Polyunsaturated fatty acid-derived lipid mediators and T cell function

Frontiers in Immunology

Volumn 5, Issue FEB, 2014, Pages

  Nicolaou, Anna ^a   Mauro, Claudio ^b   Urquhart, Paula ^a   Marelli Berg, Federica ^b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Cyclooxygenase; Eicosanoids; Endocannabinoids; Leukotrienes; Lipoxygenase; Polyunsaturated fatty acids; Prostaglandins; T cells

Indexed keywords

5 HYDROPEROXY 6,8,11,14 ICOSATETRAENOIC ACID; ARACHIDONIC ACID; BIOLOGICAL FACTOR; CANNABINOID RECEPTOR; CD4 ANTIGEN; CD8 ANTIGEN; CELECOXIB; CELL SURFACE RECEPTOR; CHEMOKINE RECEPTOR CXCR1; CHEMOKINE RECEPTOR CXCR3; CYTOCHROME P450; DIACYLGLYCEROL; ENDOCANNABINOID; FATTY ACID AMIDASE; ICOSANOID; ICOSAPENTAENOIC ACID; INDOMETACIN; LEUKOTRIENE; LIPID MEDIATOR; LIPOXYGENASE; POLYUNSATURATED FATTY ACID; PROSTACYCLIN; PROSTACYCLIN SYNTHASE; PROSTAGLANDIN; PROSTAGLANDIN E SYNTHASE; PROSTAGLANDIN SYNTHASE; PROSTANOID; THROMBOXANE; THROMBOXANE SYNTHASE; UNCLASSIFIED DRUG; UNINDEXED DRUG;

APOPTOSIS; CELL ADHESION; CELL DIFFERENTIATION; CELL FUNCTION; CELL INFILTRATION; CELL MEMBRANE; CELL MIGRATION; CELL PROLIFERATION; DIET SUPPLEMENTATION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; GENETIC ANALYSIS; GRAVES DISEASE; HUMAN; HYPERSENSITIVITY; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; INFLAMMATION; LIPID METABOLISM; LIPOGENESIS; LIVER INJURY; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

EID: 84895538329     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00075     Document Type: Review

References (215)

1. Wang R, Green DR. Metabolic checkpoints in activated T cells. Nat Immunol (2012) 13(10):907-15. doi:10.1038/ni.2386.
2. Schumacher TN, Gerlach C, van Heijst JW. Mapping the life histories of T cells. Nat Rev Immunol (2010) 10(9):621-31. doi:10.1038/nri2822.
3. Green DR. Overview: apoptotic signaling pathways in the immune system. Immunol Rev (2003) 193:5-9. doi:10.1034/j.1600-065X.2003.00045.x.
4. Wang R, Green DR. The immune diet: meeting the metabolic demands of lymphocyte activation. F1000 Biol Rep (2013) 4:9. doi:10.3410/B4-9.
5. Wang R, Dillon CP, Shi LZ, Milasta S, Carter R, Finkelstein D, et al. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity (2012) 35(6):871-82. doi:10.1016/j.immuni.2011.09.021.
6. Gerriets VA, Rathmell JC. Metabolic pathways in T cell fate and function. Trends Immunol (2012) 33(4):168-73. doi:10.1016/j.it.2012.01.010.
7. Marelli-Berg FM, Fu H, Mauro C. Molecular mechanisms of metabolic reprogramming in proliferating cells: implications for T-cell-mediated immunity. Immunology (2012) 136(4):363-9. doi:10.1111/j.1365-2567.2012.03583.x.
8. Mauro C, Fu H, Marelli-Berg FM. T cell trafficking and metabolism: novel mechanisms and targets for immunomodulation. Curr Opin Pharmacol (2012) 12(4):452-7. doi:10.1016/j.coph.2012.02.018.
9. Powell JD, Delgoffe GM. The mammalian target of rapamycin: linking T cell differentiation, function, and metabolism. Immunity (2011) 33(3):301-11. doi:10.1016/j.immuni.2010.09.002.
10. Peter C, Waldmann H, Cobbold SP. mTOR signalling and metabolic regulation of T cell differentiation. Curr Opin Immunol (2010) 22(5):655-61. doi:10.1016/j.coi.2010.08.010.
11. Jones RG, Thompson CB. Revving the engine: signal transduction fuels T cell activation. Immunity (2007) 27(2):173-8. doi:10.1016/j.immuni.2007.07.008.
12. Yamane H, Paul WE. Early signaling events that underlie fate decisions of naive CD4(+) T cells toward distinct T-helper cell subsets. Immunol Rev (2013) 252(1):12-23. doi:10.1111/imr.12032.
13. Boswell MG, Zhou W, Newcomb DC, Peebles RS Jr. PGI2 as a regulator of CD4+ subset differentiation and function. Prostaglandins Other Lipid Mediat (2011) 96(1-4):21-6. doi:10.1016/j.prostaglandins.2011.08.003.
14. Li H, Edin ML, Gruzdev A, Cheng J, Bradbury JA, Graves JP, et al. Regulation of T helper cell subsets by cyclooxygenases and their metabolites. Prostaglandins Other Lipid Mediat (2013) 104-105:74-83. doi:10.1016/j.prostaglandins.2012.11.002.
15. Macintyre AN, Finlay D, Preston G, Sinclair LV, Waugh CM, Tamas P, et al. Protein kinase B controls transcriptional programs that direct cytotoxic T cell fate but is dispensable for T cell metabolism. Immunity (2011) 34(2):224-36. doi:10.1016/j.immuni.2011.01.012.
16. Cornish GH, Sinclair LV, Cantrell DA. Differential regulation of T-cell growth by IL-2 and IL-15. Blood (2006) 108(2):600-8. doi:10.1182/blood-2005-12-4827.
17. Shi LZ, Wang R, Huang G, Vogel P, Neale G, Green DR, et al. HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J Exp Med (2011) 208(7):1367-76. doi:10.1084/jem.20110278.
18. Michalek RD, Gerriets VA, Jacobs SR, Macintyre AN, MacIver NJ, Mason EF, et al. Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J Immunol (2011) 186(6):3299-303. doi:10.4049/jimmunol.1003613.
19. van der Windt GJ, Everts B, Chang CH, Curtis JD, Freitas TC, Amiel E, et al. Mitochondrial respiratory capacity is a critical regulator of CD8+ T cell memory development. Immunity (2012) 36(1):68-78. doi:10.1016/j.immuni.2011.12.007.
20. Shaikh SR, Jolly CA, Chapkin RS. n-3 Polyunsaturated fatty acids exert immunomodulatory effects on lymphocytes by targeting plasma membrane molecular organization. Mol Aspects Med (2012) 33(1):46-54. doi:10.1016/j.mam.2011.10.002.
21. Calder PC. The relationship between the fatty acid composition of immune cells and their function. Prostaglandins Leukot Essent Fatty Acids (2008) 79(3-5):101-8. doi:10.1016/j.plefa.2008.09.016.
22. Kew S, Mesa MD, Tricon S, Buckley R, Minihane AM, Yaqoob P. Effects of oils rich in eicosapentaenoic and docosahexaenoic acids on immune cell composition and function in healthy humans. Am J Clin Nutr (2004) 79(4):674-81.
23. Petursdottir DH, Hardardottir I. Dietary fish oil decreases secretion of T helper (Th) 1-type cytokines by a direct effect on murine splenic T cells but enhances secretion of a Th2-type cytokine by an effect on accessory cells. Br J Nutr (2009) 101(7):1040-6. doi:10.1017/S0007114508048290.
24. Thies F, Nebe-von-Caron G, Powell JR, Yaqoob P, Newsholme EA, Calder PC. Dietary supplementation with gamma-linolenic acid or fish oil decreases T lymphocyte proliferation in healthy older humans. J Nutr (2001) 131(7):1918-27.
25. Verlengia R, Gorjao R, Kanunfre CC, Bordin S, Martins De Lima T, Martins EF, et al. Comparative effects of eicosapentaenoic acid and docosahexaenoic acid on proliferation, cytokine production, and pleiotropic gene expression in Jurkat cells. J Nutr Biochem (2004) 15(11):657-65. doi:10.1016/j.jnutbio.2004.04.008.
26. Shaikh SR, Edidin M. Immunosuppressive effects of polyunsaturated fatty acids on antigen presentation by human leukocyte antigen class I molecules. J Lipid Res (2007) 48(1):127-38. doi:10.1194/jlr.M600365-JLR200.
27. Jaudszus A, Gruen M, Watzl B, Ness C, Roth A, Lochner A, et al. Evaluation of suppressive and pro-resolving effects of EPA and DHA in human primary monocytes and T-helper cells. J Lipid Res (2013) 54(4):923-35. doi:10.1194/jlr.P031260.
28. Grimminger F, Grimm H, Fuhrer D, Papavassilis C, Lindemann G, Blecher C, et al. Omega-3 lipid infusion in a heart allotransplant model. Shift in fatty acid and lipid mediator profiles and prolongation of transplant survival. Circulation (1996) 93(2):365-71. doi:10.1161/01.CIR.93.2.365.
29. van der Heide JJ, Bilo HJ, Donker JM, Wilmink JM, Tegzess AM. Effect of dietary fish oil on renal function and rejection in cyclosporine-treated recipients of renal transplants. N Engl J Med (1993) 329(11):769-73. doi:10.1056/NEJM199309093291105.
30. 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. Am J Transplant (2009) 9(6):1294-307. doi:10.1111/j.1600-6143.2009.02641.x.
31. Iwami D, Nonomura K, Shirasugi N, Niimi M. Immunomodulatory effects of eicosapentaenoic acid through induction of regulatory T cells. Int Immunopharmacol (2011) 11(3):384-9. doi:10.1016/j.intimp.2010.11.035.
32. Kendall AC, Nicolaou A. Bioactive lipid mediators in skin inflammation and immunity. Prog Lipid Res (2013) 52(1):141-64. doi:10.1016/j.plipres.2012.10.003.
33. Hirata T, Narumiya S. Prostanoids as regulators of innate and adaptive immunity. Adv Immunol (2013) 116:143-74. doi:10.1016/B978-0-12-394300-2.00005-3.
34. Harizi H, Corcuff JB, Gualde N. Arachidonic-acid-derived eicosanoids: roles in biology and immunopathology. Trends Mol Med (2008) 14(10):461-9. doi:10.1016/j.molmed.2008.08.005.
35. Massey KA, Nicolaou A. Lipidomics of polyunsaturated-fatty-acid-derived oxygenated metabolites. Biochem Soc Trans (2012) 39(5):1240-6. doi:10.1042/BST0391240.
36. Ueda N, Tsuboi K, Uyama T. Metabolism of endocannabinoids and related N-acylethanolamines: canonical and alternative pathways. FEBS J (2013) 280(9):1874-94. doi:10.1111/febs.12152.
37. Dennis EA, Cao J, Hsu YH, Magrioti V, Kokotos G. Phospholipase A2 enzymes: physical structure, biological function, disease implication, chemical inhibition, and therapeutic intervention. Chem Rev (2011) 111(10):6130-85. doi:10.1021/cr200085w.
38. Tessier C, Hichami A, Khan NA. Implication of three isoforms of PLA(2) in human T-cell proliferation. FEBS Lett (2002) 520(1-3):111-6. doi:10.1016/S0014-5793(02)02779-5.
39. Hichami A, Joshi B, Simonin AM, Khan NA. Role of three isoforms of phospholipase A2 in capacitative calcium influx in human T-cells. Eur J Biochem (2002) 269(22):5557-63. doi:10.1046/j.1432-1033.2002.03261.x.
40. Burgermeister E, Endl J, Scheuer WV. Activation of cytosolic phospholipase A2 in human T-lymphocytes involves inhibitor-kappaB and mitogen-activated protein kinases. Eur J Pharmacol (2003) 466(1-2):169-80. doi:10.1016/S0014-2999(03)01492-4.
41. Roshak AK, Capper EA, Stevenson C, Eichman C, Marshall LA. Human calcium-independent phospholipase A2 mediates lymphocyte proliferation. J Biol Chem (2000) 275(46):35692-8. doi:10.1074/jbc.M002273200.
42. Le Gouvello S, Colard O, Theodorou I, Bismuth G, Tarantino N, Debre P. CD2 triggering stimulates a phospholipase A2 activity beside the phospholipase C pathway in human T lymphocytes. J Immunol (1990) 144(6):2359-64.
43. Cifone MG, Cironi L, Santoni A, Testi R. Diacylglycerol lipase activation and 5-lipoxygenase activation and translocation following TCR/CD3 triggering in T cells. Eur J Immunol (1995) 25(4):1080-6. doi:10.1002/eji.1830250433.
44. Calder PC. Polyunsaturated fatty acids and inflammatory processes: new twists in an old tale. Biochimie (2009) 91(6):791-5. doi:10.1016/j.biochi.2009.01.008.
45. Murakami M, Kudo I. Prostaglandin E synthase: a novel drug target for inflammation and cancer. Curr Pharm Des (2006) 12(8):943-54. doi:10.2174/138161206776055912.
46. Hara S, Kamei D, Sasaki Y, Tanemoto A, Nakatani Y, Murakami M. Prostaglandin E synthases: understanding their pathophysiological roles through mouse genetic models. Biochimie (2010) 92(6):651-9. doi:10.1016/j.biochi.2010.02.007.
47. Urade Y, Eguchi N. Lipocalin-type and hematopoietic prostaglandin D synthases as a novel example of functional convergence. Prostaglandins Other Lipid Mediat (2002) 6(8-69):375-82. doi:10.1016/S0090-6980(02)00042-4.
48. Surh YJ, Na HK, Park JM, Lee HN, Kim W, Yoon IS, et al. 15-Deoxy-delta(1)(2),(1)(4)-prostaglandin J(2), an electrophilic lipid mediator of anti-inflammatory and pro-resolving signaling. Biochem Pharmacol (2011) 82(10):1335-51. doi:10.1016/j.bcp.2011.07.100.
49. Scher JU, Pillinger MH. 15d-PGJ2: the anti-inflammatory prostaglandin? Clin Immunol (2005) 114(2):100-9. doi:10.1016/j.clim.2004.09.008.
50. Watanabe K. Prostaglandin F synthase. Prostaglandins Other Lipid Mediat (2002) 6(8-69):401-7. doi:10.1016/S0090-6980(02)00044-8.
51. Cathcart MC, Reynolds JV, O'Byrne KJ, Pidgeon GP. The role of prostacyclin synthase and thromboxane synthase signaling in the development and progression of cancer. Biochim Biophys Acta (2010) 1805(2):153-66. doi:10.1016/j.bbcan.2010.01.006.
52. Woodward DF, Jones RL, Narumiya S. International union of basic and clinical pharmacology. LXXXIII: classification of prostanoid receptors, updating 15 years of progress. Pharmacol Rev (2012) 63(3):471-538. doi:10.1124/pr.110.003517.
53. Breyer RM, Bagdassarian CK, Myers SA, Breyer MD. Prostanoid receptors: subtypes and signaling. Annu Rev Pharmacol Toxicol (2001) 41:661-90. doi:10.1146/annurev.pharmtox.41.1.661.
54. Tai HH, Ensor CM, Tong M, Zhou H, Yan F. Prostaglandin catabolizing enzymes. Prostaglandins Other Lipid Mediat (2002) 6(8-69):483-93. doi:10.1016/S0090-6980(02)00050-3.
55. Brash AR. Lipoxygenases: occurrence, functions, catalysis, and acquisition of substrate. J Biol Chem (1999) 274(34):23679-82. doi:10.1074/jbc.274.34.23679.
56. Dobrian AD, Lieb DC, Cole BK, Taylor-Fishwick DA, Chakrabarti SK, Nadler JL. Functional and pathological roles of the 12-and 15-lipoxygenases. Prog Lipid Res (2011) 50(1):115-31. doi:10.1016/j.plipres.2010.10.005.
57. Kuhn H, O'Donnell VB. Inflammation and immune regulation by 12/15-lipoxygenases. Prog Lipid Res (2006) 45(4):334-56. doi:10.1016/j.plipres.2006.02.003.
58. Murphy RC, Gijon MA. Biosynthesis and metabolism of leukotrienes. Biochem J (2007) 405(3):379-95. doi:10.1042/BJ20070289.
59. Powell WS, Rokach J. Biochemistry, biology and chemistry of the 5-lipoxygenase product 5-oxo-ETE. Prog Lipid Res (2005) 44(2-3):154-83. doi:10.1016/j.plipres.2005.04.002.
60. Lecomte M, Laneuville O, Ji C, DeWitt DL, Smith WL. Acetylation of human prostaglandin endoperoxide synthase-2 (cyclooxygenase-2) by aspirin. J Biol Chem (1994) 269(18):13207-15.
61. Claria J, Lee MH, Serhan CN. Aspirin-triggered lipoxins (15-epi-LX) are generated by the human lung adenocarcinoma cell line (A549)-neutrophil interactions and are potent inhibitors of cell proliferation. Mol Med (1996) 2(5):583-96.
62. Serhan CN, Hong S, Gronert K, Colgan SP, Devchand PR, Mirick G, et al. Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med (2002) 196(8):1025-37. doi:10.1084/jem.20020760.
63. Serhan CN, Yang R, Martinod K, Kasuga K, Pillai PS, Porter TF, et al. Maresins: novel macrophage mediators with potent antiinflammatory and proresolving actions. J Exp Med (2009) 206(1):15-23. doi:10.1084/jem.20081880.
64. Chacon P, Vega A, Monteseirin J, El Bekay R, Alba G, Perez-Formoso JL, et al. Induction of cyclooxygenase-2 expression by allergens in lymphocytes from allergic patients. Eur J Immunol (2005) 35(8):2313-24. doi:10.1002/eji.255590583.
65. Xu L, Zhang L, Yi Y, Kang HK, Datta SK. Human lupus T cells resist inactivation and escape death by upregulating COX-2. Nat Med (2004) 10(4):411-5. doi:10.1038/nm1005.
66. Iniguez MA, Martinez-Martinez S, Punzon C, Redondo JM, Fresno M. An essential role of the nuclear factor of activated T cells in the regulation of the expression of the cyclooxygenase-2 gene in human T lymphocytes. J Biol Chem (2000) 275(31):23627-35. doi:10.1074/jbc.M001381200.
67. Feldon SE, O'Loughlin CW, Ray DM, Landskroner-Eiger S, Seweryniak KE, Phipps RP. Activated human T lymphocytes express cyclooxygenase-2 and produce proadipogenic prostaglandins that drive human orbital fibroblast differentiation to adipocytes. Am J Pathol (2006) 169(4):1183-93. doi:10.2353/ajpath.2006.060434.
68. Mahic M, Yaqub S, Johansson CC, Tasken K, Aandahl EM. FOXP3+CD4+CD25+ adaptive regulatory T cells express cyclooxygenase-2 and suppress effector T cells by a prostaglandin E2-dependent mechanism. J Immunol (2006) 177(1):246-54.
69. Pablos JL, Santiago B, Carreira PE, Galindo M, Gomez-Reino JJ. Cyclooxygenase-1 and-2 are expressed by human T cells. Clin Exp Immunol (1999) 115(1):86-90. doi:10.1046/j.1365-2249.1999.00780.x.
70. Genaro AM, Sterin-Borda L, Gorelik G, Borda E. Prostanoids synthesis in lymphocyte subpopulations by adrenergic and cholinergic receptor stimulation. Int J Immunopharmacol (1992) 14(7):1145-51. doi:10.1016/0192-0561(92)90049-Q.
71. Gasser O, Schmid TA, Zenhaeusern G, Hess C. Cyclooxygenase regulates cell surface expression of CXCR3/1-storing granules in human CD4+ T cells. J Immunol (2006) 177(12):8806-12.
72. Kalinski P. Regulation of immune responses by prostaglandin E2. J Immunol (2011) 188(1):21-8. doi:10.4049/jimmunol.1101029.
73. Rocca B, Spain LM, Pure E, Langenbach R, Patrono C, FitzGerald GA. Distinct roles of prostaglandin H synthases 1 and 2 in T-cell development. J Clin Invest (1999) 103(10):1469-77. doi:10.1172/JCI6400.
74. Barrie A, Khare A, Henkel M, Zhang Y, Barmada MM, Duerr R, et al. Prostaglandin E2 and IL-23 plus IL-1beta differentially regulate the Th1/Th17 immune response of human CD161(+) CD4(+) memory T cells. Clin Transl Sci (2011) 4(4):268-73. doi:10.1111/j.1752-8062.2011.00300.x.
75. Li H, Edin ML, Bradbury JA, Graves JP, DeGraff LM, Gruzdev A, et al. Cyclooxygenase-2 inhibits T helper cell type 9 differentiation during allergic lung inflammation via down-regulation of IL-17RB. Am J Respir Crit Care Med (2013) 187(8):812-22. doi:10.1164/rccm.201211-2073OC.
76. Li B, Reynolds JM, Stout RD, Bernlohr DA, Suttles J. Regulation of Th17 differentiation by epidermal fatty acid-binding protein. J Immunol (2009) 182(12):7625-33. doi:10.4049/jimmunol.0804192.
77. Kaul V, Van Kaer L, Das G, Das J. Prostanoid receptor 2 signaling protects T helper 2 cells from BALB/c mice against activation-induced cell death. J Biol Chem (2012) 287(30):25434-9. doi:10.1074/jbc.C111.324707.
78. Khayrullina T, Yen JH, Jing H, Ganea D. In vitro differentiation of dendritic cells in the presence of prostaglandin E2 alters the IL-12/IL-23 balance and promotes differentiation of Th17 cells. J Immunol (2008) 181(1):721-35.
79. Miles EA, Aston L, Calder PC. In vitro effects of eicosanoids derived from different 20-carbon fatty acids on T helper type 1 and T helper type 2 cytokine production in human whole-blood cultures. Clin Exp Allergy (2003) 33(5):624-32. doi:10.1046/j.1365-2222.2003.01637.x.
80. Napolitani G, Acosta-Rodriguez EV, Lanzavecchia A, Sallusto F. Prostaglandin E2 enhances Th17 responses via modulation of IL-17 and IFN-gamma production by memory CD4+ T cells. Eur J Immunol (2009) 39(5):1301-12. doi:10.1002/eji.200838969.
81. Sreeramkumar V, Fresno M, Cuesta N. Prostaglandin E2 and T cells: friends or foes? Immunol Cell Biol (2012) 90(6):579-86. doi:10.1038/icb.2011.75.
82. Rana S, Byrne SN, MacDonald LJ, Chan CY, Halliday GM. Ultraviolet B suppresses immunity by inhibiting effector and memory T cells. Am J Pathol (2008) 172(4):993-1004. doi:10.2353/ajpath.2008.070517.
83. Krause P, Bruckner M, Uermosi C, Singer E, Groettrup M, Legler DF. Prostaglandin E(2) enhances T-cell proliferation by inducing the costimulatory molecules OX40L, CD70, and 4-1BBL on dendritic cells. Blood (2009) 113(11):2451-60. doi:10.1182/blood-2008-05-157123.
84. Muthuswamy R, Mueller-Berghaus J, Haberkorn U, Reinhart TA, Schadendorf D, Kalinski P. PPGE(2) transiently enhances DC expression of CCR7 but inhibits the ability of DCs to produce CCL19 and attract naive T cells. Blood (2010) 116(9):1454-9. doi:10.1182/blood-2009-12-258038.
85. Shimabukuro-Vornhagen A, Liebig TM, Koslowsky T, Theurich S, von Bergwelt-Baildon MS. The ratio between dendritic cells and T cells determines whether prostaglandin E2 has a stimulatory or inhibitory effect. Cell Immunol (2013) 281(1):62-7. doi:10.1016/j.cellimm.2013.01.001.
86. Mrabet-Dahbi S, Maurer M. Does allergy impair innate immunity? Leads and lessons from atopic dermatitis. Allergy (2011) 65(11):1351-6. doi:10.1111/j.1398-9995.2010.02452.x.
87. Deckers J, Branco Madeira F, Hammad H. Innate immune cells in asthma. Trends Immunol (2013) 34(11):540-7. doi:10.1016/j.it.2013.08.004.
88. Nagamachi M, Sakata D, Kabashima K, Furuyashiki T, Murata T, Segi-Nishida E, et al. Facilitation of Th1-mediated immune response by prostaglandin E receptor EP1. J Exp Med (2007) 204(12):2865-74. doi:10.1084/jem.20070773.
89. Esaki Y, Li Y, Sakata D, Yao C, Segi-Nishida E, Matsuoka T, et al. Dual roles of PGE2-EP4 signaling in mouse experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A (2010) 107(27):12233-8. doi:10.1073/pnas.0915112107.
90. Yao C, Sakata D, Esaki Y, Li Y, Matsuoka T, Kuroiwa K, et al. Prostaglandin E2-EP4 signaling promotes immune inflammation through Th1 cell differentiation and Th17 cell expansion. Nat Med (2009) 15(6):633-40. doi:10.1038/nm.1968.
91. Valitutti S, Dessing M, Lanzavecchia A. Role of cAMP in regulating cytotoxic T lymphocyte adhesion and motility. Eur J Immunol (1993) 23(4):790-5. doi:10.1002/eji.1830230403.
92. Santoli D, Zurier RB. Prostaglandin E precursor fatty acids inhibit human IL-2 production by a prostaglandin E-independent mechanism. J Immunol (1989) 143(4):1303-9.
93. Van Epps DE. Suppression of human lymphocyte migration by PGE2. Inflammation (1981) 5(1):81-7. doi:10.1007/BF00910782.
94. Koga Y, Tanaka K, Yokoyama M, Taniguchi K, Nomoto K. Thymus cell migration in a prostaglandin-mediated system. Immunobiology (1985) 169(5):486-502. doi:10.1016/S0171-2985(85)80004-8.
95. Wiemer AJ, Hegde S, Gumperz JE, Huttenlocher A. A live imaging cell motility screen identifies prostaglandin E2 as a T cell stop signal antagonist. J Immunol (2011) 187(7):3663-70. doi:10.4049/jimmunol.1100103.
96. Jordan ML, Hoffman RA, Debe EF, Simmons RL. In vitro locomotion of allosensitized T lymphocyte clones in response to metabolites of arachidonic acid is subset specific. J Immunol (1986) 137(2):661-8.
97. Jordan ML, Hoffman RA, Debe EF, West MA, Simmons RL. Prostaglandin E2 mediates subset-specific effects on the functional responses of allosensitized T lymphocyte clones. Transplantation (1987) 43(1):117-23. doi:10.1097/00007890-198701000-00026.
98. Jordan ML, Vidgen DF, Wright J, Odell M, Mills GB. Sustained increases in cytosolic calcium during T lymphocyte allosensitization, proliferation, and acquisition of locomotor function. Transplantation (1991) 51(2):464-8.
99. Oppenheimer-Marks N, Kavanaugh AF, Lipsky PE. Inhibition of the transendothelial migration of human T lymphocytes by prostaglandin E2. J Immunol (1994) 152(12):5703-13.
100. Mesri M, Liversidge J, Forrester JV. Prostaglandin E2 and monoclonal antibody to lymphocyte function-associated antigen-1 differentially inhibit migration of T lymphocytes across microvascular retinal endothelial cells in rat. Immunology (1996) 88(3):471-7. doi:10.1046/j.1365-2567.1996.d01-671.x.
101. Leppert D, Hauser SL, Kishiyama JL, An S, Zeng L, Goetzl EJ. Stimulation of matrix metalloproteinase-dependent migration of T cells by eicosanoids. FASEB J (1995) 9(14):1473-81.
102. Karavitis J, Hix LM, Shi YH, Schultz RF, Khazaie K, Zhang M. Regulation of COX2 expression in mouse mammary tumor cells controls bone metastasis and PGE2-induction of regulatory T cell migration. PLoS One (2012) 7(9):e46342. doi:10.1371/journal.pone.0046342.
103. Harris SG, Padilla J, Koumas L, Ray D, Phipps RP. Prostaglandins as modulators of immunity. Trends Immunol (2002) 23(3):144-50. doi:10.1016/S1471-4906(01)02154-8.
104. Tanaka K, Ogawa K, Sugamura K, Nakamura M, Takano S, Nagata K. Cutting edge: differential production of prostaglandin D2 by human helper T cell subsets. J Immunol (2000) 164(5):2277-80.
105. Mutalithas K, Guillen C, Day C, Brightling CE, Pavord ID, Wardlaw AJ. CRTH2 expression on T cells in asthma. Clin Exp Immunol (2010) 161(1):34-40. doi:10.1111/j.1365-2249.2010.04161.x.
106. Tanaka K, Hirai H, Takano S, Nakamura M, Nagata K. Effects of prostaglandin D2 on helper T cell functions. Biochem Biophys Res Commun (2004) 316(4):1009-14. doi:10.1016/j.bbrc.2004.02.151.
107. Hirai H, Tanaka K, Yoshie O, Ogawa K, Kenmotsu K, Takamori Y, et al. Prostaglandin D2 selectively induces chemotaxis in T helper type 2 cells, eosinophils, and basophils via seven-transmembrane receptor CRTH2. J Exp Med (2001) 193(2):255-61. doi:10.1084/jem.193.2.255.
108. Schuligoi R, Sedej M, Waldhoer M, Vukoja A, Sturm EM, Lippe IT, et al. Prostaglandin H2 induces the migration of human eosinophils through the chemoattractant receptor homologous molecule of Th2 cells, CRTH2. J Leukoc Biol (2009) 85(1):136-45. doi:10.1189/jlb.0608387.
109. Pettipher R. The roles of the prostaglandin D(2) receptors DP(1) and CRTH2 in promoting allergic responses. Br J Pharmacol (2008) 153(Suppl 1):S191-9. doi:10.1038/sj.bjp.0707488.
110. Yamamoto Y, Otani S, Hirai H, Nagata K, Aritake K, Urade Y, et al. Dual functions of prostaglandin D2 in murine contact hypersensitivity via DP and CRTH2. Am J Pathol (2011) 179(1):302-14. doi:10.1016/j.ajpath.2011.03.047.
111. Raman P, Kaplan BL, Kaminski NE. 15-Deoxy-Delta(1)(2),(1)(4)-prostaglandin J(2)-glycerol, a putative metabolite of 2-arachidonoyl glycerol and a peroxisome proliferator-activated receptor gamma ligand, modulates nuclear factor of activated T cells. J Pharmacol Exp Ther (2013) 342(3):816-26. doi:10.1124/jpet.112.193003.
112. Sykes L, MacIntyre DA, Yap XJ, Ponnampalam S, Teoh TG, Bennett PR. Changes in the Th1:Th2 cytokine bias in pregnancy and the effects of the anti-inflammatory cyclopentenone prostaglandin 15-deoxy-Delta(12,14)-prostaglandin J2. Mediators Inflamm (2012) 2012:416739. doi:10.1155/2012/416739.
113. Perez-Novo CA, Holtappels G, Vinall SL, Xue L, Zhang N, Bachert C, et al. CRTH2 mediates the activation of human Th2 cells in response to PGD(2) released from IgE/anti-IgE treated nasal polyp tissue. Allergy (2009) 65(3):304-10. doi:10.1111/j.1398-9995.2009.02204.x.
114. Xue L, Gyles SL, Barrow A, Pettipher R. Inhibition of PI3K and calcineurin suppresses chemoattractant receptor-homologous molecule expressed on Th2 cells (CRTH2)-dependent responses of Th2 lymphocytes to prostaglandin D(2). Biochem Pharmacol (2007) 73(6):843-53. doi:10.1016/j.bcp.2006.11.021.
115. Xue L, Barrow A, Pettipher R. Interaction between prostaglandin D and chemoattractant receptor-homologous molecule expressed on Th2 cells mediates cytokine production by Th2 lymphocytes in response to activated mast cells. Clin Exp Immunol (2009) 156(1):126-33. doi:10.1111/j.1365-2249.2008.03871.x.
116. Vinall SL, Townsend ER, Pettipher R. A paracrine role for chemoattractant receptor-homologous molecule expressed on T helper type 2 cells (CRTH2) in mediating chemotactic activation of CRTH2+ CD4+ T helper type 2 lymphocytes. Immunology (2007) 121(4):577-84. doi:10.1111/j.1365-2567.2007.02606.x.
117. Ahmed SR, McGettrick HM, Yates CM, Buckley CD, Ratcliffe MJ, Nash GB, et al. Prostaglandin D2 regulates CD4+ memory T cell trafficking across blood vascular endothelium and primes these cells for clearance across lymphatic endothelium. J Immunol (2011) 187(3):1432-9. doi:10.4049/jimmunol.1100299.
118. Shirasaki H, Kikuchi M, Kanaizumi E, Himi T. Accumulation of CRTH2-positive leukocytes in human allergic nasal mucosa. Ann Allergy Asthma Immunol (2009) 102(2):110-5. doi:10.1016/S1081-1206(10)60239-6.
119. Gyles SL, Xue L, Townsend ER, Wettey F, Pettipher R. A dominant role for chemoattractant receptor-homologous molecule expressed on T helper type 2 (Th2) cells (CRTH2) in mediating chemotaxis of CRTH2+ CD4+ Th2 lymphocytes in response to mast cell supernatants. Immunology (2006) 119(3):362-8. doi:10.1111/j.1365-2567.2006.02440.x.
120. Gosset P, Bureau F, Angeli V, Pichavant M, Faveeuw C, Tonnel AB, et al. Prostaglandin D2 affects the maturation of human monocyte-derived dendritic cells: consequence on the polarization of naive Th cells. J Immunol (2003) 170(10):4943-52.
121. Gosset P, Pichavant M, Faveeuw C, Bureau F, Tonnel AB, Trottein F. Prostaglandin D2 affects the differentiation and functions of human dendritic cells: impact on the T cell response. Eur J Immunol (2005) 35(5):1491-500. doi:10.1002/eji.200425319.
122. Zhao J, Legge K, Perlman S. Age-related increases in PGD(2) expression impair respiratory DC migration, resulting in diminished T cell responses upon respiratory virus infection in mice. J Clin Invest (2011) 121(12):4921-30. doi:10.1172/JCI59777.
123. Li H, Bradbury JA, Dackor RT, Edin ML, Graves JP, DeGraff LM, et al. Cyclooxygenase-2 regulates Th17 cell differentiation during allergic lung inflammation. Am J Respir Crit Care Med (2011) 184(1):37-49. doi:10.1164/rccm.201010-1637OC.
124. Zhou W, Hashimoto K, Goleniewska K, O'Neal JF, Ji S, Blackwell TS, et al. Prostaglandin I2 analogs inhibit proinflammatory cytokine production and T cell stimulatory function of dendritic cells. J Immunol (2007) 178(2):702-10.
125. Nakajima S, Honda T, Sakata D, Egawa G, Tanizaki H, Otsuka A, et al. Prostaglandin I2-IP signaling promotes Th1 differentiation in a mouse model of contact hypersensitivity. J Immunol (2010) 184(10):5595-603. doi:10.4049/jimmunol.0903260.
126. Wu KK, Papp AC, Manner CE, Hall ER. Interaction between lymphocytes and platelets in the synthesis of prostacyclin. J Clin Invest (1987) 79(6):1601-6. doi:10.1172/JCI112995.
127. Liu W, Li H, Zhang X, Wen D, Yu F, Yang S, et al. Prostaglandin I2-IP signalling regulates human Th17 and Treg cell differentiation. Prostaglandins Leukot Essent Fatty Acids (2013) 89(5):335-44. doi:10.1016/j.plefa.2013.08.006.
128. Jaffar Z, Ferrini ME, Buford MC, Fitzgerald GA, Roberts K. Prostaglandin I2-IP signaling blocks allergic pulmonary inflammation by preventing recruitment of CD4+ Th2 cells into the airways in a mouse model of asthma. J Immunol (2007) 179(9):6193-203.
129. Zhou W, Dowell DR, Huckabee MM, Newcomb DC, Boswell MG, Goleniewska K, et al. Prostaglandin I2 signaling drives Th17 differentiation and exacerbates experimental autoimmune encephalomyelitis. PLoS One (2012) 7(5):e33518. doi:10.1371/journal.pone.0033518.
130. Kabashima K, Murata T, Tanaka H, Matsuoka T, Sakata D, Yoshida N, et al. Thromboxane A2 modulates interaction of dendritic cells and T cells and regulates acquired immunity. Nat Immunol (2003) 4(7):694-701. doi:10.1038/ni943.
131. Thomas DW, Rocha PN, Nataraj C, Robinson LA, Spurney RF, Koller BH, et al. Proinflammatory actions of thromboxane receptors to enhance cellular immune responses. J Immunol (2003) 171(12):6389-95.
132. Ushikubi F, Aiba Y, Nakamura K, Namba T, Hirata M, Mazda O, et al. Thromboxane A2 receptor is highly expressed in mouse immature thymocytes and mediates DNA fragmentation and apoptosis. J Exp Med (1993) 178(5):1825-30. doi:10.1084/jem.178.5.1825.
133. Kohyama K, Hashimoto M, Abe S, Kodaira K, Yukawa T, Hozawa S, et al. Thromboxane A2 receptor +795T >C and chemoattractant receptor-homologous molecule expressed on Th2 cells-466T >C gene polymorphisms in patients with aspirin-exacerbated respiratory disease. Mol Med Rep (2012) 5(2):477-82. doi:10.3892/mmr.2011.680.
134. Kumar GS, Das UN. 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(6):331-4. doi:10.1016/0952-3278(94)90242-9.
135. Cook-Moreau JM, El-Makhour Hojeij Y, Barriere G, Rabinovitch-Chable HC, Faucher KS, Sturtz FG, et al. Expression of 5-lipoxygenase (5-LOX) in T lymphocytes. Immunology (2007) 122(2):157-66. doi:10.1111/j.1365-2567.2007.02621.x.
136. Cai Y, Kumar RK, Zhou J, Foster PS, Webb DC. Ym1/2 promotes Th2 cytokine expression by inhibiting 12/15(S)-lipoxygenase: identification of a novel pathway for regulating allergic inflammation. J Immunol (2009) 182(9):5393-9. doi:10.4049/jimmunol.0803874.
137. Kato K, Koshihara Y, Fujiwara M, Murota S. Augmentation of 12-lipoxygenase activity of lymph node and spleen T cells in autoimmune mice MRL/1. Prostaglandins Leukot Med (1983) 12(3):273-80. doi:10.1016/0262-1746(83)90005-7.
138. el Makhour-Hojeij Y, Baclet MC, Chable-Rabinovitch H, Beneytout JL, Cook J. Expression of 5-lipoxygenase in lymphoblastoid B and T cells. Prostaglandins (1994) 48(1):21-9. doi:10.1016/0090-6980(94)90093-0.
139. Atluru D, Lianos EA, Goodwin JS. Arachidonic acid inhibits 5-lipoxygenase in human T cells. Biochem Biophys Res Commun (1986) 135(2):670-6. doi:10.1016/0006-291X(86)90045-8.
140. Goodarzi K, Goodarzi M, Tager AM, Luster AD, von Andrian UH. Leukotriene B4 and BLT1 control cytotoxic effector T cell recruitment to inflamed tissues. Nat Immunol (2003) 4(10):965-73. doi:10.1038/ni972.
141. Tager AM, Bromley SK, Medoff BD, Islam SA, Bercury SD, Friedrich EB, et al. Leukotriene B4 receptor BLT1 mediates early effector T cell recruitment. Nat Immunol (2003) 4(10):982-90. doi:10.1038/ni970.
142. Costa MF, de Souza-Martins R, de Souza MC, Benjamim CF, Piva B, Diaz BL, et al. Leukotriene B4 mediates gammadelta T lymphocyte migration in response to diverse stimuli. J Leukoc Biol (2010) 87(2):323-32. doi:10.1189/jlb.0809563.
143. Medeiros AI, Sa-Nunes A, Turato WM, Secatto A, Frantz FG, Sorgi CA, et al. Leukotrienes are potent adjuvant during fungal infection: effects on memory T cells. J Immunol (2008) 181(12):8544-51.
144. Luster AD, Tager AM. T-cell trafficking in asthma: lipid mediators grease the way. Nat Rev Immunol (2004) 4(9):711-24. doi:10.1038/nri1438.
145. Nancey S, Boschetti G, Hacini F, Sardi F, Durand PY, Le Borgne M, et al. Blockade of LTB(4)/BLT(1) pathway improves CD8(+) T-cell-mediated colitis. Inflamm Bowel Dis (2011) 17(1):279-88. doi:10.1002/ibd.21404.
146. Chen H, Qin J, Wei P, Zhang J, Li Q, Fu L, et al. Effects of leukotriene B4 and prostaglandin E2 on the differentiation of murine Foxp3+ T regulatory cells and Th17 cells. Prostaglandins Leukot Essent Fatty Acids (2009) 80(4):195-200. doi:10.1016/j.plefa.2009.01.006.
147. DiMeo D, Tian J, Zhang J, Narushima S, Berg DJ. Increased interleukin-10 production and Th2 skewing in the absence of 5-lipoxygenase. Immunology (2007) 123(2):250-62. doi:10.1111/j.1365-2567.2007.02694.x.
148. Arcoleo F, Milano S, D'Agostino P, Cillari E. Effect of exogenous leukotriene B4 (LTB4) on BALB/c mice splenocyte production of Th1 and Th2 lymphokines. Int J Immunopharmacol (1995) 17(6):457-63. doi:10.1016/0192-0561(95)00038-4.
149. Dornand J, Gerber M. Mechanisms of IL2 production impairment by lipoxygenase inhibitors in activated Jurkat cells. J Lipid Mediat (1991) 4(1):23-38.
150. Laidlaw TM, Boyce JA. Cysteinyl leukotriene receptors, old and new; implications for asthma. Clin Exp Allergy (2013) 42(9):1313-20. doi:10.1111/j.1365-2222.2012.03982.x.
151. Parmentier CN, Fuerst E, McDonald J, Bowen H, Lee TH, Pease JE, et al. Human T(H)2 cells respond to cysteinyl leukotrienes through selective expression of cysteinyl leukotriene receptor 1. J Allergy Clin Immunol (2012) 129(4):1136-42. doi:10.1016/j.jaci.2012.01.057.
152. Prinz I, Gregoire C, Mollenkopf H, Aguado E, Wang Y, Malissen M, et al. The type 1 cysteinyl leukotriene receptor triggers calcium influx and chemotaxis in mouse alpha beta-and gamma delta effector T cells. J Immunol (2005) 175(2):713-9.
153. Xue L, Barrow A, Fleming VM, Hunter MG, Ogg G, Klenerman P, et al. Leukotriene E4 activates human Th2 cells for exaggerated proinflammatory cytokine production in response to prostaglandin D2. J Immunol (2011) 188(2):694-702. doi:10.4049/jimmunol.1102474.
154. Bailey JM, Vanderhoek JY, Makheja AN, Pupillo M. Activation of mitogen-induced T-lymphocyte proliferation by leukotriene C-4. Biochem Soc Trans (1997) 25(3):503S.
155. Dannull J, Schneider T, Lee WT, de Rosa N, Tyler DS, Pruitt SK. Leukotriene C4 induces migration of human monocyte-derived dendritic cells without loss of immunostimulatory function. Blood (2012) 119(13):3113-22. doi:10.1182/blood-2011-10-385930.
156. Zhang Y, Styhler A, Powell WS. Synthesis of 5-oxo-6,8,11,14-eicosatetraenoic acid by human monocytes and lymphocytes. J Leukoc Biol (1996) 59(6):847-54.
157. Erlemann KR, Rokach J, Powell WS. Oxidative stress stimulates the synthesis of the eosinophil chemoattractant 5-oxo-6,8,11,14-eicosatetraenoic acid by inflammatory cells. J Biol Chem (2004) 279(39):40376-84. doi:10.1074/jbc.M401294200.
158. Bacon KB, Camp RD. Lipid lymphocyte chemoattractants in psoriasis. Prostaglandins (1990) 40(6):603-14. doi:10.1016/0090-6980(90)90005-G.
159. Bacon KB, Camp RD, Cunningham FM, Woollard PM. Contrasting in vitro lymphocyte chemotactic activity of the hydroxyl enantiomers of 12-hydroxy-5,8,10,14-eicosatetraenoic acid. Br J Pharmacol (1988) 95(3):966-74. doi:10.1111/j.1476-5381.1988.tb11727.x.
160. Kumar KA, Arunasree KM, Roy KR, Reddy NP, Aparna A, Reddy GV, et al. Effects of (15S)-hydroperoxyeicosatetraenoic acid and (15S)-hydroxyeicosatetraenoic acid on the acute-lymphoblastic-leukaemia cell line Jurkat: activation of the Fas-mediated death pathway. Biotechnol Appl Biochem (2009) 52(Pt 2):121-33. doi:10.1042/BA20070264.
161. Bailey JM, Bryant RW, Low CE, Pupillo MB, Vanderhoek JY. Regulation of T-lymphocyte mitogenesis by the leukocyte product 15-hydroxy-eicosatetraenoic acid (15-HETE). Cell Immunol (1982) 67(1):112-20. doi:10.1016/0008-8749(82)90203-9.
162. Bailey JM, Fletcher M, Vanderhoek JY, Makheja AN. Regulation of human T-lymphocyte proliferative responses by the lipoxygenase product 15-HETE. Biochem Soc Trans (1997) 25(2):247S.
163. Hadjiagapiou C, Travers JB, Fertel RH, Sprecher H. Metabolism of 15-hydroxy-5,8,11,13-eicosatetraenoic acid by MOLT-4 cells and blood T-lymphocytes. J Biol Chem (1990) 265(8):4369-73.
164. Jeon SG, Moon HG, Kim YS, Choi JP, Shin TS, Hong SW, et al. 15-Lipoxygenase metabolites play an important role in the development of a T-helper type 1 allergic inflammation induced by double-stranded RNA. Clin Exp Allergy (2009) 39(6):908-17. doi:10.1111/j.1365-2222.2009.03211.x.
165. Lin KT, Godfrey HP, Spokas EG, Sun FF, Wong PY. Modulation of LTB4 receptor in T-lymphocytes by lipoxin A4 (LXA4) and its role in delayed-type hypersensitivity. Adv Exp Med Biol (1999) 447:151-63. doi:10.1007/978-1-4615-4861-4_14.
166. Lin KT, Dudhane A, Godfrey HP, Wong PY. Identification and characterization of a high-affinity leukotriene B4 receptor on guinea pig T lymphocytes and its regulation by lipoxin A4. J Pharmacol Exp Ther (1996) 277(2):679-84.
167. Ariel A, Chiang N, Arita M, Petasis NA, Serhan CN. Aspirin-triggered lipoxin A4 and B4 analogs block extracellular signal-regulated kinase-dependent TNF-alpha secretion from human T cells. J Immunol (2003) 170(12):6266-72.
168. Zhang B, Jia H, Liu J, Yang Z, Jiang T, Tang K, et al. Depletion of regulatory T cells facilitates growth of established tumors: a mechanism involving the regulation of myeloid-derived suppressor cells by lipoxin A4. J Immunol (2010) 185(12):7199-206. doi:10.4049/jimmunol.1001876.
169. Ariel A, Li PL, Wang W, Tang WX, Fredman G, Hong S, et al. The docosatriene protectin D1 is produced by TH2 skewing and promotes human T cell apoptosis via lipid raft clustering. J Biol Chem (2005) 280(52):43079-86. doi:10.1074/jbc.M509796200.
170. Kim TH, Kim GD, Jin YH, Park YS, Park CS. Omega-3 fatty acid-derived mediator, resolvin E1, ameliorates 2,4-dinitrofluorobenzene-induced atopic dermatitis in NC/Nga mice. Int Immunopharmacol (2012) 14(4):384-91. doi:10.1016/j.intimp.2012.08.005.
171. Vassiliou EK, Kesler OM, Tadros JH, Ganea D. Bone marrow-derived dendritic cells generated in the presence of resolvin E1 induce apoptosis of activated CD4+ T cells. J Immunol (2008) 181(7):4534-44.
172. Rajasagi NK, Reddy PB, Suryawanshi A, Mulik S, Gjorstrup P, Rouse BT. Controlling herpes simplex virus-induced ocular inflammatory lesions with the lipid-derived mediator resolvin E1. J Immunol (2011) 186(3):1735-46. doi:10.4049/jimmunol.1003456.
173. Bambang KN, Lambert DG, Lam PM, Quenby S, Maccarrone M, Konje JC. Immunity and early pregnancy events: are endocannabinoids the missing link? J Reprod Immunol (2012) 96(1-2):8-18. doi:10.1016/j.jri.2012.10.003.
174. Maccarrone M, Bari M, Battista N, Finazzi-Agro A. Endocannabinoid degradation, endotoxic shock and inflammation. Curr Drug Targets Inflamm Allergy (2002) 1(1):53-63. doi:10.2174/1568010023344878.
175. Nagarkatti P, Pandey R, Rieder SA, Hegde VL, Nagarkatti M. Cannabinoids as novel anti-inflammatory drugs. Future Med Chem (2009) 1(7):1333-49. doi:10.4155/fmc.09.93.
176. Rieder SA, Chauhan A, Singh U, Nagarkatti M, Nagarkatti P. Cannabinoid-induced apoptosis in immune cells as a pathway to immunosuppression. Immunobiology (2009) 215(8):598-605. doi:10.1016/j.imbio.2009.04.001.
177. Maccarrone M, De Petrocellis L, Bari M, Fezza F, Salvati S, Di Marzo V, et al. Lipopolysaccharide downregulates fatty acid amide hydrolase expression and increases anandamide levels in human peripheral lymphocytes. Arch Biochem Biophys (2001) 393(2):321-8. doi:10.1006/abbi.2001.2500.
178. Maccarrone M, Bari M, Di Rienzo M, Finazzi-Agro A, Rossi A. Progesterone activates fatty acid amide hydrolase (FAAH) promoter in human T lymphocytes through the transcription factor Ikaros. Evidence for a synergistic effect of leptin. J Biol Chem (2003) 278(35):32726-32. doi:10.1074/jbc.M302123200.
179. Coopman K, Smith LD, Wright KL, Ward SG. Temporal variation in CB2R levels following T lymphocyte activation: evidence that cannabinoids modulate CXCL12-induced chemotaxis. Int Immunopharmacol (2007) 7(3):360-71. doi:10.1016/j.intimp.2006.11.008.
180. Daaka Y, Friedman H, Klein TW. Cannabinoid receptor proteins are increased in Jurkat, human T-cell line after mitogen activation. J Pharmacol Exp Ther (1996) 276(2):776-83.
181. Robinson RH, Meissler JJ, Breslow-Deckman JM, Gaughan J, Adler MW, Eisenstein TK. Cannabinoids inhibit T-cells via cannabinoid receptor 2 in an in vitro assay for graft rejection, the mixed lymphocyte reaction. J Neuroimmune Pharmacol (2013) 8(5):1239-50. doi:10.1007/s11481-013-9485-1.
182. Ziring D, Wei B, Velazquez P, Schrage M, Buckley NE, Braun J. Formation of B and T cell subsets require the cannabinoid receptor CB2. Immunogenetics (2006) 58(9):714-25. doi:10.1007/s00251-006-0138-x.
183. Sipe JC, Arbour N, Gerber A, Beutler E. Reduced endocannabinoid immune modulation by a common cannabinoid 2 (CB2) receptor gene polymorphism: possible risk for autoimmune disorders. J Leukoc Biol (2005) 78(1):231-8. doi:10.1189/jlb.0205111.
184. Hegde VL, Hegde S, Cravatt BF, Hofseth LJ, Nagarkatti M, Nagarkatti PS. Attenuation of experimental autoimmune hepatitis by exogenous and endogenous cannabinoids: involvement of regulatory T cells. Mol Pharmacol (2008) 74(1):20-33. doi:10.1124/mol.108.047035.
185. Eisenstein TK, Meissler JJ, Wilson Q, Gaughan JP, Adler MW. Anandamide and Delta9-tetrahydrocannabinol directly inhibit cells of the immune system via CB2 receptors. J Neuroimmunol (2007) 189(1-2):17-22. doi:10.1016/j.jneuroim.2007.06.001.
186. Cencioni MT, Chiurchiu V, Catanzaro G, Borsellino G, Bernardi G, Battistini L, et al. Anandamide suppresses proliferation and cytokine release from primary human T-lymphocytes mainly via CB2 receptors. PLoS One (2010) 5(1):e8688. doi:10.1371/journal.pone.0008688.
187. Schwarz H, Blanco FJ, Lotz M. Anadamide, an endogenous cannabinoid receptor agonist inhibits lymphocyte proliferation and induces apoptosis. J Neuroimmunol (1994) 55(1):107-15. doi:10.1016/0165-5728(94)90152-X.
188. Sarker KP, Maruyama I. Anandamide induces cell death independently of cannabinoid receptors or vanilloid receptor 1: possible involvement of lipid rafts. Cell Mol Life Sci (2003) 60(6):1200-8.
189. Joseph J, Niggemann B, Zaenker KS, Entschladen F. Anandamide is an endogenous inhibitor for the migration of tumor cells and T lymphocytes. Cancer Immunol Immunother (2004) 53(8):723-8. doi:10.1007/s00262-004-0509-9.
190. Lissoni P, Tintori A, Fumagalli L, Brivio F, Messina G, Parolini D, et al. The endocannabinoid anandamide neither impairs in vitro T-cell function nor induces regulatory T-cell generation. Anticancer Res (2008) 28(6A):3743-8.
191. Lenglet S, Thomas A, Soehnlein O, Montecucco F, Burger F, Pelli G, et al. Fatty acid amide hydrolase deficiency enhances intraplaque neutrophil recruitment in atherosclerotic mice. Arterioscler Thromb Vasc Biol (2013) 33(2):215-23. doi:10.1161/ATVBAHA.112.300275.
192. Ribeiro A, Ferraz-de-Paula V, Pinheiro ML, Sakai M, Costa-Pinto FA, Palermo-Neto J. Anandamide prior to sensitization increases cell-mediated immunity in mice. Int Immunopharmacol (2010) 10(4):431-9. doi:10.1016/j.intimp.2009.12.017.
193. Chen J, Lu RT, Lai R, Dinh T, Paul D, Venadas S, et al. Bimatoprost-induced calcium signaling in human T-cells does not involve prostanoid FP or TP receptors. Curr Eye Res (2009) 34(3):184-95. doi:10.1080/02713680802669781.
194. Jorda MA, Verbakel SE, Valk PJ, Vankan-Berkhoudt YV, Maccarrone M, Finazzi-Agro A, et al. Hematopoietic cells expressing the peripheral cannabinoid receptor migrate in response to the endocannabinoid 2-arachidonoylglycerol. Blood (2002) 99(8):2786-93. doi:10.1182/blood.V99.8.2786.
195. Basu S, Ray A, Dittel BN. Cannabinoid receptor 2 is critical for the homing and retention of marginal zone B lineage cells and for efficient T-independent immune responses. J Immunol (2011) 187(11):5720-32. doi:10.4049/jimmunol.1102195.
196. Kishimoto S, Muramatsu M, Gokoh M, Oka S, Waku K, Sugiura T. Endogenous cannabinoid receptor ligand induces the migration of human natural killer cells. J Biochem (2005) 137(2):217-23. doi:10.1093/jb/mvi021.
197. Maestroni GJ. The endogenous cannabinoid 2-arachidonoyl glycerol as in vivo chemoattractant for dendritic cells and adjuvant for Th1 response to a soluble protein. FASEB J (2004) 18(15):1914-6. doi:10.1096/fj.04-2190fje.
198. Rockwell CE, Snider NT, Thompson JT, Vanden Heuvel JP, Kaminski NE. Interleukin-2 suppression by 2-arachidonoyl glycerol is mediated through peroxisome proliferator-activated receptor gamma independently of cannabinoid receptors 1 and 2. Mol Pharmacol (2006) 70(1):101-11. doi:10.1124/mol.105.019117.
199. Rockwell CE, Raman P, Kaplan BL, Kaminski NE. A COX-2 metabolite of the endogenous cannabinoid, 2-arachidonoyl glycerol, mediates suppression of IL-2 secretion in activated Jurkat T cells. Biochem Pharmacol (2008) 76(3):353-61. doi:10.1016/j.bcp.2008.05.005.
200. McCusker MM, Grant-Kels JM. Healing fats of the skin: the structural and immunologic roles of the omega-6 and omega-3 fatty acids. Clin Dermatol (2010) 28(4):440-51. doi:10.1016/j.clindermatol.2010.03.020.
201. Woodworth HL, McCaskey SJ, Duriancik DM, Clinthorne JF, Langohr IM, Gardner EM, et al. Dietary fish oil alters T lymphocyte cell populations and exacerbates disease in a mouse model of inflammatory colitis. Cancer Res (2011) 70(20):7960-9. doi:10.1158/0008-5472.CAN-10-1396.
202. Monk JM, Jia Q, Callaway E, Weeks B, Alaniz RC, McMurray DN, et al. Th17 cell accumulation is decreased during chronic experimental colitis by (n-3) PUFA in Fat-1 mice. J Nutr (2011) 142(1):117-24. doi:10.3945/jn.111.147058.
203. Vassilopoulos D, Zurier RB, Rossetti RG, Tsokos GC. Gammalinolenic acid and dihomogammalinolenic acid suppress the CD3-mediated signal transduction pathway in human T cells. Clin Immunol Immunopathol (1997) 83(3):237-44. doi:10.1006/clin.1997.4343.
204. Kim W, Khan NA, McMurray DN, Prior IA, Wang N, Chapkin RS. Regulatory activity of polyunsaturated fatty acids in T-cell signaling. Prog Lipid Res (2010) 49(3):250-61. doi:10.1016/j.plipres.2010.01.002.
205. Bassaganya-Riera J, Hontecillas R. Dietary conjugated linoleic acid and n-3 polyunsaturated fatty acids in inflammatory bowel disease. Curr Opin Clin Nutr Metab Care (2010) 13(5):569-73. doi:10.1097/MCO.0b013e32833b648e.
206. Cao S, Ren J, Sun L, Gu G, Yuan Y, Li J. Fish oil-supplemented parenteral nutrition prolongs survival while beneficially altering phospholipids' fatty acid composition and modulating immune function in rat sepsis. Shock (2011) 36(2):184-90. doi:10.1097/SHK.0b013e31821e4f8b.
207. Cawood AL, Ding R, Napper FL, Young RH, Williams JA, Ward MJ, et al. Eicosapentaenoic acid (EPA) from highly concentrated n-3 fatty acid ethyl esters is incorporated into advanced atherosclerotic plaques and higher plaque EPA is associated with decreased plaque inflammation and increased stability. Atherosclerosis (2010) 212(1):252-9. doi:10.1016/j.atherosclerosis.2010.05.022.
208. Chen EP, Smyth EM. COX-2 and PGE2-dependent immunomodulation in breast cancer. Prostaglandins Other Lipid Mediat (2011) 96(1-4):14-20. doi:10.1016/j.prostaglandins.2011.08.005.
209. Ott J, Hiesgen C, Mayer K. Lipids in critical care medicine. Prostaglandins Leukot Essent Fatty Acids (2011) 85(5):267-73. doi:10.1016/j.plefa.2011.04.011.
210. Suzuki D, Furukawa K, Kimura F, Shimizu H, Yoshidome H, Ohtsuka M, et al. Effects of perioperative immunonutrition on cell-mediated immunity, T helper type 1 (Th1)/Th2 differentiation, and Th17 response after pancreaticoduodenectomy. Surgery (2010) 148(3):573-81. doi:10.1016/j.surg.2010.01.017.
211. Marik PE, Flemmer M. Immunonutrition in the surgical patient. Minerva Anestesiol (2012) 78(3):336-42.
212. Furuhjelm C, Jenmalm MC, Falth-Magnusson K, Duchen K. Th1 and Th2 chemokines, vaccine-induced immunity, and allergic disease in infants after maternal omega-3 fatty acid supplementation during pregnancy and lactation. Pediatr Res (2011) 69(3):259-64. doi:10.1203/PDR.0b013e3182072229.
213. Kong W, Yen JH, Ganea D. Docosahexaenoic acid prevents dendritic cell maturation, inhibits antigen-specific Th1/Th17 differentiation and suppresses experimental autoimmune encephalomyelitis. Brain Behav Immun (2011) 25(5):872-82. doi:10.1016/j.bbi.2010.09.012.
214. Ye P, Li J, Wang S, Xie A, Sun W, Xia J. Eicosapentaenoic acid disrupts the balance between Tregs and IL-17+ T cells through PPARgamma nuclear receptor activation and protects cardiac allografts. J Surg Res (2011) 173(1):161-70. doi:10.1016/j.jss.2010.08.052.
215. 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. Pediatr Allergy Immunol (2011) 22(5):497-504. doi:10.1111/j.1399-3038.2010.01133.x.