Critical role of COX-1 in prostacyclin production by human endothelial cells under modification of hydroperoxide tone

FASEB Journal

Volumn 23, Issue 2, 2009, Pages 605-612

  Bolego, Chiara ^a,c   Buccellati, Carola ^a   Prada, Alberto ^b   Gaion, Rosa Maria ^c   Folco, Giancarlo ^a   Sala, Angelo ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b RHO HOSPITAL   (Italy)

^c UNIVERSITY OF PADOVA   (Italy)

Author keywords

12 HpETE; COX 2 heterodimers; Isoprostanes; Prostaglandin; Selective cyclooxygenase inhibitors

Indexed keywords

12 HYDROPEROXY EICOSATETRAENOIC ACID; 4 [5 (4 CHLOROPHENYL) 3 TRIFLUOROMETHYL 1H PYRAZOL 1 YL]BENZENESULFONAMIDE; 5 (4 CHLOROPHENYL) 1 (4 METHOXYPHENYL) 3 TRIFLUOROMETHYL 1H PYRAZOLE; ARACHIDONIC ACID; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; ENZYME INHIBITOR; FR 122047; GLUTATHIONE; HETERODIMER; HYDROPEROXIDE; ICOSATETRAENOIC ACID; INTERLEUKIN 1BETA; ISOPROSTANE; PROSTACYCLIN; UNCLASSIFIED DRUG;

ARTICLE; ASSAY; ENDOTHELIUM CELL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; THROMBOCYTE ACTIVATION;

ARACHIDONIC ACID; CELLS, CULTURED; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYCLOOXYGENASE INHIBITORS; ENDOTHELIAL CELLS; EPOPROSTENOL; GLUTATHIONE; HUMANS; HYDROGEN PEROXIDE; ISOENZYMES; LEUKOTRIENES; PROTEIN MULTIMERIZATION;

EID: 59649128513     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-106591     Document Type: Article

References (39)

1. Smith, W. L., and Song, I. (2002) The enzymology of prostaglandin endoperoxide H synthases-1 and -2. Prostaglandins Other Lipid Medial 69, 115-128
2. Caughey, G. E., Cleland, L. G., Penglis, P. S., Gamble, J. R., and James, M. J. (2001) Roles of cyclooxygenase (COX)-1 and COX-2 in prostanoid production by human endothelial cells: selective up-regulation of prostacyclin synthesis by COX-2. J. Immunol. 167, 2831-2838
3. Mitchell, J. A., and Warner, T. D. (2006) COX isoforms in the cardiovascular system: understanding the activities of non-steroidal anti-inflammatory drugs. Nat. Rev. Drug Discov. 5, 75-86
4. Shimizu, T., Ohto, T., and Kita, Y. (2006) Cytosolic phospholipase A2: biochemical properties and physiological roles. IUBMB Life 58, 328-333
5. Karim, S., Habib, A., Levy-Toledano, S., and Maclouf, J. (1996) Cyclooxygenase-1 and -2 of endothelial cells utilize exogenous or endogenous arachidonic acid for transcellular production of thromboxane. J. Biol. Chem. 271, 12042-12048
6. Camacho, M., Lopez-Belmonte, J., and Vila, L. (1998) Rate of vasoconstrictor prostanoids released by endothelial cells depends on cyclooxygenase-2 expression and prostaglandin I synthase activity. Circ. Res. 83, 353-365
7. Folco, G., and Murphy, R. C. (2006) Eicosanoid transcellular biosynthesis: from cell-cell interactions to in vivo tissue responses. Pharmacol. Rev. 58, 375-388
8. Kulmacz, R. J. (1998) Cellular regulation of prostaglandin H synthase catalysis. FEBS Lett. 430, 154-157
9. Davidge, S. T. (2001) Prostaglandin H synthase and vascular function. Circ. Res. 89, 650-660
10. Okahara, K., Sun, B., and Kambayashi, J. (1998) Upregulation of prostacyclin synthesis-related gene expression by shear stress in vascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 18, 1922-1926
11. James, M. J., Penglis, P. S., Caughey, G. E., Demasi, M., and Cleland, L. G. (2001) Eicosanoid production by human monocytes: does COX-2 contribute to a self-limiting inflammatory response? Inflamm. Res. 50, 249-253
12. Topper, J. N., Cai, J., Falb, D., and Gimbrone, M. A., Jr. (1996) Identification of vascular endothelial genes differentially responsive to fluid mechanical stimuli: cyclooxygenase-2, manganese superoxide dismutase, and endothelial cell nitric oxide synthase are selectively up-regulated by steady laminar shear stress. Proc. Natl. Acad. Sci. U. S. A. 93, 10417-10422
13. McAdam, B. F., Catella-Lawson, F., Mardini, I. A., Kapoor, S., Lawson, J. A., and FitzGerald, G. A. (1999) Systemic biosynthesis of prostacyclin by cyclooxygenase (COX)-2: the human pharmacology of a selective inhibitor of COX-2. Proc. Natl. Acad. Sci. U. S. A. 96, 272-277
14. Flavahan, N. A. (2007) Balancing prostanoid activity in the human vascular system. Trends Pharmacol. Sci. 28, 106 -110
15. Zidar, N., Dolenc-Strazar, Z., Jeruc, J., Jerse, M., Balazic, J., Gartner, U., Jermol, U., Zupanc, T., and Stajer, D. (2007) Expression of cyclooxygenase-1 and cyclooxygenase-2 in the normal human heart and in myocardial infarction. Cardiovasc. Pathol. 16, 300-304
16. Radi, Z. A., and Ostroski, R. (2007) Pulmonary and cardiorenal cyclooxygenase-1 (COX-1), -2 (COX-2), and microsomal prostaglandin E synthase-1 (mPGES-1) and -2 (mPGES-2) expression in a hypertension model. Mediators Inflamm. 2007, 85091
17. Yu, Y., Fan, J., Chen, X. S., Wang, D., Klein-Szanto, A. J., Campbell, R. L., FitzGerald, G. A., and Funk, C. D. (2006) Genetic model of selective COX2 inhibition reveals novel heterodimer signaling. Nat. Med. 12, 699-704
18. Patrignani, P., Panara, M. R., Greco, A., Fusco, O., Natoli, C., Iacobelli, S., Cipollone, F., Ganci, A., Creminon, C., Maclouf, J., and Patrono, C. (1994) Biochemical and pharmacological characterization of the cyclooxygenase activity of human blood prostaglandin endoperoxide synthases. J. Pharmacol. Exp. Ther. 271, 1705-1712
19. Habib, A., Creminon, C., Frobert, Y., Grassi, J., Pradelles, P., and Maclouf, J. (1993) Demonstration of an inducible cyclooxygenase in human endothelial cells using antibodies raised against the carboxyl-terminal region of the cyclooxygenase-2. J. Biol. Chem. 268, 23448-23454
20. Habib, A., Martinuzzo, M. E., Carreras, L. O., Levy-Toledano, S., and Maclouf, J. (1995) Increased expression of inducible cyclooxygenase-2 in human endothelial cells by antiphospholipid antibodies. Thromb. Haemost. 74, 770-777
21. Penning, T. D., Talley, J. J., Bertenshaw, S. R., Carter, J. S., Collins, P. W., Docter, S., Graneto, M. J., Lee, L. F., Malecha, J. W., Miyashiro, J. M., Rogers, R. S., Rogier, D. J., Yu, S. S., Anderson, G. D., Burton, E. G., Cogburn, J. N., Gregory, S. A., Koboldt, C. M., Perkins, W. E., Seibert, K., Veenhuizen, A. W., Zhang, Y. Y., and Isakson, P. C. (1997) Synthesis and biological evaluation of the 1,5-diarylpyrazole class of cyclooxygenase-2 inhibitors: identification of 4-[5-(4-methylphenyl)-3-(trifluoro-methyl)-1H- pyrazol-1-yl]benze nesulfonamide (SC-58635, celecoxib). J. Med. Chem. 40, 1347-1365
22. Ochi, T., Motoyama, Y., and Goto, T. (2000) The analgesic effect profile of FR122047, a selective cyclooxygenase-1 inhibitor, in chemical nociceptive models. Eur. J. Pharmacol. 391, 49 -54
23. Chen, W., Pawelek, T. R., and Kulmacz, R. J. (1999) Hydroperoxide dependence and cooperative cyclooxygenase kinetics in prostaglandin H synthase-1 and -2. J. Biol. Chem. 274, 20301-20306
24. Shitashige, M., Morita, I., and Murota, S. (1998) Different substrate utilization between prostaglandin endoperoxide H synthase-1 and -2 in NIH3T3 fibroblasts. Biochim. Biophys. Acta 1389, 57-66
25. Coffey, M. J., Jarvis, G. E., Gibbins, J. M., Coles, B., Barrett, N. E., Wylie, O. R., and O'Donnell, V. B. (2004) Platelet 12-lipoxygenase activation via glycoprotein VI: involvement of multiple signaling pathways in agonist control of HpETE synthesis. Circ. Res. 94, 1598-1605
26. Kokura, S., Wolf, R. E., Yoshikawa, T., Granger, D. N., and Aw, T. Y. (1999) Molecular mechanisms of neutrophil-endothelial cell adhesion induced by redox imbalance. Circ. Res. 84, 516 -524
27. Mitchell, J. A., Lucas, R., Vojnovic, I., Hasan, K., Pepper, J. R., and Warner, T. D. (2006) Stronger inhibition by nonsteroid anti-inflammatory drugs of cyclooxygenase-1 in endothelial cells than platelets offers an explanation for increased risk of thrombotic events. FASEB J. 20, 2468-2475
28. Bolego, C., Buccellati, C., Radaelli, T., Cetin, I., Puglisi, L., Folco, G., and Sala, A. (2006) eNOS, COX-2, and prostacyclin production are impaired in endothelial cells from diabetics. Biochem. Biophys. Res. Commun. 339, 188 -190
29. Warner, T. D., Vojnovic, I., Bishop-Bailey, D., and Mitchell, J. A. (2006) Influence of plasma protein on the potencies of inhibitors of cyclooxygenase-1 and -2. FASEB J. 20, 542-544
30. Pepicelli, O., Fedele, E., Berardi, M., Raiteri, M., Levi, G., Greco, A., Ajmone-Cat, M. A., and Minghetti, L. (2005) Cyclo-oxygenase-1 and -2 differently contribute to prostaglandin E2 synthesis and lipid peroxidation after in vivo activation of N-methyl-D-aspartate receptors in rat hippocampus. J. Neurochem. 93, 1561-1567
31. Kurumbail, R. G., Stevens, A. M., Gierse, J. K., McDonald, J. J., Stegeman, R. A., Pak, J. Y., Gildehaus, D., Miyashiro, J. M., Penning, T. D., Seibert, K., Isakson, P. C., and Stallings, W. C. (1996) Structural basis for selective inhibition of cyclooxygenase-2 by anti-inflammatory agents. Nature 384, 644-648
32. Picot, D., Loll, P. J., and Garavito, R. M. (1994) The X-ray crystal structure of the membrane protein prostaglandin H2 synthase-1. Nature 367, 243-249
33. Swinney, D. C., Mak, A. Y., Barnett, J., and Ramesha, C. S. (1997) Differential allosteric regulation of prostaglandin H synthase 1 and 2 by arachidonic acid. J. Biol. Chem. 272, 12393-12398
34. 2 in mixed incubations of endothelial cells and aspirin-treated platelets strongly depends on the prostaglandin I-synthase activity. Thromb. Res. 99, 155-164
35. Riendeau, D., Guay, J., Weech, P. K., Laliberte, F., Yergey, J., Li, C., Desmarais, S., Perrier, H., Liu, S., Nicoll-Griffith, D., and et al. (1994) Arachidonyl trifluoromethyl ketone, a potent inhibitor of 85-kDa phospholipase A2, blocks production of arachidonate and 12-hydroxyeicosatetraenoic acid by calcium ionophore-challenged platelets. J. Biol. Chem. 269, 15619-15624
36. Smith, W. L., DeWitt, D. L., and Garavito, R. M. (2000) Cyclooxygenases: structural, cellular, and molecular biology. Annu. Rev. Biochem. 69, 145-182
37. Nugteren, D. H. (1975) Arachidonate lipoxygenase in blood platelets. Biochim. Biophys. Acta 380, 299-307
38. Siegel, M. I., McConnell, R. T., Porter, N. A., and Cuatrecasas, P. (1980) Arachidonate metabolism via lipoxygenase and 12L-hydroperoxy-5,8,10,14- icosatetraenoic acid peroxidase sensitive to anti-inflammatory drugs. Proc. Natl. Acad. Sci. U. S. A. 77, 308-312
39. Kulmacz, R. J., and Wang, L. H. (1995) Comparison of hydroperoxide initiator requirements for the cyclooxygenase activities of prostaglandin H synthase-1 and -2. J. Biol. Chem. 270, 24019-24023