[en] The acid-sensitive, two-pore domain K(+) channel, TASK-1, contributes to the background K(+) conductance and membrane potential (Em) of rat and human pulmonary artery (PA) smooth muscle cells (SMC), but its role in regulating tone remains elusive. This study aimed to clarify the role of TASK-1 by determining the functional properties of PA from mice in which the TASK-1 gene was deleted (TASK-1/3 KO), in comparison with wild type (WT) C57BL/6 controls. Small vessel wire myography was used to measure isometric tension developed by intact PA. Em and currents were recorded from freshly isolated PASMC using the perforated patch-clamp technique. Reverse-transcription polymerase chain reaction (RT-PCR) was used to estimate K(+) channel expression. We could find no difference between PA from WT and TASK-1/3 KO TASK KO mice. They showed similar constrictor responses to a range of agonists and K(+) concentrations, the K(+) channel blockers 4-aminopyridine, tetraethylammonuim ions and XE991. Treprostinil, proposed to dilate by activating TASK-1, was just as effective in TASK-1/3 KO arteries. Blocking Ca(2+) influx with nifedipine (1 muM) or levcromakalim (10 muM) had no effect on resting tone in either strain. The resting Em of PASMC and its responses to K(+) channel blockers were unchanged in TASK-1/3 KO mice as were voltage-activated K(+) currents, including the non-inactivating K(+) current (I(KN)) measured at 0 mV. The Em was, however, depolarised in comparison with other species. Mouse I(KN) was much smaller than in rat and showed no sensitivity to pH. The results imply that TASK-1 does not form a functional channel in mouse PASMC.
Disciplines :
Pharmacy, pharmacology & toxicology
Author, co-author :
Manoury, B.
Lamalle, Caroline ; Université de Liège - ULiège > Département de pharmacie > Analyse des médicaments
Oliveira, R.
Reid, J.
Gurney, A. M.
Language :
English
Title :
Contractile and electrophysiological properties of pulmonary artery smooth muscle are not altered in TASK-1 knockout mice.
Publication date :
April 2011
Journal title :
Journal of Physiology
ISSN :
0022-3751
eISSN :
1469-7793
Publisher :
Blackwell Publishing, New York, United States - New York
Aller MI, Veale EL, Linden AM, Sandu C, Schwaninger M, Evans LJ, Korpi ER, Mathie A, Wisden W & Brickley SG (2005). Modifying the subunit composition of TASK channels alters the modulation of a leak conductance in cerebellar granule neurons. J Neurosci 25, 11455-11467.
Archer SL, London B, Hampl V, Wu X, Nsair A, Puttagunta L, Hashimoto K, Waite RE & Michelakis ED (2001). Impairment of hypoxic pulmonary vasoconstriction in mice lacking the voltage-gated potassium channel Kv1.5. FASEB J 15, 1801-1803.
Archer SL, Reeve HL, Michelakis E, Puttagunta L, Waite R, Nelson DP, Dinauer MC & Weir EK (1999). O 2 sensing is preserved in mice lacking the gp91 phox subunit of NADPH oxidase. Proc Natl Acad Sci U S A 96, 7944-7949.
Archer SL, Wu XC, Thebaud B, Nsair A, Bonnet S, Tyrrell B, McMurtry MS, Hashimoto K, Harry G & Michelakis ED (2004). Preferential expression and function of voltage-gated, O 2-sensitive K + channels in resistance pulmonary arteries explains regional heterogeneity in hypoxic pulmonary vasoconstriction: ionic diversity in smooth muscle cells. Circ Res 95, 308-318.
Barry PH & Lynch JW (1991). Liquid junction potentials and small cell effects in patch-clamp analysis. J Membr Biol 121, 101-117.
Bieger D (2006). β-Adrenoceptor mediated responses in rat pulmonary artery: putative role of TASK-1 related K channels. Naunyn Schmiedebergs Arch Pharmacol 373, 186-196.
Brickley SG, Aller MI, Sandu C, Veale EL, Alder FG, Sambi H, Mathie A & Wisden W (2007). TASK-3 two-pore domain potassium channels enable sustained high-frequency firing in cerebellar granule neurons. J Neurosci 27, 9329-9340.
Casteels R, Kitamura K, Kuriyama H & Suzuki H (1977a). Excitation-contraction coupling in the smooth muscle cells of the rabbit main pulmonary artery. J Physiol 271, 63-79.
Casteels R, Kitamura K, Kuriyama H & Suzuki H (1977b). The membrane properties of the smooth muscle cells of the rabbit main pulmonary artery. J Physiol 271, 41-61.
Chin KM & Rubin LJ (2008). Pulmonary arterial hypertension. J Am Coll Cardiol 51, 1527-1538.
Choi YS, Jeong YS, Ok SH, Shin IW, Lee SH, Park JY, Hwang EM, Hah YS & Sohn JT (2010). The direct effect of levobupivacaine in isolated rat aorta involves lipoxygenase pathway activation and endothelial nitric oxide release. Anesth Analg 110, 341-349.
Clapp LH & Gurney AM (1991). Modulation of calcium movements by nitroprusside in isolated vascular smooth muscle cells. Pflugers Arch 418, 462-470.
Clapp LH & Gurney AM (1992). ATP-sensitive K + channels regulate resting potential of pulmonary arterial smooth muscle cells. Am J Physiol Heart Circ Physiol 262, H916-H920.
Delmas P & Brown DA (2005). Pathways modulating neural KCNQ/M (Kv7) potassium channels. Nat Rev Neurosci 6, 850-862.
Evans AM, Osipenko ON & Gurney AM (1996). Properties of a novel K + current that is active at resting potential in rabbit pulmonary artery smooth muscle cells. J Physiol 496, 407-420.
Evans AM, Osipenko ON, Haworth SG & Gurney AM (1998). Resting potentials and potassium currents during development of pulmonary artery smooth muscle cells. Am J Physiol Heart Circ Physiol 275, H887-H899.
Gardener MJ, Johnson IT, Burnham MP, Edwards G, Heagerty AM & Weston AH (2004). Functional evidence of a role for two-pore domain potassium channels in rat mesenteric and pulmonary arteries. Br J Pharmacol 142, 192-202.
Goldstein SA, Bayliss DA, Kim D, Lesage F, Plant LD & Rajan S (2005). International Union of Pharmacology. LV. Nomenclature and molecular relationships of two-P potassium channels. Pharmacol Rev 57, 527-540.
Gonczi M, Szentandrassy N, Johnson IT, Heagerty AM & Weston AH (2006). Investigation of the role of TASK-2 channels in rat pulmonary arteries; pharmacological and functional studies following RNA interference procedures. Br J Pharmacol 147, 496-505.
Gurney A & Manoury B (2009). Two-pore potassium channels in the cardiovascular system. Eur Biophys J 38, 305-318.
Gurney AM, Osipenko ON, MacMillan D & Kempsill FE (2002). Potassium channels underlying the resting potential of pulmonary artery smooth muscle cells. Clin Exp Pharmacol Physiol 29, 330-333.
Gurney AM, Osipenko ON, MacMillan D, McFarlane KM, Tate RJ & Kempsill FE (2003). Two-pore domain K channel, TASK-1, in pulmonary artery smooth muscle cells. Circ Res 93, 957-964.
Heitzmann D, Derand R, Jungbauer S, Bandulik S, Sterner C, Schweda F, El WA, Lalli E, Guy N, Mengual R, Reichold M, Tegtmeier I, Bendahhou S, Gomez-Sanchez CE, Aller MI, Wisden W, Weber A, Lesage F, Warth R & Barhanin J (2008). Invalidation of TASK1 potassium channels disrupts adrenal gland zonation and mineralocorticoid homeostasis. EMBO J 27, 179-187.
Joshi S, Balan P & Gurney AM (2006). Pulmonary vasoconstrictor action of KCNQ potassium channel blockers. Respir Res 7, 31.
Joshi S, Sedivy V, Hodyc D, Herget J & Gurney AM (2009). KCNQ modulators reveal a key role for KCNQ potassium channels in regulating the tone of rat pulmonary artery smooth muscle. J Pharmacol Exp Ther 329, 368-376.
Kindler CH, Yost CS & Gray AT (1999). Local anesthetic inhibition of baseline potassium channels with two pore domains in tandem. Anesthesiology 90, 1092-1102.
Ko EA, Burg ED, Platoshyn O, Msefya J, Firth AL & Yuan JX (2007). Functional characterization of voltage-gated K + channels in mouse pulmonary artery smooth muscle cells. Am J Physiol Cell Physiol 293, C928-C937.
Lesage F & Lazdunski M (2000). Molecular and functional properties of two-pore-domain potassium channels. Am J Physiol Renal Physiol 279, F793-F801.
MacLean MR, Deuchar GA, Hicks MN, Morecroft I, Shen S, Sheward J, Colston J, Loughlin L, Nilsen M, Dempsie Y & Harmar A (2004). Overexpression of the 5-hydroxytryptamine transporter gene: effect on pulmonary hemodynamics and hypoxia-induced pulmonary hypertension. Circulation 109, 2150-2155.
Maingret F, Patel AJ, Lazdunski M & Honore E (2001). The endocannabinoid anandamide is a direct and selective blocker of the background K + channel TASK-1. EMBO J 20, 47-54.
Manoury B, Etheridge SL, Reid J & Gurney AM (2009). Organ culture mimics the effects of hypoxia on membrane potential, K + channels and vessel tone in pulmonary artery. Br J Pharmacol 158, 848-861.
Mathie A (2007). Neuronal two-pore-domain potassium channels and their regulation by G protein-coupled receptors. J Physiol 578, 377-385.
McCulloch KM, Kempsill FE, Buchanan KJ & Gurney AM (2000). Regional distribution of potassium currents in the rabbit pulmonary arterial circulation. Exp Physiol 85, 487-496.
Nelson MT, Patlak JB, Worley JF & Standen NB (1990). Calcium channels, potassium channels, and voltage dependence of arterial smooth muscle tone. Am J Physiol Cell Physiol 259, C3-C18.
Olschewski A, Li Y, Tang B, Hanze J, Eul B, Bohle RM, Wilhelm J, Morty RE, Brau ME, Weir EK, Kwapiszewska G, Klepetko W, Seeger W & Olschewski H (2006). Impact of TASK-1 in human pulmonary artery smooth muscle cells. Circ Res 98, 1072-1080.
Osipenko ON & Gurney AM. (1995). The identification of the ionic currents in human intrapulmonary artery myocytes. Br J Pharmacol 116, P406.
Osipenko ON, Alexander D, MacLean MR & Gurney AM (1998). Influence of chronic hypoxia on the contributions of non-inactivating and delayed rectifier K currents to the resting potential and tone of rat pulmonary artery smooth muscle. Br J Pharmacol 124, 1335-1337.
Osipenko ON, Evans AM & Gurney AM (1997). Regulation of the resting potential of rabbit pulmonary artery myocytes by a low threshold, O 2-sensing potassium current. Br J Pharmacol 120, 1461-1470.
Peng W, Michael JR, Hoidal JR, Karwande SV & Farrukh IS (1998). ET-1 modulates K Ca-channel activity and arterial tension in normoxic and hypoxic human pulmonary vasculature. Am J Physiol Lung Cell Mol Physiol 275, L729-L739.
Platoshyn O, Brevnova EE, Burg ED, Yu Y, Remillard CV & Yuan JX (2006). Acute hypoxia selectively inhibits KCNA5 channels in pulmonary artery smooth muscle cells. Am J Physiol Cell Physiol 290, C907-C916.
Post JM, Gelband CH & Hume JR (1995). [Ca 2+] i inhibition of K + channels in canine pulmonary artery. Novel mechanism for hypoxia-induced membrane depolarization. Circ Res 77, 131-139.
Rae J, Cooper K, Gates P & Watsky M (1991). Low access resistance perforated patch recordings using amphotericin B. J Neurosci Methods 37, 15-26.
Randall MD, Alexander SP, Bennett T, Boyd EA, Fry JR, Gardiner SM, Kemp PA, McCulloch AI & Kendall DA (1996). An endogenous cannabinoid as an endothelium-derived vasorelaxant. Biochem Biophys Res Commun 229, 114-120.
Remillard CV & Yuan JX (2004). Activation of K + channels: an essential pathway in programmed cell death. Am J Physiol Lung Cell Mol Physiol 286, L49-L67.
Schubert R, Serebryakov VN, Mewes H & Hopp HH (1997). Iloprost dilates rat small arteries: role of K ATP- and K Ca-channel activation by cAMP-dependent protein kinase. Am J Physiol Heart Circ Physiol 272, H1147-H1156.
Shah S (2008). Effects of modulators of TASK potassium channels on rat pulmonary artery tone. Bioscience Horizons 1, 114-121.
Shimoda LA, Sylvester JT & Sham JS (1998). Inhibition of voltage-gated K + current in rat intrapulmonary arterial myocytes by endothelin-1. Am J Physiol Lung Cell Mol Physiol 274, L842-L853.
Shimoda LA, Sylvester JT, Booth GM, Shimoda TH, Meeker S, Undem BJ & Sham JS (2001b). Inhibition of voltage-gated K + currents by endothelin-1 in human pulmonary arterial myocytes. Am J Physiol Lung Cell Mol Physiol 281, L1115-L1122.
Smirnov SV, Beck R, Tammaro P, Ishii T & Aaronson PI (2002). Electrophysiologically distinct smooth muscle cell subtypes in rat conduit and resistance pulmonary arteries. J Physiol 538, 867-878.
Tang B, Li Y, Nagaraj C, Morty RE, Gabor S, Stacher E, Voswinckel R, Weissmann N, Leithner K, Olschewski H & Olschewski A (2009). Endothelin-1 inhibits background two-pore domain channel TASK-1 in primary human pulmonary artery smooth muscle cells. Am J Respir Cell Mol Biol 41, 476-483.
Trapp S, Aller MI, Wisden W & Gourine AV (2008a). A role for TASK-1 (KCNK3) channels in the chemosensory control of breathing. J Neurosci 28, 8844-8850.
Trapp S, Aller MI, Wisden W & Gourine AV (2008b). A role for TASK-1 (KCNK3) channels in the chemosensory control of breathing. J Neurosci 28, 8844-8850.
Walsh JV Jr & Singer JJ (1980). Penetration-induced hyperpolarization as evidence for Ca 2+ activation of K + conductance in isolated smooth muscle cells. Am J Physiol Cell Physiol 239, C182-C189.
Ward JP & Snetkov VA (2004). Determination of signaling pathways responsible for hypoxic pulmonary vasoconstriction: use of the small vessel myograph. Methods Enzymol 381, 71-87.
White R, Ho WS, Bottrill FE, Ford WR & Hiley CR (2001). Mechanisms of anandamide-induced vasorelaxation in rat isolated coronary arteries. Br J Pharmacol 134, 921-929.
Xu M, Platoshyn O, Makino A, Dillmann WH, Akassoglou K, Remillard CV & Yuan JX (2008). Characterization of agonist-induced vasoconstriction in mouse pulmonary artery. Am J Physiol Heart Circ Physiol 294, H220-H228.
Yeung SY, Pucovsky V, Moffatt JD, Saldanha L, Schwake M, Ohya S & Greenwood IA (2007). Molecular expression and pharmacological identification of a role for K v7 channels in murine vascular reactivity. Br J Pharmacol 151, 758-770.