Regulatory activity of polyunsaturated fatty acids in T-cell signaling

Progress in Lipid Research

Volumn 49, Issue 3, 2010, Pages 250-261

  Kim, Wooki ^a   Khan, Naim A ^b   McMurray, David N ^a,c   Prior, Ian A ^d   Wang, Naisyin ^a   Chapkin, Robert S ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITÉ DE BOURGOGNE   (France)

^c TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^d UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Docosahexaeonic acid; Eicosapentaenoic acid; Lipid rafts; Lymphocyte; Membrane biology; Protein kinase C

Indexed keywords

BIOLOGICAL MARKER; DIACYLGLYCEROL; GANGLIOSIDE GM1; IMMUNOSUPPRESSIVE AGENT; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE A2; POLYUNSATURATED FATTY ACID; PROTEIN KINASE C;

AMINO ACID SYNTHESIS; ANTIGEN PRESENTING CELL; APOPTOSIS; BIOCHEMISTRY; CALCIUM SIGNALING; CELL POLARITY; ENZYME ACTIVATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; IMMUNOLOGICAL SYNAPSE; LABELING INDEX; LIPID RAFT; LYMPHOCYTE DIFFERENTIATION; MOLECULAR PROBE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; SUPPRESSOR CELL; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH2 CELL;

APOPTOSIS; CALCIUM SIGNALING; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FATTY ACIDS, UNSATURATED; PROTEIN KINASE C; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 77952107281     PISSN: 01637827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plipres.2010.01.002     Document Type: Review

References (155)

1. Chapkin R.S. Reappraisal of the essential fatty acids. In: Chow C.K. (Ed). Fatty acids in foods and their health implications. 3rd ed. (2008), CRC Press, New York 675-691
2. Lewis R.A., Austen K.F., and Soberman R.J. Leukotrienes and other products of the 5-lipoxygenase pathway. Biochemistry and relation to pathobiology in human diseases. N Engl J Med 323 (1990) 645-655
3. Lands W.E. Biosynthesis of prostaglandins. Annu Rev Nutr 11 (1991) 41-60
4. Calder P.C. N-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr 83 (2006) 1505S-1519S
5. Calder P.C. Dietary modification of inflammation with lipids. Proc Nutr Soc 61 (2002) 345-358
6. Serhan C.N. Systems approach to inflammation resolution: identification of novel anti-inflammatory and pro-resolving mediators. J Thromb Haemost 7 Suppl. 1 (2009) 44-48
7. Calder P.C. Polyunsaturated fatty acids and inflammatory processes: new twists in an old tale. Biochimie 91 (2009) 791-795
8. Spector A.A. Essentiality of fatty acids. Lipids 34 Suppl. (1999) S1-S3
9. Simopoulos A.P. Omega-3 fatty acids in health and disease and in growth and development. Am J Clin Nutr 54 (1991) 438-463
10. Kremer J.M. Clinical studies of omega-3 fatty acid supplementation in patients who have rheumatoid arthritis. Rheum Dis Clin North Am 17 (1991) 391-402
11. Nielsen G.L., Faarvang K.L., Thomsen B.S., Teglbjaerg K.L., Jensen L.T., Hansen T.M., et al. The effects of dietary supplementation with n-3 polyunsaturated fatty acids in patients with rheumatoid arthritis: a randomized, double blind trial. Eur J Clin Invest 22 (1992) 687-691
12. Skoldstam L., Borjesson O., Kjallman A., Seiving B., and Akesson B. Effect of six months of fish oil supplementation in stable rheumatoid arthritis. A double-blind, controlled study. Scand J Rheumatol 21 (1992) 178-185
13. Geusens P., Wouters C., Nijs J., Jiang Y., and Dequeker J. Long-term effect of omega-3 fatty acid supplementation in active rheumatoid arthritis. A 12-month, double-blind, controlled study. Arthritis Rheum 37 (1994) 824-829
14. Calder P.C. Session 3: joint nutrition society and Irish nutrition and dietetic institute symposium on 'nutrition and autoimmune disease' PUFA, inflammatory processes and rheumatoid arthritis. Proc Nutr Soc 67 (2008) 409-418
15. Galarraga B., Ho M., Youssef H.M., Hill A., McMahon H., Hall C., et al. Cod liver oil (n-3 fatty acids) as a non-steroidal anti-inflammatory drug sparing agent in rheumatoid arthritis. Rheumatology (Oxford) 47 (2008) 665-669
16. Kremer J.M. n-3 fatty acid supplements in rheumatoid arthritis. Am J Clin Nutr 71 (2000) 349S-351S
17. Dawczynski C., Schubert R., Hein G., Muller A., Eidner T., Vogelsang H., et al. Long-term moderate intervention with n-3 long-chain PUFA-supplemented dairy products: effects on pathophysiological biomarkers in patients with rheumatoid arthritis. Br J Nutr 101 (2009) 1517-1526
18. Yaqoob P., and Calder P. Effects of dietary lipid manipulation upon inflammatory mediator production by murine macrophages. Cell Immunol 163 (1995) 120-128
19. Endres S., Meydani S.N., Ghorbani R., Schindler R., and Dinarello C.A. Dietary supplementation with n-3 fatty acids suppresses interleukin-2 production and mononuclear cell proliferation. J Leukocyte Biol 54 (1993) 599-603
20. Meydani S.N., Endres S., Woods M.M., Goldin B.R., Soo C., Morrill-Labrode A., et al. Oral (n-3) fatty acid supplementation suppresses cytokine production and lymphocyte proliferation: comparison between young and older women. J Nutr 121 (1991) 547-555
21. Jolly C.A., McMurray D.N., and Chapkin R.S. Effect of dietary n-3 fatty acids on interleukin-2 and interleukin-2 receptor alpha expression in activated murine lymphocytes. Prostag Leukot Essent Fatty Acids 58 (1998) 289-293
22. Bittiner S.B., Tucker W.F., Cartwright I., and Bleehen S.S. A double-blind, randomised, placebo-controlled trial of fish oil in psoriasis. Lancet 1 (1988) 378-380
23. Bjorneboe A., Soyland E., Bjorneboe G.E., Rajka G., and Drevon C.A. Effect of dietary supplementation with eicosapentaenoic acid in the treatment of atopic dermatitis. Br J Dermatol 117 (1987) 463-469
24. Bates D., Cartlidge N.E., French J.M., Jackson M.J., Nightingale S., Shaw D.A., et al. A double-blind controlled trial of long chain n-3 polyunsaturated fatty acids in the treatment of multiple sclerosis. J Neurol Neurosurg Psychiatry 52 (1989) 18-22
25. Lauer K. The risk of multiple sclerosis in the USA in relation to sociogeographic features: a factor-analytic study. J Clin Epidemiol 47 (1994) 43-48
26. Kampman M.T., Wilsgaard T., and Mellgren S.I. Outdoor activities and diet in childhood and adolescence relate to MS risk above the Arctic Circle. J Neurol 254 (2007) 471-477
27. Schwarz S., Knorr C., Geiger H., and Flachenecker P. Complementary and alternative medicine for multiple sclerosis. Mult Scler 14 (2008) 1113-1119
28. Cleland L.G., James M.J., and Proudman S.M. The role of fish oils in the treatment of rheumatoid arthritis. Drugs 63 (2003) 845-853
29. Mehta L.R., Dworkin R.H., and Schwid S.R. Polyunsaturated fatty acids and their potential therapeutic role in multiple sclerosis. Nat Clin Pract Neurol 5 (2009) 82-92
30. Fetterman Jr. J.W., and Zdanowicz M.M. Therapeutic potential of n-3 polyunsaturated fatty acids in disease. Am J Health Syst Pharm 66 (2009) 1169-1179
31. Mosmann T.R., and Sad S. The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today 17 (1996) 138-146
32. Liblau R.S., Singer S.M., and McDevitt H.O. Th1 and Th2 CD4+ T cells in the pathogenesis of organ-specific autoimmune diseases. Immunol Today 16 (1995) 34-38
33. Arrington J.L., Chapkin R.S., Switzer K.C., Morris J.S., and McMurray D.N. Dietary n-3 polyunsaturated fatty acids modulate purified murine T-cell subset activation. Clin Exp Immunol 125 (2001) 499-507
34. Kleemann R., Scott F.W., Worz-Pagenstert U., Nimal Ratnayake W.M., and Kolb H. Impact of dietary fat on Th1/Th2 cytokine gene expression in the pancreas and gut of diabetes-prone BB rats. J Autoimmun 11 (1998) 97-103
35. Wallace F.A., Miles E.A., Evans C., Stock T.E., Yaqoob P., and Calder P.C. Dietary fatty acids influence the production of Th1- but not Th2-type cytokines. J Leukocyte Biol 69 (2001) 449-457
36. Mizota T., Fujita-Kambara C., Matsuya N., Hamasaki S., Fukudome T., Goto H., et al. Effect of dietary fatty acid composition on Th1/Th2 polarization in lymphocytes. JPEN J Parenter Enteral Nutr 33 (2009) 390-396
37. Sierra S., Lara-Villoslada F., Comalada M., Olivares M., and Xaus J. Dietary fish oil n-3 fatty acids increase regulatory cytokine production and exert anti-inflammatory effects in two murine models of inflammation. Lipids 41 (2006) 1115-1125
38. Zhang P., Smith R., Chapkin R.S., and 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 135 (2005) 1745-1751
39. Switzer K.C., McMurray D.N., Morris J.S., and Chapkin R.S. (n-3) Polyunsaturated fatty acids promote activation-induced cell death in murine T lymphocytes. J Nutr 133 (2003) 496-503
40. Switzer K.C., Fan Y.Y., Wang N., McMurray D.N., and Chapkin R.S. Dietary n-3 polyunsaturated fatty acids promote activation-induced cell death in Th1-polarized murine CD4+ T-cells. J Lipid Res 45 (2004) 1482-1492
41. Tsou S.S., Chiu W.C., Yeh C.L., Hou Y.C., and Yeh S.L. Effects of omega-3 fatty acids on inflammatory mediators and splenocyte cytokine mRNA expressions in rats with polymicrobial sepsis. Nutrition 24 (2008) 484-491
42. Maes M., Mihaylova I., Kubera M., and Bosmans E. Why fish oils may not always be adequate treatments for depression or other inflammatory illnesses: docosahexaenoic acid, an omega-3 polyunsaturated fatty acid, induces a Th-1-like immune response. Neuroendocrinol Lett 28 (2007) 875-880
43. Matsuda A., Furukawa K., Takasaki H., Suzuki H., Kan H., Tsuruta H., et al. Preoperative oral immune-enhancing nutritional supplementation corrects TH1/TH2 imbalance in patients undergoing elective surgery for colorectal cancer. Dis Colon Rectum 49 (2006) 507-516
44. Lin M.T., Yeh S.L., Yeh C.L., Lai Y.N., Chang K.J., Lee P.H., et al. Parenteral n-3 fatty acids modulate inflammatory and immune response in rats undergoing total gastrectomy. Shock 25 (2006) 56-60
45. Zhang P., Kim W., Zhou L., Wang N., Ly L., McMurray M., et al. Dietary fish oil inhibits antigen-specific Th1 cell development by suppression of clonal expansion. J Nutr 136 (2006) 2391-2398
46. Ho I.C., and Glimcher L.H. Transcription: tantalizing times for T cells. Cell 109 Suppl. (2002) S109-120
47. Szabo S.J., Kim S.T., Costa G.L., Zhang X., Fathman C.G., and Glimcher L.H. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100 (2000) 655-669
48. Yamashita M., Ukai-Tadenuma M., Miyamoto T., Sugaya K., Hosokawa H., Hasegawa A., et al. Essential role of GATA3 for the maintenance of type 2 helper T (Th2) cytokine production and chromatin remodeling at the Th2 cytokine gene loci. J Biol Chem 279 (2004) 26983-26990
49. Issemann I., Prince R.A., Tugwood J.D., and Green S. The peroxisome proliferator-activated receptor: retinoid X receptor heterodimer is activated by fatty acids and fibrate hypolipidaemic drugs. J Mol Endocrinol 11 (1993) 37-47
50. Attakpa E., Hichami A., Simonin A.M., Sanson E.G., Dramane K.L., and Khan N.A. Docosahexaenoic acid modulates the expression of T-bet and GATA-3 transcription factors, independently of PPARalpha, through suppression of MAP kinase activation. Biochimie 91 (2009) 1359-1365
51. Shaikh S.R., Dumaual A.C., Castillo A., LoCascio D., Siddiqui R.A., Stillwell W., et al. Oleic and docosahexaenoic acid differentially phase separate from lipid raft molecules: a comparative NMR, DSC, AFM, and detergent extraction study. Biophys J 87 (2004) 1752-1766
52. Shaikh S.R., Rockett B.D., Salameh M., and Carraway K. Docosahexaenoic acid modifies the clustering and size of lipid rafts and the lateral organization and surface expression of MHC class I of EL4 cells. J Nutr 139 (2009) 1632-1639
53. Denys A., Hichami A., and Khan N.A. n-3 PUFAs modulate T-cell activation via protein kinase C-alpha and -epsilon and the NF-kappaB signaling pathway. J Lipid Res 46 (2005) 752-758
54. 2+-independent phospholipase A(2) enzymes from P388D(1) macrophages and Chinese hamster ovary cells. J Biol Chem 272 (1997) 8576-8580
55. Le Gouvello S., Colard O., Theodorou I., Bismuth G., Tarantino N., and Debre P. CD2 triggering stimulates a phospholipase A2 activity beside the phospholipase C pathway in human T lymphocytes. J Immunol 144 (1990) 2359-2364
56. 2 in remodeling and increased susceptibility of proliferating T cells to CoA-independent transacyclase inhibitor-induced apoptosis. J Biol Chem 276 (2001) 17568-17575
57. Roshak A.K., Capper E.A., Stevenson C., Eichman C., and Marshall L.A. Human calcium-independent phospholipase A2 mediates lymphocyte proliferation. J Biol Chem 275 (2000) 35692-35698
58. Tessier C., Hichami A., and Khan N.A. Implication of three isoforms of PLA(2) in human T-cell proliferation. FEBS Lett 520 (2002) 111-116
59. Hichami A., Joshi B., Simonin A.M., and Khan N.A. Role of three isoforms of phospholipase A2 in capacitative calcium influx in human T-cells. Eur J Biochem 269 (2002) 5557-5563
60. Smith-Garvin J.E., Koretzky G.A., and Jordan M.S. T cell activation. Annu Rev Immunol 27 (2009) 591-619
61. Acuto O., Di Bartolo V., and Michel F. Tailoring T-cell receptor signals by proximal negative feedback mechanisms. Nat Rev Immunol 8 (2008) 699-712
62. Horejsi V., Zhang W., and Schraven B. Transmembrane adaptor proteins: organizers of immunoreceptor signalling. Nat Rev Immunol 4 (2004) 603-616
63. Sieh M., Batzer A., Schlessinger J., and Weiss A. GRB2 and phospholipase C-gamma 1 associate with a 36- to 38-kilodalton phosphotyrosine protein after T-cell receptor stimulation. Mol Cell Biol 14 (1994) 4435-4442
64. Rudd C.E., Taylor A., and Shneider H. CD28 and CTLA-4 coreceptor expression and signal transduction. Immunol Rev 229 (2009) 12-26
65. Nishizuka Y. Discovery and prospect of protein kinase C research: epilogue. J Biochem 133 (2003) 155-158
66. Yoshida K., Asaoka Y., and Nishizuka Y. Platelet activation by simultaneous actions of diacylglycerol and unsaturated fatty acids. Proc Natl Acad Sci USA 89 (1992) 6443-6446
67. Shinomura T., Asaoka Y., Oka M., Yoshida K., and Nishizuka Y. Synergistic action of diacylglycerol and unsaturated fatty acid for protein kinase C activation: its possible implications. Proc Natl Acad Sci USA 88 (1991) 5149-5153
68. Speizer L.A., Watson M.J., and Brunton L.L. Differential effects of omega-3 fish oils on protein kinase activities in vitro. Am J Physiol 261 (1991) E109-E114
69. Fan Y.Y., Ly L.H., Barhoumi R., McMurray D.N., and Chapkin R.S. Dietary docosahexaenoic acid suppresses T cell protein kinase C theta lipid raft recruitment and IL-2 production. J Immunol 173 (2004) 6151-6160
70. Denys A., Hichami A., and Khan N.A. Eicosapentaenoic acid and docosahexaenoic acid modulate MAP kinase (ERK1/ERK2) signaling in human T cells. J Lipid Res 42 (2001) 2015-2020
71. Denys A., Hichami A., Maume B., and Khan N.A. Docosahexaenoic acid modulates phorbol ester-induced activation of extracellular signal-regulated kinases 1 and 2 in NIH/3T3 cells. Lipids 36 (2001) 813-818
72. Jolly C.A., Jiang Y.H., Chapkin R.S., and McMurray D.N. Dietary (n-3) polyunsaturated fatty acids suppress murine lymphoproliferation, interleukin-2 secretion, and the formation of diacylglycerol and ceramide. J Nutr 127 (1997) 37-43
73. Bechoua S., Dubois M., Nemoz G., Lagarde M., and Prigent A.F. Docosahexaenoic acid lowers phosphatidate level in human activated lymphocytes despite phospholipase D activation. J Lipid Res 39 (1998) 873-883
74. Madani S., Hichami A., Cherkaoui-Malki M., and Khan N.A. Diacylglycerols containing Omega 3 and Omega 6 fatty acids bind to RasGRP and modulate MAP kinase activation. J Biol Chem 279 (2004) 1176-1183
75. Madani S., Hichami A., Legrand A., Belleville J., and Khan N.A. Implication of acyl chain of diacylglycerols in activation of different isoforms of protein kinase C. FASEB J 15 (2001) 2595-2601
76. Jude S., Martel E., Vincent F., Besson P., Couet C., Ogilvie G.K., et al. Dietary long-chain n-3 fatty acids modify blood and cardiac phospholipids and reduce protein kinase-C-delta and protein kinase-C-epsilon translocation. Br J Nutr 98 (2007) 1143-1151
77. Quann E.J., Merino E., Furuta T., and Huse M. Localized diacylglycerol drives the polarization of the microtubule-organizing center in T cells. Nat Immunol 10 (2009) 627-635
78. Oh-hora M., and Rao A. Calcium signaling in lymphocytes. Curr Opin Immunol 20 (2008) 250-258
79. Putney Jr. J.W. Type 3 inositol 1,4,5-trisphosphate receptor and capacitative calcium entry. Cell Calcium 21 (1997) 257-261
80. Oh-hora M. Calcium signaling in the development and function of T-lineage cells. Immunol Rev 231 (2009) 210-224
81. 2+ pool in T cells through a mechanism independent of phosphoinositide turnover. J Biol Chem 265 (1990) 902-907
82. Bonin A., and Khan N.A. Regulation of calcium signalling by docosahexaenoic acid in human T-cells. Implication of CRAC channels. J Lipid Res 41 (2000) 277-284
83. Denys A., Aires V., Hichami A., and Khan N.A. Thapsigargin-stimulated MAP kinase phosphorylation via CRAC channels and PLD activation: inhibitory action of docosahexaenoic acid. FEBS Lett 564 (2004) 177-182
84. Aires V., Hichami A., Moutairou K., and Khan N.A. Docosahexaenoic acid and other fatty acids induce a decrease in pHi in Jurkat T-cells. Br J Pharmacol 140 (2003) 1217-1226
85. Triboulot C., Hichami A., Denys A., and Khan N.A. Dietary (n-3) polyunsaturated fatty acids exert antihypertensive effects by modulating calcium signaling in T cells of rats. J Nutr 131 (2001) 2364-2369
86. Guermouche B., Yessoufou A., Soulimane N., Merzouk H., Moutairou K., Hichami A., et al. n-3 fatty acids modulate T-cell calcium signaling in obese macrosomic rats. Obes Res 12 (2004) 1744-1753
87. Zeyda M., Staffler G., Horejsi V., Waldhausl W., and Stulnig T.M. LAT displacement from lipid rafts as a molecular mechanism for the inhibition of T cell signaling by polyunsaturated fatty acids. J Biol Chem 277 (2002) 28418-28423
88. Stulnig T.M., Berger M., Sigmund T., Raederstorff D., Stockinger H., and Waldhausl W. Polyunsaturated fatty acids inhibit T cell signal transduction by modification of detergent-insoluble membrane domains. J Cell Biol 143 (1998) 637-644
89. Montell C. Drosophila TRP channels. Pflugers Arch 451 (2005) 19-28
90. Hofmann T., Obukhov A.G., Schaefer M., Harteneck C., Gudermann T., and Schultz G. Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397 (1999) 259-263
91. Gamberucci A., Giurisato E., Pizzo P., Tassi M., Giunti R., McIntosh D.P., et al. Diacylglycerol activates the influx of extracellular cations in T-lymphocytes independently of intracellular calcium-store depletion and possibly involving endogenous TRP6 gene products. Biochem J 364 (2002) 245-254
92. Aires V., Hichami A., Boulay G., and Khan N.A. Activation of TRPC6 calcium channels by diacylglycerol (DAG)-containing arachidonic acid: a comparative study with DAG-containing docosahexaenoic acid. Biochimie 89 (2007) 926-937
93. Cantrell D.A. GTPases and T cell activation. Immunol Rev 192 (2003) 122-130
94. Robbins D.J., Zhen E., Cheng M., Xu S., Ebert D., and Cobb M.H. MAP kinases ERK1 and ERK2: pleiotropic enzymes in a ubiquitous signaling network. Adv Cancer Res 63 (1994) 93-116
95. Hii C.S., Ferrante A., Edwards Y.S., Huang Z.H., Hartfield P.J., Rathjen D.A., et al. Activation of mitogen-activated protein kinase by arachidonic acid in rat liver epithelial WB cells by a protein kinase C-dependent mechanism. J Biol Chem 270 (1995) 4201-4204
96. Rao G.N., Baas A.S., Glasgow W.C., Eling T.E., Runge M.S., and Alexander R.W. Activation of mitogen-activated protein kinases by arachidonic acid and its metabolites in vascular smooth muscle cells. J Biol Chem 269 (1994) 32586-32591
97. Dulin N.O., Sorokin A., and Douglas J.G. Arachidonate-induced tyrosine phosphorylation of epidermal growth factor receptor and Shc-Grb2-Sos association. Hypertension 32 (1998) 1089-1093
98. Barry O.P., Kazanietz M.G., Pratico D., and FitzGerald G.A. Arachidonic acid in platelet microparticles up-regulates cyclooxygenase-2-dependent prostaglandin formation via a protein kinase C/mitogen-activated protein kinase-dependent pathway. J Biol Chem 274 (1999) 7545-7556
99. Denys A., Hichami A., and Khan N.A. Eicosapentaenoic acid and docosahexaenoic acid modulate MAP kinase enzyme activity in human T-cells. Mol Cell Biochem 232 (2002) 143-148
100. Gorjao R., Hirabara S.M., de Lima T.M., Cury-Boaventura M.F., and Curi R. Regulation of interleukin-2 signaling by fatty acids in human lymphocytes. J Lipid Res 48 (2007) 2009-2019
101. Massaro M., Habib A., Lubrano L., Del Turco S., Lazzerini G., Bourcier T., et al. The omega-3 fatty acid docosahexaenoate attenuates endothelial cyclooxygenase-2 induction through both NADP(H) oxidase and PKC epsilon inhibition. Proc Natl Acad Sci USA 103 (2006) 15184-15189
102. Hagiwara S., Makita Y., Gu L., Tanimoto M., Zhang M., Nakamura S., et al. Eicosapentaenoic acid ameliorates diabetic nephropathy of type 2 diabetic KKAy/Ta mice. involvement of MCP-1 suppression and decreased ERK1/2 and p38 phosphorylation. Nephrol Dial Transplant 21 (2006) 605-615
103. Kim H.H., Shin C.M., Park C.H., Kim K.H., Cho K.H., Eun H.C., et al. Eicosapentaenoic acid inhibits UV-induced MMP-1 expression in human dermal fibroblasts. J Lipid Res 46 (2005) 1712-1720
104. Lo C.J., Chiu K.C., Fu M., Chu A., and Helton S. Fish oil modulates macrophage P44/P42 mitogen-activated protein kinase activity induced by lipopolysaccharide. JPEN J Parenter Enteral Nutr 24 (2000) 159-163
105. Bousserouel S., Brouillet A., Bereziat G., Raymondjean M., and Andreani M. Different effects of n-6 and n-3 polyunsaturated fatty acids on the activation of rat smooth muscle cells by interleukin-1 beta. J Lipid Res 44 (2003) 601-611
106. Yessoufou A., Ple A., Moutairou K., Hichami A., and Khan N.A. Docosahexaenoic acid reduces suppressive and migratory functions of CD4+CD25+ regulatory T-cells. J Lipid Res 50 (2009) 2377-2388
107. Zhang X.F., Settleman J., Kyriakis J.M., Takeuchi-Suzuki E., Elledge S.J., Marshall M.S., et al. Normal and oncogenic p21ras proteins bind to the amino-terminal regulatory domain of c-Raf-1. Nature 364 (1993) 308-313
108. Ebinu J.O., Bottorff D.A., Chan E.Y., Stang S.L., Dunn R.J., and Stone J.C. RasGRP, a Ras guanyl nucleotide- releasing protein with calcium- and diacylglycerol-binding motifs. Science 280 (1998) 1082-1086
109. Carrasco S., and Merida I. Diacylglycerol-dependent binding recruits PKCtheta and RasGRP1 C1 domains to specific subcellular localizations in living T lymphocytes. Mol Biol Cell 15 (2004) 2932-2942
110. Lorenzo P.S., Beheshti M., Pettit G.R., Stone J.C., and Blumberg P.M. The guanine nucleotide exchange factor RasGRP is a high -affinity target for diacylglycerol and phorbol esters. Mol Pharmacol 57 (2000) 840-846
111. Phillips R., Ursell T., Wiggins P., and Sens P. Emerging roles for lipids in shaping membrane-protein function. Nature 459 (2009) 379-385
112. Pike L.J. Rafts defined: a report on the Keystone symposium on lipid rafts and cell function. J Lipid Res 47 (2006) 1597-1598
113. Shaw A.S. Lipid rafts: now you see them, now you don't. Nat Immunol 7 (2006) 1139-1142
114. Heerklotz H. Triton promotes domain formation in lipid raft mixtures. Biophys J 83 (2002) 2693-2701
115. Kenworthy A.K. Have we become overly reliant on lipid rafts? Talking Point on the involvement of lipid rafts in T-cell activation. EMBO Rep 9 (2008) 531-535
116. Jury E.C., Flores-Borja F., and Kabouridis P.S. Lipid rafts in T cell signalling and disease. Semin Cell Dev Biol 18 (2007) 608-615
117. Hanzal-Bayer M.F., and Hancock J.F. Lipid rafts and membrane traffic. FEBS Lett 581 (2007) 2098-2104
118. He H.T., and Marguet D. T-cell antigen receptor triggering and lipid rafts: a matter of space and time scales. Talking Point on the involvement of lipid rafts in T-cell activation. EMBO Rep 9 (2008) 525-530
119. Munro S. Lipid rafts: elusive or illusive?. Cell 115 (2003) 377-388
120. Burack W.R., Lee K.H., Holdorf A.D., Dustin M.L., and Shaw A.S. Cutting edge: quantitative imaging of raft accumulation in the immunological synapse. J Immunol 169 (2002) 2837-2841
121. Hullin-Matsuda F., and Kobayashi T. Monitoring the distribution and dynamics of signaling microdomains in living cells with lipid-specific probes. Cell Mol Life Sci 64 (2007) 2492-2504
122. Chichili G.R., and Rodgers W. Clustering of membrane raft proteins by the actin cytoskeleton. J Biol Chem 282 (2007) 36682-36691
123. Jacobson K., and Dietrich C. Looking at lipid rafts?. Trends Cell Biol 9 (1999) 87-91
124. Owen D.M., Neil M.A., French P.M., and Magee A.I. Optical techniques for imaging membrane lipid microdomains in living cells. Semin Cell Dev Biol 18 (2007) 591-598
125. Weber G., and Farris F.J. Synthesis and spectral properties of a hydrophobic fluorescent probe: 6-propionyl-2-(dimethylamino)naphthalene. Biochemistry 18 (1979) 3075-3078
126. Gaus K., Zech T., and Harder T. Visualizing membrane microdomains by Laurdan 2-photon microscopy. Mol Membr Biol 23 (2006) 41-48
127. Kim H.M., Choo H.J., Jung S.Y., Ko Y.G., Park W.H., Jeon S.J., et al. A two-photon fluorescent probe for lipid raft imaging: C-laurdan. ChemBioChem 8 (2007) 553-559
128. Gaus K., Gratton E., Kable E.P., Jones A.S., Gelissen I., Kritharides L., et al. Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc Natl Acad Sci USA 100 (2003) 15554-15559
129. Gaus K., Chklovskaia E., Fazekas de St Groth B., Jessup W., and Harder T. Condensation of the plasma membrane at the site of T lymphocyte activation. J Cell Biol 171 (2005) 121-131
130. Stauffer T.P., and Meyer T. Compartmentalized IgE receptor-mediated signal transduction in living cells. J Cell Biol 139 (1997) 1447-1454
131. Harder T., Scheiffele P., Verkade P., and Simons K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 141 (1998) 929-942
132. Hancock J.F., and Prior I.A. Electron microscopic imaging of Ras signaling domains. Methods 37 (2005) 165-172
133. Prior IA, Parton RG, Hancock JF. Observing cell surface signaling domains using electron microscopy. Sci STKE 2003:PL9.
134. Prior I.A., Harding I.A., Yan J., Sluimer J., Parton R.G., and Hancock J.F. GTP-dependent segregation of H-ras from lipid rafts is required for biological activity. Nat Cell Biol 3 (2001) 368-375
135. Friedl P., den Boer A.T., and Gunzer M. Tuning immune responses: diversity and adaptation of the immunological synapse. Nat Rev Immunol 5 (2005) 532-545
136. Geyeregger R., Zeyda M., Zlabinger G.J., Waldhausl W., and Stulnig T.M. Polyunsaturated fatty acids interfere with formation of the immunological synapse. J Leukocyte Biol 77 (2005) 680-688
137. + T cells by affecting lipid raft formation. J Immunol 181 (2008) 6236-6243
138. Fan Y.-Y., McMurray D.N., Ly L.H., and Chapkin R.S. Dietary (n-3) polyunsaturated fatty acids remodel mouse T-cell lipid rafts. J Nutr 133 (2003) 1913-1920
139. Wassall S.R., and Stillwell W. Docosahexaenoic acid domains: the ultimate non-raft membrane domain. Chem Phys Lipids 153 (2008) 57-63
140. Chapkin R.S., Wang N., Fan Y.-Y., Lupton J.R., and Prior I.A. Docosahexaenoic acid alters the size and distribution of cell surface microdomains. Biochim Biophys Acta (BBA) Biomembr 1778 (2008) 466-471
141. Omerovic J., and Prior I.A. Compartmentalized signalling: ras proteins and signalling nanoclusters. FEBS J 276 (2009) 1817-1825
142. Zech T., Ejsing C.S., Gaus K., de Wet B., Shevchenko A., Simons K., et al. Accumulation of raft lipids in T-cell plasma membrane domains engaged in TCR signalling. EMBO J 28 (2009) 466-476
143. Ly L.H., Smith R., Switzer K.C., Chapkin R.S., and McMurray D.N. Dietary eicosapentaenoic acid modulates CTLA-4 expression in murine CD4+ T-cells. Prostaglandins Leukot Essent Fatty Acids 74 (2006) 29-37
144. Cooper J.A. MAP kinase pathways. Straight and narrow or tortuous and intersecting?. Curr Biol 4 (1994) 1118-1121
145. Zeyda M., Szekeres A.B., Saemann M.D., Geyeregger R., Stockinger H., Zlabinger G.J., et al. Suppression of T cell signaling by polyunsaturated fatty acids: selectivity in inhibition of mitogen-activated protein kinase and nuclear factor activation. J Immunol 170 (2003) 6033-6039
146. Ly L.H., Smith III R., Chapkin R.S., and McMurray D.N. Dietary n-3 polyunsaturated fatty acids suppress splenic CD4(+) T cell function in interleukin (IL)-10(-/-) mice. Clin Exp Immunol 139 (2005) 202-209
147. Green D.R., Droin N., and Pinkoski M. Activation-induced cell death in T cells. Immunol Rev 193 (2003) 70-81
148. Fernandes G., Chandrasekar B., Luan X., and Troyer D.A. Modulation of antioxidant enzymes and programmed cell death by n-3 fatty acids. Lipids 31 Suppl. (1996) S91-96
149. Avula C.P., Zaman A.K., Lawrence R., and Fernandes G. Induction of apoptosis and apoptotic mediators in Balb/C splenic lymphocytes by dietary n-3 and n-6 fatty acids. Lipids 34 (1999) 921-927
150. Siddiqui R.A., Jenski L.J., Neff K., Harvey K., Kovacs R.J., and Stillwell W. Docosahexaenoic acid induces apoptosis in Jurkat cells by a protein phosphatase-mediated process. Biochim Biophys Acta 1499 (2001) 265-275
151. Heimli H., Giske C., Naderi S., Drevon C.A., and Hollung K. Eicosapentaenoic acid promotes apoptosis in Ramos cells via activation of caspase-3 and -9. Lipids 37 (2002) 797-802
152. Imboden J., Weyand C., and Goronzy J. Antigen recognition by a human T cell clone leads to increases in inositol trisphosphate. J Immunol 138 (1987) 1322-1324
153. Billah M.M., and Anthes J.C. The regulation and cellular functions of phosphatidylcholine hydrolysis. Biochem J 269 (1990) 281-291
154. Khan N.A., and Hichami A. Ionotrophic 5-hydroxytryptamine type 3 receptor activates the protein kinase C-dependent phospholipase D pathway in human T-cells. Biochem J 344 Pt. 1 (1999) 199-204
155. Kim W., Fan Y., Smith R., Patil B., Jayaprakasha G.K., McMurray D.N., et al. Dietary curcumin and limonis suppress T-cell proliferation and interleukin-2 production in mice. J Nutr 139 (2009) 1042-1048