Published online before print October 9, 2003, doi: 10.1161/01.RES.0000099883.68414.61
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
© 2003 American Heart Association, Inc.
Cellular Biology |
Two-Pore Domain K Channel, TASK-1, in Pulmonary Artery Smooth Muscle Cells
From the Department of Physiology and Pharmacology (A.M.G., R.J.T.), University of Strathclyde, Glasgow, UK; Quintiles Scotland Ltd (O.N.O., K.M.M.), Heriot-Watt University Research Park, Edinburgh, UK; Institute of Biomedical and Life Sciences (D.M.), University of Glasgow, Glasgow, UK; Argyll and Clyde NHS (F.E.J.K.), Royal Alexandra Hospital, Paisley, UK.
Correspondence to Prof Alison M. Gurney, Department of Physiology and Pharmacology, University of Strathclyde, 27 Taylor St, Glasgow, UK G4 0NR. E-mail a.m.gurney{at}strath.ac.uk
Pulmonary vascular tone is strongly influenced by the resting membrane potential of smooth muscle cells, depolarization promoting Ca2+ influx, and contraction. The resting potential is determined largely by the activity of K+-selective ion channels, the molecular nature of which has been debated for some time. In this study, we provide strong evidence that the two-pore domain K+ channel, TASK-1, mediates a noninactivating, background K+ current (IKN), which sets the resting membrane potential in rabbit pulmonary artery smooth muscle cells (PASMCs). TASK-1 mRNA was found to be present in PASMCs, and the membranes of PASMCs contained TASK-1 protein. Both IKN and the resting potential were found to be exquisitely sensitive to extracellular pH, acidosis inhibiting the current and causing depolarization. Moreover, IKN and the resting potential were enhanced by halothane (1 mmol/L), inhibited by Zn2+ (100 to 200 µmol/L) and anandamide (10 µmol/L), but insensitive to cytoplasmic Ca2+. These properties are all diagnostic of TASK-1 channels and add to previously identified features of IKN that are shared with TASK-1, such as inhibition by hypoxia, low sensitivity to 4-aminopyridine and quinine and insensitivity to tetraethylammonium ions. It is therefore concluded that TASK-1 channels are major contributors to the resting potential in pulmonary artery smooth muscle. They are likely to play an important role in mediating pulmonary vascular responses to changes in extracellular pH, and they could be responsible for the modulatory effects of pH on hypoxic pulmonary vasoconstriction.
Key Words: two-pore domain K channel • pulmonary artery myocyte • smooth muscle • resting potential
This article has been cited by other articles:
 |
|
 |
|
  B. Tang, Y. Li, C. Nagaraj, R. E. Morty, S. Gabor, E. Stacher, R. Voswinckel, N. Weissmann, K. Leithner, H. Olschewski, et al. Endothelin-1 Inhibits Background Two-Pore Domain Channel TASK-1 in Primary Human Pulmonary Artery Smooth Muscle Cells Am. J. Respir. Cell Mol. Biol., October 1, 2009; 41(4): 476 - 483. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. J. Park, Y.-S. Chun, K. S. Park, S. J. Kim, S.-O. Choi, H.-L. Kim, and J.-W. Park Identification of subdomains in NADPH oxidase-4 critical for the oxygen-dependent regulation of TASK-1 K+ channels Am J Physiol Cell Physiol, October 1, 2009; 297(4): C855 - C864. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. E. Lloyd, S. P. Marrelli, and R. M. Bryan Jr. cGMP does not activate two-pore domain K+ channels in cerebrovascular smooth muscle Am J Physiol Heart Circ Physiol, June 1, 2009; 296(6): H1774 - H1780. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Joshi, V. Sedivy, D. Hodyc, J. Herget, and A. M. Gurney KCNQ Modulators Reveal a Key Role for KCNQ Potassium Channels in Regulating the Tone of Rat Pulmonary Artery Smooth Muscle J. Pharmacol. Exp. Ther., April 1, 2009; 329(1): 368 - 376. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. L. Firth, K. H. Yuill, and S. V. Smirnov Mitochondria-dependent regulation of Kv currents in rat pulmonary artery smooth muscle cells Am J Physiol Lung Cell Mol Physiol, July 1, 2008; 295(1): L61 - L70. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. D. Shah Effects of modulators of TASK potassium channels on rat pulmonary artery tone Bioscience Horizons, June 1, 2008; 1(2): 114 - 121. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. J. Hwang, N. O'Kane, C. Singer, S. M. Ward, K. M. Sanders, and S. D. Koh Block of inhibitory junction potentials and TREK-1 channels in murine colon by Ca2+ store-active drugs J. Physiol., February 15, 2008; 586(4): 1169 - 1184. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. M. Bryan Jr, B. K. Joseph, E. Lloyd, and N. J. Rusch Starring TREK-1: The Next Generation of Vascular K+ Channels Circ. Res., July 20, 2007; 101(2): 119 - 121. [Full Text] [PDF]
|
|
|
|
|
|
N. Blondeau, O. Petrault, S. Manta, V. Giordanengo, P. Gounon, R. Bordet, M. Lazdunski, and C. Heurteaux Polyunsaturated Fatty Acids Are Cerebral Vasodilators via the TREK-1 Potassium Channel Circ. Res., July 20, 2007; 101(2): 176 - 184. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Kiyoshi, D. Yamazaki, S. Ohya, M. Kitsukawa, K. Muraki, S.-y. Saito, Y. Ohizumi, and Y. Imaizumi Molecular and electrophysiological characteristics of K+ conductance sensitive to acidic pH in aortic smooth muscle cells of WKY and SHR Am J Physiol Heart Circ Physiol, December 1, 2006; 291(6): H2723 - H2734. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. Fantozzi, O. Platoshyn, A. H. Wong, S. Zhang, C. V. Remillard, M. R. Furtado, O. V. Petrauskene, and J. X.-J. Yuan Bone morphogenetic protein-2 upregulates expression and function of voltage-gated K+ channels in human pulmonary artery smooth muscle cells Am J Physiol Lung Cell Mol Physiol, November 1, 2006; 291(5): L993 - L1004. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. K. Weir and A. Olschewski Role of ion channels in acute and chronic responses of the pulmonary vasculature to hypoxia Cardiovasc Res, September 1, 2006; 71(4): 630 - 641. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Wareing, X. Bai, F. Seghier, C. M. Turner, S. L. Greenwood, P. N. Baker, M. J. Taggart, and G. K. Fyfe Expression and function of potassium channels in the human placental vasculature Am J Physiol Regulatory Integrative Comp Physiol, August 1, 2006; 291(2): R437 - R446. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. M. Bryan Jr., J. You, S. C. Phillips, J. J. Andresen, E. E. Lloyd, P. A. Rogers, S. E. Dryer, and S. P. Marrelli Evidence for two-pore domain potassium channels in rat cerebral arteries Am J Physiol Heart Circ Physiol, August 1, 2006; 291(2): H770 - H780. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 X. Fu, D. G. Beer, J. Behar, J. Wands, D. Lambeth, and W. Cao cAMP-response Element-binding Protein Mediates Acid-induced NADPH Oxidase NOX5-S Expression in Barrett Esophageal Adenocarcinoma Cells J. Biol. Chem., July 21, 2006; 281(29): 20368 - 20382. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Musset, S. G. Meuth, G. X. Liu, C. Derst, S. Wegner, H.-C. Pape, T. Budde, R. Preisig-Muller, and J. Daut Effects of divalent cations and spermine on the K+ channel TASK-3 and on the outward current in thalamic neurons J. Physiol., May 1, 2006; 572(3): 639 - 657. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Olschewski, Y. Li, B. Tang, J. Hanze, B. Eul, R. M. Bohle, J. Wilhelm, R. E. Morty, M. E. Brau, E. K. Weir, et al. Impact of TASK-1 in Human Pulmonary Artery Smooth Muscle Cells Circ. Res., April 28, 2006; 98(8): 1072 - 1080. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. M. Sanders and S. Don Koh Two-pore-domain potassium channels in smooth muscles: new components of myogenic regulation J. Physiol., January 1, 2006; 570(1): 37 - 43. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Yun Cho, E. A. Beckett, S. A. Baker, I. Han, K. J. Park, K. Monaghan, S. M. Ward, K. M. Sanders, and S. D. Koh A pH-sensitive potassium conductance (TASK) and its function in the murine gastrointestinal tract J. Physiol., May 15, 2005; 565(1): 243 - 259. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 X. Bai, G. J Bugg, S. L Greenwood, J. D Glazier, C. P Sibley, P. N Baker, M. J Taggart, and G. K Fyfe Expression of TASK and TREK, two-pore domain K+ channels, in human myometrium Reproduction, April 1, 2005; 129(4): 525 - 530. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. D. Burmester, K.-D. Schluter, J. Daut, and P. J. Hanley Enantioselective Actions of Bupivacaine and Ropivacaine on Coronary Vascular Resistance at Cardiotoxic Concentrations Anesth. Analg., March 1, 2005; 100(3): 707 - 712. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Dubuis, M. Potier, R. Wang, and C. Vandier Continuous inhalation of carbon monoxide attenuates hypoxic pulmonary hypertension development presumably through activation of BKCa channels Cardiovasc Res, February 15, 2005; 65(3): 751 - 761. [Abstract] [Full Text] [PDF]
|
|