Fish oil increases raft size and membrane order of B cells accompanied by differential effects on function

Journal of Lipid Research

Volumn 53, Issue 4, 2012, Pages 674-685

  Rockett, Benjamin Drew ^a   Teague, Heather ^a   Harris, Mitchel ^a   Melton, Mark ^a   Williams, Justin ^b   Wassall, Stephen R ^b   Shaikh, Saame Raza ^a  

^a EAST CAROLINA UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

Antigen presenting cell; Cytokines; Detergent resistant membrane; Docosahexaenoic acid; Lymphocytes

Indexed keywords

CHOLERA TOXIN; DOCOSAHEXAENOIC ACID; FISH OIL; ICOSAPENTAENOIC ACID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; SPHINGOMYELIN;

ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; BODY WEIGHT; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL ISOLATION; CONTROLLED STUDY; CROSS LINKING; CYTOKINE PRODUCTION; FOOD INTAKE; LIPID RAFT; MALE; MEMBRANE STRUCTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPLEEN WEIGHT;

ANIMALS; B-LYMPHOCYTES; BODY WEIGHT; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CROSS-LINKING REAGENTS; DETERGENTS; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; FISH OILS; G(M1) GANGLIOSIDE; LIPOPOLYSACCHARIDES; LYMPHOCYTE ACTIVATION; MALE; MEMBRANE MICRODOMAINS; MICE; MICE, INBRED C57BL; PHOSPHATIDYLETHANOLAMINES;

EID: 84859404610     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M021782     Document Type: Article

References (52)

1. Calder, P. C. 2006. n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am. J. Clin. Nutr. 83: 1505S-1519S. (Pubitemid 44713092)
2. Duda, M. K., K. M. O'Shea, A. Tintinu, W. Xu, R. J. Khairallah, B. R. Barrows, D. J. Chess, A. M. Azimzadeh, W. S. Harris, V. G. Sharov, et al. 2009. Fish oil, but not flaxseed oil, decreases inflammation and prevents pressure overload-induced cardiac dysfunction. Cardiovasc. Res. 81: 319-327.
3. Harris, W. S., D. Mozaffarian, M. Lefevre, C. D. Toner, J. Colombo, S. C. Cunnane, J. M. Holden, D. M. Klurfeld, M. C. Morris, and J. Whelan. 2009. Towards establishing dietary reference intakes for eicosapentaenoic and docosahexaenoic acids. J. Nutr. 139: 804S-819S.
4. Calder, P. C. 2008. The relationship between the fatty acid composition of immune cells and their function. Prostaglandins Leukot. Essent. Fatty Acids. 79: 101-108.
5. Yaqoob, P., and S. R. Shaikh. 2010. The nutritional and clinical significance of lipid rafts. Curr. Opin. Clin. Nutr. Metab. Care. 13: 156-166.
6. Kim, W., Y-Y. Fan, R. Barhoumi, R. Smith, D. N. McMurray, and R. S. Chapkin. 2008. 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. 181: 6236-6243.
7. Shaikh, S. R., A. C. Dumaual, A. Castillo, D. LoCascio, R. A. Siddiqui, W. Stillwell, and S. R. Wassall. 2004. Oleic and docosahexaenoic acid differentially phase separate from lipid raft molecules: a comparative NMR, DSC, AFM, and detergent extraction study. Biophys. J. 87: 1752-1766. (Pubitemid 39167031)
8. 2H-NMR study. Biophys. J. 95: 203-214.
9. Grimm, M. O. W., J. Kuchenbecker, S. Grösgen, V. K. Burg, B. Hundsdörfer, T. L. Rothhaar, P. Friess, M. C. de Wilde, L. M. Broersen, B. Penke, et al. 2011. Docosahexaenoic acid reduces amyloid beta production via multiple pleiotropic mechanisms. J. Biol. Chem. 286: 14028-14039.
10. Aliche-Djoudi, F., N. Podechard, M. Chevanne, P. Nourissat, D. Catheline, P. Legrand, M-T. Dimanche-Boitrel, D. Lagadic-Gossmann, and O. Sergent. 2011. Physical and chemical modulation of lipid rafts by a dietary n-3 polyunsaturated fatty acid increases ethanol-induced oxidative stress. Free Radic. Biol. Med. 51: 2018-2030.
11. Bonilla, D. L., L. H. Ly, Y-Y. Fan, R. S. Chapkin, and D. N. McMurray. 2010. Incorporation of a dietary omega 3 fatty acid impairs murine macrophage responses to Mycobacterium tuberculosis. PLoS ONE. 5: e10878.
12. Ruth, M. R., S. D. Proctor, and C. J. Field. 2009. Feeding long-chain n-3 polyunsaturated fatty acids to obese leptin receptor-deficient JCR:LA-cp rats modifies immune function and lipid-raft fatty acid composition. Br. J. Nutr. 101: 1341-1350.
13. Winer, D. A., S. Winer, L. Shen, P. P. Wadia, J. Yantha, G. Paltser, H. Tsui, P. Wu, M. G. Davidson, M. N. Alonso, et al. 2011. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat. Med. 17: 610-617.
14. Hikada, M., and M. Zouali. 2010. Multistoried roles for B lymphocytes in autoimmunity. Nat. Immunol. 11: 1065-1068.
15. Rockett, B. D., A. Franklin, M. Harris, H. Teague, A. Rockett, and S. R. Shaikh. 2011. Membrane raft organization is more sensitive to disruption by (n-3) PUFA than nonraft organization in EL4 and B cells. J. Nutr. 141: 1041-1048.
16. Rockett, B. D., M. Salameh, K. Carraway, K. Morrison, and S. R. Shaikh. 2010. n-3 PUFA improves fatty acid composition, prevents palmitate-induced apoptosis, and differentially modifies B cell cytokine secretion in vitro and ex vivo. J. Lipid Res. 51: 1284-1297.
17. Kim, W., D. N. McMurray, and R. S. Chapkin. 2010. n-3 polyunsaturated fatty acids-physiological relevance of dose. Prostaglandins Leukot. Essent. Fatty Acids. 82: 155-158.
18. Shaikh, S. R., B. D. Rockett, M. Salameh, and K. Carraway. 2009. 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: 1632-1639.
19. 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.
20. Davis, J. H., K. R. Jeffrey, M. Bloom, M. I. Valic, and T. P. Higgs. 1976. Quadrupolar echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains. Chem. Phys. Lett. 42: 390-394.
21. Bacia, K., D. Scherfeld, N. Kahya, and P. Schwille. 2004. Fluorescence correlation spectroscopy relates rafts in model and native membranes. Biophys. J. 87: 1034-1043. (Pubitemid 39095082)
22. Parasassi, T., G. De Stasio, A. d'Ubaldo, and E. Gratton. 1990. Phase fluctuation in phospholipid membranes revealed by Laurdan fluorescence. Biophys. J. 57: 1179-1186. (Pubitemid 20203441)
23. Miguel, L., D. M. Owen, C. Lim, C. Liebig, J. Evans, A. I. Magee, and E. C. Jury. 2011. Primary human CD4 + T cells have diverse levels of membrane lipid order that correlate with their function. J. Immunol. 186: 3505-3516.
24. Rockett, B. D., M. Harris, and S. R. Shaikh. 2012. High dose of an n-3 polyunsaturated fatty acid diet lowers activity of C57BL/6 mice. Prostaglandins Leukot. Essent. Fatty Acids. In press. doi.org/10.1016/j. plefa.2011.12.001.
25. Zech, T., C. S. Ejsing, K. Gaus, B. de Wet, A. Shevchenko, K. Simons, and T. Harder. 2009. Accumulation of raft lipids in T-cell plasma membrane domains engaged in TCR signalling. EMBO J. 28: 466-476.
26. Switzer, K. C., Y-Y. Fan, N. Wang, D. N. McMurray, and R. S. Chapkin. 2004. Dietary n-3 polyunsaturated fatty acids promote activation-induced cell death in Th1-polarization murine CD4+T-cells. J. Lipid Res. 45: 1482-1492. (Pubitemid 39006976)
27. 2H NMR reveal differences with phosphatidylcholines. J. Am. Chem. Soc. 128: 5375-5383.
28. Heerklotz, H. 2002. Triton promotes domain formation in lipid raft mixtures. Biophys. J. 83: 2693-2701. (Pubitemid 35265761)
29. Lingwood, D., and K. Simons. 2007. Detergent resistance as a tool in membrane research. Nat. Protoc. 2: 2159-2165. (Pubitemid 351565854)
30. Jin, L., A. C. Millard, J. P. Wuskell, X. Dong, D. Wu, H. A. Clark, and L. M. Loew. 2006. Characterization and application of a new optical probe for membrane lipid domains. Biophys. J. 90: 2563-2575.
31. Stillwell, W., and S. R. Wassall. 2003. Docosahexaenoic acid: membrane properties of a unique fatty acid. Chem. Phys. Lipids. 126: 1-27. (Pubitemid 37297962)
32. Schley, P. D., D. N. Brindley, and C. J. Field. 2007. (n-3) PUFA alter raft lipid composition and decrease epidermal growth factor receptor levels in lipid rafts of human breast cancer cells. J. Nutr. 137: 548-553. (Pubitemid 46397481)
33. Fan, Y-Y., L. H. Ly, R. Barhoumi, D. N. McMurray, and R. S. Chapkin. 2004. Dietary docosahexaenoic acid suppresses T cell protein kinase Cθ lipid raft recruitment and IL-2 production. J. Immunol. 173: 6151-6160. (Pubitemid 39487772)
34. 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. (Pubitemid 36666535)
35. Mihailescu, M., O. Soubias, D. Worcester, S. H. White, and K. Gawrisch. 2011. Structure and dynamics of cholesterol-containing polyunsaturated lipid membranes studied by neutron diffraction and NMR. J. Membr. Biol. 239: 63-71.
36. Macdonald, J. L., and L. J. Pike. 2005. A simplified method for the preparation of detergent-free lipid rafts. J. Lipid Res. 46: 1061-1067.
37. Kheirallah, S., P. Caron, E. Gross, A. Quillet-Mary, J. Bertrand- Michel, J-J. Fournié, G. Laurent, and C. Bezombes. 2010. Rituximab inhibits B-cell receptor signaling. Blood. 115: 985-994.
38. Lingwood, D., J. Ries, P. Schwille, and K. Simons. 2008. Plasma membranes are poised for activation of raft phase coalescence at physiological temperature. Proc. Natl. Acad. Sci. USA. 105: 10005-10010.
39. van Zanten, T. S., J. Gómez, C. Manzo, A. Cambi, J. Buceta, R. Reigada, and M. F. Garcia-Parajo. 2010. Direct mapping of nanoscale compositional connectivity on intact cell membranes. Proc. Natl. Acad. Sci. USA. 107: 15437-15442.
40. Hsu, C-S., W-C. Chiu, C-L. Yeh, Y-C. Hou, S-Y. Chou, and S-L. Yeh. 2006. Dietary fish oil enhances adhesion molecule and interleukin-6 expression in mice with polymicrobial sepsis. Br. J. Nutr. 96: 854-860. (Pubitemid 46454561)
41. Blok, W. L., M. F. de Bruijn, P. J. Leenen, W. M. Eling, N. van Rooijen, E. R. Stanley, W. A. Buurman, and J. W. van der Meer. 1996. Dietary n-3 fatty acids increase spleen size and postendotoxin circulating TNF in mice; role of macrophages, macrophage precursors, and colony-stimulating factor-1. J. Immunol. 157: 5569-5573. (Pubitemid 126448979)
42. Petursdottir, D. H., and I. Hardardottir. 2007. Dietary fish oil increases the number of splenic macrophages secreting TNF-alpha and IL-10 but decreases the secretion of these cytokines by splenic T cells from mice. J. Nutr. 137: 665-670. (Pubitemid 46397500)
43. Weldon, S. M., A. C. Mullen, C. E. Loscher, L. A. Hurley, and H. M. Roche. 2007. Docosahexaenoic acid induces an anti-inflammatory profile in lipopolysaccharide-stimulated human THP-1 macrophages more effectively than eicosapentaenoic acid. J. Nutr. Biochem. 18: 250-258. (Pubitemid 46389578)
44. Weatherill, A. R., J. Y. Lee, L. Zhao, D. G. Lemay, H. S. Youn, and D. H. Hwang. 2005. Saturated and polyunsaturated fatty acids reciprocally modulate dendritic cell functions mediated through TLR4. J. Immunol. 174: 5390-5397. (Pubitemid 40593178)
45. Zeyda, M., M. D. Säemann, K. M. Stuhlmeier, D. G. Mascher, P. N. Nowotny, G. J. Zlabinger, W. Waldhäusl, and T. M. Stulnig. 2005. Polyunsaturated fatty acids block dendritic cell activation and function independently of NF-kappa B activation. J. Biol. Chem. 280: 14293-14301. (Pubitemid 40517332)
46. Beli, E., M. Li, C. Cuff, and J. J. Pestka. 2008. Docosahexaenoic acid-enriched fish oil consumption modulates immunoglobulin responses to and clearance of enteric reovirus infection in mice. J. Nutr. 138: 813-819. (Pubitemid 351469429)
47. Weise, C., K. Hilt, M. Milovanovic, D. Ernst, R. Rühl, and M. Worm. 2011. Inhibition of IgE production by docosahexaenoic acid is mediated by direct interference with STAT6 and NFκB pathway in human B cells. J. Nutr. Biochem. 22: 269-275.
48. Lauritzen, L., T. M. R. Kjær, T. Porsgaard, M. B. Fruekilde, H. Mu, and H. Frøkiær. 2011. Maternal intake of fish oil but not of linseed oil reduces the antibody response in neonatal mice. Lipids. 46: 171-178.
49. Selvaraj, R. K., and G. Cherian. 2004. Dietary n-3 fatty acids reduce the delayed hypersensitivity reaction and antibody production more than n-6 fatty acids in broiler birds. Eur. J. Lipid Sci. Technol. 106: 3-10. (Pubitemid 38253156)
50. Shaikh, S. R., and M. Edidin. 2007. Immunosuppressive effects of polyunsaturated fatty acids on antigen presentation by human leukocyte antigen class I molecules. J. Lipid Res. 48: 127-138. (Pubitemid 46052904)
51. Sanderson, P., G. G. MacPherson, C. H. Jenkins, and P. C. Calder. 1997. Dietary fish oil diminishes the antigen presentation activity of rat dendritic cells. J. Leukoc. Biol. 62: 771-777. (Pubitemid 28015625)
52. Chapkin, R. S., J. L. Arrington, T. V. Apanasovich, R. J. Carroll, and D. N. McMurray. 2002. Dietary n-3 PUFA affect TcR-mediated activation of purified murine T cells and accessory cell function in co-cultures. Clin. Exp. Immunol. 130: 12-18.