Optical probing of a dynamic membrane interaction that regulates the TREK1 channel

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 6, 2011, Pages 2605-2610

  Sandoz, Guillaume ^a,b   Bell, Sarah C ^a   Isacoff, Ehud Y ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Ion channel; Phosphatidylinositol 4,5 biphosphate; Prozac; Two pore domain K+

Indexed keywords

FLUOXETINE; GQ COUPLED RECEPTOR; INOSITOL PHOSPHATE; MEMBRANE PROTEIN; MEMBRANE RECEPTOR; PHOSPHOLIPID; TREK1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CYTOPLASM; DISSOCIATION; EPIFLUORESCENCE MICROSCOPY; FEMALE; MEMBRANE BINDING; MEMBRANE CHANNEL; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; REGULATORY MECHANISM;

ANIMALS; ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; CELL MEMBRANE; FATTY ACIDS, UNSATURATED; FLUOXETINE; HEK293 CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; ISCHEMIA; MICE; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; OOCYTES; PHOSPHOLIPIDS; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; PROTEIN STRUCTURE, TERTIARY; XENOPUS LAEVIS;

MUS;

EID: 79952302529     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1015788108     Document Type: Article

References (38)

1. Fink M, et al. (1996) Cloning, functional expression and brain localization of a novel unconventional outward rectifier K+ channel. EMBO J 15:6854-6862.
2. Maingret F, et al. (2000) TREK-1 is a heat-activated background K(+) channel. EMBO J 19:2483-2491.
3. Patel AJ, et al. (1998) A mammalian two pore domain mechano-gated S-like K+ channel. EMBO J 17:4283-4290. (Pubitemid 28362619)
4. Sandoz G, Douguet D, Chatelain F, Lazdunski M, Lesage F (2009) Extracellular acidification exerts opposite actions on TREK1 and TREK2 potassium channels via a single conserved histidine residue. Proc Natl Acad Sci USA 106:14628-14633.
5. Maingret F, Patel AJ, Lesage F, Lazdunski M, Honoré E (1999) Mechano- or acid stimulation, two interactive modes of activation of the TREK-1 potassium channel. J Biol Chem 274:26691-26696.
6. Fink M, et al. (1998) A neuronal two P domain K+ channel stimulated by arachidonic acid and polyunsaturated fatty acids. EMBO J 17:3297-3308. (Pubitemid 28279504)
7. Maingret F, Patel AJ, Lesage F, Lazdunski M, Honoré E (2000) Lysophospholipids open the two-pore domain mechano-gated K(+) channels TREK-1 and TRAAK. J Biol Chem 275:10128-10133. (Pubitemid 30202065)
8. Chemin J, et al. (2005) A phospholipid sensor controls mechanogating of the K+ channel TREK-1. EMBO J 24:44-53. (Pubitemid 40188462)
9. Lopes CM, et al. (2005) PIP2 hydrolysis underlies agonist-induced inhibition and regulates voltage gating of two-pore domain K+ channels. J Physiol 564:117-129. (Pubitemid 40542192)
10. Patel AJ, et al. (1999) Inhalational anesthetics activate two-pore-domain background K+ channels. Nat Neurosci 2:422-426. (Pubitemid 30491251)
11. Duprat F, et al. (2000) The neuroprotective agent riluzole activates the two P domain K(+) channels TREK-1 and TRAAK. Mol Pharmacol 57:906-912. (Pubitemid 30253373)
12. Sandoz G, et al. (2006) AKAP150, a switch to convert mechano-, pH- and arachidonic acid-sensitive TREK K(+) channels into open leak channels. EMBO J 25:5864-5872. (Pubitemid 44967769)
13. Sandoz G, et al. (2008) Mtap2 is a constituent of the protein network that regulates twik-related K+ channel expression and trafficking. J Neurosci 28:8545-8552.
14. Murbartián J, Lei Q, Sando JJ, Bayliss DA (2005) Sequential phosphorylation mediates receptor- and kinase-induced inhibition of TREK-1 background potassium channels. J Biol Chem 280:30175-30184. (Pubitemid 41216196)
15. Kennard LE, et al. (2005) Inhibition of the human two-pore domain potassium channel, TREK-1, by fluoxetine and its metabolite norfluoxetine. Br J Pharmacol 144:821-829. (Pubitemid 40516121)
16. Heurteaux C, et al. (2004) TREK-1, a K+ channel involved in neuroprotection and general anesthesia. EMBO J 23:2684-2695. (Pubitemid 38988239)
17. Alloui A, et al. (2006) TREK-1, a K+ channel involved in polymodal pain perception. EMBO J 25:2368-2376. (Pubitemid 44012220)
18. Heurteaux C, et al. (2006) Deletion of the background potassium channel TREK-1 results in a depression-resistant phenotype. Nat Neurosci 9:1134-1141. (Pubitemid 44306306)
19. Honoré E, Maingret F, Lazdunski M, Patel AJ (2002) An intracellular proton sensor commands lipid-andmechano-gatingof the K(+) channel TREK-1.EMBOJ 21:2968-2976. (Pubitemid 34670381)
20. Mannuzzu LM, Moronne MM, Isacoff EY (1996) Direct physical measure of conformational rearrangement underlying potassium channel gating. Science 271:213-216. (Pubitemid 26033303)
21. Murata Y, Iwasaki H, Sasaki M, Inaba K, Okamura Y (2005) Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435:1239-1243. (Pubitemid 40943089)
22. Várnai P, Balla T (2007) Visualization and manipulation of phosphoinositide dynamics in live cells using engineered protein domains. Pflugers Arch 455:69-82. (Pubitemid 47403977)
23. Halaszovich CR, Schreiber DN, Oliver D (2009) Ci-VSP is a depolarization-activated phosphatidylinositol-4,5-bisphosphate and phosphatidylinositol-3,4,5-trisphosphate 5′-phosphatase. J Biol Chem 284:2106-2113.
24. Balla T, Varnai P (2009) Visualization of cellular phosphoinositide pools with GFP-fused protein-domains. Curr Protoc Cell Biol, Chapter 24:Unit 24.4.
25. Kohout SC, et al. (2010) Electrochemical coupling in the voltage-dependent phosphatase Ci-VSP. Nat Chem Biol 6:369-375.
26. Kalejta RF, Shenk T, Beavis AJ (1997) Use of a membrane-localized green fluorescent protein allows simultaneous identification of transfected cells and cell cycle analysis by flow cytometry. Cytometry 29:286-291. (Pubitemid 28032094)
27. Ulbrich MH, Isacoff EY (2008) Rules of engagement for NMDA receptor subunits. Proc Natl Acad Sci USA 105:14163-14168.
28. Tombola F, Ulbrich MH, Isacoff EY (2008) The voltage-gated proton channel Hv1 has two pores, each controlled by one voltage sensor. Neuron 58:546-556. (Pubitemid 351672357)
29. Zhang H, He C, Yan X, Mirshahi T, Logothetis DE (1999) Activation of inwardly rectifying K+ channels by distinct PtdIns(4,5)P2 interactions. Nat Cell Biol 1:183-188.
30. Kohout SC, Ulbrich MH, Bell SC, Isacoff EY (2008) Subunit organization and functional transitions in Ci-VSP. Nat Struct Mol Biol 15:106-108.
31. Suh BC, Inoue T, Meyer T, Hille B (2006) Rapid chemically induced changes of PtdIns (4,5)P2 gate KCNQ ion channels. Science 314:1454-1457.
32. Varnai P, Thyagarajan B, Rohacs T, Balla T (2006) Rapidly inducible changes in phosphatidylinositol 4,5-bisphosphate levels influence multiple regulatory functions of the lipid in intact living cells. J Cell Biol 175:377-382. (Pubitemid 44708062)
33. McLaughlin S, Hangyás-Mihályné G, Zaitseva I, Golebiewska U (2005) Reversible - through calmodulin - electrostatic interactions between basic residues on proteins and acidic lipids in the plasma membrane. Biochem Soc Symp 72):189-198. (Pubitemid 46126852)
34. Perlis RH, et al. (2008) Pharmacogenetic analysis of genes implicated in rodent models of antidepressant response: Association of TREK1 and treatment resistance in the STAR(*)D study. Neuropsychopharmacology 33:2810-2819.
35. Mazella J, et al. (2010) Spadin, a sortilin-derived peptide, targeting rodent TREK-1 channels: A new concept in the antidepressant drug design. PLoS Biol 8:e1000355.
36. DiNitto JP, Cronin TC, Lambright DG (2003) Membrane recognition and targeting by lipid-binding domains. Sci STKE 2003:re16.
37. Rohács T, Chen J, Prestwich GD, Logothetis DE (1999) Distinct specificities of inwardly rectifying K(+) channels for phosphoinositides. J Biol Chem 274:36065-36072.
38. Rohács T, et al. (2003) Specificity of activation by phosphoinositides determines lipid regulation of Kir channels. Proc Natl Acad Sci USA 100:745-750. (Pubitemid 36126123)