The role of marine omega-3 (n-3) fatty acids in inflammatory processes, atherosclerosis and plaque stability

Molecular Nutrition and Food Research

Volumn 56, Issue 7, 2012, Pages 1073-1080

  Calder, Philip C ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Cytokine; Docosahexaenoic acid; Eicosanoid; Eicosapentaenoic acid; Inflammation

Indexed keywords

AUTACOID; FISH OIL; NONSTEROID ANTIINFLAMMATORY AGENT; OMEGA 3 FATTY ACID;

ANIMAL; AQUATIC SPECIES; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CHEMISTRY; DRUG ANTAGONISM; FUNCTIONAL FOOD; HUMAN; IMMUNOLOGY; METABOLISM; REVIEW; VASCULAR ENDOTHELIUM;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; AQUATIC ORGANISMS; ATHEROSCLEROSIS; ENDOTHELIUM, VASCULAR; FATTY ACIDS, OMEGA-3; FISH OILS; FUNCTIONAL FOOD; HUMANS; INFLAMMATION MEDIATORS; PLAQUE, ATHEROSCLEROTIC;

EID: 84863542201     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201100710     Document Type: Review

References (74)

1. Glass, C. K., Witztum, J. L., Atherosclerosis: the road ahead. Cell 2001, 104, 503-516.
2. Ross, R., Mechanisms of disease - atherosclerosis - an inflammatory disease. N. Eng. J. Med. 1999, 340, 115-126.
3. Blake, G. J., Ridker, P. M., Novel clinical markers of vascular wall inflammation. Circ. Res. 2001, 89, 763-771.
4. Hansson, G. K., Inflammation, atherosclerosis, and coronary heart disease. N. Eng. J. Med. 2005, 352, 1685-1695.
5. Hallenbeck, J. M., Hansson, G. K., Becker, K. J. Immunology of ischemic vascular disease: plaque to attack. Trends Immunol. 2005, 26, 550-556.
6. Ridker, P. M., Buring, J. E., Rifai, N., Soluble P-selectin and the risk of future cardiovascular events. Circulation 2001, 103, 491-495
7. Ridker, P. M., Hennekens, C. H., Roitman-Johnson, B., Stampfer, M. J. et al., Plasma concentration of soluble intercellular adhesion molecule 1 and risks of future myocardial infarction in apparently healthy men. Lancet 1998, 351, 88-92.
8. Hwang, S. J., Ballantyne, C. M., Sharrett, A. R., Smith, L. C. et al., Circulating adhesion molecules VCAM-1, ICAM-1, and E-selectin in carotid atherosclerosis and incident coronary heart disease cases: the Atherosclerosis Risk in Communities (ARIC) study. Circulation 1997, 96, 4219-4225.
9. Ridker, P. M., Rifai, N., Stampfer, M. J., Hennekens, C. H., Plasma concentration of interleukin-6 and the risk of future myocardial infarction among apparently healthy men. Circulation 2000, 101, 1767-1772.
10. Calder, P. C., Burdge, G. C., in: Nicolaou, A., Kokotos, G. (Eds.), Bioactive Lipids The Oily Press, Bridgewater 2004, pp. 1-36.
11. Lee, T. H., Hoover, R. L., Williams, J. D., Sperling, R. I. et al., Effects of dietary enrichment with eicosapentaenoic acid and docosahexaenoic acid on in vitro neutrophil and monocyte leukotriene generation and neutrophil function. N. Eng. J. Med. 1985, 312, 1217-1224.
12. Endres, S., Ghorbani, R., Kelley, V. E., Georgilis, K. et al., The effect of dietary supplementation with n-3 polyunsaturated fatty acids on the synthesis of interleukin-1 and tumor necrosis factor by mononuclear cells. N. Eng. J. Med. 1989, 320, 265-271.
13. Sperling, R. I., Benincaso, A. I., Knoell, C. T., Larkin, J. K. et al., Dietary ω-3 polyunsaturated fatty acids inhibit phosphoinositide formation and chemotaxis in neutrophils. J. Clin. Invest. 1993, 91, 651-660.
14. Gibney, M. J., Hunter, B., The effects of short- and long-term supplementation with fish oil on the incorporation of n-3 polyunsaturated fatty acids into cells of the immune system in healthy volunteers. Eur. J. Clin. Nutr. 1993, 47, 255-259.
15. Caughey, G. E., Mantzioris, E., Gibson, R. A., Cleland, L. G. et al., The effect on human tumor necrosis factor α and interleukin 1β production of diets enriched in n-3 fatty acids from vegetable oil or fish oil. Am. J. Clin. Nutr. 1996, 63, 116-122.
16. Yaqoob, P., Pala, H. S., Cortina-Borja, M., Newsholme, E. A. et al., Encapsulated fish oil enriched in α-tocopherol alters plasma phospholipid and mononuclear cell fatty acid compositions but not mononuclear cell functions. Eur. J. Clin. Invest. 2000, 30, 260-274.
17. Healy, D. A., Wallace, F. A., Miles, E. A., Calder, P. C. et al., The effect of low to moderate amounts of dietary fish oil on neutrophil lipid composition and function. Lipids 2000, 35, 763-768.
18. Thies, F., Nebe-von-Caron, G., Powell, J. R., Yaqoob, P. et al., Dietary supplementation with γ-linolenic acid or fish oil decreases T lymphocyte proliferation in healthy older humans. J. Nutr. 2001, 131, 1918-1927.
19. Kew, S., Banerjee, T., Minihane, A. M., Finnegan, Y. E. et al., Relation between the fatty acid composition of peripheral blood mononuclear cells and measures of immune cell function in healthy, free-living subjects aged 25-72 y. Am. J. Clin. Nutr. 2003, 77, 1278-1286.
20. Miles, E. A., Banerjee, T., Calder, P. C., The influence of different combinations of gamma-linolenic, stearidonic and eicosapentaenoic acids on the fatty acid composition of blood lipids and mononuclear cells in human volunteers. Prost. Leuk. Essent. Fatty Acids 2004, 70, 529-538.
21. Kew, S., Mesa, M. D., Tricon, S., Buckley, R. et al., Effects of oils rich in eicosapentaenoic and docosahexaenoic acids on immune cell composition and function in healthy humans. Am. J. Clin. Nutr. 2004, 79, 674-681.
22. Rees, D., Miles, E. A., Banerjee, T., Wells, S. J. et al., Dose-related effects of eicosapentaenoic acid on innate immune function in healthy humans: a comparison of young and older men. Am. J. Clin. Nutr. 2006, 83, 331-342.
23. Lewis, R. A., Austen, K. F., Soberman, R. J., Leukotrienes and other products of the 5-lipoxygenase pathway: biochemistry and relation to pathobiology in human diseases. N. Eng. J. Med. 1990, 323, 645-655.
24. Tilley, S. L., Coffman, T. M., Koller, B. H., Mixed messages: modulation of inflammation and immune responses by prostaglandins and thromboxanes. J. Clin. Invest. 2001, 108, 15-23.
25. Calder, P. C., Polyunsaturated fatty acids and inflammatory processes: new twists in an old tale. Biochimie 2009, 91, 791-795.
26. Faber, J., Berkhout, M., Vos, A. P., Sijben, J. W. et al., Supplementation with a fish oil-enriched, high-protein medical food leads to rapid incorporation of EPA into white blood cells and modulates immune responses within one week in healthy men and women. J. Nutr. 2011, 141, 964-970.
27. Calder, P. C., N-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am. J. Clin. Nutr. 2006, 83, 1505S-1519S.
28. Calder, P. C., The relationship between the fatty acid composition of immune cells and their function. Prostaglandins Leukot. Essent. Fatty Acids 2008, 79, 101-108.
29. Calder, P. C., Fatty acids and inflammation: the cutting edge between food and pharma. Eur. J. Pharmacol. 2011, 618, S50-S58.
30. Meydani, S. N., Endres, S., Woods, M. M., Goldin, B. R. et al., Oral (n-3) fatty acid supplementation suppresses cytokine production and lymphocyte proliferation: comparison between young and older women. J. Nutr. 1991, 121, 547-555.
31. Von Schacky, C., Kiefl, R., Jendraschak, E., Kaminski, W. E., N-3 fatty acids and cysteinyl-leukotriene formation in humans in vitro, ex vivo and in vivo. J. Lab. Clin. Med. 1993, 121, 302-309.
32. Wada, M., DeLong, C. J., Hong, Y. H., Rieke, C. J. et al., Enzymes and receptors of prostaglandin pathways with arachidonic acid-derived versus eicosapentaenoic acid-derived substrates and products. J. Biol. Chem. 2007, 282, 22254-22266.
33. Tull, S. P., Yates, C. M., Maskrey, B. H., O'Donnell, V. B. et al., Omega-3 fatty acids and inflammation: novel interactions reveal a new step in neutrophil recruitment. PLoS Biol. 2009, 7, e1000177.
34. Serhan, C. N., Clish, C. B., Brannon, J., Colgan, S. P. et al., Novel functional sets of lipid-derived mediators with anti-inflammatory actions generated from omega-3 fatty acids via cyclooxygenase 2-nonsteroidal anti-inflammatory drugs and transcellular processing. J. Exp. Med. 2000, 192, 1197-1204.
35. Serhan, C. N., Hong, S., Gronert, K., Colgan, S. P. et al., Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter pro-inflammation signals. J. Exp. Med. 2002, 196, 1025-1037.
36. Serhan, C. N., Chiang, N., van Dyke, T. E., Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 2008, 8, 349-361.
37. Schmidt, E. B., Pedersen, J. O., Ekelund, S., Grunnet, N. et al., Cod liver oil inhibits neutrophil and monocyte chemotaxis in healthy males. Atherosclerosis 1989, 77, 53-57.
38. Schmidt, E. B., Varming, K., Pedersen, J. O., Lervang, H. H. et al., Long term supplementation with n-3 fatty acids. ii. Effect on neutrophil and monocyte chemotaxis. Scand. J. Clin. Lab. Invest. 1992, 52, 229-236.
39. Luostarinen, R., Siegbahn, A., Saldeen, T., Effect of dietary fish oil supplemented with different doses of vitamin E on neutrophil chemotaxis in healthy volunteers. Nutr. Res. 1992, 12, 1419-1430.
40. Kumar, A., Takada, Y., Boriek, A. M., Aggarwal, B. B., Nuclear factor-kappaB: its role in health and disease. J. Mol. Med. 2004, 82, 434-448.
41. Sigal, L. H., Basic science for the clinician 39: NF-kappaB-function, activation, control, and consequences. J. Clin. Rheumatol. 2006, 12, 207-211.
42. Lo, C. J., Chiu, K. C., Fu, M., Lo, R., Helton, S., Fish oil decreases macrophage tumor necrosis factor gene transcription by altering the NFκB activity. J. Surg. Res. 1999, 82, 216-222.
43. Babcock, T. A., Novak, T., Ong, E., Jho, D. H. et al., Modulation of lipopolysaccharide-stimulated macrophage tumor necrosis factor-α production by ω-3 fatty acid is associated with differential cyclooxygenase-2 protein expression and is independent of interleukin-10. J. Surg. Res. 2002, 107, 135-139.
44. Novak, T. E., Babcock, T. A., Jho, D. H., Helton, W. S. et al., NF-κB inhibition by ω-3 fatty acids modulates LPS-stimulated macrophage TNF-α transcription. Am. J. Physiol. 2003, 284, L84-L89.
45. Zhao, Y., Joshi-Barve, S., Barve, S., Chen, L. H., Eicosapentaenoic acid prevents LPS-induced TNF-α expression by preventing NF-κB activation. J. Am. Coll. Nutr. 2004, 23, 71-78.
46. De Caterina, R., Cybulsky, M. I., Clinton, S. K., Gimbrone, M. A. et al., The omega-3 fatty acid docosahexaenoate reduces cytokine-induced expression of proatherogenic and proinflammatory proteins in human endothelial cells. Arterioscler. Thromb. 1994, 14, 1829-1836.
47. Weber, C., Erl, W., Pietsch, A., Danesch, U. et al., Docosahexaenoic acid selectively attenuates induction of vascular cell adhesion molecule-1 and subsequent monocytic cell adhesion to human endothelilal cells stimulated by tumor necrosis factor-α. Atheroscler. Thromb. Vasc. Biol. 1995, 15, 622-628.
48. Collie-Duguid, E. S., Wahle, K. W., Inhibitory effect of fish oil n-3 polyunsaturated fatty acids on the expression of endothelial cell adhesion molecules. Biochem. Biophys. Res. Commun. 1996, 220, 969-974.
49. Hughes, D. A., Southon, S., Pinder, A. C., (n-3) Polyunsaturated fatty acids modulate the expression of functionally associated molecules on human monocytes in vitro. J. Nutr. 1996, 126, 603-610.
50. Miles, E. A., Wallace, F. A., Calder, P. C., Dietary fish oil reduces intercellular adhesion molecule 1 and scavenger receptor expression on murine macrophages. Atherosclerosis 2000, 152, 43-50.
51. De Caterina, R., Libby, P., Control of endothelial leukocyte adhesion molecules by fatty acids. Lipids 1996, 31, S57-S63.
52. Yates, C. M., Tull, S. P., Madden, J., Calder, P. C. et al., Docosahexaenoic acid inhibits the adhesion of flowing neutrophils to cytokine stimulated human umbilical vein endothelial cells. J. Nutr. 2011, 141, 1331-1334.
53. Hughes, D. A., Pinder, A. C., Piper, Z., Johnson, I. T. et al., Fish oil supplementation inhibits the expression of major histocompatibility complex class II molecules and adhesion molecules on human monocytes. Am. J. Clin. Nutr. 1996, 63, 267-272.
54. Miles, E. A., Thies, F., Wallace, F. A., Powell, J. R. et al., Influence of age and dietary fish oil on plasma soluble adhesion molecule concentrations. Clin. Sci. 2001, 100, 91-100.
55. Khalfoun, B., Thibault, F., Watier, H., Bardos, P. et al., Docosahexaenoic and eicosapentaenoic acids inhibit in vitro human endothelial cell production of interleukin-6. Adv. Exp. Biol. Med. 1997, 400, 589-597.
56. Billiar, T. R., Bankey, P. E., Svingen, B. A. Curran, R. D. et al., Fatty acid uptake and Kupffer Cell function: fish oil alters eicosanoid and monokine production to endotoxin stimulation. Surgery 1988, 104, 343-349.
57. Renier, G., Skamene, E., de Sanctis, J., Radzioch, D., Dietary n-3 polyunsaturated fatty acids prevent the development of atherosclerotic lesions in mice: modulation of macrophage secretory activities. Arterioscler. Thomb. 1993, 13, 1515-1524.
58. Yaqoob, P., Calder, P. C., Effects of dietary lipid manipulation upon inflammatory mediator production by murine macrophages. Cell. Immunol. 1995, 163, 120-128.
59. Baumann, K. H., Hessel, F., Larass, I., Muller, T. et al., Dietary ω-3, ω-6, and ω-9 unsaturated fatty acids and growth factor and cytokine gene expression in unstimulated and stimulated monocytes. Arterioscler. Thromb. Vasc. Biol. 1999, 19, 59-66.
60. Trebble, T., Arden, N. K., Stroud, M. A., Wootton, S. A. et al., Inhibition of tumour necrosis factor-α and interleukin-6 production by mononuclear cells following dietary fish-oil supplementation in healthy men and response to antioxidant co-supplementation. Brit. J. Nutr. 2003, 90, 405-412.
61. Burr, M. L., Gilbert, J. F., Holliday, R. M., Elwood, P. C. et al., Effects of changes in fat, fish and fibre intake on death and myocardial reinfarction: diet and reinfarction trial (DART). Lancet 1989, ii, 757-761.
62. Siscovick, D. S., Raghunathan, T. E., King, I., Weinmann, S. et al., Dietary intake and cell membrane levels of long-chain n-3 polyunsaturated fatty acids and the risk of primary cardiac arrest. J. Am. Med. Assoc. 1995, 274, 1363-1367.
63. Anonymous. Dietary supplementation with n-3 polyunsaturated fatty acids and vitamin E after myocardial infarction: results of the GISSI-Prevenzione trial. Lancet 1999, 354, 447-455.
64. Hu, F. B., Bronner, L., Willett, W. C., Stampfer, M. J. et al., Fish and omega-3 fatty acid intake and risk of coronary heart disease in women. J. Am. Med. Assoc. 2002, 287, 1815-1821
65. Lemaitre, R. N., King, I. B., Mozaffarian, D., Kuller, L. H. et al., n-3 Polyunsaturated fatty acids, fatal ischemic heart disease, and nonfatal myocardial infarction in older adults: the Cardiovascular Health Study. Am. J. Clin. Nutr. 2003, 77, 319-325.
66. Yokoyama, M., Origasa, H., Matsuzaki, M., Matsuzawa, Y. et al., Japan EPA lipid intervention study (JELIS) investigators. Effects of eicosapentaenoic acid on major coronary events in hypercholesterolaemic patients (JELIS): a randomised open-label, blinded endpoint analysis. Lancet 2007, 369, 1090-1098.
67. Albert, C. M., Campos, H., Stampfer, M. J., Ridker, P. M. et al., Blood levels of long-chain n-3 fatty acids and the risk of sudden death. N. Eng. J. Med. 2002, 346, 1113-1118.
68. Plutzky, J., Atherosclerotic plaque rupture: emerging insights and opportunities. Am. J. Cardiol. 1999, 84, 15J-20J.
69. Stary, H. C., Chander, A. B., Dinsmore, R. E., The definition of advanced type of atherosclerotic lesions and a histological classification of atherosclerosis. Circulation 1995, 92, 1355-1374.
70. Thies, F., Garry, J. M. C., Yaqoob, P., Rerkasem, K. et al., Association of n-3 polyunsaturated fatty acids with stability of atherosclerotic plaques: a randomised controlled trial. Lancet 2003, 361, 477-485.
71. Cawood, A. L., Ding, R., Napper, F. L., Young, R. H. et al., Eicosapentaenoic acid (EPA) from highly concentrated n-3 fatty acid ethyl esters is incorporated into advanced atherosclerotic plaques and higher plaque EPA is associated with decreased plaque inflammation and increased stability. Atherosclerosis 2010, 212, 252-259.
72. Matsumoto, M., Sata, M., Fukuda, D., Tanaka, K. et al., Orally administered eicosapentaenoic acid reduces and stabilizes atherosclerotic lesions in ApoE-deficient mice. Atherosclerosis 2008, 197, 524-533.
73. Calder, P. C., n-3 Fatty acids and cardiovascular disease: evidence explained and mechanisms explored. Clin. Sci. 2004, 107, 1-11.
74. Saravanan, P., Davidson, N. C., Schmidt, E. B., Calder, P. C., Cardiovascular effects of marine omega-3 fatty acids. Lancet 2010, 376, 540-550.