Exogenous modification of platelet membranes with the omega-3 fatty acids EPA and DHA reduces platelet procoagulant activity and thrombus formation

American Journal of Physiology - Cell Physiology

Volumn 304, Issue 3, 2013, Pages

  Larson, Mark K ^a   Tormoen, Garth W ^b   Weaver, Lucinda J ^a   Luepke, Kristen J ^a   Patel, Ishan A ^b   Hjelmen, Carl E ^a   Ensz, Nicole M ^a   McComas, Leah S ^a   McCarty, Owen J T ^b  

^a AUGUSTANA COLLEGE   (United States)

^b Oregon Health and Science University Department of Biomedical Engineering   (United States)

Author keywords

Cardiovascular disease; Coagulation; Fibrin; Thrombin

Indexed keywords

DOCOSAHEXAENOIC ACID; FIBRIN; ICOSAPENTAENOIC ACID; PHOSPHATIDYLSERINE; PROCOAGULANT; THROMBIN;

ARTICLE; BLOOD CLOTTING; CATALYSIS; CONTROLLED STUDY; DIETARY INTAKE; FEMALE; FLOW CYTOMETRY; HUMAN; HYPOTHESIS; IN VITRO STUDY; MALE; PRIORITY JOURNAL; THROMBOCYTE MEMBRANE; WESTERN BLOTTING;

BLOOD COAGULATION; BLOOD PLATELETS; CELL MEMBRANE; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; FATTY ACIDS, OMEGA-3; FEMALE; HUMANS; MALE; PHOSPHATIDYLSERINES; PLATELET AGGREGATION; THROMBIN; THROMBOSIS;

EID: 84873379827     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00174.2012     Document Type: Article

References (33)

1. Berny MA, Munnix IC, Auger JM, Schols SE, Cosemans JM, Panizzi P, Bock PE, Watson SP, McCarty OJ, Heemskerk JW. Spatial distribution of factor Xa, thrombin, and fibrin(ogen) on thrombi at venous shear. PLos One 5: e10415, 2010.
2. Berny MA, Patel IA, White-Adams TC, Simonson P, Gruber A, Rugonyi S, McCarty OJ. Rational design of an ex vivo model of thrombosis. Cell Mol Bioeng 3: 187-189, 2010.
3. Buckwalter JA, Blythe WB, Brinkhous KM. Effect of blood platelets on prothrombin utilization of dog and human plasmas. Am J Physiol 159: 316-321, 1949.
4. Chen P, Vericel E, Lagarde M, Guichardant M. Poxytrins, a class of oxygenated products from polyunsaturated fatty acids, potently inhibit blood platelet aggregation. FASEB J 25: 382-388, 2011.
5. De Caterina R. n-3 fatty acids in cardiovascular disease. N Engl J Med 364: 2439-2450, 2011.
6. Din JN, Harding SA, Valerio CJ, Sarma J, Lyall K, Riemersma RA, Newby DE, Flapan AD. Dietary intervention with oil rich fish reduces platelet-monocyte aggregation in man. Atherosclerosis 197: 290-296, 2008.
7. Dona M, Fredman G, Schwab JM, Chiang N, Arita M, Goodarzi A, Cheng G, von Andrian UH, Serhan CN. Resolvin E1, an EPA-derived mediator in whole blood, selectively counterregulates leukocytes and platelets. Blood 112: 848-855, 2008.
8. Driss F, Vericel E, Lagarde M, Dechavanne M, Darcet P. Inhibition of platelet aggregation and thromboxane synthesis after intake of small amount of eicosapentaenoic acid. Thromb Res 36: 389-396, 1984.
9. Falati S, Gross P, Merrill-Skoloff G, Furie BC, Furie B. Real-time in vivo imaging of platelets, tissue factor and fibrin during arterial thrombus formation in the mouse. Nat Med 8: 1175-1181, 2002.
10. Fredman G, Van Dyke TE, Serhan CN. Resolvin E1 regulates adeno-sine diphosphate activation of human platelets. Arterioscler Thromb Vasc Biol 30: 2005-2013, 2010.
11. Geleijnse JM, Giltay EJ, Grobbee DE, Donders AR, Kok FJ. Blood pressure response to fish oil supplementation: metaregression analysis of randomized trials. J Hypertens 20: 1493-1499, 2002.
12. Guillot N, Caillet E, Laville M, Calzada C, Lagarde M, Vericel E. Increasing intakes of the long-chain omega-3 docosahexaenoic acid: effects on platelet functions and redox status in healthy men. FASEB J 23: 2909-2916, 2009.
13. Harris WS. Expert opinion: omega-3 fatty acids and bleeding-cause for concern? Am J Cardiol 99: 44C-46C, 2007.
14. Haynes LM, Dubief YC, Mann KG. Membrane binding events in the initiation and propagation phases of tissue factor-initiated zymogen activation under flow. J Biol Chem 287: 5225-5234, 2012.
15. Itakura A, Verbout NG, Phillips KG, Insall RH, Gailani D, Tucker EI, Gruber A, McCarty OJ. Activated factor XI inhibits chemotaxis of polymorphonuclear leukocytes. J Leukoc Biol 90: 923-927, 2011.
16. Larson MK, Ashmore JH, Harris KA, Vogelaar JL, Pottala JV, Sprehe M, Harris WS. Effects of omega-3 acid ethyl esters and aspirin, alone and in combination, on platelet function in healthy subjects. Thromb Haemost 100: 634-641, 2008.
17. Larson MK, Shearer GC, Ashmore JH, Anderson-Daniels JM, Graslie EL, Tholen JT, Vogelaar JL, Korth AJ, Nareddy V, Sprehe M, Harris WS. Omega-3 fatty acids modulate collagen signaling in human platelets. Prostaglandins Leukot Essent Fatty Acids 84: 93-98, 2011.
18. Leaf A, Kang JX, Xiao YF, Billman GE. Clinical prevention of sudden cardiac death by n-3 polyunsaturated fatty acids and mechanism of prevention of arrhythmias by n-3 fish oils. Circulation 107: 2646-2652, 2003.
19. Li XL, Steiner M. Fish oil: a potent inhibitor of platelet adhesiveness. Blood 76: 938-945, 1990.
20. Locke D, Chen H, Liu Y, Liu C, Kahn ML. Lipid rafts orchestrate signaling by the platelet receptor glycoprotein VI. J Biol Chem 277: 18801-18809, 2002.
21. Lopes SM, Trimbo SL, Mascioli EA, Blackburn GL. Human plasma fatty acid variations and how they are related to dietary intake. Am J Clin Nutr 53: 628-637, 1991.
22. Marchioli R, Barzi F, Bomba E, Chieffo C, Di Gregorio D, Di Mascio R, Franzosi MG, Geraci E, Levantesi G, Maggioni AP, Mantini L, Marfisi RM, Mastrogiuseppe G, Mininni N, Nicolosi GL, Santini M, Schweiger C, Tavazzi L, Tognoni G, Tucci C, Valagussa F. Early protection against sudden death by n-3 polyunsaturated fatty acids after myocardial infarction: time-course analysis of the results of the Gruppo Italiano per lo Studio della Sopravvivenza nell'Infarto Miocardico (GISSI)-Prevenzione. Circulation 105: 1897-1903, 2002.
23. Miletich JP, Jackson CM, Majerus PW. Interaction of coagulation factor Xa with human platelets. Proc Natl Acad Sci USA 74: 4033-4036, 1977.
24. Monroe DM, Hoffman M, Roberts HR. Platelets and thrombin generation. Arterioscler Thromb Vasc Biol 22: 1381-1389, 2002.
25. Mozaffarian D, Gottdiener JS, Siscovick DS. Intake of tuna or other broiled or baked fish versus fried fish and cardiac structure, function, and hemodynamics. Am J Cardiol 97: 216-222, 2006.
26. Mozaffarian D, Wu JH. Omega-3 fatty acids and cardiovascular disease: effects on risk factors, molecular pathways, and clinical events. J Am Coll Cardiol 58: 2047-2067, 2011.
27. Pepe S, McLennan PL. Cardiac membrane fatty acid composition modulates myocardial oxygen consumption and postischemic recovery of contractile function. Circulation 105: 2303-2308, 2002.
28. Schwertz H, Koster S, Kahr WH, Michetti N, Kraemer BF, Weitz DA, Blaylock RC, Kraiss LW, Greinacher A, Zimmerman GA, Weyrich AS. Anucleate platelets generate progeny. Blood 115: 3801-3809, 2010.
29. Tracy PB, Nesheim ME, Mann KG. Coordinate binding of factor Va and factor Xa to the unstimulated platelet. J Biol Chem 256: 743-751, 1981.
30. Vanschoonbeek K, Feijge MA, Paquay M, Rosing J, Saris W, Kluft C, Giesen PL, de Maat MP, Heemskerk JW. Variable hypocoagulant effect of fish oil intake in humans: modulation of fibrinogen level and thrombin generation. Arterioscler Thromb Vasc Biol 24: 1734-1740, 2004.
31. White-Adams TC, Berny MA, Patel IA, Tucker EI, Gailani D, Gruber A, McCarty OJ. Laminin promotes coagulation and thrombus formation in a factor XII-dependent manner. J Thromb Haemost 8: 1295-1301, 2010.
32. Wood JP, Silveira JR, Maille NM, Haynes LM, Tracy PB. Prothrombin activation on the activated platelet surface optimizes expression of pro-coagulant activity. Blood 117: 1710-1718, 2011.
33. Zucker ML, Bilyeu DS, Helmkamp GM, Harris WS, Dujovne CA. Effects of dietary fish oil on platelet function and plasma lipids in hyperlipo-proteinemic and normal subjects. Atherosclerosis 73: 13-22, 1988.