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Aging Clinical and Experimental Research

, Volume 7, Issue 1, pp 40–48 | Cite as

Modulation of antioxidant activities and immune response by food restriction in aging Fischer-344 rats

  • D. S. Byun
  • J. T. Venkatraman
  • B. P. Yu
  • Gabriel Fernandes
Orginal Article

Abstract

Food restriction delays the loss of several cellular immune functions, retards the onset of many diseases during aging and, consequently, extends life span significantly in laboratory rodents. The present study was undertaken to determine whether the age- associated loss in immune function is linked to changes in microsomal and mitochondrial membranes of spleens in Fischer- 344 (F- 344) male rats. In this study, we determined cytosolic superoxide dismutase activity (SOD), fluidity and cholesterol content in the splenic microsomal and mitochondrial membranes, and DNA synthesis and IL- 2 production in spleen cells from young and old ad libitum-fed (AL) and food restricted (FR) rats. The results show that proliferative response to phytohemagglutinin (PHA) and concanavalin A (Con- A) was significantly higher in the spleen cells of 18- month- and 24- month- old FR rats, as compared to their age- matched AL controls. Cytosolic SOD activity in the 24- month- old AL rats decreased by 28% as compared to 6- month- old AL rats, whereas in FR old rats, the loss was only 12%, suggesting that food restriction prevents loss in cytosolic SOD activity in spleens. Our data are consistent with the notion that food restriction modulates loss in immune response of splenocytes by maintaining both cytosolic SOD activity and membrane fluidity during aging. (Aging Clin. Exp. Res. 7: 40–48, 1995)

Keywords

Aging food restriction fluidity lipid composition superoxide dismutase 

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References

  1. 1.
    Fernandes G.: Nutritional factors: Modulating effects on immune function and aging. Pharmacol. Rev. 36: 123S–129S, 1984.PubMedGoogle Scholar
  2. 2.
    Good R.A., Gajjar A.J.: Diet, immunity and longevity. In: Hutchinson M.L., Munro H.N., (Eds.), Nutrition and Aging. Academic Press, New York, 1986, pp. 235.CrossRefGoogle Scholar
  3. 3.
    Weindruch R., Walford R.: The Retardation of Aging and Disease by Dietary Restriction. Charles C.Thomas, Springfield, IL, 1988.Google Scholar
  4. 4.
    Spector A.A., Yorek M.A.: Membrane lipid composition and cellular function. J. Lipid Res. 26: 1015–1035, 1985.PubMedGoogle Scholar
  5. 5.
    Shinitzky M.: Physiology of membrane fluidity. CRC Press, Boca Raton, Florida, 1984.Google Scholar
  6. 6.
    Venkatraman J.T., Fernandes G.: Modulation of age-related alterations in membrane composition and receptor-associated immune functions by food restriction in Fischer 344 rats. Mech. Ageing Dev. 63: 227–244, 1992.CrossRefGoogle Scholar
  7. 7.
    Stubbs C.D., Smith A.D.: The modification of mammalian membrane polyunsaturated fatty acid composition in relation to membrane fluidity and function. Biochim. Biophys. Acta 779: 89–137, 1984.PubMedCrossRefGoogle Scholar
  8. 8.
    Clandinin M.T., Cheema S., Field C.J., Garg M.L., Venkatraman J.T., Clandinin T.R.: Dietary fat: The exogenous determination of membrane structure and cell function. FASEB J. 5: 2761–2769, 1991.PubMedGoogle Scholar
  9. 9.
    Yu B.P.: Cellular defense against damage from reactive oxygen species. Physiol. Rev. 74: 139–162, 1994.PubMedGoogle Scholar
  10. 10.
    Harman D.: The aging process. Proc. Natl. Acad. Sci. U.S.A. 78: 7124–7128, 1981.PubMedCrossRefGoogle Scholar
  11. 11.
    Pryor W.A.: The free-radical theory of aging revisited: A critique and a suggested disease-specific theory. In: Warner H.R., Butler R.N., Sprott R.L., Schneider E.L. (Eds.), Modern Biological Theories of Aging. Raven Press, New York, 1987, pp. 89–112.Google Scholar
  12. 12.
    Mead J.F.: Free radical mechanisms of lipid damage and consequence for cellular membranes. In: Pryor W.A. (Ed.), Free Radicals in Biology. N.Y. Academic Press, New York, 1976, Vol 1, pp. 51.CrossRefGoogle Scholar
  13. 13.
    Rivnay B., Bergaman S., Shinitzky M., Globerson A.: Correlations between membrane viscosity, serum cholesterol, lymphocytes activation and aging in man. Mech. Ageing Dev. 12: 119–126, 1980.PubMedCrossRefGoogle Scholar
  14. 14.
    Heidrich M.L., Hendricks L.C., Cook D.E.: Effect of dietary 2-mercaptoethanol on the life span, immune system, tumor incidence and lipid peroxidation damage in spleen lymphocytes of aging BC3F1 mice. Mech. Ageing Dev. 27: 341–358, 1984.CrossRefGoogle Scholar
  15. 15.
    Yu B.P.: A hypothesis regarding the extension of life by dietary restriction. Geriatrics 44: 87–90, 1989.PubMedGoogle Scholar
  16. 16.
    Sohal R.S.: The free radical hypothesis of aging: An appraisal of the current status. Aging Clin. Exp. Res. 5: 3–17, 1993.Google Scholar
  17. 17.
    Chen J.J., Yu B.P.: Alterations in mitochondrial membrane fluidity by lipid peroxidation products. Free Rad. Biol. Med. (in press).Google Scholar
  18. 18.
    Choi J.H., Yu B.P.: Brain synaptosomal aging: Free radicals and membrane fluidity. Free Rad. Biol. Med. (in press).Google Scholar
  19. 19.
    Laganiere S., Fernandes G.: Study on the lipid composition of aging Fischer-344 rat lymphoid cells: Effect of long-term caloric restriction. Lipids 26: 472–478, 1991.PubMedCrossRefGoogle Scholar
  20. 20.
    Tiwari R.K., Venkatraman J.T., Cinader B., Flory J., Wierzbicki A., Clandinin M.T.: Influence of genotype on phospholipid fatty acid composition of splenic T and B lymphocytes in MRL/MPJ-lpr mice. Immunol. Lett. 17: 151–158, 1988.PubMedCrossRefGoogle Scholar
  21. 21.
    Clandinin M.T., Hargreaves K., Venkatraman J.T., Garg M.L., Sebakova E., Thomson A.B.R.: Alteration of structural lipid composition and the biological activity of subcellular membranes by dietary fat. In: Leger C.L., Bereziat G., Colloque G. (Eds.), Biomembranes in Nutrition, INSERM, Paris, France, 1985, 163–171.Google Scholar
  22. 22.
    Fernandes G., Flescher E., Venkatraman J.T.: Modulation of cellular immunity, fatty acid composition, fluidity and Ca2+ influx by food restriction in aging rats. Age: Immunol. Infec. Dis. 2: 117–125, 1990.Google Scholar
  23. 23.
    Yu B.P., Masoro E.J., McMahan C.A.: Nutritional influences on aging of Fischer-344 rats. I. Physical, metabolic, and longevity characteristics. J. Gerontol. 40: 657–670, 1985.PubMedCrossRefGoogle Scholar
  24. 24.
    Iwai H., Fernandes G.: Immunological functions in food-restricted rats; enhanced expression of high-affinity IL-2 receptors on splenic T cells. Immunol. Lett. 23: 125–132, 1989.PubMedCrossRefGoogle Scholar
  25. 25.
    Laganiere S., Yu B.P.: Effect of chronic food restriction in aging rats. I. Liver subcellular membranes. Mech. Ageing Dev. 48: 207–219, 1989.PubMedCrossRefGoogle Scholar
  26. 26.
    McCord J.M., Fridovich I.: Superoxide dismutase: An enzymatic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244: 6049–6055, 1969.PubMedGoogle Scholar
  27. 27.
    Yu B.P., Suescun E.A., Yang S.Y.: Effect of age-related lipid peroxidation on membrane fluidity and phospholipase A2: modulation by dietary restriction. Mech. Ageing Dev. 65: 17–33, 1992.PubMedCrossRefGoogle Scholar
  28. 28.
    Rudel L.L., Morris M.D.: Determination of cholesterol using Ophtalaldehyde. J. Lipid Res. 14: 364–366, 1973.PubMedGoogle Scholar
  29. 29.
    Witting L.A., Horwitt M.K.: Effect of degree of fatty acid unsaturation on tocopherol-induced creatinuria. J. Nutr. 82: 19–33, 1964.PubMedGoogle Scholar
  30. 30.
    Thoman M.L., Weigle W.O.: The cellular and subcellular bases of immunosenescence. Adv. Immunol. 46: 221–261, 1989.PubMedCrossRefGoogle Scholar
  31. 31.
    Makinodan T., Chang M.P., Norman D.C., Li S.C.: Vulnerability of T-cell lineage to aging. In: Goidl E.A. (Ed.), Aging and immune response-cellular and humoral aspects. Marcel Dekker, New York, 1987, pp. 27.Google Scholar
  32. 32.
    Venkatraman J.T., Fernandes G.: Mechanisms of delayed autoimmune disease in B/W mice by omega-3 lipids and food restriction. In: Chandra R.K. (Ed.), Nutrition and Immunology. ARTS Biomedical Publishers and Distributors, St. John’s, Newfoundland, 1992, pp. 309–323.Google Scholar
  33. 33.
    Fernandes G., Venkatraman J.T.: Effect of food restriction on immunoregulation and aging. In: Watson R.A. (Ed.), Handbook of Nutrition in Aged. CRC Press, Vol. 2, 1993, pp. 331-346.Google Scholar
  34. 34.
    Weindruch R.: Retardation of aging by caloric restriction in mice. In: Ingram D.K., Baker III G.T., Shock N.W. (Eds.), The po- tential for nutritional modulation of aging process. Food & Nutrition Press, Inc., Trumbull, CT, 1991, pp. 109–121.Google Scholar
  35. 35.
    Fernandes G.: Modulation of immune functions and aging by n-3 fatty acids and/or calorie restriction. In: Ingram D.K., Baker G.T., Shock N.W. (Eds.), The potential for nutritional modulation of aging process. Food and Nutrition Press, Trumbull, CT, 1991, pp. 263–287.Google Scholar
  36. 36.
    Fong T.C., Makinodan T.: In situ hybridization analysis of the age-associated decline in IL-2 mRNA expressing murine T cells. Cell. Immunol. 118: 199, 1989.PubMedCrossRefGoogle Scholar
  37. 37.
    Femandes G., Venkatraman J.T., Flescher E., Laganiere S., Iwai H., Gray P.: Prevention in the decline of membrane-associated functions in immune cells during aging by food restriction. In: Fishbein L. (Ed.), Biological Effects of Dietary Restriction. Springer-Verlag, Berlin, Germany, 1991, pp. 172–182.CrossRefGoogle Scholar
  38. 38.
    Venkatraman J.T., Tiwari R.K., Cinader B., Flory J., Wierzbicki A., Clandinin M.T.: Influence of genotype on diet-induced changes in membrane phosphatidylcholine and phos- phatidylethanolamine composition of splenocytes, liver nuclear envelope and liver mitochondria. Lipids 26: 198–202, 1991.PubMedCrossRefGoogle Scholar
  39. 39.
    Yu B.P., Laganiere S., Kim J.W.: Influence of life-prolonging food restriction on membrane lipoperoxidation and antioxidant status. In: Simic G.M., Taylor K.A., Ward J.F., Von Sonntag C. (Eds.), Oxygen Radicals in Biology and Medicine. Plenum Press, New York, NY, 1989, pp. 1067–1073.Google Scholar
  40. 40.
    Semsei I., Rao G., Richardson A.: Changes in the expression of superoxide dismutase and catalase as a function of age and dietary restriction. Biochem. Biophys. Res. Commun. 164: 620–625, 1989.PubMedCrossRefGoogle Scholar
  41. 41.
    Lee D.W., Yu B.P.: Modulation of free radicals and superoxide dismutase by age and dietary restriction. Aging Clin. Exp. Res. 2: 357–362, 1990.Google Scholar
  42. 42.
    Venkatraman J.T., Fernandes G.: Influence of food restriction and aging on the binding of insulin to liver nuclei in Fischer-344 rats. Age 14: 45–51, 1991.CrossRefGoogle Scholar
  43. 43.
    Fernandes G., Venkatraman J.T.: Dietary restriction: Effect on immunological function and aging. In: Klurfeld D.M. (Ed.), Human Nutrition: A Comprehensive Treatise. Plenum Publishing Corporation, New York, NY, 1993, pp. 91–120.Google Scholar
  44. 44.
    Fernandes G., Venkatraman J.T.: Modulation of immune function during aging by dietary restriction. Age and Nutrition 3: 202–211, 1992.Google Scholar
  45. 45.
    Pahlavani M.A., Cheung H.K., Cai N-S., Richardson A.: Influence of dietary restriction and aging on gene expression in the immune system of rats. In: Goldstein A.L. (Ed.), Biomedical advances in aging. Plenum Press, New York, 1990, pp. 259.CrossRefGoogle Scholar
  46. 46.
    Provinciali M., Fabris N., Pieri C.: Improvement of natural killer cell activity by in vitro active lipids (AL 721) administration in old mice. Mech. Ageing Dev. 52: 245, 1990.PubMedCrossRefGoogle Scholar
  47. 47.
    Damen J., De Widt J., Hilkmann H., Blitterswijk W.J.V.: Effect of dietary lipids on plasma lipoproteins and fluidity of Iymphoid cell membrane in normal and leukemic mice. Biochim. Biophys. Acta 943: 166, 1988.PubMedCrossRefGoogle Scholar
  48. 48.
    Hrelia S., Bordoni A., Celadon M., Turchetto E., Biagi P.L., Rossi C.A.: Age-related changes in linolenate and α-linolenate desaturation of rat liver microsomes. Biochem. Biophys. Res. Commun. 163: 348–355, 1989.PubMedCrossRefGoogle Scholar
  49. 49.
    Huber L.A., Xu Q.B., Jurgens G., Bock E., Buhler K.: Correlation of lymphocyte lipid composition membrane microviscosity and mitogen response in the aged. Eur. J. Immunol. 21: 2761–2765, 1991.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Internal Publishing Switzerland 1995

Authors and Affiliations

  • D. S. Byun
    • 1
    • 4
  • J. T. Venkatraman
    • 1
    • 5
  • B. P. Yu
    • 2
  • Gabriel Fernandes
    • 1
    • 2
    • 3
  1. 1.Department of MedicineThe University of Texas Health Science CenterSan AntonioUSA
  2. 2.Department of MicrobiologySan AntonioUSA
  3. 3.Department of PhysiologyThe University of Texas Health Science CenterSan AntonioUSA
  4. 4.Department of Nutrition and Food ScienceCollege of Natural Science, National Fisheries, University of PusanPusanKorea
  5. 5.Nutrition ProgramState University of New York at BuffaloBuffaloUSA

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