A high-throughput functional screen identifies small molecule regulators of temperature- and mechano-sensitive K2P channels

ACS Chemical Biology

Volumn 8, Issue 8, 2013, Pages 1841-1851

  Bagriantsev, Sviatoslav N ^a,d   Ang, Kean Hooi ^a   Gallardo Godoy, Alejandra ^a   Clark, Kimberly A ^a   Arkin, Michelle R ^a   Renslo, Adam R ^a   Minor, Daniel L ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,7 DICHLORO 9,9 DIMETHYL(1H TETRAZOL 5 YL) ETHYL] 9,10 DIHYDROACRIDINE; ACRIDINE DERIVATIVE; ML 6733; POTASSIUM; POTASSIUM CHANNEL; POTASSIUM CHANNEL KCNQ2; SMALL MOLECULE TRANSPORT AGENT; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOPHYSICS; CELL STIMULATION; CHANNEL GATING; CONTROLLED STUDY; ELECTRIC ACTIVITY; ELECTROPHYSIOLOGY; GROWTH INHIBITION; HETEROLOGOUS EXPRESSION; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; HUMAN TISSUE; MAMMAL; MECHANICAL SENSITIVITY; MOLECULAR LIBRARY; NONHUMAN; OOCYTE; POTASSIUM CURRENT; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION; TEMPERATURE SENSITIVITY; VOLTAGE CLAMP; XENOPUS; YEAST;

BIOLOGICAL ASSAY; DRUG EVALUATION, PRECLINICAL; MODELS, BIOLOGICAL; MOLECULAR STRUCTURE; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; PROTEIN BINDING; SMALL MOLECULE LIBRARIES; TEMPERATURE; YEASTS;

EID: 84882796314     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb400289x     Document Type: Article

References (51)

1. Enyedi, P. and Czirjak, G. (2010) Molecular background of leak K+ currents: two-pore domain potassium channels Physiol. Rev. 90, 559-605
2. Lesage, F. and Barhanin, J. (2011) Molecular physiology of pH-sensitive background K(2P) channels Physiology 26, 424-437
3. Es-Salah-Lamoureux, Z., Steele, D. F., and Fedida, D. (2010) Research into the therapeutic roles of two-pore-domain potassium channels Trends Pharmacol. Sci. 31, 587-595
4. Lotshaw, D. P. (2007) Biophysical, pharmacological, and functional characteristics of cloned and native mammalian two-pore domain K+ channels Cell Biochem. Biophys. 47, 209-256
5. Fink, M., Duprat, F., Lesage, F., Reyes, R., Romey, G., Heurteaux, C., and Lazdunski, M. (1996) Cloning, functional expression and brain localization of a novel unconventional outward rectifier K+ channel EMBO J. 15, 6854-6862
6. Noel, J., Sandoz, G., and Lesage, F. (2011) Molecular regulations governing TREK and TRAAK channel functions Channels (Austin) 5, 402-409
7. Honore, E. (2007) The neuronal background K2P channels: focus on TREK1 Nat. Rev. Neurosci. 8, 251-261
8. Maingret, F., Lauritzen, I., Patel, A. J., Heurteaux, C., Reyes, R., Lesage, F., Lazdunski, M., and Honore, E. (2000) TREK-1 is a heat-activated background K(+) channel EMBO J. 19, 2483-2491
9. Patel, A. J., Honore, E., Maingret, F., Lesage, F., Fink, M., Duprat, F., and Lazdunski, M. (1998) A mammalian two pore domain mechano-gated S-like K+ channel EMBO J. 17, 4283-4290
10. Patel, A. J., Honore, E., Lesage, F., Fink, M., Romey, G., and Lazdunski, M. (1999) Inhalational anesthetics activate two-pore-domain background K+ channels Nat. Neurosci. 2, 422-426
11. Alloui, A., Zimmermann, K., Mamet, J., Duprat, F., Noel, J., Chemin, J., Guy, N., Blondeau, N., Voilley, N., Rubat-Coudert, C., Borsotto, M., Romey, G., Heurteaux, C., Reeh, P., Eschalier, A., and Lazdunski, M. (2006) TREK-1, a K+ channel involved in polymodal pain perception EMBO J. 25, 2368-2376
12. Noel, J., Zimmermann, K., Busserolles, J., Deval, E., Alloui, A., Diochot, S., Guy, N., Borsotto, M., Reeh, P., Eschalier, A., and Lazdunski, M. (2009) The mechano-activated K+ channels TRAAK and TREK-1 control both warm and cold perception EMBO J. 28, 1308-1318
13. Heurteaux, C., Guy, N., Laigle, C., Blondeau, N., Duprat, F., Mazzuca, M., Lang-Lazdunski, L., Widmann, C., Zanzouri, M., Romey, G., and Lazdunski, M. (2004) TREK-1, a K+ channel involved in neuroprotection and general anesthesia EMBO J. 23, 2684-2695
14. Heurteaux, C., Lucas, G., Guy, N., El Yacoubi, M., Thummler, S., Peng, X. D., Noble, F., Blondeau, N., Widmann, C., Borsotto, M., Gobbi, G., Vaugeois, J. M., Debonnel, G., and Lazdunski, M. (2006) Deletion of the background potassium channel TREK-1 results in a depression-resistant phenotype Nat. Neurosci. 9, 1134-1141
15. Solt, K. and Forman, S. A. (2007) Correlating the clinical actions and molecular mechanisms of general anesthetics Curr. Opin. Anaesthesiol. 20, 300-306
16. Lesage, F., Terrenoire, C., Romey, G., and Lazdunski, M. (2000) Human TREK2, a 2P domain mechano-sensitive K+ channel with multiple regulations by polyunsaturated fatty acids, lysophospholipids, and Gs, Gi, and Gq protein-coupled receptors J. Biol. Chem. 275, 28398-28405
17. Gruss, M., Bushell, T. J., Bright, D. P., Lieb, W. R., Mathie, A., and Franks, N. P. (2004) Two-pore-domain K+ channels are a novel target for the anesthetic gases xenon, nitrous oxide, and cyclopropane Mol. Pharmacol. 65, 443-452
18. Duprat, F., Lesage, F., Patel, A. J., Fink, M., Romey, G., and Lazdunski, M. (2000) The neuroprotective agent riluzole activates the two P domain K(+) channels TREK-1 and TRAAK Mol. Pharmacol. 57, 906-912
19. Kennard, L. E., Chumbley, J. R., Ranatunga, K. M., Armstrong, S. J., Veale, E. L., and Mathie, A. (2005) Inhibition of the human two-pore domain potassium channel, TREK-1, by fluoxetine and its metabolite norfluoxetine Br. J. Pharmacol. 144, 821-829
20. Sandoz, G., Bell, S. C., and Isacoff, E. Y. (2011) Optical probing of a dynamic membrane interaction that regulates the TREK1 channel Proc. Natl. Acad. Sci. U.S.A. 108, 2605-2610
21. Bagriantsev, S. N., Clark, K. A., and Minor, D. L., Jr. (2012) Metabolic and thermal stimuli control K(2P)2.1 (TREK-1) through modular sensory and gating domains EMBO J. 31, 3297-3308
22. Bagriantsev, S. N., Peyronnet, R., Clark, K. A., Honore, E., and Minor, D. L., Jr. (2011) Multiple modalities converge on a common gate to control K2P channel function EMBO J. 30, 3594-3606
23. Piechotta, P. L., Rapedius, M., Stansfeld, P. J., Bollepalli, M. K., Ehrlich, G., Andres-Enguix, I., Fritzenschaft, H., Decher, N., Sansom, M. S., Tucker, S. J., and Baukrowitz, T. (2011) The pore structure and gating mechanism of K2P channels EMBO J. 30, 3607-3619
24. + transporters Mol. Cell. Biol. 11, 4266-4273
25. + channel in yeast Mol. Biol. Cell 6, 1231-1240
26. Minor, D. L., Jr., Masseling, S. J., Jan, Y. N., and Jan, L. Y. (1999) Transmembrane structure of an inwardly rectifying potassium channel Cell 96, 879-891
27. Chatelain, F. C., Gazzarrini, S., Fujiwara, Y., Arrigoni, C., Domigan, C., Ferrara, G., Pantoja, C., Thiel, G., Moroni, A., and Minor, D. L., Jr. (2009) Selection of inhibitor-resistant viral potassium channels identifies a selectivity filter site that affects barium and amantadine block PloS One 4, e7496
28. Zaks-Makhina, E., Kim, Y., Aizenman, E., and Levitan, E. S. (2004) Novel neuroprotective K+ channel inhibitor identified by high-throughput screening in yeast Mol. Pharmacol. 65, 214-219
29. Zaks-Makhina, E., Li, H., Grishin, A., Salvador-Recatala, V., and Levitan, E. S. (2009) Specific and slow inhibition of the kir2.1 K+ channel by gambogic acid J. Biol. Chem. 284, 15432-15438
30. Chatelain, F. C., Alagem, N., Xu, Q., Pancaroglu, R., Reuveny, E., and Minor, D. L., Jr. (2005) The pore helix dipole has a minor role in inward rectifier channel function Neuron 47, 833-843
31. Nakayama, G. R., Caton, M. C., Nova, M. P., and Parandoosh, Z. (1997) Assessment of the Alamar Blue assay for cellular growth and viability in vitro J. Immunol. Methods 204, 205-208
32. Gaber, R. F., Styles, C. A., and Fink, G. R. (1988) TRK1 encodes a plasma membrane protein required for high-affinity potassium transport in Saccharomyces cerevisiae Mol. Cell. Biol. 8, 2848-2859
33. Loukin, S. H., Vaillant, B., Zhou, X. L., Spalding, E. P., Kung, C., and Saimi, Y. (1997) Random mutagenesis reveals a region important for gating of the yeast K+ channel Ykc1 EMBO J. 16, 4817-4825
34. Zhang, J. H., Chung, T. D., and Oldenburg, K. R. (1999) A simple statistical parameter for use in evaluation and validation of high throughput screening assays J. Biomol. Screening 4, 67-73
35. Xiong, Q., Gao, Z., Wang, W., and Li, M. (2008) Activation of Kv7 (KCNQ) voltage-gated potassium channels by synthetic compounds Trends Pharmacol. Sci. 29, 99-107
36. 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
37. 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
38. Chemin, J., Patel, A. J., Duprat, F., Lauritzen, I., Lazdunski, M., and Honore, E. (2005) A phospholipid sensor controls mechanogating of the K+ channel TREK-1 EMBO J. 24, 44-53
39. Honore, E., Maingret, F., Lazdunski, M., and Patel, A. J. (2002) An intracellular proton sensor commands lipid- and mechano-gating of the K(+) channel TREK-1 EMBO J. 21, 2968-2976
40. Segal-Hayoun, Y., Cohen, A., and Zilberberg, N. (2010) Molecular mechanisms underlying membrane-potential-mediated regulation of neuronal K2P2.1 channels Mol. Cell. Neurosci. 43, 117-126
41. Rapedius, M., Schmidt, M. R., Sharma, C., Stansfeld, P. J., Sansom, M. S., Baukrowitz, T., and Tucker, S. J. (2012) State-independent intracellular access of quaternary ammonium blockers to the pore of TREK-1 Channels (Austin) 6, 473-478
42. 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
43. 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
44. Yuill, K. H., Stansfeld, P. J., Ashmole, I., Sutcliffe, M. J., and Stanfield, P. R. (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
45. Niemeyer, M. I., Cid, L. P., Pena-Munzenmayer, G., and Sepulveda, F. V. (2010) Separate Gating Mechanisms Mediate the Regulation of K2P Potassium Channel TASK-2 by Intra- and Extracellular pH J. Biol. Chem. 285, 16467-16475
46. Nayak, T. K., Harinath, S., Nama, S., Somasundaram, K., and Sikdar, S. K. (2009) Inhibition of human two-pore domain K+ channel TREK1 by local anesthetic lidocaine: negative cooperativity and half-of-sites saturation kinetics Mol. Pharmacol. 76, 903-917
47. Takahira, M., Sakurai, M., Sakurada, N., and Sugiyama, K. (2005) Fenamates and diltiazem modulate lipid-sensitive mechano-gated 2P domain K(+) channels Pflugers Arch. 451, 474-478
48. Cadaveira-Mosquera, A., Ribeiro, S. J., Reboreda, A., Perez, M., and Lamas, J. A. (2011) Activation of TREK currents by the neuroprotective agent riluzole in mouse sympathetic neurons J. Neurosci. 31, 1375-1385
49. Lopes, C. M., Rohacs, T., Czirjak, G., Balla, T., Enyedi, P., and Logothetis, D. E. (2005) PIP2 hydrolysis underlies agonist-induced inhibition and regulates voltage gating of two-pore domain K+ channels J. Physiol. 564, 117-129
50. Sandoz, G., Douguet, D., Chatelain, F., Lazdunski, M., and Lesage, F. (2009) Extracellular acidification exerts opposite actions on TREK1 and TREK2 potassium channels via a single conserved histidine residue Proc. Natl. Acad. Sci. U.S.A. 106, 14628-14633
51. Tertyshnikova, S., Knox, R. J., Plym, M. J., Thalody, G., Griffin, C., Neelands, T., Harden, D. G., Signor, L., Weaver, D., Myers, R. A., and Lodge, N. J. (2005) BL-1249 [(5,6,7,8-tetrahydro-naphthalen-1-yl)-[2-(1H-tetrazol-5-yl)- phenyl]-amine]: a putative potassium channel opener with bladder-relaxant properties J. Pharmacol. Exp. Ther. 313, 250-259