The polyunsaturated fatty acids arachidonic acid and docosahexaenoic acid induce mouse dendritic cells maturation but reduce T-cell responses in vitro

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Carlsson, Johan A ^a   Wold, Agnes E ^a   Sandberg, Ann Sofie ^b   Östman, Sofia M ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACID; B7 ANTIGEN; CD40 ANTIGEN; CD69 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; DOCOSAHEXAENOIC ACID; GAMMA INTERFERON; ICOSAPENTAENOIC ACID; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; LINOLEIC ACID; LINOLENIC ACID; OLEIC ACID; OVALBUMIN; PROGRAMMED DEATH 1 LIGAND 1; PROSTAGLANDIN E2; TRANSCRIPTION FACTOR FOXP3; BIOLOGICAL MARKER;

ANIMAL CELL; ARTICLE; CELL MATURATION; COCULTURE; CONTROLLED STUDY; DENDRITIC CELL; FATTY ACID ANALYSIS; FLOW CYTOMETRY; GAS CHROMATOGRAPHY; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; NONHUMAN; PHENOTYPE; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; LYMPHOCYTE ACTIVATION; METABOLISM; SPLEEN;

ANIMALS; ARACHIDONIC ACID; BIOMARKERS; CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; DENDRITIC CELLS; DOCOSAHEXAENOIC ACIDS; GENE EXPRESSION REGULATION; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; SPLEEN; T-LYMPHOCYTES;

EID: 84957552114     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0143741     Document Type: Article

References (61)

1. Knight SC. Specialized perinodal fat fuels and fashions immunity. Immunity. 2008; 28(2): 135-8. Epub 2008/02/16. doi: 10.1016/j.immuni.2008.01.003 PMID: 18275823.
2. Murphy MG. Dietary fatty acids and membrane protein function. The Journal of nutritional biochemistry. 1990; 1(2): 68-79. Epub 1990/02/01. PMID: 15539188.
3. Sala-Vila A, Miles EA, Calder PC. Fatty acid composition abnormalities in atopic disease: Evidence explored and role in the disease process examined. Clinical and experimental allergy: Journal of the British Society for Allergy and Clinical Immunology. 2008; 38(9): 1432-50. Epub 2008/07/31. doi: 10. 1111/j.1365-2222.2008.03072.x PMID: 18665842.
4. Shapiro AC, Wu D, Meydani SN. Eicosanoids derived from arachidonic and eicosapentaenoic acids inhibit T cell proliferative response. Prostaglandins. 1993; 45(3): 229-40. PMID: 8387219.
5. Calder PC, Bond JA, Bevan SJ, Hunt SV, Newsholme EA. Effect of fatty acids on the proliferation of concanavalin A-stimulated rat lymph node lymphocytes. The International journal of biochemistry. 1991; 23(5-6): 579-88. Epub 1991/01/01. PMID: 2065818.
6. Brouard C, Pascaud M. Modulation of rat and human lymphocyte function by n-6 and n-3 polyunsaturated fatty acids and acetylsalicylic acid. Annals of nutrition & metabolism. 1993; 37(3): 146-59. PMID: 8373139.
7. Jolly CA, Jiang YH, Chapkin RS, McMurray DN. Dietary (n-3) polyunsaturated fatty acids suppress murine lymphoproliferation, interleukin-2 secretion, and the formation of diacylglycerol and ceramide. The Journal of nutrition. 1997; 127(1): 37-43. PMID: 9040541.
8. Zurier RB, Rossetti RG, Seiler CM, Laposata M. Human peripheral blood T lymphocyte proliferation after activation of the T cell receptor: Effects of unsaturated fatty acids. Prostaglandins, leukotrienes, and essential fatty acids. 1999; 60(5-6): 371-5. PMID: 10471124.
9. DeMarco DM, Santoli D, Zurier RB. Effects of fatty acids on proliferation and activation of human synovial compartment lymphocytes. J Leukoc Biol. 1994; 56(5): 612-5. PMID: 7964169.
10. Calder PC. Fatty-Acids, Dietary Lipids and Lymphocyte Functions. Biochemical Society transactions. 1995; 23(2): 302-9. WOS: A1995RE08500020. PMID: 7672330
11. Brix S, Lund P, Kjaer TM, Straarup EM, Hellgren LI, Frøkiaer H. CD4(+) T-cell activation is differentially modulated by bacteria-primed dendritic cells, but is generally down-regulated by n-3 polyunsaturated fatty acids. Immunology. 2010; 129(3): 338-50. Epub 2009/11/17. doi: 10.1111/j.1365-2567.2009. 03163.x PMID: 19909377; PubMed Central PMCID: PMC2826679.
12. Zeyda M, Szekeres AB, Säemann MD, Geyeregger R, Stockinger H, Zlabinger GJ, et al. Suppression of T cell signaling by polyunsaturated fatty acids: Selectivity in inhibition of mitogen-activated protein kinase and nuclear factor activation. Journal of immunology. 2003; 170(12): 6033-9. PMID: 12794131.
13. Johansson S, Lönnqvist A, Östman S, Sandberg AS, Wold AE. Long-chain polyunsaturated fatty acids are consumed during allergic inflammation and affect T helper type 1 (Th1)- And Th2-mediated hypersensitivity differently. Clin Exp Immunol. 2010; 160(3): 411-9. Epub 2010/02/13. doi: 10.1111/j.1365- 2249.2010.04107.x PMID: 20148912; PubMed Central PMCID: PMC2883112.
14. Ganguly D, Haak S, Sisirak V, Reizis B. The role of dendritic cells in autoimmunity. Nature reviews Immunology. 2013; 13(8): 566-77. doi: 10.1038/nri3477 PMID: 23827956.
15. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, et al. Immunobiology of dendritic cells. Annual review of immunology. 2000; 18: 767-811. doi: 10.1146/annurev.immunol.18.1.767 PMID: 10837075.
16. Wu L, Dakic A. Development of dendritic cell system. Cellular & molecular immunology. 2004; 1 (2): 112-8. PMID: 16212897.
17. Zarnani AH, Moazzeni SM, Shokri F, Salehnia M, Jeddi-Tehrani M. Kinetics of murine decidual dendritic cells. Reproduction. 2007; 133(1): 275-83. doi: 10.1530/rep.1.01232 PMID: 17244753.
18. Süss G, Shortman K. A subclass of dendritic cells kills CD4 T cells via Fas/Fas-ligand-induced apoptosis. The Journal of experimental medicine. 1996; 183(4): 1789-96. PMID: 8666935; PubMed Central PMCID: PMC2192509.
19. Maldonado-López R, De Smedt T, Michel P, Godfroid J, Pajak B, Heirman C, et al. CD8alpha+ and CD8alpha- subclasses of dendritic cells direct the development of distinct T helper cells in vivo. The Journal of experimental medicine. 1999; 189(3): 587-92. PMID: 9927520; PubMed Central PMCID: PMC2192907.
20. Berchtold S, Muhl-Zurbes P, Heufler C, Winklehner P, Schuler G, Steinkasserer A. Cloning, recombinant expression and biochemical characterization of the murine CD83 molecule which is specifically upregulated during dendritic cell maturation. FEBS letters. 1999; 461(3): 211-6. PMID: 10567699.
21. Zheng Y, Manzotti CN, Liu M, Burke F, Mead KI, Sansom DM. CD86 and CD80 differentially modulate the suppressive function of human regulatory T cells. Journal of immunology. 2004; 172(5): 2778-84. Epub 2004/02/24. PMID: 14978077.
22. Krummel MF, Allison JP. CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. The Journal of experimental medicine. 1995; 182(2): 459-65. PMID: 7543139; PubMed Central PMCID: PMC2192127.
23. Fife BT, Pauken KE, Eagar TN, Obu T, Wu J, Tang Q, et al. Interactions between PD-1 and PD-L1 promote tolerance by blocking the TCR-induced stop signal. Nature immunology. 2009; 10(11): 1185-92. doi: 10.1038/ni.1790 PMID: 19783989; PubMed Central PMCID: PMC2778301.
24. Francisco LM, Sage PT, Sharpe AH. The PD-1 pathway in tolerance and autoimmunity. Immunological reviews. 2010; 236: 219-42. doi: 10.1111/j.1600-065X.2010.00923.x PMID: 20636820; PubMed Central PMCID: PMC2919275.
25. Zeyda M, Säemann MD, Stuhlmeier KM, Mascher DG, Nowotny PN, Zlabinger GJ, et al. Polyunsaturated fatty acids block dendritic cell activation and function independently of NF-kappaB activation. The Journal of biological chemistry. 2005; 280(14): 14293-301. doi: 10.1074/jbc.M410000200 PMID: 15684433.
26. Sanderson P, MacPherson GG, Jenkins CH, Calder PC. Dietary fish oil diminishes the antigen presentation activity of rat dendritic cells. J Leukoc Biol. 1997; 62(6): 771-7. PMID: 9400818.
27. Teague H, Rockett BD, Harris M, Brown DA, Shaikh SR. Dendritic cell activation, phagocytosis and CD69 expression on cognate T cells are suppressed by n-3 long-chain polyunsaturated fatty acids. Immunology. 2013; 139(3): 386-94. doi: 10.1111/imm.12088 PMID: 23373457; PubMed Central PMCID: PMC3701185.
28. Weatherill AR, Lee JY, Zhao L, Lemay DG, Youn HS, Hwang DH. Saturated and polyunsaturated fatty acids reciprocally modulate dendritic cell functions mediated through TLR4. Journal of immunology. 2005; 174(9): 5390-7. Epub 2005/04/22. PMID: 15843537.
29. Wang H, Hao Q, Li QR, Yan XW, Ye S, Li YS, et al. Omega-3 polyunsaturated fatty acids affect lipopolysaccharide- induced maturation of dendritic cells through mitogen-activated protein kinases p38. Nutrition. 2007; 23(6): 474-82. doi: 10.1016/j.nut.2007.04.002 PMID: 17499970.
30. Kong W, Yen JH, Vassiliou E, Adhikary S, Toscano MG, Ganea D. Docosahexaenoic acid prevents dendritic cell maturation and in vitro and in vivo expression of the IL-12 cytokine family. Lipids in health and disease. 2010; 9: 12. doi: 10.1186/1476-511X-9-12 PMID: 20122166; PubMed Central PMCID: PMC2827414.
31. Hughes DA, Southon S, Pinder AC. (n-3) Polyunsaturated fatty acids modulate the expression of functionally associated molecules on human monocytes in vitro. The Journal of nutrition. 1996; 126(3): 603-10. PMID: 8598544.
32. Zapata-Gonzalez F, Rueda F, Petriz J, Domingo P, Villarroya F, Diaz-Delfin J, et al. 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. 2008; 84(4): 1172-82. doi: 10.1189/jlb.1007688 PMID: 18632990.
33. Itakura H, Yokoyama M, Matsuzaki M, Saito Y, Origasa H, Ishikawa Y, et al. Relationships between plasma fatty acid composition and coronary artery disease. J Atheroscler Thromb. 2011; 18(2): 99-107. PMID: 21099130.
34. Marangoni F, Angeli MT, Colli S, Eligini S, Tremoli E, Sirtori CR, et al. Changes of n-3 and n-6 fatty acids in plasma and circulating cells of normal subjects, after prolonged administration of 20: 5 (EPA) and 22: 6 (DHA) ethyl esters and prolonged washout. Biochimica et biophysica acta. 1993; 1210(1): 55-62. PMID: 8257719.
35. Prazma CM, Yazawa N, Fujimoto Y, Fujimoto M, Tedder TF. CD83 expression is a sensitive marker of activation required for B cell and CD4+ T cell longevity in vivo. Journal of immunology. 2007; 179 (7): 4550-62. Epub 2007/09/20. PMID: 17878352.
36. Lechmann M, Berchtold S, Hauber J, Steinkasserer A. CD83 on dendritic cells: More than just a marker for maturation. Trends in immunology. 2002; 23(6): 273-5. PMID: 12072358.
37. Francisco LM, Salinas VH, Brown KE, Vanguri VK, Freeman GJ, Kuchroo VK, et al. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. The Journal of experimental medicine. 2009; 206(13): 3015-29. doi: 10.1084/jem.20090847 PMID: 20008522; PubMed Central PMCID: PMC2806460.
38. Zheng Y, Rudensky AY. Foxp3 in control of the regulatory T cell lineage. Nature immunology. 2007; 8 (5): 457-62. doi: 10.1038/ni1455 PMID: 17440451.
39. Iwami D, Zhang Q, Aramaki O, Nonomura K, Shirasugi N, Niimi M. Purified eicosapentaenoic acid induces prolonged survival of cardiac allografts and generates regulatory T cells. American journal of transplantation: Official journal of the American Society of Transplantation and the American Society of Transplant Surgeons. 2009; 9(6): 1294-307. doi: 10.1111/j.1600-6143.2009.02641.x PMID: 19459813.
40. Weise C, Heunemann C, Loddenkemper C, Herz U, van Tol EA, Worm M. Dietary docosahexaenoic acid in combination with arachidonic acid ameliorates allergen-induced dermatitis in mice. Pediatric allergy and immunology: Official publication of the European Society of Pediatric Allergy and Immunology. 2011; 22(5): 497-504. Epub 2011/02/08. doi: 10.1111/j.1399-3038.2010.01133.x PMID: 21294775.
41. Wang L, Pino-Lagos K, de Vries VC, Guleria I, Sayegh MH, Noelle RJ. Programmed death 1 ligand signaling regulates the generation of adaptive Foxp3+CD4+ regulatory T cells. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105(27): 9331-6. doi: 10.1073/ pnas.0710441105 PMID: 18599457; PubMed Central PMCID: PMC2442817.
42. Brunet JF, Denizot F, Luciani MF, Roux-Dosseto M, Suzan M, Mattei MG, et al. A new member of the immunoglobulin superfamily-CTLA-4. Nature. 1987; 328(6127): 267-70. doi: 10.1038/328267a0 PMID: 3496540.
43. Zheng SG, Wang JH, Stohl W, Kim KS, Gray JD, Horwitz DA. TGF-beta requires CTLA-4 early after T cell activation to induce FoxP3 and generate adaptive CD4+CD25+ regulatory cells. Journal of immunology. 2006; 176(6): 3321-9. PMID: 16517699.
44. Linsley PS, Greene JL, Tan P, Bradshaw J, Ledbetter JA, Anasetti C, et al. Coexpression and functional cooperation of CTLA-4 and CD28 on activated T lymphocytes. The Journal of experimental medicine. 1992; 176(6): 1595-604. PMID: 1334116; PubMed Central PMCID: PMC2119471.
45. Freeman GJ, Long AJ, Iwai Y, Bourque K, Chernova T, Nishimura H, et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. The Journal of experimental medicine. 2000; 192(7): 1027-34. PMID: 11015443; PubMed Central PMCID: PMC2193311.
46. Ishida Y, Agata Y, Shibahara K, Honjo T. Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J. 1992; 11(11): 3887-95. PMID: 1396582; PubMed Central PMCID: PMC556898.
47. Fujimoto Y, Tu L, Miller AS, Bock C, Fujimoto M, Doyle C, et al. CD83 expression influences CD4+ T cell development in the thymus. Cell. 2002; 108(6): 755-67. PMID: 11955430.
48. Hirano N, Butler MO, Xia Z, Ansen S, von Bergwelt-Baildon MS, Neuberg D, et al. Engagement of CD83 ligand induces prolonged expansion of CD8+ T cells and preferential enrichment for antigen specificity. Blood. 2006; 107(4): 1528-36. doi: 10.1182/blood-2005-05-2073 PMID: 16239433; PubMed Central PMCID: PMC1895397.
49. Prechtel AT, Turza NM, Theodoridis AA, Steinkasserer A. CD83 knockdown in monocyte-derived dendritic cells by small interfering RNA leads to a diminished T cell stimulation. Journal of immunology. 2007; 178(9): 5454-64. PMID: 17442926.
50. Aerts-Toegaert C, Heirman C, Tuyaerts S, Corthals J, Aerts JL, Bonehill A, et al. CD83 expression on dendritic cells and T cells: Correlation with effective immune responses. European journal of immunology. 2007; 37(3): 686-95. doi: 10.1002/eji.200636535 PMID: 17301951.
51. Kuwano Y, Prazma CM, Yazawa N, Watanabe R, Ishiura N, Kumanogoh A, et al. CD83 influences cellsurface MHC class II expression on B cells and other antigen-presenting cells. International immunology. 2007; 19(8): 977-92. doi: 10.1093/intimm/dxm067 PMID: 17804692.
52. Kretschmer B, Luthje K, Guse AH, Ehrlich S, Koch-Nolte F, Haag F, et al. CD83 modulates B cell function in vitro: Increased IL-10 and reduced Ig secretion by CD83Tg B cells. PloS one. 2007; 2(8): E755. doi: 10.1371/journal.pone.0000755 PMID: 17710154; PubMed Central PMCID: PMC1940313.
53. Hock BD, Haring LF, Steinkasserer A, Taylor KG, Patton WN, McKenzie JL. The soluble form of CD83 is present at elevated levels in a number of hematological malignancies. Leukemia research. 2004; 28 (3): 237-41. PMID: 14687618.
54. Lechmann M, Krooshoop DJ, Dudziak D, Kremmer E, Kuhnt C, Figdor CG, et al. The extracellular domain of CD83 inhibits dendritic cell-mediated T cell stimulation and binds to a ligand on dendritic cells. The Journal of experimental medicine. 2001; 194(12): 1813-21. PMID: 11748282; PubMed Central PMCID: PMC2193570.
55. Chen L, Zhu Y, Zhang G, Gao C, Zhong W, Zhang X. CD83-stimulated monocytes suppress T-cell immune responses through production of prostaglandin E2. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108(46): 18778-83. doi: 10.1073/pnas.1018994108 PMID: 22065790; PubMed Central PMCID: PMC3219128.
56. Cramer SO, Trumpfheller C, Mehlhoop U, More S, Fleischer B, von Bonin A. Activation-induced expression of murine CD83 on T cells and identification of a specific CD83 ligand on murine B cells. International immunology. 2000; 12(9): 1347-51. PMID: 10967030.
57. Sampath H, Ntambi JM. Polyunsaturated fatty acid regulation of gene expression. Nutrition reviews. 2004; 62(9): 333-9. PMID: 15497766.
58. Gosset P, Charbonnier AS, Delerive P, Fontaine J, Staels B, Pestel J, et al. Peroxisome proliferatoractivated receptor gamma activators affect the maturation of human monocyte-derived dendritic cells. European journal of immunology. 2001; 31(10): 2857-65. PMID: 11592060.
59. Klotz L, Dani I, Edenhofer F, Nolden L, Evert B, Paul B, et al. Peroxisome proliferator-activated receptor gamma control of dendritic cell function contributes to development of CD4+ T cell anergy. Journal of immunology. 2007; 178(4): 2122-31. PMID: 17277116.
60. Herber DL, Cao W, Nefedova Y, Novitskiy SV, Nagaraj S, Tyurin VA, et al. Lipid accumulation and dendritic cell dysfunction in cancer. Nature medicine. 2010; 16(8): 880-6. doi: 10.1038/nm.2172 PMID: 20622859; PubMed Central PMCID: PMC2917488.
61. Ibrahim J, Nguyen AH, Rehman A, Ochi A, Jamal M, Graffeo CS, et al. Dendritic Cell Populations With Different Concentrations of Lipid Regulate Tolerance and Immunity in Mouse and Human Liver. Gastroenterology. 2012. Epub 2012/06/19. doi: 10.1053/j.gastro.2012.06.003 PMID: 22705178.