Epoxyeicosatrienoic acids and cardioprotection: The road to translation

Journal of Molecular and Cellular Cardiology

Volumn 74, Issue , 2014, Pages 199-208

  Oni Orisan, Akinyemi ^a,b   Alsaleh, Nasser ^d   Lee, Craig R ^a,b,c   Seubert, John M ^d  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b University of North Carolina   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Cardioprotection; Epoxyeicosatrienoic acid; Mitochondrial preservation; Myocardial ischemia reperfusion injury; Personalized medicine; Soluble epoxide hydrolase

Indexed keywords

CYTOCHROME P450; CYTOCHROME P450 EPOXYGENASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; EPOXYICOSATRIENOIC ACID; HYDROLASE INHIBITOR; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; SOLUBLE EPOXIDE HYDROLASE INHIBITOR; UNCLASSIFIED DRUG; CARDIOTONIC AGENT; EPOXIDE HYDROLASE; ICOSANOID;

ACUTE HEART INFARCTION; APOPTOSIS; CARDIOVASCULAR RISK; CELL SURVIVAL; CHRONIC DRUG ADMINISTRATION; COMORBIDITY; CORONARY ARTERY OCCLUSION; DRUG HALF LIFE; DRUG SOLUBILITY; ENDOTHELIUM CELL; GENETIC VARIABILITY; HEART FAILURE; HEART INFARCTION SIZE; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE FAILURE; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HEART RIGHT VENTRICLE INFARCTION; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; HUMAN; INTRACELLULAR SIGNALING; ISCHEMIC CARDIOMYOPATHY; NONHUMAN; NONISCHEMIC CARDIOMYOPATHY; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; RISK FACTOR; SMOOTH MUSCLE FIBER; STRUCTURE ACTIVITY RELATION; TREATMENT OUTCOME; CLINICAL TRIAL (TOPIC); DRUG EFFECTS; GENE EXPRESSION; GENETICS; HEART MUSCLE; METABOLISM; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; PATHOLOGY; PERSONALIZED MEDICINE; TRANSLATIONAL RESEARCH;

CARDIOTONIC AGENTS; CLINICAL TRIALS AS TOPIC; CYTOCHROME P-450 ENZYME SYSTEM; EICOSANOIDS; ENDOTHELIAL CELLS; EPOXIDE HYDROLASES; GENE EXPRESSION; HUMANS; INDIVIDUALIZED MEDICINE; MITOCHONDRIA, HEART; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; MYOCYTES, CARDIAC; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84904751780     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.05.016     Document Type: Review

References (116)

1. Canada PHAo 2009 tracking heart disease and stroke in Canada 2009, [Ottawa, ON]. Canada PHAo (Ed.).
2. Go A.S., Mozaffarian D., Roger V.L., Benjamin E.J., Berry J.D., Borden W.B., et al. Heart disease and stroke statistics-2013 update: a report from the American Heart Association. Circulation 2013, 127:e6-e245.
3. Davies M.J., Thomas A.C. Plaque fissuring-the cause of acute myocardial infarction, sudden ischaemic death, and crescendo angina. Br Heart J 1985, 53:363-373.
4. Yellon D.M., Hausenloy D.J. Myocardial reperfusion injury. N Engl J Med 2007, 357:1121-1135.
5. Imig J.D., Hammock B.D. Soluble epoxide hydrolase as a therapeutic target for cardiovascular diseases. Nat Rev Drug Discov 2009, 8:794-805.
6. Deng Y., Theken K.N., Lee C.R. Cytochrome p450 epoxygenases, soluble epoxide hydrolase, and the regulation of cardiovascular inflammation. J Mol Cell Cardiol 2010, 48:331-341.
7. Seubert J.M., Zeldin D.C., Nithipatikom K., Gross G.J. Role of epoxyeicosatrienoic acids in protecting the myocardium following ischemia/reperfusion injury. Prostaglandins Other Lipid Mediat 2007, 82:50-59.
8. Nithipatikom K., Gross G.J. Review article: epoxyeicosatrienoic acids: novel mediators of cardioprotection. J Cardiovasc Pharmacol Ther 2010, 15:112-119.
9. Imig J.D. Epoxides and soluble epoxide hydrolase in cardiovascular physiology. Physiol Rev 2012, 92:101-130.
10. Theken K.N., Lee C.R. Genetic variation in the cytochrome P450 epoxygenase pathway and cardiovascular disease risk. Pharmacogenomics 2007, 8:1369-1383.
11. Capdevila J.H., Falck J.R., Estabrook R.W. Cytochrome P450 and the arachidonate cascade. FASEB J 1992, 6:731-736.
12. Spector A.A., Fang X., Snyder G.D., Weintraub N.L. Epoxyeicosatrienoic acids (EETs): metabolism and biochemical function. Prog Lipid Res 2004, 43:55-90.
13. Wu S., Moomaw C.R., Tomer K.B., Falck J.R., Zeldin D.C. Molecular cloning and expression of CYP2J2, a human cytochrome P450 arachidonic acid epoxygenase highly expressed in heart. J Biol Chem 1996, 271:3460-3468.
14. DeLozier T.C., Kissling G.E., Coulter S.J., Dai D., Foley J.F., Bradbury J.A., et al. Detection of human CYP2C8, CYP2C9, and CYP2J2 in cardiovascular tissues. Drug Metab Dispos 2007, 35:682-688.
15. Larsson C., White I., Johansson C., Stark A., Meijer J. Localization of the human soluble epoxide hydrolase gene (EPHX2) to chromosomal region 8p21-p12. Hum Genet 1995, 95:356-358.
16. Enayetallah A.E., French R.A., Thibodeau M.S., Grant D.F. Distribution of soluble epoxide hydrolase and of cytochrome P450 2C8, 2C9, and 2J2 in human tissues. J Histochem Cytochem 2004, 52:447-454.
17. Gross G.J., Falck J.R., Gross E.R., Isbell M., Moore J., Nithipatikom K. Cytochrome P450 and arachidonic acid metabolites: role in myocardial ischemia/reperfusion injury revisited. Cardiovasc Res 2005, 68:18-25.
18. Poeckel D., Funk C.D. The 5-lipoxygenase/leukotriene pathway in preclinical models of cardiovascular disease. Cardiovasc Res 2010, 86:243-253.
19. Yuhki K., Kojima F., Kashiwagi H., Kawabe J., Fujino T., Narumiya S., et al. Roles of prostanoids in the pathogenesis of cardiovascular diseases: novel insights from knockout mouse studies. Pharmacol Ther 2011, 129:195-205.
20. Baum S.J., Kris-Etherton P.M., Willett W.C., Lichtenstein A.H., Rudel L.L., Maki K.C., et al. Fatty acids in cardiovascular health and disease: a comprehensive update. J Clin Lipidol 2012, 6:216-234.
21. Shen H.C., Hammock B.D. Discovery of inhibitors of soluble epoxide hydrolase: a target with multiple potential therapeutic indications. J Med Chem 2011, 55:1789-1808.
22. Arnold C., Markovic M., Blossey K., Wallukat G., Fischer R., Dechend R., et al. Arachidonic acid-metabolizing cytochrome P450 enzymes are targets of {omega}-3 fatty acids. J Biol Chem 2010, 285:32720-32733.
23. Imig J.D., Elmarakby A., Nithipatikom K., Wei S., Capdevila J.H., Tuniki V.R., et al. Development of epoxyeicosatrienoic acid analogs with in vivo anti-hypertensive actions. Front Physiol 2010, 1:157.
24. Gauthier K.M., Deeter C., Krishna U.M., Reddy Y.K., Bondlela M., Falck J.R., et al. 14,15-Epoxyeicosa-5(Z)-enoic acid: a selective epoxyeicosatrienoic acid antagonist that inhibits endothelium-dependent hyperpolarization and relaxation in coronary arteries. Circ Res 2002, 90:1028-1036.
25. Oni-Orisan A., Deng Y., Schuck R.N., Theken K.N., Edin M.L., Lih F.B., et al. Dual modulation of cyclooxygenase and CYP epoxygenase metabolism and acute vascular inflammation in mice. Prostaglandins Other Lipid Mediat 2013, 104-105:67-73.
26. Batchu S.N., Law E., Brocks D.R., Falck J.R., Seubert J.M. Epoxyeicosatrienoic acid prevents postischemic electrocardiogram abnormalities in an isolated heart model. J Mol Cell Cardiol 2009, 46:67-74.
27. Liu Y., Dang H.X., Li D., Pang W., Hammock B.D., Zhu Y. Inhibition of soluble epoxide hydrolase attenuates high-fat-diet-induced hepatic steatosis by reduced systemic inflammatory status in mice. PLoS ONE 2012, 7.
28. Ferdinandy P., Schulz R., Baxter G.F. Interaction of cardiovascular risk factors with myocardial ischemia/reperfusion injury, preconditioning, and postconditioning. Pharmacol Rev 2007, 59:418-458.
29. Hausenloy D.J., Yellon D.M. New directions for protecting the heart against ischaemia-reperfusion injury: targeting the Reperfusion Injury Salvage Kinase (RISK)-pathway. Cardiovasc Res 2004, 61:448-460.
30. + channels and p42/p44 MAPK pathway. Circ Res 2004, 95:506-514.
31. Seubert J.M., Sinal C.J., Graves J., DeGraff L.M., Bradbury J.A., Lee C.R., et al. Role of soluble epoxide hydrolase in postischemic recovery of heart contractile function. Circ Res 2006, 99:442-450.
32. Nithipatikom K., Moore J.M., Isbell M.A., Falck J.R., Gross G.J. Epoxyeicosatrienoic acids in cardioprotection: ischemic versus reperfusion injury. Am J Physiol Heart Circ Physiol 2006, 291:H537-H542.
33. Gross G.J., Gauthier K.M., Moore J., Falck J.R., Hammock B.D., Campbell W.B., et al. Effects of the selective EET antagonist, 14,15-EEZE, on cardioprotection produced by exogenous or endogenous EETs in the canine heart. Am J Physiol Heart Circ Physiol 2008, 294:H2838-H2844.
34. Gross G.J., Hsu A., Falck J.R., Nithipatikom K. Mechanisms by which epoxyeicosatrienoic acids (EETs) elicit cardioprotection in rat hearts. J Mol Cell Cardiol 2007, 42:687-691.
35. Gross G.J., Hsu A., Pfeiffer A.W., Nithipatikom K. Roles of endothelial nitric oxide synthase (eNOS) and mitochondrial permeability transition pore (mPTP) in epoxyeicosatrienoic acid (EET)-induced cardioprotection against infarction in intact rat hearts. J Mol Cell Cardiol 2013, 59:20-29.
36. Batchu S.N., Lee S.B., Qadhi R.S., Chaudhary K.R., El-Sikhry H., Kodela R., et al. Cardioprotective effect of a dual acting epoxyeicosatrienoic acid analogue towards ischaemia reperfusion injury. Br J Pharmacol 2011, 162:897-907.
37. Batchu S.N., Chaudhary K.R., El-Sikhry H., Yang W., Light P.E., Oudit G.Y., et al. Role of PI3Kα and sarcolemmal ATP-sensitive potassium channels in epoxyeicosatrienoic acid mediated cardioprotection. J Mol Cell Cardiol 2012, 53:43-52.
38. Bodiga S., Zhang R., Jacobs D.E., Larsen B.T., Tampo A., Manthati V.L., et al. Protective actions of epoxyeicosatrienoic acid: dual targeting of cardiovascular PI3K and KATP channels. J Mol Cell Cardiol 2009, 46:978-988.
39. Wu S., Chen W., Murphy E., Gabel S., Tomer K.B., Foley J., et al. Molecular cloning, expression, and functional significance of a cytochrome P450 highly expressed in rat heart myocytes. J Biol Chem 1997, 272:12551-12559.
40. Merkel M.J., Liu L., Cao Z., Packwood W., Young J., Alkayed N.J., et al. Inhibition of soluble epoxide hydrolase preserves cardiomyocytes: role of STAT3 signaling. Am J Physiol Heart Circ Physiol 2010, 298:H679-H687.
41. Chaudhary K.R., Batchu S.N., Das D., Suresh M.R., Falck J.R., Graves J.P., et al. Role of B-type natriuretic peptide in epoxyeicosatrienoic acid-mediated improved post-ischaemic recovery of heart contractile function. Cardiovasc Res 2009, 83:362-370.
42. Gross G.J., Baker J.E., Hsu A., Wu H.-e., Falck J.R., Nithipatikom K. Evidence for a role of opioids in epoxyeicosatrienoic acid-induced cardioprotection in rat hearts. Am J Physiol Heart Circ Physiol 2010, 298:H2201-H2207.
43. Machado N.G., Alves M.G., Carvalho R.A., Oliveira P.J. Mitochondrial involvement in cardiac apoptosis during ischemia and reperfusion: can we close the box?. Cardiovasc Toxicol 2009, 9:211-227.
44. Dhanasekaran A., Gruenloh S.K., Buonaccorsi J.N., Zhang R., Gross G.J., Falck J.R., et al. Multiple antiapoptotic targets of the PI3K/Akt survival pathway are activated by epoxyeicosatrienoic acids to protect cardiomyocytes from hypoxia/anoxia. Am J Physiol Heart Circ Physiol 2008, 294:H724-H735.
45. Solaini G., Harris D.A. Biochemical dysfunction in heart mitochondria exposed to ischaemia and reperfusion. Biochem J 2005, 390:377-394.
46. Halestrap A.P., Clarke S.J., Javadov S.A. Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc Res 2004, 61:372-385.
47. Miura T., Tanno M. The mPTP and its regulatory proteins: final common targets of signalling pathways for protection against necrosis. Cardiovasc Res 2012, 94:181-189.
48. Katragadda D., Batchu S.N., Cho W.J., Chaudhary K.R., Falck J.R., Seubert J.M. Epoxyeicosatrienoic acids limit damage to mitochondrial function following stress in cardiac cells. J Mol Cell Cardiol 2009, 46:867-875.
49. Batchu S.N., Lee S.B., Samokhvalov V., Chaudhary K.R., El-Sikhry H., Weldon S.M., et al. Novel soluble epoxide hydrolase inhibitor protects mitochondrial function following stress. Can J Physiol Pharmacol 2012, 90:811-823.
50. Samokhvalov V., Alsaleh N., El-Sikhry H.E., Jamieson K.L., Chen C.B., Lopaschuk D.G., et al. Epoxyeicosatrienoic acids protect cardiac cells during starvation by modulating an autophagic response. Cell Death Dis 2013, 4:e885.
51. Chaudhary K.R., Cho W.J., Yang F., Samokhvalov V., El-Sikhry H.E., Daniel E.E., et al. Effect of ischemia reperfusion injury and epoxyeicosatrienoic acids on caveolin expression in mouse myocardium. J Cardiovasc Pharmacol 2013, 61:258-263.
52. + channels. Microcirculation 2008, 15:137-150.
53. Wang D., Dubois R.N. Epoxyeicosatrienoic acids: a double-edged sword in cardiovascular diseases and cancer. J Clin Invest 2012, 122:19-22.
54. van Nieuwenhoven F.A., Turner N.A. The role of cardiac fibroblasts in the transition from inflammation to fibrosis following myocardial infarction. Vascul Pharmacol 2013, 58:182-188.
55. Sutton M.G., Sharpe N. Left ventricular remodeling after myocardial infarction: pathophysiology and therapy. Circulation 2000, 101:2981-2988.
56. Mehta D., Curwin J., Gomes J.A., Fuster V. Sudden death in coronary artery disease: acute ischemia versus myocardial substrate. Circulation 1997, 96:3215-3223.
57. Carrabba N., Parodi G., Valenti R., Migliorini A., Bellandi B., Antoniucci D. Prognostic value of reverse left ventricular remodeling after primary angioplasty for STEMI. Atherosclerosis 2012, 222:123-128.
58. Li N., Liu J.Y., Timofeyev V., Qiu H., Hwang S.H., Tuteja D., et al. Beneficial effects of soluble epoxide hydrolase inhibitors in myocardial infarction model: insight gained using metabolomic approaches. J Mol Cell Cardiol 2009, 47:835-845.
59. Kompa A.R., Wang B.H., Xu G., Zhang Y., Ho P.-Y., Eisennagel S., et al. Soluble epoxide hydrolase inhibition exerts beneficial anti-remodeling actions post-myocardial infarction. Int J Cardiol 2013, 167:210-219.
60. Merabet N., Bellien J., Glevarec E., Nicol L., Lucas D., Remy-Jouet I., et al. Soluble epoxide hydrolase inhibition improves myocardial perfusion and function in experimental heart failure. J Mol Cell Cardiol 2012, 52:660-666.
61. Sirish P., Li N., Liu J.-Y., Lee K.S.S., Hwang S.H., Qiu H., et al. 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 2013, 110:5618-5623.
62. Dec G.W., Fuster V. Idiopathic dilated cardiomyopathy. N Engl J Med 1994, 331:1564-1575.
63. Xu D., Li N., He Y., Timofeyev V., Lu L., Tsai H.-J., et al. Prevention and reversal of cardiac hypertrophy by soluble epoxide hydrolase inhibitors. Proc Natl Acad Sci U S A 2006, 103:18733-18738.
64. Ai D., Pang W., Li N., Xu M., Jones P.D., Yang J., et al. Soluble epoxide hydrolase plays an essential role in angiotensin II-induced cardiac hypertrophy. Proc Natl Acad Sci U S A 2009, 106:564-569.
65. Zhao G., Wang J., Xu X., Jing Y., Tu L., Li X., et al. Epoxyeicosatrienoic acids protect rat hearts against tumor necrosis factor-alpha-induced injury. J Lipid Res 2012, 53:456-466.
66. Westphal C., Spallek B., Konkel A., Marko L., Qadri F., DeGraff L.M., et al. CYP2J2 overexpression protects against arrhythmia susceptibility in cardiac hypertrophy. PLoS ONE 2013, 8:e73490.
67. Monti J., Fischer J., Paskas S., Heinig M., Schulz H., Gosele C., et al. Soluble epoxide hydrolase is a susceptibility factor for heart failure in a rat model of human disease. Nat Genet 2008, 40:529-537.
68. Souders C.A., Bowers S.L.K., Baudino T.A. Cardiac fibroblast: the renaissance cell. Circ Res 2009, 105:1164-1176.
69. Fang X., Kaduce T.L., Weintraub N.L., Harmon S., Teesch L.M., Morisseau C., et al. Pathways of epoxyeicosatrienoic acid metabolism in endothelial cells. J Biol Chem 2001, 276:14867-14874.
70. Ai D., Fu Y., Guo D., Tanaka H., Wang N., Tang C., et al. Angiotensin II up-regulates soluble epoxide hydrolase in vascular endothelium in vitro and in vivo. Proc Natl Acad Sci U S A 2007, 104:9018-9023.
71. Edin M.L., Wang Z., Bradbury J.A., Graves J.P., Lih F.B., DeGraff L.M., et al. Endothelial expression of human cytochrome p450 epoxygenase CYP2C8 increases susceptibility to ischemia-reperfusion injury in isolated mouse heart. FASEB J 2011, 25:3436-3447.
72. Quyyumi A.A., Ozkor M. Vasodilation by hyperpolarization beyond NO. Hypertension 2006, 48:1023-1025.
73. + channels in coronary smooth muscle through a guanine nucleotide binding protein. Circ Res 1997, 80:877-884.
74. Oltman C.L., Weintraub N.L., VanRollins M., Dellsperger K.C. Epoxyeicosatrienoic acids and dihydroxyeicosatrienoic acids are potent vasodilators in the canine coronary microcirculation. Circ Res 1998, 83:932-939.
75. Pozzi A., Zent R. Regulation of endothelial cell functions by basement membrane- and arachidonic acid-derived products. Wiley Interdiscip Rev Syst Biol Med 2009, 1:254-272.
76. Chung N.A., Lydakis C., Belgore F., Blann A.D., Lip G.Y. Angiogenesis in myocardial infarction. An acute or chronic process?. Eur Heart J 2002, 23:1604-1608.
77. Xu D.-y., Davis B.B., Wang Z.-h., Zhao S.-p., Wasti B., Liu Z.-l., et al. A potent soluble epoxide hydrolase inhibitor, t-AUCB, acts through PPARγ to modulate the function of endothelial progenitor cells from patients with acute myocardial infarction. Int J Cardiol 2013, 167:1298-1304.
78. Kania G., Blyszczuk P., Eriksson U. Mechanisms of cardiac fibrosis in inflammatory heart disease. Trends Cardiovasc Med 2009, 19:247-252.
79. Deng Y., Edin M.L., Theken K.N., Schuck R.N., Flake G.P., Kannon M.A., et al. Endothelial CYP epoxygenase overexpression and soluble epoxide hydrolase disruption attenuate acute vascular inflammatory responses in mice. FASEB J 2011, 25:703-713.
80. Spiecker M., Darius H., Hankeln T., Soufi M., Sattler A.M., Schaefer J.R., et al. Risk of coronary artery disease associated with polymorphism of the cytochrome P450 epoxygenase CYP2J2. Circulation 2004, 110:2132-2136.
81. Liu P.-Y., Li Y.-H., Chao T.-H., Wu H.-L., Lin L.-J., Tsai L.-M., et al. Synergistic effect of cytochrome P450 epoxygenase CYP2J2*7 polymorphism with smoking on the onset of premature myocardial infarction. Atherosclerosis 2007, 195:199-206.
82. Lee C.R., North K.E., Bray M.S., Couper D.J., Heiss G., Zeldin D.C. CYP2J2 and CYP2C8 polymorphisms and coronary heart disease risk: the atherosclerosis risk in communities (ARIC) study. Pharmacogenet Genomics 2007, 17:349-358.
83. Yasar U., Bennet A.M., Eliasson E., Lundgren S., Wiman B., De Faire U., et al. Allelic variants of cytochromes P450 2C modify the risk for acute myocardial infarction. Pharmacogenetics 2003, 13:715-720.
84. Lee C.R., North K.E., Bray M.S., Fornage M., Seubert J.M., Newman J.W., et al. Genetic variation in soluble epoxide hydrolase (EPHX2) and risk of coronary heart disease: the atherosclerosis risk in communities (ARIC) study. Hum Mol Genet 2006, 15:1640-1649.
85. Fornage M., Lee C.R., Doris P.A., Bray M.S., Heiss G., Zeldin D.C., et al. The soluble epoxide hydrolase gene harbors sequence variation associated with susceptibility to and protection from incident ischemic stroke. Hum Mol Genet 2005, 14:2829-2837.
86. Fornage M., Boerwinkle E., Doris P.A., Jacobs D., Liu K., Wong N.D. Polymorphism of the soluble epoxide hydrolase is associated with coronary artery calcification in African-American subjects. Circulation 2004, 109:335-339.
87. Wei Q., Doris P.A., Pollizotto M.V., Boerwinkle E., Jacobs D.R., Siscovick D.S., et al. Sequence variation in the soluble epoxide hydrolase gene and subclinical coronary atherosclerosis: interaction with cigarette smoking. Atherosclerosis 2007, 190:26-34.
88. Lee C.R., Pretorius M., Schuck R.N., Burch L.H., Bartlett J., Williams S.M., et al. Genetic variation in soluble epoxide hydrolase (EPHX2) is associated with forearm vasodilator responses in humans. Hypertension 2011, 57:116-122.
89. Fava C., Montagnana M., Danese E., Almgren P., Hedblad B., Engstrom G., et al. Homozygosity for the EPHX2 K55R polymorphism increases the long-term risk of ischemic stroke in men: a study in Swedes. Pharmacogenet Genomics 2010, 20:94-103.
90. Theken K.N., Schuck R.N., Edin M.L., Tran B., Ellis K., Bass A., et al. Evaluation of cytochrome P450-derived eicosanoids in humans with stable atherosclerotic cardiovascular disease. Atherosclerosis 2012, 222:530-536.
91. Schuck R.N., Theken K.N., Edin M.L., Caughey M., Bass A., Ellis K., et al. Cytochrome P450-derived eicosanoids and vascular dysfunction in coronary artery disease patients. Atherosclerosis 2013, 227:442-448.
92. Lefer D.J., Bolli R. Development of an NIH consortium for preclinical assessment of cardioprotective therapies (CAESAR): a paradigm shift in studies of infarct size limitation. J Cardiovasc Pharmacol Ther 2011, 16:332-339.
93. Khan M.A., Liu J., Kumar G., Skapek S.X., Falck J.R., Imig J.D. Novel orally active epoxyeicosatrienoic acid (EET) analogs attenuate cisplatin nephrotoxicity. FASEB J 2013, 27:2946-2956.
94. Hye Khan M.A., Neckar J., Manthati V., Errabelli R., Pavlov T.S., Staruschenko A., et al. Orally active epoxyeicosatrienoic acid analog attenuates kidney injury in hypertensive Dahl salt-sensitive rat. Hypertension 2013, 62:905-913.
95. Liu J.Y., Lin Y.P., Qiu H., Morisseau C., Rose T.E., Hwang S.H., et al. Substituted phenyl groups improve the pharmacokinetic profile and anti-inflammatory effect of urea-based soluble epoxide hydrolase inhibitors in murine models. Eur J Pharm Sci 2013, 48:619-627.
96. Hutchens M.P., Nakano T., Dunlap J., Traystman R.J., Hurn P.D., Alkayed N.J. Soluble epoxide hydrolase gene deletion reduces survival after cardiac arrest and cardiopulmonary resuscitation. Resuscitation 2008, 76:89-94.
97. Loot A.E., Fleming I. Cytochrome P450-derived epoxyeicosatrienoic acids and pulmonary hypertension: central role of transient receptor potential C6 channels. J Cardiovasc Pharmacol 2011, 57:140-147.
98. Keseru B., Barbosa-Sicard E., Popp R., Fisslthaler B., Dietrich A., Gudermann T., et al. Epoxyeicosatrienoic acids and the soluble epoxide hydrolase are determinants of pulmonary artery pressure and the acute hypoxic pulmonary vasoconstrictor response. FASEB J 2008, 22:4306-4315.
99. Keseru B., Barbosa-Sicard E., Schermuly R.T., Tanaka H., Hammock B.D., Weissmann N., et al. Hypoxia-induced pulmonary hypertension: comparison of soluble epoxide hydrolase deletion vs. inhibition. Cardiovasc Res 2010, 85:232-240.
100. Krotz F., Riexinger T., Buerkle M.A., Nithipatikom K., Gloe T., Sohn H.Y., et al. Membrane-potential-dependent inhibition of platelet adhesion to endothelial cells by epoxyeicosatrienoic acids. Arterioscler Thromb Vasc Biol 2004, 24:595-600.
101. Krotz F., Hellwig N., Burkle M.A., Lehrer S., Riexinger T., Mannell H., et al. A sulfaphenazole-sensitive EDHF opposes platelet-endothelium interactions in vitro and in the hamster microcirculation in vivo. Cardiovasc Res 2010, 85:542-550.
102. Heizer M.L., McKinney J.S., Ellis E.F. 14,15-Epoxyeicosatrienoic acid inhibits platelet aggregation in mouse cerebral arterioles. Stroke 1991, 22:1389-1393.
103. O'Gara P.T., Kushner F.G., Ascheim D.D., Casey D.E., Chung M.K., de Lemos J.A., et al. 2013 ACCF/AHA guideline for the management of ST-elevation myocardial infarction: executive summary: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. Circulation 2013, 127:529-555.
104. Writing Committee M., Jneid H., Anderson J.L., Wright R.S., Adams C.D., Bridges C.R., et al. 2012 ACCF/AHA focused update of the guideline for the management of patients with unstable angina/non-ST-elevation myocardial infarction (updating the 2007 guideline and replacing the 2011 focused update): a report of the American College of Cardiology Foundation/American Heart Association Task Force on practice guidelines. Circulation 2012, 126:875-910.
105. Jung F., Schulz C., Blaschke F., Muller D.N., Mrowietz C., Franke R.P., et al. Effect of cytochrome P450-dependent epoxyeicosanoids on Ristocetin-induced thrombocyte aggregation. Clin Hemorheol Microcirc 2012, 52:403-416.
106. Panigrahy D., Edin M.L., Lee C.R., Huang S., Bielenberg D.R., Butterfield C.E., et al. Epoxyeicosanoids stimulate multiorgan metastasis and tumor dormancy escape in mice. J Clin Invest 2012, 122:178-191.
107. Panigrahy D., Greene E.R., Pozzi A., Wang D.W., Zeldin D.C. EET signaling in cancer. Cancer Metastasis Rev 2011, 30:525-540.
108. Panigrahy D., Kalish B.T., Huang S., Bielenberg D.R., Le H.D., Yang J., et al. Epoxyeicosanoids promote organ and tissue regeneration. Proc Natl Acad Sci U S A 2013, 110:13528-13533.
109. Kalish B.T., Kieran M.W., Puder M., Panigrahy D. The growing role of eicosanoids in tissue regeneration, repair, and wound healing. Prostaglandins Other Lipid Mediat 2013, 104:130-138.
110. Zhang G., Panigrahy D., Mahakian L.M., Yang J., Liu J.Y., Stephen Lee K.S., et al. Epoxy metabolites of docosahexaenoic acid (DHA) inhibit angiogenesis, tumor growth, and metastasis. Proc Natl Acad Sci U S A 2013, 110:6530-6535.
111. Hwang S.H., Wecksler A.T., Zhang G., Morisseau C., Nguyen L.V., Fu S.H., et al. Synthesis and biological evaluation of sorafenib- and regorafenib-like sEH inhibitors. Bioorg Med Chem Lett 2013, 23:3732-3737.
112. Falck J.R., Kodela R., Manne R., Atcha K.R., Puli N., Dubasi N., et al. 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 2009, 52:5069-5075.
113. Mitra R., Guo Z., Milani M., Mesaros C., Rodriguez M., Nguyen J., et al. CYP3A4 mediates growth of estrogen receptor-positive breast cancer cells in part by inducing nuclear translocation of phospho-Stat3 through biosynthesis of (+/-)-14,15-epoxyeicosatrienoic acid (EET). J Biol Chem 2011, 286:17543-17559.
114. Chaudhary K.R., Zordoky B.N.M., Edin M.L., Alsaleh N., El-Kadi A.O.S., Zeldin D.C., et al. Differential effects of soluble epoxide hydrolase inhibition and CYP2J2 overexpression on postischemic cardiac function in aged mice. Prostaglandins Other Lipid Mediat 2013, 104-105:8-17.
115. Zhu P., Peck B., Licea-Perez H., Callahan J.F., Booth-Genthe C. Development of a semi-automated LC/MS/MS method for the simultaneous quantitation of 14,15-epoxyeicosatrienoic acid, 14,15-dihydroxyeicosatrienoic acid, leukotoxin and leukotoxin diol in human plasma as biomarkers of soluble epoxide hydrolase activity in vivo. J Chromatogr B Analyt Technol Biomed Life Sci 2011, 879:2487-2493.
116. Chaudhary K.R., Abukhashim M., Hwang S.H., Hammock B.D., Seubert J.M. Inhibition of soluble epoxide hydrolase by trans-4-[4-(3-adamantan-1-yl-ureido)-cyclohexyloxy]-benzoic acid is protective against ischemia-reperfusion injury. J Cardiovasc Pharmacol 2010, 55:67-73.