Dietary n-3 polyunsaturated fatty acids promote activation-induced cell death in Th1-polarized murine CD4+ T-cells

Journal of Lipid Research

Volumn 45, Issue 8, 2004, Pages 1482-1492

  Switzer, Kirsten C ^a   Fan, Yang Yi ^a   Wang, Naisyin ^a   McMurray, David N ^a,b   Chapkin, Robert S ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

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

Author keywords

Docosahexaenoic acid; Eicosapentaenoic acid; Interferon ; Lipid rafts

Indexed keywords

CD4 ANTIGEN; CORN OIL; DOCOSAHEXAENOIC ACID; FISH OIL; GAMMA INTERFERON; ICOSAPENTAENOIC ACID; INTERLEUKIN 4; LIPOCORTIN 5; OMEGA 3 FATTY ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROPIDIUM IODIDE; RECOMBINANT INTERLEUKIN 12; RECOMBINANT INTERLEUKIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; CYTOKINE RELEASE; DENSITY GRADIENT CENTRIFUGATION; FAT INTAKE; FEMALE; HELPER CELL; INFLAMMATION; LIPID BILAYER; LIPID COMPOSITION; LYMPHOCYTE CULTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; STATISTICAL ANALYSIS; TH1 CELL;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; DIETARY FATS, UNSATURATED; FATTY ACIDS, OMEGA-3; FATTY ACIDS, UNSATURATED; MEMBRANE MICRODOMAINS; MICE; TH1 CELLS; TRIGLYCERIDES;

EID: 3442900750     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: 10.1194/jlr.M400028-JLR200     Document Type: Article

References (56)

1. Abbas, A. K., K. M. Murphy, and A. Sher. 1996. Functional diversity of helper T lymphocytes. Nature. 383: 787-793.
2. Liblau, R. S., S. M. Singer, and H. O. McDevitt. 1995. Th1 and Th2 CD4+ T cells in the pathogenesis of organ-specific autoimmune diseases. Immunol. Today. 16: 34-38.
3. Zhang, X., T. Brunner, L. Carter, R. W. Dutton, P. Rogers, L. Bradley, T. Sato, J. C. Reed, D. Green, and S. L. Swain. 1997. Unequal death in T helper cell (Th) 1 and Th2 effectors: Th1, but not Th2, effectors undergo rapid Fas/FasL-mediated apoptosis. J. Exp. Med. 185: 1837-1849.
4. Yahata, T., N. Abe, C. Yahata, Y. Ohmi, A. Ohta, K. Iwakabe, S. Habu, H. Yagita, H. Kitamura, N. Matsuki, M. Nakui, M. Sato, and T. Nishimura. 1999. The essential role of phorbol ester-sensitive protein kinase C isoforms in activation-induced cell death of Th1 cells. Eur. J. Immunol. 29: 727-732.
5. Ramsdell, F., M. S. Seaman, R. E. Miller, K. S. Picha, M. K. Kennedy, and D. H. Lynch. 1994. Differential ability of Th1 and Th2 T cells to express Fas ligand and to undergo activation-induced cell death. Int. Immunol. 6: 1545-1553.
6. Varadhachary, A. S., M. Edidin, A. M. Hanlon, M. E. Peter, P. H. Krammer, and P. Salgame. 2001. Phosphatidylinositol 3′-kinase blocks CD95 aggregation and caspase-8 cleavage at the death-inducing signaling complex by modulating lateral diffusion of CD95. J. Immunol. 166: 6564-6569.
7. Refaeli, Y., L. Van Parijs, C. A. London, J. Tschopp, and A. K. Abbas. 1998. Biochemical mechanisms of IL-2-regulated Fas-mediated T cell apoptosis. Immunity. 8: 615-623.
8. Dhein, J., H. Walczak, C. Baumler, K. M. Debatin, and P. H. Krammer. 1995. Autocrine T-cell suicide mediated by APO-1/(Fas/CD95). Nature. 373: 438-441.
9. Scheel-Toellner, D., K. Wang, R. Singh, S. Majeed, K. Raza, S. J. Curnow, M. Salmon, and J. M. Lord. 2002. The death-inducing signalling complex is recruited to lipid rafts in Fas-induced apoptosis. Biochem. Biophys. Res. Commun. 297: 876-879.
10. Brown, D. A., and E. London. 2000. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275: 17221-17224.
11. Balamuth, F., D. Leitenberg, J. Unternaehrer, I. Mellman, and K. Bottomly. 2001. Distinct patterns of membrane microdomain partitioning in Th1 and Th2 cells. Immunity. 15: 729-738.
12. Muppidi, J. R., and R. M. Siegel. 2004. Ligand-independent redistribution of Fas (CD95) into lipid rafts mediates clonotypic T cell death. Nat. Immunol. 5: 182-189.
13. Leitenberg, D., F. Balamuth, and K. Bottomly. 2001. Changes in the T cell receptor macromolecular signaling complex and membrane microdomains during T cell development and activation. Semin. Immunol. 13: 129-138.
14. Fan, Y. Y., D. N. McMurray, L. H. Ly, and R. S. Chapkin. 2003. Dietary (n-3) polyunsaturated fatty acids remodel mouse T-cell lipid rafts. J. Nutr. 133: 1913-1920.
15. Stulnig, T. M., J. Huber, N. Leitinger, E. M. Imre, P. Angelisova, P. Nowotny, and W. Waldhausl. 2001. Polyunsaturated eicosapentaenoic acid displaces proteins from membrane rafts by altering raft lipid composition. J. Biol. Chem. 276: 37335-37340.
16. Calder, P. C. 1998. Dietary fatty acids and the immune system. Nutr. Rev. 56 (Suppl.): 70-83.
17. Chapkin, R. S., D. N. McMurray, and C. A. Jolly. 1999. Dietary n-3 polyunsaturated fatty acids modulate T cell lymphocyte activation: clinical relevance in treating diseases of chronic inflammation. In Nutrition and Immunology: Principles and Practice. M.E. Gershwin, B. German, and C. Keen, editors. Plenum, New York. 121-134.
18. Kremer, J. M. 2000. n-3 fatty acid supplements in rheumatoid arthritis. Am. J. Clin. Nutr 71 (Suppl.): 349-351.
19. Arrington, J. L., R. S. Chapkin, K. C. Switzer, J. S. Morris, and D. N. McMurray. 2001. Dietary n-3 polyunsaturated fatty acids modulate purified murine T-cell subset activation. Clin. Exp. Immunol. 125: 499-507.
20. Switzer, K. C., D. N. McMurray, J. S. Morris, and R. S. Chapkin. 2003. (n-3) polyunsaturated fatty acids promote activation-induced cell death in murine T lymphocytes. J. Nutr. 133: 496-503.
21. Yaqoob, P., E. A. Newsholme, and P. C. Calder. 1995. Influence of cell culture conditions on diet-induced changes in lymphocyte fatty acid composition. Biochim. Biophys. Acta. 1255: 333-340.
22. Pompos, L. J., and K. L. Fritsche. 2002. Antigen-driven murine CD4+ T lymphocyte proliferation and interleukin-2 production are diminished by dietary (n-3) polyunsaturated fatty acids. J. Nutr. 132: 3293-3300.
23. Arrington, J. L., D. N. McMurray, K. C. Switzer, Y. Y. Fan, and R. S. Chapkin. 2001. Docosahexaenoic acid suppresses function of the CD28 costimulatory membrane receptor in primary, murine and Jurkat T cells. J. Nutr. 131: 1147-1153.
24. National Research Council. 1995. Nutrient requirements for laboratory animals. 4th edition. National Academic Press, Washington, D.C.
25. Yamashita, M., M. Katsumata, M. Iwashima, M. Kimura, C. Shimizu, T. Kamata, T. Shin, N. Seki, S. Suzuki, M. Taniguchi, and T. Nakayama. 2000. T cell receptor-induced calcineurin activation regulates T helper type 2 cell development by modifying the interleukin 4 receptor signaling complex. J. Exp. Med. 191: 1869-1879.
26. Tamir, A., M. D. Eisenbraun, G. G. Garcia, and R. A. Miller. 2000. Age-dependent alterations in the assembly of signal transduction complexes at the site of T cell/APC interaction. J. Immunol. 165: 1243-1251.
27. Folch, J., M. Lees, and G. H. Sloane Stanley. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226: 497-509.
28. Rousseeuw, P. J., and A. M. Leroy. 1987. Robust Regression and Outlier Detection. Wiley, New York.
29. Martin, S.J., C. P. Reutelingsperger, A. J. McGahon, J. A. Rader, R. C. van Schie, D. M. LaFace, and D. R. Green. 1995. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182: 1545-1556.
30. Bacso, Z., R. B. Everson, and J. F. Eliason. 2000. The DNA of annexin V binding apoptotic cells is highly fragmented. Cancer Res. 60: 4623-4628.
31. Swinnen, J. V., P. P. Van Veldhoven, L. Timmermans, E. De Schrijver, K. Brusselmans, F. Vanderhoydonc, T. Van de Sande, H. Heemers, W. Heyns, and G. Verhoeven. 2003. Fatty acid synthase drives the synthesis of phospholipids partitioning into detergent-resistant membrane microdomains. Biochem. Biophys. Res. Commun. 302: 898-903.
32. Spector, A. A. 1999. Essentiality of fatty acids. Lipids. 34 (Suppl.): 1-3.
33. Simopoulos, A. P. 1991. Omega-3 fatty acids in health and disease and in growth and development. Am. J. Clin. Nutr. 54: 438-463.
34. Meydani, S. N., S. Endres, M. M. Woods, B. R. Goldin, C. Soo, A. Morrill-Labrode, C. A. Dinarello, and S. L. Gorbach. 1991. Oral (n-3) fatty acid supplementation suppresses cytokine production and lymphocyte proliferation: comparison between young and older women. J. Nutr. 121: 547-555.
35. Yaqoob, P. 2003. Fatty acids as gatekeepers of immune cell regulation. Trends Immunol. 24: 639-645.
36. Nagata, C., N. Takatsuka, and H. Shimizu. 2002. Soy and fish oil intake and mortality in a Japanese community. Am. J. Epidemiol. 156: 824-831.
37. Gibney, M. J. 1997. Incorporation of n-3 polyunsaturated fatty acids into processed foods. Br. J. Nutr. 78: 193-195.
38. Yaqoob, P., E. A. Newsholme, and P. C. Calder. 1994. The effect of dietary lipid manipulation on rat lymphocyte subsets and proliferation. Immunology. 82: 603-610.
39. Fritsche, K. L., M. Byrge, and C. Feng. 1999. Dietary omega-3 polyunsaturated fatty acids from fish oil reduce interleukin-12 and interferon-gamma production in mice. Immunol. Lett. 65: 167-173.
40. Wallace, F. A., E. A. Miles, C. Evans, T. E. Stock, P. Yaqoob, and P. C. Calder. 2001. Dietary fatty acids influence the production of Th1- but not Th2-type cytokines. J. Leukoc. Biol. 69: 449-457.
41. Oarada, M., T. Tsuduki, T. Suzuki, T. Miyazawa, T. Nikawa, G. Hong-quan, and N. Kurita. 2003. Dietary supplementation with docosahexaenoic acid, but not with eicosapentaenoic acid, reduces host resistance to fungal infection in mice. Biochim. Biophys. Acta. 1622: 151-160.
42. Fritsche, K. L., C. Feng, and J. N. Berg. 1997. Dietary fish oil enhances circulating interferon-gamma in mice during listeriosis without altering in vitro production of this cytokine. J. Interferon Cytokine Res. 17: 271-277.
43. Fritsche, K. L., M. Anderson, and C. Feng. 2000. Consumption of eicosapentaenoic acid and docosahexaenoic acid impair murine interleukin-12 and interferon-gamma production in vivo. J. Infect. Dis. 182 (Suppl. 1): 54-61.
44. Hueber, A. O., A. M. Bernard, Z. Herincs, A. Couzinet, and H. T. He. 2002. An essential role for membrane rafts in the initiation of Fas/CD95-triggered cell death in mouse thymocytes. EMBO Rep. 3: 190-196.
45. Xavier, R., T. Brennan, Q. Li, C. McCormack, and B. Seed. 1998. Membrane compartmentation is required for efficient T cell activation. Immunity. 8: 723-732.
46. Grassme, H., A. Jekle, A. Richle, H. Schwarz, J. Berger, K. Sandhoff, R. Kolesnick, and E. Gulbins. 2001. CD95 signaling via ceramide-rich membrane rafts. J. Biol. Chem. 276: 20589-20596.
47. Refaeli, Y., L. Van Parijs, S. I. Alexander, and A. K. Abbas. 2002. Interferon gamma is required for activation-induced death of T lymphocytes. J. Exp. Med. 196: 999-1005.
48. Subramaniam, P. S., and H. M. Johnson. 2002. Lipid microdomains are required sites for the selective endocytosis and nuclear translocation of IFN-gamma, its receptor chain IFN-gamma receptor-1, and the phosphorylation and nuclear translocation of STAT1alpha. J. Immunol. 169: 1959-1969.
49. Yano, S., P. Ghosh, H. Kusaba, M. Buchholz, and D. L. Longo. 2003. Effect of promoter methylation on the regulation of IFN-gamma gene during in vitro differentiation of human peripheral blood T cells into a Th2 population. J. Immunol. 171: 2510-2516.
50. Katamura, K., T. Fukui, T. Kiyomasu, J. Iio, G. Tai, H. Ueno, T. Heike, M. Mayumi, and K. Furusho. 1998. IL-4 and prostaglandin E2 inhibit hypomethylation of the 5′ regulatory region of IFN-gamma gene during differentiation of naive CD4+ T cells. Mol. Immunol. 35: 39-45.
51. Endres, S., R. Ghorbani, V. E. Kelley, K. Georgilis, G. Lonnemann, J. W. van der Meer, J. G. Cannon, T. S. Rogers, M. S. Klempner, P. C. Weber, E. J. Schaefer, S. M. Wolff, and C. A. Dinarello. 1989. The effect of dietary supplementation with n-3 polyunsaturated fatty acids on the synthesis of interleukin-1 and tumor necrosis factor by mononuclear cells. N. Engl. J. Med. 320: 265-271.
52. Brash, A. R. 2001. Arachidonic acid as a bioactive molecule. J. Clin. Invest. 107: 1339-1345.
53. Chung, S. W., B. Y. Kang, and T. S. Kim. 2003. Inhibition of interleukin-4 production in CD4+ T cells by peroxisome proliferator-activated receptor-gamma (PPAR-gamma) ligands: involvement of physical association between PPAR-gamma and the nuclear factor of activated T cells transcription factor. Mol. Pharmacol. 64: 1169-1179.
54. Marx, N., B. Kehrle, K. Kohlhammer, M. Grub, W. Koenig, V. Hombach, P. Libby, and J. Plutzky. 2002. PPAR activators as antiinflammatory mediators in human T lymphocytes: implications for atherosclerosis and transplantation- associated arteriosclerosis. Circ. Res. 90: 703-710.
55. Fan, Y. Y., T. E. Spencer, N. Wang, M. P. Moyer, and R. S. Chapkin. 2003. Chemopreventive n-3 fatty acids activate RXRalpha in colonocytes. Carcinogenesis. 24: 1541-1548.
56. Xu, H. E., M. H. Lambert, V. G. Montana, D. J. Parks, S. G. Blanchard, P. J. Brown, D. D. Sternbach, J. M. Lehmann, G. B. Wisely, T. M. Willson, S. A. Kliewer, and M. V. Milburn. 1999. Molecular recognition of fatty acids by peroxisome proliferator-activated receptors. Mol. Cell. 3: 397-403.