Regulation of KCa2.3 and endothelium-dependent hyperpolarization (EDH) in the rat middle cerebral artery: the role of lipoxygenase metabolites and isoprostanes
Background and Purpose. In rat middle cerebral arteries, endothelium-dependent hyperpolarization (EDH) is mediated by activation of calcium-activated potassium (KCa) channels specifically KCa2.3 and KCa3.1. Lipoxygenase (LOX) products function as endothelium-derived hyperpolarizing factors (EDHFs) in rabbit arteries by stimulating KCa2.3. We investigated if LOX products contribute to EDH in rat cerebral arteries.
References
[1]
Campbell WB, Falck JR. 2007. Arachidonic acid metabolites as endothelium-derived hyperpolarizing factors. Hypertension 49:590-596
[2]
Campbell WB, Gauthier KM. 2013. Inducible endothelium-derived hyperpolarizing factor: role of the 15-lipoxygenase-EDHF pathway. Journal of Cardiovascular Pharmacology 61:176-187
[3]
Campbell WB, Gebremedhin D, Pratt PF, Harder DR. 1996. Identification of epoxyeicosatrienoic acids as endothelium-derived hyperpolarizing factors. Circulation Research 78:415-423
[4]
Campbell WB, Spitzbarth N, Gauthier KM, Pfister SL. 2003. 11,12,15-Trihydroxyeicosatrienoic acid mediates ACh-induced relaxations in rabbit aorta. American Journal of Physiology - Heart and Circulatory Physiology 285:H2648-H2656
[5]
Chawengsub Y, Aggarwal NT, Nithipatikom K, Gauthier KM, Anjaiah S, Hammock BD, Falck JR, Campbell WB. 2008. Identification of 15-hydroxy-11,12-epoxyeicosatrienoic acid as a vasoactive 15-lipoxygenase metabolite in rabbit aorta. American Journal of Physiology - Heart and Circulatory Physiology 294:H1348-H1356
[6]
Chawengsub Y, Gauthier KM, Campbell WB. 2009. Role of arachidonic acid lipoxygenase metabolites in the regulation of vascular tone. American Journal of Physiology - Heart and Circulatory Physiology 297:H495-H507
[7]
Cipolla MJ, Smith J, Kohlmeyer MM, Godfrey JA. 2009. SKCa and IKCa channels, myogenic tone, and vasodilator responses in middle cerebral arteries and parenchymal arterioles: effect of ischemia and reperfusion. Stroke 40:1451-1457
[8]
Crankshaw D. 1995. Effects of the isoprostane, 8-epi-prostaglandin F2[alpha], on the contractility of the human myometrium in vitro. European Journal of Pharmacology 285:151-158
[9]
Earley S. 2011. Endothelium-dependent cerebral artery dilation mediated by transient receptor potential and Ca2 +-activated K + channels. Journal of Cardiovascular Pharmacology 57:148-153
[10]
Edwards G, Dora KA, Gardener MJ, Garland CJ, Weston AH. 1998. K + is an endothelium-derived hyperpolarizing factor in rat arteries. Nature 396:269-272
[11]
Edwards G, Feletou M, Weston AH. 2010. Endothelium-derived hyperpolarising factors and associated pathways: a synopsis. Pflugers Archiv: European Journal of Physiology 459:863-879
[12]
Elmhurst JL, Betti PA, Rangachari PK. 1997. Intestinal effects of isoprostanes: evidence for the involvement of prostanoid EP and TP receptors. Journal of Pharmacology and Experimental Therapeutics 282:1198-1205
[13]
Garland CJ, McPherson GA. 1992. Evidence that nitric oxide does not mediate the hyperpolarisation and relaxation to acetylcholine in the rat small mesenteric artery. British Journal of Pharmacology 105:429-435
[14]
Haque MZ, Majid DSA. 2008. Reduced renal responses to nitric oxide synthase inhibition in mice lacking the gene for gp91phox subunit of NAD(P)H oxidase. American Journal of Physiology - Renal Physiology 295:F758-F764
[15]
Hecker M, Bara AT, Bauersachs J, Busse R. 1994. Characterization of endothelium-derived hyperpolarizing factor as a cytochrome P450-derived arachidonic acid metabolite in mammals. Journal of Physiology 481:407-414
[16]
Hutcheson IR, Chaytor AT, Evans WH, Griffith TM. 1999. Nitric oxide-independent relaxations to acetylcholine and A23187 involve different routes of heterocellular communication. Role of Gap junctions and phospholipase A2. Circulation Research 84:53-63
[17]
Kohler R, Kaistha BP, Wulff H. 2010. Vascular KCa-channels as therapeutic targets in hypertension and restenosis disease. Expert Opinion on Therapeutic Targets 14:143-155
[18]
Kopkan L, Majid DSA. 2006. Enhanced superoxide activity modulates renal function in NO-deficient hypertensive rats. Hypertension 47:568-572
[19]
Krtz F, Hellwig N, Bürkle MA, Lehrer S, Riexinger T, Mannell H, Sohn H-Y, Klauss V, Pohl U. 2010. A sulfaphenazole-sensitive EDHF opposes platelet–endothelium interactions in vitro and in the hamster microcirculation in vivo. Cardiovascular Research 85:542-550
[20]
Liu J-Y, Tsai H-J, Hwang SH, Jones PD, Morisseau C, Hammock BD. 2009. Pharmacokinetic optimization of four soluble epoxide hydrolase inhibitors for use in a murine model of inflammation. British Journal of Pharmacology 156:284-296
[21]
Marrelli SP, Eckmann MS, Hunte MS. 2003. Role of endothelial intermediate conductance KCa channels in cerebral EDHF-mediated dilations. American Journal of Physiology - Heart and Circulatory Physiology 285:H1590-H1599
[22]
Marrelli SP, O’Neil RG, Brown RC, Bryan RM. 2007. PLA2 and TRPV4 channels regulate endothelial calcium in cerebral arteries. American Journal of Physiology - Heart and Circulatory Physiology 292:H1390-H1397
[23]
McNeish AJ, Dora KA, Garland CJ. 2005. Possible role for K + in endothelium-derived hyperpolarizing factor-linked dilatation in rat middle cerebral artery. Stroke 36:1526-1532
[24]
McNeish AJ, Garland CJ. 2007. Thromboxane A2 inhibition of SKCa after NO synthase block in rat middle cerebral artery. British Journal of Pharmacology 151:441-449
[25]
McNeish AJ, Jimenez-Altayo F, Cottrell GS, Garland CJ. 2012. Statins and selective inhibition of Rho kinase protect small conductance calcium-activated potassium channel function (KCa2.3) in cerebral arteries. PLoS ONE 7:e46735
[26]
McNeish AJ, Sandow SL, Neylon CB, Chen MX, Dora KA, Garland CJ. 2006. Evidence for involvement of both IKCa and SKCa channels in hyperpolarizing responses of the rat middle cerebral artery. Stroke 37:1277-1282
[27]
Miller AA, Drummond GR, Schmidt HHHW, Sobey CG. 2005. NADPH oxidase activity and function are profoundly greater in cerebral versus systemic arteries. Circulation Research 97:1055-1062
[28]
Minamiyama Y, Takemura S, Imaoka S, Funae Y, Tanimoto Y, Inoue M. 1997. Irreversible inhibition of cytochrome P450 by nitric oxide. Journal of Pharmacology and Experimental Therapeutics 283:1479-1485
[29]
Mombouli J-V, Bissiriou I, Agboton VD, Vanhoutte PM. 1996. Bioassay of endothelium-derived hyperpolarizing factor. Biochemical and Biophysical Research Communications 221:484-488
[30]
Morrow JD, Hill KE, Burk RF, Nammour TM, Badr KF, Roberts LJ. 1990. A series of prostaglandin F2-like compounds are produced in vivo in humans by a non-cyclooxygenase, free radical-catalyzed mechanism. Proceedings of the National Academy of Sciences of the United States of America 87:9383-9387
[31]
Nithipatikom K, DiCamelli RF, Kohler S, Gumina RJ, Falck JR, Campbell WB, Gross GJ. 2001a. Determination of cytochrome P450 metabolites of arachidonic acid in coronary venous plasma during ischemia and reperfusion in dogs. Analytical Biochemistry 292:115-124
Nithipatikom K, Laabs ND, Isbell MA, Campbell WB. 2003. Liquid chromatographic-mass spectrometric determination of cyclooxygenase metabolites of arachidonic acid in cultured cells. Journal of Chromatography B 785:135-145
[34]
Patrono C, FitzGerald GA. 1997. Isoprostanes: potential markers of oxidant stress in atherothrombotic disease. Arteriosclerosis, Thrombosis, and Vascular Biology 17:2309-2315
[35]
Pfister SL, Spitzbarth N, Nithipatikom K, Edgemond WS, Falck JR, Campbell WB. 1998. Identification of the 11,14,15- and 11,12,15-trihydroxyeicosatrienoic acids as endothelium-derived relaxing factors of rabbit aorta. The Journal of Biological Chemistry 273:30879-30887
[36]
Rosolowsky M, Campbell WB. 1993. Role of PGI2 and epoxyeicosatrienoic acids in relaxation of bovine coronary arteries to arachidonic acid. American Journal of Physiology - Heart and Circulatory Physiology 264:H327-H335
[37]
Rosolowsky M, Campbell WB. 1996. Synthesis of hydroxyeicosatetraenoic (HETEs) and epoxyeicosatrienoic acids (EETs) by cultured bovine coronary artery endothelial cells. Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism 1299:267-277
[38]
Sandow SL, Tare M, Coleman HA, Hill CE, Parkington HC. 2002. Involvement of myoendothelial gap junctions in the actions of endothelium-derived hyperpolarizing factor. Circulation Research 90:1108-1113
Wang B, Pan J, Wang L, Zhu H, Yu R, Zou Y. 2006. Associations of plasma 8-isoprostane levels with the presence and extent of coronary stenosis in patients with coronary artery disease. Atherosclerosis 184:425-430
[41]
Watanabe T, Medina JF, Haeggstrm JZ, Rdmark O, Samuelsson B. 1993. Molecular cloning of a 12-lipoxygenase cDNA from rat brain. European Journal of Biochemistry 212:605-612
[42]
You J, Golding EM, Bryan RM. 2005. Arachidonic acid metabolites, hydrogen peroxide, and EDHF in cerebral arteries. American Journal of Physiology - Heart and Circulatory Physiology 289:H1077-H1083
[43]
You J, Marrelli SP, Bryan RM. 2002. Role of cytoplasmic phospholipase A2 in endothelium-derived hyperpolarizing factor dilations of rat middle cerebral arteries. Journal of Cerebral Blood Flow & Metabolism 22:1239-1247
[44]
Zheng X, Zinkevich NS, Gebremedhin D, Gauthier KM, Nishijima Y, Fang J, Wilcox DA, Campbell WB, Gutterman DD, Zhang DX. 2013. Arachidonic acid-induced dilation in human coronary arterioles: convergence of signaling mechanisms on endothelial TRPV4-mediated Ca2 + entry. Journal of the American Heart Association 2:e000080
[45]
Zink MH, Oltman CL, Lu T, Katakam PVG, Kaduce TL, Lee H-C, Dellsperger KC, Spector AA, Myers PR, Weintraub NL. 2001. 12-Lipoxygenase in porcine coronary microcirculation: implications for coronary vasoregulation. American Journal of Physiology - Heart and Circulatory Physiology 280:H693-H704
