Hydrogen peroxide induces vasorelaxation by enhancing 4-aminopyridine-sensitive Kv currents through S-glutathionylation

Pflugers Archiv European Journal of Physiology

Volumn 467, Issue 2, 2015, Pages 285-297

  Park, Sang Woong ^a   Noh, Hyun Ju ^a   Sung, Dong Jun ^b   Kim, Jae Gon ^c   Kim, Jeong Min ^a   Ryu, Shin Young ^d   Kang, Kyeong Jin ^e   Kim, Bokyung ^a   Bae, Young Min ^a   Cho, Hana ^c  

^a Konkuk University School of Medicine   (South Korea)

^b Konkuk University   (South Korea)

^c Samsung Medical Center   (South Korea)

^d Seoul National University   (South Korea)

^e Sungkyunkwan University   (South Korea)

Author keywords

H2O2; Kv channel; Mesenteric artery; Oxidative stress; S glutathionylation

Indexed keywords

FAMPRIDINE; GLUTATHIONE; GLUTATHIONE REDUCTASE; HYDROGEN PEROXIDE; POTASSIUM CHANNEL; POTASSIUM CHANNEL BLOCKING AGENT;

ACTION POTENTIAL; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; MALE; MESENTERIC ARTERY; METABOLISM; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT; VASCULAR SMOOTH MUSCLE; VASODILATATION;

4-AMINOPYRIDINE; ACTION POTENTIALS; ANIMALS; CELLS, CULTURED; GLUTATHIONE; GLUTATHIONE REDUCTASE; HYDROGEN PEROXIDE; MALE; MESENTERIC ARTERIES; MUSCLE, SMOOTH, VASCULAR; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS; RATS; RATS, SPRAGUE-DAWLEY; VASODILATION;

EID: 84926303832     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1513-3     Document Type: Article

References (82)

1. Aracena-Parks P, Goonasekera SA, Gilman CP, Dirksen RT, Hidalgo C, Hamilton SL (2006) Identification of cysteines involved in S-nitrosylation, S-glutathionylation, and oxidation to disulfides in ryanodine receptor type 1. J Biol Chem 281(52):40354–40368. doi:10.1074/jbc.M600876200
2. + channels are regulated by mitochondria-derived hydrogen peroxide. Biol Chem 385(3–4):205–216
3. + currents. Biochem Biophys Res Commun 347(2):468–476
4. + 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
5. Barlow RS, White RE (1998) Hydrogen peroxide relaxes porcine coronary arteries by stimulating BKCa channel activity. Am J Physiol 275(4 Pt 2):H1283–H1289
6. Beny JL, von der Weid PY (1991) Hydrogen peroxide: an endogenous smooth muscle cell hyperpolarizing factor. Biochem Biophys Res Commun 176(1):378–384
7. Bienert GP, Moller AL, Kristiansen KA, Schulz A, Moller IM, Schjoerring JK, Jahn TP (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282(2):1183–1192
8. Bienert GP, Schjoerring JK, Jahn TP (2006) Membrane transport of hydrogen peroxide. Biochim Biophys Acta 1758(8):994–1003
9. Bimboese P, Gibson CJ, Schmidt S, Xiang W, Ehrlich BE (2011) Isoform-specific regulation of the inositol 1,4,5-trisphosphate receptor by O-linked glycosylation. J Biol Chem 286(18):15688–15697. doi:10.1074/jbc.M110.206482
10. Boveris A, Chance B (1973) The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J 134(3):707–716
11. Burke TM, Wolin MS (1987) Hydrogen peroxide elicits pulmonary arterial relaxation and guanylate cyclase activation. Am J Physiol 252(4 Pt 2):H721–H732
12. Caouette D, Dongmo C, Berube J, Fournier D, Daleau P (2003) Hydrogen peroxide modulates the Kv1.5 channel expressed in a mammalian cell line. Naunyn Schmiedeberg’s Arch Pharmacol 368(6):479–486
13. Chandrasekhar KD, Lvov A, Terrenoire C, Gao GY, Kass RS, Kobertz WR (2011) O-glycosylation of the cardiac I(Ks) complex. J Physiol 589(Pt 15):3721–3730. doi:10.1113/jphysiol.2011.211284
14. + channels in mediating heterogeneous microvascular responses to acetylcholine in different vascular beds. J Pharmacol Exp Ther 282(3):1473–1479
15. Cohen G (1994) Enzymatic/nonenzymatic sources of oxyradicals and regulation of antioxidant defenses. Ann N Y Acad Sci 738:8–14
16. Coleman HA, Tare M, Parkington HC (2004) Endothelial potassium channels, endothelium-dependent hyperpolarization and the regulation of vascular tone in health and disease. Clin Exp Pharmacol Physiol 31(9):641–649
17. Cruzado MC, Risler NR, Miatello RM, Yao G, Schiffrin EL, Touyz RM (2005) Vascular smooth muscle cell NAD(P)H oxidase activity during the development of hypertension: effect of angiotensin II and role of insulin-like growth factor-1 receptor transactivation. Am J Hypertens 18(1):81–87. doi:10.1016/j.amjhyper.2004.09.001
18. Cseko C, Bagi Z, Koller A (2004) Biphasic effect of hydrogen peroxide on skeletal muscle arteriolar tone via activation of endothelial and smooth muscle signaling pathways. J Appl Physiol 97(3):1130–1137. doi:10.1152/japplphysiol.00106.2004
19. Dai S, Hall DD, Hell JW (2009) Supramolecular assemblies and localized regulation of voltage-gated ion channels. Physiol Rev 89(2):411–452. doi:10.1152/physrev.00029.2007
20. Dalle-Donne I, Milzani A, Gagliano N, Colombo R, Giustarini D, Rossi R (2008) Molecular mechanisms and potential clinical significance of S-glutathionylation. Antioxid Redox Signal 10(3):445–473
21. Dalle-Donne I, Rossi R, Colombo G, Giustarini D, Milzani A (2009) Protein S-glutathionylation: a regulatory device from bacteria to humans. Trends Biochem Sci 34(2):85–96. doi:10.1016/j.tibs.2008.11.002
22. Dalle-Donne I, Rossi R, Giustarini D, Colombo R, Milzani A (2007) S-glutathionylation in protein redox regulation. Free Radic Biol Med 43(6):883–898. doi:10.1016/j.freeradbiomed.2007.06.014
23. Dugan LL, Sensi SL, Canzoniero LM, Handran SD, Rothman SM, Lin TS, Goldberg MP, Choi DW (1995) Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J Neurosci 15(10):6377–6388
24. + is an endothelium-derived hyperpolarizing factor in rat arteries. Nature 396(6708):269–272
25. Finkel T (1998) Oxygen radicals and signaling. Curr Opin Cell Biol 10(2):248–253
26. Firth AL, Remillard CV, Platoshyn O, Fantozzi I, Ko EA, Yuan JX (2011) Functional ion channels in human pulmonary artery smooth muscle cells: voltage-dependent cation channels. Pulm Cir 1(1):48–71. doi:10.4103/2045-8932.78103
27. Gao YJ, Lee RM (2005) Hydrogen peroxide is an endothelium-dependent contracting factor in rat renal artery. Br J Pharmacol 146(8):1061–1068
28. 2+, and superoxide anion levels. J Pharmacol Exp Ther 328(1):19–27. doi:10.1124/jpet.108.144295
29. Hatoum OA, Binion DG, Miura H, Telford G, Otterson MF, Gutterman DD (2005) Role of hydrogen peroxide in ACh-induced dilation of human submucosal intestinal microvessels. Am J Physiol Heart Circ Physiol 288(1):H48–H54. doi:10.1152/ajpheart.00663.2004
30. Heinle H (1984) Vasoconstriction of carotid artery induced by hydroperoxides. Arch Int Physiol Biochim 92(4):267–271
31. 2 across water channels. J Exp Bot 51(353):2053–2066
32. Kamp TJ, Hell JW (2000) Regulation of cardiac L-type calcium channels by protein kinase A and protein kinase C. Circ Res 87(12):1095–1102
33. Kim SH, Bae YM, Sung DJ, Park SW, Woo NS, Kim B, Cho SI (2007) Ketamine blocks voltage-gated K(+) channels and causes membrane depolarization in rat mesenteric artery myocytes. Pflugers Arch 454(6):891–902. doi:10.1007/s00424-007-0240-4
34. Kozlowska H, Baranowska M, Gromotowicz A, Malinowska B (2007) Endothelium-derived hyperpolarizing factor (EDHF): potential involvement in the physiology and pathology of blood vessels. Postepy Hig Med Dosw 61:555–564 (Online)
35. Lacza Z, Puskar M, Kis B, Perciaccante JV, Miller AW, Busija DW (2002) Hydrogen peroxide acts as an EDHF in the piglet pial vasculature in response to bradykinin. Am J Physiol Heart Circ Physiol 283(1):H406–H411
36. Liu Y, Fiskum G, Schubert D (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem 80(5):780–787
37. + channel-mediated vasodilation. Vasc Pharmacol 38(1):43–49
38. Lucchesi PA, Belmadani S, Matrougui K (2005) Hydrogen peroxide acts as both vasodilator and vasoconstrictor in the control of perfused mouse mesenteric resistance arteries. J Hypertens 23(3):571–579
39. Ma HP (2011) Hydrogen peroxide stimulates the epithelial sodium channel through a phosphatidylinositide 3-kinase-dependent pathway. J Biol Chem 286(37):32444–32453. doi:10.1074/jbc.M111.254102
40. Marvar PJ, Hammer LW, Boegehold MA (2007) Hydrogen peroxide-dependent arteriolar dilation in contracting muscle of rats fed normal and high salt diets. Microcirculation 14(8):779–791. doi:10.1080/10739680701444057
41. Matoba T, Shimokawa H, Kubota H, Morikawa K, Fujiki T, Kunihiro I, Mukai Y, Hirakawa Y, Takeshita A (2002) Hydrogen peroxide is an endothelium-derived hyperpolarizing factor in human mesenteric arteries. Biochem Biophys Res Commun 290(3):909–913
42. Matoba T, Shimokawa H, Nakashima M, Hirakawa Y, Mukai Y, Hirano K, Kanaide H, Takeshita A (2000) Hydrogen peroxide is an endothelium-derived hyperpolarizing factor in mice. J Clin Invest 106(12):1521–1530
43. + channels in smooth muscle cells by a mitochondrial redox sensor. Circ Res 91(6):478–486
44. 2-sensor in resistance artery smooth muscle cells. J Mol Cell Cardiol 37(6):1119–1136
45. Nelson MT, Quayle JM (1995) Physiological roles and properties of potassium channels in arterial smooth muscle. Am J Physiol 268(4 Pt 1):C799–C822
46. Nistico R, Piccirilli S, Cucchiaroni ML, Armogida M, Guatteo E, Giampa C, Fusco FR, Bernardi G, Nistico G, Mercuri NB (2008) Neuroprotective effect of hydrogen peroxide on an in vitro model of brain ischaemia. Br J Pharmacol 153(5):1022–1029. doi:10.1038/sj.bjp.0707587
47. Nowicki PT, Flavahan S, Hassanain H, Mitra S, Holland S, Goldschmidt-Clermont PJ, Flavahan NA (2001) Redox signaling of the arteriolar myogenic response. Circ Res 89(2):114–116
48. Palen DI, Ouhtit A, Belmadani S, Lucchesi PA, Matrougui K (2006) Hydrogen peroxide acts as relaxing factor in human vascular smooth muscle cells independent of map-kinase and nitric oxide. Front Biosci 11:2526–2534
49. + channels in coronary arterial smooth muscle cells. Life Sci 77(5):512–527. doi:10.1016/j.lfs.2004.10.073
50. 2 terminus of Kv2.1 to channel activation. Am J Physiol 273(6 Pt 1):C1849–C1858
51. + channel in oxygen-sensitive pulmonary artery myocytes. EMBO J 16(22):6615–6625. doi:10.1093/emboj/16.22.6615
52. Quyyumi AA, Ozkor M (2006) Vasodilation by hyperpolarization: beyond NO. Hypertension 48(6):1023–1025
53. Rengifo J, Gibson CJ, Winkler E, Collin T, Ehrlich BE (2007) Regulation of the inositol 1,4,5-trisphosphate receptor type I by O-GlcNAc glycosylation. J Neurosci 27(50):13813–13821. doi:10.1523/jneurosci.2069-07.2007
54. 2 activates redox- and 4-aminopyridine-sensitive Kv channels in coronary vascular smooth muscle. Am J Physiol Heart Circ Physiol 292(3):H1404–H1411
55. + channels. Am J Physiol Heart Circ Physiol 291(5):H2473–H2482
56. Rougier JS, Albesa M, Abriel H (2010) Ubiquitylation and SUMOylation of cardiac ion channels. J Cardiovasc Pharmacol 56(1):22–28. doi:10.1097/FJC.0b013e3181daaff9
57. Saitoh S, Zhang C, Tune JD, Potter B, Kiyooka T, Rogers PA, Knudson JD, Dick GM, Swafford A, Chilian WM (2006) Hydrogen peroxide: a feed-forward dilator that couples myocardial metabolism to coronary blood flow. Arterioscler Thromb Vasc Biol 26(12):2614–2621
58. Sato A, Sakuma I, Gutterman DD (2003) Mechanism of dilation to reactive oxygen species in human coronary arterioles. Am J Physiol Heart Circ Physiol 285(6):H2345–H2354. doi:10.1152/ajpheart.00458.2003
59. Schafer FQ, Buettner GR (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30(11):1191–1212
60. Shi Y, Chen X, Wu Z, Shi W, Yang Y, Cui N, Jiang C, Harrison RW (2008) cAMP-dependent protein kinase phosphorylation produces interdomain movement in SUR2B leading to activation of the vascular KATP channel. J Biol Chem 283(12):7523–7530. doi:10.1074/jbc.M709941200
61. Shi W, Cui N, Shi Y, Zhang X, Yang Y, Jiang C (2007) Arginine vasopressin inhibits Kir6.1/SUR2B channel and constricts the mesenteric artery via V1a receptor and protein kinase C. Am J Physiol Regul Integr Comp Physiol 293(1):R191–R199. doi:10.1152/ajpregu.00047.2007
62. Shi Y, Wu Z, Cui N, Shi W, Yang Y, Zhang X, Rojas A, Ha BT, Jiang C (2007) PKA phosphorylation of SUR2B subunit underscores vascular KATP channel activation by beta-adrenergic receptors. Am J Physiol Regul Integr Comp Physiol 293(3):R1205–R1214. doi:10.1152/ajpregu.00337.2007
63. Shi WW, Yang Y, Shi Y, Jiang C (2012) K(ATP) channel action in vascular tone regulation: from genetics to diseases. Sheng Li Xue Bao 64(1):1–13
64. Sobey CG (2001) Potassium channel function in vascular disease. Arterioscler Thromb Vasc Biol 21(1):28–38
65. Somers MJ, Mavromatis K, Galis ZS, Harrison DG (2000) Vascular superoxide production and vasomotor function in hypertension induced by deoxycorticosterone acetate-salt. Circulation 101(14):1722–1728
66. Sung DJ, Noh HJ, Kim JG, Park SW, Kim B, Cho H, Bae YM (2013) Serotonin contracts the rat mesenteric artery by inhibiting 4-aminopyridine-sensitive Kv channels via the 5-HT2A receptor and Src tyrosine kinase. Exp Mol Med 45:e67. doi:10.1038/emm.2013.116
67. Suvorava T, Lauer N, Kumpf S, Jacob R, Meyer W, Kojda G (2005) Endogenous vascular hydrogen peroxide regulates arteriolar tension in vivo. Circulation 112(16):2487–2495. doi:10.1161/circulationaha.105.543157
68. 2+ release in cardiac myocytes. Free Radic Biol Med 24(2):318–325
69. Takaki A, Morikawa K, Murayama Y, Yamagishi H, Hosoya M, Ohashi J, Shimokawa H (2008) Roles of endothelial oxidases in endothelium-derived hyperpolarizing factor responses in mice. J Cardiovasc Pharmacol 52(6):510–517
70. Takaki A, Morikawa K, Tsutsui M, Murayama Y, Tekes E, Yamagishi H, Ohashi J, Yada T, Yanagihara N, Shimokawa H (2008) Crucial role of nitric oxide synthases system in endothelium-dependent hyperpolarization in mice. J Exp Med 205(9):2053–2063
71. Tang H, Viola HM, Filipovska A, Hool LC (2011) Ca(v)1.2 calcium channel is glutathionylated during oxidative stress in guinea pig and ischemic human heart. Free Radic Biol Med 51(8):1501–1511
72. Thakali K, Davenport L, Fink GD, Watts SW (2006) Pleiotropic effects of hydrogen peroxide in arteries and veins from normotensive and hypertensive rats. Hypertension 47(3):482–487
73. Thomas G, Ramwell P (1986) Induction of vascular relaxation by hydroperoxides. Biochem Biophys Res Commun 139(1):102–108
74. Wei EP, Kontos HA, Beckman JS (1996) Mechanisms of cerebral vasodilation by superoxide, hydrogen peroxide, and peroxynitrite. Am J Physiol 271(3 Pt 2):H1262–H1266
75. Xu C, Lu Y, Tang G, Wang R (1999) Expression of voltage-dependent K(+) channel genes in mesenteric artery smooth muscle cells. Am J Physiol 277(5 Pt 1):G1055–G1063
76. Yada T, Shimokawa H, Hiramatsu O, Kajita T, Shigeto F, Goto M, Ogasawara Y, Kajiya F (2003) Hydrogen peroxide, an endogenous endothelium-derived hyperpolarizing factor, plays an important role in coronary autoregulation in vivo. Circulation 107(7):1040–1045
77. Yang Y, Shi W, Chen X, Cui N, Konduru AS, Shi Y, Trower TC, Zhang S, Jiang C (2011) Molecular basis and structural insight of vascular K(ATP) channel gating by S-glutathionylation. J Biol Chem 286(11):9298–9307
78. Yang Y, Shi W, Cui N, Wu Z, Jiang C (2010) Oxidative stress inhibits vascular K(ATP) channels by S-glutathionylation. J Biol Chem 285(49):38641–38648
79. Yang Y, Shi Y, Guo S, Zhang S, Cui N, Shi W, Zhu D, Jiang C (2008) PKA-dependent activation of the vascular smooth muscle isoform of KATP channels by vasoactive intestinal polypeptide and its effect on relaxation of the mesenteric resistance artery. Biochim Biophys Acta 1778(1):88–96. doi:10.1016/j.bbamem.2007.08.030
80. Yogi A, Callera GE, Hipolito UV, Silva CR, Touyz RM, Tirapelli CR (2010) Ethanol-induced vasoconstriction is mediated via redox-sensitive cyclo-oxygenase-dependent mechanisms. Clin Sci (Lond) 118(11):657–668
81. + channel activation. Circ Res 110(3):471–480
82. Zimmermann AK, Loucks FA, Schroeder EK, Bouchard RJ, Tyler KL, Linseman DA (2007) Glutathione binding to the Bcl-2 homology-3 domain groove: a molecular basis for Bcl-2 antioxidant function at mitochondria. J Biol Chem 282(40):29296–29304