Fish-oil supplementation alters numbers of circulating endothelial progenitor cells and microparticles independently of eNOS genotype

American Journal of Clinical Nutrition

Volumn 100, Issue 5, 2014, Pages 1232-1243

  Wu, Szu Yun ^a   Mayneris Perxachs, Jordi ^a   Lovegrove, Julie A ^a   Todd, Susan ^a   Yaqoob, Parveen ^a  

^a UNIVERSITY OF READING   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FISH OIL; GLUCOSE; LIPID; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PLACEBO; TRIACYLGLYCEROL; BIOLOGICAL MARKER; GLUCOSE BLOOD LEVEL; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; NOS3 PROTEIN, HUMAN; OMEGA 3 FATTY ACID;

ADULT; AGED; ARTICLE; BLOOD PRESSURE; BLOOD SAMPLING; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CONTROLLED STUDY; CROSSOVER PROCEDURE; DIET SUPPLEMENTATION; DIETARY INTAKE; DOUBLE BLIND PROCEDURE; ENDOTHELIAL MICROPARTICLE; ENDOTHELIAL PROGENITOR CELL; FEMALE; FLOW CYTOMETRY; GENOTYPE; GLUCOSE BLOOD LEVEL; HUMAN; LIPID BLOOD LEVEL; LIPID COMPOSITION; MAJOR CLINICAL STUDY; MALE; PLATELET MICROPARTICLE; RANDOMIZED CONTROLLED TRIAL; TONOMETRY; TRIACYLGLYCEROL BLOOD LEVEL; BLOOD; CARDIOVASCULAR DISEASES; DRUG EFFECTS; GENETIC POLYMORPHISM; GENETICS; MEMBRANE MICROPARTICLE; METABOLISM; MIDDLE AGED; PROSPECTIVE STUDY; RISK FACTOR; THROMBOCYTE; YOUNG ADULT;

ADULT; AGED; BIOLOGICAL MARKERS; BLOOD GLUCOSE; BLOOD PLATELETS; BLOOD PRESSURE; CARDIOVASCULAR DISEASES; CELL-DERIVED MICROPARTICLES; CHOLESTEROL, HDL; CHOLESTEROL, LDL; DIETARY SUPPLEMENTS; DOUBLE-BLIND METHOD; ENDOTHELIAL PROGENITOR CELLS; FATTY ACIDS, OMEGA-3; FEMALE; FISH OILS; GENOTYPE; HUMANS; MALE; MIDDLE AGED; NITRIC OXIDE SYNTHASE TYPE III; POLYMORPHISM, GENETIC; PROSPECTIVE STUDIES; RISK FACTORS; TRIGLYCERIDES; YOUNG ADULT;

EID: 84908127765     PISSN: 00029165     EISSN: 19383207     Source Type: Journal    
DOI: 10.3945/ajcn.114.088880     Document Type: Article

References (49)

1. Lekakis J, Abraham P, Balbarini A, Blann A, Boulanger CM, Cockcroft J, Cosentino F, Deanfield J, Gallino A, Ikonomidis I, et al. Methods for evaluating endothelial function: a position statement from the European Society of Cardiology Working Group on Peripheral Circulation. Eur J Cardiovasc Prev Rehabil 2011;18:775-89.
2. Burger D, Touyz RM. Cellular biomarkers of endothelial health: microparticles, endothelial progenitor cells, and circulating endothelial cells. J Am Soc Hypertens 2012;6:85-99.
3. Sabatier F, Camoin-Jau L, Anfosso F, Sampol J, Dignat-George F. Circulating endothelial cells, microparticles and progenitors: key players towards the definition of vascular competence. J Cell Mol Med 2009;13:454-71.
4. Nozaki T, Sugiyama S, Koga H, Sugamura K, Ohba K, Matsuzawa Y, Sumida H, Matsui K, Jinnouchi H, Ogawa H. Significance of a multiple biomarkers strategy including endothelial dysfunction to improve risk stratification for cardiovascular events in patients at high risk for coronary heart disease. J Am Coll Cardiol 2009;54:601-8.
5. Kunz GA, Liang G, Cuculoski F, Gregg D, Vata KC, Shaw LK, Goldschmidt-Clermont PJ, Dong CM, Taylor DA, Peterson ED. Circulating endothelial progenitor cells predict coronary artery disease severity. Am Heart J 2006;152:190-5 (Published erratum appears in Am Heart J 2006;152:776.).
6. Werner N, Kosiol S, Schiegl T, Ahlers P, Walenta K, Link A, Bohm M, Nickenig G. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med 2005;353:999-1007.
7. Vafeiadou K, Weech M, Sharma V, Yaqoob P, Todd S, Williams CM, Jackson KG, Lovegrove JA. A review of the evidence for the effects of total dietary fat, saturated, monounsaturated and n-6 polyunsaturated fatty acids on vascular function, endothelial progenitor cells and microparticles. Br J Nutr 2012;107:303-24.
8. Egert S, Stehle P. Impact of n-3 fatty acids on endothelial function: results from human interventions studies. Curr Opin Clin Nutr Metab Care 2011;14:121-31.
9. Wang Q, Liang XH, Wang LY, Lu XF, Huang JF, Cao J, Li HF, Gu DF. Effect of omega-3 fatty acids supplementation on endothelial function: a meta-analysis of randomized controlled trials. Atherosclerosis 2012;221:536-43.
10. Casas JP, Cavalleri GL, Bautista LE, Smeeth L, Humphries SE, Hingorani AD. Endothelial nitric oxide synthase gene polymorphisms and cardiovascular disease: a HuGE review. Am J Epidemiol 2006;164:921-35.
11. Thompson AK, Newens KJ, Jackson KG, Wright J, Williams CM. Glu298Asp polymorphism influences the beneficial effects of fish oil fatty acids on postprandial vascular function. J Lipid Res 2012;53:2205-13.
12. Ferguson JF, Phillips CM, McMonagle J, Perez-Martinez P, Shaw DI, Lovegrove JA, Helal O, Defoort C, Gjelstad IMF, Drevon CA, et al. NOS3 gene polymorphisms are associated with risk markers of cardiovascular disease, and interact with omega-3 polyunsaturated fatty acids. Atherosclerosis 2010;211:539-44.
13. Wilson PW, D'Agostino RB, Levy D, Belanger AM, Silbershatz H, Kannel WB. Prediction of coronary heart disease using risk factor categories. Circulation 1998;97:1837-47.
14. Chong MF, George TW, Alimbetov D, Jin YN, Weech M, Macready AL, Spencer JPE, Kennedy OB, Minihane AM, Gordon MH, et al. Impact of the quantity and flavonoid content of fruits and vegetables on markers of intake in adults with an increased risk of cardiovascular disease: the FLAVURS trial. Eur J Nutr 2013;52:361-78.
15. Weech M, Vafeiadou K, Hasaj M, Todd S, Yaqoob P, Jackson KG, Lovegrove JA. Development of a food-exchange model to replace saturated fat with MUFAs and n-6 PUFAs in adults at moderate cardiovascular risk. J Nutr 2014;144:846-55.
16. Paradossi U, Ciofini E, Clerico A, Botto N, Biagini A, Colombo MG. Endothelial function and carotid intima-media thickness in young healthy subjects among endothelial nitric oxide synthase Glu(298)-> Asp and T-786 -> C polymorphisms. Stroke 2004;35:1305-9.
17. Treasure T, MacRae KD. Minimisation: the platinum standard for trials? Randomisation doesn't guarantee similarity of groups; minimisation does. BMJ 1998;317:362-3.
18. Mulligan AA, Luben RN, Bhaniani A, Parry-Smith DJ, O'Connor L, Khawaja AP, Forouhi NG, Khaw KT. A new tool for converting food frequency questionnaire data into nutrient and food group values: FETA research methods and availability. BMJ Open 2014;4:e004503.
19. Rizos EC, Ntzani EE, Bika E, Kostapanos MS, Elisaf MS. Association between omega-3 fatty acid supplementation and risk of major cardiovascular disease events a systematic review and meta-analysis. JAMA 2012;308:1024-33.
20. Kwak SM, Myung SK, Lee YJ, Seo HG, Grp KM-AS. Efficacy of omega-3 fatty acid supplements (eicosapentaenoic acid and docosahexaenoic acid) in the secondary prevention of cardiovascular disease a meta-analysis of randomized, double-blind, placebo-controlled trials. Arch Intern Med 2012;172:686-94.
21. Delgado-Lista J, Perez-Martinez P, Lopez-Miranda J, Perez-Jimenez F. Long chain omega-3 fatty acids and cardiovascular disease: a systematic review. Br J Nutr 2012;107:S201-13.
22. Balk EM, Lichtenstein AH, Chung M, Kupelnick B, Chew P, Lau J. Effects of omega-3 fatty acids on serum markers of cardiovascular disease risk: a systematic review. Atherosclerosis 2006;189:19-30.
23. Mozaffarian D, Geelen A, Brouwer IA, Geleijnse JM, Zock PL, Katan MB. Effect of fish oil on heart rate in humans - A meta-analysis of randomized controlled trials. Circulation 2005;112:1945-52.
24. Hall WL. Dietary saturated and unsaturated fats as determinants of blood pressure and vascular function. Nutr Res Rev 2009;22:18-38.
25. Paradossi U, Ciofini E, Clerico A, Botto N, Biagini A, Colombo MG. Endothelial function and carotid intima-media thickness in young healthy subjects among endothelial nitric oxide synthase Glu298->Asp and T-786->C polymorphisms. Stroke 2004;35:1305-9.
26. Skulas-Ray AC, Kris-Etherton PM, Harris WS, Heuvel JPV, Wagner PR, West SG. Dose-response effects of omega-3 fatty acids on triglycerides, inflammation, and endothelial function in healthy persons with moderate hypertriglyceridemia. Am J Clin Nutr 2011;93:243-52.
27. Devaraj S, Chien A, Rao B, Chen XP, Jialal I. Modulation of endothelial progenitor cell number and function with n-3 polyunsaturated fatty acids. Atherosclerosis 2013;228:94-7.
28. Turgeon J, Dussault S, Maingrette F, Groleau J, Haddad P, Perez G, Rivard A. Fish oil-enriched diet protects against ischemia by improving angiogenesis, endothelial progenitor cell function and post-natal neovascularization. Atherosclerosis 2013;229:295-303.
29. Wong CY, Yiu KH, Li SW, Lee S, Tam S, Lau CP, Tse HF. Fish-oil supplement has neutral effects on vascular and metabolic function but improves renal function in patients with type 2 diabetes mellitus. Diabet Med 2010;27:54-60.
30. Case J, Mead LE, Bessler WK, Prater D, White HA, Saadatzadeh MR, Bhavsar JR, Yoder MC, Haneline LS, Ingram DA. Human CD34(+)AC133(+)VEGFR-2(+) cells are not endothelial progenitor cells but distinct, primitive hematopoietic progenitors. Exp Hematol 2007;35:1109-18.
31. Fatini C, Sticchi E, Cesari F, Gori AM, Cioni G, De Stefano M, Bertoni E, Paudice N, Salvadori M, Zanazzi M, et al. Relationship among endothelial response to hyperemia, bone marrow-derived progenitor cells, and parathyroid hormone in renal transplantation. Transplantation 2012;93:835-41.
32. Aicher A, Heeschen C, Mildner-Rihm C, Urbich C, Ihling C, Technau-Ihling K, Zeiher AM, Dimmeler S. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 2003;9:1370-6.
33. Bodin S, Welch MD. Plasma membrane organization is essential for balancing competing pseudopod- and uropod-promoting signals during neutrophil polarization and migration. Mol Biol Cell 2005;16:5773-83.
34. Balakumar P, Taneja G. Fish oil and vascular endothelial protection: bench to bedside. Free Radic Biol Med 2012;53:271-9.
35. Zhang HF, Wang L, Yuan HJ, Ma YH, Wang YF, Hu ZY, Su Y, Zhao ZG. PPAR-gamma agonist pioglitazone prevents apoptosis of endothelial progenitor cells from rat bone marrow. Cell Biol Int 2013;37:430-5.
36. Gensch C, Clever YP, Werner C, Hanhoun M, Bohm M, Laufs U. The PPAR-gamma agonist pioglitazone increases neoangiogenesis and prevents apoptosis of endothelial progenitor cells. Atherosclerosis 2007;192:67-74.
37. Chiva-Blanch G, Condines X, Magraner E, Roth I, Valderas-Martinez P, Arranz S, Casas R, Martinez-Huelamo M, Vallverdu-Queralt A, Quifer-Rada P, et al. The non-alcoholic fraction of beer increases stromal cell derived factor 1 and the number of circulating endothelial progenitor cells in high cardiovascular risk subjects: a randomized clinical trial. Arterioscler Thromb Vasc Biol 2014;233:518-24.
38. Morel O, Jesel L, Hugel B, Douchet MP, Zupan M, Chauvin M, Freyssinet JM, Toti F. Protective effects of vitamin C on endothelium damage and platelet activation during myocardial infarction in patients with sustained generation of circulating microparticles. J Thromb Haemost 2003;1:171-7.
39. Esposito K, Ciotola M, Giugliano D. Pioglitazone reduces endothelial microparticles in the metabolic syndrome. Arterioscl Throm Vas Biol 2006;26:1926-7.
40. Del Turco S, Basta G, Lazzerini G, Evangelista M, Rainaldi G, Tanganelli P, Christensen JH, Schmidt EB, De Caterina R. Effect of the administration of n-3 polyunsaturated fatty acids on circulating levels of microparticles in patients with a previous myocardial infarction. Haematologica 2008;93:892-9.
41. Zucker ML, Bilyeu DS, Helmkamp GM, Harris WS, Dujovne CA. Effects of dietary fish oil on platelet-function and plasma-lipids in hyperlipoproteinemic and normal subjects. Atherosclerosis 1988;73:13-22.
42. Yokoyama M, Origasa H, Matsuzaki M, Matsuzawa Y, Saito Y, Ishikawa Y, Oikawa S, Sasaki J, Hishida H, Itakura H, et al. Effects of eicosapentaenoic acid on major coronary events in hypercholesterolaemic patients (JELIS): a randomised openlabel, blinded endpoint analysis. Lancet 2007;369:1090-8.
43. Marchioli R, Barzi F, Bomba E, Chieffo C, Di Gregorio D, Di Mascio R, Franzosi MG, Geraci E, Levantesi G, Maggioni AP, et al. 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 2002;105:1897-903.
44. Pot GK, Brouwer IA, Enneman A, Rijkers GT, Kampman E, Geelen A. No effect of fish oil supplementation on serum inflammatory markers and their interrelationships: a randomized controlled trial in healthy, middle-aged individuals. Eur J Clin Nutr 2009;63:1353-9.
45. Chrysohoou C, Panagiotakos DB, Pitsavos C, Antoniades C, Skoumas J, Brown M, Stefanadis C. Evidence for association between endothelial nitric oxide synthase gene polymorphism (G894T) and inflammatory markers: the ATTICA study. Am Heart J 2004;148:733-8.
46. Antoniades C, Tousoulis D, Vasiliadou C, Pitsavos C, Chrysochoou C, Panagiotakos D, Tentolouris C, Marinou K, Koumallos N, Stefanadis C. Genetic polymorphism on endothelial nitric oxide synthase affects endothelial activation and inflammatory response during the acute phase of myocardial infarction. J Am Coll Cardiol 2005;46:1101-9.
47. Moon J, Yoon S, Kim E, Shin C, Jo SA, Jo I. Lack of evidence for contribution of Glu298Asp (G894T) polymorphism of endothelial nitric oxide synthase gene to plasma nitric oxide levels. Thromb Res 2002;107:129-34.
48. Li R, Lyn D, Lapu-Bula R, Oduwole A, Igho-Pemu P, Lankford B, Morgan A, Nkemdechi S, Liu G, Pack C, et al. Relation of endothelial nitric oxide synthase gene to plasma nitric oxide level, endothelial function, and blood pressure in African Americans. Am J Hypertens 2004;17:560-7.
49. Xin W, Wei W, Li X. Effect of fish oil supplementation on fasting vascular endothelial function in humans: a meta-analysis of randomized controlled trials. PLoS One 2012;7:e46028.