Inducible endothelium-derived hyperpolarizing factor: Role of the 15-lipoxygenase-EDHF pathway

Journal of Cardiovascular Pharmacology

Volumn 61, Issue 3, 2013, Pages 176-187

  Campbell, William B ^a   Gauthier, Kathryn M ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

15 lipoxygenase; endothelium derived hyperpolarizing factor; HEETA; potassium channels; THETA; vascular relaxation

Indexed keywords

ACETYLCHOLINE; ARACHIDONATE 15 LIPOXYGENASE; ARACHIDONIC ACID; BRADYKININ; CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM CHANNEL; CHOLESTEROL; ENDOTHELIUM DERIVED HYPERPOLARIZING FACTOR; EPOXYICOSATRIENOIC ACID; ESTROGEN; HYDROGEN PEROXIDE; INTERLEUKIN 13; INTERLEUKIN 4; NITRIC OXIDE SYNTHASE; OXIDOREDUCTASE; POTASSIUM; POTASSIUM CHANNEL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANEMIA; ARTICLE; ATHEROSCLEROSIS; BLOOD VESSEL TONE; CONDUCTANCE; CONGESTIVE HEART FAILURE; DIABETES MELLITUS; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; EPIGENETICS; FATTY ACID METABOLISM; HUMAN; HYPERCHOLESTEROLEMIA; HYPERPOLARIZATION; HYPERTENSION; HYPOXIA; INSULIN RESISTANCE; ISCHEMIC PRECONDITIONING; ISOLATED ARTERY; MESENTERIC ARTERY; METABOLITE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN SECRETION; REGULATORY MECHANISM; REPERFUSION INJURY; SHEAR STRESS; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; SYNTHESIS; VASODILATATION;

ANIMALS; ARACHIDONATE 15-LIPOXYGENASE; ARACHIDONIC ACID; BIOLOGICAL FACTORS; ENDOTHELIUM, VASCULAR; HUMANS; NATRIURETIC PEPTIDE, C-TYPE; SIGNAL TRANSDUCTION; UP-REGULATION; VASODILATION;

EID: 84875218727     PISSN: 01602446     EISSN: 15334023     Source Type: Journal    
DOI: 10.1097/FJC.0b013e31828165db     Document Type: Article

References (115)

1. Furchgott RF. Role of endothelium in responses of vascular smooth muscle. Circ Res. 1983;53:557-573.
2. Cohen RA, Vanhoutte PM. Endothelium-dependent hyperpolarization: beyond nitric oxide and cyclic GMP. Circulation. 1995;92:3337-3349.
3. Feletou M, Vanhoutte PM. Endothelium-derived hyperpolarizing factor. Where are we now? Arterioscler Thromb Vasc Biol. 2006;26:1215-1225.
4. Campbell WB, Fleming I. Epoxyeicosatrienoic acids and endotheliumdependent responses. Pflugers Arch. 2010;459:881-895.
5. Nagao T, Illiano S, Vanhoutte PM. Heterogenous distribution of endothelium-dependent relaxations resistant to N-nitro-L-arginine in rats. Am J Physiol. 1992;263:H1090-H1094.
6. Campbell WB, Falck Jr. Arachidonic acid metabolites as endotheliumderived hyperpolarizing factors. Hypertension. 2007;49:590-596.
7. Matoba T, Shimokawa H, Nakashima M, et al. Hydrogen peroxide is an endothelium-derived hyperpolarizing factor in mice. J Clin Invest. 2000;106:1521-1530.
8. Griffith TM. Endothelium-dependent smooth muscle hyperpolarization: do gap junctions provide a unifying hypothesis? Br J Pharmacol. 2004; 141:881-903.
9. Chauhan SD, Nilsson H, Ahluwalia A, et al. Release of c-type natriuretic peptide accounts for the biological activity of endothelium-derived hyperpolarizing factor. Proc Natl Acad Sci U S A. 2003;100:1426-1431.
10. Edwards G, Dora KA, Gardener MJ, et al. K is an endothelium-derived hyperpolarizing factor in rat arteries. Nature. 1998;396:269-272.
11. Chawengsub Y, Gauthier KM, Campbell WB. Role of arachidonic acid lipoxygenase metabolites in the regulation of vascular tone. Am J Physiol. 2009;297:H495-H507.
12. Edwards G, Feletou M, Gardener MJ, et al. Role of gap junctions in the responses to EDHF in rat and guinea-pig small arteries. Br J Pharmacol. 1999;128:1788-1794.
13. Edwards G, Feletou M, Weston AH. Endothelium-derived hyperpolarizing factors and associated pathways: a synopsis. Pflugers Arch. 2010; 459:863-879.
14. Griffith OW, Stuehr DJ. Nitric oxide synthases: properties and catalytic mechanism. Annu Rev Physiol. 1995;57:707-736.
15. Dubois RN, Abramson SB, Crofford L, et al. Cyclooxygenase in biology and disease. FASEB J. 1998;12:1063-1073.
16. Suga S, Itoh H, Komatsu H, et al. Cytokine-induced c-type natriuretic peptide (CNP) secretion from vascular endothelial cells. Endocrinology. 1993;133:3038-3041.
17. Suga S, Nakao K, Itoh H, et al. Endothelial production of c-type natriuretic peptide and its marked augmentation by transforming growth factor-beta. J Clin Invest. 1992;90:1145-1149.
18. Sellitti DF, Koles N, Mendonca MC. Regulation of c-type natriuretic peptide expression. Peptides. 2011;32:1964-1971.
19. Faraci FM, Didion SP. Vascular protection: superoxide dismutase isoforms in the vessel wall. Arterioscler Thromb Vasc Biol. 2004;24:1367-1373.
20. Shimokawa H. Hydrogen peroxide as an endothelium-derived hyperpolarizing factor. Pflugers Arch. 2010;459:915-922.
21. Gorlach A, Brandes RP, Nguyen K, et al. A gp91phox containing NADPH oxidase selectively expressed in endothelial cells is a major source of oxygen radical generation in the arterial wall. Circ Res. 2000;87:26-32.
22. Xi Q, Cheranov SY, Jaggar JH. Mitochrondria-derived reactive oxygen species dilate cerebral arteries by activating Ca sparks. Circ Res. 2005; 97:354-362.
23. Capdevila J, Chacos N, Werringloer J, et al. Liver microsomal cytochrome P450 and the oxidative metabolism of archidonic acid. Proc Natl Acad Sci U S A. 1981;78:5362-5366.
24. Zeldin DC. Epoxygenase pathways of arachidonic acid metabolism. J Biol Chem. 2001;276:36059-36062.
25. Campbell WB, Gebremedhin D, Pratt PF, et al. Identification of epoxyeicosatrienoic acids as endothelium-derived hyperpolarizing factors. Circ Res. 1996;78:415-423.
26. Fissllthaler B, Hinsch N, Chataigneau T, et al. Nifedipine increases cytochrome P4502C expression and endothelium-derived hyperpolarizing factor-mediated responses in coronary arteries. Hypertension. 2000; 36:270-275.
27. Bauersachs J, Christ M, Ertl G, et al. Cytochrome P450 2C expression and EDHF-mediated relaxation in porcine coronary arteries is increased by cortisol. Cardiovasc Res. 2002;54:669-675.
28. Earley S, Pastuszyn A, Walker BR. Cytochrome p-450 epoxygenase products contribute to attenuated vasoconstriction after chronic hypoxia. Am J Physiol Heart Circ Physiol. 2003;285:H127-H136.
29. Fissllthaler B, Michaelis UR, Randriamboavonjy V, et al. Cytochrome P450 epoxygenases and vascular tone: novel role for HMG-CoA reductase inhibitors in the regulation of CYP 2C expression. Biochim Biophys Acta. 2003;1619:332-339.
30. Kessler P, Popp R, Busse R, et al. Proinflammatory mediators chronically downregulate the formation of the endothelium-derived hyperpolarizing factor in arteries via a nitric oxide/cyclic GMP-dependent mechanism. Circulation. 1999;99:1878-1884.
31. Campbell WB, Spitzbarth N, Gauthier KM, et al. 11,12,15- Trihydroxyeicosatrienoic acid mediates acetylcholine-induced relaxations in the rabbit aorta. Am J Physiol. 2003;285:H2648-H2656.
32. Tang X, Aggarwal N, Holmes BB, et al. Age-related decrease in 15-lipoxygenase contributes to reduced vasorelaxation in rabbit aorta. Am J Physiol. 2008;294:H679-H687.
33. Aggarwal NT, Gauthier KM, Campbell WB. 15-Lipoxygenase metabolites contribute to age-related reduction in acetylcholine-induced hypotension in rabbits. Am J Physiol. 2008;295:H89-H96.
34. Pfister SL, Spitzbarth N, Edgemond W, et al. Vasorelaxation by an endothelium-derived metabolite of arachidonic acid. Am J Physiol. 1996;270:H1021-H1030.
35. Tang X, Spitzbarth N, Kuhn H, et al. Interleukin-13 upregulates vasodilatory 15-lipoxygenase eicosanoids in rabbit aorta. Arterioscler Thromb Vasc Biol. 2003;23:1768-1774.
36. Zhu D, Medhora M, Campbell WB, et al. Chronic hypoxia activates lung 15-lipoxygenase, which catalyzes production of 15-HETE and enhances constriction in neonatal rabbit pulmonary arteries. Circ Res. 2003;92:992-1000.
37. Pfister SL. Role of lipoxygenase metabolites of arachidonic acid in enhanced pulmonary artery contractions of female rabbits. Hypertension. 2011;57:825-832.
38. Furchgott RF, Zawadzki JV. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature. 1980; 288:373-376.
39. DeMey JG, Claeys M, Vanhoutte PM. Endothelium-dependent inhibitory effects of acetylcholine, adenosine triphosphate, thrombin and arachidonic acid in the canine femoral artery. J Pharmacol Exp Ther. 1982;222:166-173.
40. Van de Voorde J, Leusen I. Role of the endothelium in the vasodilator response of rat thoracic aorta to histamine. Eur J Pharmacol. 1983;28: 113-120.
41. Forstermann U, Mugge A, Frolich JC. Endothelium-dependent relaxations of human epicardial coronary arteries: frequent lack of effect of acetylcholine. Eur J Pharmacol. 1986;128:277-281.
42. Förstermann U, Alheid U, Frolich JG, et al. Mechanisms of action of lipoxygenase and cytochrome p-450-mono-oxygenase inhibitors in blocking endothelium-dependent vasodilation. Br J Pharmacol. 1988; 93:569-578.
43. Förstermann U, Hertting G, Neufang B. The role of endothelial and nonendothelial prostaglandins in the relaxation of isolated blood vessels of the rabbit induced by bradykinin and acetylcholine. Br J Pharmacol. 1986;87:521-532.
44. Minami Y, Toda N. Possible involvement of 5-lipoxygenase products in the generation of endothelium derived relaxing factor. J Pharmacol Exp Ther. 1989;250:1055-1060.
45. Miller AW, Katakam PVG, Lee H-C, et al. Arachidonic acid-induced vasodilation of rat small mesenteric arteries is lipoxygenase-dependent. J Pharmacol Exp Ther. 2003;304:139-144.
46. Stapleton PA, Goodwill AG, James ME, et al. Altered mechanisms of endothelium-dependent dilation in skeletal muscle arterioles with genetic hypercholesterolemia. Am J Physiol. 2007;293:R1110-R1119.
47. Gauthier KM, Goldman DH, Aggarwal NT, et al. Role of arachidonic acid lipoxygenase metabolites in acetylcholine-induced relaxations in mouse arteries. Am J Physiol. 2010;300:H725-H735.
48. Tang X, Holmes BB, Nithipatikom K, et al. Reticulocyte 15-lipoxygenase-1 is important in acetylcholine-induced endothelium-dependent vasorelaxation in rabbit aorta. Arterioscler Thromb Vasc Biol. 2006;26:78-84.
49. Gauthier KM, Spitzbarth N, Edwards EM, et al. Apamin-sensitive k+ currents mediate arachidonic acid-induced relaxations of rabbit aorta. Hypertension. 2004;43:413-419.
50. Pfister SL, Campbell WB. Arachidonic acid- and acetylcholine-induced relaxations of rabbit aorta. Hypertension. 1992;20:682-689.
51. Singer HA, Peach MJ. Endothelium-dependent relaxation of rabbit aorta. I. Relaxation stimulated by arachidonic acid. J Pharmacol Exp Ther. 1983;226:790-795.
52. Förstermann U, Neufang B. The endothelium-dependent vasodilator effect of acetylcholine: characterization of the endothelial relaxing factor with inhibitors of arachidonic acid metabolism. Eur J Pharmacol. 1984;103:65-70.
53. Rosolowsky M, Campbell WB. Role of PGI2 and EETs in the relaxation of bovine coronary arteries to arachidonic acid. Am J Physiol. 1993;264: H327-H335.
54. Zhang DX, Gauthier KM, Chawengsub Y, et al. Cyclooxygenase- and lipoxygenase-dependent relaxations to arachidonic acid in rabbit small mesenteric arteries. Am J Physiol. 2005;288:H302-H309.
55. Zhang DX, Gauthier KM, Chawengsub Y, et al. ACh-induced relaxations of rabbit small mesenteric arteries: role of arachidonic acid metabolites and K. Am J Physiol. 2007;293:H152-H159.
56. Chawengsub Y, Aggarwal NT, Nithipatikom K, et al. Identification of 15-hydroxy-11,12-epoxyeicosatrienoic acid as a vasoactive 15-lipoxygenase metabolite in rabbit aorta. Am J Physiol. 2008;294:H1348-H1356.
57. Yamamoto S. Mammalian lipoxygenases: molecular structures and functions. Biochim Biophys Acta. 1992;1128:117-131.
58. Kuhn H, WaltherM, Kuban RJ.Mammalian arachidonate 15-lipoxygenases structure, function, and biological implications. Prostaglandins Other Lipid Mediat. 2002;68-69:263-290.
59. Yoshimoto T, Takahashi Y. Arachidonate 12-lipoxygenases. Prostaglandins Other Lipid Mediat. 2002;68-69:245-262.
60. Watanabe T, Medina JF, Haeggstrom JZ, et al. Molecular cloning of a 12-lipoxygenase cDNA from rat brain. Eur J Biochem. 1993;212:605- 612.
61. Freire-Moar J, Alavi-Nassab A, Ng M, et al. Cloning and characterization of a murine macrophage lipoxygenase. Biochim Biophys Acta. 1995;1254:112-116.
62. Fulton D, McGiff JC, Quilley J. Role of phospholipase C and phospholipase A2 in the nitric oxide-independent vasodilator effect of bradykinin in the rat perfused heart. J Pharmacol Exp Ther. 1996;278:518-526.
63. Tang X, Edwards EM, Holmes BB, et al. Role of phospholipase C and diacylglyceride lipase pathway in arachidonic acid release and acetylcholine-induced vascular relaxation in rabbit aorta. Am J Physiol. 2006;290:H37-H45.
64. Pfister SL, Spitzbarth N, Nithipatikom K, et al. Identification of 11,14,15- and 11,12,15-trihydroxyeicosatrienoic acids as endotheliumderived relaxing factors of rabbit aorta. J Biol Chem. 1998;273:30879- 30887.
65. Gauthier KM, Chawengsub Y, Goldman DM, et al. 11(R),12(S),15(S)- trihydroxyeicosa-5(Z),8(Z),13(E)-trienoic acid: an endothelium-derived 15-lipoxygenase metabolite that relaxes rabbit aorta. Am J Physiol. 2008;294:H1467-H1472.
66. Zink MH, Oltman CL, Lu T, et al. 12-Lipoxygenase in porcine coronary microcirculation: implications for coronary vasoregulation. Am J Physiol. 2001;280:H693-H704.
67. Ma YH, Harder DR, Clark JE, et al. Effects of 12-HETE on isolated dog renal arcuate arteries. Am J Physiol. 1991;261:H451-H456.
68. Aggarwal N, Chawengsub Y, Gauthier KM, et al. Endothelial 15- lipoxygenase-1 overexpression increases acetylcholine-induced hypotension and vasorelaxation in rabbits. Hypertension. 2008;51:246-251.
69. Aggarwal N, Holmes BB, Cui L, et al. Adenoviral expression of 15-lipoxygenase-1 in rabbit aortic endothelium: role in arachidonic acid-induced relaxation. Am J Physiol. 2007;292:H1033-H1041.
70. Kuhn H, Heydeck D, Brinckman R, et al. Regulation of cellular 15-lipoxygenase activity on pretranslational, translational and posttranslational levels. Lipids. 1999;34:s2273-s2279.
71. Kelavkar UP, Harya NS, Hutzley J, et al. DNA methylation paradigm shift: 15-lipoxygenase-1 upregulation in prostatic intraepithelial neoplasia and prostate cancer by atypical promoter hypermethylation. Prostaglandins Other Lipid Mediat. 2007;82:185-197.
72. Heydeck D, Thomas L, Schnurr K, et al. Interleukin-4 and 13 induce upregulation of the murine macrophage 12/15-lipoxygenase activity: evidence for the involvement of transcription factor STAT6. Blood. 1998;92:2503-2510.
73. Xu B, Bhattacharjee A, Roy B, et al. Role of protein kinase c isoforms in the regulation of interleukin-13-induced 15-lipoxygenase gene expression in human monocytes. J Biol Chem. 2004;279:15954-15960.
74. Kelavkar UP, Wang S, Badr KF. Ku autoantigen (DNA helicase) is required for interleukins-13/-4-induction of 15-lipoxygenase-1 gene expression in human epithelial cells. Genes Immun. 2000;1:237-250.
75. Shureiqi I, Zuo X, Broaddus R, et al. The transcription factor GATA-6 is overexpressed in vivo and contributes to silencing 15-LOX-1 in vitro in human colon cancer. FASEB J. 2007;21:743-753.
76. Ostareck DH, Ostareck-Lederer A, Wilm M, et al. mRNA silencing in erythroid differentiation: hnRNP K and hnRNP E1 regulate 15- lipoxygenase translation from the 30 end. Cell. 1997;89:597-606.
77. Bomsztyk K, Denisenko O, Ostrowski J. HnRNP K: one protein multiple processes. BioEssays. 2004;26:629-638.
78. Habelhah H, Shah K, Huang L, et al. ERK phosphorylation drives cytoplasmic accumulation of hnRNP-K and inhibition of mRNA translation. Nat Cell Biol. 2001;3:325-330.
79. Goto K, Fujii K, Onaka U, et al. Angiotensin-converting enzyme inhibitor prevents age-related endothelial dysfunction. Hypertension. 2000; 36:581-587.
80. Bajpai AK, Blaskova E, Pakala SB, et al. 15(S)-HETE production in human retinal microvascular endothelial cells by hypoxia: novel role for MEK1 in 15(S)-HETE induced angiogenesis. Invest Ophthalmol Vis Sci. 2007;48:4930-4938.
81. Zhang L, Ma J, Shen T, et al. Platelet-derived growth factor (PDGF) induces pulmonary vascular remodeling through 15-LO/15-HETE pathway under hypoxic conditions. Cell Signal. 2012;24:1931-1939.
82. Yla-Herttuala S, Rosenfeld ME, Parthasarathy S, et al. Gene expression in macrophage-rich human atherosclerotic lesions. 15-Lipoxygenase and acetyl low density lipoprotein receptor messenger RNA colocalize with oxidation specific lipid-protein adducts. J Clin Invest. 1991;87: 1146-1152.
83. Hiltunen T, Luoma J, Nikkari T, et al. Induction of 15-lipoxygenase mRNA and protein in early atherosclerotic lesions. Circulation. 1995; 92:3297-3303.
84. Trebus F, Heydeck D, Schimke I, et al. Transient experimental anemia in cholesterol-fed rabbits induces systemic overexpression of the reticulocytetype 15-lipoxygenase and protects from aortic lipid deposition. Prostaglandins Leukot Essent Fatty Acids. 2002;67:419-428.
85. Lee YW, Kuhn H, Kaiser S, et al. Interleukin-4 induces transcription of the 15-lipoxygenase-I gene in human endothelial cells. J Lipid Res. 2001;42:783-791.
86. Luksha L, Poston L, Gustafsson JA, et al. The oestrogen receptor beta contributes to sex related differences in endothelial function of murine small arteries via EDHF. J Physiol. 2006;577:945-955.
87. Woodman OL, Boujaoude M. Chronic treatment of male rats with daidzein or 17 beta-oestradiol induces the contribution of EDHF to endothelium-dependent relaxation. Br J Pharmacol. 2004;141: 322-328.
88. Nawate S, Fukao M, Sakuma I, et al. Reciprocal changes in endothelium- derived hyperpolarizing factor- and nitric oxide-system in the mesenteric artery of adult female rats following ovariectomy. Br J Pharmacol. 2005;144:178-189.
89. Maccarrone M, Bari M, Battista N, et al. Estrogen stimulates arachidonylethanolamide release from human endothelial cells and platelet activation. Blood. 2002;100:4040-4048.
90. Natarajan R, Gu J-L, Rossi J, et al. Elevated glucose and angiotensin II increase 12-lipoxygenase activity and expression in porcine aortic smooth muscle cells. Proc Natl Acad Sci U S A. 1993;90:4947-4951.
91. Natarajan R, Bai W, Rangarajan V, et al. Platelet-derived growth factor BB mediated regulation of 12-lipoxygenase in porcine aortic smooth muscle cells. J Cell Physiol. 1996;169:391-400.
92. Limor R, Kaplan M, Sharon O, et al. Aldosterone up-regulates 12- and 15-lipoxygenase expression and LDL oxidation in human vascular smooth muscle cells. J Cell Biochem. 2009;108: 1203-1210.
93. Kim Y-S, Xu Z-G, Reddy MA, et al. Novel interactions between TGFbeta1 actions and the 12/15-lipoxygenase pathway in mesangial cells. J Am Soc Nephrol. 2005;16:352-362.
94. Kim JH, Kang YJ, Kim HS. IL-8/CXCL8 upregulates 12-lipoxygenase expression in vascular smooth muscle cells from spontaneously hypertensive rats. Immune Netw. 2009;9:106-113.
95. Titterington JS, Sukhanov S, Higashi Y, et al. Growth hormone-releasing peptide-2 suppresses vascular oxidative stress in ApoE2/2 mice but does not reduce atherosclerosis. Endocrinology. 2009;150:5478-5487.
96. Limor R, Sharon O, Knoll E, et al. Lipoxygenase-derived metabolites are regulators of peroxisome proliferator-activated receptor gamma-2 expression in human vascular smooth muscle cells. Am J Hypertens. 2008;21:219-223.
97. Wang Y, Zhu D, An Y, et al. Preeclampsia activates 15-lipoxygenase and its metabolite 15-hydroxyeicosatetraenoic acid enhances constriction in umbilical arteries. Prostaglandins Leukot Essent Fatty Acids. 2012;86:79-84.
98. Aggarwal NT, Gauthier KM, Campbell WB. Endothelial nitric oxide and 15-lipoxygenase metabolites independently mediate relaxations of the rabbit aorta. Vascul Pharmacol. 2012;56:106-112.
99. Feletou M, Vanhoutte PM. Endothelial dysfunction: a multifaceted disorder. Am J Physiol. 2006;291:H985-H1002.
100. Van de Voorde J, Vanheel B, Leusen I. Endothelium-dependent relaxation and hyperpolarization in aorta from control and renal hypertensive rats. Circ Res. 1992;70:1-8.
101. Fujii K, Tominaga M, Ohmori S, et al. Decreased endothelium-dependent hyperpolarizations to acetylcholine in smooth muscle of the mesenteric artery of spontaneously hypertensive rats. Circ Res. 1992;70:660-669.
102. Michel FS, Mann GS, Man RYK, et al. Hypertension and the absence of EDHF-mediated responses favour endothelium-dependent contractions in renal arteries of rats. Br J Pharmacol. 2008;155:217-226.
103. Weston AH, Porter EL, Harno E, et al. Impairment of endothelial SKCA channels and of downstream hyperpolarizing pathways in mesenteric arteries from spontaneously hypertensive rats. Br J Pharmacol. 2010;160:836-843.
104. Taddei S, Varsari D, Cipriano A, et al. Identification of a cytochrome P450 2C9-derived endothelium-derived hyperpolarizing factor in human essential hypertensive patients. J Am Coll Cardiol. 2006;48:508-515.
105. Bellien J, Joannides R. Epoxyeicosatrienoic acid pathway in human health and disease. J Cardiovasc Pharmacol. 2012;61:188-196.
106. Bellien J, Iacob M, Remy-Jouet I, et al. Epoxyeicosatrienoic acids contribute with altered nitric oxide and endothelin-1 pathways to conduit artery endothelial dysfunction in essential hypertension. Circulation. 2012;125:1266-1275.
107. Fukao M, Hattori Y, Kanno M, et al. Alterations in endotheliumdependent hyperpolarization and relaxation in mesenteric arteries from streptozotocin-induced diabetic rats. Br J Pharmacol. 1997; 121:1383-1391.
108. Wigg SJ, Tare M, Tonta MA, et al. Comparison of effects of diabetes mellitus on an EDHF-dependent and an EDHF-independent artery. Am J Physiol. 2001;281:H232-H240.
109. Brondum E, Kold-Petersen H, Simonsen U, et al. NS309 restores EDHF-type relaxation in mesenteric small arteries from type 2 diabetic ZDF rats. Br J Pharmacol. 2010;159:154-165.
110. Leo CH, Hart JL, Woodman OL. Impairment of both nitric oxidemediated and EDHF-type relaxation in small mesenteric arteries from rats with streptozotocin-induced diabetes. Br J Pharmacol. 2011;162: 365-377.
111. Katakam PVG, Hoenig M, Ujhelyi MR, et al. Cytochrome P450 activity and endothelial dysfunction in insulin resistance. J Vasc Res. 2000;37: 426-434.
112. Malmsjo M, Bergdahl A, Zhao XH, et al. Enhanced acetylcholine and P2Y-receptor stimulated vascular EDHF-dilatation in congestive heart failure. Cardiovasc Res. 1999;43:200-209.
113. Ueda A, Ohyanagi M, Koida S, et al. Enhanced release of endotheliumderived hyperpolarizing factor in small coronary arteries from rats with congestive heart failure. Clin Exp Pharmacol Physiol. 2005;32: 615-621.
114. Katz SD, Krum H. Acetylcholine-mediated vasodilation in the forearm circulation of patients with heart failure: indirect evidence for the role of endothelium-derived hyperpolarizing factor. Am J Cardiol. 2001;87: 1089-1092.
115. Rath G, Saliez J, Behets G, et al. Vascular hypoxic preconditioning relies on TRPV4-dependent calcium influx and proper intercellular gap junctions communication. Arterioscler Thromb Vasc Biol. 2012; 32:2241-2249.