Acid-sensitive TWIK and TASK two-pore domain potassium channels change ion selectivity and become permeable to sodium in extracellular acidification

Journal of Biological Chemistry

Volumn 287, Issue 44, 2012, Pages 37145-37153

  Ma, Liqun ^a   Zhang, Xuexin ^a   Zhou, Min ^b   Chen, Haijun ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR FUNCTION; EXTRACELLULAR; EXTRACELLULAR PH; ION SELECTIVITY; POTASSIUM CHANNELS; RELATIVE PERMEABILITY;

BIOCHEMISTRY;

BIOLOGY;

MEGLUMINE; POTASSIUM CHANNEL; POTASSIUM ION; SODIUM ION; TASK 1 POTASSIUM CHANNEL; TASK 3 POTASSIUM CHANNEL; TWIK POTASSIUM CHANNEL; UNCLASSIFIED DRUG;

ACIDIFICATION; ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL MEMBRANE DEPOLARIZATION; CELL PERMEABILIZATION; CELL PH; CONTROLLED STUDY; ELECTROCHEMISTRY; EXTRACELLULAR SPACE; FEMALE; HETEROLOGOUS EXPRESSION; ION PERMEABILITY; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN DOMAIN; REGULATORY MECHANISM;

AMINO ACID MOTIFS; AMINO ACID SUBSTITUTION; ANIMALS; CHO CELLS; CRICETINAE; EXTRACELLULAR FLUID; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; MEMBRANE POTENTIALS; MICE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; NERVE TISSUE PROTEINS; PATCH-CLAMP TECHNIQUES; PERMEABILITY; POTASSIUM CHANNELS; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; PROTEIN STRUCTURE, TERTIARY; RATS; SODIUM;

EID: 84868227336     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.398164     Document Type: Article

References (44)

1. Goldstein, S. A., Bayliss, D. A., Kim, D., Lesage, F., Plant, L. D., and Rajan, S. (2005) International Union of Pharmacology. LV. Nomenclature and molecular relationships of two-P potassium channels. Pharmacol. Rev. 57, 527-540
2. + channels. Cell Biochem. Biophys. 47, 209-256
3. + currents: two-pore domain potassium channels. Physiol. Rev. 90, 559-605
4. + channel K2P1. Cell 121, 37-47
5. Cohen, A., Ben-Abu, Y., Hen, S., and Zilberberg, N. (2008) A novel mechanism for human K2P2.1 channel gating: facilitation of C-type gating by protonation of extracellular histidine residues. J. Biol. Chem. 283, 19448-19455
6. + channel to sense external pH variations near physiological pH. EMBO J. 16, 5464-5471
7. Lopes, C. M., Gallagher, P. G., Buck, M. E., Butler, M. H., and Goldstein, S. A. (2000) Proton block and voltage gating are potassium-dependent in the cardiac leak channel Kcnk3. J. Biol. Chem. 275, 16969-16978
8. + channel family. J. Biol. Chem. 275, 9340-9347
9. + channel: an extracellular histidine as pH sensor. J. Biol. Chem. 275, 16650-16657
10. + channel family. J. Biol. Chem. 279, 28063-28070
11. Keshavaprasad, B., Liu, C., Au, J. D., Kindler, C. H., Cotten, J. F., and Yost, C. S. (2005) Species-specific differences in response to anesthetics and other modulators by the K2P channel TRESK. Anesth. Analg. 101, 1042-1049
12. Lopes, C. M., Zilberberg, N., and Goldstein, S. A. (2001) Block of Kcnk3 by protons: evidence that 2-P-domain potassium channel subunits function as homodimers. J. Biol. Chem. 276, 24449-24452
13. Steidl, J. V., and Yool, A. J. (1999) Differential sensitivity of voltage-gated potassium channels Kv1.5 and Kv1.2 to acidic pH and molecular identification of pH sensor. Mol. Pharmacol. 55, 812-820
14. Coulter, K. L., Périer, F., Radeke, C. M., and Vandenberg, C. A. (1995) Identification and molecular localization of a pH-sensing domain for the inward rectifier potassium channel HIR. Neuron 15, 1157-1168
15. + channel. Am. J. Physiol. Cell Physiol. 283, C1114-C1121
16. Li, X., Bett, G. C., Jiang, X., Bondarenko, V. E., Morales, M. J., and Rasmusson, R. L. (2003) Regulation of N-and C-type inactivation of Kv1.4 by pHo and K+: evidence for transmembrane communication. Am. J. Physiol. Heart Circ. Physiol. 284, H71-H80
17. + channel subunits: kinetic properties and expression in rat heart. Am. J. Physiol. 277, H1669-H1678
18. Clarke, C. E., Veale, E. L., Wyse, K., Vandenberg, J. I., and Mathie, A. (2008) The M1P1-loop of TASK3 K2P channels apposes the selectivity filter and influences channel function. J. Biol. Chem. 283, 16985-16992
19. Ma, L., Zhang, X., and Chen, H. (2011) TWIK-1 two-pore domain potassium channels change ion selectivity and conduct inward leak sodium currents in hypokalemia. Sci. Signal. 4, ra37
20. Goldstein, S. A. (2011) K2P potassium channels, mysterious and paradoxically exciting. Sci. Signal. 4, pe35
21. Hille, B. (2001) Ion Channels of Excitable Membranes, Third Ed., p. 469 Sinauer Associates, Inc., Sunderland, MA
22. + channels expressed in Xenopus oocytes. J. Physiol. 562, 687-696
23. Yuill, K., Ashmole, I., and Stanfield, P. R. (2004) The selectivity filter of the tandem pore potassium channel TASK-1 and its pH sensitivity and ionic selectivity. Pflugers Arch. 448, 63-69
24. Miller, A. N., and Long, S. B. (2012) Crystal structure of the human twopore domain potassium channel K2P1. Science 335, 432-436
25. Stansfeld, P. J., Grottesi, A., Sands, Z. A., Sansom, M. S., Gedeck, P., Gosling, M., Cox, B., Stanfield, P. R., Mitcheson, J. S., and Sutcliffe, M. J. (2008) Insight into the mechanism of inactivation and pH sensitivity in potassium channels from molecular dynamics simulations. Biochemistry 47, 7414-7422
26. Zhou, M., Xu, G., Xie, M., Zhang, X., Schools, G. P., Ma, L., Kimelberg, H. K., and Chen, H. (2009) TWIK-1 and TREK-1 are potassium channels contributing significantly to astrocyte passive conductance in rat hippocampal slices. J. Neurosci. 29, 8551-8564
27. Meadows, H. J., and Randall, A. D. (2001) Functional characterization of human TASK-3, an acid-sensitive two-pore domain potassium channel. Neuropharmacology 40, 551-559
28. + channel with a novel structure. EMBO J. 15, 1004-1011
29. + channel. FEBS Lett. 402, 28-32
30. Ordög, B., Brutyó, E., Puskás, L. G., Papp, J. G., Varró, A., Szabad, J., and Boldogkoi, Z. (2006) Gene expression profiling of human cardiac potassium and sodium channels. Int. J. Cardiol. 111, 386-393
31. Gaborit, N., Le Bouter, S., Szuts, V., Varro, A., Escande, D., Nattel, S., and Demolombe, S. (2007) Regional and tissue-specific transcript signatures of ion channel genes in the non-diseased human heart. J. Physiol. 582, 675-693
32. Ma, L., Xie, Y. P., Zhou, M., and Chen, H. (2012) Silent TWIK-1 potassium channels conduct monovalent cation currents. Biophys. J. 102, L34-L36
33. Nie, X., Arrighi, I., Kaissling, B., Pfaff, I., Mann, J., Barhanin, J., and Vallon, V. (2005) Expression and insights on function of potassium channel TWIK-1 in mouse kidney. Pflugers Arch. 451, 479-488
34. Lesage, F., and Barhanin, J. (2011) Molecular physiology of pH-sensitive background K2P channels. Physiology (Bethesda) 26, 424-437
35. Chatelain, F. C., Bichet, D., Douguet, D., Feliciangeli, S., Bendahhou, S., Reichold, M., Warth, R., Barhanin, J., and Lesage, F. (2012) TWIK1, a unique background channel with variable ion selectivity. Proc. Natl. Acad. Sci. U.S.A. 109, 5499-5504
36. Renigunta, V., Yuan, H., Zuzarte, M., Rinné, S., Koch, A., Wischmeyer, E., Schlichthörl, G., Gao, Y., Karschin, A., Jacob, R., Schwappach, B., Daut, J., and Preisig-Müller, R. (2006) The retention factor p11 confers an endoplasmic reticulum-localization signal to the potassium channel TASK-1. Traffic 7, 168-181
37. Kiss, L., LoTurco, J., and Korn, S. J. (1999) Contribution of the selectivity filter to inactivation in potassium channels. Biophys. J. 76, 253-263
38. 2+. J. Physiol. 541, 9-24
39. + channel kv1.4 by acidosis: protonation of an extracellular histidine slows the recovery from N-type inactivation. J. Physiol. 526, 253-264
40. Mathie, A., Al-Moubarak, E., and Veale, E. L. (2010) Gating of two-pore domain potassium channels. J. Physiol. 588, 3149-3156
41. Cohen, A., Ben-Abu, Y., and Zilberberg, N. (2009) Gating the pore of potassium leak channels. Eur. Biophys. J. 39, 61-73
42. Zilberberg, N., Ilan, N., and Goldstein, S. A. (2001) KCNKØ: opening and closing the 2-P-domain potassium leak channel entails "C-type" gating of the outer pore. Neuron 32, 635-648
43. Feliciangeli, S., Tardy, M. P., Sandoz, G., Chatelain, F. C., Warth, R., Barhanin, J., Bendahhou, S., and Lesage, F. (2010) Potassium channel silencing by constitutive endocytosis and intracellular sequestration. J. Biol. Chem. 285, 4798-4805
44. O'Kelly, I., Butler, M. H., Zilberberg, N., and Goldstein, S. A. (2002) Forward transport: 14-3-3 binding overcomes retention in endoplasmic reticulum by dibasic signals. Cell 111, 577-588