Hypoxia induces K v channel current inhibition by increased NADPH oxidase-derived reactive oxygen species

Free Radical Biology and Medicine

Volumn 52, Issue 6, 2012, Pages 1033-1042

  Mittal, Manish ^a,g   Gu, Xiang Q ^b   Pak, Oleg ^a   Pamenter, Matthew E ^b   Haag, Daniela ^a   Fuchs, D Beate ^a   Schermuly, Ralph T ^c   Ghofrani, H A ^a   Brandes, Ralf P ^d   Seeger, Werner ^a   Grimminger, Friedrich ^a   Haddad, Gabriel G ^b,e,f   Weissmann, Norbert ^a  

^a JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^d GOETHE UNIVERSITY   (Germany)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^f RADY CHILDREN'S HOSPITAL   (United States)

^g UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

hypoxia; Kv channels; NADPH oxidases; NOX4; Pulmonary hypertension; Reactive oxygen species

Indexed keywords

APOCYNIN; POTASSIUM CHANNEL KV1.5; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SMALL INTERFERING RNA; ACETOPHENONE DERIVATIVE; NOX4 PROTEIN, RAT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL CELL; ANIMAL TISSUE; ARTERY MUSCLE; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME REGULATION; HYPOXIA; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; PULMONARY ARTERY; PULMONARY HYPERTENSION; RAT; UPREGULATION; ANIMAL; ANOXIA; CELL CULTURE; DRUG EFFECT; GENETICS; METABOLISM; MOUSE; OXIDATION REDUCTION REACTION; PATHOLOGY; PROTEIN TRANSPORT; SMOOTH MUSCLE FIBER; SPRAGUE DAWLEY RAT;

MUS; RATTUS;

ACETOPHENONES; ANIMALS; ANOXIA; CELLS, CULTURED; HYPERTENSION, PULMONARY; KV1.5 POTASSIUM CHANNEL; MALE; MICE; MYOCYTES, SMOOTH MUSCLE; NADPH OXIDASE; OXIDATION-REDUCTION; PROTEIN TRANSPORT; PULMONARY ARTERY; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING;

EID: 84857233841     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.12.004     Document Type: Article

References (61)

1. N. Weissmann, F. Grimminger, D. Walmrath, and W. Seeger Hypoxic vasoconstriction in buffer-perfused rabbit lungs Respir. Physiol. 100 2 1995 159 169
2. E.K. Weir, J. Lopez-Barneo, K.J. Buckler, and S.L. Archer Acute oxygen-sensing mechanisms N. Engl. J. Med. 353 19 2005 2042 2055
3. N. Sommer, A. Dietrich, R.T. Schermuly, H.A. Ghofrani, T. Gudermann, R. Schulz, W. Seeger, F. Grimminger, and N. Weissmann Regulation of hypoxic pulmonary vasoconstriction: basic mechanisms Eur. Respir. J. 32 6 2008 1639 1651
4. C.V. Remillard, and J.X. Yuan High altitude pulmonary hypertension: role of K+ and Ca2+ channels High Alt. Med. Biol. 6 2 2005 133 146
5. R. Moudgil, E.D. Michelakis, and S.L. Archer Hypoxic pulmonary vasoconstriction J. Appl. Physiol. 98 1 2005 390 403
6. R.D. Guzy, and P.T. Schumacker Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia Exp. Physiol. 91 5 2006 807 819
7. W. Wu Hypoxia divergently regulates production of reactive oxygen species in human pulmonary and coronary artery smooth muscle cells October 2007
8. N. Weissmann, S. Zeller, R.U. Schafer, C. Turowski, M. Ay, K. Quanz, H.A. Ghofrani, R.T. Schermuly, L. Fink, W. Seeger, and F. Grimminger Impact of mitochondria and NADPH oxidases on acute and sustained hypoxic pulmonary vasoconstriction Am. J. Respir. Cell Mol. Biol. 34 4 2006 505 513
9. N. Weissmann, A. Tadic, J. Hanze, F. Rose, S. Winterhalder, M. Nollen, R.T. Schermuly, H.A. Ghofrani, W. Seeger, and F. Grimminger Hypoxic vasoconstriction in intact lungs: a role for NADPH oxidase-derived H(2)O(2)? Am. J. Physiol. Lung Cell Mol. Physiol. 279 4 2000 L683 L690
10. G.B. Waypa, and P.T. Schumacker Hypoxic pulmonary vasoconstriction: redox events in oxygen sensing J. Appl. Physiol. 98 1 2005 404 414
11. F. Grimminger, N. Weissmann, R. Spriestersbach, E. Becker, S. Rosseau, and W. Seeger Effects of NADPH oxidase inhibitors on hypoxic vasoconstriction in buffer-perfused rabbit lungs Am. J. Physiol. 268 5 Pt 1 1995 L747 L752
12. J.X. Yuan Oxygen-sensitive K(+) channel(s): where and what? Am. J. Physiol. Lung Cell Mol. Physiol. 281 6 2001 L1345 L1349
13. G.G. Haddad, and C. Jiang O2-sensing mechanisms in excitable cells: role of plasma membrane K+ channels Annu. Rev. Physiol. 59 1997 23 42
14. C. Jiang, and G.G. Haddad Oxygen deprivation inhibits a K+ channel independently of cytosolic factors in rat central neurons J. Physiol. 481 Pt 1 1994 15 26
15. R. Moudgil, E.D. Michelakis, and S.L. Archer 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 8 2006 615 632
16. W.A. Coetzee, Y. Amarillo, J. Chiu, A. Chow, D. Lau, T. McCormack, H. Moreno, M.S. Nadal, A. Ozaita, D. Pountney, M. Saganich, M.E. Vega-Saenz de, and B. Rudy Molecular diversity of K+ channels Ann. N. Y. Acad. Sci. 30 868 1999 233 285
17. S.L. Archer, E. Souil, A.T. Dinh-Xuan, B. Schremmer, J.C. Mercier, Y.A. El, L. Nguyen-Huu, H.L. Reeve, and V. Hampl 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 11 1998 2319 2330
18. D.S. Hogg, A.R. Davies, G. McMurray, and R.Z. Kozlowski K(V)2.1 channels mediate hypoxic inhibition of I(KV) in native pulmonary arterial smooth muscle cells of the rat Cardiovasc. Res. 55 2 2002 349 360
19. S.L. Archer, J.A. Will, and E.K. Weir Redox status in the control of pulmonary vascular tone Herz 11 3 1986 127 141
20. S.V. Smirnov, T.P. Robertson, J.P. Ward, and P.I. Aaronson Chronic hypoxia is associated with reduced delayed rectifier K+ current in rat pulmonary artery muscle cells Am. J. Physiol. 266 1 Pt 2 1994 H365 H370
21. O. Platoshyn, Y. Yu, V.A. Golovina, S.S. McDaniel, S. Krick, L. Li, J.Y. Wang, L.J. Rubin, and J.X. Yuan Chronic hypoxia decreases K(V) channel expression and function in pulmonary artery myocytes Am. J. Physiol. Lung Cell Mol. Physiol. 280 4 2001 L801 L812
22. J.W. Landsberg, and J.X. Yuan Calcium and TRP channels in pulmonary vascular smooth muscle cell proliferation News Physiol. Sci. 19 2004 44 50
23. S. Bonnet, S.L. Archer, J. Allalunis-Turner, A. Haromy, C. Beaulieu, R. Thompson, C.T. Lee, G.D. Lopaschuk, L. Puttagunta, S. Bonnet, G. Harry, K. Hashimoto, C.J. Porter, M.A. Andrade, B. Thebaud, and E.D. Michelakis A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth Cancer Cell 11 1 2007 37 51
24. S. Bonnet, E.D. Michelakis, C.J. Porter, M.A. Andrade-Navarro, B. Thebaud, S. Bonnet, A. Haromy, G. Harry, R. Moudgil, M.S. McMurtry, E.K. Weir, and S.L. Archer An abnormal mitochondrial-hypoxia inducible factor-1alpha-Kv channel pathway disrupts oxygen sensing and triggers pulmonary arterial hypertension in fawn hooded rats: similarities to human pulmonary arterial hypertension Circulation 113 22 2006 2630 2641 6
25. E.D. Michelakis, B. Thebaud, E.K. Weir, and S.L. Archer 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 6 2004 1119 1136
26. S.L. Archer, M. Gomberg-Maitland, M.L. Maitland, S. Rich, J.G. Garcia, and E.K. Weir Mitochondrial metabolism, redox signaling, and fusion: a mitochondria-ROS-HIF-1alpha-Kv1.5 O2-sensing pathway at the intersection of pulmonary hypertension and cancer Am. J. Physiol. Heart Circ. Physiol. 294 2 2008 H570 H578
27. J.R. Desireddi, K.N. Farrow, J.D. Marks, G.B. Waypa, and P.T. Schumacker Hypoxia increases ROS signaling and cytosolic Ca(2+) in pulmonary artery smooth muscle cells of mouse lungs slices Antioxid. Redox Signal. 12 5 2010 595 602
28. G.B. Waypa, J.D. Marks, R. Guzy, P.T. Mungai, J. Schriewer, D. Dokic, and P.T. Schumacker Hypoxia triggers subcellular compartmental redox signaling in vascular smooth muscle cells Circ. Res. 106 3 2010 526 535
29. G.B. Waypa, R. Guzy, P.T. Mungai, M.M. Mack, J.D. Marks, M.W. Roe, and P.T. Schumacker Increases in mitochondrial reactive oxygen species trigger hypoxia-induced calcium responses in pulmonary artery smooth muscle cells Circ. Res. 99 9 2006 970 978
30. A.Y. Chi, G.B. Waypa, P.T. Mungai, and P.T. Schumacker Prolonged hypoxia increases ROS signaling and RhoA activation in pulmonary artery smooth muscle and endothelial cells Antioxid. Redox Signal. 12 5 2010 603 610
31. J.D. Lambeth, K.H. Krause, and R.A. Clark NOX enzymes as novel targets for drug development Semin. Immunopathol. 30 3 2008 339 363
32. K. Bedard, and K.H. Krause The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology Physiol. Rev. 87 1 2007 245 313
33. J.D. Lambeth NOX enzymes and the biology of reactive oxygen Nat. Rev. Immunol. 4 3 2004 181 189
34. R.P. Brandes Vascular functions of NADPH oxidases Hypertension 56 2010 17 21
35. R.P. Brandes, N. Weissmann, and K. Schröder NADPH oxidases in cardiovascular disease Free Radic. Biol. Med. 49 5 2010 687 706
36. M. Mittal, M. Roth, P. Konig, S. Hofmann, E. Dony, P. Goyal, A.C. Selbitz, R.T. Schermuly, H.A. Ghofrani, G. Kwapiszewska, W. Kummer, W. Klepetko, M.A. Hoda, L. Fink, J. Hanze, W. Seeger, F. Grimminger, H.H. Schmidt, and N. Weissmann Hypoxia-dependent regulation of nonphagocytic NADPH oxidase subunit NOX4 in the pulmonary vasculature Circ. Res. 101 3 2007 258 267
37. S. Ismail, A. Sturrock, P. Wu, B. Cahill, K. Norman, T. Huecksteadt, K. Sanders, T. Kennedy, and J. Hoidal NOX4 mediates hypoxia-induced proliferation of human pulmonary artery smooth muscle cells: the role of autocrine production of transforming growth factor-{beta}1 and insulin-like growth factor binding protein-3 Am. J. Physiol. Lung Cell Mol. Physiol. 296 3 2009 L489 L499
38. S. Li, S.S. Tabar, V. Malec, B.G. Eul, W. Klepetko, N. Weissmann, F. Grimminger, W. Seeger, F. Rose, and J. Hanze NOX4 regulates ROS levels under normoxic and hypoxic conditions, triggers proliferation, and inhibits apoptosis in pulmonary artery adventitial fibroblasts Antioxid. Redox Signal. 10 10 2008 1687 1698
39. R. Dumitrascu, N. Weissmann, H.A. Ghofrani, E. Dony, K. Beuerlein, H. Schmidt, J.P. Stasch, M.J. Gnoth, W. Seeger, F. Grimminger, and R.T. Schermuly Activation of soluble guanylate cyclase reverses experimental pulmonary hypertension and vascular remodeling Circulation 113 2 2006 286 295
40. M. Roth, M. Rupp, S. Hofmann, M. Mittal, B. Fuchs, N. Sommer, N. Parajuli, K. Quanz, D. Schubert, E. Dony, R.T. Schermuly, H.A. Ghofrani, U. Sausbier, K. Rutschmann, S. Wilhelm, W. Seeger, P. Ruth, F. Grimminger, M. Sausbier, and N. Weissmann Heme oxygenase-2 and large-conductance Ca2 +-activated K+ channels: lung vascular effects of hypoxia Am. J. Respir. Crit. Care Med. 180 4 2009 353 364
41. N. Weissmann, A. Dietrich, B. Fuchs, H. Kalwa, M. Ay, R. Dumitrascu, A. Olschewski, U. Storch, M. Schnitzler, H.A. Ghofrani, R.T. Schermuly, O. Pinkenburg, W. Seeger, F. Grimminger, and T. Gudermann Classical transient receptor potential channel 6 (TRPC6) is essential for hypoxic pulmonary vasoconstriction and alveolar gas exchange Proc. Natl. Acad Sci. U. S. A. 103 50 2006 19093 19098
42. P. Goyal, N. Weissmann, F. Rose, F. Grimminger, H.J. Schäfers, W. Seeger, and J. Hänze Identification of novel Nox4 splice variants with impact on ROS levels in A549 cells Biochem. Biophys. Res. Commun. 329 1 2005 32 39
43. K. Chen, M.T. Kirber, H. Xiao, Y. Yang, and J.F. Keaney Jr. Regulation of ROS signal transduction by NADPH oxidase 4 localization J. Cell Biol. 181 7 2008 1129 1139
44. J.X. Yuan, A.M. Aldinger, M. Juhaszova, J. Wang, J.V. Conte Jr., S.P. Gaine, J.B. Orens, and L.J. Rubin Dysfunctional voltage-gated K+ channels in pulmonary artery smooth muscle cells of patients with primary pulmonary hypertension Circulation 98 14 1998 1400 1406 6
45. C.E. McCartney, H. McClafferty, J.M. Huibant, E.G. Rowan, M.J. Shipston, and I.C. Rowe A cysteine-rich motif confers hypoxia sensitivity to mammalian large conductance voltage- and Ca-activated K (BK) channel alpha-subunits Proc. Natl. Acad. Sci. U. S. A. 102 49 2005 17870 17876
46. O. Platoshyn, E.E. Brevnova, E.D. Burg, Y. Yu, C.V. Remillard, and J.X. Yuan Acute hypoxia selectively inhibits KCNA5 channels in pulmonary artery smooth muscle cells Am. J. Physiol. Cell Physiol. 290 3 2006 C907 C916
47. J.M. Post, J.R. Hume, S.L. Archer, and E.K. Weir Direct role for potassium channel inhibition in hypoxic pulmonary vasoconstriction Am. J. Physiol. 262 4 Pt 1 1992 C882 C890
48. X.J. Yuan, W.F. Goldman, M.L. Tod, L.J. Rubin, and M.P. Blaustein Hypoxia reduces potassium currents in cultured rat pulmonary but not mesenteric arterial myocytes Am. J. Physiol. 264 2 Pt 1 1993 L116 L123
49. X.D. Tang, M.L. Garcia, S.H. Heinemann, and T. Hoshi Reactive oxygen species impair Slo1 BK channel function by altering cysteine-mediated calcium sensing Nat. Struct. Mol. Biol. 11 2 2004 171 178
50. D.D. Gutterman, H. Miura, and Y. Liu Redox modulation of vascular tone: focus of potassium channel mechanisms of dilation Arterioscler. Thromb. Vasc. Biol. 25 4 2005 671 678
51. J. Wang, M. Juhaszova, L.J. Rubin, and X.J. Yuan Hypoxia inhibits gene expression of voltage-gated K+ channel alpha subunits in pulmonary artery smooth muscle cells J. Clin. Invest. 100 9 1997 2347 2353
52. 2-sensitive potassium channel Kv1.5 reduces pulmonary hypertension and restores hypoxic pulmonary vasoconstriction in chronically hypoxic rats Circulation 107 15 2003 2037 2044
53. S. Heumuller, S. Wind, E. Barbosa-Sicard, H.H. Schmidt, R. Busse, K. Schroder, and R.P. Brandes Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant Hypertension 51 2 2008 211 217
54. R.M. Touyz, X. Chen, F. Tabet, G. Yao, G. He, M.T. Quinn, P.J. Pagano, and E.L. Schiffrin Expression of a functionally active gp91phox-containing neutrophil-type NAD(P)H oxidase in smooth muscle cells from human resistance arteries: regulation by angiotensin II Circ. Res. 90 11 2002 1205 1213
55. Kahles T. NADPH oxidase plays a central role in blood-brain barrier damage in experimental, stroke. 2007 November.
56. N. Anilkumar, R. Weber, M. Zhang, A. Brewer, and A.M. Shah NOX4 and nox2 NADPH oxidases mediate distinct cellular redox signaling responses to agonist stimulation Arterioscler. Thromb. Vasc. Biol. 28 7 2008 1347 1354
57. A. Cogolludo, G. Frazziano, L. Cobeno, L. Moreno, F. Lodi, E. Villamor, J. Tamargo, and F. Perez-Vizcaino Role of reactive oxygen species in Kv channel inhibition and vasoconstriction induced by TP receptor activation in rat pulmonary arteries Ann. N. Y. Acad. Sci. 1091 2006 41 51
58. A.E. Dikalova, A.T. Bikineyeva, K. Budzyn, R.R. Nazarewicz, L. McCann, W. Lewis, D.G. Harrison, and S.I. Dikalov Therapeutic targeting of mitochondrial superoxide in hypertension Circ. Res. 107 1 2010 106 116
59. J.T. Hulme, E.A. Coppock, A. Felipe, J.R. Martens, and M.M. Tamkun Oxygen sensitivity of cloned voltage-gated K(+) channels expressed in the pulmonary vasculature Circ. Res. 85 6 1999 489 497
60. F. Duprat, E. Guillemare, G. Romey, M. Fink, F. Lesage, M. Lazdunski, and E. Honore Susceptibility of cloned K+ channels to reactive oxygen species Proc. Natl. Acad. Sci. U. S. A. 92 25 1995 11796 11800
61. N. Weissmann, F. Grimminger, A. Olschewski, and W. Seeger Hypoxic pulmonary vasoconstriction: a multifactorial response? Am. J. Physiol. Lung Cell Mol. Physiol. 281 2 2001 L314 L317