Diabetic CVD - soluble epoxide hydrolase as a target

Cardiovascular and Hematological Agents in Medicinal Chemistry

Volumn 10, Issue 3, 2012, Pages 212-222

  Lorthioir, Aurelien ^a   Guerrot, Dominique ^a   Joannides, Robinson ^a,b,c   Bellien, Jeremy ^a,b,c  

^a ROUEN UNIVERSITY HOSPITAL   (France)

^b Université Normandie de Rouen   (France)

^c UNIVERSITY OF ROUEN   (France)

Author keywords

Antihypertensive agent; Cardiovascular diseases; Cytochrome P450 epoxygenase; Diabetes; Endothelium; Epoxyeicosatrienoic acids; Insulin release; Insulin resistance; Soluble epoxide hydrolase; Vasodilatation

Indexed keywords

ANTIDIABETIC AGENT; CARDIOVASCULAR AGENT; CYTOCHROME P450; ENZYME INHIBITOR; EPOXIDE HYDROLASE; EPOXYICOSATRIENOIC ACID; GLUCOSE; ICOSANOID; SOLUBLE EPOXIDE HYDROLASE INHIBITOR; UNCLASSIFIED DRUG;

BIOAVAILABILITY; DIABETIC CARDIOMYOPATHY; DIABETIC PATIENT; DISEASE ASSOCIATION; DISEASE COURSE; DRUG EFFECT; ENDOTHELIAL DYSFUNCTION; ENZYME SYNTHESIS; GLUCOSE BLOOD LEVEL; HUMAN; INSULIN RELEASE; INSULIN SENSITIVITY; METABOLIC DISORDER; MORBIDITY; NONHUMAN; PANCREAS ISLET; PATHOPHYSIOLOGY; REVIEW; RISK FACTOR; VASCULAR ENDOTHELIUM; VASODILATATION;

EID: 84864530745     PISSN: 18715257     EISSN: 18756182     Source Type: Journal    
DOI: 10.2174/187152512802651042     Document Type: Review

References (92)

1. Nelson, S.E. Management of patients with type 2 diabetes. Cur. Med. Res. Opin., 2011, 27(10), 1931-1947.
2. Wild, S.; Roglic, G.; Green, A.; Sicree, R.; King, H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care, 2004, 27(5), 1047-1053.
3. Booth, G.L.; Kapral, M.K.; Fung, K.; Tu, J.V. Relation between age and cardiovascular disease in men and women with diabetes compared with non-diabetic people: a population-based retrospective cohort study. Lancet, 2006, 368(9529), 29-36.
4. Molyneaux, L.M.; Constantino, M.I.; McGill, M.; Zilkens, R.; Yue, D.K. Better glycaemic control and risk reduction of diabetic complications in Type 2 diabetes: comparison with the DCCT. Diabetes Res. Clin. Pract., 1998, 42(2), 77-83.
5. Boussageon, R.; Bejan-Angoulvant, T.; Saadatian-Elahi, M.; Lafont, S.; Bergeonneau, C.; Kassaï, B.; Erpeldinger, S.; Wright, J.M.; Gueyffier, F.; Cornu, C. Effect of intensive glucose lowering treatment on all cause mortality, cardiovascular death, and microvascular events in type 2 diabetes: meta-analysis of randomised controlled trials. BMJ, 2011, 343, d4169.
6. Gaede, P.; Vedel, P.; Larsen, N.; Jensen, G.V.; Parving, H.H.; Pedersen, O. Multifactorial intervention and cardiovascular disease in patients with type 2 diabetes. N. Engl. J. Med., 2003, 348(5), 383-393.
7. Griffin, S.J.; Borch-Johnsen, K.; Davies, M.J.; Khunti, K.; Rutten, G.E.; Sandbæk, A.; Sharp, S.J.; Simmons, R.K.; van den Donk, M.; Wareham, N.J.; Lauritzen, T. Effect of early intensive multifactorial therapy on 5-year cardiovascular outcomes in individuals with type 2 diabetes detected by screening (ADDITIONEurope): a cluster-randomised trial. Lancet, 2011, 378(9786), 156-167.
8. Joannides, R.; Bellien, J.; Thuillez C. Clinical methods for the evaluation of endothelial function--a focus on resistance arteries. Fundam. Clin. Pharmacol., 2006, 20(3), 311-320.
9. Bellien, J.; Joannides, R.; Richard, V.; Thuillez, C. Modulation of cytochrome-derived epoxyeicosatrienoic acids pathway: a promising pharmacological approach to prevent endothelial dysfunction in cardiovascular diseases? Pharmacol. Ther., 2011, 131(1), 1-17.
10. Zenere, B.M.; Arcaro, G.; Saggiani, F.; Rossi, L.; Muggeo, M.; Lechi, A. Noninvasive detection of functional alterations of the arterial wall in IDDM patients with and without microalbuminuria. Diabetes Care, 1995, 18(7), 975-982.
11. McVeigh, G.E.; Brennan, G.M.; Johnston, G.D.; McDermott, B.J.; McGrath, L.T.; Henry, W.R.; Andrews, J.W.; Hayes, J.R. Impaired endothelium-dependent and independent vasodilation in patients with type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia, 1992, 35(8), 771-776.
12. Steinberg, H.O.; Chaker, H.; Leaming, R.; Johnson, A.; Brechtel, G.; Baron, A.D. Obesity/insulin resistance is associated with endothelial dysfunction. Implications for the syndrome of insulin resistance. J. Clin. Invest., 1996, 97(11), 2601-2610.
13. Rossi, R.; Cioni, E.; Nuzzo, A.; Origliani, G.; Modena, M.G. Endothelial-dependent vasodilation and incidence of type 2 diabetes in a population of healthy postmenopausal women. Diabetes Care, 2005, 28(3), 702-707.
14. Nitenberg, A.; Valensi, P.; Sachs, R.; Cosson, E.; Attali, J.R.; Antony, I. Prognostic value of epicardial coronary artery constriction to the cold pressor test in type 2 diabetic patients with angiographically normal coronary arteries and no other major coronary risk factors. Diabetes Care, 2004, 27(1), 208-215.
15. Hamilton, S.J.; Chew, G.T.; Davis, T.M.; Watts, G.F. Prevalence and predictors of abnormal arterial function in statin-treated type 2 diabetes mellitus patients. Metabolism, 2012, 61(3), 349-35.
16. Xu, J.; Zou, M.H. Molecular insights and therapeutic targets for diabetic endothelial dysfunction. Circulation, 2009, 120(13), 1266-1286.
17. Ding, H.; Triggle, C.R. Endothelial dysfunction in diabetes: multiple targets for treatment. Pflugers Arch., 2010, 459(6), 977-994.
18. Giacco, F.; Brownlee, M. Oxidative stress and diabetic complications. Circ. Res., 2010, 107(9), 1058-1070.
19. Fitzgerald, S.M.; Kemp-Harper, B.K.; Tare, M.; Parkington, H.C. Role of endothelium-derived hyperpolarizing factor in endothelial dysfunction during diabetes. Clin. Exp. Pharmacol. Physiol., 2005, 32(5-6), 482-487.
20. Gao, X.; Martinez-Lemus, L.A.; Zhang, C. Endothelium-derived hyperpolarizing factor and diabetes. World J. Cardiol., 2011, 3(1), 25-31.
21. Bellien, J.; Thuillez, C.; Joannides R. Contribution of endotheliumderived hyperpolarizing factors to the regulation of vascular tone in humans. Fundam. Clin. Pharmacol., 2008, 22(4), 363-377.
22. Archer, S.L.; Gragasin, F.S.; Wu, X.; Wang, S.; McMurtry, S.; Kim, D.H.; Platonov, M.; Koshal, A.; Hashimoto, K.; Campbell, W.B.; Falck, J.R.; Michelakis, E.D. SourceVascular Biology Group. Endothelium-derived hyperpolarizing factor in human internal mammary artery is 11,12-epoxyeicosatrienoic acid and causes relaxation by activating smooth muscle BK(Ca) channels. Circulation, 2003, 107(5), 769-776.
23. Huang, A.; Sun, D.; Jacobson, A.; Carroll, M.A.; Falck, J.R.; Kaley, G. Epoxyeicosatrienoic acids are released to mediate shear stress-dependent hyperpolarization of arteriolar smooth muscle. Circ. Res., 2005, 96(3), 376-383.
24. Halcox, J.P.; Narayanan, S.; Cramer-Joyce, L.; Mincemoyer, R.; Quyyumi, A.A. Characterization of endothelium-derived hyperpolarizing factor in the human forearm microcirculation. Am. J. Physiol. Heart Circ. Physiol., 2001, 280(6), H2470-H2477.
25. Hillig, T.; Krustrup, P.; Fleming, I.; Osada, T.; Saltin, B.; Hellsten, Y. Cytochrome P450 2C9 plays an important role in the regulation of exercise-induced skeletal muscle blood flow and oxygen uptake in humans. J. Physiol., 2003, 546(Pt. 1), 307-314.
26. Taddei, S.; Versari, D.; Cipriano, A.; Ghiadoni, L.; Galetta, F.; Franzoni, F.; Magagna, A.; Virdis, A.; Salvetti, A. Identification of a cytochrome P450 2C9-derived endothelium-derived hyperpolarizing factor in essential hypertensive patients. J. Am. Coll. Cardiol., 2006, 48(3), 508-515.
27. Passauer, J.; Büssemaker, E.; Lässig, G.; Pistrosch, F.; Fauler, J.; Gross, P.; Fleming, I. Baseline blood flow and bradykinin-induced vasodilator responses in the human forearm are insensitive to the cytochrome P450 2C9 (CYP2C9) inhibitor sulphaphenazole. Clin. Sci. (Lond.), 2003, 105(4), 513-518.
28. Fichtlscherer, S.; Dimmeler, S.; Breuer, S.; Busse, R.; Zeiher, A.M.; Fleming, I. Inhibition of cytochrome P450 2C9 improves endothelium-dependent, nitric oxide-mediated vasodilatation in patients with coronary artery disease. Circulation, 2004, 109(2), 178-183.
29. Miura, H.; Wachtel, R.E.; Liu, Y.; Loberiza, F.R. Jr.; Saito, T.; Miura, M.; Gutterman, D.D. Flow-induced dilation of human coronary arterioles: important role of Ca(2+)-activated K(+) channels. Circulation, 2001, 103(15), 1992-1998.
30. Bellien, J.; Joannides, R.; Iacob, M.; Arnaud, P.; Thuillez, C. Evidence for a basal release of a cytochrome-related endotheliumderived hyperpolarizing factor in the radial artery in humans. Am. J. Physiol. Heart Circ. Physiol., 2006, 290(4), H1347-H1352.
31. Bellien, J.; Iacob, M.; Gutierrez, L.; Isabelle, M.; Lahary, A.; Thuillez, C.; Joannides, R. Crucial role of NO and endotheliumderived hyperpolarizing factor in human sustained conduit artery flow-mediated dilatation. Hypertension, 2006, 48(6), 1088-1094.
32. Bellien, J.; Iacob, M.; Remy-Jouet, I.; Lucas, D.; Monteil, C.; Gutierrez L.; Mercier A.; Thuillez, C.; Joannides R. Epoxyeicosatrienoic acids contribute with altered NO and endothelin-1 pathways to conduit artery endothelial dysfunction in essential hypertension. Circulation, 2012, 125(10), 1266-1275.
33. Node, K.; Huo, Y.; Ruan, X.; Yang, B.; Spiecker, M.; Ley K.; Zeldin, D.C.; Liao, J.K. Anti-inflammatory properties of cytochrome P450 epoxygenase-derived eicosanoids. Science, 1999, 285(5431), 1276-1279.
34. Liu, Y.; Zhang, Y.; Schmelzer, K.; Lee, T.S.; Fang, X.; Zhu, Y.; Spector, A.A.; Gill, S.; Morisseau, C.; Hammock, B.D.; Shyy, J.Y. The antiinflammatory effect of laminar flow: the role of PPARgamma, epoxyeicosatrienoic acids, and soluble epoxide hydrolase. Proc. Natl. Acad. Sci. USA, 2005, 102(46), 16747-16752.
35. Krötz, F.; Riexinger, T.; Buerkle, M.A.; Nithipatikom, K.; Gloe, T.; Sohn, H.Y.; Campbell, W.B.; Pohl, U. Membrane-potentialdependent inhibition of platelet adhesion to endothelial cells by epoxyeicosatrienoic acids. Arterioscler. Thromb. Vasc. Biol., 2004, 24(3), 595-600.
36. Fitzpatrick, F.A.; Ennis, M.D.; Baze, M.E.; Wynalda, M.A.; McGee, J.E.; Liggett, W.F. Inhibition of cyclooxygenase activity and platelet aggregation by epoxyeicosatrienoic acids. Influence of stereochemistry. J. Biol. Chem., 1986, 261(32), 15334-15338.
37. Node, K.; Ruan, X.L.; Dai, J.; Yang, S.X.; Graham, L.; Zeldin, D.C.; Liao J.K. Activation of Galpha s mediates induction of tissue-type plasminogen activator gene transcription by epoxyeicosatrienoic acids. J. Biol. Chem., 2001, 276(19), 15983-15989.
38. Giannarelli, C.; Virdis, A.; De Negri, F.; Magagna, A.; Duranti, E.; Salvetti, A.; Taddei, S. Effect of sulfaphenazole on tissue plasminogen activator release in normotensive subjects and hypertensive patients. Circulation, 2009, 119(12), 1625-1633.
39. Sun, J.; Sui, X.; Bradbury, J.A.; Zeldin, D.C.; Conte, M.S.; Liao, J.K. Inhibition of vascular smooth muscle cell migration by cytochrome p450 epoxygenase-derived eicosanoids. Circ. Res., 2002, 90(9), 1020-1027.
40. Fleming, I. Epoxyeicosatrienoic acids, cell signaling and angiogenesis. Prostaglandins Other Lipid Mediat., 2007, 82(1-4), 60-67.
41. Zeldin, D.C.; Foley, J.; Boyle, J.E.; Moomaw, C.R.; Tomer, K.B.; Parker, C.; Steenbergen, C.; Wu, S. Predominant expression of an arachidonate epoxygenase in islets of Langerhans cells in human and rat pancreas. Endocrinology, 1997, 138(3), 1338-1346.
42. Falck, J.R.; Manna, S.; Moltz, J.; Chacos, N.; Capdevila, J. Epoxyeicosatrienoic acids stimulate glucagon and insulin release from isolated rat pancreatic islets. Biochem. Biophys. Res. Commun., 1983, 114(2), 743-749.
43. 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(4), 447-454.
44. Luo, P.; Chang, H.H.; Zhou, Y.; Zhang, S.; Hwang, S.H.; Morisseau, C.; Wang, C.Y.; Inscho, E.W.; Hammock, B.D.; Wang, M.H. Inhibition or deletion of soluble epoxide hydrolase prevents hyperglycemia, promotes insulin secretion, and reduces islet apoptosis. J. Pharmacol. Exp. Ther., 2010, 334(2), 430-438.
45. Sharoyko, V.V.; Zaitseva, I.I.; Leibiger, B.; Efendi, S.; Berggren, P.O.; Zaitsev, S.V. Arachidonic acid signaling is involved in the mechanism of imidazoline-induced KATP channel-independent stimulation of insulin secretion. Cell. Mol. Life Sci., 2007, 64(22), 2985-2993.
46. Skepner, J.E.; Shelly, L.D.; Ji, C.; Reidich, B.; Luo, Y. Chronic treatment with epoxyeicosatrienoic acids modulates insulin signaling and prevents insulin resistance in hepatocytes. Prostaglandins Other Lipid Mediat., 2011, 94(1-2), 3-8.
47. Yoshida, S.; Hirai, A.; Tamura, Y.; Yoshida, S. Possible involvement of arachidonic acid metabolites of cytochrome P450 monooxygenase pathway in vasopressin-stimulated glycogenolysis in isolated rat hepatocytes. Arch. Biochem. Biophys., 1990, 280(2), 346-351.
48. Ng, V.Y.; Huang, Y.; Reddy, L.M.; Falck, J.R.; Lin, E.T.; Kroetz, D.L. Cytochrome P450 eicosanoids are activators of peroxisome proliferator-activated receptor alpha. Drug Metab. Dispos., 2007, 35(7), 1126-1134.
49. Kim, D.H.; Vanella, L.; Inoue, K.; Burgess, A.; Gotlinger, K.; Manthati, V.L.; Koduru, S.R.; Zeldin, D.C.; Falck, J.R.; Schwartzman, M.L.; Abraham, N.G. Epoxyeicosatrienoic acid agonist regulates human mesenchymal stem cell-derived adipocytes through activation of HO-1-pAKT signaling and a decrease in PPAR_. Stem Cells Dev., 2010, 19(12), 1863-1873.
50. De Taeye, B.M.; Morisseau, C.; Coyle, J.; Covington, J.W.; Luria, A.; Yang, J.; Murphy, S.B.; Friedman, D.B.; Hammock, B.D.; Vaughan, D.E. Expression and regulation of soluble epoxide hydrolase in adipose tissue. Obesity (Silver Spring)., 2010, 18(3), 489-498.
51. Wang, C.P.; Hung, W.C.; Yu, T.H.; Chiu, C.A.; Lu, L.F.; Chung, F.M.; Hung, C.H.; Shin, S.J.; Chen, H.J.; Lee, Y.J. Genetic variation in the G-50T polymorphism of the cytochrome P450 epoxygenase CYP2J2 gene and the risk of younger onset type 2 diabetes among Chinese population: potential interaction with body mass index and family history. Exp. Clin. Endocrinol. Diabetes, 2010, 118(6), 346-352.
52. Ohtoshi, K.; Kaneto, H.; Node, K.; Nakamura, Y.; Shiraiwa, T.; Matsuhisa, M.; Yamasaki, Y. Association of soluble epoxide hydrolase gene polymorphism with insulin resistance in type 2 diabetic patients. Biochem. Biophys. Res. Commun., 2005, 331(1), 347-350.
53. Katakam, P.V.; Hoenig, M.; Ujhelyi, M.R.; Miller, A.W. Cytochrome P450 activity and endothelial dysfunction in insulin resistance. J. Vasc. Res., 2000, 37(5), 426-434.
54. Zhao, X.; Dey, A.; Romanko, O.P.; Stepp, D.W.; Wang, M.H.; Zhou, Y.; Jin, L.; Pollock, J.S.; Webb, R.C.; Imig, J.D. Decreased epoxygenase and increased epoxide hydrolase expression in the mesenteric artery of obese Zucker rats. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2004, 288(1), R188-R196.
55. Zhao, X.; Quigley, J.E.; Yuan, J.; Wang, M.H.; Zhou, Y.; Imig, J.D. PPAR-alpha activator fenofibrate increases renal CYP-derived eicosanoid synthesis and improves endothelial dilator function in obese Zucker rats. Am. J. Physiol. Heart Circ. Physiol., 2006, 290(6), H2187-H2195.
56. Park, Y.; Capobianco, S.; Gao, X.; Falck, J.R.; Dellsperger, K.C.; Zhang, C. Role of EDHF in type 2 diabetes-induced endothelial dysfunction. Am. J. Physiol. Heart Circ. Physiol., 2008, 295(5), H1982-H1988.
57. Morgan, E.T. Regulation of cytochrome p450 by inflammatory mediators: why and how? Drug Metab. Dispos., 2001, 29(3), 207-212.
58. Tsai S.H.; Hein, T.W.; Kuo, L.; Yang, V.C. High glucose impairs EDHF-mediated dilation of coronary arterioles via reduced cytochrome P450 activity. Microvasc. Res., 2011, 82(3), 356-363.
59. Miller, A.W.; Dimitropoulou, C.; Han, G.; White, R.E.; Busija, D.W.; Carrier, G.O. Epoxyeicosatrienoic acid-induced relaxation is impaired in insulin resistance Am. J. Physiol. Heart Circ. Physiol., 2001, 281(4), H1524-H1531.
60. Luo, P.; Zhou, Y.; Chang, H.H.; Zhang, J.; Seki, T.; Wang, C.Y.; Inscho, E.W.; Wang, M.H. Glomerular 20-HETE, EETs, and TGFbeta1 in diabetic nephropathy. Am. J. Physiol. Renal Physiol., 2009, 296(3), F556-F563.
61. Burdon, K.P.; Lehtinen, A.B.; Langefeld, C.D.; Carr, J.J.; Rich, S.S.; Freedman, B.I.; Herrington, D.; Bowden, D.W. Genetic analysis of the soluble epoxide hydrolase gene, EPHX2, in subclinical cardiovascular disease in the Diabetes Heart Study. Diab. Vasc. Dis. Res., 2008, 5(2), 128-134.
62. Schwartzman, M.L.; Iserovich, P.; Gotlinger, K.; Bellner, L.; Dunn, M.W.; Sartore, M.; Grazia Pertile, M.; Leonardi, A.; Sathe, S.; Beaton, A.; Trieu, L.; Sack, R. Profile of lipid and protein autacoids in diabetic vitreous correlates with the progression of diabetic retinopathy. Diabetes, 2010, 59(7), 1780-1788.
63. Seubert, J.; Yang, B.; Bradbury, J.A.; Graves, J.; Degraff, L.M.; Gabel, S.; Gooch, R.; Foley, J.; Newman, J.; Mao, L.; Rockman, H.A.; Hammock, B.D.; Murphy, E.; Zeldin, D.C. Enhanced postischemic functional recovery in CYP2J2 transgenic hearts involves mitochondrial ATP-sensitive K+ channels and p42/p44 MAPK pathway. Circ. Res., 2004, 95(5), 506-514.
64. Fisslthaler, B.; Michaelis, U.R.; Randriamboavonjy, V.; Busse, R.; Fleming, I. 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(3), 332-339.
65. Argiriadi, M.A.; Morisseau, C.; Hammock, B.D.; Christianson, D.W. Detoxification of environmental mutagens and carcinogens: structure, mechanism, and evolution of liver epoxide hydrolase. Proc. Natl. Acad. Sci. USA, 1999, 96(19), 10637-10642.
66. Newman, J.W.; Morisseau, C.; Harris, T.R.; Hammock, B.D. The soluble epoxide hydrolase encoded by EPXH2 is a bifunctional enzyme with novel lipid phosphate phosphatase activity. Proc. Natl. Acad. Sci. USA, 2003, 100(4), 1558-1563.
67. Tsai, H.J.; Hwang, S.H.; Morisseau, C.; Yang, J.; Jones, P.D.; Kasagami, T.; Pharmacokinetic screening of soluble epoxide hydrolase inhibitors in dogs. Eur. J. Pharm. Sci., 2010, 40(3), 222-238.
68. Anandan, S.K.; Webb, H.K.; Chen, D.; Wang, Y.X.; Aavula, B.R.; Cases, S.; Cheng, Y.; Do, Z.N.; Mehra, U.; Tran, V.; Vincelette, J.; Waszczuk, J.; White, K.; Wong, K.R.; Zhang, L.N.; Jones, P.D.; Hammock, B.D.; Patel, D.V.; Whitcomb, R.; MacIntyre, D.E.; Sabry, J.; Gless, R. 1-(1-acetyl-piperidin-4-yl)-3-adamantan-1-ylurea (AR9281) as a potent, selective, and orally available soluble epoxide hydrolase inhibitor with efficacy in rodent models of hypertension and dysglycemia. Bioorg. Med. Chem. Lett., 2011, 21(3), 983-938.
69. Sudhahar, V.; Shaw, S.; Imig, J.D. Epoxyeicosatrienoic acid analogs and vascular function. Curr. Med. Chem., 2010, 17(12), 1181-1190.
70. Falck, J.R.; Kodela, R.; Manne, R.; Atcha, R.; Puli, N.; Dubasi, N.; Manthati, V.L.; Capdevila, J.H.; Yi, X.Y.; Goldman, D.H.; Morisseau, C.; Hammock, B.D.; Campbell, W.B. 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(16), 5069-5075.
71. Luria, A.; Bettaieb, A.; Xi, Y.; Shieh, G.J.; Liu, H.C.; Inoue, H.; Tsai, H.J.; Imig, J.D.; Haj, F.G.; Hammock, B.D. Soluble epoxide hydrolase deficiency alters pancreatic islet size and improves glucose homeostasis in a model of insulin resistance. Proc. Natl. Acad. Sci. USA, 2011, 108(22), 9038-9043.
72. Xu, X.; Zhao, C.X.; Wang, L.; Tu, L.; Fang, X.; Zheng, C.; Edin, M.L.; Zeldin, D.C.; Wang, D.W. Increased CYP2J3 expression reduces insulin resistance in fructose-treated rats and db/db mice. Diabetes, 2010, 59(4), 997-1005.
73. Chen, G.; Wang, P.; Zhao, G.; Xu, G.; Gruzdev, A.; Zeldin, D.C.; Wang, D.W. Cytochrome P450 epoxygenase CYP2J2 attenuates nephropathy in streptozotocin-induced diabetic mice. Prostaglandins Other Lipid Mediat., 2011, 96(1-4), 63-71.
74. Iyer, A.; Kauter, K.; Alam, M.A.; Hwang, S.H.; Morisseau, C.; Hammock, B.D.; Brown, L. Pharmacological inhibition of soluble epoxide hydrolase ameliorates diet-induced metabolic syndrome in rats. Exp. Diabetes Res., 2012, 2012, 758614.
75. EnayetAllah, A.E.; Luria, A.; Luo, B.; Tsai, H.J.; Sura, P.; Hammock, B.D.; Grant, D.F. Opposite regulation of cholesterol levels by the phosphatase and hydrolase domains of soluble epoxide hydrolase. J. Biol. Chem., 2008, 283(52), 36592-36598.
76. do Carmo, J.M.; da Silva, A.A.; Morgan, J.; Jim Wang, Y.X.; Munusamy, S.; Hall, J.E. Inhibition of soluble epoxide hydrolase reduces food intake and increases metabolic rate in obese mice. Nutr. Metab. Cardiovasc. Dis., 2010 Dec 27. [Epub ahead of print]
77. Sodhi, K.; Inoue, K.; Gotlinger, K.H.; Canestraro, M.; Vanella, L.; Kim, D.H.; Manthati, V.L.; Koduru, S.R.; Falck, J.R.; Schwartzman, M.L.; Abraham, N.G. Epoxyeicosatrienoic acid agonist rescues the metabolic syndrome phenotype of HO-2-null mice. J. Pharmacol. Exp. Ther., 2009, 331(3), 906-916.
78. Elmarakby, A.A.; Faulkner, J.; Al-Shabrawey, M.; Wang, M.H.; Maddipati, K.R.; Imig, J.D. Deletion of soluble epoxide hydrolase gene improves renal endothelial function and reduces renal inflammation and injury in streptozotocin-induced type 1 diabetes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 301(5), R1307-R1317.
79. Huang, H.; Morisseau, C.; Wang, J.; Yang, T.; Falck, J.R.; Hammock, B.D.; Wang, M.H. Increasing or stabilizing renal epoxyeicosatrienoic acid production attenuates abnormal renal function and hypertension in obese rats. Am. J. Physiol. Renal Physiol., 2007, 293(1), F342-F349.
80. Olearczyk, J.J.; Quigley, J.E.; Mitchell, B.C.; Yamamoto, T.; Kim, I.H.; Newman, J.W.; Luria, A.; Hammock, B.D.; Imig, J.D. Administration of a substituted adamantyl urea inhibitor of soluble epoxide hydrolase protects the kidney from damage in hypertensive Goto-Kakizaki rats. Clin. Sci. (Lond.), 2009, 116(1), 61-70.
81. Zhang, L.N.; Vincelette, J.; Chen, D.; Gless, R.D.; Anandan, S.K.; Rubanyi, G.M.; Webb, H.K.; MacIntyre, D.E.; Wang, Y.X. Inhibition of soluble epoxide hydrolase attenuates endothelial dysfunction in animal models of diabetes, obesity and hypertension. Eur. J. Pharmacol., 2011, 654(1), 68-74.
82. Gómez-Marcos, M.A.; Recio-Rodríguez, J.I.; Rodríguez-Sánchez, E.; Castaño-Sánchez, Y.; de Cabo-Laso, A.; Sánchez-Salgado, B.; Rodríguez-Martín, C.; Castaño-Sánchez, C.; Gómez-Sánchez, L.; García-Ortiz, L. Central blood pressure and pulse wave velocity: relationship to target organ damage and cardiovascular morbiditymortality in diabetic patients or metabolic syndrome. An observational prospective study. LOD-DIABETES study protocol. BMC Public Health., 2010, 10, 143.
83. Ulu, A.; Davis, B.B.; Tsai, H.J.; Kim, I.H.; Morisseau, C.; Inceoglu, B.; Fiehn, O.; Hammock, B.D.; Weiss, R.H. Soluble epoxide hydrolase inhibitors reduce the development of atherosclerosis in apolipoprotein e-knockout mouse model. J. Cardiovasc. Pharmacol., 2008, 52(4), 314-323.
84. Zhang, L.N.; Vincelette, J.; Cheng, Y.; Mehra, U.; Chen, D.; Anandan, S.K.; Gless, R.; Webb, H.K.; Wang, Y.X. Inhibition of soluble epoxide hydrolase attenuated atherosclerosis, abdominal aortic aneurysm formation, and dyslipidemia. Arterioscler. Thromb. Vasc. Biol., 2009, 29(9), 1265-1270.
85. Simpkins, A.N.; Rudic, R.D.; Roy, S.; Tsai, H.J.; Hammock, B.D.; Imig J.D. Soluble epoxide hydrolase inhibition modulates vascular remodeling. Am. J. Physiol. Heart Circ. Physiol., 2010, 298(3), H795-H806.
86. Yousif, M.H.; Benter, I.F.; Roman, R.J. Cytochrome P450 metabolites of arachidonic acid play a role in the enhanced cardiac dysfunction in diabetic rats following ischaemic reperfusion injury. Auton. Autacoid Pharmacol., 2009, 29(1-2), 33-41.
87. Yousif, M.H.; Benter, I.F. Role of cytochrome P450 metabolites of arachidonic acid in regulation of corporal smooth muscle tone in diabetic and older rats. Vascul. Pharmacol., 2007, 47(5-6), 281-287.
88. Chen, D.; Whitcomb, R.; Macintyre, E.; Tran, V.; Do, Z.N.; Sabry, J.; Patel, D.V.; Anandan, S.K.; Gless, R.; Webb, H.K. Pharmacokinetics and pharmacodynamics of AR9281, an inhibitor of soluble epoxide hydrolase, in single-and multiple-dose studies in healthy human subjects. J. Clin. Pharmacol., 2011, 52(3), 319-328.
89. Keserü, B.; Barbosa-Sicard, E.; Popp, R.; Fisslthaler, B.; Dietrich, A.; Gudermann, T.; Hammock, B.D.; Falck, J.R.; Weissmann, N.; Busse, R.; Fleming, I. Epoxyeicosatrienoic acids and the soluble epoxide hydrolase are determinants of pulmonary artery pressure and the acute hypoxic pulmonary vasoconstrictor response. FASEB J., 2008, 22(12), 4306-4315.
90. Keserü, B.; Barbosa-Sicard, E.; Schermuly, R.T.; Tanaka, H.; Hammock, B.D.; Weissmann, N.; Fisslthaler, B. Fleming, I. Hypoxia-induced pulmonary hypertension: comparison of soluble epoxide hydrolase deletion vs. inhibition. Cardiovasc. Res., 2010, 85(1), 232-240.
91. Panigrahy, D.; Greene, E.R.; Pozzi, A.; Wang, D.W.; Zeldin, D.C. EET signaling in cancer. Cancer Metastasis Rev., 2011, 30(3-4), 525-540.
92. Panigrahy, D.; Edin, M.L.; Lee, C.R.; Huang, S.; Bielenberg, D.R.; Butterfield, C.E.; Barnés C.M.; Mammoto, A.; Mammoto, T.; Luria, A.; Benny, O.; Chaponis, D.M.; Dudley, A.C.; Greene, E.R.; Vergilio, J.A.; Pietramaggiori, G.; Scherer-Pietramaggiori, S.S.; Short, S.M.; Seth, M.; Lih, F.B.; Tomer, K.B.; Yang, J.; Schwendener, R.A.; Hammock, B.D.; Falck, J.R.; Manthati, V.L.; Ingber, D.E.; Kaipainen, A.; D'Amore, P.A.; Kieran, M.W.; Zeldin, D.C. Epoxyeicosanoids stimulate multiorgan metastasis and tumor dormancy escape in mice. J. Clin. Invest., 2012, 122(1), 178-191.