11,12-EET Stimulates the Association of BK Channel α and β1 Subunits in Mitochondria to Induce Pulmonary Vasoconstriction

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Loot, Annemarieke E ^a   Moneke, Isabelle ^a   Keserü, Benjamin ^a   Oelze, Matthias ^b   Syzonenko, Tetyana ^a   Daiber, Andreas ^b   Fleming, Ingrid ^a  

^a GOETHE UNIVERSITY   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2 HYDROXY 5 TRIFLUOROMETHYLPHENYL) 5 TRIFLUOROMETHYL 2(3H) BENZIMIDAZOLONE; 11,12 EPOXY 5,8,14 ICOSATRIENOIC ACID; DYE; ENZYME INHIBITOR; EPOXIDE HYDROLASE INHIBITOR; EPOXYICOSATRIENOIC ACID; IBERIOTOXIN; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL ALPHA SUBUNIT; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL BETA SUBUNIT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; PROSTACYCLIN; PROSTAGLANDIN SYNTHASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CELL POPULATION; CELL STIMULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEPOLARIZATION; HUMAN; HUMAN CELL; HYPERPOLARIZATION; HYPOXIA; LUNG ALVEOLUS WALL; LUNG ARTERY PRESSURE; LUNG VASOCONSTRICTION; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PULMONARY ARTERY; PULMONARY ARTERY SMOOTH MUSCLE CELL; SMOOTH MUSCLE FIBER;

8,11,14-EICOSATRIENOIC ACID; ANIMALS; ANOXIA; ARTERIAL PRESSURE; EPOXIDE HYDROLASES; GENE DELETION; HEK293 CELLS; HUMANS; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNEL ALPHA SUBUNITS; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNEL BETA SUBUNITS; LUNG; MEMBRANE POTENTIAL, MITOCHONDRIAL; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MITOCHONDRIA; PULMONARY ARTERY; VASOCONSTRICTION;

MUS;

EID: 84866708034     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046065     Document Type: Article

References (46)

1. Sommer N, Dietrich A, Schermuly RT, Ghofrani HA, Gudermann T, et al. (2008) Regulation of hypoxic pulmonary vasoconstriction: basic mechanisms. Eur Respir J 32: 1639-1651.
2. Michelakis ED, Thebaud B, Weir EK, Archer SL, (2004) Hypoxic pulmonary vasoconstriction: redox regulation of O2-sensitive K+ channels by a mitochondrial O2-sensor in resistance artery smooth muscle cells. J Mol Cell Cardiol 37: 1119-1136.
3. Weissmann N, Sommer N, Schermuly RT, Ghofrani HA, Seeger W, et al. (2006) Oxygen sensors in hypoxic pulmonary vasoconstriction. Cardiovasc Res 71: 620-629.
4. Moudgil R, Michelakis ED, Archer SL, (2006) The role of K+ channels in determining pulmonary vascular tone, oxygen sensing, cell proliferation, and apoptosis: implications in hypoxic pulmonary vasoconstriction and pulmonary arterial hypertension. Microcirculation 13: 615-632.
5. Weir EK, Olschewski A, (2006) Role of ion channels in acute and chronic responses of the pulmonary vasculature to hypoxia. Cardiovasc Res 71: 630-641.
6. Pokreisz P, Fleming I, Kiss L, Barbosa-Sicard E, Fisslthaler B, et al. (2006) Cytochrome P450 epoxygenase gene function in hypoxic pulmonary vasoconstriction and pulmonary vascular remodeling. Hypertension 47: 762-770.
7. Kiss L, Roder Y, Bier J, Weissmann N, Seeger W, et al. (2008) Direct eicosanoid profiling of the hypoxic lung by comprehensive analysis via capillary liquid chromatography with dual online photodiode-array and tandem mass-spectrometric detection. Anal Bioanal Chem 390: 697-714.
8. Keserü B, Barbosa-Sicard E, Popp R, Fisslthaler B, Dietrich A, et al. (2008) Epoxyeicosatrienoic acids and the soluble epoxide hydrolase are determinants of pulmonary artery pressure and the acute hypoxic pulmonary vasoconstrictor response. FASEB J 22: 4306-4315.
9. Wei AD, Gutman GA, Aldrich R, Chandy KG, Grissmer S, et al. (2005) International Union of Pharmacology. LII. Nomenclature and molecular relationships of calcium-activated potassium channels. Pharmacol Rev 57: 463-472.
10. Campbell WB, Fleming I, (2010) Epoxyeicosatrienoic acids and endothelium-dependent responses. Pflugers Arch 459: 881-895.
11. Loot AE, Fleming I, (2011) Cytochrome P450-derived epoxyeicosatrienoic acids and pulmonary hypertension: Central role of transient receptor potential (TRP) C6 channels. J Cardiovasc Pharmacol 57: 140-147.
12. Keserü B, Barbosa-Sicard E, Schermuly RT, Tanaka H, Hammock BD, et al. (2010) Hypoxia-induced pulmonary hypertension: comparison of soluble epoxide hydrolase deletion versus inhibition. Cardiovasc Res 85: 232-240.
13. Jiang Z, Wallner M, Meera P, Toro L, (1999) Human and rodent MaxiK channel β subunit genes: cloning and characterization. Genomics 55: 57-67.
14. Morisseau C, Goodrow MH, Newman JW, Wheelock CE, Dowdy DL, et al. (2002) Structural refinement of inhibitors of urea-based soluble epoxide hydrolases. Biochem Pharmacol 63: 1599-1608.
15. Gauthier KM, Deeter C, Krishna UM, Reddy YK, Bondlela M, et al. (2002) 14,15-Epoxyeicosa-5(Z)-enoic acid: a selective epoxyeicosatrienoic acid antagonist that inhibits endothelium-dependent hyperpolarization and relaxation in coronary arteries. Circ Res 90: 1028-1036.
16. Pluger S, Faulhaber J, Furstenau M, Lohn M, Waldschutz R, et al. (2000) Mice with disrupted BK channel β1 subunit gene feature abnormal Ca2+ spark/STOC coupling and elevated blood pressure. Circ Res 87: E53-E60.
17. Weissmann N, Akkayagil E, Quanz K, Schermuly RT, Ghofrani HA, et al. (2004) Basic features of hypoxic pulmonary vasoconstriction in mice. Respir Physiol Neurobiol 139: 191-202.
18. Weissmann N, Dietrich A, Fuchs B, Kalwa H, Ay M, et al. (2006) Classical transient receptor potential channel 6 (TRPC6) is essential for hypoxic pulmonary vasoconstriction and alveolar gas exchange. Proc Natl Acad Sci USA 103: 19093-19098.
19. McCobb DP, Fowler NL, Featherstone T, Lingle CJ, Saito M, et al. (1995) A human calcium-activated potassium channel gene expressed in vascular smooth muscle. Am J Physiol 269: H767-H777.
20. Randriamboavonjy V, Pistrosch F, Bolck B, Schwinger RH, Dixit M, et al. (2008) Platelet sarcoplasmic endoplasmic reticulum Ca2+-ATPase and μ-calpain activity are altered in type 2 diabetes mellitus and restored by rosiglitazone. Circulation 117: 52-60.
21. Fleming I, Hecker M, Busse R, (1994) Intracellular alkalinization induced by bradykinin sustains activation of the constitutive nitric oxide synthase in endothelial cells. Circ Res 74: 1220-1226.
22. Spear RK, Lumeng L, (1978) A method for isolating lung mitochondria from rabbits, rats, and mice with improved respiratory characteristics. Anal Biochem 90: 211-219.
23. Trenker M, Malli R, Fertschai I, Levak-Frank S, Graier WF, (2007) Uncoupling proteins 2 and 3 are fundamental for mitochondrial Ca2+ uniport. Nat Cell Biol 9: 445-452.
24. Bauersachs J, Popp R, Hecker M, Sauer E, Fleming I, et al. (1996) Nitric oxide attenuates the release of endothelium-derived hyperpolarizing factor. Circulation 94: 3341-3347.
25. Roth M, Rupp M, Hofmann S, Mittal M, Fuchs B, et al. (2009) Heme oxygenase-2 and large-conductance Ca2+-activated K+ channels: lung vascular effects of hypoxia. Am J Respir Crit Care Med 180: 353-364.
26. Xu W, Liu Y, Wang S, McDonald T, Van Eyk JE, et al. (2002) Cytoprotective role of Ca2+- activated K+ channels in the cardiac inner mitochondrial membrane. Science 298: 1029-1033.
27. Wu RS, Marx SO, (2010) The BK potassium channel in the vascular smooth muscle and kidney: α- and β-subunits. Kidney Int 78: 963-974.
28. Sweet TB, Cox DH, (2009) Measuring the influence of the BKCa β1 subunit on Ca2+ binding to the BKCa channel. J Gen Physiol 133: 139-150.
29. Chen Y, Falck JR, Manthati VL, Jat JL, Campbell WB, (2011) 20-Iodo-14,15-epoxyeicosa-8(Z)-enoyl-3-azidophenylsulfonamide: photoaffinity labeling of a 14,15-epoxyeicosatrienoic acid receptor. Biochemistry 50: 3840-3848.
30. Fukao M, Mason HS, Kenyon JL, Horowitz B, Keef KD, (2001) Regulation of BKCa channels expressed in human embryonic kidney 293 cells by epoxyeicosatrienoic acid. Mol Pharmacol 59: 16-23.
31. Michaelis UR, Fleming I, (2006) From endothelium-derived hyperpolarizing factor (EDHF) to angiogenesis: Epoxyeicosatrienoic acids (EETs) and cell signaling. Pharmacol Ther 111: 584-595.
32. Ling S, Sheng JZ, Braun AP, (2004) The calcium-dependent activity of large-conductance, calcium-activated K+ channels is enhanced by Pyk2- and Hck-induced tyrosine phosphorylation. Am J Physiol Cell Physiol 287: C698-C706.
33. Earley S, Heppner TJ, Nelson MT, Brayden JE, (2005) TRPV4 forms a novel Ca2+ signaling complex with ryanodine receptors and BKCa channels. Circ Res 97: 1270-1279.
34. Earley S, Pauyo T, Drapp R, Tavares MJ, Liedtke W, et al. (2009) TRPV4-dependent dilation of peripheral resistance arteries influences arterial pressure. Am J Physiol Heart Circ Physiol 297: H1096-H1102.
35. Fleming I, Rueben A, Popp R, Fisslthaler B, Schrodt S, et al. (2007) Epoxyeicosatrienoic acids regulate TRP channel-dependent Ca2+ signaling and hyperpolarization in endothelial cells. Arterioscler Thromb Vasc Biol 27: 2612-2618.
36. Kim EY, Zou S, Ridgway LD, Dryer SE, (2007) β1-subunits increase surface expression of a large-conductance Ca2+-activated K+ channel isoform. J Neurophysiol 97: 3508-3516.
37. Nimigean CM, Magleby KL, (1999) The β subunit increases the Ca2+ sensitivity of large conductance Ca2+-activated potassium channels by retaining the gating in the bursting states. J Gen Physiol 113: 425-440.
38. Vang A, Mazer J, Casserly B, Choudhary G, (2010) Activation of endothelial BKCa channels causes pulmonary vasodilation. Vascul Pharmacol 53: 122-129.
39. Graier WF, Frieden M, Malli R, (2007) Mitochondria and Ca2+ signaling: old guests, new functions. Pflugers Arch 455: 375-396.
40. Bauersachs J, Popp R, Hecker M, Sauer E, Fleming I, et al. (1996) Nitric oxide attenuates the release of endothelium-derived hyperpolarizing factor. Circulation 94: 3341-3347.
41. Potente M, Fisslthaler B, Busse R, Fleming I, (2003) 11,12-Epoxyeicosatrienoic acid-induced inhibition of FOXO factors promotes endothelial proliferation by down-regulating p27Kip1. J Biol Chem 278: 29619-29625.
42. Michaelis UR, Fisslthaler B, Medhora M, Harder D, Fleming I, et al. (2003) Cytochrome P450 2C9-derived epoxyeicosatrienoic acids induce angiogenesis via cross-talk with the epidermal growth factor receptor (EGFR). FASEB J 17: 770-772.
43. Schubert R, Nelson MT, (2001) Protein kinases: tuners of the BKCa channel in smooth muscle. Trends Pharmacol Sci 22: 505-512.
44. Gielis JF, Lin JY, Wingler K, van Schil PEY, Schmidt HH, et al. (2011) Pathogenetic role of eNOS uncoupling in cardiopulmonary disorders. Free Radic Biol Med 50: 765-776.
45. Fike CD, Kaplowitz MR, Zhang Y, Pfister SL, (2005) Cyclooxygenase-2 and an early stage of chronic hypoxia-induced pulmonary hypertension in newborn pigs. J Appl Physiol 98: 1111-1118.
46. Ahn YT, Kim YM, Adams ES, Lyu SC, Alvira CM, et al. (2012) Hypoxia inducible factor 1α regulates KCNMB1 expression in human pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 302: L352-L359.