Omega-3 fatty acids suppress Th2-associated cytokine gene expressions and GATA transcription factors in mast cells

Journal of Nutritional Biochemistry

Volumn 24, Issue 5, 2013, Pages 868-876

  Park, Bo Kyung ^a   Park, Sunyoung ^a   Park, Jun Beom ^a   Park, Min Chul ^b   Min, Tae Sun ^c   Jin, Mirim ^a  

^a Daejeon University   (South Korea)

^b Seoul National University   (South Korea)

^c R and D Policy Team National Research Foundation of Korea   (South Korea)

Author keywords

GATA 1 GATA 2; Mast cells; NC Nga murine atopic model; Omega 3 fatty acids; Th2 cytokines

Indexed keywords

CYCLOSPORIN A; CYTOKINE; FISH OIL; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; MESSENGER RNA; OMEGA 3 FATTY ACID; TRANSCRIPTION FACTOR GATA; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR GATA 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DERMATITIS; GENE EXPRESSION; MALE; MAST CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TH2 CELL;

ANIMALS; DERMATITIS; DOWN-REGULATION; FATTY ACIDS, OMEGA-3; FISH OILS; FLOW CYTOMETRY; GATA1 TRANSCRIPTION FACTOR; GATA2 TRANSCRIPTION FACTOR; GENE EXPRESSION; INTERLEUKIN-13; INTERLEUKIN-4; INTERLEUKIN-5; MALE; MAST CELLS; MICE; REAL-TIME POLYMERASE CHAIN REACTION; TH2 CELLS;

MURINAE;

EID: 84876800359     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2012.05.007     Document Type: Article

References (54)

1. Fritsche K. Fatty acids as modulators of the immune response. Annu Rev Nutr 2006, 26:45-73.
2. Prescott S.L., Calder P.C. N-3 polyunsaturated fatty acids and allergic disease. Curr Opin Clin Nutr Metab Care 2004, 7:123-129.
3. Dunstan J.A., Mori T.A., Barden A., Beilin L.J., Taylor A.L., Holt P.G., et al. Maternal fish oil supplementation in pregnancy reduces interleukin-13 levels in cord blood of infants at high risk of atopy. Clin Exp Allergy 2003, 33:442-448.
4. Olsen S.F., Osterdal M.L., Salvig J.D., Mortensen L.M., Rytter D., Secher N.J., et al. Fish oil intake compared with olive oil intake in late pregnancy and asthma in the offspring: 16 y of registry-based follow-up from a randomized controlled trial. Am J Clin Nutr 2008, 88:167-175.
5. Thijs C., Muller A., Rist L., Kummeling I., Snijders B.E., Huber M., et al. Fatty acids in breast milk and development of atopic eczema and allergic sensitisation in infancy. Allergy 2011, 66:58-67.
6. Kumar G.S., Das U.N. Effect of prostaglandins and their precursors on the proliferation of human lymphocytes and their secretion of tumor necrosis factor and various interleukins. Prostaglandins Leukot Essent Fatty Acids 1994, 50:331-334.
7. Bhattacharya A., Sun D., Rahman M., Fernandes G. Different ratios of eicosapentaenoic and docosahexaenoic omega-3 fatty acids in commercial fish oils differentially alter pro-inflammatory cytokines in peritoneal macrophages from C57BL/6 female mice. J Nutr Biochem 2007, 18:23-30.
8. Prescott S.L., Barden A.E., Mori T.A., Dunstan J.A. Maternal fish oil supplementation in pregnancy modifies neonatal leukotriene production by cord-blood-derived neutrophils. Clin Sci (Lond) 2007, 113:409-416.
9. Gueck T., Seidel A., Fuhrmann H. Effects of essential fatty acids on mediators of mast cells in culture. Prostaglandins Leukot Essent Fatty Acids 2003, 68:317-322.
10. Gueck T., Seidel A., Fuhrmann H. Consequences of eicosapentaenoic acid (n-3) and arachidonic acid (n-6) supplementation on mast cell mediators. J Anim Physiol Anim Nutr (Berl). 2004, 88:259-265.
11. Gueck T., Seidel A., Baumann D., Meister A., Fuhrmann H. Alterations of mast cell mediator production and release by gamma-linolenic and docosahexaenoic acid. Vet Dermatol 2004, 15:309-314.
12. Triggiani M., Connell T.R., Chilton F.H. Evidence that increasing the cellular content of eicosapentaenoic acid does not reduce the biosynthesis of platelet-activating factor. J Immunol 1990, 145:2241-2248.
13. Bradding P., Walls A.F., Holgate S.T. The role of the mast cell in the pathophysiology of asthma. J Allergy Clin Immunol 2006, 117:1277-1284.
14. Kalesnikoff J., Galli S.J. New developments in mast cell biology. Nat Immunol 2008, 9:1215-1223.
15. Kitawaki T., Kadowaki N., Sugimoto N., Kambe N., Hori T., Miyachi Y., et al. IgE-activated mast cells in combination with pro-inflammatory factors induce Th2-promoting dendritic cells. Int Immunol 2006, 18:1789-1799.
16. Kouro T., Takatsu K. IL-5- and eosinophil-mediated inflammation: from discovery to therapy. Int Immunol 2009, 21:1303-1309.
17. Taube C., Stassen M. Mast cells and mast cell-derived factors in the regulation of allergic sensitization. Chem Immunol Allergy 2008, 94:58-66.
18. Weiss D.L., Brown M.A. Regulation of IL-4 production in mast cells: a paradigm for cell-type-specific gene expression. Immunol Rev 2001, 179:35-47.
19. Monticelli S., Lee D.U., Nardone J., Bolton D.L., Rao A. Chromatin-based regulation of cytokine transcription in Th2 cells and mast cells. Int Immunol 2005, 17:1513-1524.
20. Szabo S.J., Glimcher L.H., Ho I.C. Genes that regulate interleukin-4 expression in T cells. Curr Opin Immunol 1997, 9:776-781.
21. Lavender P., Cousins D., Lee T. Regulation of Th2 cytokine gene transcription. Chem Immunol 2000, 78:16-29.
22. Henkel G., Brown M.A. PU.1 and GATA: components of a mast cell-specific interleukin 4 intronic enhancer. Proc Natl Acad Sci USA 1994, 91:7737-7741.
23. Kwan M., Powell D.R., Nachman T.Y., Brown M.A. An intron GATA-binding site regulates chromatin accessibility and is essential for IL-4 gene expression in mast cells. Eur J Immunol 2005, 35:1267-1274.
24. Masuda A., Hashimoto K., Yokoi T., Doi T., Kodama T., Kume H., et al. Essential role of GATA transcriptional factors in the activation of mast cells. J Immunol 2007, 178:360-368.
25. Prieschl E.E., Gouilleux-Gruart V., Walker C., Harrer N.E., Baumruker T. A nuclear factor of activated T cell-like transcription factor in mast cells is involved in IL-5 gene regulation after IgE plus antigen stimulation. J Immunol 1995, 154:6112-6119.
26. Masuda A., Yoshikai Y., Kume H., Matsuguchi T. The interaction between GATA proteins and activator protein-1 promotes the transcription of IL-13 in mast cells. J Immunol 2004, 173:5564-5573.
27. Yun M.R., Lee J.Y., Park H.S., Heo H.J., Park J.Y., Bae S.S., et al. Oleic acid enhances vascular smooth muscle cell proliferation via phosphatidylinositol 3-kinase/Akt signaling pathway. Pharmacol Res 2006, 54:97-102.
28. Nieto N. Ethanol and fish oil induce NFkappaB transactivation of the collagen alpha2(I) promoter through lipid peroxidation-driven activation of the PKC-PI3K-Akt pathway. Hepatology 2007, 45:1433-1445.
29. Leung D.Y., Hirsch R.L., Schneider L., Moody C., Takaoka R., Li S.H., et al. Thymopentin therapy reduces the clinical severity of atopic dermatitis. J Allergy Clin Immunol 1990, 85:927-933.
30. Zon L.I., Gurish M.F., Stevens R.L., Mather C., Reynolds D.S., Austen K.F., et al. GATA-binding transcription factors in mast cells regulate the promoter of the mast cell carboxypeptidase A gene. J Biol Chem 1991, 266:22948-22953.
31. Watanabe N., Tomimori Y., Saito K., Miura K., Wada A., Tsudzuki M., et al. Chymase inhibitor improves dermatitis in NC/Nga mice. Int Arch Allergy Immunol 2002, 128:229-234.
32. Galli S.J., Tsai M., Piliponsky A.M. The development of allergic inflammation. Nature 2008, 454:445-454.
33. Grimbaldeston M.A., Metz M., Yu M., Tsai M., Galli S.J. Effector and potential immunoregulatory roles of mast cells in IgE-associated acquired immune responses. Curr Opin Immunol 2006, 18:751-760.
34. Wallace F.A., Miles E.A., Evans C., Stock T.E., Yaqoob P., Calder P.C. Dietary fatty acids influence the production of Th1- but not Th2-type cytokines. J Leukoc Biol 2001, 69:449-457.
35. Chang H.H., Chen C.S., Lin J.Y. Dietary perilla oil inhibits proinflammatory cytokine production in the bronchoalveolar lavage fluid of ovalbumin-challenged mice. Lipids 2008, 43:499-506.
36. Zhang P., Smith R., Chapkin R.S., McMurray D.N. Dietary (n-3) polyunsaturated fatty acids modulate murine Th1/Th2 balance toward the Th2 pole by suppression of Th1 development. J Nutr 2005, 135:1745-1751.
37. El Gazzar M.A. Thymoquinone suppressses in vitro production of IL-5 and IL-13 by mast cells in response to lipopolysaccharide stimulation. Inflamm Res 2007, 56:345-351.
38. Merika M., Orkin S.H. DNA-binding specificity of GATA family transcription factors. Mol Cell Biol 1993, 13:3999-4010.
39. Visvader J., Adams J.M. Megakaryocytic differentiation induced in 416B myeloid cells by GATA-2 and GATA-3 transgenes or 5-azacytidine is tightly coupled to GATA-1 expression. Blood 1993, 82:1493-1501.
40. Migliaccio A.R., Rana R.A., Sanchez M., Lorenzini R., Centurione L., Bianchi L., et al. GATA-1 as a regulator of mast cell differentiation revealed by the phenotype of the GATA-1low mouse mutant. J Exp Med 2003, 197:281-296.
41. Tsai F.Y., Orkin S.H. Transcription factor GATA-2 is required for proliferation/survival of early hematopoietic cells and mast cell formation, but not for erythroid and myeloid terminal differentiation. Blood 1997, 89:3636-3643.
42. Boyes J., Byfield P., Nakatani Y., Ogryzko V. Regulation of activity of the transcription factor GATA-1 by acetylation. Nature 1998, 396:594-598.
43. Hernandez-Hernandez A., Ray P., Litos G., Ciro M., Ottolenghi S., Beug H., et al. Acetylation and MAPK phosphorylation cooperate to regulate the degradation of active GATA-1. EMBO J 2006, 25:3264-3274.
44. Collavin L., Gostissa M., Avolio F., Secco P., Ronchi A., Santoro C., et al. Modification of the erythroid transcription factor GATA-1 by SUMO-1. Proc Natl Acad Sci USA 2004, 101:8870-8875.
45. Calder P.C. The relationship between the fatty acid composition of immune cells and their function. Prostaglandins Leukot Essent Fatty Acids 2008, 79:101-108.
46. Lee J.Y., Ye J., Gao Z., Youn H.S., Lee W.H., Zhao L., et al. Reciprocal modulation of Toll-like receptor-4 signaling pathways involving MyD88 and phosphatidylinositol 3-kinase/AKT by saturated and polyunsaturated fatty acids. J Biol Chem 2003, 278:37041-37051.
47. Mirnikjoo B., Brown S.E., Kim H.F., Marangell L.B., Sweatt J.D., Weeber E.J. Protein kinase inhibition by omega-3 fatty acids. J Biol Chem 2001, 276:10888-10896.
48. Deckelbaum R.J., Worgall T.S., Seo T. n-3 fatty acids and gene expression. Am J Clin Nutr 2006, 83:1520S-1525S.
49. Yu Y.L., Chiang Y.J., Chen Y.C., Papetti M., Juo C.G., Skoultchi A.I., et al. MAPK-mediated phosphorylation of GATA-1 promotes Bcl-XL expression and cell survival. J Biol Chem 2005, 280:29533-29542.
50. Madani S., Hichami A., Cherkaoui-Malki M., Khan N.A. Diacylglycerols containing Omega 3 and Omega 6 fatty acids bind to RasGRP and modulate MAP kinase activation. J Biol Chem 2004, 279:1176-1183.
51. Yamashita M., Nakayama T. Progress in allergy signal research on mast cells: regulation of allergic airway inflammation through toll-like receptor 4-mediated modification of mast cell function. J Pharmacol Sci 2008, 106:332-335.
52. Jiang C., Ting A.T., Seed B. PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines. Nature 1998, 391:82-86.
53. Calder P.C. Polyunsaturated fatty acids, inflammatory processes and inflammatory bowel diseases. Mol Nutr Food Res 2008, 52:885-897.
54. Connor W.E. Importance of n-3 fatty acids in health and disease. Am J Clin Nutr 2000, 71:171S-175S.