 and TRAAK Mol Pharmacol 57 906 912 10779373
33. C Eduljee TW Claydon V Viswanathan D Fedida SJ Kehl 2007 SCAM analysis reveals a discrete region of the pore turret that modulates slow inactivation in Kv1.5 Am J Physiol Cell Physiol 292 C1041 C1052 10.1152/ajpcell.00274.2006 10.1152/ajpcell.00274.2006 16956964 (Pubitemid 46440397)
34. + channel EMBO J 15 6854 6862 9003761
35. 2P channels and their role in general anaesthesia and neuroprotection Trends Pharmacol Sci 25 601 608 10.1016/j.tips.2004.09.003 10.1016/j.tips.2004.09.003 15491783 (Pubitemid 39371151)
36. + channels Biochem Biophys Res Commun 282 249 256 10.1006/bbrc.2001.4562 10.1006/bbrc.2001.4562 11263999 (Pubitemid 32924371)
37. SA Goldstein D Bockenhauer I O'Kelly N Zilberberg 2001 Potassium leak channels and the KCNK family of two-P-domain subunits Nat Rev Neurosci 2 175 184 10.1038/35058574 10.1038/35058574 11256078 (Pubitemid 33673370)
38. + channels in human T lymphocytes Biophys J 55 203 206 10.1016/S0006-3495(89)82793-6 10.1016/S0006-3495(89)82793-6 2784693
39. A Gurney B Manoury 2009 Two-pore potassium channels in the cardiovascular system Eur Biophys J 38 305 318 10.1007/s00249-008-0326-8 10.1007/s00249-008- 0326-8 18449536
40. + channel, TALK-1 Am J Physiol Cell Physiol 285 C529 C538 12724142
41. C Heurteaux G Lucas N Guy M El Yacoubi S Thummler XD Peng F Noble N Blondeau C Widmann M Borsotto G Gobbi JM Vaugeois G Debonnel M Lazdunski 2006 Deletion of the background potassium channel TREK-1 results in a depression-resistant phenotype Nat Neurosci 9 1134 1141 10.1038/nn1749 10.1038/nn1749 16906152 (Pubitemid 44306306)
42. Hille B (2001) Ion channels of excitable membranes, 3rd edn. Sinauer Associates Press, Sanderland
43. 2P channels: focus on TREK1 Nat Rev Neurosci 8 251 261 10.1038/nrn2117 10.1038/nrn2117 17375039 (Pubitemid 46452327)
44. + channel TREK-1 EMBO J 21 2968 2976 10.1093/emboj/cdf288 10.1093/emboj/cdf288 12065410 (Pubitemid 34670381)
45. Y Jiang A Lee J Chen M Cadene BT Chait R MacKinnon 2002 The open pore conformation of potassium channels Nature 417 523 526 10.1038/417523a 10.1038/417523a 12037560 (Pubitemid 34595913)
46. + channels of the TALK family Biochem Biophys Res Commun 315 836 844 10.1016/j.bbrc.2004.01.137 10.1016/j.bbrc.2004.01.137 14985088 (Pubitemid 38249379)
47. D Kang C Choe E Cavanaugh D Kim 2007 Properties of single two-pore domain TREK-2 channels expressed in mammalian cells J Physiol 583 57 69 10.1113/jphysiol.2007.136150 10.1113/jphysiol.2007.136150 17540699 (Pubitemid 47244244)
48. 2+) J Physiol 541 9 24 10.1113/jphysiol.2001.014456 10.1113/jphysiol.2001.014456 12015417 (Pubitemid 35190181)
49. + channel family J Biol Chem 275 9340 9347 10.1074/jbc.275.13.9340 10.1074/jbc.275.13.9340 10734076 (Pubitemid 30185157)
50. + channels by pressure, free fatty acids and alkali Pflugers Arch 442 64 72 10.1007/s004240000496 10.1007/s004240000496 11374070 (Pubitemid 32336826)
51. HT Kurata D Fedida 2006 A structural interpretation of voltage-gated potassium channel inactivation Prog Biophys Mol Biol 92 185 208 10.1016/j.pbiomolbio.2005.10.001 10.1016/j.pbiomolbio.2005.10.001 16316679 (Pubitemid 43913276)
52. N Lalevee B Monier S Senatore L Perrin M Semeriva 2006 Control of cardiac rhythm by ORK1, a Drosophila two-pore domain potassium channel Curr Biol 16 1502 1508 10.1016/j.cub.2006.05.064 10.1016/j.cub.2006.05.064 16890525 (Pubitemid 44142975)
53. + channels Neuron 27 573 583 10.1016/S0896-6273(00) 00067-2 10.1016/S0896-6273(00)00067-2 11055439
54. + channel with multiple regulations by polyunsaturated fatty acids, lysophospholipids, and Gs, Gi, and Gq protein-coupled receptors J Biol Chem 275 28398 28405 10.1074/jbc.M002822200 10.1074/jbc.M002822200 10880510
55. J Liu M Zhang M Jiang GN Tseng 2002 Structural and functional role of the extracellular s5-p linker in the HERG potassium channel J Gen Physiol 120 723 737 10.1085/jgp.20028687 10.1085/jgp.20028687 12407082 (Pubitemid 35332590)
56. + channel Science 309 897 903 10.1126/science.1116269 10.1126/science.1116269 16002581 (Pubitemid 41099919)
57. CM Lopes PG Gallagher ME Buck MH Butler SA Goldstein 2000 Proton block and voltage gating are potassium-dependent in the cardiac leak channel Kcnk3 J Biol Chem 275 16969 16978 10.1074/jbc.M001948200 10.1074/jbc.M001948200 10748056 (Pubitemid 30398937)
58. CM Lopes N Zilberberg SA Goldstein 2001 Block of Kcnk3 by protons. Evidence that 2-P-domain potassium channel subunits function as homodimers J Biol Chem 276 24449 24452 10.1074/jbc.C100184200 10.1074/jbc.C100184200 11358956
59. + channels J Physiol 564 117 129 10.1113/jphysiol.2004.081935 10.1113/jphysiol.2004.081935 15677683 (Pubitemid 40542192)
60. + channels Channels Austin 1 124 134 18690021
61. J Lopez-Barneo T Hoshi SH Heinemann RW Aldrich 1993 Effects of external cations and mutations in the pore region on C-type inactivation of Shaker potassium channels Receptors Channels 1 61 71 8081712
62. DP Lotshaw 2006 Biophysical and pharmacological characteristics of native two-pore domain TASK channels in rat adrenal glomerulosa cells J Membr Biol 210 51 70 10.1007/s00232-005-7012-x 10.1007/s00232-005-7012-x 16794780 (Pubitemid 44048350)
63. + channels Biochemistry 43 13242 13247 10.1021/bi048377v 10.1021/bi048377v 15491131
64. F Maingret AJ Patel F Lesage M Lazdunski E Honore 1999 Mechano- or acid stimulation, two interactive modes of activation of the TREK-1 potassium channel J Biol Chem 274 26691 26696 10.1074/jbc.274.38.26691 10.1074/jbc.274.38.26691 10480871 (Pubitemid 29440003)
65. + channel EMBO J 19 2483 2491 10.1093/emboj/19.11.2483 10.1093/emboj/19.11.2483 10835347
66. + channels TREK-1 and TRAAK J Biol Chem 275 10128 10133 10.1074/jbc.275.14.10128 10.1074/jbc.275.14.10128 10744694 (Pubitemid 30202065)
67. A Mathie 2007 Neuronal two-pore-domain potassium channels and their regulation by G protein-coupled receptors J Physiol 578 377 385 10.1113/jphysiol.2006.121582 10.1113/jphysiol.2006.121582 17068099 (Pubitemid 46092203)
68. + channel 1 (TASK1) and TASK3 channels to the control of activity modes in thalamocortical neurons J Neurosci 23 6460 6469 12878686
69. (+) channels TASK-1 and -2 Pflugers Arch 445 577 583 12634929
70. + channel, TASK2 Proc Natl Acad Sci USA 102 16102 16106 10.1073/pnas.0506870102 10.1073/pnas.0506870102 16239344 (Pubitemid 41552874)
71. D Mu L Chen X Zhang LH See CM Koch C Yen JJ Tong L Spiegel KC Nguyen A Servoss Y Peng L Pei JR Marks S Lowe T Hoey LY Jan WR McCombie MH Wigler S Powers 2003 Genomic amplification and oncogenic properties of the KCNK9 potassium channel gene Cancer Cell 3 297 302 10.1016/S1535-6108(03)00054-0 10.1016/S1535-6108(03)00054-0 12676587 (Pubitemid 37443884)
72. J Murbartian Q Lei JJ Sando DA Bayliss 2005 Sequential phosphorylation mediates receptor- and kinase-induced inhibition of TREK-1 background potassium channels J Biol Chem 280 30175 30184 10.1074/jbc.M503862200 10.1074/jbc. M503862200 16006563 (Pubitemid 41216196)
73. + channel Proc Natl Acad Sci USA 104 666 671 10.1073/pnas.0606173104 10.1073/pnas.0606173104 17197424 (Pubitemid 46123082)
74. + channels expressed in Xenopus oocytes J Physiol 562 687 696 10.1113/jphysiol.2004.079020 10.1113/jphysiol.2004.079020 15611021 (Pubitemid 40246787)
75. EM Ogielska RW Aldrich 1999 Functional consequences of a decreased potassium affinity in a potassium channel pore. Ion interactions and C-type inactivation J Gen Physiol 113 347 358 10.1085/jgp.113.2.347 10.1085/jgp.113.2.347 9925829 (Pubitemid 29219804)
76. + channels J Gen Physiol 116 181 190 10.1085/jgp.116.2.181 10.1085/jgp.116.2.181 10919865 (Pubitemid 30637003)
77. G Panyi C Deutsch 2006 Cross talk between activation and slow inactivation gates of Shaker potassium channels J Gen Physiol 128 547 559 10.1085/jgp.200609644 10.1085/jgp.200609644 17043151 (Pubitemid 44664632)
78. G Panyi C Deutsch 2007 Probing the cavity of the slow inactivated conformation of Shaker potassium channels J Gen Physiol 129 403 418 10.1085/jgp.200709758 10.1085/jgp.200709758 17438120 (Pubitemid 46686456)
79. + channels Nat Neurosci 2 422 426 10.1038/8084 10.1038/8084 10321245 (Pubitemid 30491251)
80. + channel J Biol Chem 275 28722 28730 10.1074/jbc.M003755200 10.1074/jbc.M003755200 10887187
81. + channel function Proc Natl Acad Sci USA 100 7803 7807 10.1073/pnas.1232448100 10.1073/pnas.1232448100 12782791 (Pubitemid 36760050)
82. + channel. An extracellular histiding as pH sensor J Biol Chem 275 16650 16657 10.1074/jbc.M000030200 10.1074/jbc.M000030200 10747866 (Pubitemid 30398893)
83. + channel from human kidney J Biol Chem 273 30863 30869 10.1074/jbc.273.47.30863 10.1074/jbc.273.47.30863 9812978 (Pubitemid 28533086)
84. 2P10.1 (TREK-2) by the amino-terminus: role of alternative translation initiation J Physiol 586 5651 5663 10.1113/jphysiol. 2008.161927 10.1113/jphysiol.2008.161927 18845607
85. PJ Stansfeld A Grottesi ZA Sands MS Sansom P Gedeck M Gosling B Cox PR Stanfield JS Mitcheson MJ Sutcliffe 2008 Insight into the mechanism of inactivation and pH sensitivity in potassium channels from molecular dynamics simulations Biochemistry 47 7414 7422 10.1021/bi800475j 10.1021/bi800475j 18558719 (Pubitemid 351991020)
86. JG Starkus L Kuschel MD Rayner SH Heinemann 1997 Ion conduction through C-type inactivated Shaker channels J Gen Physiol 110 539 550 10.1085/jgp.110.5.539 10.1085/jgp.110.5.539 9348326 (Pubitemid 27494944)
87. JG Starkus Z Varga R Schonherr SH Heinemann 2003 Mechanisms of the inhibition of Shaker potassium channels by protons Pflugers Arch 447 44 54 10.1007/s00424-003-1121-0 10.1007/s00424-003-1121-0 12920598 (Pubitemid 38177656)
88. + channel, is modulated by multiple neurotransmitters in motoneurons Neuron 25 399 410 10.1016/S0896-6273(00)80903-4 10.1016/S0896-6273(00)80903-4 10719894 (Pubitemid 30831794)
89. D Thomas LD Plant CM Wilkens ZA McCrossan SA Goldstein 2008 Alternative translation initiation in rat brain yields K(2P)2.1 potassium channels permeable to sodium Neuron 58 859 870 10.1016/j.neuron.2008.04.016 10.1016/j.neuron.2008. 04.016 18579077 (Pubitemid 351842748)
90. + channel S5P extracellular linker: role of an amphipathic alpha-helix in C-type inactivation J Biol Chem 278 42136 42148 10.1074/jbc.M212824200 10.1074/jbc.M212824200 12902341 (Pubitemid 37310481)
91. EL Veale LE Kennard GL Sutton G MacKenzie C Sandu A Mathie 2007 G(alpha)q-mediated regulation of TASK3 two-pore domain potassium channels: the role of protein kinase C Mol Pharmacol 71 1666 1675 10.1124/mol.106.033241 10.1124/mol.106.033241 17374744 (Pubitemid 47010919)
92. I Voloshyna A Besana M Castillo T Matos IB Weinstein M Mansukhani RB Robinson C Cordon-Cardo SJ Feinmark 2008 TREK-1 is a novel molecular target in prostate cancer Cancer Res 68 1197 1203 10.1158/0008-5472.CAN-07-5163 10.1158/0008-5472.CAN-07-5163 18281496 (Pubitemid 351272239)
93. + channel coupled to GABAB receptors in mammalian respiratory neurons Neuroreport 8 1667 1670 10.1097/00001756-199705060-00021 10.1097/00001756-199705060-00021 9189911
94. + channel allows inactivation to be modulated by metal binding Biophys J 66 1068 1075 10.1016/S0006-3495(94)80888-4 10.1016/S0006-3495(94)80888-4 8038379
95. + channel Cell 111 231 239 10.1016/S0092-8674(02)01013-9 10.1016/S0092-8674(02)01013-9 12408867 (Pubitemid 35292443)
96. K Yuill I Ashmole PR Stanfield 2004 The selectivity filter of the tandem pore potassium channel TASK-1 and its pH sensitivity and ionic selectivity Pflugers Arch 448 63 69 10.1007/s00424-003-1218-5 10.1007/s00424-003-1218-5 14722774 (Pubitemid 38657206)
97. KH Yuill PJ Stansfeld I Ashmole MJ Sutcliffe PR Stanfield 2007 The selectivity, voltage-dependence and acid sensitivity of the tandem pore potassium channel TASK-1: contributions of the pore domains Pflugers Arch 455 333 348 10.1007/s00424-007-0282-7 10.1007/s00424-007-0282-7 17541788 (Pubitemid 47546791)
98. N Zilberberg N Ilan R Gonzalez-Colaso SA Goldstein 2000 Opening and closing of KCNKO potassium leak channels is tightly regulated J Gen Physiol 116 721 734 10.1085/jgp.116.5.721 10.1085/jgp.116.5.721 11055999 (Pubitemid 30826562)
99. N Zilberberg N Ilan SA Goldstein 2001 KCNKO: opening and closing the 2-P-domain potassium leak channel entails "C-type" gating of the outer pore Neuron 32 635 648 10.1016/S0896-6273(01)00503-7 10.1016/S0896-6273(01) 00503-7 11719204 (Pubitemid 33145197)