Inhalation of the BKCa -opener NS1619 attenuates right ventricular pressure and improves oxygenation in the rat monocrotaline model of pulmonary hypertension

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Revermann, Marc ^a,b   Neofitidou, Skevi ^a   Kirschning, Thomas ^a   Schloss, Manuel ^b   Brandes, Ralf P ^b   Hofstetter, Christian ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2 HYDROXY 5 TRIFLUOROMETHYLPHENYL) 5 TRIFLUOROMETHYL 2(3H) BENZIMIDAZOLONE; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; ARTERY MUSCLE; ARTICLE; BLOOD GAS ANALYSIS; BLOOD OXYGENATION; CARDIOPULMONARY HEMODYNAMICS; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVATION; HEART RIGHT VENTRICLE PRESSURE; IN VITRO STUDY; MALE; NONHUMAN; OUTCOME ASSESSMENT; OXYGEN SUPPLY; PROTEIN EXPRESSION; PULMONARY ARTERY; PULMONARY HYPERTENSION; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ADMINISTRATION, INHALATION; ANIMALS; BENZIMIDAZOLES; BLOTTING, WESTERN; CELL PROLIFERATION; CELLS, CULTURED; HEMODYNAMICS; HYPERTENSION, PULMONARY; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MALE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MONOCROTALINE; MYOCYTES, SMOOTH MUSCLE; OXYGEN; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-SIS; PULMONARY ARTERY; RATS; RATS, SPRAGUE-DAWLEY; VENTRICULAR DYSFUNCTION, RIGHT; VENTRICULAR PRESSURE;

EID: 84900336432     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086636     Document Type: Article

References (47)

1. Badesch DB, Champion HC, Sanchez MA, Hoeper MM, Loyd JE, et al. (2009) Diagnosis and assessment of pulmonary arterial hypertension. J Am Coll Cardiol 54: S55-S66. S0735-1097(09)01214-5 [pii];10.1016/j.jacc.2009.04.011 [doi].
2. Barst RJ, Gibbs JS, Ghofrani HA, Hoeper MM, McLaughlin VV, et al. (2009) Updated evidence-based treatment algorithm in pulmonary arterial hypertension. J Am Coll Cardiol 54: S78-S84. S0735-1097(09)01223-6 [pii];10.1016/j.jacc.2009. 04.017 [doi].
3. Vang A, Mazer J, Casserly B, Choudhary G (2010) Activation of endothelial BKCa channels causes pulmonary vasodilation. Vascul Pharmacol 53: 122-129. S1537-1891(10)00088-1 [pii];10.1016/j.vph.2010.05.001 [doi].
4. Edwards G, Niederste-Hollenberg A, Schneider J, Noack T, Weston AH (1994) Ion channel modulation by NS 1619, the putative BKCa channel opener, in vascular smooth muscle. Br J Pharmacol 113: 1538-1547. (Pubitemid 24364445)
5. Bonnet S, Archer SL (2007) 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 115: 56-69. S0163-7258(07)00076-9 [pii];10.1016/j.pharmthera.2007.03.014 [doi].
6. Brayden JE, Nelson MT (1992) Regulation of arterial tone by activation of calcium-dependent potassium channels. Science 256: 532-535.
7. Blackiston DJ, McLaughlin KA, Levin M (2009) Bioelectric controls of cell proliferation: ion channels, membrane voltage and the cell cycle. Cell Cycle 8: 3519-3528. 9888 [pii].
8. Revermann M, Barbosa-Sicard E, Dony E, Schermuly RT, Morisseau C, et al. (2009) Inhibition of the soluble epoxide hydrolase attenuates monocrotaline-induced pulmonary hypertension in rats. J Hypertens 27: 322-331.
9. Dahal BK, Cornitescu T, Tretyn A, Pullamsetti SS, Kosanovic D, et al. (2010) Role of epidermal growth factor inhibition in experimental pulmonary hypertension. Am J Respir Crit Care Med 181: 158-167. 200811-1682OC [pii];10.1164/rccm.200811-1682OC [doi].
10. Archer SL, Souil E, Dinh-Xuan AT, Schremmer B, Mercier JC, et al. (1998) 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 101: 2319-2330. 10.1172/JCI333 [doi]. (Pubitemid 28270426)
11. Zhao YJ, Wang J, Rubin LJ, Yuan XJ (1998) Roles of K+ and Cl- channels in cAMP-induced pulmonary vasodilation. Exp Lung Res 24: 71-83. (Pubitemid 28092536)
12. Barnes PJ, Liu SF (1995) Regulation of pulmonary vascular tone. Pharmacol Rev 47: 87-131.
13. Nelson MT, Quayle JM (1995) Physiological roles and properties of potassium channels in arterial smooth muscle. Am J Physiol 268: C799-C822.
14. Bonnet S, Savineau JP, Barillot W, Dubuis E, Vandier C, et al. (2003) Role of Ca(2+)-sensitive K(+) channels in the remission phase of pulmonary hypertension in chronic obstructive pulmonary diseases. Cardiovasc Res 60: 326-336. S0008636303005273 [pii].
15. Bae YM, Park MK, Lee SH, Ho WK, Earm YE (1999) Contribution of Ca2+- activated K+ channels and non-selective cation channels to membrane potential of pulmonary arterial smooth muscle cells of the rabbit. J Physiol 514 (Pt 3): 747-758. (Pubitemid 29060321)
16. Nagaoka T, Fagan KA, Gebb SA, Morris KG, Suzuki T, et al. (2005) Inhaled Rho kinase inhibitors are potent and selective vasodilators in rat pulmonary hypertension. Am J Respir Crit Care Med 171: 494-499. 200405-637OC [pii];10.1164/rccm.200405-637OC [doi].
17. White RE, Kryman JP, El-Mowafy AM, Han G, Carrier GO (2000) cAMP-dependent vasodilators cross-activate the cGMP-dependent protein kinase to stimulate BK(Ca) channel activity in coronary artery smooth muscle cells. Circ Res 86: 897-905. (Pubitemid 30246988)
18. Bolotina VM, Najibi S, Palacino JJ, Pagano PJ, Cohen RA (1994) Nitric oxide directly activates calcium-dependent potassium channels in vascular smooth muscle. Nature 368: 850-853. 10.1038/368850a0 [doi]. (Pubitemid 24137748)
19. Barman SA, Zhu S, Han G, White RE (2003) cAMP activates BKCa channels in pulmonary arterial smooth muscle via cGMP-dependent protein kinase. Am J Physiol Lung Cell Mol Physiol 284: L1004-L1011. 10.1152/ajplung.00295.2002 [doi];00295.2002 [pii].
20. Montani D, Chaumais MC, Guignabert C, Gunther S, Girerd B, et al. (2013) Targeted therapies in pulmonary arterial hypertension. Pharmacol Ther. S0163-7258(13)00207-6 [pii];10.1016/j.pharmthera.2013.10.002 [doi].
21. Carlino C, Tobias JD, Schneider RI, Heller RL, Alpert MA, et al. (2010) Pulmonary hemodynamic response to acute combination and monotherapy with sildenafil and brain natriuretic peptide in rats with monocrotaline-induced pulmonary hypertension. Am J Med Sci 339: 55-59. 10.1097/MAJ.0-b013e3181c078d7 [doi].
22. Falcao-Pires I, Goncalves N, Henriques-Coelho T, Moreira-Goncalves D, Roncon-Albuquerque R, et al. (2009) Apelin decreases myocardial injury and improves right ventricular function in monocrotaline-induced pulmonary hypertension. Am J Physiol Heart Circ Physiol 296: H2007-H2014. 00089.2009 [pii];10.1152/ajpheart.00089.2009 [doi].
23. Cui B, Cheng YS, Dai DZ, Li N, Zhang TT, et al. (2009) CPU0213, a non-selective ETA/ETB receptor antagonist, improves pulmonary arteriolar remodeling of monocrotaline-induced pulmonary hypertension in rats. Clin Exp Pharmacol Physiol 36: 169-175. CEP5044 [pii];10.1111/j.1440-1681.2008.05044.x [doi].
24. 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. 10.1126/science.1074360 [doi];298/5595/1029 [pii].
25. Dimitropoulou C, White RE, Ownby DR, Catravas JD (2005) Estrogen reduces carbachol-induced constriction of asthmatic airways by stimulating largeconductance voltage and calcium-dependent potassium channels. Am J Respir Cell Mol Biol 32: 239-247. 2004-0331OC [pii];10.1165/rcmb.2004-0331OC [doi].
26. Bowring NE, Arch JR, Buckle DR, Taylor JF (1993) Comparison of the airways relaxant and hypotensive potencies of the potassium channel activators BRL 55834 and levcromakalim (BRL 38227) in vivo in guinea-pigs and rats. Br J Pharmacol 109: 1133-1139. (Pubitemid 23216783)
27. Short AD, Bian J, Ghosh TK, Waldron RT, Rybak SL, et al. (1993) Intracellular Ca2+ pool content is linked to control of cell growth. Proc Natl Acad Sci U S A 90: 4986-4990. (Pubitemid 23182960)
28. Lang F, Foller M, Lang KS, Lang PA, Ritter M, et al. (2005) Ion channels in cell proliferation and apoptotic cell death. J Membr Biol 205: 147-157. 10.1007/s00232-005-0780-5 [doi]. (Pubitemid 41803692)
29. Cook SJ, Lockyer PJ (2006) Recent advances in Ca(2+)-dependent Ras regulation and cell proliferation. Cell Calcium 39: 101-112. S0143-4160(05)00206-X [pii];10.1016/j.ceca.2005.10.014 [doi].
30. Dick GM, Tune JD (2010) Role of potassium channels in coronary vasodilation. Exp Biol Med (Maywood) 235: 10-22. 235/1/10 [pii];10.1258/ebm. 2009.009201 [doi].
31. Perros F, Montani D, Dorfmuller P, Durand-Gasselin I, Tcherakian C, et al. (2008) Platelet-derived growth factor expression and function in idiopathic pulmonary arterial hypertension. Am J Respir Crit Care Med 178: 81-88. 200707-1037OC [pii];10.1164/rccm.200707-1037OC [doi].
32. Humbert M, Monti G, Fartoukh M, Magnan A, Brenot F, et al. (1998) Platelet-derived growth factor expression in primary pulmonary hypertension: comparison of HIV seropositive and HIV seronegative patients. Eur Respir J 11: 554-559. (Pubitemid 28194842)
33. Schermuly RT, Dony E, Ghofrani HA, Pullamsetti S, Savai R, et al. (2005) Reversal of experimental pulmonary hypertension by PDGF inhibition. J Clin Invest 115: 2811-2821. 10.1172/JCI24838 [doi]. (Pubitemid 41434408)
34. Ghofrani HA, Seeger W, Grimminger F (2005) Imatinib for the treatment of pulmonary arterial hypertension. N Engl J Med 353: 1412-1413. 353/13/1412 [pii];10.1056/NEJMc051946 [doi].
35. Pullamsetti S, Krick S, Yilmaz H, Ghofrani HA, Schudt C, et al. (2005) Inhaled tolafentrine reverses pulmonary vascular remodeling via inhibition of smooth muscle cell migration. Respir Res 6: 128. 1465-9921-6-128 [pii];10.1186/1465-9921-6-128 [doi].
36. Hoeper MM, Barst RJ, Bourge RC, Feldman J, Frost AE, et al. (2013) Imatinib mesylate as add-on therapy for pulmonary arterial hypertension: results of the randomized IMPRES study. Circulation 127: 1128-1138. CIRCULATIONAHA. 112.000765 pii];10.1161/CIRCULATIONAHA.112.000765 [doi].
37. Chang H, Ma YG, Wang YY, Song Z, Li Q, et al. (2011) High glucose alters apoptosis and proliferation in HEK293 cells by inhibition of cloned BK Ca channel. J Cell Physiol 226: 1660-1675. 10.1002/jcp.22497 [doi].
38. Han X, Xi L, Wang H, Huang X, Ma X, et al. (2008) The potassium ion channel opener NS1619 inhibits proliferation and induces apoptosis in A2780 ovarian cancer cells. Biochem Biophys Res Commun 375: 205-209. S0006-291X(08)01494-0 [pii];10.1016/j.bbrc.2008.07.161 [doi].
39. Costa RS, Assreuy J (2005) Multiple potassium channels mediate nitric oxide-induced inhibition of rat vascular smooth muscle cell proliferation. Nitric Oxide 13: 145-151. S1089-8603(05)00076-5 [pii];10.1016/j.niox.2005.05.010 [doi].
40. 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. 10.1126/science.1074360 [doi];298/5595/1029 [pii].
41. Bentzen BH, Osadchii O, Jespersen T, Hansen RS, Olesen SP, et al. (2009) Activation of big conductance Ca(2+)-activated K (+) channels (BK) protects the heart against ischemia-reperfusion injury. Pflugers Arch 457: 979-988. 10.1007/s00424-008-0583-5 [doi].
42. Redel A, Lange M, Jazbutyte V, Lotz C, Smul TM, et al. (2008) Activation of mitochondrial large-conductance calcium-activated K+ channels via protein kinase A mediates desflurane-induced preconditioning. Anesth Analg 106: 384-91, table. 106/2/384 [pii];10.1213/ane.0b013e318160650f [doi].
43. Yun J, Park H, Ko JH, Lee W, Kim K, et al. (2010) Expression of Ca2+ -activated K+ channels in human dermal fibroblasts and their roles in apoptosis. Skin Pharmacol Physiol 23: 91-104. 000265680 [pii];10.1159/000265680 [doi].
44. Krick S, Platoshyn O, McDaniel SS, Rubin LJ, Yuan JX (2001) Augmented K(+) currents and mitochondrial membrane depolarization in pulmonary artery myocyte apoptosis. Am J Physiol Lung Cell Mol Physiol 281: L887-L894.
45. Aranda M, Bradford KK, Pearl RG (1999) Combined therapy with inhaled nitric oxide and intravenous vasodilators during acute and chronic experimental pulmonary hypertension. Anesth Analg 89: 152-158. (Pubitemid 29293325)
46. Tuder RM, Abman SH, Braun T, Capron F, Stevens T, et al. (2009) Development and pathology of pulmonary hypertension. J Am Coll Cardiol 54: S3-S9. S0735-1097(09)01212-1 [pii];10.1016/j.jacc.2009.04.009 [doi].
47. Sandow SL, Grayson TH (2009) Limits of isolation and culture: intact vascular endothelium and BKCa. Am J Physiol Heart Circ Physiol 297: H1-H7. 00042.2009 [pii];10.1152/ajpheart.00042.2009 [doi].