Metabolic products of soluble epoxide hydrolase are essential for monocyte chemotaxis to MCP-1 in vitro and in vivo

Journal of Lipid Research

Volumn 54, Issue 2, 2013, Pages 436-447

  Kundu, Suman ^a   Roome, Talat ^a   Bhattacharjee, Ashish ^a,b   Carnevale, Kevin A ^a,d   Yakubenko, Valentin P ^a,b   Zhang, Renliang ^a   Hwang, Sung Hee ^c   Hammock, Bruce D ^c   Cathcart, Martha K ^a,b  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Des Moines University College of Osteopathic Medicine   (United States)

Author keywords

Cell migration; Dihydroxyeicosatrienoic acid; Fatty acid metabolism; Inflammation; Phospholipase A2

Indexed keywords

ARACHIDONIC ACID; CYTOCHROME P450; CYTOSOLIC PHOSPHOLIPASE A2; DIHYDROXYICOSATRIENOIC ACID; EPOXIDE HYDROLASE; EPOXYICOSATRIENOIC ACID; ICOSATRIENOIC ACID; LIPOXYGENASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MONOCYTE CHEMOTACTIC PROTEIN 1; PROSTAGLANDIN SYNTHASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME METABOLISM; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MONOCYTE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANIMALS; ARACHIDONIC ACID; CHEMOKINE CCL2; CHEMOTAXIS; CYTOCHROME P-450 ENZYME SYSTEM; ENZYME INHIBITORS; EPOXIDE HYDROLASES; FATTY ACIDS, MONOUNSATURATED; FEMALE; HUMANS; LIPOXYGENASE; MICE; MONOCYTES; PHOSPHOLIPASES A2, CYTOSOLIC; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; SOLUBILITY;

EID: 84872458939     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M031914     Document Type: Article

References (63)

1. Deshmane, S. L., S. Kremlev, S. Amini, and B. E. Sawaya. 2009. Monocyte chemoattractant protein-1 (MCP-1): an overview. J. Interferon Cytokine Res. 29: 313-326.
2. Cathcart, M. K. 2009. Signal-activated phospholipase regulation of leukocyte chemotaxis. J. Lipid Res. 50 (Suppl.): 231-236.
3. Kowala, M. C., R. Recce, S. Beyer, C. Gu, and M. Valentine. 2000. Characterization of atherosclerosis in LDL receptor knockout mice: macrophage accumulation correlates with rapid and sustained expression of aortic MCP-1/JE. Atherosclerosis. 149: 323-330. (Pubitemid 30145542)
4. Gu, L., Y. Okada, S. K. Clinton, C. Gerard, G. K. Sukhova, P. Libby, and B. J. Rollins. 1998. Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptordeficient mice. Mol. Cell. 2: 275-281. (Pubitemid 128373654)
5. Boring, L., J. Gosling, M. Cleary, and I. F. Charo. 1998. Decreased lesion formation in CCR2-/- mice reveals a role for chemokines in the initiation of atherosclerosis. Nature. 394: 894-897. (Pubitemid 28410911)
6. Charo, I. F., S. J. Myers, A. Herman, C. Franci, A. J. Connolly, and S. R. Coughlin. 1994. Molecular cloning and functional expression of two monocyte chemoattractant protein 1 receptors reveals alternative splicing of the carboxyl-terminal tails. Proc. Natl. Acad. Sci. USA. 91: 2752-2756. (Pubitemid 24139426)
7. Mishra, R. S., K. A. Carnevale, and M. K. Cathcart. 2008. iPLA2beta: front and center in human monocyte chemotaxis to MCP-1. J. Exp. Med. 205: 347-359. (Pubitemid 351281601)
8. Li, Q., and M. K. Cathcart. 1997. Selective inhibition of cytosolic phospholipase A2 in activated human monocytes. Regulation of superoxide anion production and low density lipoprotein oxidation. J. Biol. Chem. 272: 2404-2411. (Pubitemid 27058529)
9. Spector, A. A. 2009. Arachidonic acid cytochrome P450 epoxygenase pathway. J. Lipid Res. 50 (Suppl.): 52-56.
10. Hwang, S. H., H. J. Tsai, J. Y. Liu, C. Morisseau, and B. D. Hammock. 2007. Orally bioavailable potent soluble epoxide hydrolase inhibitors. J. Med. Chem. 50: 3825-3840. (Pubitemid 47292046)
11. Cathcart, M. K., D. W. Morel, and G. M. Chisolm III. 1985. Monocytes and neutrophils oxidize low density lipoprotein making it cytotoxic. J. Leukoc. Biol. 38: 341-350. (Pubitemid 15243435)
12. Cathcart, M. K., A. K. McNally, D. W. Morel, and G. M. Chisolm III. 1989. Superoxide anion participation in human monocyte-mediated oxidation of low-density lipoprotein and conversion of low-density lipoprotein to a cytotoxin. J. Immunol. 142: 1963-1969. (Pubitemid 19081549)
13. 2 integrin activation prevents alternative activation of human and murine macrophages and impedes foam cell formation. Circ. Res. 108: 544-554.
14. Falk, W., R. H. Goodwin, Jr., and E. J. Leonard. 1980. A 48-well micro chemotaxis assembly for rapid and accurate measurement of leukocyte migration. J. Immunol. Methods. 33: 239-247.
15. Roy, B., A. Bhattacharjee, B. Xu, D. Ford, A. L. Maizel, and M. K. Cathcart. 2002. IL-13 signal transduction in human monocytes: phosphorylation of receptor components, association with Jaks, and phosphorylation/activation of Stats. J. Leukoc. Biol. 72: 580-589.
16. Yue, H., S. A. Jansen, K. I. Strauss, M. R. Borenstein, M. F. Barbe, L. J. Rossi, and E. Murphy. 2007. A liquid chromatography/mass spectrometric method for simultaneous analysis of arachidonic acid and its endogenous eicosanoid metabolites prostaglandins, dihydroxyeicosatrienoic acids, hydroxyeicosatetraenoic acids, and epoxyeicosatrienoic acids in rat brain tissue. J. Pharm. Biomed. Anal. 43: 1122-1134. (Pubitemid 46185820)
17. Zaoui, A., Y. Cherrah, N. Mahassini, K. Alaoui, H. Amarouch, and M. Hassar. 2002. Acute and chronic toxicity of Nigella sativa fixed oil. Phytomedicine. 9: 69-74. (Pubitemid 34184213)
18. Pillaia, P. G., and P. Suresh 2011. Evaluation of acute and sub-acute toxicity of methanolic extract of Caesalpinia Bonducella. Euro. J. Sci. Res. 53: 462-469.
19. Koster, K., M. Anderson, and E. J. DeBeer. 1959. Acetic acid analgesic screening. Fed. Proc. 18: 418-420.
20. Carnevale, K. A., and M. K. Cathcart. 2001. Calcium-independent phospholipase A(2) is required for human monocyte chemotaxis to monocyte chemoattractant protein 1. J. Immunol. 167: 3414-3421. (Pubitemid 32852586)
21. Xu, D., N. Li, Y. He, V. Timofeyev, L. Lu, H. J. Tsai, I. H. Kim, D. Tuteja, R. K. Mateo, A. Singapuri, et al. 2006. Prevention and reversal of cardiac hypertrophy by soluble epoxide hydrolase inhibitors. Proc. Natl. Acad. Sci. USA. 103: 18733-18738. (Pubitemid 44913479)
22. Yen, H., Y. Zhang, S. Penfold, and B. J. Rollins. 1997. MCP-1-mediated chemotaxis requires activation of non-overlapping signal transduction pathways. J. Leukoc. Biol. 61: 529-532. (Pubitemid 27219848)
23. Wain, J. H., J. A. Kirby, and S. Ali. 2002. Leucocyte chemotaxis: examination of mitogen-activated protein kinase and phosphoinositide 3-kinase activation by monocyte chemoattractant proteins-1, -2, -3 and -4. Clin. Exp. Immunol. 127: 436-444. (Pubitemid 34437815)
24. Stebbins, K. J., A. R. Broadhead, C. S. Baccei, J. M. Scott, Y. P. Truong, H. Coate, N. S. Stock, A. M. Santini, P. Fagan, P. Prodanovich, et al. 2010. Pharmacological blockade of the DP2 receptor inhibits cigarette smoke-induced inflammation, mucus cell metaplasia, and epithelial hyperplasia in the mouse lung. J. Pharmacol. Exp. Ther. 332: 764-775.
25. Maddox, J. F., and C. N. Serhan. 1996. Lipoxin A4 and B4 are potent stimuli for human monocyte migration and adhesion: selective inactivation by dehydrogenation and reduction. J. Exp. Med. 183: 137-146.
26. Gross, G. J., J. R. Falck, E. R. Gross, M. Isbell, J. Moore, and K. Nithipatikom. 2005. Cytochrome P450 and arachidonic acid metabolites: role in myocardial ischemia/reperfusion injury revisited. Cardiovasc. Res. 68: 18-25. (Pubitemid 41253552)
27. Lee, D. Y., H. S. Shin, S. K. Bae, and M. G. Lee. 2006. Effects of enzyme inducers and inhibitors on the pharmacokinetics of intravenous omeprazole in rats. Biopharm. Drug Dispos. 27: 209-218. (Pubitemid 44122106)
28. Nithipatikom, K., D. M. Brody, A. T. Tang, V. L. Manthati, J. R. Falck, C. L. Williams, and W. B. Campbell. 2010. Inhibition of carcinoma cell motility by epoxyeicosatrienoic acid (EET) antagonists. Cancer Sci. 101: 2629-2636.
29. Jiang, J. G., Y. G. Ning, C. Chen, D. Ma, Z. J. Liu, S. Yang, J. Zhou, X. Xiao, X. A. Zhang, M. L. Edin, et al. 2007. Cytochrome p450 epoxygenase promotes human cancer metastasis. Cancer Res. 67: 6665-6674. (Pubitemid 47105512)
30. Yu, Z., F. Xu, L. M. Huse, C. Morisseau, A. J. Draper, J. W. Newman, C. Parker, L. Graham, M. M. Engler, B. D. Hammock, et al. 2000. Soluble epoxide hydrolase regulates hydrolysis of vasoactive epoxyeicosatrienoic acids. Circ. Res. 87: 992-998.
31. Spector, A. A., X. Fang, G. D. Snyder, and N. L. Weintraub. 2004. Epoxyeicosatrienoic acids (EETs): metabolism and biochemical function. Prog. Lipid Res. 43: 55-90. (Pubitemid 37433867)
32. Raichel, L., S. Berger, N. Hadad, L. Kachko, M. Karter, I. Szaingurten-Solodkin, R. O. Williams, M. Feldmann, and R. Levy. 2008. Reduction of cPLA2alpha overexpression: an efficient antiinflammatory therapy for collagen-induced arthritis. Eur. J. Immunol. 38: 2905-2915.
33. Imig, J. D., and B. D. Hammock. 2009. Soluble epoxide hydrolase as a therapeutic target for cardiovascular diseases. Nat. Rev. Drug Discov. 8: 794-805.
34. Fang, X. 2006. Soluble epoxide hydrolase: a novel target for the treatment of hypertension. Recent Pat. Cardiovasc. Drug Discov. 1: 67-72.
35. Imig, J. D., A. N. Simpkins, M. Renic, and D. R. Harder. 2011. Cytochrome P450 eicosanoids and cerebral vascular function. Expert Rev. Mol. Med. 13: e7.
36. Wagner, K., B. Inceoglu, S. S. Gill, and B. D. Hammock. 2011. Epoxygenated fatty acids and soluble epoxide hydrolase inhibition: novel mediators of pain reduction. J. Agric. Food Chem. 59: 2816-2824.
37. do Carmo, J. M., A. A. da Silva, J. Morgan, Y. X. Jim Wang, S. Munusamy, and J. E. Hall. 2012. Inhibition of soluble epoxide hydrolase reduces food intake and increases metabolic rate in obese mice. Nutr. Metab. Cardiovasc. Dis. 22: 598-604.
38. Norwood, S., J. Liao, B. D. Hammock, and G. Y. Yang. 2010. Epoxyeicosatrienoic acids and soluble epoxide hydrolase: potential therapeutic targets for inflammation and its induced carcinogenesis. Am. J. Transl. Res. 2: 447-457.
39. Goulitquer, S., Y. Dreano, F. Berthou, L. Corcos, and D. Lucas. 2008. Determination of epoxyeicosatrienoic acids in human red blood cells and plasma by GC/MS in the NICI mode. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 876: 83-88.
40. Spector, A. A., and A. W. Norris. 2007. Action of epoxyeicosatrienoic acids on cellular function. Am. J. Physiol. Cell Physiol. 292: C996-C1012. (Pubitemid 46442641)
41. Pozzi, A., I. Macias-Perez, T. Abair, S. Wei, Y. Su, R. Zent, J. R. Falck, and J. H. Capdevila. 2005. 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: 27138-27146. (Pubitemid 41040752)
42. Batchu, S. N., S. B. Lee, R. S. Qadhi, K. R. Chaudhary, H. El-Sikhry, R. Kodela, J. R. Falck, and J. M. Seubert. 2011. Cardioprotective effect of a dual acting epoxyeicosatrienoic acid analogue towards ischaemia reperfusion injury. Br. J. Pharmacol. 162: 897-907.
43. Abukhashim, M., G. J. Wiebe, and J. M. Seubert. 2011. Regulation of forskolin-induced cAMP production by cytochrome P450 epoxygenase metabolites of arachidonic acid in HEK293 cells. Cell Biol. Toxicol. 27: 321-332.
44. Behm, D. J., A. Ogbonna, C. Wu, C. L. Burns-Kurtis, and S. A. Douglas. 2009. Epoxyeicosatrienoic acids function as selective, endogenous antagonists of native thromboxane receptors: identification of a novel mechanism of vasodilation. J. Pharmacol. Exp. Ther. 328: 231-239.
45. Hirt, D. L., J. Capdevila, J. R. Falck, M. D. Breyer, and H. R. Jacobson. 1989. Cytochrome P450 metabolites of arachidonic acid are potent inhibitors of vasopressin action on rabbit cortical collecting duct. J. Clin. Invest. 84: 1805-1812. (Pubitemid 20016184)
46. Fang, X., T. L. Kaduce, N. L. Weintraub, M. VanRollins, and A. A. Spector. 1996. Functional implications of a newly characterized pathway of 11,12-epoxyeicosatrienoic acid metabolism in arterial smooth muscle. Circ. Res. 79: 784-793. (Pubitemid 26317826)
47. Weintraub, N. L., X. Fang, T. L. Kaduce, M. VanRollins, P. Chatterjee, and A. A. Spector. 1997. Potentiation of endothelium-dependent relaxation by epoxyeicosatrienoic acids. Circ. Res. 81: 258-267. (Pubitemid 27342493)
48. Fang, X., S. Hu, B. Xu, G. D. Snyder, S. Harmon, J. Yao, Y. Liu, B. Sangras, J. R. Falck, N. L. Weintraub, et al. 2006. 14,15- Dihydroxyeicosatrienoic acid activates peroxisome proliferator-activated receptor-alpha. Am. J. Physiol. Heart Circ. Physiol. 290: H55-H63.
49. Liu, Y., Y. Zhang, K. Schmelzer, T. S. Lee, X. Fang, Y. Zhu, A. A. Spector, S. Gill, C. Morisseau, B. D. Hammock, et al. 2005. The antiinflammatory effect of laminar flow: the role of PPARgamma, epoxyeicosatrienoic acids, and soluble epoxide hydrolase. Proc. Natl. Acad. Sci. USA. 102: 16747-16752. (Pubitemid 41688848)
50. Lu, T., P. V. Katakam, M. VanRollins, N. L. Weintraub, A. A. Spector, and H. C. Lee. 2001. Dihydroxyeicosatrienoic acids are potent activators of Ca(2+)-activated K(+) channels in isolated rat coronary arterial myocytes. J. Physiol. 534: 651-667. (Pubitemid 32700865)
51. Gijón, M. A., and C. C. Leslie. 1999. Regulation of arachidonic acid release and cytosolic phospholipase A2 activation. J. Leukoc. Biol. 65: 330-336. (Pubitemid 29109704)
52. Lin, L. L., M. Wartmann, A. Y. Lin, J. L. Knopf, A. Seth, and R. J. Davis. 1993. cPLA2 is phosphorylated and activated by MAP kinase. Cell. 72: 269-278. (Pubitemid 23044941)
53. Bhattacharjee, A., A. Mulya, S. Pal, B. Roy, G. M. Feldman, and M. K. Cathcart. 2010. Monocyte 15-lipoxygenase gene expression requires ERK1/2 MAPK activity. J. Immunol. 185: 5211-5224.
54. Moghaddam, M. F., D. F. Grant, J. M. Cheek, J. F. Greene, K. C. Williamson, and B. D. Hammock. 1997. Bioactivation of leukotoxins to their toxic diols by epoxide hydrolase. Nat. Med. 3: 562-566. (Pubitemid 27198657)
55. Zheng, J., C. G. Plopper, J. Lakritz, D. H. Storms, and B. D. Hammock. 2001. Leukotoxin-diol: a putative toxic mediator involved in acute respiratory distress syndrome. Am. J. Respir. Cell Mol. Biol. 25: 434-438. (Pubitemid 33037675)
56. Wang, Y. X., A. Ulu, L. N. Zhang, and B. Hammock. 2010. Soluble epoxide hydrolase in atherosclerosis. Curr. Atheroscler. Rep. 12: 174-183.
57. Schmelzer, K. R., L. Kubala, J. W. Newman, I. H. Kim, J. P. Eiserich, and B. D. Hammock. 2005. Soluble epoxide hydrolase is a therapeutic target for acute inflammation. Proc. Natl. Acad. Sci. USA. 102: 9772-9777. (Pubitemid 40993644)
58. Deng, Y., M. L. Edin, K. N. Theken, R. N. Schuck, G. P. Flake, M. A. Kannon, L. M. DeGraff, F. B. Lih, J. Foley, J. A. Bradbury, et al. 2011. Endothelial CYP epoxygenase overexpression and soluble epoxide hydrolase disruption attenuate acute vascular inflammatory responses in mice. FASEB J. 25: 703-713.
59. Liu, J. Y., J. Yang, B. Inceoglu, H. Qiu, A. Ulu, S. H. Hwang, N. Chiamvimonvat, and B. D. Hammock. 2010. Inhibition of soluble epoxide hydrolase enhances the anti-inflammatory effects of aspirin and 5-lipoxygenase activation protein inhibitor in a murine model. Biochem. Pharmacol. 79: 880-887.
60. Inceoglu, B., S. L. Jinks, K. R. Schmelzer, T. Waite, I. H. Kim, and B. D. Hammock. 2006. Inhibition of soluble epoxide hydrolase reduces LPS-induced thermal hyperalgesia and mechanical allodynia in a rat model of inflammatory pain. Life Sci. 79: 2311-2319. (Pubitemid 44666069)
61. Zhao, X., T. Yamamoto, J. W. Newman, I. H. Kim, T. Watanabe, B. D. Hammock, J. Stewart, J. S. Pollock, D. M. Pollock, and J. D. Imig. 2004. Soluble epoxide hydrolase inhibition protects the kidney from hypertension-induced damage. J. Am. Soc. Nephrol. 15: 1244-1253. (Pubitemid 38526005)
62. Tsai, H. J., S. H. Hwang, C. Morisseau, J. Yang, P. D. Jones, T. Kasagami, I. H. Kim, and B. D. Hammock. 2010. Pharmacokinetic screening of soluble epoxide hydrolase inhibitors in dogs. Eur. J. Pharm. Sci. 40: 222-238.
63. Ulu, A., S. Appt, C. Morisseau, S. H. Hwang, P. D. Jones, T. E. Rose, H. Dong, J. Lango, J. Yang, H. J. Tsai, et al. 2012. Pharmacokinetics and in vivo potency of soluble epoxide hydrolase inhibitors in cynomolgus monkeys. Br. J. Pharmacol. 165:1401-1412.