Redox regulation of ion channels in the pulmonary circulation

Antioxidants and Redox Signaling

Volumn 22, Issue 6, 2015, Pages 465-485

  Olschewski, Andrea ^a,b   Weir, Edward Kenneth ^c  

^a LUDWIG BOLTZMANN INSTITUTE FOR LUNG VASCULAR RESEARCH   (Austria)

^b MEDICAL UNIVERSITY OF GRAZ   (Austria)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUFFER; CALCIUM HANDLING PROTEIN; CYSTEINE; GLUTATHIONE; ION CHANNEL; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NITRIC OXIDE; POTASSIUM CHANNEL; PROTEIN; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SERINE; THIOREDOXIN; THREONINE; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG; CALCIUM;

ELECTRON TRANSPORT; HUMAN; HYPOXIA; ION CONDUCTANCE; LUNG BLOOD VESSEL; LUNG CIRCULATION; LUNG VASCULAR RESISTANCE; MEMBRANE STEADY POTENTIAL; MITOCHONDRION; NITRATION; NITROSYLATION; NONHUMAN; OXIDATION; OXIDATION REDUCTION POTENTIAL; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; S NITROSYLATION; TRANS PLASMA MEMBRANE ELECTRON TRANSPORT; CHANNEL GATING; METABOLISM; OXIDATION REDUCTION REACTION;

CALCIUM; GLUTATHIONE; HUMANS; ION CHANNEL GATING; ION CHANNELS; NADP; NITRIC OXIDE; OXIDATION-REDUCTION; PULMONARY CIRCULATION; REACTIVE OXYGEN SPECIES; THIOREDOXINS;

EID: 84923106525     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2014.5899     Document Type: Review

References (190)

1. Albarwani S, Robertson BE, Nye PC, and Kozlowski RZ. Biophysical properties of Ca2 + - and Mg-ATP-activated K+ channels in pulmonary arterial smooth muscle cells isolated from the rat. Pflugers Arch 428: 446-454, 1994
2. Archer SL, Gomberg-Maitland M, Maitland ML, Rich S, GarciafigureJG, and Weir EK. Mitochondrial metabolism, redox signaling, and fusion: a mitochondria-ROS-HIF-1 alpha-Kv1.5 O2-sensing pathway at the intersection of pulmonary hypertension and cancer. Am J Physiol Heart Circ Physiol 294: H570-H578, 2008
3. This reference has been deleted
4. This reference has been deleted. 4. Archer SL, Huang J, Henry T, Peterson D, and Weir EK. A redox-based O2 sensor in rat pulmonary vasculature. Circ Res 73: 1100-1112, 1993
5. Archer SL, Huang JM, Reeve HL, Hampl V, Tolarova S, Michelakis E, and Weir EK. Differential distribution of electrophysiologically distinct myocytes in conduit and resistance arteries determines their response to nitric oxide and hypoxia. Circ Res 78: 431-442, 1996
6. Archer SL, Nelson DP, and Weir EK. Detection of activated O2 species in vitro and in rat lungs by chemiluminescence. J Appl Physiol 67: 1912-1921, 1989
7. Archer SL, Souil E, Dinh-Xuan AT, Schremmer B, Mercier JC, El Yaagoubi A, Nguyen-Huu L, Reeve HL, and Hampl V. Molecular identification of the role of voltagegated 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, 1998
8. Archer SL, Tolins JP, Raij L, and Weir EK. Hypoxic pulmonary vasoconstriction is enhanced by inhibition of the synthesis of an endothelium derived relaxing factor. Biochem Biophys Res Commun 164: 1198-1205, 1989
9. Archer SL, Will JA, and Weir EK. Redox status in the control of pulmonary vascular tone. Herz 11: 127-141, 1986
10. Asada K, Kurokawa J, and Furukawa T. Redox- and calmodulin-dependent S-nitrosylation of the KCNQ1 channel. J Biol Chem 284: 6014-6020, 2009
11. Audi SH, Bongard RD, Dawson CA, Siegel D, Roerig DL, and Merker MP. Duroquinone reduction during passage through the pulmonary circulation. Am J Physiol Lung Cell Mol Physiol 285: L1116-L1131, 2003
12. Balzer M, Lintschinger B, and Groschner K. Evidence for a role of Trp proteins in the oxidative stress-induced membrane conductances of porcine aortic endothelial cells. Cardiovasc Res 42: 543-549, 1999
13. Bogeski I, Kappl R, Kummerow C, Gulaboski R, Hoth M, and Niemeyer BA. Redox regulation of calcium ion channels: chemical and physiological aspects. Cell Calcium 50: 407-423, 2011
14. Bogeski I, Kummerow C, Al-Ansary D, Schwarz EC, Koehler R, Kozai D, Takahashi N, Peinelt C, Griesemer D, Bozem M, Mori Y, Hoth M, and Niemeyer BA. Differential redox regulation of ORAI ion channels: a mechanism to tune cellular calcium signaling. Sci Signal 3: ra24, 2010
15. Bongard RD, Krenz GS, Gastonguay AJ, Williams CL, Lindemer BJ, and Merker MP. Characterization of the threshold for NAD(P)H: quinone oxidoreductase activity in intact sulforaphane-treated pulmonary arterial endothelial cells. Free Radic Biol Med 50: 953-962, 2011
16. Bongard RD, Lindemer BJ, Krenz GS, and Merker MP. Preferential utilization of NADPH as the endogenous electron donor for NAD(P)H: quinone oxidoreductase 1 (NQO1) in intact pulmonary arterial endothelial cells. Free Radic Biol Med 46: 25-32, 2009
17. This reference has been deleted.
18. Bongard RD, Myers CR, Lindemer BJ, Baumgardt S, Gonzalez FJ, and Merker MP. Coenzyme Q(1) as a probe for mitochondrial complex I activity in the intact perfused hyperoxia-exposed wild-type and Nqo1-null mouse lung. Am J Physiol Lung Cell Mol Physiol 302: L949-L958, 2012
19. Bonnet S, Michelakis ED, Porter CJ, Andrade-Navarro MA, Thebaud B, Bonnet S, Haromy A, Harry G, Moudgil R, McMurtry MS, Weir EK, and Archer SL. 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: 2630-2641, 2006
20. Bradford JR and Dean HP. The pulmonary circulation. J Physiol 16: 34-96, 1894
21. Campbell DL, Stamler JS, and Strauss HC. Redox modulation of L-type calcium channels in ferret ventricular myocytes. Dual mechanism regulation by nitric oxide and S-nitrosothiols. J Gen Physiol 108: 277-293, 1996
22. Chen B, Nelin VE, Locy ML, Jin Y, and Tipple TE. Thioredoxin-1 mediates hypoxia-induced pulmonary artery smooth muscle cell proliferation. Am J Physiol Lung Cell Mol Physiol 305: L389-L395, 2013
23. Chen CA, Wang TY, Varadharaj S, Reyes LA, Hemann C, Talukder MA, Chen YR, Druhan LJ, and Zweier JL. Sglutathionylation uncouples eNOS and regulates its cellular and vascular function. Nature 468: 1115-1118, 2010
24. Coggins MP and Bloch KD. Nitric oxide in the pulmonary vasculature. Arterioscler Thromb Vasc Biol 27: 1877- 1885, 2007
25. Crane FL, Sun IL, Clark MG, Grebing C, and Low H. Transplasma-membrane redox systems in growth and development. Biochim Biophys Acta 811: 233-264, 1985
26. Day RM, Suzuki YJ, Lum JM, White AC, and Fanburg BL. Bleomycin upregulates expression of gammaglutamylcysteine synthetase in pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol 282: L1349-L1357, 2002
27. Del PD, Avigliano L, Savini I, and Catani MV. Transplasma membrane electron transport in mammals: functional significance in health and disease. Antioxid Redox Signal 14: 2289-2318, 2011
28. Dromparis P, Sutendra G, and Michelakis ED. The role of mitochondria in pulmonary vascular remodeling. J Mol Med (Berl) 88: 1003-1010, 2010
29. Drose S and Brandt U. Molecular mechanisms of superoxide production by the mitochondrial respiratory chain. Adv Exp Med Biol 748: 145-169, 2012
30. Euler v US and Liljestrand G. Observations on the pulmonary arterial blood pressure in the cat. Acta Physiol Scand 12: 301-320, 1946
31. Evans AM, Osipenko ON, and Gurney AM. Properties of a novel K+ current that is active at resting potential in rabbit pulmonary artery smooth muscle cells. J Physiol 496: 407-420, 1996
32. Fagan KA, Fouty BW, Tyler RC, Morris KG, Jr., Hepler LK, Sato K, LeCras TD, Abman SH, Weinberger HD, Huang PL, McMurtry IF, and Rodman DM. The pulmonary circulation of homozygous or heterozygous eNOSnull mice is hyperresponsive to mild hypoxia. J Clin Invest 103: 291-299, 1999
33. Fagan KA, Tyler RC, Sato K, Fouty BW, Morris KG Jr., Huang PL, McMurtry IF, and Rodman DM. Relative contributions of endothelial, inducible, and neuronal NOS to tone in the murine pulmonary circulation. Am J Physiol 277: L472-L478, 1999
34. Fernandes AP and Holmgren A. Glutaredoxins: glutathione- dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Antioxid Redox Signal 6: 63-74, 2004
35. Firth AL, Gordienko DV, Yuill KH, and Smirnov SV. Cellular localization of mitochondria contributes to Kv channel-mediated regulation of cellular excitability in pulmonary but not mesenteric circulation. Am J Physiol Lung Cell Mol Physiol 296: L347-L360, 2009
36. Forstermann U. Nitric oxide and oxidative stress in vascular disease. Pflugers Arch 459: 923-939, 2010
37. Gamper N, Zaika O, Li Y, Martin P, Hernandez CC, Perez MR, Wang AY, Jaffe DB, and Shapiro MS. Oxidative modification of M-type K( + ) channels as a mechanism of cytoprotective neuronal silencing. EMBO J 25: 4996-5004, 2006
38. Ghofrani HA, Morrell NW, Hoeper MM, Olschewski H, Peacock AJ, Barst RJ, Shapiro S, Golpon H, Toshner M, Grimminger F, and Pascoe S. Imatinib in pulmonary arterial hypertension patients with inadequate response to established therapy. Am J Respir Crit Care Med 182: 1171-1177, 2010
39. Gomez R, Nunez L, Vaquero M, Amoros I, Barana A, de PT, Macaya C, Maroto L, Rodriguez E, Caballero R, Lopez-Farre A, Tamargo J, and Delpon E. Nitric oxide inhibits Kv4.3 and human cardiac transient outward potassium current (Ito1). Cardiovasc Res 80: 375-384, 2008
40. Gonzalez DR, Beigi F, Treuer AV, and Hare JM. Deficient ryanodine receptor S-nitrosylation increases sarcoplasmic reticulum calcium leak and arrhythmogenesis in cardiomyocytes. Proc Natl Acad Sci U S A 104: 20612-20617, 2007
41. Graham S, Ding M, Ding Y, Sours-Brothers S, Luchowski R, Gryczynski Z, Yorio T, Ma H, and Ma R. Canonical transient receptor potential 6 (TRPC6), a redox-regulated cation channel. J Biol Chem 285: 23466-23476, 2010
42. Grebing C, Crane FL, Low H, and Hall K. A transmembranous NADH-dehydrogenase in human erythrocyte membranes. J Bioenerg Biomembr 16: 517-533, 1984
43. Griffith OW. Biologic and pharmacologic regulation of mammalian glutathione synthesis. Free Radic Biol Med 27: 922-935, 1999
44. Groschner K, Rosker C, and Lukas M. Role of TRP channels in oxidative stress. Novartis Found Symp 258: 222-230, 2004
45. Grupe M, Myers G, Penner R, and Fleig A. Activation of store-operated I(CRAC) by hydrogen peroxide. Cell Calcium 48: 1-9, 2010
46. Gurney AM and Joshi S. The role of twin pore domain and other K+ channels in hypoxic pulmonary vasoconstriction. Novartis Found Symp 272: 218-228, 2006
47. Gurney AM, Osipenko ON, MacMillan D, McFarlane KM, Tate RJ, and Kempsill FE. Two-pore domain K channel, TASK-1, in pulmonary artery smooth muscle cells. Circ Res 93: 957-964, 2003
48. Haldar SM and Stamler JS. S-nitrosylation: integrator of cardiovascular performance and oxygen delivery. J Clin Invest 123: 101-110, 2013
49. Hawkins BJ, Irrinki KM, Mallilankaraman K, Lien YC, Wang Y, Bhanumathy CD, Subbiah R, Ritchie MF, Soboloff J, Baba Y, Kurosaki T, Joseph SK, Gill DL, and Madesh M. S-glutathionylation activates STIM1 and alters mitochondrial homeostasis. J Cell Biol 190: 391-405, 2010
50. Heiner I, Eisfeld J, Halaszovich CR, Wehage E, Jungling E, Zitt C, and Luckhoff A. Expression profile of the transient receptor potential (TRP) family in neutrophil granulocytes: evidence for currents through long TRP channel 2 induced by ADP-ribose and NAD. Biochem J 371(Pt 3): 1045-1053, 2003
51. Hidalgo C and Donoso P. Crosstalk between calcium and redox signaling: from molecular mechanisms to health implications. Antioxid Redox Signal 10: 1275-1312, 2008
52. Hille B. Potassium Channels and Chloride Channels. Ion Channels of Excitable Membranes. Sunderland: Sinauer Associates, Inc., 2001, pp. 131-167
53. Hori M and Nishida K. Oxidative stress and left ventricular remodelling after myocardial infarction. Cardiovasc Res 81: 457-464, 2009
54. Hu HL, Zhang ZX, Chen CS, Cai C, Zhao JP, and Wang X. Effects of mitochondrial potassium channel and membrane potential on hypoxic human pulmonary artery smooth muscle cells. Am J Respir Cell Mol Biol 42: 661-666, 2010
55. Hu XQ and Zhang L. Function and regulation of large conductance Ca(2 + )-activated K+ channel in vascular smooth muscle cells. Drug Discov Today 17: 974-987, 2012
56. Jernigan NL, Broughton BR, Walker BR, and Resta TC. Impaired NO-dependent inhibition of store- and receptoroperated calcium entry in pulmonary vascular smooth muscle after chronic hypoxia. Am J Physiol Lung Cell Mol Physiol 290: L517-L525, 2006
57. Jernigan NL, Walker BR, and Resta TC. Reactive oxygen species mediate RhoA/Rho kinase-induced Ca2 + sensitization in pulmonary vascular smooth muscle following chronic hypoxia. Am J Physiol Lung Cell Mol Physiol 295: L515-L529, 2008
58. Joshi S, Balan P, Gurney AM. Pulmonary vasoconstrictor action of KCNQ potassium channel blockers. Respir Res. 7:31, 2006
59. Joshi S, Sedivy V, Hodyc D, Herget J, and Gurney AM. 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, 2009
60. Kilberg MS and Christensen HN. Electron-transferring enzymes in the plasma membrane of the Ehrlich ascites tumor cell. Biochemistry 18: 1525-1530, 1979
61. Kilfoil PJ, Tipparaju SM, Barski OA, and Bhatnagar A. Regulation of ion channels by pyridine nucleotides. Circ Res 112: 721-741, 2013
62. Killilea DW, Hester R, Balczon R, Babal P, and Gillespie MN. Free radical production in hypoxic pulmonary artery smooth muscle cells. Am J Physiol 279: L408-L412, 2000
63. Knock GA and Ward JP. Redox regulation of protein kinases as a modulator of vascular function. Antioxid Redox Signal 15: 1531-1547, 2011
64. Kolisek M, Beck A, Fleig A, and Penner R. Cyclic ADPribose and hydrogen peroxide synergize with ADP-ribose in the activation of TRPM2 channels. Mol Cell 18: 61-69, 2005
65. Kuhr FK, Smith KA, Song MY, Levitan I, and Yuan JX. New mechanisms of pulmonary arterial hypertension: role of Ca(2)( + ) signaling. Am J Physiol Heart Circ Physiol 302: H1546-H1562, 2012
66. Kukreja RC, Weaver AB, and Hess ML. Sarcolemmal Na( + )-K( + )-ATPase: inactivation by neutrophil-derived free radicals and oxidants. Am J Physiol 259(Pt 2): H1330-H1336, 1990
67. Kwapiszewska G, Markart P, Dahal BK, Kojonazarov B, Marsh LM, Schermuly RT, Taube C, Meinhardt A, Ghofrani HA, Steinhoff M, Seeger W, Preissner KT, Olschewski A, Weissmann N, and Wygrecka M. PAR-2 inhibition reverses experimental pulmonary hypertension. Circ Res 110: 1179-1191, 2012
68. Lassegue B and Griendling KK. NADPH oxidases: functions and pathologies in the vasculature. Arterioscler Thromb Vasc Biol 30: 653-661, 2010
69. Lassegue B, San MA, and Griendling KK. Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system. Circ Res 110: 1364-1390, 2012
70. Le Cras TD and McMurtry IF. Nitric oxide production in the hypoxic lung. Am J Physiol Lung Cell Mol Physiol 280: L575-L582, 2001
71. Le Cras TD, Tyler RC, Horan MP, Morris KG, Tuder RM, McMurtry IF, Johns RA, and Abman SH. Effects of chronic hypoxia and altered hemodynamics on endothelial nitric oxide synthase expression in the adult rat lung. J Clin Invest 101: 795-801, 1998
72. Lee YM, Kim BJ, Chun YS, So I, Choi H, Kim MS, and Park JW. NOX4 as an oxygen sensor to regulate TASK-1 activity. Cell Signal 18: 499-507, 2006
73. Lemos VS, Poburko D, Liao CH, Cole WC, and van BC. Na + entry via TRPC6 causes Ca2 + entry via NCX reversal in ATP stimulated smooth muscle cells. Biochem Biophys Res Commun 352: 130-134, 2007
74. Li Q, Sun B, Wang X, Jin Z, Zhou Y, Dong L, Jiang LH, and Rong W. A crucial role for hydrogen sulfide in oxygen sensing via modulating large conductance calciumactivated potassium channels. Antioxid Redox Signal 12: 1179-1189, 2010
75. Lima B, Forrester MT, Hess DT, and Stamler JS. S-nitrosylation in cardiovascular signaling. Circ Res 106: 633-646, 2010
76. Lin SJ and Guarente L. Nicotinamide adenine dinucleotide, a metabolic regulator of transcription, longevity and disease. Curr Opin Cell Biol 15: 241-246, 2003
77. Linley JE, Pettinger L, Huang D, Gamper N. M channel enhancers and physiological M channel block. J Physiol. 590:793-807, 2012
78. Liu JQ, Sham JS, Shimoda LA, Kuppusamy P, and Sylvester JT. Hypoxic constriction and reactive oxygen species in porcine distal pulmonary arteries. Am J Physiol Lung Cell Mol Physiol 285: L322-L333, 2003
79. Liu SQ, Jin H, Zacarias A, Srivastava S, and Bhatnagar A. Binding of pyridine nucleotide coenzymes to the betasubunit of the voltage-sensitive K+ channel. J Biol Chem 276: 11812-11820, 2001
80. Lock JT, Sinkins WG, and Schilling WP. Protein Sglutathionylation enhances Ca2 + -induced Ca2 + release via the IP3 receptor in cultured aortic endothelial cells. J Physiol 590(Pt 15): 3431-3447, 2012
81. This reference has been deleted
82. This reference has been deleted. 80. Lu W, Wang J, Peng G, Shimoda LA, and Sylvester JT. Knockdown of stromal interaction molecule 1 attenuates store-operated Ca2 + entry and Ca2 + responses to acute hypoxia in pulmonary arterial smooth muscle. Am J Physiol Lung Cell Mol Physiol 297: L17-L25, 2009
83. Lu W, Wang J, Shimoda LA, and Sylvester JT. Differences in STIM1 and TRPC expression in proximal and distal pulmonary arterial smooth muscle are associated with differences in Ca2 + responses to hypoxia. Am J Physiol Lung Cell Mol Physiol 295: L104-L113, 2008
84. Lushington GH, Zaidi A, and Michaelis ML. Theoretically predicted structures of plasma membrane Ca(2 + )- ATPase and their susceptibilities to oxidation. J Mol Graph Model 24: 175-185, 2005
85. Ly JD and Lawen A. Transplasma membrane electron transport: enzymes involved and biological function. Redox Rep 8: 3-21, 2003
86. Mandegar M and Yuan JX. Role of K+ channels in pulmonary hypertension. Vascul Pharmacol 38: 25-33, 2002
87. Marshall C, Mamary AJ, Verhoeven AJ, and Marshall BE. Pulmonary artery NADPH-oxidase is activated in hypoxic pulmonary vasoconstriction. Am J Respir Cell Mol Biol 15: 633-644, 1996
88. McMurtry IF, Davidson AB, Reeves JT, and Grover RF. Inhibition of hypoxic pulmonary vasoconstriction by calcium antagonists in isolated rat lungs. Circ Res 38: 99-104, 1976
89. Mehdi MZ, Pandey NR, Pandey SK, and Srivastava AK. H2O2-induced phosphorylation of ERK1/2 and PKB requires tyrosine kinase activity of insulin receptor and c- Src. Antioxid Redox Signal 7: 1014-1020, 2005
90. Mehta JP, Campian JL, Guardiola J, Cabrera JA, Weir EK, and Eaton JW. Generation of oxidants by hypoxic human pulmonary and coronary smooth-muscle cells. Chest 133: 1410-1414, 2008
91. Michelakis ED, Hampl V, Nsair A, Wu X, Harry G, Haromy A, Gurtu R, and Archer SL. Diversity in mitochondrial function explains differences in vascular oxygen sensing. Circ Res 90: 1307-1315, 2002
92. Michelakis ED, Rebeyka I, Wu XC, Nsair A, Thebaud B, Hashimoto K, Dyck JRB, Haromy A, Harry G, Barr A, and Archer SL. O2 sensing in the human ductus arteriosus: regulation of voltage-gated K+ channels in smooth muscle cells by a mitochondrial redox sensor. Circ Res 91: 478-486, 2002
93. Mikami A, Imoto K, Tanabe T, Niidome T, Mori Y, Takeshima H, Narumiya S, and Numa S. Primary structure and functional expression of the cardiac dihydropyridinesensitive calcium channel. Nature 340: 230-233, 1989
94. Mittal M, Gu XQ, Pak O, Pamenter ME, Haag D, Fuchs DB, Schermuly RT, Ghofrani HA, Brandes RP, Seeger W, Grimminger F, Haddad GG, and Weissmann N. Hypoxia induces Kv channel current inhibition by increased NADPH oxidase-derived reactive oxygen species. Free Radic Biol Med 52: 1033-1042, 2012
95. Mohazzab KM and Wolin MS. Properties of a superoxide anion-generating microsomal NADH oxidoreductase, a potential pulmonary artery PO2 sensor. Am J Physiol 267: L823-L831, 1994
96. Morio Y and McMurtry IF. Ca2 + release from ryanodinesensitive store contributes to mechanism of hypoxic vasoconstriction in rat lungs. J Appl Physiol 92: 527-534, 2002
97. Moudgil R, Michelakis ED, and Archer SL. Hypoxic pulmonary vasoconstriction. J Appl Physiol 98: 390-403, 2005
98. Moudgil R, Michelakis ED, and 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 13: 615-632, 2006
99. Murphy AJ. Sulfhydryl group modification of sarcoplasmic reticulum membranes. Biochemistry 15: 4492-4496, 1976
100. Nagaraj C, Tang B, Balint Z, Wygrecka M, Hrzenjak A, Kwapiszewska G, Stacher E, Lindenmann J, Weir EK, Olschewski H, Olschewski A. Src tyrosine kinase is crucial for potassium channel function in human pulmonary arteries. Eur Respir J. 41:85-95, 2013
101. Nakashima I, Kato M, Akhand AA, Suzuki H, Takeda K, Hossain K, and Kawamoto Y. Redox-linked signal transduction pathways for protein tyrosine kinase activation. Antioxid Redox Signal 4: 517-531, 2002
102. Nelson MT and Quayle JM. Physiological roles and properties of potassium channels in arterial smooth muscle. Am J Physiol 268: C799-C822, 1995
103. Nunez L, Vaquero M, Gomez R, Caballero R, Mateos- Caceres P, Macaya C, Iriepa I, Galvez E, Lopez-Farre A, Tamargo J, and Delpon E. Nitric oxide blocks hKv1.5 channels by S-nitrosylation and by a cyclic GMP-dependent mechanism. Cardiovasc Res 72: 80-89, 2006
104. Olschewski A, Hong Z, Nelson DP, and Weir EK. Graded response of K+ current, membrane potential, and [Ca2 + ]i to hypoxia in pulmonary arterial smooth muscle. Am J Physiol Lung Cell Mol Physiol 283: L1143-L1150, 2002
105. Olschewski A, Hong Z, Peterson DA, Nelson DP, Porter VA, and Weir EK. Opposite effects of redox status on membrane potential, cytosolic calcium, and tone in pulmonary arteries and ductus arteriosus. Am J Physiol Lung Cell Mol Physiol 286: L15-L22, 2004
106. 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, and Olschewski H. Impact of TASK-1 in human pulmonary artery smooth muscle cells. Circ Res 98: 1072-1080, 2006
107. Olschewski A and Weir EK. Hypoxic pulmonary vasoconstriction and hypertension. In: Pulmonary Circulation: Diseases and Their Treatment, edited by Peacock AJ and Rubin LJ. London: Arnold, 2004, pp. 33-44
108. Ooi L, Gigout S, Pettinger L, and Gamper N. Triple cysteine module within M-type K+ channels mediates reciprocal channel modulation by nitric oxide and reactive oxygen species. J Neurosci 33: 6041-6046, 2013
109. Osipenko ON, Evans AM, and Gurney AM. Regulation of the resting potential of rabbit pulmonary artery myocytes by a low threshold, O2-sensing potassium current. Br J Pharmacol 120: 1461-1470, 1997
110. Paddenberg R, Goldenberg A, Faulhammer P, Braun- Dullaeus RC, and Kummer W. Mitochondrial complex II is essential for hypoxia-induced ROS generation and vasoconstriction in the pulmonary vasculature. Adv Exp Med Biol 536: 163-169, 2003
111. Paky A, Michael JR, Burke-Wolin TM, Wolin MS, and Gurtner GH. Endogenous production of superoxide by rabbit lungs: effects of hypoxia or metabolic inhibitors. J Appl Physiol 74: 2868-2874, 1993
112. Palace V, Kumar D, Hill MF, Khaper N, and Singal PK. Regional differences in non-enzymatic antioxidants in the heart under control and oxidative stress conditions. J Mol Cell Cardiol 31: 193-202, 1999
113. Pan Y, Weng J, Cao Y, Bhosle RC, and Zhou M. Functional coupling between the Kv1.1 channel and aldoketoreductase Kvbeta1. J Biol Chem 283: 8634-8642, 2008
114. Pan Y, Weng J, Levin EJ, and Zhou M. Oxidation of NADPH on Kvbeta1 inhibits ball-and-chain type inactivation by restraining the chain. Proc Natl Acad Sci U S A 108: 5885-5890, 2011
115. Park JW, Chun YS, Kim MS, Park YC, Kwak SJ, and Park SC. Metabolic modulation of cellular redox potential can improve cardiac recovery from ischemia-reperfusion injury. Int J Cardiol 65: 139-147, 1998
116. Park MK, Lee SH, Lee SJ, Ho WK, and Earm YE. Different modulation of Ca-activated K channels by the intracellular redox potential in pulmonary and ear arterial smooth muscle cells of the rabbit. Pflugers Arch 430: 308-314, 1995
117. Peng W, Hoidal JR, and Farrukh IS. Role of a novel KCa opener in regulating K+ channels of hypoxic human pulmonary vascular cells. Am J Respir Cell Mol Biol 20: 737-745, 1999
118. Perez-Vizcaino F, Cogolludo A, and Moreno L. Reactive oxygen species signaling in pulmonary vascular smooth muscle. Respir Physiol Neurobiol 174: 212-220, 2010
119. Pongs O. Molecular biology of voltage-dependent potassium channels. Physiol Rev 72: S69-S88, 1992
120. Post JM, Gelband CH, and Hume JR. [Ca2 + ]i inhibition of K+ channels in canine pulmonary artery. Novel mechanism for hypoxia-induced membrane depolarization. Circ Res 77: 131-139, 1995
121. Post JM, Hume JR, Archer SL, and Weir EK. Direct role for potassium channel inhibition in hypoxic pulmonary vasoconstriction. Am J Physiol 262: C882-C890, 1992
122. Poteser M, Graziani A, Rosker C, Eder P, Derler I, Kahr H, Zhu MX, Romanin C, and Groschner K. TRPC3 and TRPC4 associate to form a redox-sensitive cation channel. Evidence for expression of native TRPC3-TRPC4 heteromeric channels in endothelial cells. J Biol Chem 281: 13588-13595, 2006
123. Poteser M, Romanin C, Schreibmayer W, Mayer B, and Groschner K. S-nitrosation controls gating and conductance of the alpha 1 subunit of class C L-type Ca(2 + ) channels. J Biol Chem 276: 14797-14803, 2001
124. Quinlan TR, Li D, Laubach VE, Shesely EG, Zhou N, and Johns RA. eNOS-deficient mice show reduced pulmonary vascular proliferation and remodeling to chronic hypoxia. Am J Physiol Lung Cell Mol Physiol 279: L641-L650, 2000
125. Rathore R, Zheng YM, Li XQ, Wang QS, Liu QH, Ginnan R, Singer HA, Ho YS, and Wang YX. Mitochondrial ROS-PKCepsilon signaling axis is uniquely involved in hypoxic increase in [Ca2 + ]i in pulmonary artery smooth muscle cells. Biochem Biophys Res Commun 351: 784-790, 2006
126. Rathore R, Zheng YM, Niu CF, Liu QH, Korde A, Ho YS, and Wang YX. Hypoxia activates NADPH oxidase to increase [ROS]i and [Ca2 + ]i through the mitochondrial ROS-PKCepsilon signaling axis in pulmonary artery smooth muscle cells. Free Radic Biol Med 45: 1223-1231, 2008
127. Ray PD, Huang BW, and Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24: 981-990, 2012
128. Reeve HL, Tolarova S, Nelson DP, Archer S, and Weir EK. Redox control of oxygen sensing in the rabbit ductus arteriosus. J Physiol 533: 253-261, 2001
129. Reeve HL, Weir EK, Nelson DP, Peterson DA, and Archer SL. Opposing effects of oxidants and antioxidants on K+ channel activity and tone in rat vascular tissue. Exp Physiol 80: 825-834, 1995
130. Robbins J. KCNQ potassium channels: physiology, pathophysiology, and pharmacology. Pharmacol Ther 90: 1-19, 2001
131. Robertson TP, Hague D, Aaronson PI, and Ward JP. Voltage-independent calcium entry in hypoxic pulmonary vasoconstriction of intrapulmonary arteries of the rat. J Physiol 525: 669-680, 2000
132. Rozanski GJ and Xu Z. Glutathione and K+ channel remodeling in postinfarction rat heart. Am J Physiol Heart Circ Physiol 282: H2346-H2355, 2002
133. Sahoo N, Schonherr R, Hoshi T, and Heinemann SH. Cysteines control the N- and C-linker-dependent gating of KCNH1 potassium channels. Biochim Biophys Acta 1818: 1187-1195, 2012
134. Schach C, Xu M, Platoshyn O, Keller SH, and Yuan JX. Thiol oxidation causes pulmonary vasodilation by activating K + channels and inhibiting store-operated Ca2 + channels. Am J Physiol Lung Cell Mol Physiol 292: L685-L698, 2007
135. Schumacker PT. Lung cell hypoxia: role of mitochondrial reactive oxygen species signaling in triggering responses. Proc Am Thorac Soc 8: 477-484, 2011
136. Scragg JL, Dallas ML, Wilkinson JA, Varadi G, and Peers C. Carbon monoxide inhibits L-type Ca2 + channels via redox modulation of key cysteine residues by mitochondrial reactive oxygen species. J Biol Chem 283: 24412-24419, 2008
137. Seddon M, Looi YH, and Shah AM. Oxidative stress and redox signalling in cardiac hypertrophy and heart failure. Heart 93: 903-907, 2007
138. Seimetz M, Parajuli N, Pichl A, Veit F, Kwapiszewska G, Weisel FC, Milger K, Egemnazarov B, Turowska A, Fuchs B, Nikam S, Roth M, Sydykov A, Medebach T, Klepetko W, Jaksch P, Dumitrascu R, Garn H, Voswinckel R, Kostin S, Seeger W, Schermuly RT, Grimminger F, Ghofrani HA, and Weissmann N. Inducible NOS inhibition reverses tobacco-smoke-induced emphysema and pulmonary hypertension in mice. Cell 147: 293-305, 2011
139. Shimoda LA. Hypoxic regulation of ion channels and transporters in pulmonary vascular smooth muscle. Adv Exp Med Biol 661: 221-235, 2010
140. Shimoda LA and Polak J. Hypoxia. 4. Hypoxia and ion channel function. Am J Physiol Cell Physiol 300: C951-C967, 2011
141. Shimoda LA and Undem C. Interactions between calcium and reactive oxygen species in pulmonary arterial smooth muscle responses to hypoxia. Respir Physiol Neurobiol 174: 221-229, 2010
142. Simon F, Leiva-Salcedo E, Armisen R, Riveros A, Cerda O, Varela D, Eguiguren AL, Olivero P, and Stutzin A. Hydrogen peroxide removes TRPM4 current desensitization conferring increased vulnerability to necrotic cell death. J Biol Chem 285: 37150-37158, 2010
143. Sommer N, Dietrich A, Schermuly RT, Ghofrani HA, Gudermann T, Schulz R, Seeger W, Grimminger F, and Weissmann N. Regulation of hypoxic pulmonary vasoconstriction: basic mechanisms. Eur Respir J 32: 1639-1651, 2008
144. Song MY, Makino A, and Yuan JX. Role of reactive oxygen species and redox in regulating the function of transient receptor potential channels. Antioxid Redox Signal 15: 1549-1565, 2011
145. Steinbicker AU, Liu H, Jiramongkolchai K, Malhotra R, Choe EY, Busch CJ, Graveline AR, Kao SM, Nagasaka Y, Ichinose F, Buys ES, Brouckaert P, Zapol WM, and Bloch KD. Nitric oxide regulates pulmonary vascular smooth muscle cell expression of the inducible cAMP early repressor gene. Nitric Oxide 25: 294-302, 2011
146. Steudel W, Ichinose F, Huang PL, Hurford WE, Jones RC, Bevan JA, Fishman MC, and Zapol WM. Pulmonary vasoconstriction and hypertension in mice with targeted disruption of the endothelial nitric oxide synthase (NOS 3) gene. Circ Res 81: 34-41, 1997
147. Steudel W, Scherrer-Crosbie M, Bloch KD, Weimann J, Huang PL, Jones RC, Picard MH, and Zapol WM. Sustained pulmonary hypertension and right ventricular hypertrophy after chronic hypoxia in mice with congenital deficiency of nitric oxide synthase 3. J Clin Invest 101: 2468-2477, 1998
148. Sturrock A, Cahill B, Norman K, Huecksteadt TP, Hill K, Sanders K, Karwande SV, Stringham JC, Bull DA, Gleich M, Kennedy TP, and Hoidal JR. Transforming growth factor-beta1 induces Nox4 NAD(P)H oxidase and reactive oxygen species-dependent proliferation in human pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 290: L661-L673, 2006
149. Sun J, Morgan M, Shen RF, Steenbergen C, and Murphy E. Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport. Circ Res 101: 1155-1163, 2007
150. Sun J, Picht E, Ginsburg KS, Bers DM, Steenbergen C, and Murphy E. Hypercontractile female hearts exhibit increased S-nitrosylation of the L-type Ca2 + channel alpha1 subunit and reduced ischemia/reperfusion injury. Circ Res 98: 403-411, 2006
151. Sun J, Yamaguchi N, Xu L, Eu JP, Stamler JS, and Meissner G. Regulation of the cardiac muscle ryanodine receptor by O(2) tension and S-nitrosoglutathione. Biochemistry 47: 13985-13990, 2008
152. Svoboda LK, Reddie KG, Zhang L, Vesely ED, Williams ES, Schumacher SM, O'Connell RP, Shaw R, Day SM, Anumonwo JM, Carroll KS, and Martens JR. Redoxsensitive sulfenic acid modification regulates surface expression of the cardiovascular voltage-gated potassium channel Kv1.5. Circ Res 111: 842-853, 2012
153. Sylvester JT, Shimoda LA, Aaronson PI, and Ward JP. Hypoxic pulmonary vasoconstriction. Physiol Rev 92: 367-520, 2012
154. Tabet F, Savoia C, Schiffrin EL, and Touyz RM. Differential calcium regulation by hydrogen peroxide and superoxide in vascular smooth muscle cells from spontaneously hypertensive rats. J Cardiovasc Pharmacol 44: 200-208, 2004
155. Tang K, Li X, Zheng MQ, and Rozanski GJ. Role of apoptosis signal-regulating kinase-1-c-Jun NH2- terminal kinase-p38 signaling in voltage-gated K + channel remodeling of the failing heart: regulation by thioredoxin. Antioxid Redox Signal 14: 25-35, 2011
156. ten Freyhaus H, Dumitrescu D, Berghausen E, Vantler M, Caglayan E, and Rosenkranz S. Imatinib mesylate for the treatment of pulmonary arterial hypertension. Expert Opin Investig Drugs 21: 119-134, 2012
157. Thuringer D and Findlay I. Contrasting effects of intracellular redox couples on the regulation of maxi-K channels in isolated myocytes from rabbit pulmonary artery. J Physiol 500: 583-592, 1997
158. Tipparaju SM, Li XP, Kilfoil PJ, Xue B, Uversky VN, Bhatnagar A, and Barski OA. Interactions between the Cterminus of Kv1.5 and Kvbeta regulate pyridine nucleotide- dependent changes in channel gating. Pflugers Arch 463: 799-818, 2012
159. Tipparaju SM, Liu SQ, Barski OA, and Bhatnagar A. NADPH binding to beta-subunit regulates inactivation of voltage-gated K( + ) channels. Biochem Biophys Res Commun 359: 269-276, 2007
160. Tipparaju SM, Saxena N, Liu SQ, Kumar R, and Bhatnagar A. Differential regulation of voltage-gated K+ channels by oxidized and reduced pyridine nucleotide coenzymes. Am J Physiol Cell Physiol 288: C366-C376, 2005
161. Tonks NK. Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol 7: 833-846, 2006
162. Ueda K, Valdivia C, Medeiros-Domingo A, Tester DJ, Vatta M, Farrugia G, Ackerman MJ, and Makielski JC. Syntrophin mutation associated with long QT syndrome through activation of the nNOS-SCN5A macromolecular complex. Proc Natl Acad Sci U S A 105: 9355-9360, 2008
163. Viola HM, Arthur PG, and Hool LC. Transient exposure to hydrogen peroxide causes an increase in mitochondria- derived superoxide as a result of sustained alteration in L-type Ca2 + channel function in the absence of apoptosis in ventricular myocytes. Circ Res 100: 1036-1044, 2007
164. Wang QS, Zheng YM, Dong L, Ho YS, Guo Z, and Wang YX. Role of mitochondrial reactive oxygen species in hypoxia-dependent increase in intracellular calcium in pulmonary artery myocytes. Free Radic Biol Med 42: 642-653, 2007
165. Wang X, Tong M, Chinta S, Raj JU, and Gao Y. Hypoxia- induced reactive oxygen species downregulate ETB receptor-mediated contraction of rat pulmonary arteries. Am J Physiol Lung Cell Mol Physiol 290: L570-L578, 2006
166. Wang Y, Coe Y, Toyoda O, and Coceani F. Involvement of endothelin-1 in hypoxic pulmonary vasoconstriction in the lamb. J Physiol 482: 421-434, 1995
167. Wang YX and Zheng YM. ROS-dependent signaling mechanisms for hypoxic Ca(2 + ) responses in pulmonary artery myocytes. Antioxid Redox Signal 12: 611-623, 2010
168. Waypa GB, Chandel NS, and Schumacker PT. Model for hypoxic pulmonary vasoconstriction involving mitochondrial oxygen sensing. Circ Res 88: 1259-1266, 2001
169. Waypa GB, Guzy R, Mungai PT, Mack MM, Marks JD, Roe MW, and Schumacker PT. Increases in mitochondrial reactive oxygen species trigger hypoxia-induced calcium responses in pulmonary artery smooth muscle cells. Circ Res 99: 970-978, 2006
170. Waypa GB and Schumacker PT. Hypoxic pulmonary vasoconstriction: redox events in oxygen sensing. J Appl Physiol 98: 404-414, 2005
171. Waypa GB and Schumacker PT. Hypoxia-induced changes in pulmonary and systemic vascular resistance: where is the O2 sensor? Respir Physiol Neurobiol 174: 201-211, 2010
172. Wehage E, Eisfeld J, Heiner I, Jungling E, Zitt C, and Luckhoff A. Activation of the cation channel long transient receptor potential channel 2 (LTRPC2) by hydrogen peroxide. A splice variant reveals a mode of activation independent of ADP-ribose. J Biol Chem 277: 23150-23156, 2002
173. Weir EK, Hong Z, and Chen Y. Superoxide dismutase: master and commander? Eur Respir J 36: 234-236, 2010
174. Weir EK and Olschewski A. Role of ion channels in acute and chronic responses of the pulmonary vasculature to hypoxia. Cardiovasc Res 71: 630-641, 2006
175. Weir EK, Will JA, Lundquist LJ, Eaton JW, and Chesler E. Diamide inhibits pulmonary vasoconstriction induced by hypoxia or prostaglandin F2 alpha. Proc Soc Exp Biol Med 173: 96-103, 1983
176. Weissmann N, Kuzkaya N, Fuchs B, Tiyerili V, Schafer RU, Schutte H, Ghofrani HA, Schermuly RT, Schudt C, Sydykov A, Egemnazarow B, Seeger W, and Grimminger F. Detection of reactive oxygen species in isolated, perfused lungs by electron spin resonance spectroscopy. Respir Res 6: 86, 2005
177. Weissmann N, Vogels H, Schermuly RT, Ghofrani HA, Hanze J, Fink L, Rose F, Seeger W, and Grimminger F. Measurement of exhaled hydrogen peroxide from rabbit lungs. Biol Chem 385: 259-264, 2004
178. Weng J, Cao Y, Moss N, and Zhou M. Modulation of voltage-dependent Shaker family potassium channels by an aldo-keto reductase. J Biol Chem 281: 15194-15200, 2006
179. Wu W, Platoshyn O, Firth AL, and Yuan JX. Hypoxia divergently regulates production of reactive oxygen species in human pulmonary and coronary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 293: L952-L959, 2007
180. Xie ZJ, Wang YH, Askari A, Huang WH, Klaunig JE, and Askari A. Studies on the specificity of the effects of oxygen metabolites on cardiac sodium pump. J Mol Cell Cardiol 22: 911-920, 1990
181. Xu KY and Becker LC. Ultrastructural localization of glycolytic enzymes on sarcoplasmic reticulum vesticles. J Histochem Cytochem 46: 419-427, 1998
182. Xu SZ, Sukumar P, Zeng F, Li J, Jairaman A, English A, Naylor J, Ciurtin C, Majeed Y, Milligan CJ, Bahnasi YM, Al-Shawaf E, Porter KE, Jiang LH, Emery P, Sivaprasadarao A, and Beech DJ. TRPC channel activation by extracellular thioredoxin. Nature 451: 69-72, 2008
183. Yang Y, Jin X, and Jiang C. S-glutathionylation of ion channels: insights into the regulation of channel functions, thiol modification crosstalk, and mechanosensing. Antioxid Redox Signal 20: 937-951, 2014
184. Yang Y, Shi W, Chen X, Cui N, Konduru AS, Shi Y, Trower TC, Zhang S, and Jiang C. Molecular basis and structural insight of vascular K(ATP) channel gating by Sglutathionylation. J Biol Chem 286: 9298-9307, 2011
185. Yoshida T, Inoue R, Morii T, Takahashi N, Yamamoto S, Hara Y, Tominaga M, Shimizu S, Sato Y, and Mori Y. Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat Chem Biol 2: 596-607, 2006
186. Yuan XJ. Voltage-gated K+ currents regulate resting membrane potential and [Ca2 + ]i in pulmonary arterial myocytes. Circ Res 77: 370-378, 1995
187. Yuan XJ, Wang J, Juhaszova M, Golovina VA, and Rubin LJ. Molecular basis and function of voltage-gated K+ channels in pulmonary arterial smooth muscle cells. Am J Physiol 274: L621-L635, 1998
188. Zhang H, Tao L, Jiao X, Gao E, Lopez BL, Christopher TA, Koch W, and Ma XL. Nitrative thioredoxin inactivation as a cause of enhanced myocardial ischemia/reperfusion injury in the aging heart. Free Radic Biol Med 43: 39-47, 2007
189. Zhang SL, Yeromin AV, Zhang XH, Yu Y, Safrina O, Penna A, Roos J, Stauderman KA, and Cahalan MD. Genome-wide RNAi screen of Ca(2 + ) influx identifies genes that regulate Ca(2 + ) release-activated Ca(2 + ) channel activity. Proc Natl Acad Sci U S A 103: 9357-9362, 2006
190. Zheng MQ, Li X, Tang K, Sharma NM, Wyatt TA, Patel KP, Gao L, Bidasee KR, and Rozanski GJ. Pyruvate restores beta-adrenergic sensitivity of L-type Ca(2 + ) channels in failing rat heart: role of protein phosphatase. Am J Physiol Heart Circ Physiol 304: H1352-H1360, 2013