Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-28T00:20:15.691Z Has data issue: false hasContentIssue false

Influence of very low dietary intake of marine oil on some fuctional aspects of immune cells in healthy elderly people

Published online by Cambridge University Press:  01 August 2008

Shaliha Bechoua
Affiliation:
Institut National de la Santé et de la Recherche Médicale U352, Laboratoire de Biochimie et Pharmacologie, INSA-Lyon, France
Madeleine Dubois
Affiliation:
Institut National de la Santé et de la Recherche Médicale U352, Laboratoire de Biochimie et Pharmacologie, INSA-Lyon, France
Evelyne Véricel
Affiliation:
Institut National de la Santé et de la Recherche Médicale U352, Laboratoire de Biochimie et Pharmacologie, INSA-Lyon, France
Paul Chapuy
Affiliation:
Service de Gériatrie, Hôpital des Charpennes, Villeurbanne, France
Michel Lagarde
Affiliation:
Institut National de la Santé et de la Recherche Médicale U352, Laboratoire de Biochimie et Pharmacologie, INSA-Lyon, France
Annie-France Prigent*
Affiliation:
Institut National de la Santé et de la Recherche Médicale U352, Laboratoire de Biochimie et Pharmacologie, INSA-Lyon, France
*
*Corresponding author: Dr Annie-France Prigent, fax +33 4 72 43 85 24, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Ageing is a multifactorial process involving decreased antioxidant defences and immune functions. n-3 Polyunsaturated fatty acids have been associated with human health benefits, especially against inflammatory and autoimmune diseases. However, their immunomodulatory effects were usually observed with high dosages (>2 g/d) known to increase lipid peroxidation. In contrast, very low doses, that may prevent lipid peroxidation, might affect the immune system differently. To study the latter hypothesis further, we investigated whether the supplementation of healthy elderly people with very low doses of marine oil (MO), a docosahexaenoate (DHA)- and eicosapentaenoate (EPA)-rich triacylglycerol, was able to affect lymphocyte proliferation and biochemical markers known to be altered with age. In a randomized, double-blind design, twenty healthy elderly subjects were assigned to a placebo group (600 mg sunflower oil/d) or to a group consuming 600 mg MO/d providing 150 mg DHA + 30 mg (EPA) for 6 weeks. At day 42, the proliferative responses of lymphocytes to several mitogens were significantly (P<0·01) decreased in the MO group compared with control values. This was accompanied by a slight lowering of their cytosolic cyclic nucleotide phosphodiesterase (PDE) activity, a marked and significant (P<0·05) increase of their particulate PDE activity (+56–57 %) and a slight but significant (P<0·05) increase in cyclic nucleotide intracellular levels. At the same time, the glutathione peroxidase activity was markedly and significantly (P<0·01) depressed in the MO group. None of these modifications could be seen in the placebo group. Collectively, these results demonstrate that even very low doses of n-3 fatty acids are sufficient to affect the immune responses of elderly subjects.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2003

References

Agence Française de Sécurité Sanitaire des Aliments Establissement public de l'etat, Maisons-Alfort, France.Google Scholar
Alexander-North, LS, North, JA, Kiminyo, KP, Buettner, GR & Spector, AA (1994) Polyunsaturated fatty acids increase lipid radical formation induced by oxidant stress in endothelial cells. Journal of Lipid Research 35, 17731785.CrossRefGoogle ScholarPubMed
Ayala, A & Chaudry, IH (1995) Dietary n-3 polyunsaturated fatty acid modulation of immune cell function before or after trauma. Nutrition 11, 111.Google ScholarPubMed
Bechoua, S, Dubois, M, Dominguez, Z, Goncalves, A, Némoz, G, Lagarde, M & Prigent, AF (1999) Protective effect of docosahexaenoic acid against hydrogen peroxide induced oxidative stress in human lymphocytes. Biochemical Pharmacology 57, 10211030.CrossRefGoogle ScholarPubMed
Bechoua, S, Dubois, M, Némoz, G, Lagarde, M & Prigent, AF (1998) Docosahexaenoic acid lowers phosphatidate level in human activated lymphocytes despite phospholipase D activation. Journal of Lipid Research 39, 873883.CrossRefGoogle ScholarPubMed
Beckman, KB & Ames, BN (1998) The free radical theory of aging matures. Physiological Reviews 78, 547581.CrossRefGoogle ScholarPubMed
Bellisola, G, Galassini, S, Moschini, G, Poli, G, Perona, G & Guidi, GC (1992) Selenium and glutathione peroxidase variations induced by polyunsaturated fatty acid oral supplementation in humans. Clinica Chimica Acta 205, 7585.CrossRefGoogle ScholarPubMed
Boukhchache, D & Lagarde, M (1982) Interaction between prostaglandin precursors during their oxygenation by human platelets. Biochimica et Biophysica Acta 713, 386392.CrossRefGoogle ScholarPubMed
Bradford, MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle Scholar
Burns, EA & Goodwin, JS (1997) Immunodeficiency of aging. Drugs and Aging 11, 374397.CrossRefGoogle ScholarPubMed
Calder, PC & Newsholme, EA (1992) Polyunsaturated fatty acids suppress human peripheral blood lymphocyte proliferation and interleukin-2 production. Clinical Science 82, 695700.CrossRefGoogle ScholarPubMed
Calder, PC & Newsholme, EA (1993) Influence of antioxidant vitamins on fatty acid inhibition of lymphocyte proliferation. Biochemistry and Molecular Biology International 29, 175183.Google ScholarPubMed
Calder, PC, Yaqoob, P, Thies, F, Wallace, FA & Miles, EA (2002) Fatty acids and lymphocyte functions. British Journal of Nutrition 87, 831848.CrossRefGoogle ScholarPubMed
Calzada, C, Véricel, E & Lagarde, M (1992) Lower levels of lipid peroxidation in human platelets incubated with eicosapentaenoic acid. Biochimica et Biophysica Acta 1127, 147152.CrossRefGoogle ScholarPubMed
Crosby, AJ, Wahle, KWJ & Duthie, GG (1996) Modulation of glutathione peroxidase activity in human vascular endothelial cells by fatty acids and cytokine interleukin-1β. Biochimica et Biophysica Acta 1303, 187192.CrossRefGoogle Scholar
Croset, M, Véricel, E, Rigaud, M, Hanss, M, Courpron, P, Dechavanne, M & Lagarde, M (1990) Functions and tocopherol content of blood platelets from elderly people after low intake of purified eicosapentaenoic acid. Thrombosis Research 57, 112.CrossRefGoogle ScholarPubMed
Dröge, W, Eck, H-P, Gmünder, H & Mihm, S (1991) Requirement for prooxidant and antioxidant states in T cell mediated immune responses. Relevance for the pathogenic mechanism of AIDS? Klinische Wochenschrift 69, 11191122.CrossRefGoogle Scholar
Endres, S, De Caterina, R, Schmidt, EB & Kristensen, SD (1995) n-3 Polyunsaturated fatty acids: update. European Journal of Clinical Investigation 25, 629638.CrossRefGoogle ScholarPubMed
Endres, S, Meydani, SN, Ghorbani, R, Schindler, R & Dinarello, CA (1993) Dietary supplementation with n-3 fatty acids suppresses interleukin-2 production and mononuclear cell proliferation. Journal of Leukocyte Biology 54, 599603.CrossRefGoogle ScholarPubMed
Fortin, PR, Lew, RA, Liang, MH, Wright, EA, Beckett, LA, Chalmers, TC & Sperling, RI (1995) Validation of a meta analysis: the effects of fish oil in rheumatoid arthritis. Journal of Clinical Epidemiology 48, 13791390.CrossRefGoogle ScholarPubMed
Joulain, C, Guichardant, M, Lagarde, M & Prigent, AF (1995) Influence of polyunsaturated fatty acids on lipid metabolism in human blood mononuclear cells and early biochemical events associated with lymphocyte activation. Journal of Lipid Mediators and Cell Signalling 11, 6379.CrossRefGoogle ScholarPubMed
Joulain, C, Prigent, AF, Némoz, G & Lagarde, M (1994) Increased glutathione peroxidase activity in human blood mononuclear cells upon in vitro incubation with ω-3 fatty acids. Biochemical Pharmacology 47, 13151323.CrossRefGoogle Scholar
Kariv, I, Ferguson, FG & Confer, FL (1992) Age- and strain-related differences in murine spleen cell responses to different activation signals. Cellular Immunology 140, 6780.CrossRefGoogle ScholarPubMed
Kramer, TR, Schoene, N, Douglass, LW, Judd, JT, Ballard-Barbash, R, Taylor, PR, Bhagavan, HN & Nair, PP (1991) Increased vitamin E intake restores fish-oil-induced suppressed blastogenesis of mitogen-stimulated T lymphocytes. American Journal of Clinical Nutrition 54, 896902.CrossRefGoogle ScholarPubMed
Kumar, GS, Das, UN, Kumar, KV, Madhavi, N, Das, NP & Tan, BKH (1992) Effect of n-6 and n-3 fatty acids on the proliferation of human lymphocytes and their secretion of TNF-α and IL-2 in vitro. Nutrition Research 12, 815823.CrossRefGoogle Scholar
Lemaitre, D, Véricel, E, Polette, A & Lagarde, M (1997) Effects of fatty acids on human platelet glutathione peroxidase: possible role of oxidative stress. Biochemical Pharmacology 53, 479486.CrossRefGoogle ScholarPubMed
Meskini, N, Hosni, M, Némoz, G, Lagarde, M & Prigent, AF (1992) Early increase in lymphocyte cyclic nucleotide phospho-diesterase activity upon mitogenic activation of human peripheral blood mononuclear cells. Journal of Cellular Physiology 150, 140148.CrossRefGoogle Scholar
Meskini, N, Macovschi, O, Prigent, AF, Némoz, G, Chapuy, P & Lagarde, M (1990) Decreased cyclic nucleotide phospho-diesterase activity in human peripheral blood mononuclear cells from elderly women. Clinical Science 79, 467470.CrossRefGoogle Scholar
Meskini, N, Némoz, G, Chapuy, P, Haond, P, Pageaux, JF, Véricel, E, Lagarde, M & Prigent, AF (1993) Glutathione peroxidase activity and metabolism of arachidonic acid in peripheral blood mononuclear cells from elderly subjects. Clinical Science 85, 203211.CrossRefGoogle ScholarPubMed
Meydani, SN (1996) Effect of (n-3) polyunsaturated fatty acids on cytokine production and their biologic function. Nutrition 12, Suppl., S8S14.Google ScholarPubMed
Miles, EA & Calder, PC (1998) Modulation of immune function by dietary fatty acids. Proceedings of the Nutrition Society 57, 277292.CrossRefGoogle ScholarPubMed
Mohan, IK & Das, UN (1997) Oxidant stress, anti-oxidants and essential fatty acids in essential fatty acids in systemic lupus erythematosus. Prostaglandins, Leukotrienes and Essential Fatty Acids 56, 193198.CrossRefGoogle ScholarPubMed
Muggli, RD (1989) Dietary oils increase the requirements for vitamin in human. In Health Effects of Fish and Fish Oils, pp. 201210 [Chandra, RK, editor]. St John's, Newfoundland: Arts Biomedical Publishers.Google Scholar
Murphy, MG (1990) Dietary fatty acids and membrane protein function. Journal of Nutritional Biochemistry 1, 6879.CrossRefGoogle ScholarPubMed
Nair, PP, Judd, JT, Berlin, E, Taylor, PR, Shami, S, Sainz, E & Bhagavan, HN (1993) Dietary fish oil-induced changes in the distribution of alpha-tocopherol, retinol, and beta-carotene in plasma, red blood cells, and platelets: modulation by vitamin E. American Journal of Clinical Nutrition 58, 98102.CrossRefGoogle ScholarPubMed
Paglia, DE & Valentine, WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. Journal of Laboratory and Clinical Medicine 70, 158169.Google ScholarPubMed
Peterson, LD, Thies, F, Sanderson, P, Newsholme, EA & Calder, PC (1998) Low level of eicosapentaenoic and docosahexaenoic acids mimic the effects of fish oil upon rat lymphocytes. Life Sciences 62, 22092217.CrossRefGoogle ScholarPubMed
Rose, DP (1997) Effects of dietary fatty acids on breast and prostate cancers: evidence from in vitro experiments and animal studies. American Journal of Clinical Nutrition 66, Suppl., 1513S1522S.CrossRefGoogle ScholarPubMed
Simopoulos, PA (1991) Omega-3 fatty acids in health and disease and in growth and development. American Journal of Clinical Nutrition 54, 438463.CrossRefGoogle ScholarPubMed
Skalhegg, BS, Landmark, BF, Doskeland, SO, Hansson, V, Lea, T & Jahnsen, T (1992) Cyclic AMP-dependent protein kinase type I mediates the inhibitory effects of 3′,5′-cyclic adenosine monophosphate on cell replication in human T lymphocytes. Journal of Biological Chemistry 267, 1570715714.CrossRefGoogle Scholar
Solana, R, Villanueva, JL, Pena, J & De la Fuente, M (1991) Cell mediated immunity in ageing. Comparative Biochemistry and Physiology 99A, 14.Google Scholar
Thies, F, Nebe-von-Caron, G, Powell, JR, Yaqoob, P, Newsholme, EA & Calder, PC (2001) Dietary supplementation with γ-linolenic acid or fish oil decreases T lymphocyte proliferation in healthy older humans. Journal of Nutrition 131, 19181927.CrossRefGoogle ScholarPubMed
Tian, L, Cai, Q & Wei, H (1998) Alterations of antioxidant enzymes and oxidative damage to macromolecules in different organs of rats during aging. Free Radical in Biology and Medicine 24, 14771484.CrossRefGoogle ScholarPubMed
Véricel, E, Calzada, C, Chapuy, P & Lagarde, M (1999) The influence of low intake of n-3 fatty acids on platelets in elderly people. Atherosclerosis 147, 187192.CrossRefGoogle ScholarPubMed