Bioactive products formed in humans from fish oils

Journal of Lipid Research

Volumn 56, Issue 9, 2015, Pages 1808-1820

  Skarke, Carsten ^a   Alamuddin, Naji ^a   Lawson, John A ^a   Li, Xuanwen ^a   Ferguson, Jane F ^a   Reilly, Muredach P ^a   FitzGerald, Garret A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Inflammation; Lipids; Resolution

Indexed keywords

ARACHIDONIC ACID; BACTERIUM LIPOPOLYSACCHARIDE; CREATININE; EPOXYICOSATRIENOIC ACID; FISH OIL; ISOPROSTANE DERIVATIVE; LIPID; OMEGA 3 ACID ETHYL ESTER; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PHOSPHOLIPID DERIVATIVE; SPECIALIZED PRORESOLVING MEDIATOR; UNCLASSIFIED DRUG; ANTIINFLAMMATORY AGENT; AUTACOID; CD59 ANTIGEN; LIPOPOLYSACCHARIDE;

ADULT; ARTICLE; BLOOD PRESSURE; BLOOD SAMPLING; CREATININE URINE LEVEL; DRUG MEGADOSE; ERYTHROCYTE MEMBRANE; FEMALE; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; INFLAMMATION; MALE; NORMAL HUMAN; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; SPECIALIZED PRORESOLVING MEDIATOR FORMATION; SUPPLEMENTATION; THROMBOCYTE AGGREGATION; TREATMENT DURATION; URINALYSIS; BLOOD; CHEMICALLY INDUCED; CONTROLLED STUDY; DIET THERAPY; DIETARY SUPPLEMENT; DRUG EFFECTS; LIPID METABOLISM; RANDOMIZED CONTROLLED TRIAL; SYNTHESIS;

ADULT; ANTI-INFLAMMATORY AGENTS; ANTIGENS, CD59; DIETARY SUPPLEMENTS; FATTY ACIDS, OMEGA-3; FEMALE; FISH OILS; HEALTHY VOLUNTEERS; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; LIPID METABOLISM; LIPOPOLYSACCHARIDES; MALE;

EID: 84940995668     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M060392     Document Type: Article

References (64)

1. Hu, F. B., L. Bronner, W. C. Willett, M. J. Stampfer, K. M. Rexrode, C. M. Albert, D. Hunter, and J. E. Manson. 2002. Fish and omega-3 fatty acid intake and risk of coronary heart disease in women. JAMA. 287: 1815-1821.
2. Amano, T., T. Matsubara, T. Uetani, M. Kato, B. Kato, T. Yoshida, K. Harada, S. Kumagai, A. Kunimura, Y. Shinbo, et al. 2011. Impact of omega-3 polyunsaturated fatty acids on coronary plaque instability: an integrated backscatter intravascular ultrasound study. Atherosclerosis. 218: 110-116.
3. de Oliveira Otto, M. C., J. H. Wu, A. Baylin, D. Vaidya, S. S. Rich, M. Y. Tsai, D. R. Jacobs, Jr., and D. Mozaffarian. 2013. Circulating and dietary omega-3 and omega-6 polyunsaturated fatty acids and incidence of CVD in the Multi-Ethnic Study of Atherosclerosis. J. Am. Heart Assoc. 2: e000506.
4. GISSI-Prevenzione Investigators. 1999. Dietary supplementation with n-3 polyunsaturated fatty acids and vitamin E after myocardial infarction: results of the GISSI-Prevenzione trial. Gruppo Italiano per lo Studio della Sopravvivenza nell'Infarto miocardico. Lancet. 354: 447-455.
5. Yokoyama, M., H. Origasa, M. Matsuzaki, Y. Matsuzawa, Y. Saito, Y. Ishikawa, S. Oikawa, J. Sasaki, H. Hishida, H. Itakura, et al. 2007. Effects of eicosapentaenoic acid on major coronary events in hypercholesterolaemic patients (JELIS): a randomised open-label, blinded endpoint analysis. Lancet. 369: 1090-1098.
6. Hooper, L., R. L. Thompson, R. A. Harrison, C. D. Summerbell, A. R. Ness, H. J. Moore, H. V. Worthington, P. N. Durrington, J. P. Higgins, N. E. Capps, et al. 2006. Risks and benefits of omega 3 fats for mortality, cardiovascular disease, and cancer: systematic review. BMJ. 332: 752-760.
7. Wang, C., W. S. Harris, M. Chung, A. H. Lichtenstein, E. M. Balk, B. Kupelnick, H. S. Jordan, and J. Lau. 2006. n-3 Fatty acids from fish or fish-oil supplements, but not alpha-linolenic acid, benefit cardiovascular disease outcomes in primary- and secondary-prevention studies: a systematic review. Am. J. Clin. Nutr. 84: 5-17.
8. Hu, F. B., and J. E. Manson. 2012. Omega-3 fatty acids and secondary prevention of cardiovascular disease-is it just a fish tale?: comment on "Efficacy of omega-3 fatty acid supplements (eicosapentaenoic acid and docosahexaenoic acid) in the secondary prevention of cardiovascular disease". Arch. Intern. Med. 172: 694-696.
9. Shearer, G. C., O. V. Savinova, and W. S. Harris. 2012. Fish oil-how does it reduce plasma triglycerides? Biochim. Biophys. Acta. 1821: 843-851.
10. Morris, M. C., F. Sacks, and B. Rosner. 1993. Does fish oil lower blood pressure? A meta-analysis of controlled trials. Circulation. 88: 523-533.
11. Knapp, H. R., and G. A. FitzGerald. 1989. The antihypertensive effects of fish oil. A controlled study of polyunsaturated fatty acid supplements in essential hypertension. N. Engl. J. Med. 320: 1037-1043.
12. Knapp, H. R., I. A. Reilly, P. Alessandrini, and G. A. FitzGerald. 1986. In vivo indexes of platelet and vascular function during fish-oil administration in patients with atherosclerosis. N. Engl. J. Med. 314: 937-942.
13. De Caterina, R. 2011. n-3 Fatty acids in cardiovascular disease. N. Engl. J. Med. 364: 2439-2450.
14. Serhan, C. N., C. B. Clish, J. Brannon, S. P. Colgan, N. Chiang, and K. Gronert. 2000. Novel functional sets of lipid-derived mediators with antiinflammatory actions generated from omega-3 fatty acids via cyclooxygenase 2-nonsteroidal antiinflammatory drugs and transcellular processing. J. Exp. Med. 192: 1197-1204.
15. Hong, S., K. Gronert, P. R. Devchand, R. L. Moussignac, and C. N. Serhan. 2003. Novel docosatrienes and 17S-resolvins generated from docosahexaenoic acid in murine brain, human blood, and glial cells. Autacoids in anti-inflammation. J. Biol. Chem. 278: 14677-14687.
16. Chiang, N., and C. N. Serhan. 2006. Cell-cell interaction in the transcellular biosynthesis of novel omega-3-derived lipid mediators. Methods Mol. Biol. 341: 227-250.
17. Oh, S. F., P. S. Pillai, A. Recchiuti, R. Yang, and C. N. Serhan. 2011. Pro-resolving actions and stereoselective biosynthesis of 18S E-series resolvins in human leukocytes and murine inflammation. J. Clin. Invest. 121: 569-581.
18. Liao, Z., J. Dong, W. Wu, T. Yang, T. Wang, L. Guo, L. Chen, D. Xu, and F. Wen. 2012. Resolvin D1 attenuates inflammation in lipopolysaccharide-induced acute lung injury through a process involving the PPARgamma/NF-kappaB pathway. Respir. Res. 13: 110.
19. Mas, E., K. D. Croft, P. Zahra, A. Barden, and T. A. Mori. 2012. Resolvins D1, D2, and other mediators of self-limited resolution of inflammation in human blood following n-3 fatty acid supplementation. Clin. Chem. 58: 1476-1484.
20. Colas, R. A., M. Shinohara, J. Dalli, N. Chiang, and C. N. Serhan. 2014. Identification and signature profiles for pro-resolving and inflammatory lipid mediators in human tissue. Am. J. Physiol. Cell Physiol. 307: C39-C54.
21. Ho, K. J., M. Spite, C. D. Owens, H. Lancero, A. H. Kroemer, R. Pande, M. A. Creager, C. N. Serhan, and M. S. Conte. 2010. Aspirin-triggered lipoxin and resolvin E1 modulate vascular smooth muscle phenotype and correlate with peripheral atherosclerosis. Am. J. Pathol. 177: 2116-2123.
22. Arita, M., F. Bianchini, J. Aliberti, A. Sher, N. Chiang, S. Hong, R. Yang, N. A. Petasis, and C. N. Serhan. 2005. Stereochemical assignment, antiinflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1. J. Exp. Med. 201: 713-722.
23. Clària, J., B. T. Nguyen, A. L. Madenci, C. K. Ozaki, and C. N. Serhan. 2013. Diversity of lipid mediators in human adipose tissue depots. Am. J. Physiol. Cell Physiol. 304: C1141-C1149.
24. Fischer, R., A. Konkel, H. Mehling, K. Blossey, A. Gapelyuk, N. Wessel, C. von Schacky, R. Dechend, D. N. Muller, M. Rothe, et al. 2014. Dietary omega-3 fatty acids modulate the eicosanoid profile in man primarily via the CYP-epoxygenase pathway. J. Lipid Res. 55: 1150-1164.
25. Giera, M., A. Ioan-Facsinay, R. Toes, F. Gao, J. Dalli, A. M. Deelder, C. N. Serhan, and O. A. Mayboroda. 2012. Lipid and lipid mediator profiling of human synovial fluid in rheumatoid arthritis patients by means of LC-MS/MS. Biochim. Biophys. Acta. 1821: 1415-1424.
26. Kalish, B. T., H. D. Le, J. M. Fitzgerald, S. Wang, K. Seamon, K. M. Gura, K. Gronert, and M. Puder. 2013. Intravenous fish oil lipid emulsion promotes a shift toward anti-inflammatory proresolving lipid mediators. Am. J. Physiol. Gastrointest. Liver Physiol. 305: G818-G828.
27. Keelan, J. A., E. Mas, N. D'Vaz, J. A. Dunstan, S. Li, A. E. Barden, P. J. Mark, B. J. Waddell, S. L. Prescott, and T. A. Mori. 2015. Effects of maternal n-3 fatty acid supplementation on placental cytokines, pro-resolving lipid mediators and their precursors. Reproduction. 149: 171-178.
28. Recchiuti, A., M. Codagnone, A. M. Pierdomenico, C. Rossi, V. C. Mari, E. Cianci, F. Simiele, V. Gatta, and M. Romano. 2014. Immunoresolving actions of oral resolvin D1 include selective regulation of the transcription machinery in resolution-phase mouse macrophages. FASEB J. 28: 3090-3102.
29. Prüss, H., B. Rosche, A. B. Sullivan, B. Brommer, O. Wengert, K. Gronert, and J. M. Schwab. 2013. Proresolution lipid mediators in multiple sclerosis - differential, disease severity-dependent synthesis - a clinical pilot trial. PLoS One. 8: e55859.
30. Sasaki, A., H. Fukuda, N. Shiida, N. Tanaka, A. Furugen, J. Ogura, S. Shuto, N. Mano, and H. Yamaguchi. 2015. Determination of omega-6 and omega-3 PUFA metabolites in human urine samples using UPLC/MS/MS. Anal. Bioanal. Chem. 407: 1625-1639.
31. Wang, X., M. Zhu, E. Hjorth, V. Cortes-Toro, H. Eyjolfsdottir, C. Graff, I. Nennesmo, J. Palmblad, M. Eriksdotter, K. Sambamurti, et al. 2015. Resolution of inflammation is altered in Alzheimer's disease. Alzheimers Dement. 11: 40.e1-2-50.e1-2.
32. Weiss, G. A., H. Troxler, G. Klinke, D. Rogler, C. Braegger, and M. Hersberger. 2013. 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: 89.
33. Arita, M., T. Ohira, Y. P. Sun, S. Elangovan, N. Chiang, and C. N. Serhan. 2007. Resolvin E1 selectively interacts with leukotriene B4 receptor BLT1 and ChemR23 to regulate inflammation. J. Immunol. 178: 3912-3917.
34. Hasturk, H., A. Kantarci, T. Ohira, M. Arita, N. Ebrahimi, N. Chiang, N. A. Petasis, B. D. Levy, C. N. Serhan, and T. E. Van Dyke. 2006. RvE1 protects from local inflammation and osteoclast- mediated bone destruction in periodontitis. FASEB J. 20: 401-403.
35. Isobe, Y., M. Arita, S. Matsueda, R. Iwamoto, T. Fujihara, H. Nakanishi, R. Taguchi, K. Masuda, K. Sasaki, D. Urabe, et al. 2012. Identification and structure determination of a novel anti-inflammatory mediator resolvin E3, 17,18-dihydroxy-eicosapentaenoic acid. J. Biol. Chem. 287: 10525-10534.
36. Liu, G., M. Fiala, M. T. Mizwicki, J. Sayre, L. Magpantay, A. Siani, M. Mahanian, M. Chattopadhyay, A. La Cava, and M. Wiedau-Pazos. 2012. Neuronal phagocytosis by inflammatory macrophages in ALS spinal cord: inhibition of inflammation by resolvin D1. Am. J. Neurodegener. Dis. 1: 60-74.
37. Pedersen, A. K., and G. A. FitzGerald. 1985. Cyclooxygenase inhibition, platelet function, and metabolite formation during chronic sulfinpyrazone dosing. Clin. Pharmacol. Ther. 37: 36-42.
38. Ferguson, J. F., C. K. Mulvey, P. N. Patel, R. Y. Shah, J. Doveikis, W. Zhang, J. Tabita-Martinez, K. Terembula, M. Eiden, A. Koulman, et al. 2014. Omega-3 PUFA supplementation and the response to evoked endotoxemia in healthy volunteers. Mol. Nutr. Food Res. 58: 601-613.
39. Rodriguez, A. R., and B. W. Spur. 2012. Total synthesis of resolvin D1, a potent anti-inflammatory lipid mediator. Tetrahedron Lett. 53: 6990-6994.
40. Rodriguez, A. R., and B. W. Spur. 2012. Total synthesis of the macrophage derived anti-inflammatory lipid mediator Maresin 1. Tetrahedron Lett. 53: 4169-4172.
41. Balas, L., M. Guichardant, T. Durand, and M. Lagarde. 2014. Confusion between protectin D1 (PD1) and its isomer protectin DX (PDX). An overview on the dihydroxy-docosatrienes described to date. Biochimie. 99: 1-7.
42. Chang, C. T., P. Patel, N. Kang, J. A. Lawson, W. L. Song, W. S. Powell, G. A. FitzGerald, and J. Rokach. 2008. Eicosapentaenoic-acid-derived isoprostanes: synthesis and discovery of two major isoprostanes. Bioorg. Med. Chem. Lett. 18: 5523-5527.
43. Jacobo, S. H., C. T. Chang, G. J. Lee, J. A. Lawson, W. S. Powell, D. Pratico, G. A. FitzGerald, and J. Rokach. 2006. Total synthesis of 8,12-iso-iPF3alpha-VI, an EPA-derived isoprostane: stereoselective introduction of the fifth asymmetric center. J. Org. Chem. 71: 1370-1379.
44. Chang, C. T., P. Patel, V. Gore, W. L. Song, J. A. Lawson, W. S. Powell, G. A. FitzGerald, and J. Rokach. 2009. A new approach to the synthesis of polyunsaturated deuterated isoprostanes: total synthesis of d4-5-epi-8,12-iso-iPF3alpha-VI and d4-8,12-iso-iPF3alpha-VI. Bioorg. Med. Chem. Lett. 19: 6755-6758.
45. Kim, S., W. S. Powell, J. A. Lawson, S. H. Jacobo, D. Pratico, G. A. FitzGerald, K. Maxey, and J. Rokach. 2005. iPF2alpha-III-17,18,19,20-d4: total synthesis and metabolism. Bioorg. Med. Chem. Lett. 15: 1613-1617.
46. Lawson, J. A., J. Rokach, and G. A. FitzGerald. 1999. Isoprostanes: formation, analysis and use as indices of lipid peroxidation in vivo. J. Biol. Chem. 274: 24441-24444.
47. Song, W. L., J. A. Lawson, M. Wang, H. Zou, and G. A. FitzGerald. 2007. Noninvasive assessment of the role of cyclooxygenases in cardiovascular health: a detailed HPLC/MS/MS method. Methods Enzymol. 433: 51-72.
48. Folch, J., M. Lees, and G. H. Sloane Stanley. 1957. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226: 497-509.
49. Spite, M., J. Claria, and C. N. Serhan. 2014. Resolvins, specialized proresolving lipid mediators, and their potential roles in metabolic diseases. Cell Metab. 19: 21-36.
50. Serhan, C. N. 2014. Pro-resolving lipid mediators are leads for resolution physiology. Nature. 510: 92-101.
51. Daviglus, M. L., J. Stamler, A. J. Orencia, A. R. Dyer, K. Liu, P. Greenland, M. K. Walsh, D. Morris, and R. B. Shekelle. 1997. Fish consumption and the 30-year risk of fatal myocardial infarction. N. Engl. J. Med. 336: 1046-1053.
52. Wada, M., C. J. DeLong, Y. H. Hong, C. J. Rieke, I. Song, R. S. Sidhu, C. Yuan, M. Warnock, A. H. Schmaier, C. Yokoyama, et al. 2007. Enzymes and receptors of prostaglandin pathways with arachidonic acid-derived versus eicosapentaenoic acid-derived substrates and products. J. Biol. Chem. 282: 22254-22266.
53. Miyahara, T., S. Runge, A. Chatterjee, M. Chen, G. Mottola, J. M. Fitzgerald, C. N. Serhan, and M. S. Conte. 2013. D-series resolvin attenuates vascular smooth muscle cell activation and neointimal hyperplasia following vascular injury. FASEB J. 27: 2220-2232.
54. Schwab, J. M., N. Chiang, M. Arita, and C. N. Serhan. 2007. Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature. 447: 869-874.
55. Challis, J. R., and D. Tulchinsky. 1974. A comparison between the concentration of prostaglandin F in human plasma and serum. Prostaglandins. 5: 27-31.
56. Ricciotti, E., and G. A. FitzGerald. 2011. Prostaglandins and inflammation. Arterioscler. Thromb. Vasc. Biol. 31: 986-1000.
57. Moertl, D., A. Hammer, S. Steiner, R. Hutuleac, K. Vonbank, and R. Berger. 2011. Dose-dependent effects of omega-3-polyunsaturated fatty acids on systolic left ventricular function, endothelial function, and markers of inflammation in chronic heart failure of nonischemic origin: a double-blind, placebo-controlled, 3-arm study. Am. Heart J. 161: 915.e1-915.e9.
58. Psychogios, N., D. D. Hau, J. Peng, A. C. Guo, R. Mandal, S. Bouatra, I. Sinelnikov, R. Krishnamurthy, R. Eisner, B. Gautam, et al. 2011. The human serum metabolome. PLoS One. 6: e16957.
59. Dawczynski, C., K. A. Massey, C. Ness, M. Kiehntopf, S. Stepanow, M. Platzer, M. Grun, A. Nicolaou, and G. Jahreis. 2013. Randomized placebo-controlled intervention with n-3 LC-PUFA-supplemented yoghurt: effects on circulating eicosanoids and cardiovascular risk factors. Clin. Nutr. 32: 686-696.
60. Keyes, K. T., Y. Ye, Y. Lin, C. Zhang, J. R. Perez-Polo, P. Gjorstrup, and Y. Birnbaum. 2010. Resolvin E1 protects the rat heart against reperfusion injury. Am. J. Physiol. Heart Circ. Physiol. 299: H153-H164.
61. Seki, H., K. Fukunaga, M. Arita, H. Arai, H. Nakanishi, R. Taguchi, T. Miyasho, R. Takamiya, K. Asano, A. Ishizaka, et al. 2010. The anti-inflammatory and proresolving mediator resolvin E1 protects mice from bacterial pneumonia and acute lung injury. J. Immunol. 184: 836-843.
62. Settimio, R., D. F. Clara, F. Franca, S. Francesca, and D. Michele. 2012. Resolvin D1 reduces the immunoinflammatory response of the rat eye following uveitis. Mediators Inflamm. 2012: 318621.
63. Tjonahen, E., S. F. Oh, J. Siegelman, S. Elangovan, K. B. Percarpio, S. Hong, M. Arita, and C. N. Serhan. 2006. Resolvin E2: identification and anti-inflammatory actions: pivotal role of human 5-lipoxygenase in resolvin E series biosynthesis. Chem. Biol. 13: 1193-1202.
64. Wang, Q., X. Zheng, Y. Cheng, Y. L. Zhang, H. X. Wen, Z. Tao, H. Li, Y. Hao, Y. Gao, L. M. Yang, et al. 2014. Resolvin D1 stimulates alveolar fluid clearance through alveolar epithelial sodium channel, Na,K-ATPase via ALX/cAMP/PI3K pathway in lipopolysaccharide-induced acute lung injury. J. Immunol. 192: 3765-3777.