Cytochrome P450 epoxygenase pathway of polyunsaturated fatty acid metabolism

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1851, Issue 4, 2015, Pages 356-365

  Spector, Arthur A ^a   Kim, Hee Yong ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

Arachidonic acid (AA); Docosahexaenoic acid (DHA); Eicosapentaenoic acid (EPA); Epoxydocosapentaenoic acid (EpDPE); Epoxyeicosatetraenoic acid (EpETE); Epoxyeicosatrienoic acid (EET)

Indexed keywords

ARACHIDONIC ACID; CYTOCHROME P450; DOCOSAHEXAENOIC ACID; EPOXYDOCOSAPENTAENOIC ACID DERIVATIVE; EPOXYEICOSATETRAENOIC ACID DERIVATIVE; EPOXYICOSATRIENOIC ACID; ION CHANNEL; LINOLEIC ACID; PHOSPHOLIPID; POLYUNSATURATED FATTY ACID; UNCLASSIFIED DRUG; EPOXIDE; ISOENZYME; UNSATURATED FATTY ACID;

ANGIOGENESIS; ANTIINFLAMMATORY ACTIVITY; ARTICLE; EPOXIDATION; FATTY ACID METABOLISM; FATTY ACID SYNTHESIS; HEART ARRHYTHMIA; HEART PROTECTION; HUMAN; HYDROLYSIS; METASTASIS; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; SIGNAL TRANSDUCTION; VASODILATATION; ANIMAL; DISEASES; HOMEOSTASIS; METABOLISM;

ANIMALS; ARACHIDONIC ACID; CYTOCHROME P-450 ENZYME SYSTEM; DISEASE; EPOXY COMPOUNDS; FATTY ACIDS, UNSATURATED; HOMEOSTASIS; HUMANS; ISOENZYMES; SIGNAL TRANSDUCTION;

EID: 84922507875     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2014.07.020     Document Type: Review

References (169)

1. J.H. Capdevila, J.R. Falck, and R.C. Harris Cytochrome P450 and arachidonic acid bioactivation: molecular and functional properties of arachidonic acid monooxygenases J. Lipid Res. 41 2000 163 181
2. E.H. Oliw Oxygenation of polyunsaturated fatty acids by cytochrome P450 monooxygenases Prog. Lipid Res. 33 1994 329 354
3. R. Roman P-450 metabolites of arachidonic acid in the control of cardiovascular function Physiol. Rev. 82 2002 131 185
4. I. Fleming, and R. Busse Endothelium-derived epoxyeicosatrienoic acids and vascular function Hypertension 47 2006 629 633
5. W.B. Campbell, and I. Fleming Epoxyeicosatrienoic acids and endothelium-dependent responses Pflugers Arch. 459 2010 881 895
6. S.L. Pfister, K.M. Gauthier, and W.B. Campbell Vascular pharmacology of epoxyeicosatrienoic acids Adv. Pharmacol. 60 2010 27 59
7. J.D. Imig Epoxides and soluble epoxide hydrolase in cardiovascular physiology Physiol. Rev. 92 2012 101 130
8. D.C. Zeldin Epoxygenase pathways of fatty acid metabolism J. Biol. Chem. 276 2001 36059 36062
9. A.A. Spector, X. Fang, G.D. Snyder, and N.L. Weintraub Epoxyeicosatrienoic acids (EETs): metabolism and biochemical function Prog. Lipid Res. 43 2004 55 90
10. I. Fleming Epoxyeicosatrienoic acids, cell signaling and angiogenesis Prostaglandins Other Lipid Mediat. 82 2007 60 67
11. B.T. Larsen, W.B. Campbell, and D.D. Gutterman Beyond vasodilation: non-vasomotor roles of epoxyeicosatrienoic acids in the cardiovascular system Trends Pharmacol. Sci. 28 2007 32 38
12. Y. Deng, K.N. Theken, and C.R. Lee Cytochrome P450 epoxygenases, soluble epoxide hydrolase, and the regulation of cardiovascular inflammation J. Mol. Cell. Cardiol. 48 2010 331 341
13. K. Nithipatikom, and G.R. Gross Epoxyeicosatrienoic acids: novel mediators of cardioprotection J. Cardiovasc. Pharmacol. Ther. 15 2010 112 119
14. K. Wagner, B. Inceoglu, and B.D. Hammock Soluble epoxide hydrolase inhibition, epoxygenated fatty acids and nociception Prostaglandins Other Lipid Mediat. 96 2011 78 83
15. G. Zhang, S. Kodani, and B.D. Hammock Stabilized epoxygenated fatty acids regulate inflammation, pain, angiogenesis and cancer Prog. Lipid Res. 53 2014 108 123
16. C. Morisseau, B. Inceoglu, K. Schmelzer, H.-J. Tsai, S.L. Jinks, and C.M. Hegedus Naturally occurring monoexoxides of eicosapentaenoic acid and docosahexaenoic acid are bioselective antihyperalgesic lipids J. Lipid Res. 51 2010 3481 3490
17. C. Westphal, A. Konkel, and W.-H. Schunck CYP-eicosanoids - a new link between omega-3 fatty acids and cardiac disease? Prostaglandins Other Lipid Mediat. 96 2011 99 108
18. G. Zhang, D. Panigrahy, L.M. Mahakian, J. Yang, J.-Y. Liu, and K.S.S. Lee Epoxy metabolites of docosahexaenoic acid (DHA) inhibit angiogenesis, tumor growth, and metastasis Proc. Natl. Acad. Sci. U. S. A. 110 2013 6530 6535
19. N.L. Weintraub, X. Fang, T.L. Kaduce, M. VanRollins, P. Chatterjee, and A.A. Spector Potentiation of endothelium-dependent relaxation by epoxyeicosatrienoic acids Circ. Res. 81 1997 258 267
20. Y. Liu, Y. Zhang, K. Schmelzer, T.S. Lee, X. Fang, and Y. Zhu The anti-inflammatory effect of laminar flow: the role of PPARγ, epoxyeicosatrienoic acids, and soluble epoxide hydrolase Proc. Natl. Acad. Sci. U. S. A. 102 2005 16747 16752
21. W.B. Campbell, and J.R. Falck Arachidonic acid metabolites as endothelium-derived hyperpolarizing factors Hypertension 49 2007 590 596
22. A.A. Spector, and A.W. Norris Action of epoxyeicosatrienoic acids on cellular function Am. J. Physiol. Cell Physiol. 292 2007 C996 C1012
23. + channel activity Am. J. Physiol. Ren. Fluid Electrolyte Physiology 270 1996 F822 F832
24. + channels by epoxyeicosatrienoic acids: a structural determinant study Mol. Pharmacol. 62 2002 1076 1083
25. M.F. Moghaddam, D.F. Grant, J.M. Cheek, J.F. Greene, K.C. Williamson, and B.D. Hammock Bioactivation of leukotoxins to their toxic diols by epoxide hydrolase Nat. Med. 3 1997 562 566
26. G.C. Shearer, W.S. Harris, T.L. Pedersen, and J.W. Newman Detection of omega-3 oxylipins in human plasma and response to treatment with omega-3 acid ethyl esters J. Lipid Res. 51 2010 2074 2081
27. M. VanRollins, R.C. Baker, H.W. Sprecher, and R.C. Murphy Oxidation of docosahexaenoic acid by rat liver microsomes J. Biol. Chem. 259 1984 5776 5783
28. M. Fer, Y. Dréano, D. Lucas, L. Corcos, J.-P. Salaün, and F. Berthou Metabolism of eicosapentaenoic and docosahexaenoic acid by recombinant cytochromes P450 Arch. Biochem. Biophys. 471 2008 116 125
29. D. Lucas, S. Goulitquer, J. Marienhagen, M. Fer, Y. Dreano, and U. Schwaneberg Stereoselective epoxydation of the last double bond of polyunsaturated fatty acids by human cytochromes P450 J. Lipid Res. 51 2010 1125 1133
30. C. Arnold, M. Markovic, K. Blossey, G. Wallukat, R. Fischer, and R. Dechend Arachidonic acid-metabolizing cytochrome P450 enzymes are targets of ω-3 fatty acids J. Biol. Chem. 285 2010 32720 32733
31. M. VanRollins Epoxygenase metabolites of docosahexaenoic and eicosapentaenoic acids inhibit platelet aggregation at concentrations below those affecting thromboxane synthesis J. Pharmacol. Exp. Ther. 274 1995 798 804
32. R.L. Widstrom, A.W. Norris, and A.A. Spector Binding of cytochrome P450 monooxygenase and lipooxygenase pathway products by heart fatty acid-binding protein Biochemistry 40 2001 1070 1076
33. R.L. Widstrom, A.W. Norris, J. van der Veer, and A.A. Spector Fatty acid-binding proteins inhibit hydration of epoxyeicosatrienoic acids by soluble epoxide hydrolase Biochemistry 42 2003 11762 11767
34. G.C. Shearer, and J.W. Newman Lipoprotein lipase releases esterified oxylipins from very low-density lipoproteins Prostaglandins Leukot. Essent. Fat. Acids 79 2008 215 222
35. E.L. Klett, S. Chen, M.L. Edin, L.O. Li, O. Ilkayeva, D.C. Zeldin, C.B. Newgard, and R.A. Coleman Diminished acyl-CoA synthetase isoform 4 activity in INS 832/13 cells reduces cellular epoxyeicosatrienoic acid levels and results in impaired glucose-stimulated insulin secretion J. Biol. Chem. 288 2013 21618 21629
36. J. Chen, J.H. Capdevila, D.C. Zeldin, and R.L. Rosenberg Inhibition of cardiac L-type calcium channels by epoxyeicosatrienoic acids Mol. Pharmacol. 55 1999 288 295
37. J. Chen, J.-K. Chen, J.R. Falck, J.S. Guthi, S. Anjaiah, and J.H. Capdevila Mitogenic activity and signaling mechanism of 2-(14,15-epoxyeicosatrienoyl)glycerol, a novel cytochrome p450 arachidonate metabolite Mol. Cell. Biol. 27 2007 3023 3034
38. J. Chen, J.-K. Chen, J.D. Imig, S. Wei, D.L. Hackney, and J.S. Guthi Identification of novel endogenous cytochrome p450 arachidonate metabolites with high affinity for cannabinoid receptors J. Biol. Chem. 283 2008 24514 24524
39. J.W. Newman, C. Morriseau, and B.D. Hammock Epoxide hydrolases: their role and interactions with lipid metabolism Prog. Lipid Res. 44 2005 1 51
40. A. Marowsky, J. Burgener, J.R. Falck, and M.A. Arand Distribution of soluble and microsomal epoxide hydrolase in the mouse brain and its contribution to cerebral epoxyeicosatrienoic acid metabolism Neuroscience 163 2009 646 661
41. S. Rawal, C. Morriseau, B.D. Hammock, and A.C. Shivachar Differential subcellular distribution and colocalization of the microsomal and soluble epoxide hydrolases in cultured neonatal rat brain cortical astrocytes J. Neurosci. Res. 87 2009 218 227
42. R.A. Bianco, K. Agassandian, M.D. Cassell, A.A. Spector, and C.D. Sigmund Characterization of transgenic mice with neuron-specific expression of soluble epoxide hydrolase Brain Res. 1291 2009 60 72
43. J.W. Nelson, R.M. Subrahmanyan, S.A. Summers, X. Xiao, and N.J. Alkayed Soluble epoxide hydrolase dimerization is required for hydrolase activity J. Biol. Chem. 288 2013 7697 7703
44. A. Cronin, S. Mowbray, H. Dürk, S. Homberg, I. Fleming, and B. Fisslthaler The N-terminal domain of mammalian soluble epoxide hydrolase is a phosphatase Proc. Natl. Acad. Sci. U. S. A. 100 2003 1552 1557
45. J.W. Newman, C. Morriseau, T.R. Harris, and B.D. Hammock The soluble epoxide hydrolase encoded by EPXH2 is a bifunctional enzyme with a novel lipid phosphate phosphatase activity Proc. Natl. Acad. Sci. U. S. A. 100 2003 1558 1563
46. A.E. Enayetallah, and D.F. Grant Effects of human soluble epoxide hydrolase polymorphisms on isoprenoid phosphate hydrolysis Biochem. Biophys. Res. Commun. 341 2006 254 260
47. A. Oguro, and S. Imaoka Lysophosphatidic acids are new substrates for the phosphatase domain of soluble epoxide hydrolase J. Lipid Res. 53 2012 505 512
48. A. Oguro, K. Sakamoto, S. Suzuki, and S. Imaoka Contribution of the hydrolase and phosphatase domains in soluble epoxide hydrolase to vascular endothelial growth factor expression and cell growth Biol. Pharm. Bull. 32 2009 1962 1967
49. D.C. Zeldin, S. Wei, J.R. Falck, B.D. Hammock, J.R. Snapper, and J.H. Capdevila Metabolism of epoxyeicosatrienoic acids by cytosolic epoxide hydrolase: substrate structural determinants of asymmetric catalysis Arch. Biochem. Biophys. 316 1995 443 451
50. M. VanRollins, T.L. Kaduce, X. Fang, H.R. Knapp, and A.A. Spector Arachidonic acid diols produced by cytochrome P-450 monooxygenase are incorporated into phospholipids of vascular endothelial cells J. Biol. Chem. 271 1996 14001 14009
51. B. Inceoglu, K.M. Wagner, J. Yang, A. Battaieb, N.H. Schebb, S.H. Hwang, and C. Acute augmentation of epoxygenated fatty acid levels rapidly reduces pain-related behavior in a rat model if type 1 diabetes Proc. Natl. Acad. Sci. U. S. A. 109 2012 11390 11395
52. M.J. Bruins, A.D. Dane, K. Strassburg, R.J. Vreeken, J.W. Newman, and N. Salem Jr. Plasma oxylipin profiling identifies polyunsaturated vicinal diols as responsive to arachidonic acid and docosahexaenoic acid intake in growing piglets J. Lipid Res. 54 2013 1598 1607
53. M. Decker, M. Adamska, A. Cronin, F. Di Giallonardo, J. Burgener, and A. Markowsky EH3 (ABHD9): the first member of a new epoxide hydrolase family with high activity for fatty acid epoxides J. Lipid Res. 53 2012 2038 2045
54. A.A. Spector Arachidonic acid cytochrome P450 epoxygenase pathway J. Lipid Res. 50 2009 S52 S56
55. N. Chiamvimonvat, C.-M. Ho, H.-J. Tsai, and B.D. Hammock The soluble epoxide hydrolase as a pharmaceutical target for hypertension J. Cardiovasc. Pharmacol. 50 2007 225 237
56. J.D. Imig, and B.D. Hammock Soluble epoxide hydrolase as a therapeutic target for cardiovascular disease Nat. Rev. Drug Discov. 8 2009 794 805
57. M. Revermann Pharmacologic inhibition of the soluble epoxide hydrolase Curr. Opin. Pharmacol. 10 2010 173 178
58. H. Kim, H.J. Tsai, K. Nishi, T. Kasagami, C. Morisseau, and B.D. Hammock 1.3-Disubstituted ureas functionalized with ether groups are potent inhibitors of soluble epoxide hydrolase with improved pharmacokinetic properties J. Med. Chem. 50 2007 5217 5226
59. K.L. Tran, P.A. Aronov, H. Tanaka, J.W. Newman, B.D. Hammock, and C. Morisseau Lipid sulfates and sulfonates are allosteric competitive inhibitors of the N-terminal phosphatase activity of the mammalian of soluble epoxide hydrolase Biochemistry 44 2005 12179 12187
60. S.H.H. Hwang, H.J. Tsai, J.Y. Liu, C. Morisseau, and B.D. Hammock Orally bioavailable and potent soluble epoxide hydrolase inhibitors J. Med. Chem. 50 2007 3825 3840
61. J.R. Falck, R. Kodela, R. Manne, K.R. Atcha, N. Puli, and N. Dubasi 14,15-Epoxyeicosa-5,8,11-trienoic acid (14,15-EET) surrogates containing epoxide bioisosteres: influence upon vascular relaxation and soluble epoxide hydrolase inhibition J. Med. Chem. 52 2009 5069 5075
62. Y. Liu, R. Wang, J. Li, J. Rao, W. Li, and J.R. Falck Stable EET urea agonist and soluble epoxide hydrolase inhibitor regulate rat pulmonary arteries through TRPCs Hypertens. Res. 34 2011 630 638
63. E. la Buscató, R.B. Blöcher, C. Lamers, F.-M. Klingler, S. Hahn, and D. Steinhilber Design and synthesis of dual modulators of soluble epoxide hydrolase and peroxisome proliferator-activated receptors J. Med. Chem. 55 2012 10771 10775
64. K. Meirer, C.H. Rödl, J.M. Wisniewska, S. George, A.K. Häfner, and E. la Buscató Synthesis and structural activity relationship studies of novel dual inhibitors of soluble epoxide hydrolase and 5-lipoxygenase J. Med. Chem. 56 2013 1777 1781
65. S.H. Hwang, A.T. Wecksler, G. Zhang, C. Morisseau, L.V. Nguyen, S.H. Fu, and B.D. Hammock Synthesis and biological evaluation of sorafenib- and regorafenib-like soluble epoxide hydrolase inhibitors Bioorg. Med. Chem. Lett. 23 2013 3732 3737
66. S.N. Batchu, S.B. Lee, V. Samokhvalov, K.R. Chaudhary, H. El-Sikhry, S.M. Weldon, and J.M. Seubert Novel soluble epoxide hydrolase inhibitor protects mitochondrial function following stress Can. J. Physiol. Pharmacol. 90 2012 811 823
67. C. Morisseau, S. Pakhomova, S.H. Hwang, M.E. Newcomer, and B.D. Hammock Inhibition of soluble epoxide hydrolase by fulvestrant and sulfoxides Bioorg. Med. Chem. Lett. 23 2013 3818 3821
68. S.H. Hwang, K.M. Wagner, C. Morisseau, J.Y. Liu, H. Dong, A.T. Wecksler, and B.D. Hammock Synthesis and structure-activity relationship studies of urea-containing pyrazoles as dual inhibitors of cyclooxygenase-2 and soluble epoxide hydrolase J. Med. Chem. 54 2011 3037 3050
69. X. Fang, S. Hu, T. Watanabe, N.L. Weintraub, G.D. Snyder, and J. Yao Activation of peroxisome proliferator-activated receptor α by substituted urea-derived soluble epoxide hydrolase inhibitors J. Pharmacol. Exp. Ther. 314 2005 260 270
70. E. Brand-Schrieber, J.R. Falck, and M. Schwartzman Selective inhibition of arachidonic acid epoxygenation in vivo J. Physiol. Pharmacol. 51 2000 655 672
71. K.M. Gauthier, C. Deeter, U.M. Krishna, Y.K. Reddy, M. Bondlena, and J.F. Falck 14,15-Epoxyeicosa-5(Z)enoic acid: a selective epoxyeicosatrienoic acid antagonist that inhibits endothelium-dependent hyperpolarization and relaxation in coronary arteries Circ. Res. 90 2002 1028 1036
72. J.R. Falck, G. Wallukat, N. Puli, M. Goli, C. Arnold, and A. Konkel 17(R),18(S)-Epoxyeicosatetraenoic acid, a potent eicosapentaenoic acid (EPA) derived regulator of cardiomyocyte contraction: structure-activity relationships and stable analogues J. Med. Chem. 54 2011 4109 4118
73. I.A. Bukhari, K.M. Gauthier, S.G. Jagadeesh, B. Sangras, J.R. Falck, and W.B. Campbell 14,15-Dihydroxy-eicosa-5(Z)-enoic acid selectively inhibits 14,15-epoxyeicosatrienoic acid-induced relaxations of bovine coronary arteries J. Pharmacol. Exp. Ther. 336 2011 47 55
74. I.A. Bukhari, A.J. Shah, K.M. Gauthier, K.A. Walsh, S.R. Koduru, and J.D. Imig 11,12,20-Trihydroxy-eicosa-8(Z) enoic acid: a selective inhibitor of 11,12-EET-induced relaxations of bovine coronary and rat mesenteric arteries Am. J. Physiol. Heart Circ. Physiol. 302 2012 H1574 H1583
75. C.J. Sinal, M. Myata, M. Tohkin, K. Nagata, J.R. Bend, and F.J. Gonzalez Targeted disruption of soluble hydroxide hydrolase reveals a role in blood pressure regulation J. Biol. Chem. 275 2000 40504 40510
76. C.L. Oltman, N.L. Weintraub, M. VanRollins, and K.C. Dellsperger Epoxyeicosatrienoic acids and dihydroxyeicosatrienoic acids are potent vasodilators in the canine coronary microcirculation Circ. Res. 83 1998 932 939
77. Ca channels: implications for soluble epoxide hydrolase inhibition Am. J. Physiol. Heart Circ. Physiol. 290 2006 H491 H499
78. + channels in isolated rat coronary arterial myocytes J. Physiol. 534 2001 651 667
79. X. Fang, S. Hu, B. Xu, G.D. Snyder, S. Harmon, and J. Yao 14,15-Dihydroxyeicosatrienoic acid activates peroxisome proliferator-activated receptor α Am. J. Physiol. Heart Circ. Physiol. 290 2006 H55 H63
80. V.Y. Ng, Y. Huang, L.M. Reddy, J.R. Falck, E.T. Lin, and D.L. Kroetz Cytochrome P450 eicosanoids are activators of peroxisome proliferator-activated receptor α Drug Metab. Dispos. 35 2007 1126 1134
81. M. Abukhashim, G.J. Wiebe, and J.M. Seubert Regulation of forskolin-induced cAMP production by cytochrome P450 epoxygenase metabolites of arachidonic acid in HEK293 cells Chem. Biol. Toxicol. 27 2011 321 332
82. T. Frömel, B. Jungblut, J. Hu, C. Trouvain, E. Barbosa-Sicard, and R. Popp Soluble epoxide hydrolase regulates hematopoietic progenitor cell function via generation of fatty acid diols Proc. Natl. Acad. Sci. U. S. A. 109 2012 9995 10000
83. S. Kundu, T. Roome, A. Bhattacharjee, K.A. Carnevale, V.P. Yakubenko, and R. Zhang Metabolic products of soluble epoxide hydrolase are essential for monocytic chemotaxis to MCP-1 in vitro and in vivo J. Lipid Res. 54 2013 436 447
84. X. Fang, N.L. Weintraub, C.L. Oltman, L.L. Stoll, T.L. Kaduce, and S. Harmon Human coronary endothelial cells convert 14,15-EET to a biologically active chain-shortened epoxide Am. J. Physiol. Heart Circ. Physiol. 283 2002 H2306 H2314
85. X.Y. Yi, K.M. Gauthier, K. Cui, K. Nithipatikom, J.R. Falck, and W.B. Campbell Metabolism of adrenic acid to vasodilatory 1α,1β-dihomo-epoxyeicosatrienoic acids by bovine coronary arteries Am. J. Physiol. Heart Circ. Physiol. 292 2007 H2265 H2274
86. X. Fang, T.L. Kaduce, N.L. Weintraub, S. Harmon, L.M. Teesch, and C. Morisseau Pathways of epoxyeicosatrienoic acid metabolism in endothelial cells. Implications for the vascular effects of soluble epoxide hydrolase inhibition J. Biol. Chem. 276 2001 14867 14874
87. X. Fang, N.L. Weintraub, R.B. McCaw, S. Hu, S. Harmon, and J.B. Rice Effect of soluble epoxide hydrolase inhibition on epoxyeicosatrienoic acid metabolism in human blood vessels Am. J. Physiol. Heart Circ. Physiol. 287 2004 H2412 H2420
88. L.A. Cowart, S. Wei, M.H. Hsu, E.F. Johnson, M.U. Krishna, and J.R. Falck The CYP4A isoforms hydroxylate epoxyeicosatrienoic acids to form high affinity peroxisome proliferator-activate receptor ligands J. Biol. Chem. 277 2002 35105 35112
89. M.A. Carroll, M. Balazy, P. Margiotta, J.R. Falck, and J.C. McGiff Renal vasodilator activity of 5,6-epoxyeicosatrienoic acid depends upon conversion by cyclooxygenase and release of prostaglandins J. Biol. Chem. 268 1993 12260 12266
90. N.T. Snider, R.M. Kornilov, U.M. Kent, and P.F. Hollenberg Anamdamide metabolism by human liver and kidney microsomal cytochrome P450 enzymes to form hydroxyeicosatetraenoic and epoxyeicosatrienoic acid ethanolamides J. Pharmacol. Exp. Ther. 321 2007 590 597
91. C. Sridar, N.T. Snider, and P.M. Hollenberg Anandamide oxidation by wild-type and polymorphically expressed CYP2B6 and CYP2D6 Drug Metab. Dispos. 39 2011 782 788
92. N.T. Snider, V.J. Walker, and P.F. Hollenberg Oxidation of the endogenous cannabinoid arachidonoyl ethanolamide by the cytochrome P450 monooxygenases: physiological and pharmacological implications Pharmacol. Rev. 62 2010 136 154
93. H.-Y. Kim, H.-S. Moon, D. Cao, J. Lee, K. Kevala, and S.B. Jun N-docosylhexaenoylethanolamide promotes development of hippocampal neurons Biochem. J. 435 2011 327 336
94. M.A. Rashid, M. Katakura, G. Khavebava, and H.-Y. Kim N-docosylhexaenoylethanolamine is a potent neurogenic factor for neural stem cell differentiation J. Neurochem. 125 2013 869 884
95. R. Yang, G. Fredman, S. Krishnamoorthy, N. Agrawal, D. Irimia, and D. Piomelli Decoding functional metabolomics with docosahexaenoylethanolamide (DHEA) identifies novel bioactive signals J. Biol. Chem. 286 2011 31532 31541
96. P.L. Li, C.L. Chen, R. Bortell, and W.B. Campbell 11,12-Epoxyeicosatrienoic acid stimulates endogenous mono-ADP-ribosylation in bovine coronary arterial smooth muscle cells Circ. Res. 85 1999 349 356
97. M.A. Carroll, A.B. Doumond, J. Li, M.K. Cheng, J.R. Falck, and J.C. McGiff Adenosine 2A receptor vadodilation of rat preglomerular microvessels is mediated by EETs that activate the cAMP/PKA pathway Am. J. Physiol. Ren. Physiol. 291 2006 F155 F161
98. + channels by epoxyeicosatrienoic acids in rat cardiac ventricular myocytes J. Physiol. 537 2001 821 827
99. H. Watanabe, J. Vriens, J. Prenen, G. Droogmans, T. Voets, and B. Nilius Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TPRV4 channels Nature 424 2003 434 438
100. P.Y. Wong, P.S. Lai, and J.R. Falck Mechanism and signal transduction of 14(R),15(S)-epoxyeicosatrienoic acid (14,15-EET) binding in guinea pig monocytes Prostaglandins Other Lipid Mediat. 62 2000 321 333
101. W. Yang, B.B. Holmes, V.R. Gopal, R.V. Krishna Hishore, B. Sangras, and X.-Y. Yi Characterization of 14,15-epoxyeicosatrienoyl-sulfonamides 14,15-epoxyeicosatrienoic acid agonists: use of studies of metabolism and ligand binding J. Pharmacol. Exp. Ther. 321 2007 1023 1031
102. G.D. Snyder, U. Murali Krishna, J.R. Falck, and A.A. Spector Evidence for a membrane site of action for 14,15-EET on expression of aromatase in vascular smooth muscle Am. J. Physiol. Heart Circ. Physiol. 282 2002 H1936 H1942
103. Y. Chen, J.R. Falck, V.L. Manthati, J.L. Jat, and W.B. Campbell 20-Iodo-14,15-epoxyeicosa-8(Z)-enoyl-3-azidophenylsulfonamide: photoaffinity labeling of a 14,15-epoxyeicosatrienoic acid receptor Biochemistry 50 2011 3840 3848
104. 2 receptors in rat mesenteric arteries Prostaglandins Other Lipid Mediat. 93 2010 44 51
105. D.J. Behm, A. Ogbonna, C. Wu, C.L. Burns-Kurtis, and S.A. Douglas Epoxyeicosatrienoic acids function as selective, endogenous antagonists of native thromboxane receptors: identification of a novel mechanism of vasodilation J. Pharmacol. Exp. Ther. 328 2009 231 239
106. B. Inceoglu, K.R. Schmelzer, C. Morisseau, S.L. Jinks, and B.D. Hammock Soluble epoxide hydrolase inhibition reveals novel biological functions of epoxyeicosatrienoic acids (EETs) Prostaglandins Other Lipid Mediat. 82 2007 42 49
107. Ca channels Am. J. Physiol. Heart Circ. Physiol. 280 2001 H2430 H2440
108. R. Wang, Q. Chai, T. Lu, and H.-C. Lee Activation of vascular BK channels by docosahexaenoic acid is dependent on cytochrome P450 epoxygenase activity Cardiovasc. Res. 90 2011 344 352
109. D. Ye, D. Zhang, C. Oltman, K. Dellsperger, H.-C. Lee, and M. VanRollins Cytochrome P-450 epoxygenase metabolites of docosahexaenoate potently dilate coronary arterioles by activating large- conductance calcium-activated potassium channels J. Pharmacol. Exp. Ther. 303 2002 768 776
110. C. Morin, M. Sirois, V. Echave, E. Rizcallah, and E. Rousseau Relaxing effects of 17(18)-EpETE on arterial and airway smooth muscles in human lung Am. J. Physiol. Lung Cell. Mol. Physiol. 296 2009 L130 L139
111. B. Lauterbach, E. Barbosa-Sicard, M.-H. Wang, H. Honeck, E. Kargel, and J. Theuer Cytochrome P450-dependent eicosapentaenoic acid metabolites are novel BK channel activators Hypertension 39 2002 609 613
112. H.C. Hercule, B. Salanova, K. Essin, H. Honeck, J.R. Falck, and M. Sausbier The vasodilator 17,18-epoxyeicosatetraenoic acid targets the pore-forming BKα channel subunit in rodents Exp. Physiol. 92 2007 1067 1076
113. 2 + permeable cation channel TRPV4 by cytochrome P450 epoxygenases in vascular endothelium Circ. Res. 97 2005 908 915
114. Ca channels J. Cardiovasc. Pharmacol. 57 2011 148 153
115. 2 + signaling and hyperpolarization in endothelial cells Arterioscler. Thromb. Vasc. Biol. 27 2007 2612 2618
116. A.E. Loot, and I. Fleming Cytochrome P450-derived epoxyeicosatrienoic acids and pulmonary hypertension: central role of transient receptor potential C6 channels J. Cardiovasc. Res. 57 2011 140 147
117. X. Fang, N.L. Weintraub, L.L. Stoll, and A.A. Spector Epoxyeicosatrienoic acids increase intracellular calcium concentration in vascular smooth muscle cells Hypertension 34 1999 1242 1246
118. H.-C. Lee, T. Lu, N.L. Weintraub, M. VanRollins, A.A. Spector, and E.F. Shibata Effects of epoxyeicosatrienoic acids on sodium channels in isolated rat ventricular myocytes J. Physiol. 519 1999 153 168
119. T.S. Pavlov, D.V. Ilatovskaya, V. Levchenko, D.L. Mattson, R.J. Roman, and A. Staruschenko Effects of cytochrome P-450 metabolites of arachidonic acid on epithelial sodium channel (ENaC) Am. J. Physiol. Ren. Physiol. 301 2011 F672 F681
120. N. Pidkovka, R. Rao, S. Mei, Y. Gong, R.C. Harris, and W.-H. Schunck Epoxyeicosatrienoic acids (EETs) regulate epithelial sodium channel activity by extracellular signal-regulated kinase (ERK1/2)-mediated phosphorylation J. Biol. Chem. 288 2013 5223 5231
121. A. Ulu, T.R. Harris, C. Morisseau, C. Miyabi, H. Inoue, and G. Schuster Anti-inflammatory effects of ω-3 polyunsaturated fatty acids and soluble epoxide hydrolase inhibitors in angiotensin-II-dependent hypertension J. Cardiovasc. Pharmacol. 62 2013 285 297
122. ATP channels in rats are activated by endogenous epoxyeicosatrienoic acids through different mechanisms J. Physiol. 575 2006 627 644
123. C. Yang, Y.W. Kwan, S.W. Seto, and G.H.P. Leung Inhibitory effects of epoxyeicosatrienoic acids on volume-activated chloride channels in rat mesenteric arterial smooth muscle Prostaglandins Other Lipid Mediat. 87 2008 62 67
124. D.H. Munzenmaier, and D.R. Harder Cerebral microvascular endothelial tube formation: role of astrocyte epoxyeicosatrienoic acid release Am. J. Physiol. Heart Circ. Physiol. 278 2000 H1163 H1167
125. C. Zhang, and D.R. Harder Cerebral capillary endothelial cell mitogenesis and morphogenesis induced by astrocytic epoxyeicosatrienoic acid Stroke 33 2002 2957 2964
126. M. Medhora, J. Daniels, K. Mundey, B. Fisslthaler, R. Busse, and E.R. Jacobs Epoxygenase-driven angiogenesis in human lung microvascular endothelial cells Am. J. Physiol. Heart Circ. Physiol. 284 2003 H215 H224
127. Kip1 J. Biol. Chem. 278 2003 29619 29625
128. U.R. Michaelis, B. Fisslthaler, E. Barbosa-Sicard, J.R. Falck, I. Fleming, and R. Busse Cytochrome P450 epoxygenases 2C8 and 2C9 are implicated in hypoxia-induced endothelial migration and angiogenesis J. Cell Sci. 118 2005 5489 5498
129. Y. Wang, X. Wei, X. Xiao, R. Hui, J.W. Card, and M.A. Carey Arachidonic acid epoxygenase metabolites stimulate endothelial cell growth and angiogenesis via mitogen-activated protein kinase and phosphatidylinositol-3-kinase/Akt signaling pathways J. Pharmacol. Exp. Ther. 314 2005 522 532
130. A. Pozzi, I. Macias-Perez, T. Abair, S. Wei, Y. Su, and R. Aent Characterization of 5,6- and 8,9-epoxyeicosatrienoic acids (5,6- and 8,9-EET) as potent in vivo angiogenic lipids J. Biol. Chem. 280 2005 27138 27146
131. J. Ma, L. Zhang, W. Han, T. Shen, C. Ma, and Y. Liu Activation of JNK/cJun is required for the proliferation, survival and angiogenesis induced by EET in pulmonary artery endothelial cells J. Lipid Res. 53 2012 1093 1105
132. C. Yan, S. Chen, B. You, and J. Sun Activation of sphingosine kinase-1 mediates induction of endothelial cell proliferation and angiogenesis by epoxyeicosatrienoic acids Cardiovasc. Res. 78 2008 308 314
133. A.C. Webber, R. Popp, U. Thomas Korff, R. Mechaelis, C. Urbich, and R. Busse Cytochrome P450 2C9-induced angiogenesis is dependent on EphB4 Arterioscler. Thromb. Vasc. Biol. 28 2008 1123 1129
134. B. Zhang, H. Cao, and G.N. Rao Fibroblast growth factor-2 is a downstream mediator of phosphatidylinositol 3-kinase-Akt in 14,15-epoxyeicosatrienoic acid-induced angiogenesis J. Biol. Chem. 281 2006 905 914
135. S.Y. Chenova, M. Karpurapu, D. Wang, B. Zhang, R.C. Venema, and G.N. Rao An essential role for Src-activated STAT-3 in 14,15-EET-induced VEGF expression and angiogenesis Blood 111 2008 5581 5591
136. A.L. Sander, H. Jakob, K. Sommer, C. Sadler, I. Fleming, and I. Marzi Cytochrome P450-derived epoxyeicosatrienoic acids accelerate wound epithelialization and neovascularization in the hairless mouse ear wound model Langenbeck's Arch. Surg. 396 2011 1245 1253
137. P.H. Cui, N. Petrovic, and M. Murray The ω-3 epoxide of eicosapentaenoic acid inhibits endothelial cell proliferation by p38 MAP kinase activation and cyclin D1/CDK4 down-regulation Br. J. Pharmacol. 162 2011 1143 1155
138. D. Panigrahy, E.R. Greene, A. Pozzi, D.W. Wang, and D.C. Zeldin EET signaling in cancer Cancer Metastasis Rev. 30 2010 525 540
139. D. Panigrahy, M.L. Edin, C.R. Lee, S. Huang, D.R. Bielenberg, and C.E. Butterfield Epoxyeicosanoids stimulate multiorgan metastasis and tumor dormancy escape in mice J. Clin. Invest. 122 2012 178 191
140. C. Chen, X. Wei, J. Wu, S. Yang, F. Chen, and D. Ma Cytochrome P450 2J2 is highly expressed in hematologic malignant diseases and promotes tumor cell growth J. Pharmacol. Exp. Ther. 336 2011 344 355
141. K. Nithipatikom, D.M. Brody, A.T. Tang, V.J. Mathati, C.L. Williams, and W.B. Campbell Inhibition of carcinoma cell motility by epoxyeicosatrienoic acid (EET) antagonists Cancer Sci. 101 2010 2629 2636
142. R. Mitra, M. Milani, C. Mesaros, M. Rodriguez, J. Nguyen, and X. Luo Cyp3A4 mediates growth of estrogen receptor-positive breast cancer cells in part by inducing nuclear translocation of phosphor-Stat3 through biosynthesis of (±)-14,15-epoxyeicosatrienoic acid (14,15-EET) J. Biol. Chem. 286 2011 17543 17559
143. D. Panigrahy, B.T. Kalish, S. Huang, D.R. Bielenberg, H.D. Le, and J. Yang Epoxyeicosanoids promote organ and tissue regeneration Proc. Natl. Acad. Sci. U. S. A. 110 2013 13528 13533
144. K. Node, Y. Huo, X. Ruan, Y. Yang, M. Spiecker, and K. Ley Anti-inflammatory properties of cytochrome P450 epoxygenase-derived eicosanoids Science 285 1999 1276 1279
145. Y. Deng, M.L. Edin, K.N. Theken, R.N. Schuck, G.P. Flake, and M.A. Kannon Endothelial CYP epoxygenase overexpression and soluble epoxide hydrolase disruption attenuate acute vascular inflammatory responses in mice FASEB J. 25 2011 703 713
146. Y. Gao, J. Feng, K. Ma, Z. Zhou, Y. Zhu, and Q. Xu 8,9-Epoxyeicosatrienoic acid inhibits antibody production of B-lymphocytes in mice PLoS ONE 7 2012 e40258
147. J.-X. Jiang, S.-J. Zhang, Y.-N. Liu, X.X. Lin, Y.H. Sun, and H.J. Shen EETs alleviate ox-LDL-induced inflammation by inhibiting LOX-1 receptor expression in rat pulmonary arterial endothelial cells Eur. J. Pharmacol. 727 2014 43 51
148. G. Zhao, J. Wang, X. Xu, Y. Jing, L. Tu, and X. Li Epoxyeicosatrienoic acids protect rat hearts against tumor necrosis factor-α-induced injury J. Lipid Res. 53 2012 456 466
149. C. Morin, M. Sirois, V. Echave, R. Albadine, and E. Rousseau 17,18-Epoxyeicosatetraenoic acid targets PPARγ and p38 mitogen-activated protein kinase to mediate its anti-inflammatory effects in the lung Am. J. Respir. Cell Mol. Biol. 43 2010 564 575
150. M.A.H. Khan, J. Neckář, V. Manthati, R. Errabelli, T.S. Pavlov, and A. Staruschenko Orally active epoxyeicosatrienoic acid analog attenuates kidney injury in hypertensive Dahl salt-sensitive rat Hypertension 62 2013 905 913
151. A. Bettaieb, N. Nagata, D. AbouBechara, S. Chahed, C. Morisseau, B.D. Hammock, and F.G. Haj Soluble epoxide hydrolase deficiency or inhibition attenuates diet-induced endoplasmic reticulum stress in liver and adipose tissue J. Biol. Chem. 288 2013 14189 14199
152. A. Luria, A. Battaieb, Y. Xi, G.-J. Shieh, H.-C. Liu, and H. Inoue Soluble epoxide hydrolase deficiency alters pancreatic islet size and improves glucose homeostasis in a model of insulin resistance Proc. Natl. Acad. Sci. U. S. A. 108 2011 9038 9043
153. J.J. Iliff, J. Jia, J. Nelson, T. Goyagi, J. Klaus, and N.J. Alkayed Epoxyeicosanoid signaling in CNS function and disease Prostaglandins Other Lipid Mediat. 91 2010 68 84
154. E. Abdu, D.A. Bruun, D. Yang, B. Inceoglu, B.D. Hammock, and N.J. Alkayed Epoxyeicosatrienoic acids enhance axonal growth in primary sensory and cortical neuronal cell cultures J. Neurochem. 117 2011 632 642
155. X. Liu, C. Li, D. Gebremedhin, S.H. Hwang, B.D. Harder, J.L. Falck, D.R. Harder, and R.C. Koehler Epoxyeicosatrienoic acid-dependent cerebral vasodilation evoked by metabotropic glutamate receptor activation in vivo Am. J. Physiol. Heart Circ. Physiol. 301 2011 H373 H381
156. + signaling in perivascular astrocytes Am. J. Physiol. Cell Physiol. 299 2010 C1068 C1078
157. M. Terashvili, L.T. Tseng, H. Wu, J. Narayanan, L.M. Hart, and J.R. Falck Antinociception produced by 14,15-epoxyeicosatrienoic acid is mediated by the activation of β-endorphin and met-enkephalin in the rat ventrolateral periaqueductal gray J. Pharmacol. Exp. Ther. 326 2008 614 622
158. M. Terashvili, P. Sarkar, M.V. Nostrand, J.R. Falck, and B.D. Harder The protective effect of astrocyte-derived 14,15-epoxyeicosatrienoic acid on hydrogen peroxide-induced cell injury in astrocyte-dopaminergic neuronal cell line co-culture Neuroscience 223 2012 68 76
159. B. Inceoglu, D. Zolkowska, H.J. Yoo, K.M. Wagner, J. Yang, and E. Hackett Epoxy fatty acids and inhibition of soluble epoxide hydrolase selectively modulate GABA neurotransmission to delay onset of seizures PLoS ONE 8 2013 e80922
160. B. Inceoglu, S.L. Jinks, A. Ulu, C.M. Hegedus, K. Georgi, and K.R. Schmelzer Soluble epoxide hydrolase and epoxyeicosatrienoic acids modulate two distinct analgesics pathways Proc. Natl. Acad. Sci. U. S. A. 105 2008 18901 18906
161. G.R. Gross, K.M. Gauthier, J. Moore, J.R. Falck, B.D. Hammock, and W.B. Campbell Effect of the selective EET antagonist 14,15-EEZE on cardioprotection produced by exogenous or endogenous epoxyeicosatrienoic acids in the canine heart Am. J. Physiol. Heart Circ. Physiol. 294 2008 H2838 H2844
162. G.R. Gross, K.M. Gauthier, J. Moore, W.B. Campbell, J.R. Falck, and K. Nithipatikom Evidence for role of epoxyeicosatrienoic acids in mediating ischemic preconditioning and postconditioning in dog Am. J. Physiol. Heart Circ. Physiol. 297 2009 H47 H52
163. K.R. Chaudhary, M. Abukhashim, S.H. Hwang, B.D. Hammock, and J.M. Seubert Inhibition of soluble hydroxide hydrolase by trans-4-[4-(3-adamantan-1-yl-ureido)-cyclohexyloxy]-benzoic acid is protective against ischemia-reperfusion injury J. Cardiovasc. Pharmacol. 55 2010 67 73
164. P. Sirish, N. Li, J.-Y. Liu, K.S.S. Lee, S.H.H. Hwang, and H. Qui Unique mechanistic insights into the beneficial effects of soluble epoxide hydrolase inhibitors in the prevention of cardiac fibrosis Proc. Natl. Acad. Sci. U. S. A. 110 2013 5618 5623
165. D. Katragadda, S.N. Batchu, W.J. Cho, K.R. Chaudhary, J.R. Falck, and J.M. Seubert Epoxyeicosatrienoic acids limit damage to mitochondrial function following stress in cardiac cells J. Mol. Cell. Cardiol. 46 2009 867 875
166. G.R. Gross, J.E. Baker, A. Hsu, H. Wu, J.R. Falck, and K. Nithipatikom Evidence for a role of opioids in epoxyeicosatrienoic acid-induced cardioprotection in rat hearts Am. J. Physiol. Heart Circ. Physiol. 298 2010 H2201 H2207
167. Y. Zhang, H. El-Sikhry, K.R. Chaudhary, S.N. Batchu, A. Shaylgaupour, and T.O. Jukar Overexpression of CYP2J2 provides protection against doxorubicin-induced cardiotoxicity Am. J. Physiol. Heart Circ. Physiol. 297 2009 H37 H46
168. + channels and p42/p44 MAPK pathways Circ. Res. 95 2004 506 514
169. M.L. Edin, Z. Wang, J.A. Bradbury, J.P. Graves, F.B. Lih, and L.M. DeGraff Endothelial expression of human CYP epoxygenase CYP2C8 increases susceptibility to ischemia-reperfusion injury in isolated mouse heart FASEB J. 25 2011 3436 3447