Evaluation of suppressive and pro-resolving effects of EPA and DHA in human primary monocytes and T-helper cells

Journal of Lipid Research

Volumn 54, Issue 4, 2013, Pages 923-935

  Jaudszus, Anke ^a   Gruen, Michael ^b   Watzl, Bernhard ^a   Ness, Christina ^b   Roth, Alexander ^a   Lochner, Alfred ^b   Barz, Dagmar ^c   Gabriel, Holger ^c   Rothe, Michael ^d   Jahreis, Gerhard ^b  

^a FEDERAL RESEARCH INSTITUTE OF NUTRITION AND FOOD   (Germany)

^b Institute of Nutrition   (Germany)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^d LIPIDOMIX GMBH   (Germany)

Author keywords

Cytokines; Docosahexaenoic acid; Eicosapentaenoic acid; Th cells

Indexed keywords

CD69 ANTIGEN; DOCOSAHEXAENOIC ACID; ICOSAPENTAENOIC ACID; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; LEUKOTRIENE B4; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; THROMBOXANE B2; TUMOR NECROSIS FACTOR ALPHA;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL LEVEL; CELL POPULATION; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENZYME ACTIVITY; ENZYME INHIBITION; HELPER CELL; HUMAN; HUMAN CELL; IMMUNOMODULATION; MONOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE ACTIVATION;

ARACHIDONIC ACID; BENZAMIDES; CELLS, CULTURED; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-4; INTERLEUKIN-6; MONOCYTES; PPAR GAMMA; PYRIDINES; T-LYMPHOCYTES, HELPER-INDUCER; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84875851769     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.P031260     Document Type: Article

References (61)

1. Calder, P. C. 2006. N-3 polyunsaturated fatty acids, infl ammation, and infl ammatory diseases. Am. J. Clin. Nutr. 83 : 1505S-1519S.
2. 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 fi sh or fi sh-oil supplements, but not alpha-linolenic acid, benefi t cardiovascular disease outcomes in primary-And secondary-prevention studies: a systematic review. Am. J. Clin. Nutr. 84 : 5-17.
3. León, H., M. C. Shibata, S. Sivakumaran, M. Dorgan, T. Chatterley, and R. T. Tsuyuki. 2008. Effect of fi sh oil on arrhythmias and mortality: systematic review. BMJ. 337 : a2931.
4. Nagakura, T., S. Matsuda, K. Shichijyo, H. Sugimoto, and K. Hata. 2000. Dietary supplementation with fi sh oil rich in omega-3 polyunsaturated fatty acids in children with bronchial asthma. Eur. Respir. J. 16 : 861-865.
5. Mickleborough, T. D., M. R. Lindley, A. A. Ionescu, and A. D. Fly. 2006. Protective effect of fi sh oil supplementation on exercise-induced bronchoconstriction in asthma. Chest. 129 : 39-49.
6. Balbás, G. M., M. S. Regaña, and P. U. Millet. 2011. Study on the use of omega-3 fatty acids as a therapeutic supplement in treatment of psoriasis. Clin. Cosmet. Investig. Dermatol. 4 : 73-77.
7. Caughey, G. E., M. J. James, S. M. Proudman, and L. G. Cleland. 2010. Fish oil supplementation increases the cyclooxygenase inhibitory activity of paracetamol in rheumatoid arthritis patients. Complement. Ther. Med. 18 : 171-174.
8. Calder, P. C. 2008. Polyunsaturated fatty acids, infl ammatory processes and infl ammatory bowel disease. Mol. Nutr. Food Res. 52 : 885-897.
9. Thienprasert, A., S. Samuhaseneetoo, K. Popplestone, A. L. West, E. A. Miles, and P. C. Calder. 2009. Fish oil n-3 polyunsaturated fatty acids selectively affect plasma cytokines and decrease illness in Thai schoolchildren: a randomized, double-blind, placebo-controlled intervention trial. J. Pediatr. 154 : 391-395.
10. Byleveld, P. M., G. T. Pang, R. L. Clancy, and D. C. Roberts. 1999. Fish oil feeding delays infl uenza virus clearance and impairs production of interferon-gamma and virus-specifi c immunoglobulin A in the lungs of mice. J. Nutr. 129 : 328-335.
11. Auvin, S., F. Collet, F. Gottrand, M. O. Husson, X. Leroy, C. Beermann, and B. P. Guery. 2005. Long-chain polyunsaturated fatty acids modulate lung infl ammatory response induced by Pseudomonas aeruginosa in mice. Pediatr. Res. 58 : 211-215.
12. McFarland, C. T., Y. Y. Fan, R. S. Chapkin, B. R. Weeks, and D. N. McMurray. 2008. Dietary polyunsaturated fatty acids modulate resistance to Mycobacterium tuberculosis in guinea pigs. J. Nutr. 138 : 2123-2128.
13. Schwerbrock, N. M., E. A. Karlsson, Q. Shi, P. A. Sheridan, and M. A. Beck. 2009. Fish oil-fed mice have impaired resistance to infl uenza infection. J. Nutr. 139 : 1588-1594.
14. Woodworth, H. L., S. J. McCaskey, D. M. Duriancik, J. F. Clinthome, I. M. Langohr, E. M. Gardner, and J. I. Fenton. 2010. Dietary fi sh oil alters T lymphocyte cell populations and exacerbates disease in a mouse model of infl ammatory colitis. Cancer Res. 70 : 7960-7969.
15. Anderson, M., and K. L. Fritsche. 2002. (n-3) fatty acids and infectious disease resistance. J. Nutr. 132 : 3566-3576.
16. 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 benefi ts of omega 3 fats for mortality, cardiovascular disease, and cancer: systematic review. BMJ. 332 : 752-760.
17. BfR Opinion No. 030/2009 2009. BfR recommends the setting of maximum levels for the fortifi cation of foods with omega-3 fatty acids. Accessed December 3, 2012. at http://www.bfr.bund. de/cm/349/bfr-recommends-the-setting- of-maximum-levels-for-the-fortifi cation-of-foods-with-omega-3-fatty-Acids.pdf.
18. Sijben, J. W., and P. C. Calder. 2007. Differential immunomodulation with long-chain n-3 PUFA in health and chronic disease. Proc. Nutr. Soc. 66 : 237-259.
19. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purifi cation. Can. J. Biochem. Physiol. 37 : 911-917.
20. Jaudszus, A., P. Möckel, E. Hamelmann, and G. Jahreis. 2010. Trans-10, cis-12-CLA-caused lipodystrophy is associated with profound changes of fatty acid profi les of liver, white adipose tissue and erythrocytes in mice: possible link to tissue-specifi c alterations of fatty acid desaturation. Ann. Nutr. Metab. 57 : 103-111.
21. Gomolka, B., E. Siegert, K. Blossey, W. H. Schunck, M. Rothe, and K. H. Weylandt. 2011. Analysis of omega-3 and omega-6 fatty acidderived lipid metabolite formation in human and mouse blood samples. Prostaglandins Other Lipid Mediat. 94 : 81-87.
22. Mascher, B., P. Schlenke, and M. Seyfarth. 1999. Expression and kinetics of cytokines determined by intracellular staining using fl ow cytometry. J. Immunol. Methods. 223 : 115-121.
23. Mosmann, T. R., and R. L. Coffman. 1989. Th1 and Th2 cells: Different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7 : 145-173.
24. Sabat, R., G. Grütz, K. Warszawska, S. Kirsch, E. Witte, K. Wolk, and J. Geginat. 2010. Biology of interleukin-10. Cytokine Growth Factor Rev. 21 : 331-344.
25. Haimovich, B., J. Calvano, A. D. Haimovich, S. E. Calvano, S. M. Coyle, and S. F. Lowry. 2010. In vivo endotoxin synchronizes and suppresses clock gene expression in human peripheral blood leukocytes. Crit. Care Med. 38 : 751-758.
26. Calder, P. C. 2001. Polyunsaturated fatty acids, infl ammation and immunity. Lipids. 36 : 1007-1024.
27. Samuelsson, B. 1991. Arachidonic acid metabolism: role in infl ammation. Z. Rheumatol. 50 : 3-6.
28. Isobe, Y., M. Arita, S. Matsueda, R. Iwamoto, T. Fujihara, H. Nakanishi, R. Taguchi, K. Masuda, K. Sasaki, D. Urabe, et al. 2012. Identifi cation and structure determination of novel anti-infl ammatory mediator resolvin E3, 17,18-dihydroxyeicosapentaenoic acid. J. Biol. Chem. 287 : 10525-10534.
29. Serhan, C. N., and N. A. Petasis. 2011. Resolvins and protectins in infl ammation resolution. Chem. Rev. 111 : 5922-5943.
30. Zeyda, M., A. B. Szekeres, M. D. Säemann, R. Geyeregger, H. Stockinger, G. J. Zlabinger, W. Waldhäusl, and T. M. Stulnig. 2003. Suppression of T cell signaling by polyunsaturated fatty acids: selectivity in inhibition of mitogen-Activated protein kinase and nuclear factor activation. J. Immunol. 170 : 6033-6039.
31. Akdis, M., S. Burgler, R. Crameri, T. Eiwegger, H. Fujita, E. Gomez, S. Klunker, N. Meyer, L. O'Mahony, O. Palomares, et al. 2011. Interleukins, from 1 to 37, and interferon-: receptors, functions, and roles in diseases. J. Allergy Clin. Immunol. 127 : 701-721.
32. Jain, J., C. Loh, and A. Rao. 1995. Transcriptional regulation of the IL-2 gene. Curr. Opin. Immunol. 7 : 333-342.
33. Liao, W., J. X. Lin, and W. J. Leonard. 2011. IL-2 family cytokines: new insights into the complex roles of IL-2 as a broad regulator of T helper cell differentiation. Curr. Opin. Immunol. 23 : 598-604.
34. Reddy, J., P. Chastagner, L. Fiette, X. Liu, and J. Thèze. 2001. IL-2-induced tumor necrosis factor (TNF)-beta expression: further analysis in the IL-2 knockout model, and comparison with TNF-Alpha, lymphotoxin-beta, TNFR1 and TNFR2 modulation. Int. Immunol. 13 : 135-147.
35. Clark, R. B., D. Bishop-Bailey, T. Estrada-Hernandez, T. Hla, L. Puddington, and S. J. Padula. 2000. The nuclear receptor PPAR gamma and immunoregulation: PPAR gamma mediates inhibition of helper T cell responses. J. Immunol. 164 : 1364-1371.
36. Norazmi, M. N., R. Mohamed, A. A. Nurul, and N. S. Yaacob. 2012. The modulation of PPAR-1 and PPAR-2 mRNA expression by ciglitazone in CD3/CD28-Activated naïve and memory CD4+ T cells. Clin. Dev. Immunol. 2012. : 849195.
37. Delerive, P., J. C. Fruchart, and B. Staels. 2001. Peroxisome proliferator-Activated receptors in infl ammation control. J. Endocrinol. 169 : 453-459.
38. Wang, P., P. O. Anderson, S. Chen, K. M. Paulsson, H. O. Sjogren, and S. Li. 2001. Inhibition of the transcription factors AP-1 and NFkappaB in CD4 T cells by peroxisome proliferator-Activated receptor gamma ligands. Int. Immunopharmacol. 1 : 803-812.
39. Yang, X. Y., L. H. Wang, T. Chen, D. R. Hodge, J. H. Resau, L. DaSilva, and W. L. Farrar. 2000. Activation of human T lymphocytes is inhibited by peroxisome proliferator-Activated receptor gamma (PPARgamma) agonists. PPARgamma co-Association with transcription factor NFAT. J. Biol. Chem. 275 : 4541-4544.
40. Chung, S. W., B. Y. Kang, and T. S. Kim. 2003. Inhibition of interleukin-4 production in CD4+ T cells by peroxisome proliferatoractivated receptor-gamma (PPAR-gamma) ligands: involvement of physical association of between PPAR-gamma and the nuclear factor of activated T cells transcription factor. Mol. Pharmacol. 64 : 1169-1179.
41. Lee, G., F. Elwood, J. McNally, J. Weiszmann, M. Lindstrom, K. Amaral, M. Nakamura, S. Miao, P. Cao, R. M. Learned, et al. 2002. T0070907, a selective ligand for peroxisome proliferator-Activated receptor gamma, functions as an antagonist of biochemical and cellular activities. J. Biol. Chem. 277 : 19649-19657.
42. Li, H., X. Z. Ruan, S. H. Powis, R. Fernando, W. Y. Mon, D. C. Wheeler, J. F. Moorhead, and Z. Varghese. 2005. EPA and DHA reduce LPS-induced infl ammation responses in HK-2 cells: evidence for a PPAR-gamma-dependent mechanism. Kidney Int. 67 : 867-874.
43. Draper, E., C. M. Reynolds, M. Canavan, K. H. Mills, C. E. Loscher, and H. M. Roche. 2011. Omega-3 fatty acids attenuate dendritic cell function via NF-B independent of PPAR-. J. Nutr. Biochem. 22 : 784-790.
44. Raza Shaikh, S. 2010. Diet-induced docosahexaenoic acid non-raft domains and lymphocyte function. Prostaglandins Leukot. Essent. Fatty Acids. 82 : 159-164.
45. Li, Q., M. Wang, L. Tan, C. Wang, J. Ma, N. Li, Y. Li, G. Xu, and J. Li. 2005. Docosahexaenoic acid changes lipid composition and interleukin-2 receptor signaling in membrane rafts. J. Lipid Res. 46 : 1904-1913.
46. Geyeregger, R., M. Zeyda, G. J. Zlabinger, W. Waldhäusl, and T. M. Stulnig. 2005. Polyunsaturated fatty acids interfere with formation of the immunological synapse. J. Leukoc. Biol. 77 : 680-688.
47. Li, Q., L. Tan, C. Wang, N. Li, Y. Li, G. Xu, and J. Li. 2006. Polyunsaturated eicosapentaenoic acid changes lipid composition in lipid rafts. Eur. J. Nutr. 45 : 144-151.
48. Yog, R., R. Barhoumi, D. N. McMurray, and R. S. Chapkin. 2010. N-3 polyunsaturated fatty acids suppress mitochondrial translocation of the immunological synapse and modulate calcium signaling in T cells. J. Immunol. 184 : 5864-5873.
49. Shaik, S. R., C. A. Jolly, and R. S. Chapkin. 2012. N-3 polyunsaturated fatty acids exert immunomodulatory effects on lymphocytes by targeting plasma membrane molecular organization. Mol. Aspects Med. 33 : 46-54.
50. Denys, A., A. Hichami, and N. A. Khan. 2005. N-3 PUFAs modulate T-cell activation via protein kinase C-Alpha and-epsilon and the NF-kappaB signaling pathway. J. Lipid Res. 46 : 752-758.
51. Gorjão, R., S. M. Hirabara, T. M. de Lima, M. F. Cury-Boaventura, and R. Curi. 2007. Regulation of interleukin-2 signaling by fatty acids in human lymphocytes. J. Lipid Res. 48 : 2009-2019.
52. Kew, S., M. D. Mesa, S. Tricon, R. Buckley, A. M. Minihane, and P. Yaqoob. 2004. Effects of oils rich in eicosapentaenoic and docosahexaenoic acids on immune cell composition and function in healthy humans. Am. J. Clin. Nutr. 79 : 674-681.
53. Ambarus, C. A., K. C. Santegoets, L. van Bon, M. H. Wenink, P. P. Tak, T. R. Radstake, and T. L. Baeten. 2012. Soluble immune complexes shift the TLR-induced cytokine production of distinct polarized human macrophage subsets towards IL-10. PLoS ONE. 7 : e35994.
54. Trebble, T., N. K. Arden, M. A. Strout, S. A. Wootton, G. C. Burdge, E. A. Miles, A. B. Ballinger, R. L. Thompson, and P. C. Calder. 2003. Inhibition of tumour necrosis factor-Alpha and interleukin 8 production by mononuclear cells following dietary fi sh-oil supplementation in healthy men and response to antioxidant co-supplementation. Br. J. Nutr. 90 : 405-412.
55. Lee, J. Y., A. Y. Choi, Y. T. Oh, W. Choe, E. J. Yeo, J. Ha, and I. Kang. 2012. AMP-Activated protein kinase mediates T cell activation-induced expression of FasL and COX-2 via protein kinase C theta-dependent pathway in human Jurkat T leukemia cells. Cell. Signal. 24 : 1195-1207.
56. Bryn, T., S. Yaqub, M. Mahic, K. Henjum, E. M. Aandahl, and E. Taskén. 2008. LPS-Activated monocytes suppress T-cell immune responses and induce FOXP3+ T cells through a COX-2-PGE2-dependent mechanism. Int. Immunol. 20 : 235-245.
57. Chêne, G., M. Dubourdeau, P. Balard, L. Escoubet-Lozach, C. Orphila, A. Berry, J. Bernad, M. F. Aries, M. Charveron, and B. Pipy. 2007. n-3 and n-6 polyunsaturated fatty acids induce the expression of COX-2 via PPARgamma activation in human keratinocyte HaCaT cells. Biochim. Biophys. Acta. 1771 : 576-589.
58. Bannenberg, G., and C. N. Serhan. 2010. Specialized pro-resolving lipid mediators in the infl ammatory response: an update. Biochim. Biophys. Acta. 1801 : 1260-1273.
59. Bouwens, M., O. van de Rest, N. Dellschaft, M. G. Bromhaar, L. C. de Groot, J. M. Geleijnse, M. Müller, and L. A. Afman. 2009. Fish oil supplementation induces antiinfl ammatory gene expression profi les in human blood mononuclear cells. Am. J. Clin. Nutr. 90 : 415-424.
60. Vedin, I., T. Cederholm, Y. Freund-Levi, H. Basun, A. Garlind, G. F. Irving, M. Eriksdotter-Jönhagen, L. O. Wahlund, I. Dahlmann, and J. Palmblad. 2012. Effects of DHA-rich n-3 fatty acid supplementation on gene expression in blood mononuclear leukocytes: the OmegAD study. PLoS ONE. 7 : e35425.
61. Pierre, M., M. O. Husson, R. Le Berre, J. L. Desseyn, C. Galabert, L. Béghin, C. Beermann, A. Dagenais, Y. Berthiaume, B. Cardinaud, et al. 2007. Omega-3 polyunsaturated fatty acids improve host response in chronic Pseudomonas aeruginosa lung infection in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 292 : L1422-L1431.