Prostaglandins, Leukotrienes and Essential Fatty Acids
Volume 82, Issue 4 , Pages 159-164 , April 2010

Diet-induced docosahexaenoic acid non-raft domains and lymphocyte function

  • Saame Raza Shaikh

      Affiliations

    • Department of Biochemistry and Molecular Biology, Brody School of Medicine, East Carolina University, 600 Moye Blvd, Greenville, NC 28590, USA
    • The Metabolic Institute for the Study of Diabetes and Obesity, Brody School of Medicine, East Carolina University, 600 Moye Blvd, Greenville, NC 28590, USA
    • Corresponding Author InformationTel.: +12527442595; fax: +12527333383.

References 

  1. Calder PC. n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am. J. Clin. Nutr. 2006;83:1505S–1519S
  2. Harris WS, Mozaffarian D, Lefevre M, Toner CD, Colombo J, Cunnane SC, et al. Towards establishing dietary reference intakes for eicosapentaenoic and docosahexaenoic acids. J. Nutr. 2009;139:804S–819S
  3. R.S. Chapkin, W. Kim, J.R. Lupton, D.N. McMurray, Dietary docosahexaenoic and eicosapentaenoic acid: emerging mediators of inflammation, Prostaglandins Leukotrienes Essent. Fatty Acid 81(2–3) (2009) 187–191.
  4. Fetterman JW, Zdanowicz MM. Therapeutic potential of n-3 polyunsaturated fatty acids in disease. Am. J. Health Syst. Pharm. 2009;66:1169–1179
  5. Bouwens M, van de Rest O, Dellschaft N, Bromhaar MG, de Groot LC, Geleijnse JM, et al. Fish-oil supplementation induces antiinflammatory gene expression profiles in human blood mononuclear cells. Am. J. Clin. Nutr. 2009;10:3945;/ajcn.2009.27680
  6. Calder PC. Immunomodulation by omega-3 fatty acids. Prostaglandins Leukotrienes Essent. Fatty Acids. 2007;77:327–335
  7. Pike LJ. Rafts defined: a report on the Keystone symposium on lipid rafts and cell function. J. Lipid Res. 2006;47:1597–1598
  8. Salem N, Kim HY, Yergey JA. Docosahexaenoic Acid: Membrane Function and Metabolism. New York: Academic press; 1986;319A-351.
  9. Stillwell W, Wassall SR. Docosahexaenoic acid: membrane properties of a unique fatty acid. Chem. Phys. Lipids. 2003;126:1–27
  10. Soubias O, Gawrisch K. Docosahexaenoyl chains isomerize on the sub-nanosecond time scale. J. Am. Chem. Soc. 2007;129:6678–6679
  11. Gawrisch K, Soubias O. Structure and dynamics of polyunsaturated hydrocarbon chains in lipid bilayers—significance for GPCR function. Chem. Phys. Lipids. 2008;153:64–75
  12. Eldho NV, Feller SE, Tristram-Nagle S, Polozov IV, Gawrisch K. Polyunsaturated docosahexaenoic vs docosapentaenoic acid-differences in lipid matrix properties from the loss of one double bond. J. Am. Chem. Soc. 2003;125:6409–6421
  13. Niu S, Mitchell DC, Lim S, Wen Z, Kim H, Salem N, et al. Reduced G protein-coupled signaling efficiency in retinal rod outer segments in response to n-3 fatty acid deficiency. J. Biol. Chem. 2004;279:31098–31104
  14. Grossfield A, Feller SE, Pitman MC. A role for direct interactions in the modulation of rhodopsin by n-3 polyunsaturated lipids. Proc. Natl. Acad. Sci. USA. 2006;103:4888–4893
  15. Carrillo-Tripp M, Feller SE. Evidence for a mechanism by which omega-3 polyunsaturated lipids may affect membrane protein function. Biochemistry. 2005;44:10164–10169
  16. Feller SE, Gawrisch K. Properties of docosahexaenoic-acid-containing lipids and their influence on the function of rhodopsin. Curr. Opin. Struct. Biol. 2005;15:416–422
  17. Pitman MC, Grossfield A, Suits F, Feller SE. Role of cholesterol and polyunsaturated chains in lipid–protein interactions: molecular dynamics simulation of rhodopsin in a realistic membrane environment. J. Am. Chem. Soc. 2005;127:4576–4577
  18. Feller SE. Acyl chain conformations in phospholipid bilayers: a comparative study of docosahexaenoic acid and saturated fatty acids. Chem. Phys. Lipids. 2008;153:76–80
  19. Huster D, Arnold K, Gawrisch K. Influence of docosahexaenoic acid and cholesterol on lateral lipid organization in phospholipid mixtures. Biochemistry. 1998;37:17299–17308
  20. Stillwell W, Jenski LJ, Zerouga M, Dumaual AC. Detection of lipid domains in docosahexaenoic acid-rich bilayers by acyl chain-specific FRET probes. Chem. Phys. Lipids. 2000;104:113–132
  21. Dumaual AC, Jenski LJ, Stillwell W. Liquid crystalline/gel state phase separation in docosahexaenoic acid-containing bilayers and monolayers. Biochim. Biophys. Acta. 2000;1463:395–406
  22. Shaikh SR, Brzustowicz MR, Gustafson N, Stillwell W, Wassall SR. Monounsaturated PE does not phase-separate from the lipid raft molecules sphingomyelin and cholesterol: role for polyunsaturation?. Biochemistry. 2002;41:10593–10602
  23. Shaikh SR, Cherezov V, Caffrey M, Stillwell W, Wassall SR. Interaction of cholesterol with a docosahexaenoic acid-containing phosphatidylethanolamine: trigger for microdomain/raft formation?. Biochemistry. 2003;42:12028–12037
  24. Shaikh SR, Dumaual AC, LoCassio D, Siddiqui RA, Stillwell W. Acyl chain unsaturation in PEs modulates phase separation from lipid raft molecules. Biochem. Biophys. Res. Commun. 2003;311:793–796
  25. Shaikh SR, Dumaual AC, Castillo A, LoCascio D, Siddiqui RA, 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. 2004;87:1752–1766
  26. Soni SP, LoCascio DS, Liu Y, Williams JA, Bittman R, Stillwell W, et al. Docosahexaenoic acid enhances segregation of lipids between raft and nonraft domains: 2H-NMR study. Biophys. J. 2008;95:203–214
  27. Shaikh SR, Dumaual AC, Jenski LJ, Stillwell W. Lipid phase separation in phospholipid bilayers and monolayers modeling the plasma membrane. Biochim. Biophys. Acta. 2001;1512:317–328
  28. Shaikh SR, Cherezov V, Caffrey M, Soni SP, LoCascio D, Stillwell W, et al. Molecular organization of cholesterol in unsaturated phosphatidylethanolamines: X-ray diffraction and solid state 2H NMR reveal differences with phosphatidylcholines. J. Am. Chem. Soc. 2006;128:5375–5383
  29. Brzustowicz MR, Cherezov V, Zerouga M, Caffrey M, Stillwell W, Wassall SR. Controlling membrane cholesterol content. A role for polyunsaturated (docosahexaenoate) phospholipids. Biochemistry. 2002;41:12509–12519
  30. Polozova A, Litman BJ. Cholesterol dependent recruitment of di22:6-PC by a G protein-coupled receptor into lateral domains. Biophys. J. 2000;79:2632–2643
  31. Jenski LJ, Nanda PK, Jiricko P, Stillwell W. Docosahexaenoic acid-containing phosphatidylcholine affects the binding of monoclonal antibodies to purified Kb reconstituted into liposomes. Biochim. Biophys. Acta. 2000;1467:293–306
  32. Jenski LJ, Bowker GM, Johnson MA, Ehringer WD, Fetterhoff T, Stillwell W. Docosahexaenoic acid-induced alteration of Thy-1 and CD8 expression on murine splenocytes. Biochim. Biophys. Acta. 1995;1236:39–50
  33. Maes M, Mihaylova I, Leunis JC. In chronic fatigue syndrome, the decreased levels of omega-3 poly-unsaturated fatty acids are related to lowered serum zinc and defects in T cell activation. Neuroendocrinol. Lett. 2005;26:745–751
  34. Pompos LJ, Fritsche KL. Antigen-driven murine CD4+ T lymphocyte proliferation and interleukin-2 production are diminished by dietary (n-3) polyunsaturated fatty acids. J. Nutr. 2002;132:3293–3300
  35. Arrington JL, Chapkin RS, Switzer KC, Morris JS, McMurray DN. Dietary n-3 polyunsaturated fatty acids modulate purified murine T-cell subset activation. Clin. Exp. Immunol. 2001;125:499–507
  36. Chapkin RS, Arrington JL, Apanasovich TV, Carroll RJ, McMurray DN. Dietary n-3 PUFA affect TcR-mediated activation of purified murine T cells and accessory cell function in co-cultures. Clin. Exp. Immunol. 2002;130:12–18
  37. Fan Y, Ly LH, Barhoumi R, McMurray DN, Chapkin RS. Dietary docosahexaenoic acid suppresses T cell protein kinase C θ lipid raft recruitment and IL-2 production. J. Immunol. 2004;173:6151–6160
  38. Kim W, Fan Y, Barhoumi R, Smith R, McMurray DN, Chapkin RS. n-3 polyunsaturated fatty acids suppress the localization and activation of signaling proteins at the immunological synapse in murine CD4+ T Cells by affecting lipid raft formation. J. Immunol. 2008;181:6236–6243
  39. Stulnig TM, Berger M, Sigmund T, Raederstorff D, Stockinger H, Waldhausl W. Polyunsaturated fatty acids inhibit T cell signal transduction by modification of detergent-insoluble membrane domains. J. Cell Biol. 1998;143:637–644
  40. Stulnig TM, Huber J, Leitinger N, Imre E, Angelisova P, Nowotny P, et al. Polyunsaturated eicosapentaenoic acid displaces proteins from membrane rafts by altering raft lipid composition. J. Biol. Chem. 2001;276:37335–37340
  41. Zeyda M, Staffler G, Horejsi V, Waldhausl W, Stulnig TM. LAT displacement from lipid rafts as a molecular mechanism for the inhibition of T cell signaling by polyunsaturated fatty acids. J. Biol. Chem. 2002;277:28418–28423
  42. Zeyda M, Szekeres AB, Saemann MD, Geyeregger R, Stockinger H, Zlabinger GJ, et al. Suppression of T cell signaling by polyunsaturated fatty acids: selectivity in inhibition of mitogen-activated protein kinase and nuclear factor activation. J. Immunol. 2003;170:6033–6039
  43. Ma DW, Seo J, Switzer KC, Fan YY, McMurray DN, Lupton JR, et al. n-3 PUFA and membrane microdomains: a new frontier in bioactive lipid research. J. Nutr. Biochem. 2004;15:700–706
  44. Heerklotz H. Triton promotes domain formation in lipid raft mixtures. Biophys. J. 2002;83:2693–2701
  45. Lichtenberg D, Goñi FM, Heerklotz H. Detergent-resistant membranes should not be identified with membrane rafts. Trends Biochem. Sci. 2005;30:430–436
  46. Shaikh SR, Edidin M. Polyunsaturated fatty acids, membrane organization, T cells, and antigen presentation. Am. J. Clin. Nutr. 2006;84:1277–1289
  47. Monks CR, Freiberg BA, Kupfer H, Sciaky N, Kupfer A. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature. 1998;395:82–86
  48. Zech T, Ejsing CS, 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. 2009;28:466–476
  49. Anderson M, Fritsche KL. n-3 fatty acids and infectious disease resistance. J. Nutr. 2002;132:3566–3576
  50. Shaikh SR, Edidin M. Polyunsaturated fatty acids and membrane organization: elucidating mechanisms to balance immunotherapy and susceptibility to infection. Chem. Phys. Lipids. 2008;153:24–33
  51. N.M.J. Schwerbrock, E.A. Karlsson, Q. Shi, P.A. Sheridan, M.A. Beck., Fish oil-fed mice have impaired resistance to influenza infection, J. Nutr. 139 (8) (2009) 1588–1594.
  52. Nagaraju K, Raben N, Loeffler L, Parker T, Rochon PJ, Lee E, et al. Conditional up-regulation of MHC class I in skeletal muscle leads to self-sustaining autoimmune myositis and myositis-specific autoantibodies. Proc. Natl. Acad. Sci. USA. 2000;97:9209–9214
  53. Hamilton-Williams EE, Palmer SE, Charlton B, Slattery RM. Beta cell MHC class I is a late requirement for diabetes. Proc. Natl. Acad. Sci. USA. 2003;100:6688–6693
  54. Feldmann M, Brennan FM, Maini RN. Rheumatoid arthritis. Cell. 1996;85:307–310
  55. Hughes DA, Pinder AC, Piper Z, Johnson IT, Lund EK. Fish oil supplementation inhibits the expression of major histocompatibility complex class II molecules and adhesion molecules on human monocytes. Am. J. Clin. Nutr. 1996;63:267–272
  56. Hughes DA, Pinder AC. Influence of n-3 polyunsaturated fatty acids (PUFA) on the antigen-presenting function of human monocytes. Biochem. Soc. Trans. 1996;24:389S
  57. Hughes DA, Pinder AC. n-3 polyunsaturated fatty acids inhibit the antigen-presenting function of human monocytes. Am. J. Clin. Nutr. 2000;71:357S–360S
  58. Sanderson P, MacPherson GG, Jenkins CH, Calder PC. Dietary fish oil diminishes the antigen presentation activity of rat dendritic cells. J. Leukocyte Biol. 1997;62:771–777
  59. Shaikh SR, Edidin M. Immunosuppressive effects of polyunsaturated fatty acids on antigen presentation by human leukocyte antigen class I molecules. J. Lipid Res. 2007;48:127–138
  60. Fooksman DR, Gronvall GK, Tang Q, Edidin M. Clustering class I MHC modulates sensitivity of T cell recognition. J. Immunol. 2006;176:6673–6680
  61. Kwik J, Boyle S, Fooksman D, Margolis L, Sheetz MP, Edidin M. Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4,5-bisphosphate-dependent organization of cell actin. Proc. Natl. Acad. Sci. USA. 2003;100:13964–13969
  62. Fooksman DR, Shaikh SR, Boyle S, Edidin M. Cutting edge: phosphatidylinositol 4,5-bisphosphate concentration at the APC side of the immunological synapse is required for effector T cell function. J. Immunol. 2009;182:5179–5182
  63. S.R. Shaikh, B.D. Rockett, M. Salameh, K. Carraway, 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 (9) (2009) 1632–1639.
  64. Chapkin RS, Wang N, Fan Y, Lupton JR, Prior IA. Docosahexaenoic acid alters the size and distribution of cell surface microdomains. Biochim. Biophys. Acta. 2008;1778:466–471
  65. Schley PD, Brindley DN, Field CJ. (n-3) PUFA alter raft lipid composition and decrease epidermal growth factor receptor levels in lipid rafts of human breast cancer cells. J. Nutr. 2007;137:548–553

PII: S0952-3278(10)00070-0

doi: 10.1016/j.plefa.2010.02.026

Prostaglandins, Leukotrienes and Essential Fatty Acids
Volume 82, Issue 4 , Pages 159-164 , April 2010

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