Human platelets generate phospholipid-esterified prostaglandins via cyclooxygenase-1 that are inhibited by low dose aspirin supplementation

Journal of Lipid Research

Volumn 54, Issue 11, 2013, Pages 3085-3097

  Aldrovandi, Maceler ^a   Hammond, Victoria J ^a   Podmore, Helen ^b   Hornshaw, Martin ^b   Clark, Stephen R ^a   Marnett, Lawrence J ^c   Slatter, David A ^a   Murphy, Robert C ^d   Collins, Peter W ^a   O'Donnell, Valerie B ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b Thermo Fisher Scientific   (United States)

^c VANDERBILT INGRAM CANCER CENTER   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Atherosclerosis; Oxidized phospholipids; PGE2 D2 PEs

Indexed keywords

ACETYLSALICYLIC ACID; CALCIUM; COLLAGEN; CYCLOOXYGENASE 1; CYTOSOLIC PHOSPHOLIPASE A2; IONOPHORE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLETHANOLAMINE; PHOSPHOLIPASE C; PHOSPHOLIPID; PROSTAGLANDIN; PROSTAGLANDIN D2; PROSTAGLANDIN E2; PROTEIN TYROSINE KINASE; THROMBIN;

ARTICLE; AUTOCRINE EFFECT; CALCIUM CELL LEVEL; CHEMICAL STRUCTURE; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME MECHANISM; ESTERIFICATION; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; LIPID OXIDATION; LOW DRUG DOSE; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; PROTEIN EXPRESSION; TANDEM MASS SPECTROMETRY; THROMBOCYTE ACTIVATION;

ATHEROSCLEROSIS; OXIDIZED PHOSPHOLIPIDS; PGE2/D2-PES;

ASPIRIN; BLOOD PLATELETS; CALCIUM; CYCLOOXYGENASE 1; CYCLOOXYGENASE INHIBITORS; DINOPROSTONE; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTERIFICATION; FEEDBACK, PHYSIOLOGICAL; HUMANS; INTRACELLULAR SPACE; MAP KINASE KINASE 1; PHOSPHATIDYLETHANOLAMINES; PHOSPHOLIPIDS; PLATELET ACTIVATION; PROSTAGLANDIN D2; PROSTAGLANDINS; PROTEIN KINASE C; RECEPTOR, PAR-1; SRC-FAMILY KINASES; THROMBIN;

EID: 84886061837     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M041533     Document Type: Article

References (29)

1. Kozak, K. R., S. W. Rowlinson, and L. J. Marnett. 2000. Oxygenation of the endocannabinoid, 2-arachidonylglycerol, to glyceryl prostaglandins by cyclooxygenase-2. J. Biol. Chem. 275: 33744-33749.
2. Kozak, K. R., B. C. Crews, J. D. Morrow, L. H. Wang, Y. H. Ma, R. Weinander, P. J. Jakobsson, and L. J. Marnett. 2002. Metabolism of the endocannabinoids, 2-arachidonylglycerol and anandamide, into prostaglandin, thromboxane, and prostacyclin glycerol esters and ethanolamides. J. Biol. Chem. 277: 44877-44885. (Pubitemid 36159083)
3. Hammond, V. J., A. H. Morgan, S. Lauder, C. P. Thomas, S. Brown, B. A. Freeman, C. M. Lloyd, J. Davies, A. Bush, A. L. Levonen, et al. 2012. Novel keto-phospholipids are generated by monocytes and macrophages, detected in cystic fibrosis, and activate peroxisome proliferator-activated receptor-gamma. J. Biol. Chem. 287: 41651-41666.
4. Nirodi, C. S., B. C. Crews, K. R. Kozak, J. D. Morrow, and L. J. Marnett. 2004. The glyceryl ester of prostaglandin E2 mobilizes calcium and activates signal transduction in RAW264.7 cells. Proc. Natl. Acad. Sci. USA. 101: 1840-1845. (Pubitemid 38228978)
5. Podrez, E. A., E. Poliakov, Z. Shen, R. Zhang, Y. Deng, M. Sun, P. J. Finton, L. Shan, M. Febbraio, D. P. Hajjar, et al. 2002. A novel family of atherogenic oxidized phospholipids promotes macrophage foam cell formation via the scavenger receptor CD36 and is enriched in atherosclerotic lesions. J. Biol. Chem. 277: 38517-38523. (Pubitemid 35154710)
6. Watson, A. D., N. Leitinger, M. Navab, K. F. Faull, S. Horkko, J. L. Witztum, W. Palinski, D. Schwenke, R. G. Salomon, W. Sha, et al. 1997. Structural identification by mass spectrometry of oxidized phospholipids in minimally oxidized low density lipoprotein that induce monocyte/endothelial interactions and evidence for their presence in vivo. J. Biol. Chem. 272: 13597-13607. (Pubitemid 27224791)
7. Bochkov, V. N., O. V. Oskolkova, K. G. Birukov, A. L. Levonen, C. J. Binder, and J. Stockl. 2010. Generation and biological activities of oxidized phospholipids. Antioxid. Redox Signal. 12: 1009-1059.
8. O'Donnell, V. B., and R. C. Murphy. 2012. New families of bioactive oxidized phospholipids generated by immune cells: identification and signaling actions. Blood. 120: 1985-1992.
9. Clark, S. R., C. J. Guy, M. J. Scurr, P. R. Taylor, A. P. Kift-Morgan, V. J. Hammond, C. P. Thomas, B. Coles, G. W. Roberts, M. Eberl, et al. 2011. Esterified eicosanoids are acutely generated by 5-lipoxygenase in primary human neutrophils and in human and murine infection. Blood. 117: 2033-2043.
10. Maskrey, B. H., A. Bermudez-Fajardo, A. H. Morgan, E. Stewart-Jones, V. Dioszeghy, G. W. Taylor, P. R. Baker, B. Coles, M. J. Coffey, H. Kuhn, et al. 2007. Activated platelets and monocytes generate four hydroxyphosphatidylethanolamines via lipoxygenase. J. Biol. Chem. 282: 20151-20163. (Pubitemid 47100012)
11. Morgan, A. H., V. Dioszeghy, B. H. Maskrey, C. P. Thomas, S. R. Clark, S. A. Mathie, C. M. Lloyd, H. Kuhn, N. Topley, B. C. Coles, et al. 2009. Phosphatidylethanolamine-esterified eicosanoids in the mouse: tissue localization and inflammation-dependent formation in Th-2 disease. J. Biol. Chem. 284: 21185-21191.
12. Morgan, A. H., V. J. Hammond, L. Morgan, C. P. Thomas, K. A. Tallman, Y. R. Garcia-Diaz, C. McGuigan, M. Serpi, N. A. Porter, R. C. Murphy, et al. 2010. Quantitative assays for esterified oxylipins generated by immune cells. Nat. Protoc. 5: 1919-1931.
13. Morgan, L. T., C. P. Thomas, H. Kuhn, and V. B. O'Donnell. 2010. Thrombin-activated human platelets acutely generate oxidized docosahexaenoic-acid-containing phospholipids via 12-lipoxygenase. Biochem. J. 431: 141-148.
14. Thomas, C. P., L. T. Morgan, B. H. Maskrey, R. C. Murphy, H. Kuhn, S. L. Hazen, A. H. Goodall, H. A. Hamali, P. W. Collins, and V. B. O'Donnell. 2010. Phospholipid-esterified eicosanoids are generated in agonist-activated human platelets and enhance tissue factor-dependent thrombin generation. J. Biol. Chem. 285: 6891-6903.
15. Hutchins, P. M., and R. C. Murphy. 2012. Cholesteryl ester acyl oxidation and remodeling in murine macrophages: formation of oxidized phosphatidylcholine. J. Lipid Res. 53: 1588-1597.
16. Brose, S. A., B. T. Thuen, and M. Y. Golovko. 2011. LC/MS/MS method for analysis of E(2) series prostaglandins and isoprostanes. J. Lipid Res. 52: 850-859.
17. Marnett, L. J., P. H. Siedlik, R. C. Ochs, W. R. Pagels, M. Das, K. V. Honn, R. H. Warnock, B. E. Tainer, and T. E. Eling. 1984. Mechanism of the stimulation of prostaglandin H synthase and prostacyclin synthase by the antithrombotic and antimetastatic agent, nafazatrom. Mol. Pharmacol. 26: 328-335. (Pubitemid 15157520)
18. Odenwaller, R., Y. N. Chen, and L. J. Marnett. 1990. Preparation and proteolytic cleavage of apoprostaglandin endoperoxide synthase. Methods Enzymol. 187: 479-485. (Pubitemid 20309313)
19. Rowlinson, S. W., B. C. Crews, C. A. Lanzo, and L. J. Marnett. 1999. The binding of arachidonic acid in the cyclooxygenase active site of mouse prostaglandin endoperoxide synthase-2 (COX-2). A putative L-shaped binding conformation utilizing the top channel region. J. Biol. Chem. 274: 23305-23310.
20. Murphy, R. C. Mass Spectrometry of Phospholipids: Tables of Molecular and Product Ions. Denver: Illiminated Press 2002.
21. Boutaud, O., C. J. Brame, R. G. Salomon, L. J. Roberts 2nd, and J. A. Oates. 1999. Characterization of the lysyl adducts formed from prostaglandin H2 via the levuglandin pathway. Biochemistry. 38: 9389-9396.
22. Salomon, R., D. B. Miller, S. R. Raychaudhuri, K. Avasthi, K. Lal, and B. S. Levison. 1984. Asymmetric total synthesis of levuglandin E2. J. Am. Chem. Soc. 106: 8296-8298.
23. Montrucchio, G., G. Alloatti, and G. Camussi. 2000. Role of platelet-activating factor in cardiovascular pathophysiology. Physiol. Rev. 80: 1669-1699.
24. Yamashita, A., T. Sugiura, and K. Waku. 1997. Acyltransferases and transacylases involved in fatty acid remodeling of phospholipids and metabolism of bioactive lipids in mammalian cells. J. Biochem. 122: 1-16. (Pubitemid 27346216)
25. Lewin, T. M., C. G. Van Horn, S. K. Krisans, and R. A. Coleman. 2002. Rat liver acyl-CoA synthetase 4 is a peripheral-membrane protein located in two distinct subcellular organelles, peroxisomes, and mitochondrial-associated membrane. Arch. Biochem. Biophys. 404: 263-270. (Pubitemid 34913557)
26. Gerrard, J. M., J. G. White, G. H. Rao, and D. Townsend. 1976. Localization of platelet prostaglandin production in the platelet dense tubular system. Am. J. Pathol. 83: 283-298.
27. Chi, Y., J. Min, J. F. Jasmin, M. P. Lisanti, Y. T. Chang, and V. L. Schuster. 2011. Development of a high-affinity inhibitor of the prostaglandin transporter. J. Pharmacol. Exp. Ther. 339: 633-641.
28. Greenberg, M. E., X. M. Li, B. G. Gugiu, X. Gu, J. Qin, R. G. Salomon, and S. L. Hazen. 2008. The lipid whisker model of the structure of oxidized cell membranes. J. Biol. Chem. 283: 2385-2396.
29. Wong-Ekkabut, J., Z. Xu, W. Triampo, I. M. Tang, D. P. Tieleman, and L. Monticelli. 2007. Effect of lipid peroxidation on the properties of lipid bilayers: a molecular dynamics study. Biophys. J. 93: 4225-4236. (Pubitemid 350294470)