Endothelial expression of human cytochrome P450 epoxygenase CYP2C8 increases susceptibility to ischemia-reperfusion injury in isolated mouse heart

FASEB Journal

Volumn 25, Issue 10, 2011, Pages 3436-3447

  Edin, Matthew L ^a   Wang, ZhongJing ^a   Bradbury, J Alyce ^a   Graves, Joan P ^a   Lih, Fred B ^a   DeGraff, Laura M ^a   Foley, Julie F ^a   Torphy, Robert ^a   Ronnekleiv, Oline K ^b,c   Tomer, Kenneth B ^a   Lee, Craig R ^d   Zeldin, Darryl C ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d University of North Carolina at Chapel Hill   (United States)

Author keywords

CYP2J2; EETs; Langendorff; Leukotoxin; Reactive oxygen species

Indexed keywords

CYTOCHROME P450 2C8; EPOXYICOSATRIENOIC ACID; REACTIVE OXYGEN METABOLITE; STEARIC ACID DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CONVALESCENCE; CORONARY VASCULAR RESISTANCE; DISEASE PREDISPOSITION; ENDOTHELIUM; ENZYME INHIBITION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE PRESSURE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART RATE; HYDROLYSIS; ISOLATED HEART; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; PROTEIN EXPRESSION; REPERFUSION INJURY; TRANSGENIC MOUSE; WILD TYPE;

ANIMALS; ARYL HYDROCARBON HYDROXYLASES; CYTOCHROME P-450 ENZYME SYSTEM; EICOSANOIDS; ENDOTHELIUM, VASCULAR; EPOXIDE HYDROLASES; HEART; HUMANS; MICE; MICE, TRANSGENIC; OLEIC ACIDS; PROMOTER REGIONS, GENETIC; RECEPTOR PROTEIN-TYROSINE KINASES; REPERFUSION INJURY;

MUS; MUS MUSCULUS;

EID: 80053919098     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-188300     Document Type: Article

References (56)

1. Campbell, W. B., Gebremedhin, D., Pratt, P. F., and Harder, D. R. (1996) Identification of epoxyeicosatrienoic acids as endothelium-derived hyperpolarizing factors. Circ. Res. 78, 415-423 (Pubitemid 26072547)
2. Li, P. L., and Campbell, W. B. (1997) Epoxyeicosatrienoic acids activate K+ channels in coronary smooth muscle through a guanine nucleotide binding protein. Circ. Res. 80, 877-884
3. Michaelis, U. R., Fisslthaler, B., Barbosa-Sicard, E., Falck, J. R., Fleming, I., and Busse, R. (2005) Cytochrome P450 epoxygenases 2C8 and 2C9 are implicated in hypoxia-induced endothelial cell migration and angiogenesis. J. Cell Sci. 118, 5489-5498 (Pubitemid 43079290)
4. Wang, Y., Wei, X., Xiao, X., Hui, R., Card, J. W., Carey, M. A., Wang, D. W., and Zeldin, D. C. (2005) 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, 522-532 (Pubitemid 41043832)
5. Liu, Y., Zhang, Y., Schmelzer, K., Lee, T. S., Fang, X., Zhu, Y., Spector, A. A., Gill, S., Morisseau, C., Hammock, B. D., and Shyy, J. Y. (2005) The antiinflammatory effect of laminar flow: the role of PPARgamma, epoxyeicosatrienoic acids, and soluble epoxide hydrolase. Proc. Natl. Acad. Sci. U. S. A. 102, 16747-16752 (Pubitemid 41688848)
6. Deng, Y., Edin, M. L., Theken, K. N., Schuck, R. N., Flake, G. P., Kannon, M. A., Degraff, L. M., Lih, F. B., Foley, J., Bradbury, J. A., Graves, J. P., Tomer, K. B., Falck, J. R., Zeldin, D. C., and Lee, C. R. (2011) Endothelial CYP epoxygenase overexpression and soluble epoxide hydrolase disruption attenuate acute vascular inflammatory responses in mice. FASEB J. 25, 703-713
7. Node, K., Huo, Y., Ruan, X., Yang, B., Spiecker, M., Ley, K., Zeldin, D. C., and Liao, J. K. (1999) Anti-inflammatory properties of cytochrome P450 epoxygenase-derived eicosanoids. Science 285, 1276-1279 (Pubitemid 29398616)
8. Satoh, T., Cohen, H. T., and Katz, A. I. (1993) Intracellular signaling in the regulation of renal Na-K-ATPase. II. Role of eicosanoids. J. Clin. Invest. 91, 409-415 (Pubitemid 23064121)
9. Chen, J., Capdevila, J. H., Zeldin, D. C., and Rosenberg, R. L. (1999) Inhibition of cardiac L-type calcium channels by epoxyeicosatrienoic acids. Mol. Pharmacol. 55, 288-295 (Pubitemid 29076025)
10. Spector, A. A., and Norris, A. W. (2007) Action of epoxyeicosatrienoic acids on cellular function. Am. J. Physiol. 292, C996-1012
11. Imig, J. D., and Hammock, B. D. (2009) Soluble epoxide hydrolase as a therapeutic target for cardiovascular diseases. Nat. Rev. 8, 794-805
12. Gross, G. J., and Nithipatikom, K. (2009) Soluble epoxide hydrolase: a new target for cardioprotection. Curr. Opin. Investig. Drugs 10, 253-258
13. 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., and Zeldin, D. C. (2004) Enhanced postischemic functional recovery in CYP2J2 transgenic hearts involves mitochondrial ATP-sensitive K+ channels and p42/p44 MAPK pathway. Circulation Res. 95, 506-514 (Pubitemid 39180931)
14. Seubert, J. M., Zeldin, D. C., Nithipatikom, K., and Gross, G. J. (2007) Role of epoxyeicosatrienoic acids in protecting the myocardium following ischemia/reperfusion injury. Prostaglandins Other Lipid Mediat. 82, 50-59 (Pubitemid 44880163)
15. Katragadda, D., Batchu, S. N., Cho, W. J., Chaudhary, K. R., Falck, J. R., and Seubert, J. M. (2009) Epoxyeicosatrienoic acids limit damage to mitochondrial function following stress in cardiac cells. J. Mol. Cell. Cardiol. 46, 867-875
16. Wong, P. Y., Lai, P. S., Shen, S. Y., Belosludtsev, Y. Y., and Falck, J. R. (1997) Post-receptor signal transduction and regulation of 14(R),15(S)-epoxyeicosatrienoic acid (14,15-EET) binding in U-937 cells. J. Lipid Mediat. Cell Signal. 16, 155-169 (Pubitemid 27285837)
17. Chen, J. K., Capdevila, J., and Harris, R. C. (2002) Heparin-binding EGF-like growth factor mediates the biological effects of P450 arachidonate epoxygenase metabolites in epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 99, 6029-6034 (Pubitemid 34493259)
18. Konkel, A., and Schunck, W. H. Role of cytochrome P450 enzymes in the bioactivation of polyunsaturated fatty acids. Biochim. Biophys. Acta 1814, 210-222
19. Chaudhary, K. R., Batchu, S. N., Das, D., Suresh, M. R., Falck, J. R., Graves, J. P., Zeldin, D. C., and Seubert, J. M. (2009) Role of B-type natriuretic peptide in epoxyeicosatrienoic acid-mediated improved post-ischaemic recovery of heart contractile function. Cardiovasc. Res. 83, 362-370
20. Gross, G. J., Baker, J. E., Hsu, A., Wu, H. E., Falck, J. R., and Nithipatikom, K. (2010) Evidence for a role of opioids in epoxyeicosatrienoic acid-induced cardioprotection in rat hearts. Am. J. Physiol. Heart Circ. Physiol. 298, H2201-H2207
21. Spiecker, M., Darius, H., Hankeln, T., Soufi, M., Sattler, A. M., Schaefer, J. R., Node, K., Borgel, J., Mugge, A., Lindpaintner, K., Huesing, A., Maisch, B., Zeldin, D. C., and Liao, J. K. (2004) Risk of coronary artery disease associated with polymorphism of the cytochrome P450 epoxygenase CYP2J2. Circulation 110, 2132-2136 (Pubitemid 39372490)
22. Lee, C. R., North, K. E., Bray, M. S., Couper, D. J., Heiss, G., and Zeldin, D. C. (2007) CYP2J2 and CYP2C8 polymorphisms and coronary heart disease risk: the Atherosclerosis Risk in Communities (ARIC) study. Pharmacogen. Genomics 17, 349-358 (Pubitemid 46608542)
23. Lee, C. R., North, K. E., Bray, M. S., Fornage, M., Seubert, J. M., Newman, J. W., Hammock, B. D., Couper, D. J., Heiss, G., and Zeldin, D. C. (2006) Genetic variation in soluble epoxide hydrolase (EPHX2) and risk of coronary heart disease: the Atherosclerosis Risk in Communities (ARIC) study. Hum. Mol. Genet. 15, 1640-1649 (Pubitemid 43904830)
24. Marciante, K. D., Totah, R. A., Heckbert, S. R., Smith, N. L., Lemaitre, R. N., Lumley, T., Rice, K. M., Hindorff, L. A., Bis, J. C., Hartman, B., and Psaty, B. M. (2008) Common variation in cytochrome P450 epoxygenase genes and the risk of incident nonfatal myocardial infarction and ischemic stroke. Pharmacogenet. Genom. 18, 535-543 (Pubitemid 351769921)
25. Yasar, U., Bennet, A. M., Eliasson, E., Lundgren, S., Wiman, B., De Faire, U., and Rane, A. (2003) Allelic variants of cytochromes P450 2C modify the risk for acute myocardial infarction. Pharmacogenetics 13, 715-720 (Pubitemid 38429249)
26. Granville, D. J., Tashakkor, B., Takeuchi, C., Gustafsson, A. B., Huang, C., Sayen, M. R., Wentworth, P., Jr., Yeager, M., and Gottlieb, R. A. (2004) Reduction of ischemia and reperfusion-induced myocardial damage by cytochrome P450 inhibitors. Proc. Natl. Acad. Sci. U. S. A. 101, 1321-1326 (Pubitemid 38182687)
27. Fleming, I., Michaelis, U. R., Bredenkotter, D., Fisslthaler, B., Dehghani, F., Brandes, R. P., and Busse, R. (2001) Endothelium-derived hyperpolarizing factor synthase (cytochrome P450 2C9) is a functionally significant source of reactive oxygen species in coronary arteries. Circ. Res. 88, 44-51 (Pubitemid 32064081)
28. Gustafsson, A. B., and Gottlieb, R. A. (2008) Heart mitochondria: gates of life and death. Cardiovasc. Res. 77, 334-343 (Pubitemid 351197632)
29. Hunter, A. L., Bai, N., Laher, I., and Granville, D. J. (2005) Cytochrome p450 2C inhibition reduces post-ischemic vascular dysfunction. Vasc. Pharmacol. 43, 213-219 (Pubitemid 41586207)
30. Greene, J. F., Newman, J. W., Williamson, K. C., and Hammock, B. D. (2000) Toxicity of epoxy fatty acids and related compounds to cells expressing human soluble epoxide hydrolase. Chem. Res. Toxicol. 13, 217-226 (Pubitemid 30241646)
31. Moran, J. H., Weise, R., Schnellmann, R. G., Freeman, J. P., and Grant, D. F. (1997) Cytotoxicity of linoleic acid diols to renal proximal tubular cells. Toxicol. Appl. Pharmacol. 146, 53-59 (Pubitemid 27406396)
32. Viswanathan, S., Hammock, B. D., Newman, J. W., Meerarani, P., Toborek, M., and Hennig, B. (2003) Involvement of CYP 2C9 in mediating the proinflammatory effects of linoleic acid in vascular endothelial cells. J. Am. Coll. Nutr. 22, 502-510 (Pubitemid 38010016)
33. Siegfried, M. R., Aoki, N., Lefer, A. M., Elisseou, E. M., and Zipkin, R. E. (1990) Direct cardiovascular actions of two metabolites of linoleic acid. Life Sci. 46, 427-433 (Pubitemid 20053252)
34. Sugiyama, S., Hayakawa, M., Nagai, S., Ajioka, M., and Ozawa, T. (1987) Leukotoxin, 9, 10-epoxy-12-octadecenoate, causes cardiac failure in dogs. Life Sci. 40, 225-231 (Pubitemid 17219684)
35. Nelson, D. R., Zeldin, D. C., Hoffman, S. M., Maltais, L. J., Wain, H. M., and Nebert, D. W. (2004) Comparison of cytochrome P450 (CYP) genes from the mouse and human genomes, including nomenclature recommendations for genes, pseudogenes and alternative-splice variants. Pharmacogenetics 14, 1-18 (Pubitemid 38183957)
36. Lee, C. R., Imig, J. D., Edin, M. L., Foley, J., Degraff, L. M., Bradbury, J. A., Graves, J. P., Lih, F. B., Clark, J., Myers, P., Perrow, A. L., Lepp, A. N., Kannon, M. A., Ronnekleiv, O. K., Alkayed, N. J., Falck, J. R., Tomer, K. B., and Zeldin, D. C. (2010) Endothelial expression of human cytochrome P450 epoxygenases lowers blood pressure and attenuates hypertension-induced renal injury in mice. FASEB J. 24, 3770-3781
37. Schlaeger, T. M., Bartunkova, S., Lawitts, J. A., Teichmann, G., Risau, W., Deutsch, U., and Sato, T. N. (1997) Uniform vascular-endothelial-cell- specific gene expression in both embryonic and adult transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 94, 3058-3063 (Pubitemid 27157263)
38. King, L. M., Ma, J., Srettabunjong, S., Graves, J., Bradbury, J. A., Li, L., Spiecker, M., Liao, J. K., Mohrenweiser, H., and Zeldin, D. C. (2002) Cloning of CYP2J2 gene and identification of functional polymorphisms. Mol. Pharmacol. 61, 840-852 (Pubitemid 34273164)
39. Kusmic, C., Lazzerini, G., Coceani, F., Barsacchi, R., L'Abbate, A., and Sambuceti, G. (2006) Paradoxical coronary microcirculatory constriction during ischemia: a synergic function for nitric oxide and endothelin. Am. J. Physiol. Heart Circ. Physiol. 291, H1814-H1821 (Pubitemid 44497688)
40. Mobert, J., Becker, B. F., Zahler, S., and Gerlach, E. (1997) Hemodynamic effects of isoprostanes (8-iso-prostaglandin F2alpha and E2) in isolated guinea pig hearts. J. Cardiovasc. Pharmacol. 29, 789-794 (Pubitemid 27337531)
41. Daikh, B. E., Lasker, J. M., Raucy, J. L., and Koop, D. R. (1994) Regio- and stereoselective epoxidation of arachidonic acid by human cytochromes P450 2C8 and 2C9. J. Pharmacol. Exp. Therapeut. 271, 1427-1433 (Pubitemid 24382654)
42. Zeldin, D. C., DuBois, R. N., Falck, J. R., and Capdevila, J. H. (1995) Molecular cloning, expression and characterization of an endogenous human cytochrome P450 arachidonic acid epoxygenase isoform. Arch. Biochem. Biophys. 322, 76-86
43. Wen, X., Wang, J. S., Backman, J. T., Laitila, J., and Neuvonen, P. J. (2002) Trimethoprim and sulfamethoxazole are selective inhibitors of CYP2C8 and CYP2C9, respectively. Drug Metab. Dispos. 30, 631-635 (Pubitemid 34579094)
44. Seubert, J. M., Sinal, C. J., Graves, J., DeGraff, L. M., Bradbury, J. A., Lee, C. R., Goralski, K., Carey, M. A., Luria, A., Newman, J. W., Hammock, B. D., Falck, J. R., Roberts, H., Rockman, H. A., Murphy, E., and Zeldin, D. C. (2006) Role of soluble epoxide hydrolase in postischemic recovery of heart contractile function. Circ. Res. 99, 442-450 (Pubitemid 44253701)
45. Nithipatikom, K., Moore, J. M., Isbell, M. A., Falck, J. R., and Gross, G. J. (2006) Epoxyeicosatrienoic acids in cardioprotection: ischemic versus reperfusion injury. Am. J. Physiol. Heart Circ. Physiol. 291, H537-H542 (Pubitemid 44175058)
46. Yang, B., Graham, L., Dikalov, S., Mason, R. P., Falck, J. R., Liao, J. K., and Zeldin, D. C. (2001) Overexpression of cytochrome P450 CYP2J2 protects against hypoxia-reoxygenation injury in cultured bovine aortic endothelial cells. Mol. Pharmacol. 60, 310-320 (Pubitemid 32678296)
47. King, L. M., Gainer, J. V., David, G. L., Dai, D., Goldstein, J. A., Brown, N. J., and Zeldin, D. C. (2005) Single nucleotide polymorphisms in the CYP2J2 and CYP2C8 genes and the risk of hypertension. Pharmacogenet. Genom. 15, 7-13 (Pubitemid 43205521)
48. Bylund, J., Ericsson, J., and Oliw, E. H. (1998) Analysis of cytochrome P450 metabolites of arachidonic and linoleic acids by liquid chromatography-mass spectrometry with ion trap MS. Anal. Biochem. 265, 55-68 (Pubitemid 28541793)
49. Fukushima, A., Hayakawa, M., Sugiyama, S., Ajioka, M., Ito, T., Satake, T., and Ozawa, T. (1988) Cardiovascular effects of leukotoxin (9, 10-epoxy-12-octadecenoate) and free fatty acids in dogs. Cardiovasc. Res. 22, 213-218 (Pubitemid 18075572)
50. Poyton, R. O., Ball, K. A., and Castello, P. R. (2009) Mitochondrial generation of free radicals and hypoxic signaling. Trends Endocrinol. Metabol. 20, 332-340
51. Kojda, G., and Harrison, D. (1999) Interactions between NO and reactive oxygen species: pathophysiological importance in atherosclerosis, hypertension, diabetes and heart failure. Cardiovasc. Res. 43, 562-571 (Pubitemid 29369255)
52. Mitchell, L. A., Grant, D. F., Melchert, R. B., Petty, N. M., and Kennedy, R. H. (2002) Linoleic acid metabolites act to increase contractility in isolated rat heart. Cardiovasc. Toxicol. 2, 219-230
53. Hanaki, Y., Kamiya, H., Ohno, M., Hayakawa, M., Sugiyama, S., and Ozawa, T. (1991) Leukotoxin, 9, 10-epoxy-12-octadecenoate: a possible responsible factor in circulatory shock and disseminated intravascular coagulation. Jpn. J. Med. 30, 224-228
54. Kosaka, K., Suzuki, K., Hayakawa, M., Sugiyama, S., and Ozawa, T. (1994) Leukotoxin, a linoleate epoxide: its implication in the late death of patients with extensive burns. Mol. Cell. Biochem. 139, 141-148 (Pubitemid 24371163)
55. Theken, K. N., and Lee, C. R. (2007) Genetic variation in the cytochrome P450 epoxygenase pathway and cardiovascular disease risk. Pharmacogenomics 8, 1369-1383 (Pubitemid 350162851)
56. Chaudhary, K. R., Abukhashim, M., Hwang, S. H., Hammock, B. D., and Seubert, J. M. (2010) 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. 55, 67-73