Omega-3 docosahexaenoic acid and procyanidins inhibit cyclo-oxygenase activity and attenuate NF-κB activation through a p105/p50 regulatory mechanism in macrophage inflammation

Biochemical Journal

Volumn 441, Issue 2, 2012, Pages 653-663

  Martinez Micaelo, Neus ^a   González Abuín, Noemi ^a   Terra, Ximena ^b   Richart, Cristobal ^b   Ardèvol, Anna ^a   Pinent, Monserrat ^a   Blay, Mayte ^a  

^a UNIVERSITAT ROVIRA I VIRGILI   (Spain)

^b HOSPITAL UNIVERSITARI JOAN XXIII   (Spain)

Author keywords

Cyclo oxygenase; Docosahexaenoic acid (DHA); Nuclear factor B (NF B); Omega 3 fatty acid; Procyanidin; Prostaglandin

Indexed keywords

CYCLOOXYGENASE 1; DOCOSAHEXAENOIC ACID; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; OMEGA 3 FATTY ACID; PROCYANIDIN B1; PROCYANIDIN B2; PROCYANIDIN C1; PROCYANIDIN DERIVATIVE; PROTEIN P105; PROTEIN P50; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVITY; ENZYME INHIBITION; HOMEOSTASIS; HUMAN; HUMAN CELL; IC 50; IMMUNE RESPONSE; INFLAMMATION; MACROPHAGE; MOLECULAR MECHANICS; MONOCYTE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

BIFLAVONOIDS; CATECHIN; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYCLOOXYGENASE INHIBITORS; DINOPROSTONE; DOCOSAHEXAENOIC ACIDS; FATTY ACIDS, OMEGA-3; HUMANS; I-KAPPA B PROTEINS; INFLAMMATION; INTERLEUKIN-6; NF-KAPPA B; NF-KAPPA B P50 SUBUNIT; PROANTHOCYANIDINS; TRANSCRIPTION FACTOR RELA;

EID: 84555195564     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110967     Document Type: Article

References (49)

1. Olefsky, J. M. and Glass, C. K. (2010) Macrophages, inflammation, and insulin resistance. Annu. Rev. Physiol. 72, 219-246
2. Willoughby, D. A., Moore, A. R., Colville-Nash, P. R. and Gilroy, D. (2000) Resolution of inflammation. Int. J. Immunopharmacol. 22, 1131-1135 (Pubitemid 32012972)
3. Calder, P. C. (2009) Polyunsaturated fatty acids, inflammation and inflammatory diseases. J. Pharm. Pharmacol. 61, 195
4. Linton, M. F. and Fazio, S. (2003) Macrophages, inflammation, and atherosclerosis. Int. J. Obes. 27, S35-S40 (Pubitemid 38019186)
5. Funk, C. D. (2001) Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294, 1871-1875
6. Colville-Nash, P. R. and Gilroy, D. W. (2000) Cyclooxygenase enzymes as targets for therapeutic intervention in inflammation. Drug News Perspect. 13, 587-597 (Pubitemid 32220496)
7. Smith, W. L., DeWitt, D. L. and Garavito, R. M. (2000) Cyclooxygenases: structural, cellular, and molecular biology. Annu. Rev. Biochem. 69, 145-182
8. Smith, W. L. (2008) Nutritionally essential fatty acids and biologically indispensable cyclooxygenases. Trends Biochem. Sci. 33, 27-37
9. Gilroy, D. W. and Colville-Nash, P. R. (2000) New insights into the role of COX2 in inflammation. J. Mol. Med. 78, 121-129 (Pubitemid 30337493)
10. Chandrasekharan, N. V., Dai, H., Roos, K. L. T., Evanson, N. K., Tomsik, J., Elton, T. S. and Simmons, D. L. (2002) COX-3, a cyclooxygenase-1 variant inhibited by acetaminophen and other analgesic/antipyretic drugs: cloning, structure, and expression. Proc. Natl. Acad. Sci. U.S.A. 99, 13926-13931 (Pubitemid 35215482)
11. Ghosh, S., May, M. J. and Kopp, E. B. (1998) NF-κB and rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16, 225-260 (Pubitemid 28183365)
12. Hayden, M. S., West, A. P. and Ghosh, S. (2006) NF-κB and the immune response. Oncogene 25, 6758-6780
13. Li, Q. T. and Verma, I. M. (2002) NF-κB regulation in the immune system. Nat. Rev. Immunol. 2, 725-734
14. Saccani, S., Pantano, S. and Natoli, G. (2003) Modulation of NF-κB activity by exchange of dimers. Mol. Cell 11, 1563-1574 (Pubitemid 36776542)
15. Oeckinghaus, A. and Ghosh, S. (2009) The NF-κB family of transcription factors and its regulation. Cold Spring Harb. Perspect. Biol. 1, a000034
16. Hayden, M. S. and Ghosh, S. (2004) Signaling to NF-κB. Genes Dev. 18, 2195-2224
17. Chacon, M. R., Ceperuelo-Mallafre, V., Maymo-Masip, E., Mateo-Sanz, J. M., Arola, L., Guitierrez, C., Fernandez-Real, J. M., Ardevol, A., Simon, I. and Vendrell, J. (2009) Grape-seed procyanidins modulate inflammation on human differentiated adipocytes in vitro. Cytokine 47, 137-142
18. Murphy, K. J., Chronopoulos, A. K., Singh, I., Francis, M. A., Moriarty, H., Pike, M. J., Turner, A. H., Mann, N. J. and Sinclair, A. J. (2003) Dietary flavanols and procyanidin oligomers from cocoa (Theobroma cacao) inhibit platelet function. Am. J. Clin. Nutr. 77, 1466-1473 (Pubitemid 39655281)
19. Terra, X., Montagut, G., Bustos, M., Llopiz, N., Ardevol, A., Blade, C., Fernandez-Larrea, J., Pujadas, G., Salvado, J., Arola, L. and Blay, M. (2009) Grape-seed procyanidins prevent low-grade inflammation by modulating cytokine expression in rats fed a high-fat diet. J. Nutr. Biochem. 20, 210-218
20. Yilmaz, Y. and Toledo, R. T. (2004) Health aspects of functional grape seed constituents. Trends Food Sci. Tech. 15, 422-433 (Pubitemid 39040020)
21. Calder, P. C. (2005) Polyunsaturated fatty acids and inflammation. Biochem. Soc. Trans. 33, 423-427
22. Simopoulos, A. P. (2002) Omega-3 fatty acids in inflammation and autoimmune diseases. J. Am. Coll. Nutr. 21, 495-505
23. Grimminger, F., Walmrath, D., Seeger, W. and Lasch, H. G. (1993) Antiinflammatory effects of omega-3-lipinfusion in clinical and experimental studies. Med. Welt 44, 207-216 (Pubitemid 23090204)
24. Horrocks, L. A. and Yeo, Y. K. (1999) Health benefits of docosahexaenoic acid (DHA). Pharmacol. Res. 40, 211-225 (Pubitemid 29435720)
25. Weldon, S. M., Mullen, A. C., Loscher, C. E., Hurley, L. A. and Roche, H. M. (2007) Docosahexaenoic acid induces an anti-inflammatory profile in lipopolysaccharidestimulated human THP-1 macrophages more effectively than eicosapentaenoic acid. J. Nutr. Biochem. 18, 250-258 (Pubitemid 46389578)
26. Schuehly, W., Huefner, A., Pferschy-Wenzig, E. M., Prettner, E., Adams, M., Bodensieck, A., Kunert, O., Oluwemimo, A., Haslinger, E. and Bauer, R. (2009) Design and synthesis of ten biphenyl-neolignan derivatives and their in vitro inhibitory potency against cyclooxygenase-1/2 activity and 5-lipoxygenase-mediated LTB4-formation. Bioorg. Med. Chem. 17, 4459-4465
27. Zhang, W. Y., Liu, H. Q., Xie, K. Q., Yin, L. L., Li, Y., Kwik-Uribe, C. L. and Zhu, X. Z. (2006) Procyanidin dimer B2 epicatechin-(4β-8)- epicatechin suppresses the expression of cyclooxygenase-2 in endotoxin-treated monocytic cells. Biochem. Biophys. Res. Commun. 345, 508-515
28. Serra, A., Macia, A., Romero, M. P., Salvado, M. J., Bustos, M., Fernandez-Larrea, J. and Motilva, M. J. (2009) Determination of procyanidins and their metabolites in plasma samples by improved liquid chromatography-tandem mass spectrometry. J. Chromatogr. B: Anal. Technol. Biomed. Life Sci. 877, 1169-1176
29. Serra, A., Macia, A., Romero, M. P., Valls, J., Blade, C., Arola, L. and Motilva, M. J. (2010) Bioavailability of procyanidin dimers and trimers and matrix food effects in in vitro and in vivo models. Br. J. Nutr. 103, 944-952
30. Marsen, T. A., Pollok, M., Oette, K. and Baldamus, C. A. (1992) Pharmacokinetics of omega-3-fatty-acids during ingestion of fish oil preparations. Prostaglandins Leukotrienes Essent. Fatty Acids 46, 191-196
31. Williamson, G. and Manach, C. (2005) Bioavailability and bioefficacy of polyphenols in humans. II. Review of 93 intervention studies. Am. J. Clin. Nutr. 81, 243S-255S
32. Rusca, A., Di Stefano, A. F. D., Doig, M. V., Scarsi, C. and Perucca, E. (2009) Relative bioavailability and pharmacokinetics of two oral formulations of docosahexaenoic acid/eicosapentaenoic acid after multiple-dose administration in healthy volunteers. Eur. J. Clin. Pharmacol. 65, 503-510
33. Saw, C. L. L., Huang, Y. and Kong, A. N. (2010) Synergistic anti-inflammatory effects of low doses of curcumin in combination with polyunsaturated fatty acids: docosahexaenoic acid or eicosapentaenoic acid. Biochem. Pharmacol. 79, 421-430
34. Baba, S., Osakabe, N., Natsume, M. and Terao, J. (2002) Absorption and urinary excretion of procyanidin B2 epicatechin-(4β-8)-epicatechin in rats. Free Radical Biol. Med. 33, 142-148 (Pubitemid 34681016)
35. Akira, S., Takeda, K. and Kaisho, T. (2001) Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2, 675-680 (Pubitemid 32747155)
36. Heinrich, P. C., Castell, J. V. and Andus, T. (1990) Interleukin-6 and the acute phase response. Biochem. J. 265, 621-636 (Pubitemid 20053863)
37. Kishimoto, T. (1989) The biology of interleukin-6. Blood 74, 1-10
38. Vansnick, J. (1990) Interleukin-6: an overview. Annu. Rev. Immunol. 8, 253-278
39. Tang, G. L., Minemoto, Y., Dibling, B., Purcell, N. H., Li, Z. W., Karin, M. and Lin, A. (2001) Inhibition of JNK activation through NF-κB target genes. Nature 414, 313-317 (Pubitemid 33097808)
40. Tsuchiya, S., Yamabe, M., Yamaguchi, Y., Kobayashi, Y., Konno, T. and Tada, K. (1980) Establishment and characterization of a human acute monocytic leukemia-cell line (THP-1). Int. J. Cancer 26, 171-176 (Pubitemid 10086416)
41. Daigneault, M., Preston, J. A., Marriott, H. M., Whyte, M. K. B. and Dockrell, D. H. (2010) The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLoS ONE 5, e8668
42. Smith, C. J., Morrow, J. D., Roberts, L. J. and Marnett, L. J. (1993) Differentiation of monocytoid THP-1 cells with phorbol ester induces expression of prostaglandin endoperoxide synthase-1 (COX-1). Biochem. Biophys. Res. Commun. 192, 787-793 (Pubitemid 23227391)
43. Smith, C. J., Morrow, J. D., Roberts, L. J. and Marnett, L. J. (1997) Induction of prostaglandin endoperoxide synthase-1 (COX-1) in a human promonocytic cell line by treatment with the differentiating agent TPA. In Eicosanoids and Other Bioactive Lipids in Cancer, Inflammation, and Radiation Injury 2, Pts A and B (Honn, K. V., Nigam, S. and Marnett, L. J., eds), pp. 99-106, Springer
44. Kang, Y. J., Wingerd, B. A., Arakawa, T. and Smith, W. L. (2006) Cyclooxygenase-2 gene transcription in a macrophage model of inflammation. J. Immunol. 177, 8111-8122 (Pubitemid 44846330)
45. Beinke, S., Belich, M. P. and Ley, S. C. (2002) The death domain of NF-κB1 p105 is essential for signal-induced p105 proteolysis. J. Biol. Chem. 277, 24162-24168 (Pubitemid 34951931)
46. Moorthy, A. K. and Ghosh, G. (2003) p105 center dot IκBγ and prototypical IκBs use a similar mechanism to bind but a different mechanism to regulate the subcellular localization of NF-κB. J. Biol. Chem. 278, 556-566
47. Beinke, S. and Ley, S. C. (2004) Functions of NF-κB1 and NF-κB2 in immune cell biology. Biochem. J. 382, 393-409 (Pubitemid 39243905)
48. Guan, H. C., Hou, S. H. and Ricciardi, R. P. (2005) DNA binding of repressor nuclear factor-κB p50/p50 depends on phosphorylation of Ser337 by the protein kinase A catalytic subunit. J. Biol. Chem. 280, 9957-9962
49. Tong, X., Yin, L., Washington, R., Rosenberg, D. W. and Giardina, C. (2004) The p50-p50 NF-κB complex as a stimulus-specific repressor of gene activation. Mol. Cell. Biochem. 265, 171-183 (Pubitemid 41461877)