TWIK-2 channel deficiency leads to pulmonary hypertension through a rho-kinase-mediated process

Hypertension

Volumn 64, Issue 6, 2014, Pages 1260-1265

  Pandit, Lavannya M ^a   Lloyd, Eric E ^b   Reynolds, Julia O ^c   Lawrence, William S ^d   Reynolds, Corey ^c   Wehrens, Xander H T ^a,c   Bryan, Robert M ^a,b,c  

^a MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b Children's Research Institute   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d University of Texas Medical Branch School of Medicine   (United States)

Author keywords

KCNK6; Potassium channel; Pulmonary hypertension; Rho kinase; TWIK 2

Indexed keywords

15 HYDROXY 11ALPHA,9ALPHA EPOXYMETHANOPROSTA 5,13 DIENOIC ACID; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; FASUDIL; POTASSIUM CHANNEL; RHO KINASE; TWIK 2 PROTEIN; UNCLASSIFIED DRUG; DNA; KCNK6 PROTEIN, MOUSE; TANDEM PORE DOMAIN POTASSIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; ENZYME INHIBITION; HEART LEFT VENTRICLE SIZE; HEART RIGHT VENTRICLE ENDDIASTOLIC VOLUME; MOUSE; MUSCLE FIBER CONTRACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PULMONARY ARTERY; PULMONARY HYPERTENSION; SYSTOLIC BLOOD PRESSURE; VASCULAR REMODELING; VASCULAR SMOOTH MUSCLE; ANIMAL; BIOSYNTHESIS; BLOOD PRESSURE; DEFICIENCY; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; HEART RIGHT VENTRICLE FUNCTION; KNOCKOUT MOUSE; MALE; METABOLISM; PATHOPHYSIOLOGY;

ANIMALS; BLOOD PRESSURE; DISEASE MODELS, ANIMAL; DNA; GENE EXPRESSION REGULATION; GENOTYPE; HYPERTENSION, PULMONARY; MALE; MICE; MICE, KNOCKOUT; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; PULMONARY ARTERY; RHO-ASSOCIATED KINASES; VENTRICULAR FUNCTION, RIGHT;

EID: 84922480956     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.114.03406     Document Type: Article

References (41)

1. McLaughlin VV, Archer SL, Badesch DB, Barst RJ, Farber HW, Lindner JR, Mathier MA, McGoon MD, Park MH, Rosenson RS, Rubin LJ, Tapson VF, Varga J. ACCF/AHA 2009 expert consensus document on pulmonary hypertension: a report of the American College of Cardiology Foundation Task Force on Expert Consensus Documents and the American Heart Association: developed in collaboration with the American College of Chest Physicians, American Thoracic Society, Inc., and the Pulmonary Hypertension Association. Circulation. 2009;119:2250-2294.
2. Kuhr FK, Smith KA, Song MY, Levitan I, Yuan JX. New mechanisms of pulmonary arterial hypertension: role of Ca2+ signaling. Am J Physiol Heart Circ Physiol. 2012;302:H1546-H1562.
3. Badesch DB, Raskob GE, Elliott CG, Krichman AM, Farber HW, Frost AE, Barst RJ, Benza RL, Liou TG, Turner M, Giles S, Feldkircher K, Miller DP, McGoon MD. Pulmonary arterial hypertension: baseline characteristics from the REVEAL Registry. Chest. 2010;137:376-387.
4. Simonneau G, Gatzoulis MA, Adatia I, Celermajer D, Denton C, Ghofrani A, Gomez Sanchez MA, Krishna KR, Landzberg M, Machado RF, Olschewski H, Robbins IM, Souza R. Updated clinical classification of pulmonary hypertension. J Am Coll Cardiol. 2013;62:D34-D41.
5. Stenmark KR, Davie N, Frid M, Gerasimovskaya E, Das M. Role of the adventitia in pulmonary vascular remodeling. Physiology. 2006;21:134-145.
6. Tuder RM, Marecki JC, Richter A, Fijalkowska I, Flores S. Pathology of pulmonary hypertension. Clin Chest Med. 2007;28:23-42, vii.
7. Morrell NW, Adnot S, Archer SL, Dupuis J, Jones PL, MacLean MR, McMurtry IF, Stenmark KR, Thistlethwaite PA, Weissmann N, Yuan JX, Weir EK. Cellular and molecular basis of pulmonary arterial hypertension. J Am Coll Cardiol. 2009;54(1 Suppl):S20-S31.
8. Yuan JX, Rubin LJ. Pathogenesis of pulmonary arterial hypertension: the need for multiple hits. Circulation. 2005;111:534-538.
9. Bonnet S, Archer SL. Potassium channel diversity in the pulmonary arteries and pulmonary veins: implications for regulation of the pulmonary vasculature in health and during pulmonary hypertension. Pharmacol Ther. 2007;115:56-69.
10. Moudgil R, Michelakis ED, Archer SL. 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. 2006;13:615-632.
11. Archer SL, Souil E, Dinh-Xuan AT, Schremmer B, Mercier JC, El Yaagoubi A, Nguyen-Huu L, Reeve HL, Hampl V. Molecular identification of the role of voltage-gated K+ channels, Kv1.5 and Kv2.1, in hypoxic pulmonary vasoconstriction and control of resting membrane potential in rat pulmonary artery myocytes. J Clin Invest. 1998;101:2319-2330.
12. Archer SL, Wu XC, Thébaud B, Nsair A, Bonnet S, Tyrrell B, McMurtry MS, Hashimoto K, Harry G, Michelakis ED. Preferential expression and function of voltage-gated, O2-sensitive K+ channels in resistance pulmonary arteries explains regional heterogeneity in hypoxic pulmonary vasoconstriction: ionic diversity in smooth muscle cells. Circ Res. 2004;95:308-318.
13. Archer SL, London B, Hampl V, Wu X, Nsair A, Puttagunta L, Hashimoto K, Waite RE, Michelakis ED. Impairment of hypoxic pulmonary vasoconstriction in mice lacking the voltage-gated potassium channel Kv1.5. FASEB J. 2001;15:1801-1803.
14. Rabinovitch M. Molecular pathogenesis of pulmonary arterial hypertension. J Clin Invest. 2008;118:2372-2379.
15. Wang J, Juhaszova M, Rubin LJ, Yuan XJ. Hypoxia inhibits gene expression of voltage-gated K+ channel alpha subunits in pulmonary artery smooth muscle cells. J Clin Invest. 1997;100:2347-2353.
16. Gurney AM, Osipenko ON, MacMillan D, McFarlane KM, Tate RJ, Kempsill FE. Two-pore domain K channel, TASK-1, in pulmonary artery smooth muscle cells. Circ Res. 2003;93:957-964.
17. Ma L, Roman-Campos D, Austin ED, et al. A novel channelopathy in pulmonary arterial hypertension. N Engl J Med. 2013;369:351-361.
18. Nielsen G, Wandall-Frostholm C, Sadda V, Oliván-Viguera A, Lloyd EE, Bryan RM Jr, Simonsen U, Köhler R. Alterations of N-3 polyunsaturated fatty acid-activated K2P channels in hypoxia-induced pulmonary hypertension. Basic Clin Pharmacol Toxicol. 2013;113:250-258.
19. 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. Impact of TASK-1 in human pulmonary artery smooth muscle cells. Circ Res. 2006;98:1072-1080.
20. Manoury B, Lamalle C, Oliveira R, Reid J, Gurney AM. Contractile and electrophysiological properties of pulmonary artery smooth muscle are not altered in TASK-1 knockout mice. J Physiol. 2011;589(pt 13):3231-3246.
21. Gardener MJ, Johnson IT, Burnham MP, Edwards G, Heagerty AM, Weston AH. Functional evidence of a role for two-pore domain potassium channels in rat mesenteric and pulmonary arteries. Br J Pharmacol. 2004;142:192-202.
22. Gurney A, Manoury B. Two-pore potassium channels in the cardiovascular system. Eur Biophys J. 2009;38:305-318.
23. Lloyd EE, Marrelli SP, Bryan RM Jr. cGMP does not activate two-pore domain K+ channels in cerebrovascular smooth muscle. Am J Physiol Heart Circ Physiol. 2009;296:H1774-H1780.
24. Lloyd EE, Crossland RF, Phillips SC, Marrelli SP, Reddy AK, Taffet GE, Hartley CJ, Bryan RM Jr. Disruption of K (2P) 6.1 produces vascular dysfunction and hypertension in mice. Hypertension. 2011;58:672-678.
25. Tabima DM, Hacker TA, Chesler NC. Measuring right ventricular function in the normal and hypertensive mouse hearts using admittancederived pressure-volume loops. Am J Physiol Heart Circ Physiol. 2010;299:H2069-H2075.
26. Vonk Noordegraaf A, Galiè N. The role of the right ventricle in pulmonary arterial hypertension. Eur Respir Rev. 2011;20:243-253.
27. Jiang BH, Tawara S, Abe K, Takaki A, Fukumoto Y, Shimokawa H. Acute vasodilator effect of fasudil, a Rho-kinase inhibitor, in monocrotaline-induced pulmonary hypertension in rats. J Cardiovasc Pharmacol. 2007;49:85-89.
28. Medhurst AD, Rennie G, Chapman CG, Meadows H, Duckworth MD, Kelsell RE, Gloger II, Pangalos MN. Distribution analysis of human two pore domain potassium channels in tissues of the central nervous system and periphery. Brain Res Mol Brain Res. 2001;86:101-114.
29. Patel AJ, Maingret F, Magnone V, Fosset M, Lazdunski M, Honoré E. TWIK-2, an inactivating 2P domain K+ channel. J Biol Chem. 2000;275:28722-28730.
30. Salinas M, Reyes R, Lesage F, Fosset M, Heurteaux C, Romey G, Lazdunski M. Cloning of a new mouse two-P domain channel subunit and a human homologue with a unique pore structure. J Biol Chem. 1999;274:11751-11760.
31. De Godoy MA, Rattan S. Role of rho kinase in the functional and dysfunctional tonic smooth muscles. Trends Pharmacol Sci. 2011;32:384-393.
32. Satoh K, Fukumoto Y, Shimokawa H. Rho-kinase: important new therapeutic target in cardiovascular diseases. Am J Physiol Heart Circ Physiol. 2011;301:H287-H296.
33. Cahill E, Rowan SC, Sands M, Banahan M, Ryan D, Howell K, McLoughlin P. The pathophysiological basis of chronic hypoxic pulmonary hypertension in the mouse: vasoconstrictor and structural mechanisms contribute equally. Exp Physiol. 2012;97:796-806.
34. Abe K, Shimokawa H, Morikawa K, Uwatoku T, Oi K, Matsumoto Y, Hattori T, Nakashima Y, Kaibuchi K, Sueishi K, Takeshit A. Long-term treatment with a Rho-kinase inhibitor improves monocrotaline-induced fatal pulmonary hypertension in rats. Circ Res. 2004;94:385-393.
35. Abe K, Tawara S, Oi K, Hizume T, Uwatoku T, Fukumoto Y, Kaibuchi K, Shimokawa H. Long-term inhibition of Rho-kinase ameliorates hypoxiainduced pulmonary hypertension in mice. J Cardiovasc Pharmacol. 2006;48:280-285.
36. Fagan KA, Oka M, Bauer NR, Gebb SA, Ivy DD, Morris KG, McMurtry IF. Attenuation of acute hypoxic pulmonary vasoconstriction and hypoxic pulmonary hypertension in mice by inhibition of Rho-kinase. Am J Physiol Lung Cell Mol Physiol. 2004;287:L656-L664.
37. Ishikura K, Yamada N, Ito M, Ota S, Nakamura M, Isaka N, Nakano T. Beneficial acute effects of rho-kinase inhibitor in patients with pulmonary arterial hypertension. Circ J. 2006;70:174-178.
38. Fukumoto Y, Matoba T, Ito A, Tanaka H, Kishi T, Hayashidani S, Abe K, Takeshita A, Shimokawa H. Acute vasodilator effects of a Rho-kinase inhibitor, fasudil, in patients with severe pulmonary hypertension. Heart. 2005;91:391-392.
39. Sakurada S, Takuwa N, Sugimoto N, Wang Y, Seto M, Sasaki Y, Takuwa Y. Ca2+-dependent activation of Rho and Rho kinase in membrane depolarization-induced and receptor stimulation-induced vascular smooth muscle contraction. Circ Res. 2003;93:548-556.
40. Urban NH, Berg KM, Ratz PH. K+ depolarization induces RhoA kinase translocation to caveolae and Ca2+ sensitization of arterial muscle. Am J Physiol Cell Physiol. 2003;285:C1377-C1385.
41. Fernández-Tenorio M, Porras-González C, Castellano A, Del Valle-Rodríguez A, López-Barneo J, Ureña J. Metabotropic regulation of RhoA/Rho-associated kinase by L-type Ca2+ channels: new mechanism for depolarization-evoked mammalian arterial contraction. Circ Res. 2011;108:1348-1357.