Marine omega-3 fatty acids and inflammatory processes: Effects, mechanisms and clinical relevance

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1851, Issue 4, 2015, Pages 469-484

  Calder, Philip C ^a,b,c  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY HOSPITAL SOUTHAMPTON NHS FOUNDATION TRUST   (United Kingdom)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

Cytokine; Eicosanoid; Inflammation; Lymphocyte; Macrophage; Resolvin

Indexed keywords

ARACHIDONIC ACID; BINDING PROTEIN; CELL ADHESION MOLECULE; CYTOCHROME P450; DOCOSAHEXAENOIC ACID; ENDOCANNABINOID; FATTY ACID; G PROTEIN COUPLED RECEPTOR 120; ICOSANOID; ICOSAPENTAENOIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOXYGENASE; MATRIX METALLOPROTEINASE; MEMBRANE PHOSPHOLIPID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROSTAGLANDIN SYNTHASE; THROMBOCYTE ACTIVATING FACTOR; ANTIINFLAMMATORY AGENT; AUTACOID; OMEGA 3 FATTY ACID; PHOSPHOLIPID;

ASTHMA; CELL MEMBRANE; CROHN DISEASE; DIET SUPPLEMENTATION; DRUG EFFICACY; GENE ACTIVATION; GENE EXPRESSION; GENETIC CODE; HUMAN; INFLAMMATION; LIPID COMPOSITION; LIPID RAFT; MEMBRANE DAMAGE; META ANALYSIS (TOPIC); NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RHEUMATOID ARTHRITIS; TH1 CELL; ULCERATIVE COLITIS; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALIA;

ANIMALS; ANTI-INFLAMMATORY AGENTS; FATTY ACIDS, OMEGA-3; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; LYMPHOCYTE ACTIVATION; PHOSPHOLIPIDS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84922553466     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2014.08.010     Document Type: Review

References (229)

1. P.C. Calder Omega-3 polyunsaturated fatty acids and inflammatory processes: nutrition or pharmacology? Br. J. Clin. Pharmacol. 75 2013 645 662
2. P.C. Calder n-3 fatty acids, inflammation and immunity: new mechanisms to explain old actions Proc. Nutr. Soc. 72 2013 326 336
3. G.C. Burdge, and P.C. Calder Dietary α-linolenic acid and health-related outcomes: a metabolic perspective Nutr. Res. Rev. 19 2006 26 52
4. British Nutrition Foundation Briefing Paper: N-3 Fatty Acids and Health 1999 British Nutrition Foundation London
5. B.J. Meyer, N.J. Mann, J.L. Lewis, G.C. Milligan, A.J. Sinclair, and P.R. Howe Dietary intakes and food sources of omega - 6 and omega-3 polyunsaturated fatty acids Lipids 38 2003 391 398
6. P.C. Calder The relationship between the fatty acid composition of immune cells and their function Prostaglandins Leukot. Essent. Fat. Acids 79 2008 101 108
7. P.C. Calder, J.A. Bond, D.J. Harvey, S. Gordon, and E.A. Newsholme Uptake and incorporation of saturated and unsaturated fatty acids into macrophage lipids and their effect upon macrophage adhesion and phagocytosis Biochem. J. 269 1990 807 814
8. P.C. Calder, P. Yaqoob, D.J. Harvey, A. Watts, and E.A. Newsholme The incorporation of fatty acids by lymphocytes and the effect on fatty acid composition and membrane fluidity Biochem. J. 300 1994 509 518
9. L.D. Peterson, N.M. Jeffery, F. Thies, P. Sanderson, E.A. Newsholme, and P.C. Calder Eicosapentaenoic and docosahexaenoic acids alter rat spleen leukocyte fatty acid composition and prostaglandin E2 production but have different effects on lymphocyte functions and cell-mediated immunity Lipids 33 1998 171 180
10. R.S. Chapkin, C.C. Akoh, and C.C. Miller Influence of dietary n-3 fatty acids on macrophage glycerophospholipid molecular species and peptidoleukotriene synthesis J. Lipid Res. 32 1991 1205 1213
11. T.H. Lee, R.L. Hoover, J.D. Williams, R.I. Sperling, J. Ravalese III, B.W. Spur, D.R. Robinson, E.J. Corey, R.A. Lewis, and K.F. Austen Effects of dietary enrichment with eicosapentaenoic acid and docosahexaenoic acid on in vitro neutrophil and monocyte leukotriene generation and neutrophil function N. Engl. J. Med. 312 1985 1217 1224
12. S. Endres, R. Ghorbani, V.E. Kelley, K. Georgilis, G. Lonnemann, J.M.W. van der Meer, J.G. Cannon, T.S. Rogers, M.S. Klempner, P.C. Weber, E.J. Schaeffer, S.M. Wolff, and C.A. Dinarello 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. Engl. J. Med. 320 1989 265 271
13. R.I. Sperling, A.I. Benincaso, C.T. Knoell, J.K. Larkin, K.F. Austen, and D.R. Robinson Dietary w - 3 polyunsaturated fatty acids inhibit phosphoinositide formation and chemotaxis in neutrophils J. Clin. Investig. 91 1993 651 660
14. G.E. Caughey, E. Mantzioris, R.A. Gibson, L.G. Cleland, and M.J. James 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. 63 1996 116 122
15. P. Yaqoob, H.S. Pala, M. Cortina-Borja, E.A. Newsholme, and P.C. Calder Encapsulated fish oil enriched in α-tocopherol alters plasma phospholipid and mononuclear cell fatty acid compositions but not mononuclear cell functions Eur. J. Clin. Investig. 30 2000 260 274
16. D.A. Healy, F.A. Wallace, E.A. Miles, P.C. Calder, and P. Newsholme The effect of low to moderate amounts of dietary fish oil on neutrophil lipid composition and function Lipids 35 2000 763 768
17. F. Thies, G. Nebe-von-Caron, J.R. Powell, P. Yaqoob, E.A. Newsholme, and P.C. Calder Dietary supplementation with γ-linolenic acid or fish oil decreases T lymphocyte proliferation in healthy older humans J. Nutr. 131 2001 1918 1927
18. S. Kew, T. Banerjee, A.M. Minihane, Y.E. Finnegan, R. Muggli, R. Albers, C.M. Williams, and P.C. Calder Lack of effect of foods enriched with plant- or marine-derived n-3 fatty acids on human immune function Am. J. Clin. Nutr. 77 2003 1287 1295
19. S. Kew, M.D. Mesa, S. Tricon, R. Buckley, A.M. Minihane, and P. Yaqoob Effects of oils rich in eicosapentaenoic and docosahexaenoic acids on immune cell composition and function in healthy humans Am. J. Clin. Nutr. 79 2004 674 681
20. D. Rees, E.A. Miles, T. Banerjee, S.J. Wells, C.E. Roynette, K.W.J.W. Wahle, and P.C. Calder Dose-related effects of eicosapentaenoic acid on innate immune function in healthy humans: a comparison of young and older men Am. J. Clin. Nutr. 83 2006 331 342
21. J. Faber, M. Berkhout, A.P. Vos, J.W. Sijben, P.C. Calder, J. Garssen, and A. van Helvoort 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. 141 2011 964 970
22. L.M. Browning, C.G. Walker, A.P. Mander, A.L. West, J. Madden, J.M. Gambell, S. Young, L. Wang, S.A. Jebb, and P.C. Calder Incorporation of eicosapentaenoic and docosahexaenoic acids into lipid pools when given as supplements providing doses equivalent to typical intakes of oily fish Am. J. Clin. Nutr. 96 2012 748 758
23. R.A. Lewis, K.F. Austen, and R.J. Soberman Leukotrienes and other products of the 5-lipoxygenase pathway: biochemistry and relation to pathobiology in human diseases N. Engl. J. Med. 323 1990 645 655
24. S.L. Tilley, T.M. Coffman, and B.H. Koller Mixed messages: modulation of inflammation and immune responses by prostaglandins and thromboxanes J. Clin. Invest. 108 2001 15 23
25. D.L. Kroetz, and D.C. Zeldin Cytochrome P450 pathways of arachidonic acid metabolism Curr. Opin. Lipidol. 13 2002 273 283
26. P.C. Calder, N. Ahluwalia, R. Albers, N. Bosco, R. Bourdet-Sicard, D. Haller, S.T. Holgate, L.S. Jonsson, M.E. Latulippe, A. Marcos, J. Moreines, C. M'Rini, M. Muller, G. Pawelec, R.J.J. van Neerven, B. Watzl, and J. Zhao A consideration of biomarkers to be used for evaluation of inflammation in human nutritional studies Br. J. Nutr. 109 Suppl. 1 2013 S1 S34
27. P. Yaqoob, and P.C. Calder Effects of dietary lipid manipulation upon inflammatory mediator production by murine macrophages Cell. Immunol. 163 1995 120 128
28. S.N. Meydani, S. Endres, M.M. Woods, B.R. Goldin, C. Soo, A. Morrill-Labrode, C.A. Dinarello, and S.L. Gorbach Oral (n-3) fatty acid supplementation suppresses cytokine production and lymphocyte proliferation: comparison between young and older women J. Nutr. 121 1991 547 555
29. C. Von Schacky, R. Kiefl, E. Jendraschak, and W.E. Kaminski N-3 fatty acids and cysteinyl-leukotriene formation in humans in vitro, ex vivo and in vivo J. Lab. Clin. Med. 121 1993 302 309
30. T.M. Trebble, S.A. Wootton, E.A. Miles, M. Mullee, N.K. Arden, A.B. Ballinger, M.A. Stroud, and P.C. Calder Prostaglandin E2 production and T-cell function after fish-oil supplementation: response to antioxidant co-supplementation Am. J. Clin. Nutr. 78 2003 376 382
31. J.M. Kremer, J. Bigauoette, A.V. Michalek, M.A. Timchalk, L. Lininger, R.I. Rynes, C. Huyck, J. Zieminski, and L.E. Bartholomew Effects of manipulation of dietary fatty acids on manifestations of rheumatoid arthritis Lancet 8422 1985 184 187
32. J.M. Kremer, W. Jubiz, A. Michalek, R.I. Rynes, L.E. Bartholomew, J. Bigouette, M. Timchalk, D. Beller, and L. Lininger Fish-oil supplementation in active rheumatoid arthritis Ann. Intern. Med. 106 1987 497 503
33. L.G. Cleland, J.K. French, W.H. Betts, G.A. Murphy, and M.J. Elliot Clinical and biochemical effects of dietary fish oil supplements in rheumatoid arthritis J. Rheumatol. 15 1988 1471 1475
34. L.G. Cleland, G.E. Caughey, M.J. James, and S.M. Proudman Reduction of cardiovascular risk factors with long term fish oil treatment in early rheumatoid arthritis J. Rheumatol. 33 2006 1973 1979
35. J.E. Tullekan, P.C. Limburg, F.A.J. Muskiet, and M.H. van Rijswijk Vitamin E status during dietary fish oil supplementation in rheumatoid arthritis Arthritis Rheum. 33 1990 1416 1419
36. T.B. McCall, D. O'Leary, J. Bloomfield, and C.A. O'Morain Therapeutic potential of fish oil in the treatment of ulcerative colitis Aliment. Pharmacol. Ther. 3 1989 415 424
37. A.B. Hawthorne, T.K. Daneshmend, C.J. Hawkey, A. Belluzzi, S.J. Everitt, G.K. Holmes, C. Malkinson, M.Z. Shaheen, and J.E. Willars Treatment of ulcerative colitis with fish oil supplementation: a prospective 12 months randomised controlled trial Gut 33 1992 922 928
38. W.F. Stenson, D. Cort, J. Rodgers, R. Burakoff, K. DeSchryver-Kecskemeti, T.L. Gramlich, and W. Beeken Dietary supplementation with fish oil in ulcerative colitis Ann. Intern. Med. 116 1992 609 614
39. T. Shimizu, T. Fujii, R. Suzuki, J. Igarashi, Y. Ohtsuka, S. Nagata, and Y. Yamashiro Effects of highly purified eicosapentaenoic acid on erythrocyte fatty acid composition and leukocyte and colonic mucosa leukotriene B4 production in children with ulcerative colitis J. Pediatr. Gastroenterol. Nutr. 37 2003 581 585
40. T.M. Trebble, N.K. Arden, S.A. Wootton, P.C. Calder, M. Mullee, D.R. Fine, and M.A. Stroud Fish oil and antioxidants alter the composition and function of circulating mononuclear cells in Crohn's disease Am. J. Clin. Nutr. 80 2004 1137 1144
41. C.A. Hudert, K.H. Weylandt, Y. Lu, J. Wang, S. Hong, A. Dignass, C.N. Serhan, and J.X. Kang Transgenic mice rich in endogenous omega-3 fatty acids are protected from colitis Proc. Natl. Acad. Sci. U. S. A. 103 2006 11276 11281
42. D.W. Goldman, W.C. Pickett, and E.J. Goetzl Human neutrophil chemotactic and degranulating activities of leukotriene B5 (LTB5) derived from eicosapentaenoic acid Biochem. Biophys. Res. Commun. 117 1983 282 288
43. T.H. Lee, J.M. Mencia-Huerta, C. Shih, E.J. Corey, R.A. Lewis, and K.F. Austen Characterization and biologic properties of 5,12-dihydroxy derivatives of eicosapentaenoic acid, including leukotriene-B5 and the double lipoxygenase product J. Biol. Chem. 259 1984 2383 2389
44. D. Bagga, L. Wang, R. Farias-Eisner, J.A. Glaspy, and S.T. Reddy Differential effects of prostaglandin derived from w - 6 and w - 3 polyunsaturated fatty acids on COX-2 expression and IL-6 secretion Proc. Natl. Acad. Sci. U. S. A. 100 2003 1751 1756
45. M. Wada, C.J. DeLong, Y.H. Hong, C.J. Rieke, I. Song, R.S. Sidhu, C. Yuan, M. Warnock, A.H. Schmaier, C. Yokoyama, E.M. Smyth, S.J. Wilson, G.A. FitzGerald, R.M. Garavito, X. Sui, J.W. Regan, and W.L. Smith Enzymes and receptors of prostaglandin pathways with arachidonic acid-derived versus eicosapentaenoic acid-derived substrates and products J. Biol. Chem. 282 2007 22254 22266
46. S.P. Tull, C.M. Yates, B.H. Maskrey, V.B. O'Donnell, J. Madden, R.F. Grimble, P.C. Calder, G.B. Nash, and G.E. Rainger Omega-3 fatty acids and inflammation: novel interactions reveal a new step in neutrophil recruitment PLoS Biol. 7 2009 e1000177
47. V. Di Marzo The endocannabinoid system in obesity and type 2 diabetes Diabetologia 51 2008 1356 1367
48. M.T. Cencioni, V. Chiurchiù, G. Catanzaro, G. Borsellino, G. Bernardi, L. Battistini, and M. Maccarrone Anandamide suppresses proliferation and cytokine release from primary human T-lymphocytes mainly via CB2 receptors PLoS One 5 2010 e8688
49. M. Alhouayek, D.M. Lambert, N.M. Delzenne, P.D. Cani, and G.G. Muccioli Increasing endogenous 2-arachidonoylglycerol levels counteracts colitis and related systemic inflammation FASEB J. 25 2011 2711 2721
50. A. Artmann, G. Petersen, L.I. Hellgren, J. Boberg, C. Skonberg, C. Nellemann, S.H. Hansen, and H.S. Hansen Influence of dietary fatty acids on endocannabinoid and N-acylethanolamine levels in rat brain, liver and small intestine Biochim. Biophys. Acta 1781 2008 200 212
51. B. Batetta, M. Griinari, G. Carta, E. Murru, A. Ligresti, L. Cordeddu, E. Giordano, F. Sanna, T. Bisogno, S. Uda, M. Collu, I. Bruheim, V. Di Marzo, and S. Banni Endocannabinoids may mediate the ability of (n-3) fatty acids to reduce ectopic fat and inflammatory mediators in obese Zucker rats J. Nutr. 139 2009 1495 1501
52. J.T. Wood, J.S. Williams, L. Pandarinathan, D.R. Janero, C.J. Lammi-Keefe, and A. Makriyannis Dietary docosahexaenoic acid supplementation alters select physiological endocannabinoid-system metabolites in brain and plasma J. Lipid Res. 51 2010 1416 1423
53. A. Berger, G. Crozier, T. Bisogno, P. Cavaliere, S. Innis, and V. Di Marzo Anandamide and diet: inclusion of dietary arachidonate and docosahexaenoate leads to increased brain levels of the corresponding N-acylethanolamines in piglets Proc. Natl. Acad. Sci. U. S. A. 98 2001 6402 6406
54. P. Plastina, J. Meijerink, J.P. Vincken, M. Poland, and R.F. Witkamp Inhibition of nitric oxide production by RAW264.7 macrophages by n-acyl ethanolamides Naunyn. Schmiedebergs Arch. Pharmacol. 380 2009 268
55. I. Brown, M.G. Cascio, K.W. Wahle, R. Smoum, R. Mechoulam, R.A. Ross, R.G. Pertwee, and S.D. Heys Cannabinoid receptor-dependent and -independent anti-proliferative effects of omega-3 ethanolamides in androgen receptor-positive and -negative prostate cancer cell lines Carcinogenesis 31 2010 1584 1591
56. M.G. Balvers, K.C. Verhoeckx, P. Plastina, H.M. Wortelboer, J. Meijerink, and R.F. Witkamp Docosahexaenoic acid and eicosapentaenoic acid are converted by 3T3-L1 adipocytes to N-acyl ethanolamines with anti-inflammatory properties Biochim. Biophys. Acta 1801 2010 1107 1114
57. J. Meijerink, P. Plastina, J.P. Vincken, M. Poland, M. Attya, M. Balvers, H. Gruppen, B. Gabriele, and R.F. Witkamp The ethanolamide metabolite of DHA, docosahexaenoylethanolamine, shows immunomodulating effects in mouse peritoneal and RAW264.7 macrophages: evidence for a new link between fish oil and inflammation, Brit J. Nutr. 105 2011 1789 1807
58. G. Bannenberg, and C.N. Serhan Specialized pro-resolving lipid mediators in the inflammatory response: an update Biochim. Biophys. Acta 1801 2010 1260 1273
59. C.N. Serhan, S. Yacoubian, and R. Yang Anti-inflammatory and proresolving lipid mediators Annu. Rev. Pathol. 3 2008 279 312
60. C.N. Serhan, N. Chiang, and T.E. van Dyke Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators Nat. Rev. Immunol. 8 2008 349 361
61. C.N. Serhan, and N. Chiang Resolution phase lipid mediators of inflammation: agonists of resolution Curr. Opin. Pharmacol. 13 2013 632 640
62. L. Balas, M. Guichardant, T. Durand, and M. Lagarde Confusion between protectin D1 (PD1) and its isomer protectin DX (PDX) - an overview on the dihydroxy-docosatrienes described to date Biochimie 99 2014 1 7
63. J. Dalli, R.A. Colas, and C.N. Serhan Novel n-3 immunoresolvents: structures and actions Sci. Rep. 3 2013 1940
64. S. Hong, K. Gronert, P. Devchand, R.-L. Moussignac, and C.N. Serhan Novel docosatrienes and 17S-resolvins generated from docosahexaenoic acid in murine brain, human blood and glial cells: autocoids in anti-inflammation J. Biol. Chem. 278 2003 14677 14687
65. E. Mas, K.D. Croft, P. Zahra, A. Barden, and T.A. Mori Resolvins D1, D2, and other mediators of self-limited resolution of inflammation in human blood following n-3 fatty acid supplementation Clin. Chem. 58 2012 1476 1484
66. G.A. Weiss, H. Troxler, G. Klinke, D. Rogler, C. Braegger, and M. Hersberger High levels of anti-inflammatory and pro-resolving lipid mediators lipoxins and resolvins and declining docosahexaenoic acid levels in human milk during the first month of lactation Lipids Health Dis. 12 2013 89
67. J.F. Lima-Garcia, R.C. Dutra, K. da Silva, E.M. Motta, M.M. Campos, and J.B. Calixto The precursor of resolvin D series and aspirin-triggered resolvin D1 display anti-hyperalgesic properties in adjuvant-induced arthritis in rats Br. J. Pharmacol. 164 2011 278 293
68. M. Arita, M. Yoshida, S. Hong, E. Tjonahen, J.N. Glickman, N.A. Petasis, R.S. Blumberg, and C.N. Serhan Resolvin E1, an endogenous lipid mediator derived from omega-3 eicosapentaenoic acid, protects against 2,4,6-trinitrobenzene sulfonic acid-induced colitis Proc. Natl. Acad. Sci. U. S. A. 102 2005 7621 7626
69. H. Aoki, T. Hisada, T. Ishizuka, M. Utsugi, T. Kawata, Y. Shimizu, F. Okajima, K. Dobashi, and M. Mori Resolvin E1 dampens airway inflammation and hyperresponsiveness in a murine model of asthma Biochem. Biophys. Res. Commun. 367 2008 509 515
70. O. Haworth, M. Cernadas, R. Yang, C.N. Serhan, and B.D. Levy Resolvin E1 regulates interleukin 23, interferon-gamma and lipoxin A4 to promote the resolution of allergic airway inflammation Nat. Immunol. 9 2008 873 879
71. S. Bilal, O. Haworth, L. Wu, K.H. Weylandt, B.D. Levy, and J.X. Kang Fat-1 transgenic mice with elevated omega-3 fatty acids are protected from allergic airway responses Biochim. Biophys. Acta 1812 2011 1164 1169
72. A.P. Rogerio, O. Haworth, R. Croze, S.F. Oh, M. Uddin, T. Carlo, M.A. Pfeffer, R. Priluck, C.N. Serhan, and B.D. Levy Resolvin D1 and aspirin-triggered resolvin D1 promote resolution of allergic airways responses J. Immunol. 189 2012 1983 1991
73. C.C. Martin-Chouly, V. Menier, A. Hichami, H. Youmine, F. Noel, F. Pedrono, and A.B. Legrand Modulation of PAF production by incorporation of arachidonic acid and eicosapentaenoic acid in phospholipids of human leukemic monocyte-like cells THP-1 Prostaglandins Other Lipid Mediat. 60 2000 127 135
74. M. Shikano, Y. Masuzawa, and K. Yazawa Effect of docosahexaenoic acid on the generation of platelet-activating factor by eosinophilic leukemia cells, Eol-1 J. Immunol. 150 1993 3525 3533
75. R.I. Sperling, J.L. Robin, K.A. Kylander, T.H. Lee, R.A. Lewis, and K.F. Austen The effects of n-3 polyunsaturated fatty acids on the generation of platelet-activating factor-acether by human monocytes J. Immunol. 139 1987 4186 4191
76. K.D. Croft, M.J. Sturm, J.P. Codde, R. Vandongen, and L.J. Beilin Dietary fish oils reduce plasma levels of platelet activating factor precursor (lyso-PAF) in rats Life Sci. 38 1986 1875 1882
77. S. Watanabe, M. Doshi, K. Akimoto, Y. Kiso, and T. Hamazaki Suppression of platelet-activating factor generation and modulation of arachidonate metabolism by dietary enrichment with (n - 9) eicosatrienoic acid or docosahexaenoic acid in mouse peritoneal cells Prostaglandins Other Lipid Mediat. 66 2001 109 120
78. W.C. Pickett, D. Nytko, C. Dondero-Zahn, and C. Ramesha The effect of endogenous eicosapentaenoic acid on PMN leukotriene and PAF biosynthesis Prostaglandins Leukot. Med. 23 1986 135 140
79. K.D. Croft, J.P. Codde, A. Barden, R. Vandongen, and L.J. Beilin Effect of dietary fish oils on the formation of leukotriene B4 and B5, thromboxane and platelet activating factor by rat leukocytes Clin. Exp. Pharmacol. Physiol. 15 1988 517 525
80. D.G. Payan, M.Y. Wong, T. Chernov-Rogan, F.H. Valone, W.C. Pickett, V.A. Blake, W.M. Gold, and E.J. Goetzl Alterations in human leukocyte function induced by ingestion of eicosapentaenoic acid J. Clin. Immunol. 6 1986 402 410
81. M. Triggiani, T.R. Connell, and F.H. Chilton Evidence that increasing the cellular content of eicosapentaenoic acid does not reduce the biosynthesis of platelet-activating factor J. Immunol. 145 1990 2241 2248
82. F.H. Chilton, M. Patel, A.N. Fonteh, W.C. Hubbard, and M. Triggiani Dietary n-3 fatty acid effects on neutrophil lipid composition and mediator production. Influence of duration and dosage J. Clin. Invest. 91 1993 115 122
83. R.I. Sperling, M. Weinblatt, J.L. Robin, J. Ravalese III, R.L. Hoover, F. House, J.S. Coblyn, P.A. Fraser, B.W. Spur, and D.R. Robinson Effects of dietary supplementation with marine fish oil on leukocyte lipid mediator generation and function in rheumatoid arthritis Arthritis Rheum. 30 1987 988 997
84. P.C. Calder, R. Albers, J.M. Antoine, S. Blum, R. Bourdet-Sicard, G.A. Ferns, G. Folkerts, P.S. Friedmann, G.S. Frost, F. Guarner, M. Løvik, S. Macfarlane, P.D. Meyer, L. M'Rabet, M. Serafini, W. van Eden, J. van Loo, W. Vas Dias, S. Vidry, B.M. Winklhofer-Roob, and J. Zhao Inflammatory disease processes and interactions with nutrition Br. J. Nutr. 101 2009 S1 S45
85. P.C. Calder, N. Ahluwalia, F. Brouns, T. Buetler, K. Clement, K. Cunningham, K. Esposito, L.S. Jonsson, H. Kolb, M. Lansink, A. Marcos, A. Margioris, N. Matusheski, H. Nordmann, J. O'Brien, G. Pugliese, S. Rizkalla, C. Schalkwijk, J. Tuomilehto, J. Warnberg, B. Watzl, and B.M. Winklhofer-Roob Dietary factors and low-grade inflammation in relation to overweight and obesity Br. J. Nutr. 106 Suppl. 3 2011 S5 S78
86. R. de Caterina, M.I. Cybulsky, S.K. Clinton, M.A. Gimbrone, and P. Libby The omega-3 fatty acid docosahexaenoate reduces cytokine-induced expression of proatherogenic and proinflammatory proteins in human endothelial cells Arterioscler. Thromb. 14 1994 1828 1836
87. B. Khalfoun, F. Thibault, H. Watier, P. Bardos, and Y. Lebranchu Docosahexaenoic and eicosapentaenoic acids inhibit in vitro human endothelial cell production of interleukin-6 Adv. Exp. Med. Biol. 400 1997 589 597
88. C.J. Lo, K.C. Chiu, M. Fu, R. Lo, and W.S. Helton Fish oil decreases macrophage tumor necrosis factor gene transcription by altering the NF kappa B activity J. Surg. Res. 82 1999 216 221
89. T.A. Babcock, T. Novak, E. Ong, D.H. Jho, W.S. Helton, and N.J. Espat Modulation of lipopolysaccharide-stimulated macrophage tumor necrosis factor-a production by w - 3 fatty acid is associated with differential cyclooxygenase-2 protein expression and is independent of interleukin-10 J. Surg. Res. 107 2002 135 139
90. T.E. Novak, T.A. Babcock, D.H. Jho, W.S. Helton, and N.J. Espat NF-kappa B inhibition by omega-3 fatty acids modulates LPS-stimulated macrophage TNF-alpha transcription Am. J. Physiol. 284 2003 L84 L89
91. Y. Zhao, S. Joshi-Barve, and L.H. Chen Eicosapentaenoic acid prevents LPS-induced TNF-alpha expression by preventing NF-kappaB activation J. Am. Coll. Nutr. 23 2004 71 78
92. T. Billiar, P. Bankey, B. Svingen, R.D. Curran, M.A. West, R.T. Holman, R.L. Simmons, and F.B. Cerra Fatty acid uptake and Kupffer cell function: fish oil alters eicosanoid and monokine production to endotoxin stimulation Surgery 104 1988 343 349
93. G. Renier, E. Skamene, J. de Sanctis, and D. Radzioc Dietary n-3 polyunsaturated fatty acids prevent the development of atherosclerotic lesions in mice: modulation of macrophage secretory activities Arterioscler. Thromb. 13 1993 1515 1524
94. S. Sadeghi, F.A. Wallace, and P.C. Calder Dietary lipids modify the cytokine response to bacterial lipopolysaccharide in mice Immunology 96 1999 404 410
95. S. Sierra, F. Lara-Villoslada, M. Comalada, M. Olivares, and J. Xaus Dietary eicosapentaenoic acid and docosahexaenoic acid equally incorporate as decosahexaenoic acid but differ in inflammatory effects Nutrition 24 2008 245 254
96. J.M. Kremer, D.A. Lawrence, W. Jubiz, R. DiGiacomo, R. Rynes, L.E. Bartholomew, and M. Sherman Dietary fish oil and olive oil supplementation in patients with rheumatoid arthritis Arthritis Rheum. 33 1990 810 820
97. G.T. Esperson, N. Grunnet, H.H. Lervang, G.L. Nielsen, B.S. Thomsen, K.L. Faarvang, J. Dyerberg, and E. Ernst Decreased interleukin-1 beta levels in plasma from rheumatoid arthritis patients after dietary supplementation with n-3 polyunsaturated fatty acids Clin. Rheumatol. 11 1992 393 395
98. S. Kolahi, A. Ghorbanihaghjo, S. Alizadeh, N. Rashtchizadeh, H. Argani, A.R. Khabazzi, M. Hajialilo, and E. Bahreini Fish oil supplementation decreases serum soluble receptor activator of nuclear factor-kappa B ligand/osteoprotegerin ratio in female patients with rheumatoid arthritis Clin. Biochem. 43 2010 576 580
99. R.J. Faull Adhesion molecules in health and disease Aust. N. Z. J. Med. 25 1995 720 730
100. J.M. Munro Endothelial-leukocyte adhesive interactions in inflammatory diseases Eur. Heart J. 14 Suppl. K 1993 72 77
101. S.M. Albelda, C.W. Smith, and P.A. Ward Adhesion molecules and inflammatory injury FASEB J. 8 1994 504 512
102. B.N. Cronstein Adhesion molecules in the pathogenesis of rheumatoid arthritis Curr. Opin. Rheumatol. 6 1994 300 304
103. D.O. Haskard Cell adhesion molecules in rheumatoid arthritis Curr. Opin. Rheumatol. 7 1995 229 234
104. K. Tomita, T. Tanigawa, H. Yajima, H. Sano, K. Fukutani, Y. Hitsuda, Y. Matsumoto, and T. Sasaki Expression of adhesion molecules on mononuclear cells from individuals with stable atopic asthma Clin. Exp. Allergy 27 1997 664 671
105. M.F. Nageh, E.T. Sandberg, K.R. Marotti, A.H. Lin, E.P. Melshoir, D.C. Bullard, and A.L. Beaudet Deficiency of inflammatory cell adhesion molecules protects against atherosclerosis in mice Arterioscler. Thromb. Vasc. Biol. 17 1997 1517 1520
106. Y. Kobayashi, K. Kawai, H. Honda, S. Tomida, N. Niimi, T. Tamatani, M. Miyasaka, and Y. Yoshikai Antibodies against leukocyte function-associated antigen-1 and against intercellular adhesion molecule-1 together suppress the progression of experimental allergic encephalomyelitis Cell. Immunol. 164 1995 295 305
107. E.S. Collie-Duguid, and K.W. Wahle Inhibitory effect of fish oil n-3 polyunsaturated fatty acids on the expression of endothelial cell adhesion molecules Biochem. Biophys. Res. Commun. 220 1996 969 974
108. D.A. Hughes, S. Southon, and A.C. Pinder (n-3) Polyunsaturated fatty acids modulate the expression of functionally associated molecules on human monocytes in vitro J. Nutr. 126 1996 603 610
109. H. Yamada, M. Yoshida, Y. Nakano, T. Suganami, N. Satoh, T. Mita, K. Azuma, M. Itoh, Y. Yamamoto, Y. Kamei, M. Horie, H. Watada, and Y. Ogawa In vivo and in vitro inhibition of monocyte adhesion to endothelial cells and endothelial adhesion molecules by eicosapentaenoic acid Arterioscler. Thromb. Vasc. Biol. 28 2008 2173 2179
110. E.A. Miles, F.A. Wallace, and P.C. Calder Dietary fish oil reduces intercellular adhesion molecule 1 and scavenger receptor expression on murine macrophages Atherosclerosis 152 2000 43 50
111. P. Sanderson, and P.C. Calder Dietary fish oil diminishes lymphocyte adhesion to macrophage and endothelial cell monolayers Immunology 94 1998 79 87
112. C.M. Yates, S.P. Tull, J. Madden, P.C. Calder, R.F. Grimble, G.B. Nash, and G.E. Rainger Docosahexaenoic acid inhibits the adhesion of flowing neutrophils to cytokine stimulated human umbilical vein endothelial cells J. Nutr. 141 2011 1331 1334
113. D.A. Hughes, A.C. Pinder, Z. Piper, I.T. Johnson, and E.K. Lund Fish oil supplementation inhibits the expression of major histocompatibility complex class II molecules and adhesion molecules on human monocytes Am. J. Clin. Nutr. 63 1996 267 272
114. N.T. Luu, J. Madden, P.C. Calder, R.F. Grimble, C.P. Shearman, T. Chan, S.P. Tull, N. Dastur, G.E. Rainger, and G.B. Nash Comparison of the pro-inflammatory potential of monocytes from healthy adults and those with peripheral arterial disease using an in vitro culture model Atherosclerosis 193 2007 259 268
115. E.A. Miles, F. Thies, F.A. Wallace, J.R. Powell, T.L. Hirst, E.A. Newsholme, and P.C. Calder Influence of age and dietary fish oil on plasma soluble adhesion molecule concentrations Clin. Sci. 100 2001 91 100
116. X.H. Liu, and D.P. Rose Suppression of type IV collagenase in MDA-MB-435 human breast cancer cells by eicosapentaenoic acid in vitro and in vivo Cancer Lett. 92 1995 21 26
117. I. Suzuki, M. Iigo, C. Ishikawa, T. Kuhara, M. Asamoto, T. Kunimoto, M.A. Moore, K. Yazawa, E. Araki, and H. Tsuda Inhibitory effects of oleic and docosahexaenoic acids on lung metastasis by colon-carcinoma-26 cells are associated with reduced matrix metalloproteinase-2 and -9 activities Int. J. Cancer 73 1997 607 612
118. S.H. Xia, J. Wang, and J.X. Kang Decreased n-6/n-3 fatty acid ratio reduces the invasive potential of human lung cancer cells by downregulation of cell adhesion/invasion-related genes Carcinogenesis 26 2005 779 784
119. M.H. Wu, Y.T. Tsai, K.T. Hua, K.C. Chang, M.L. Kuo, and M.T. Lin Eicosapentaenoic acid and docosahexaenoic acid inhibit macrophage-induced gastric cancer cell migration by attenuating the expression of matrix metalloproteinase 10 J. Nutr. Biochem. 23 2012 1434 1439
120. H. Chen, D. Li, G.J. Roberts, T. Saldeen, and J.L. Mehta Eicosapentanoic acid inhibits hypoxia-reoxygenation-induced injury by attenuating upregulation of MMP-1 in adult rat myocytes Cardiovasc. Res. 59 2003 7 13
121. H.H. Kim, C.M. Shin, C.H. Park, K.H. Kim, K.H. Cho, H.C. Eun, and J.H. Chung Eicosapentaenoic acid inhibits UV-induced MMP-1 expression in human dermal fibroblasts J. Lipid Res. 46 2005 1712 1720
122. H.H. Kim, S. Cho, S. Lee, K.H. Kim, K.H. Cho, H.C. Eun, and J.H. Chung Photoprotective and anti-skin-aging effects of eicosapentaenoic acid in human skin in vivo J. Lipid Res. 47 2006 921 930
123. M.M. Rahman, A. Bhattacharya, and G. Fernandes Docosahexaenoic acid is more potent inhibitor of osteoclast differentiation in RAW 264.7 cells than eicosapentaenoic acid J. Cell. Physiol. 214 2008 201 209
124. Z. Zainal, A.J. Longman, S. Hurst, K. Duggan, B. Caterson, C.E. Hughes, and J.L. Harwood Relative efficacies of omega-3 polyunsaturated fatty acids in reducing expression of key proteins in a model system for studying osteoarthritis Osteoarthr. Cartil. 17 2009 896 905
125. R.A. Hansen, M.A. Harris, G.E. Pluhar, T. Motta, S. Brevard, G.K. Ogilvie, M.J. Fettman, and K.G. Allen Fish oil decreases matrix metalloproteinases in knee synovia of dogs with inflammatory joint disease J. Nutr. Biochem. 19 2008 101 108
126. J. Vogt, V.L. Andersen, A. Andreasen, T. Obel, J.H. Christensen, and E.B. Schmidt Serum concentrations of matrix metalloproteinase-9, tissue inhibitor of matrix metalloproteinase-1 and alpha2-macroglobulin in healthy subjects after supplementation with different doses of marine n-3 fatty acids Cell. Mol. Biol. (Noisy-le-grand) 56 2010 102 109
127. E.B. Furenes, I. Seljeflot, S. Solheim, E.M. Hjerkinn, and H. Arnesen Long-term influence of diet and/or omega-3 fatty acids on matrix metalloproteinase-9 and pregnancy-associated plasma protein-A in men at high risk of coronary heart disease Scand. J. Clin. Lab. Invest. 68 2008 177 184
128. H. Aarsetøy, T. Brügger-Andersen, ∅. Hetland, H. Grundt, and D.W. Nilsen Long term influence of regular intake of high dose n-3 fatty acids on CD40-ligand, pregnancy-associated plasma protein A and matrix metalloproteinase-9 following acute myocardial infarction Thromb. Haemost. 95 2006 329 336
129. H.M. Yusof, A.L. Cawood, R. Ding, J.A. Williams, F.L. Napper, C.P. Shearman, R.F. Grimble, S.P. Payne, and P.C. Calder Limited impact of 2 g/day omega-3 fatty acid ethyl esters (Omacor®) on plasma lipids and inflammatory markers in patients awaiting carotid endarterectomy Mar. Drugs 11 2013 3569 3581
130. A.L. Cawood, R. Ding, F.L. Napper, R.H. Young, J.A. Williams, M.J. Ward, O. Gudmundsen, R. Vige, S.P. Payne, S. Ye, C.P. Shearman, P.J. Gallagher, R.F. Grimble, and P.C. Calder 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 212 2010 252 259
131. A. Kumar, Y. Takada, A.M. Boriek, and B.B. Aggarwal Nuclear factor-kappaB: its role in health and disease J. Mol. Med. 82 2004 434 448
132. L.H. Siga Basic science for the clinician 39: NF-kappaB-function, activation, control, and consequences J. Clin. Rheumatol. 12 2006 207 211
133. N.D. Perkins Integrating cell-signalling pathways with NF-kappaB and IKK function Nat. Rev. Mol. Cell Biol. 8 2007 49 62
134. J.Y. Lee, K.H. Sohn, S.H. Rhee, and D. Hwang Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 through Toll-like receptor J. Biol. Chem. 276 2001 16683 16689
135. A.R. Weatherill, J.Y. Lee, L. Zhao, D.G. Lemay, H.S. Youn, and D.H. Hwang Saturated and polyunsaturated fatty acids reciprocally modulate dendritic cell functions mediated through TLR4 J. Immunol. 174 2005 5390 5397
136. W. Kong, J.H. Yen, E. Vassiliou, S. Adhikary, M.G. Toscano, and D. Ganea Docosahexaenoic acid prevents dendritic cell maturation and in vitro and in vivo expression of the IL-12 cytokine family Lipids Health Dis. 9 2010 12
137. S.W. Wong, W.J. Kwon, A.M. Choi, H.P. Kim, K. Nakahira, and D. Hwang Fatty acids modulate Toll-like receptor 4 activation through regulation of receptor dimerization and recruitment into lipid rafts in a reactive oxygen species-dependent manner J. Biol. Chem. 284 2009 27384 27392
138. A. Szanto, and L. Nagy The many faces of PPARgamma: anti-inflammatory by any means? Immunobiology 213 2008 789 803
139. P. Desreumaux, L. Dubuquoy, S. Nutten, M. Peuchmaur, W. Englaro, K. Schoonjans, B. Derijard, B. Desvergne, W. Wahli, P. Chambon, M.D. Leibowitz, J.F. Colombel, and J. Auwerx Attenuation of colon inflammation through activators of the retinoid X receptor (RXR)/peroxisome proliferator activated receptor gamma (PPARgamma) heterodimer. A basis for new therapeutic strategies J. Exp. Med. 193 2001 827 838
140. G.G. Su, X. Wen, S.T. Bailey, W. Jiang, S.M. Rangwala, S.A. Keilbaugh, A. Flanigan, S. Murthy, M.A. Lazar, and G.D. Wu A novel therapy for colitis utilizing PPARgamma ligands to inhibit the epithelial inflammatory response J. Clin. Invest. 104 1999 383 389
141. L. Dubuquoy, C. Rousseaux, X. Thuru, L. Peyrin-Biroulet, O. Romano, P. Chavatte, M. Chamaillard, and P. Desreumaux PPARgamma as a new therapeutic target in inflammatory bowel diseases Gut 55 2006 1341 1349
142. W. Vanden Berghe, L. Vermeulen, P. Delerive, K. De Bosscher, B. Staels, and G. Haegeman A paradigm for gene regulation: inflammation, NF-kappaB and PPAR Adv. Exp. Med. Biol. 544 2003 181 196
143. B.M. Forman, J. Chen, and R.M. Evans Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors α and δ Proc. Natl. Acad. Sci. U. S. A. 94 1997 4312 4317
144. S.A. Kliewer, S.S. Sundseth, S.A. Jones, P.J. Brown, G.B. Wisely, C.S. Koble, P. Devchand, W. Wahli, T.M. Willson, J.M. Lenhard, and J.M. Lehmann Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptors α and γ Proc. Natl. Acad. Sci. U. S. A. 94 1997 4318 4323
145. M. Gottlicher, E. Widmaek, Q. Li, and J.-A. Gustafsson Fatty acids activate a chimera of the clofibric acid-activated receptor and the glucocorticoid receptor Proc. Natl. Acad. Sci. U. S. A. 89 1992 4653 4657
146. G. Krey, O. Braissant, F. L'Horset, E. Kalkhoven, M. Perroud, M.G. Parker, and W. Wahli Fatty acids, eicosanoids, and hypolipidemic agents identified as ligands of peroxisome proliferator-activated receptors by coactivator-dependent receptor ligand assay Mol. Endocrinol. 11 1997 779 791
147. F. Zapata-Gonzalez, F. Rueda, J. Petriz, P. Domingo, F. Villarroya, J. Diaz-Delfin, M.A. de Madariaga, and J.C. Domingo Human dendritic cell activities are modulated by the omega-3 fatty acid, docosahexaenoic acid, mainly through PPAR(gamma):RXR heterodimers: comparison with other polyunsaturated fatty acids J. Leukoc. Biol. 84 2008 1172 1182
148. J. Lefils-Lacourtablaise, M. Socorro, A. Géloën, P. Daira, C. Debard, E. Loizon, M. Guichardant, Z. Dominguez, H. Vidal, M. Lagarde, and N. Bernoud-Hubac The eicosapentaenoic acid metabolite 15-deoxy-δ(12,14)-prostaglandin J3 increases adiponectin secretion by adipocytes partly via a PPARγ-dependent mechanism PLoS One 8 2013 e63997
149. A.M. de Urquiza, S. Liu, M. Sjoberg, R.H. Zetterstrom, W. Griffiths, J. Sjovall, and T. Perlmann Docosahexaenoic acid, a ligand for the retinoid X receptor in mouse brain Science 290 2000 2140 2144
150. Y.Y. Fan, T.E. Spencer, N. Wang, M.P. Moyer, and R.S. Chapkin Chemopreventive n-3 fatty acids activate RXRalpha in colonocytes Carcinogenesis 24 2003 1541 1548
151. G. Liu, D.M. Bibus, A.M. Bode, W.Y. Ma, R.T. Holman, and Z. Dong Omega 3 but not omega 6 fatty acids inhibit AP-1 activity and cell transformation in JB6 cells Proc. Natl. Acad. Sci. U. S. A. 98 2001 7510 7515
152. T.A. Babcock, A. Kurland, W.S. Helton, A. Rahman, K.N. Anwar, and N.J. Espat Inhibition of activator protein-1 transcription factor activation by omega-3 fatty acid modulation of mitogen-activated protein kinase signalling kinases J. Parenter. Enter. Nutr. 27 2003 176 180
153. Y.Y. Fan, L.H. Ly, R. Barhoumi, D.N. McMurray, and R.S. Chapkin Dietary docosahexaenoic acid suppresses T cell protein kinase Cκ lipid raft recruitment and IL-2 production J. Immunol. 173 2004 6151 6160
154. Y. Zhao, and L.H. Chen Eicosapentaenoic acid prevents lipopolysaccharide-stimulated DNA binding of activator protein-1 and c-Jun N-terminal kinase activity J. Nutr. Biochem. 16 2005 78 84
155. D.Y. Oh, S. Talukdar, E.J. Bae, T. Imamura, H. Morinaga, W.Q. Fan, P. Li, W.J. Lu, S.M. Watkins, and J.M. Olefsky GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects Cell 142 2010 687 698
156. S. Romagnani The Th1/Th2 paradigm Immunol. Today 6 1997 263 266
157. M. Noak, and P. Miossec Th17 and regulatory T cell balance in autoimmune and inflammatory diseases Autoimmun. Rev. 13 2014 668 677
158. A. Liston, and D.H. Gray Homeostatic control of regulatory T cell diversity Nat. Rev. Immunol. 14 2014 154 165
159. P.C. Calder, J.A. Bond, S.J. Bevan, S.V. Hunt, and E.A. Newsholme Effect of fatty acids on the proliferation of concanavalin A-stimulated rat lymph node lymphocytes Int. J. Biochem. 23 1991 579 588
160. P.C. Calder, S.J. Bevan, and E.A. Newsholme The inhibition of T-lymphocyte proliferation by fatty acids is via an eicosanoid-independent mechanism Immunology 75 1992 108 115
161. P.C. Calder, and E.A. Newsholme Polyunsaturated fatty acids suppress human peripheral blood lymphocyte proliferation and interleukin-2 production Clin. Sci. 83 1992 695 700
162. P.C. Calder, and E.A. Newsholme Unsaturated fatty acids suppress interleukin-2 production and transferrin receptor expression by concanavalin A-stimulated rat lymphocytes Mediat. Inflamm. 1 1992 107 115
163. P. Yaqoob, E.A. Newsholme, and P.C. Calder The effect of dietary lipid manipulation on rat lymphocyte subsets and proliferation Immunology 82 1994 603 610
164. F.A. Wallace, E.A. Miles, C. Evans, T.E. Stock, P. Yaqoob, and P.C. Calder Dietary fatty acids influence the production of Th1- but not Th2-type cytokines J. Leukoc. Biol. 69 2001 449 457
165. L.D. Peterson, F. Thies, P. Sanderson, E.A. Newsholme, and P.C. Calder Low levels of eicosapentaenoic and docosahexaenoic acids mimic the effects of fish oil upon rat lymphocytes Life Sci. 62 1998 2209 2217
166. C.A. Jolly, Y.H. Jiang, R.S. Chapkin, and D.N. McMurray Dietary (n-3) polyunsaturated fatty acids suppress murine lymphoproliferation, interleukin-2 secretion, and the formation of diacylglycerol and ceramide J. Nutr. 127 1997 37 43
167. K.H. Fowler, D.N. McMurray, Y.Y. Fan, H.M. Aukema, and R.S. Chapkin Purified dietary n-3 polyunsaturated fatty acids alter diacylglycerol mass and molecular species composition in concanavalin A-stimulated murine splenocytes Biochim. Biophys. Acta 1210 1993 89 96
168. P. Zhang, R. Smith, R.S. Chapkin, and D.N. McMurray Dietary n-3 polyunsaturated fatty acids modulate the Th1/Th2 balance towards the Th2 pole by suppression of Th1 development J. Nutr. 135 2005 1745 1751
169. D.H. Petursdottir, and I. Hardardottir Dietary fish oil decreases secretion of T helper (Th) 1-type cytokines by a direct effect on murine splenic T cells but enhances secretion of a Th2-type cytokine by an effect on accessory cells Br. J. Nutr. 101 2008 1040 1046
170. J.M. Monk, Q. Jia, E. Callaway, B. Weeks, R.C. Alaniz, D.N. McMurray, and R.S. Chapkin Th17 cell accumulation is decreased during chronic experimental colitis by (n-3) PUFA in Fat-1 mice J. Nutr. 142 2012 117 124
171. J.M. Monk, T.Y. Hou, H.F. Turk, B. Weeks, C. Wu, D.N. McMurray, and R.S. Chapkin Dietary n-3 polyunsaturated fatty acids (PUFA) decrease obesity-associated Th17 cell-mediated inflammation in colitis PLoS One 7 2012 e49739
172. M.J. Allen, Y.Y. Fan, J.M. Monk, T.Y. Hou, R. Barhoumi, D.N. McMurray, and R.S. Chapkin n-3 PUFAs reduce T-helper 17 cell differentiation by decreasing responsiveness to interleukin-6 in isolated mouse splenic CD4 + T cells J. Nutr. 144 2014 1306 1313
173. C.L. May, A.J. Southworth, and P.C. Calder Inhibition of lymphocyte protein kinase C by unsaturated fatty acids Biochem. Biophys. Res. Commun. 195 1993 823 828
174. A. Denys, A. Hichami, and N.A. Khan n-3 PUFAs modulate T-cell activation via protein kinase C-alpha and -epsilon and the NF-kappaB signaling pathway J. Lipid Res. 46 2005 752 758
175. A. Denys, A. Hichami, and N.A. Khan Eicosapentaenoic acid and docosahexaenoic acid modulate MAP kinase (ERK1/ERK2) signaling in human T cells J. Lipid Res. 42 2001 2015 2020
176. A. Denys, A. Hichami, and N.A. Khan Eicosapentaenoic acid and docosahexaenoic acid modulate MAP kinase enzyme activity in human T-cells Mol. Cell. Biochem. 232 2002 143 148
177. P. Sanderson, and P.C. Calder Dietary fish oil appears to inhibit the activation of phospholipase C-γ in lymphocytes Biochim. Biophys. Acta 1392 1998 300 308
178. T. Stulnig, M. Berger, T. Sigmund, D. Raederstorff, H. Stockinger, and W. Waldhäusl Polyunsaturated fatty acids inhibit T cell signal transduction by modification of detergent-soluble membrane domains J. Cell Biol. 143 1998 637 644
179. T.M. Stulnig, J. Huber, N. Leitinger, E.M. Imre, P. Angelisova, P. Nowotny, and W. Waldhausl Polyunsaturated eicosapentaenoic acid displaces proteins from membrane rafts by altering raft lipid composition J. Biol. Chem. 276 2001 37335 37340
180. M. Zeyda, G. Staffler, V. Horejsi, and W. Waldhausl LAT displacement from lipid rafts as a molecular mechanism for the inhibition of T cell signalling by polyunsaturated fatty acids J. Biol. Chem. 277 2002 28418 28423
181. M. Zeyda, A.B. Szekeres, M.D. Saemann, R. Geyeregger, H. Stockinger, G.J. Zlabinger, W. Waldhäusl, and T.M. Stulnig Suppression of T cell signaling by polyunsaturated fatty acids: selectivity in inhibition of mitogen-activated protein kinase and nuclear factor activation J. Immunol. 170 2003 6033 6039
182. T.M. Stulnig, and M. Zeyda Immunomodulation by polyunsaturated fatty acids: impact on T-cell signalling Lipids 39 2004 1171 1175
183. M. Zeyda, and T.M. Stulnig Lipid Rafts & Co.: an integrated model of membrane organization in T cell activation Prog. Lipid Res. 45 2006 187 202
184. W. Kim, N.A. Khan, D.N. McMurray, I.A. Prior, N. Wang, and R.S. Chapkin Regulatory activity of polyunsaturated fatty acids in T-cell signalling Prog. Lipid Res. 49 2010 250 261
185. P. Yaqoob The nutritional significance of lipid rafts Annu. Rev. Nutr. 29 2009 257 282
186. P.C. Calder Polyunsaturated fatty acids alter the rules of engagement Futur. Lipidol. 2 2007 27 30
187. P.C. Calder Fat chance to enhance B cell function J. Leukoc. Biol. 93 2013 457 459
188. Y.Y. Fan, D.N. McMurray, L.H. Ly, and R.S. Chapkin Dietary n-3 polyunsaturated fatty acids remodel mouse T-cell lipid rafts J. Nutr. 133 2003 1913 1920
189. T.Y. Hou, J.M. Monk, Y.Y. Fan, R. Barhoumi, Y. Chen, G.M. Rivera, D.N. McMurray, and R.S. Chapkin n-3 polyunsaturated fatty acids suppress phosphatidylinositol-(4,5)-bisphosphate dependent actin remodeling during CD4 + T cell activation Biochem. J. 443 2012 27 37
190. S.E. Sweeney, and G.S. Firestein Rheumatoid arthritis: regulation of synovial inflammation Int. J. Biochem. Cell Biol. 36 2004 372 378
191. H. Sano, T. Hla, J.A.M. Maier, L.J. Crofford, J.P. Case, T. Maciag, and R.L. Wilder In vivo cyclooxygenase expression in synovial tissues of patients with rheumatoid arthritis and osteoarthritis and rats with adjuvant and streptococcal cell wall arthritis J. Clin. Invest. 89 1992 97 108
192. M. Feldmann, and R.N. Maini The role of cytokines in the pathogenesis of rheumatoid arthritis Rheumatology 38 Suppl. 2 1999 3 7
193. C.A. Leslie, W.A. Gonnerman, M.D. Ullman, K.C. Hayes, C. Franzblau, and E.S. Cathcart Dietary fish oil modulates macrophage fatty acids and decreases arthritis susceptibility in mice J. Exp. Med. 162 1985 1336 1339
194. D.H. Volker, P.E.B. FitzGerald, and M.L. Garg The eicosapentaenoic to docosahexaenoic acid ratio of diets affects the pathogenesis of arthritis in Lew/SSN rats J. Nutr. 130 2000 559 565
195. M. Ierna, A. Kerr, H. Scales, K. Berge, and M. Griinari Supplementation of diet with krill oil protects against experimental rheumatoid arthritis BMC Musculoskelet. Disord. 11 2010 136
196. V.R. Ramprasath, I. Eyal, S. Zchut, and P.J.H. Jones Enhanced increase of omega-3 index in healthy individuals with response to 4-week n-3 fatty acid supplementation from krill oil versus fish oil Lipids Health Dis. 12 2013 178
197. J.M. Kremer, D.A. Lawrence, G.F. Petrillo, L.L. Litts, P.M. Mullaly, R.I. Rynes, R.P. Stocker, N. Parhami, N.S. Greenstein, and B.R. Fuchs Effects of high-dose fish oil on rheumatoid arthritis after stopping nonsteroidal anti-inflammatory drugs: clinical and immune Correlates Arthritis Rheum. 38 1995 1107 1114
198. H. van der Tempel, J.E. Tullekan, P.C. Limburg, F.A.J. Muskiet, and M.H. van Rijswijk Effects of fish oil supplementation in rheumatoid arthritis Ann. Rheum. Dis. 49 1990 76 80
199. P.C. Calder PUFA, inflammatory processes and rheumatoid arthritis Proc. Nutr. Soc. 67 2008 409 418
200. E.A. Miles, and P.C. Calder Influence of marine n-3 polyunsaturated fatty acids on immune function and a systematic review of their effects on clinical outcomes in rheumatoid Arthritis Br. J. Nutr. 107 2012 S171 S184
201. P.R. Fortin, R.A. Lew, M.H. Liang, E.A. Wright, L.A. Beckett, T.C. Chalmers, and R.I. Sperling Validation of a meta analysis: the effects of fish oil in rheumatoid arthritis J. Clin. Epidemiol. 48 1995 1379 1390
202. R.J. Goldberg, and J. Katz A meta-analysis of the analgesic effects of omega-3 polyunsaturated fatty acid supplementation for inflammatory joint pain Pain 129 2009 210 233
203. W.R. Henderson Role of leukotrienes in asthma Ann. Allergy 72 1994 272 278
204. E.A. Miles, L. Aston, and P.C. Calder In vitro effects of eicosanoids derived from different 20-carbon fatty acids on T helper type 1 and T helper type 2 cytokine production in human whole-blood cultures Clin. Exp. Allergy 33 2003 624 632
205. R.L. Roper, and R.P. Phipps Prostaglandin E2 regulation of the immune response Adv. Prostaglandin Thromboxane Leukot. Res. 22 1994 101 111
206. A. Yokoyama, T. Hamazaki, A. Ohshita, N. Kohno, K. Sakai, G.D. Zhao, H. Katayama, and K. Hiwada Effect of aerosolized docosahexaenoic acid in a mouse model of atopic asthma Int. Arch. Allergy Immunol. 123 2000 327 332
207. J.P. Arm, C.E. Horton, J.M. Mencia-Huerta, F. House, N.M. Eiser, T.J. Clark, B.W. Spur, and T.H. Lee Effect of dietary supplementation with fish oil lipids on mild asthma Thorax 43 1988 84 92
208. C.M. Kirsch, D.G. Payan, M.Y. Wong, J.G. Dohlman, V.A. Blake, M.A. Petri, J. Offenberger, E.J. Goetzl, and W.M. Gold Effect of eicosapentaenoic acid in asthma Clin. Allergy 18 1988 177 187
209. K.S. Broughton, C.S. Johnson, B.K. Pace, M. Liebman, and K.M. Kleppinger Reduced asthma symptoms with n-3 fatty acid ingestion are related to 5-series leukotriene production Am. J. Clin. Nutr. 65 1997 1011 1017
210. L. Hodge, C.M. Salome, J.M. Hughes, D. Liu-Brennan, J. Rimmer, M. Allman, D. Pang, C. Armour, and A.J. Woolcock Effect of dietary intake of omega-3 and omega - 6 fatty acids on severity of asthma in children Eur. Respir. J. 11 1998 361 365
211. T. Nagakura, S. Matsuda, K. Shichijyo, H. Sugimoto, and K. Hata Dietary supplementation with fish oil rich in omega-3 polyunsaturated fatty acids in children with bronchial asthma Eur. Respir. J. 16 2000 861 865
212. F.C.K. Thien, R. Woods, S. De Luca, and M.J. Abramson Dietary marine fatty acids (fish oil) for asthma in adults and children Cochrane Database Syst. Rev. 2 2002 CD001283
213. I. Hirata, M. Murano, M. Nitta, S. Sasaki, K. Toshina, K. Maemura, and K. Katsu Estimation of mucosal inflammatory mediators in rat DSS-induced colitis - possible role of PGE2 in protection against mucosal damage Digestion 63 Suppl. 1 2001 73 80
214. N. Nieto, M.I. Torres, A. Rios, and A. Gil Dietary polyunsaturated fatty acids improve histological and biochemical alterations in rats with experimental ulcerative colitis J. Nutr. 132 2002 11 19
215. P. Sharon, and W.F. Stenson Enhanced synthesis of leukotriene B4 by colonic mucosa in inflammatory bowel disease Gastroenterology 86 1984 453 460
216. M. Masoodi, D.S. Pearl, M. Eiden, J.K. Shute, J.F. Brown, P.C. Calder, and T.M. Trebble Altered colonic mucosal polyunsaturated fatty acid (PUFA) derived lipid mediators in ulcerative colitis: new insight into relationship with disease activity and pathophysiology PLoS One 8 2013 e76532
217. L.R. Empey, W. Walker, and R.N. Fedorak Fish oil-enriched diet is mucosal protective against acetic acid-induced colitis in rats Can. J. Physiol. Pharmacol. 70 1992 660 668
218. J. Vilaseca, A. Salas, F. Guarner, R. Rodriguez, M. Martinez, and J.-R. Malagelada Dietary fish oil reduces progression of chronic inflammatory lesions in a rat model of granulomatous colitis Gut 31 1990 539 544
219. H. Yuceyar, O. Ozutemiz, A. Huseyinov, M. Saruç, M. Alkanat, S. Bor, I. Coker, and Y. Batur Is administration of n-3 fatty acids by mucosal enema protective against trinitrobenzene-induced colitis in rats? Prostaglandins Leukot. Essent. Fat. Acids 61 1999 339 345
220. R.S. Chapkin, L.A. Davidson, L. Ly, B.R. Weeks, J.R. Lupton, and D.N. McMurray Immunomodulatory effects of (n-3) fatty acids: putative link to inflammation and colon cancer J. Nutr. 137 2007 200S 204S
221. R. Lorenz, P.C. Weber, P. Szimnau, W. Heldwein, T. Strasser, and K. Loeschke Supplementation with n-3 fatty acids from fish oil in chronic inflammatory bowel disease - a randomized, placebo controlled, double-blind cross-over trial J. Intern. Med. Suppl. 731 1989 225 232
222. K. Hillier, R. Jewell, L. Dorrell, and C.L. Smith Incorporation of fatty acids from fish oil and olive oil into colonic mucosal lipids and effects upon eicosanoid synthesis in inflammatory bowel disease Gut 32 1991 1151 1155
223. P.C. Calder Polyunsaturated fatty acids, inflammatory processes and inflammatory bowel diseases Mol. Nutr. Food Res. 52 2008 885 897
224. A. Belluzzi, C. Brignola, M. Campieri, A. Pera, S. Boschi, and M. Miglioli Effect of an enteric-coated fish-oil preparation on relapses in Crohn's disease N. Engl. J. Med. 334 1996 1557 1560
225. B.G. Feagan, W.J. Sandborn, U. Mittmann, S. Bar-Meir, G. D'Haens, M. Bradette, A. Cohen, C. Dallaire, T.P. Ponich, J.W. McDonald, X. Hébuterne, P. Paré, P. Klvana, Y. Niv, S. Ardizzone, O. Alexeeva, A. Rostom, G. Kiudelis, J. Spleiss, D. Gilgen, M.K. Vandervoort, C.J. Wong, G.Y. Zou, A. Donner, and P. Rutgeerts Omega-3 free fatty acids for the maintenance of remission in Crohn disease: the EPIC Randomized Controlled Trials JAMA 299 2008 1690 1697
226. C.H. MacLean, W.A. Mojica, S.C. Morton, J. Pencharz, R. Hasenfeld, R. Garland, W. Tu, S.J. Newberry, L.K. Jungvig, J. Grossman, P. Khanna, S. Rhodes, and P. Shekelle Effects of omega-3 fatty acids on lipid and glycemic control in type II diabetes and the metabolic syndrome and on inflammatory bowel disease, rheumatoid arthritis, renal disease, systemic lupus erythematosus and osteoporosis Evidence Report/Technical Assessment no. 89. AHRQ Publication no. 04-E012-2 2004 Agency for Healthcare Research and Quality Rockville, MD
227. D. Turner, T.H. Steinhart, and A.M. Griffiths Omega 3 fatty acids (fish oil) for maintenance of remission in ulcerative colitis Cochrane Database Syst. Rev. 18 2007 CD006443
228. D. Turner, S.H. Zlotkin, P.S. Shah, and A.M. Griffiths Omega 3 fatty acids (fish oil) for maintenance of remission in Crohn's disease Cochrane Database Syst. Rev. 21 2009 CD006320
229. M. De Ley, R. de Vos, D.W. Hommes, and P. Stokkers Fish oil for induction of remission in ulcerative colitis Cochrane Database Syst. Rev. 17 2007 CD005986