Skip to main content
Immunology logoLink to Immunology
. 1998 May;94(1):79–87. doi: 10.1046/j.1365-2567.1998.00474.x

Dietary fish oil diminishes lymphocyte adhesion to macrophage and endothelial cell monolayers.

P Sanderson 1, P C Calder 1
PMCID: PMC1364334  PMID: 9708190

Abstract

To further investigate the immunomodulatory effects of dietary lipids, rats were fed on a low-fat diet or on high-fat diets that contained hydrogenated coconut, olive, safflower, evening primrose or fish oil as the principal fat source. The fish oil diet decreased the level of expression of CD2, CD11a, CD18 and CD44 on the surface of freshly prepared lymphocytes and of CD2, CD11a, CD18, CD54 (intercellular adhesion molecule-1; ICAM-1) and CD62L (L-selectin) on the surface of concanavalin A (Con A)-stimulated lymphocytes. The olive oil diet also resulted in decreased expression of some adhesion molecules. The fish or olive oil diets, and to a lesser extent the safflower or evening primrose oil diets, decreased the adhesion of both freshly prepared and Con A-stimulated lymphocytes to macrophage monolayers. The fish oil diet, and to a lesser extent the olive or evening primrose oil diets, reduced the ability of Con A-stimulated lymphocytes to adhere to untreated endothelial cells. Furthermore, the fish oil diet resulted in a 50% reduction in Con A-stimulated lymphocyte adhesion to tumour necrosis factor-alpha (TNF-alpha)-stimulated endothelial cells. This study demonstrates that dietary lipids affect the expression of functionally important adhesion molecules on the surface of lymphocytes. Furthermore, this study suggests that such diet-induced effects on adhesion molecule expression might alter the ability of lymphocytes to bind to macrophages and to endothelial cells. Of the diets studied fish oil causes the most significant effects. The results of this study suggest that a reduction in cellular infiltration may partly explain the protective effect of a fish-oil-rich diet against the development of inflammatory and cardiovascular diseases.

Full text

PDF
79

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aslan A., Triadafilopoulos G. Fish oil fatty acid supplementation in active ulcerative colitis: a double-blind, placebo-controlled, crossover study. Am J Gastroenterol. 1992 Apr;87(4):432–437. [PubMed] [Google Scholar]
  2. Bates D., Cartlidge N. E., French J. M., Jackson M. J., Nightingale S., Shaw D. A., Smith S., Woo E., Hawkins S. A., Millar J. H. A double-blind controlled trial of long chain n-3 polyunsaturated fatty acids in the treatment of multiple sclerosis. J Neurol Neurosurg Psychiatry. 1989 Jan;52(1):18–22. doi: 10.1136/jnnp.52.1.18. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Belluzzi A., Brignola C., Campieri M., Pera A., Boschi S., Miglioli M. Effect of an enteric-coated fish-oil preparation on relapses in Crohn's disease. N Engl J Med. 1996 Jun 13;334(24):1557–1560. doi: 10.1056/NEJM199606133342401. [DOI] [PubMed] [Google Scholar]
  4. Bittiner S. B., Tucker W. F., Cartwright I., Bleehen S. S. A double-blind, randomised, placebo-controlled trial of fish oil in psoriasis. Lancet. 1988 Feb 20;1(8582):378–380. doi: 10.1016/s0140-6736(88)91181-6. [DOI] [PubMed] [Google Scholar]
  5. Bjørneboe A., Søyland E., Bjørneboe G. E., Rajka G., Drevon C. A. Effect of dietary supplementation with eicosapentaenoic acid in the treatment of atopic dermatitis. Br J Dermatol. 1987 Oct;117(4):463–469. doi: 10.1111/j.1365-2133.1987.tb04926.x. [DOI] [PubMed] [Google Scholar]
  6. Calder P. C., Bond J. A., Harvey D. J., Gordon S., Newsholme E. A. Uptake and incorporation of saturated and unsaturated fatty acids into macrophage lipids and their effect upon macrophage adhesion and phagocytosis. Biochem J. 1990 Aug 1;269(3):807–814. doi: 10.1042/bj2690807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Calder P. C. Sir David Cuthbertson Medal Lecture. Immunomodulatory and anti-inflammatory effects of n-3 polyunsaturated fatty acids. Proc Nutr Soc. 1996 Jul;55(2):737–774. doi: 10.1079/pns19960069. [DOI] [PubMed] [Google Scholar]
  8. Calder P. C. n-3 polyunsaturated fatty acids and cytokine production in health and disease. Ann Nutr Metab. 1997;41(4):203–234. doi: 10.1159/000177997. [DOI] [PubMed] [Google Scholar]
  9. Cleland L. G., French J. K., Betts W. H., Murphy G. A., Elliott M. J. Clinical and biochemical effects of dietary fish oil supplements in rheumatoid arthritis. J Rheumatol. 1988 Oct;15(10):1471–1475. [PubMed] [Google Scholar]
  10. D'Ambola J. B., Aeberhard E. E., Trang N., Gaffar S., Barrett C. T., Sherman M. P. Effect of dietary (n-3) and (n-6) fatty acids on in vivo pulmonary bacterial clearance by neonatal rabbits. J Nutr. 1991 Aug;121(8):1262–1269. doi: 10.1093/jn/121.8.1262. [DOI] [PubMed] [Google Scholar]
  11. Das U. N. Beneficial effect of eicosapentaenoic and docosahexaenoic acids in the management of systemic lupus erythematosus and its relationship to the cytokine network. Prostaglandins Leukot Essent Fatty Acids. 1994 Sep;51(3):207–213. doi: 10.1016/0952-3278(94)90136-8. [DOI] [PubMed] [Google Scholar]
  12. De Caterina R., Cybulsky M. A., Clinton S. K., Gimbrone M. A., Jr, Libby P. Omega-3 fatty acids and endothelial leukocyte adhesion molecules. Prostaglandins Leukot Essent Fatty Acids. 1995 Feb-Mar;52(2-3):191–195. doi: 10.1016/0952-3278(95)90021-7. [DOI] [PubMed] [Google Scholar]
  13. Espersen G. T., Grunnet N., Lervang H. H., Nielsen G. L., Thomsen B. S., Faarvang K. L., Dyerberg J., Ernst E. Decreased interleukin-1 beta levels in plasma from rheumatoid arthritis patients after dietary supplementation with n-3 polyunsaturated fatty acids. Clin Rheumatol. 1992 Sep;11(3):393–395. doi: 10.1007/BF02207200. [DOI] [PubMed] [Google Scholar]
  14. Faull R. J. Adhesion molecules in health and disease. Aust N Z J Med. 1995 Dec;25(6):720–730. doi: 10.1111/j.1445-5994.1995.tb02861.x. [DOI] [PubMed] [Google Scholar]
  15. Fritsche K. L., Shahbazian L. M., Feng C., Berg J. N. Dietary fish oil reduces survival and impairs bacterial clearance in C3H/Hen mice challenged with Listeria monocytogenes. Clin Sci (Lond) 1997 Jan;92(1):95–101. doi: 10.1042/cs0920095. [DOI] [PubMed] [Google Scholar]
  16. Grimminger F., Grimm H., Führer D., Papavassilis C., Lindemann G., Blecher C., Mayer K., Tabesch F., Krämer H. J., Stevens J. Omega-3 lipid infusion in a heart allotransplant model. Shift in fatty acid and lipid mediator profiles and prolongation of transplant survival. Circulation. 1996 Jan 15;93(2):365–371. doi: 10.1161/01.cir.93.2.365. [DOI] [PubMed] [Google Scholar]
  17. Hawthorne A. B., Daneshmend T. K., Hawkey C. J., Belluzzi A., Everitt S. J., Holmes G. K., Malkinson C., Shaheen M. Z., Willars J. E. Treatment of ulcerative colitis with fish oil supplementation: a prospective 12 month randomised controlled trial. Gut. 1992 Jul;33(7):922–928. doi: 10.1136/gut.33.7.922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hogg N., Landis R. C. Adhesion molecules in cell interactions. Curr Opin Immunol. 1993 Jun;5(3):383–390. doi: 10.1016/0952-7915(93)90057-y. [DOI] [PubMed] [Google Scholar]
  19. Hughes D. A., Pinder A. C., Piper Z., Johnson I. T., Lund E. K. Fish oil supplementation inhibits the expression of major histocompatibility complex class II molecules and adhesion molecules on human monocytes. Am J Clin Nutr. 1996 Feb;63(2):267–272. doi: 10.1093/ajcn/63.2.267. [DOI] [PubMed] [Google Scholar]
  20. Hughes D. A., Southon S., Pinder A. C. (n-3) Polyunsaturated fatty acids modulate the expression of functionally associated molecules on human monocytes in vitro. J Nutr. 1996 Mar;126(3):603–610. doi: 10.1093/jn/126.3.603. [DOI] [PubMed] [Google Scholar]
  21. Khalfoun B., Thibault G., Bardos P., Lebranchu Y. Docosahexaenoic and eicosapentaenoic acids inhibit in vitro human lymphocyte-endothelial cell adhesion. Transplantation. 1996 Dec 15;62(11):1649–1657. doi: 10.1097/00007890-199612150-00020. [DOI] [PubMed] [Google Scholar]
  22. Kim D. N., Schmee J., Thomas W. A. Dietary fish oil added to a hyperlipidemic diet for swine results in reduction in the excessive number of monocytes attached to arterial endothelium. Atherosclerosis. 1990 Apr;81(3):209–216. doi: 10.1016/0021-9150(90)90068-t. [DOI] [PubMed] [Google Scholar]
  23. Kort W. J., de Keijzer M. H., Hekking-Weijma I., Vermeij M. Dietary fatty acids and kidney transplantation in the rat. Ann Nutr Metab. 1991;35(3):148–157. doi: 10.1159/000177639. [DOI] [PubMed] [Google Scholar]
  24. Kremer J. M., Bigauoette J., Michalek A. V., Timchalk M. A., Lininger L., Rynes R. I., Huyck C., Zieminski J., Bartholomew L. E. Effects of manipulation of dietary fatty acids on clinical manifestations of rheumatoid arthritis. Lancet. 1985 Jan 26;1(8422):184–187. doi: 10.1016/s0140-6736(85)92024-0. [DOI] [PubMed] [Google Scholar]
  25. Kremer J. M., Jubiz W., Michalek A., Rynes R. I., Bartholomew L. E., Bigaouette J., Timchalk M., Beeler D., Lininger L. Fish-oil fatty acid supplementation in active rheumatoid arthritis. A double-blinded, controlled, crossover study. Ann Intern Med. 1987 Apr;106(4):497–503. doi: 10.7326/0003-4819-106-4-497. [DOI] [PubMed] [Google Scholar]
  26. Kremer J. M., Lawrence D. A., Jubiz W., DiGiacomo R., Rynes R., Bartholomew L. E., Sherman M. Dietary fish oil and olive oil supplementation in patients with rheumatoid arthritis. Clinical and immunologic effects. Arthritis Rheum. 1990 Jun;33(6):810–820. doi: 10.1002/art.1780330607. [DOI] [PubMed] [Google Scholar]
  27. Kromann N., Green A. Epidemiological studies in the Upernavik district, Greenland. Incidence of some chronic diseases 1950-1974. Acta Med Scand. 1980;208(5):401–406. [PubMed] [Google Scholar]
  28. Kromhout D., Bosschieter E. B., de Lezenne Coulander C. The inverse relation between fish consumption and 20-year mortality from coronary heart disease. N Engl J Med. 1985 May 9;312(19):1205–1209. doi: 10.1056/NEJM198505093121901. [DOI] [PubMed] [Google Scholar]
  29. Leaf A., Weber P. C. Cardiovascular effects of n-3 fatty acids. N Engl J Med. 1988 Mar 3;318(9):549–557. doi: 10.1056/NEJM198803033180905. [DOI] [PubMed] [Google Scholar]
  30. Maurice P. D., Allen B. R., Barkley A. S., Cockbill S. R., Stammers J., Bather P. C. The effects of dietary supplementation with fish oil in patients with psoriasis. Br J Dermatol. 1987 Nov;117(5):599–606. doi: 10.1111/j.1365-2133.1987.tb07492.x. [DOI] [PubMed] [Google Scholar]
  31. Muller C. P., Stephany D. A., Shinitzky M., Wunderlich J. R. Changes in cell-surface expression of MHC and Thy-1.2 determinants following treatment with lipid modulating agents. J Immunol. 1983 Sep;131(3):1356–1362. [PubMed] [Google Scholar]
  32. Pankonin G., Reipert B., Ager A. Interactions between interleukin-2-activated lymphocytes and vascular endothelium: binding to and migration across specialized and non-specialized endothelia. Immunology. 1992 Sep;77(1):51–60. [PMC free article] [PubMed] [Google Scholar]
  33. Sanderson P., Yaqoob P., Calder P. C. Effects of dietary lipid manipulation upon graft vs host and host vs graft responses in the rat. Cell Immunol. 1995 Sep;164(2):240–247. doi: 10.1006/cimm.1995.1167. [DOI] [PubMed] [Google Scholar]
  34. Spertini O., Kansas G. S., Munro J. M., Griffin J. D., Tedder T. F. Regulation of leukocyte migration by activation of the leukocyte adhesion molecule-1 (LAM-1) selectin. Nature. 1991 Feb 21;349(6311):691–694. doi: 10.1038/349691a0. [DOI] [PubMed] [Google Scholar]
  35. Springer T. A. Adhesion receptors of the immune system. Nature. 1990 Aug 2;346(6283):425–434. doi: 10.1038/346425a0. [DOI] [PubMed] [Google Scholar]
  36. Stenson W. F., Cort D., Rodgers J., Burakoff R., DeSchryver-Kecskemeti K., Gramlich T. L., Beeken W. Dietary supplementation with fish oil in ulcerative colitis. Ann Intern Med. 1992 Apr 15;116(8):609–614. doi: 10.7326/0003-4819-116-8-609. [DOI] [PubMed] [Google Scholar]
  37. Stoolman L. M. Adhesion molecules controlling lymphocyte migration. Cell. 1989 Mar 24;56(6):907–910. doi: 10.1016/0092-8674(89)90620-x. [DOI] [PubMed] [Google Scholar]
  38. Terano T., Kojima T., Seya A., Tanabe E., Hirai A., Makuta H., Ozawa A., Fujita T., Tamura Y., Okamoto S. The effect of highly purified eicosapentaenoic acid in patients with psoriasis. Adv Prostaglandin Thromboxane Leukot Res. 1989;19:610–613. [PubMed] [Google Scholar]
  39. Yaqoob P., Newsholme E. A., Calder P. C. Influence of cell culture conditions on diet-induced changes in lymphocyte fatty acid composition. Biochim Biophys Acta. 1995 Apr 6;1255(3):333–340. doi: 10.1016/0005-2760(94)00251-s. [DOI] [PubMed] [Google Scholar]
  40. Yaqoob P., Newsholme E. A., Calder P. C. Inhibition of natural killer cell activity by dietary lipids. Immunol Lett. 1994 Jul;41(2-3):241–247. doi: 10.1016/0165-2478(94)90140-6. [DOI] [PubMed] [Google Scholar]
  41. Yaqoob P., Newsholme E. A., Calder P. C. The effect of dietary lipid manipulation on rat lymphocyte subsets and proliferation. Immunology. 1994 Aug;82(4):603–610. [PMC free article] [PubMed] [Google Scholar]
  42. Ziboh V. A., Cohen K. A., Ellis C. N., Miller C., Hamilton T. A., Kragballe K., Hydrick C. R., Voorhees J. J. Effects of dietary supplementation of fish oil on neutrophil and epidermal fatty acids. Modulation of clinical course of psoriatic subjects. Arch Dermatol. 1986 Nov;122(11):1277–1282. [PubMed] [Google Scholar]
  43. van der Heide J. J., Bilo H. J., Donker J. M., Wilmink J. M., Tegzess A. M. Effect of dietary fish oil on renal function and rejection in cyclosporine-treated recipients of renal transplants. N Engl J Med. 1993 Sep 9;329(11):769–773. doi: 10.1056/NEJM199309093291105. [DOI] [PubMed] [Google Scholar]

Articles from Immunology are provided here courtesy of British Society for Immunology

RESOURCES