Functional characterization of zebrafish K2P18.1 (TRESK) two-pore-domain K+ channels

Naunyn-Schmiedeberg's Archives of Pharmacology

Volumn 387, Issue 3, 2014, Pages 291-300

  Rahm, Ann Kathrin ^a   Wiedmann, Felix ^a   Gierten, Jakob ^a   Schmidt, Constanze ^a   Schweizer, Patrick A ^a   Becker, Rüdiger ^a   Katus, Hugo A ^a   Thomas, Dierk ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

Cellular excitability; K2P channel; K2P18.1; Leak current; Membrane potential; Zebrafish

Indexed keywords

BARIUM; IONOMYCIN; KCNK18 PROTEIN; POTASSIUM CHANNEL; POTASSIUM CHANNEL 2P 18.1; PROTEIN KINASE C; QUINIDINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CLONE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GENE EXPRESSION SYSTEM; MEMBRANE POTENTIAL; MEMBRANE STEADY POTENTIAL; MOLECULAR BIOLOGY; MOLECULE; NONHUMAN; OOCYTE; ORTHOLOGY; XENOPUS; ZEBRA FISH;

ANIMALS; CALCIUM; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DNA, COMPLEMENTARY; FEMALE; HUMANS; IN SITU HYBRIDIZATION; MEMBRANE POTENTIALS; OOCYTES; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; PROTEIN KINASE C; QUINIDINE; SPECIES SPECIFICITY; TYPE C PHOSPHOLIPASES; XENOPUS LAEVIS; ZEBRAFISH;

EID: 84896690613     PISSN: 00281298     EISSN: 14321912     Source Type: Journal    
DOI: 10.1007/s00210-013-0945-1     Document Type: Article

References (44)

1. Ackermann GE, Paw BH (2003) Zebrafish: a genetic model for vertebrate organogenesis and human disorders. Front Biosci 8:d1227-d1253
2. Andres-Enguix I, Shang L, Stansfeld PJ, Morahan JM, Sansom MS, Lafrenière RG, Roy B, Griffiths LR, Rouleau GA, Ebers GC, Cader ZM, Tucker SJ (2012) Functional analysis of missense variants in the TRESK (KCNK18) K channel. Sci Rep 2:237
3. Bautista DM, Sigal YM, Milstein AD, Garrison JL, Zorn JA, Tsuruda PR, Nicoll RA, Julius D (2008) Pungent agents from Szechuan peppers excite sensory neurons by inhibiting two-pore potassium channels. Nat Neurosci 11:772-779
4. Chae YJ, Zhang J, Au P, Sabbadini M, Xie G, Yost CS (2010) Discrete change in volatile anesthetic sensitivity in mice with inactivated tandem pore potassium ion channel TRESK. Anesthesiology 113:1326-1337
5. Czirjak G, Enyedi P (2006) Targeting of calcineurin to an NFAT-like docking site is required for the calcium-dependent activation of the background K+ channel, TRESK. J Biol Chem 281:14677-14682
6. Czirjak G, Enyedi P (2010) TRESK background K(+) channel is inhibited by phosphorylation via two distinct pathways. J Biol Chem 285:14549-14557
7. Czirjak G, Toth ZE, Enyedi P (2004) The two-pore domain K+ channel, TRESK, is activated by the cytoplasmic calcium signal through calcineurin. J Biol Chem 279:18550-18558
8. Czirják G, Vuity D, Enyedi P (2008) Phosphorylation-dependent binding of 14-3-3 proteins controls TRESK regulation. J Biol Chem 283:15672-15680
9. Dobler T, Springauf A, Tovornik S, Weber M, Schmitt A, Sedlmeier R, Wischmeyer E, Döring F (2007) TRESK two-pore-domain K+ channels constitute a significant component of background potassium currents in murine dorsal root ganglion neurones. J Physiol Lond 585:867-879
10. Dooley K, Zon LI (2000) Zebrafish: a model system for the study of human disease. Curr Opin Genet Dev 10:252-256
11. Enyedi P, Czirják G (2010) Molecular background of leak K+ currents: two-pore domain potassium channels. Physiol Rev 90:559-605
12. Gates MA, Kim L, Egan ES, Cardozo T, Sirotkin HI, Dougan ST, Lashkari D, Abagyan R, Schier AF, Talbot WS (1999) A genetic linkage map for zebrafish: comparative analysis and localization of genes and expressed sequences. Genome Res 9:334-347
13. 2P) potassium leak channels by the tyrosine kinase inhibitor genistein. Br J Pharmacol 154:1680-1690
14. Gierten J, Ficker E, Bloehs R, Schweizer PA, Zitron E, Scholz E, Karle C, Katus HA, Thomas D (2010) The human cardiac K2P3.1 (TASK-1) potassium leak channel is a molecular target for the class III antiarrhythmic drug amiodarone. Naunyn Schmiedebergs Arch Pharmacol 381:261-270
15. Gierten J, Hassel D, Schweizer PA, Becker R, Katus HA, Thomas D (2012) Identification and functional characterization of zebrafish K(2P)10.1 (TREK2) two-pore-domain K(+) channels. Biochim Biophys Acta 1818:33-41
16. Goldstein SA, Bockenhauer D, O'Kelly I, Zilberberg N (2001) Potassium leak channels and the KCNK family of two-P-domain subunits. Nat Rev Neurosci 2:175-184
17. Hassel D, Dahme T, Erdmann J, Meder B, Huge A, Stoll M, Just S, Hess A, Ehlermann P, Weichenhan D, Grimmler M, Liptau H, Hetzer R, Regitz-Zagrosek V, Fischer C, Nurnberg P, Schunkert H, Katus HA, Rottbauer W (2009) Nexilin mutations destabilize cardiac Z-disks and lead to dilated cardiomyopathy. Nat Med 15:1281-1288
18. Jowett T, Lettice L (1994) Whole-mount in situ hybridizations on zebrafish embryos using a mixture of digoxigenin- and fluorescein-labelled probes. Trends Genet 10:73-74
19. Kang D, Kim D (2006) TREK-2 (K2P10.1) and TRESK (K2P18.1) are major background K+ channels in dorsal root ganglion neurons. Am J Physiol Cell Physiol 291:C138-C146
20. Keshavaprasad B, Liu C, Au JD, Kindler CH, Cotten JF, Yost CS (2005) Species-specific differences in response to anesthetics and other modulators by the K2P channel TRESK. Anesth Analg 101:1042-1049
21. Kisselbach J, Schweizer PA, Gerstberger R, Becker R, Katus HA, Thomas D (2012) Enhancement of K2P2.1 (TREK1) background currents expressed in Xenopus oocytes by voltage-gated K+ channel β subunits. Life Sci 91:377-383
22. Lafrenière RG, Rouleau GA (2011) Migraine: role of the TRESK two-pore potassium channel. Int J Biochem Cell Biol 43:1533-1536
23. Lafrenière RG, Cader MZ, Poulin JF, Andres-Enguix I, Simoneau M, Gupta N, Boisvert K, Lafrenière F, McLaughlan S, Dubé MP, Marcinkiewicz MM, Ramagopalan S, Ansorge O, Brais B, Sequeiros J, Pereira-Monteiro JM, Griffiths LR, Tucker SJ, Ebers G, Rouleau GA (2010) A dominant-negative mutation in the TRESK potassium channel is linked to familial migraine with aura. Nat Med 16:1157-1160
24. Lieschke GJ, Currie PD (2007) Animal models of human disease: zebrafish swim into view. Nat Rev Genet 8:353-367
25. Liu C, Au JD, Zou HL, Cotten JF, Yost CS (2004) Potent activation of the human tandem pore domain K channel TRESK with clinical concentrations of volatile anesthetics. Anesth Analg 99:1715-1722
26. Liu P, Xiao Z, Ren F, Guo Z, Chen Z, Zhao H, Cao YQ (2013) Functional analysis of a migraine-associated TRESK K+ channel mutation. J Neurosci 33:12810-12824
27. Lopes CM, Rohács T, Czirják G, Balla T, Enyedi P, Logothetis DE (2005) PIP2 hydrolysis underlies agonist-induced inhibition and regulates voltage gating of two-pore domain K+ channels. J Physiol 564:117-129
28. + channels. Trends Neurosci 24:339-346
29. Rahm AK, Gierten J, Kisselbach J, Staudacher I, Staudacher K, Schweizer PA, Becker R, Katus HA, Thomas D (2012) PKC-dependent activation of human K(2P) 18.1K(+) channels. Br J Pharmacol 166:764-773
30. Sandoz G, Bell SC, Isacoff EY (2011) Optical probing of a dynamic membrane interaction that regulates the TREK1 channel. Proc Natl Acad Sci U S A 108:2605-2610
31. Sandoz G, Levitz J, Kramer RH, Isacoff EY (2012) Optical control of endogenous proteins with a photoswitchable conditional subunit reveals a role for TREK1 in GABA(B) signaling. Neuron 74:1005-1014
32. Sano Y, Inamura K, Miyake A, Mochizuki S, Kitada C, Yokoi H, Nozawa K, Okada H, Matsushime H, Furuichi K (2003) A novel two-pore domain K+ channel, TRESK, is localized in the spinal cord. J Biol Chem 278:27406-27412
33. Schmidt C, Wiedmann F, Schweizer PA, Becker R, Katus HA, Thomas D (2012) Novel electrophysiological properties of dronedarone: inhibition of human cardiac two-pore-domain potassium (K(2P)) channels. Naunyn Schmiedebergs Arch Pharmacol 385:1003-1016
34. Schmidt C, Wiedmann F, Schweizer PA, Becker R, Katus HA, Thomas D (2013) Class I antiarrhythmic drugs inhibit human cardiac two-pore-domain K+ (K2P) channels. Eur J Pharmacol 721:237-248
35. Seyler C, Duthil-Straub E, Zitron E, Gierten J, Scholz EP, Fink RH, Karle CA, Becker R, Katus HA, Thomas D (2012) TASK1 (K2P3.1) K+ current inhibition by endothelin-1 is mediated by Rho kinase-dependent channel phosphorylation. Br J Pharmacol 165:1467-1475
36. Shin JT, Fishman MC (2002) From Zebrafish to human: modular medical models. Annu Rev Genomics Hum Genet 3:311-340
37. Staudacher K, Baldea I, Kisselbach J, Staudacher I, Rahm AK, Schweizer PA, Becker R, Katus HA, Thomas D (2011a) Alternative splicing determines mRNA translation initiation and function of human K(2P)10.1K+ channels. J Physiol (Lond) 589:3709-3720
38. 2P3.1 (TASK1) K+ leak channels. Br J Pharmacol 163:1099-1110
39. Streit AK, Netter MF, Kempf F, Walecki M, Rinné S, Bollepalli MK, Preisig-Müller R, Renigunta V, Daut J, Baukrowitz T, Sansom MS, Stansfeld PJ, Decher N (2011) A specific two-pore domain potassium channel blocker defines the structure of the TASK-1 open pore. J Biol Chem 286:13977-13984
40. 2P) potassium channels: leak conductance regulators of excitability. In: Squire LR (ed) Encyclopedia of neuroscience. Academic, Oxford, pp 1207-1220
41. Thomas D, Plant LD, Wilkens CM, McCrossan ZA, Goldstein SA (2008) Alternative translation initiation in rat brain yields K2P2.1 potassium channels permeable to sodium. Neuron 58:859-870
42. Tulleuda A, Cokic B, Callejo G, Saiani B, Serra J, Gasull X (2011) TRESK channel contribution to nociceptive sensory neurons excitability: modulation by nerve injury. Mol Pain 7:30
43. Yang L, Zhao J, Milutinovic PS, Brosnan RJ, Eger EI, Sonner JM (2007) Anesthetic properties of the ketone bodies beta-hydroxybutyric acid and acetone. Anesth Analg 105:673-679
44. Yellen G (1987) Permeation in potassium channels: implications for channel structure. Annu Rev Biophys Biophys Chem 16:227-246