Advertisement

Role of Nutrients in the Cause and Prevention of Oxygen Radical Pathology

  • Harold H. Draper
  • William J. Bettger
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 366)

Abstract

Nutrients function in both the generation and catabolism of oxygen radicals, i.e., as oxidants and antioxidants. Experimental animals fed large excesses of prooxidant nutrients, such as polyunsaturated fatty acids and iron, develop pathologies that have been firmly linked to the formation of toxic concentrations of oxygen radicals in the tissues. Similar pathologies have been demonstrated to occur as a result of experimental deficiencies of some antioxidant nutrients, notably vitamin E and selenium. Clinical diseases resulting from dietary deficiencies of these nutrients also have been well documented in farm animals. There is evidence that pharmacological intakes of some antioxidants may reduce the risk of developing some clinical diseases associated with oxygen radical pathology in human subjects consuming a normal diet and ameliorate the tissue damage associated with others. It remains unclear, however, whether oxygen radical pathology occurs in humans as a result of inadequate or excessive intakes of nutrients from the general food supply.

Keywords

Lipid Peroxidation Zinc Deficiency Dietary Vitamin Sulfur Amino Acid Keshan Disease 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    K. Karlsson, J. Sandström, A. Edlund, T. Edlund, and S.L. Marklund, Pharmacokinetics of extracellular-superoxide dismutase in the vascular system, Free Rad. Biol. Med. 14:185 (1993).PubMedGoogle Scholar
  2. 2.
    T. Adachi, H. Ohta, H. Yamada, A. Futenma, K. Kato, and K. Hirano, Quantitative analysis of extracellular-superoxide dismutase in serum and urine by ELISA with monoclonal antibody, Clin. Chim. Acta 212:89 (1992).PubMedGoogle Scholar
  3. 3.
    D.A. Peterson and J.W. Eaton, Electron transfer facilitated by superoxide dismutase: a model for membrane redox systems?, Biochem. Biophys. Res. Commun. 165:164 (1989).PubMedGoogle Scholar
  4. 4.
    M.B. Yim, P.B. Chock, and E.R. Stadtman, Enzyme function of copper, zinc superoxide dismutase as a free radical generator,. J. Biol. Chem. 268:4099 (1993).PubMedGoogle Scholar
  5. 5.
    B. Halliwell and J.M.C. Gutteridge, “Free Radicals in Biology and Medicine” (2nd ed.), Clarendon Press, Oxford (1989).Google Scholar
  6. 6.
    D.R. Rosen, T. Siddique, D. Patterson, D.A. Figlewicz, P. Sapp, A. Hentati, D. Donaldson, J. Goto, J.P. O’Regan, H.-X. Deng, Z. Rahmani, A. Krizus, D. McKenna-Yasek, A. Cayabyab, S.M. Gaston, R. Berger, R.E. Tanzi, J.J. Halperin, B. Herzfeldt, R. Van den Bergh, W.-Y. Hung, T. Bird, G. Deng, D.W. Mulder, C. Smyth, N.G. Laing, E. Soriano, M.A. Pericak-Vance, J. Haines, G.A. Rouleau, J.S. Gusella, H.R. Horvitz, and R.H. Brown, Jr. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis, Nature 362:59 (1993).PubMedGoogle Scholar
  7. 7.
    S.I. Liochev and I. Fridovich, The role of O2•— in the production of HO• in vitro and in vivo, Free Rad. Biol. Med. 16:29 (1994).PubMedGoogle Scholar
  8. 8.
    J.S. Stamler, D.J. Single, and J. Loscalzo, Biochemistry of nitric oxide and its redoxactivated forms, Science 258:1898 (1992).PubMedGoogle Scholar
  9. 9.
    G. Yang, T.E.G. Candy, M. Boaro, H.E. Wilkin, P. Jones, N.B. Nazhat, R.A. Saadalla-Nazhat, and D.R. Blake, Free radical yields from the homolysis of peroxynitrous acid, Free Rad. Biol. Med. 12:327 (1992).PubMedGoogle Scholar
  10. 10.
    S.A. Lipton, Y.-B. Choi, Z.-H. Pan, S.Z. Lei, H.-S.V. Chen, N.J. Sucher, J. Loscaizo, D.J. Singel, and J.S. Stamler, A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds, Nature 364: 626 (1993).PubMedGoogle Scholar
  11. 11.
    Y. Henry, M. Lepoivre, J.-C. Drapier, C. Ducrocq, J.-L. Boucher, and A. Guissani, EPR characterization of molecular targets for NO in mammalian cells and organelles, FASEB J. 7:1124 (1993).PubMedGoogle Scholar
  12. 12.
    Y. Rayssiguier, E. Gueux, L. Bussiere, and A. Mazur, Copper deficiency increases the susceptibility of lipoproteins and tissues to peroxidation in rats, J. Nutr. 123:1343 (1993).PubMedGoogle Scholar
  13. 13.
    M. Fields, J. Ferretti, J.C. Smith, and S. Reiser, Interaction between dietary carbohydrate and copper nutriture on lipid peroxidation in rat tissues, Biol. Trace Elem. Res. 6:379 (1984).Google Scholar
  14. 14.
    M. Fields, C.G. Lewis, M. Lure, and W.E. Antholine, The influence of gender on developing copper deficiency and on free radical generation of rats fed a fructose diet, Metabolism 41:989 (1992).PubMedGoogle Scholar
  15. 15.
    S.K. Nelson, C-J. Huang, M.M. Mathias, and K.G.D. Allen, Copper-marginal and copper-deficient diets decrease aortic prostacyclin production and copper-dependent superoxide dismutase activity, and increase aortic lipid peroxidation in rats, J. Nutr. 122:2101 (1992).PubMedGoogle Scholar
  16. 16.
    J.R. Prohaska, Biochemical changes in copper deficiency, J. Nutr. Biochem. 1:453 (1990).Google Scholar
  17. 17.
    R.G. Allen, Oxygen-reactive species and antioxidant responses during development: the metabolic paradox of cellular differentiation, Proc. Soc. Exp. Biol. Med. 196:117 (1991).PubMedGoogle Scholar
  18. 18.
    A.S. Prasad, A. Miele, Jr., Z. Farid, H.H. Sandstead, A.R. Schubert, and W.J. Darby, Biochemical studies on dwarfism, hypogonadism and anemia, Arch. Intern. Med. 111:407 (1963).PubMedGoogle Scholar
  19. 19.
    R.A. DiSilvestro and G.P. Carlson, Effects of mild zinc deficiency, plus or minus acute phase response, on CC14 hepatotoxicity, Free Rad. Biol. Med. 16:57 (1994).PubMedGoogle Scholar
  20. 20.
    J.D. Hammermueller, T.M. Bray, and W.J. Bettger, Effect of zinc and copper deficiency on microsomal NADPH-dependent active oxygen generation in rat lung and liver J. Nutr. 117:894 (1987).PubMedGoogle Scholar
  21. 21.
    J.F. Sullivan, M.M. Jetton, H.K. Hahn, and R.E. Burch, Enhanced lipid peroxidation in liver microsomes of zinc-deficient rats, Am. J. Clin. Nutr. 33:51 (1980).PubMedGoogle Scholar
  22. 22.
    T.M. Bray and W.J. Bettger, The physiological role of zinc as an antioxidant, Free Rad. Biol. Med. 8:281 (1990).PubMedGoogle Scholar
  23. 23.
    W.J. Bettger, and B.L. O’Dell, Physiological roles of zinc in the plasma membrane of mammalian cells, J. Nutr. Biochem. 4:194 (1993).Google Scholar
  24. 24.
    S. Zidenberg-Cherr, C.L. Keen, B. Lönnerdal, and L.S. Hurley, Superoxide dismutase activity and lipid peroxidation in the rat: developmental correlations affected by manganese deficiency,. J. Nutr. 113:2498 (1983).PubMedGoogle Scholar
  25. 25.
    K.H. Thompson, D.V. Godin, and M. Lee, Tissue antioxidant status in streptozotocin-induced diabetes in rats. Effects of dietary manganese deficiency, Biol. Trace Elem. Res. 35:213 (1992).PubMedGoogle Scholar
  26. 26.
    K.H. Thompson and M. Lee, Effects of manganese and vitamin E deficiencies on antioxidant enzymes in streptozotocin-diabetic rats, J. Nutr. Biochem. 4:476 (1993).Google Scholar
  27. 27.
    S. Samman, Dietary versus cellular zinc: the antioxidant paradox, Free Rad. Biol. Med. 14:95 (1993).PubMedGoogle Scholar
  28. 28.
    K.T. Tamai, E.B. Gralla, L.M. Ellerby, J.S. Valentine, and D.J. Thiele, Yeast and mammalian metallothioneins functionally substitute for yeast copper-zinc superoxide dismutase, Proc. Natl. Acad. Sci. USA 90:8013 (1993).PubMedGoogle Scholar
  29. 29.
    M. Sato and I. Bremner, Oxygen free radicals and metallothionein, Free Rad. Biol. Med. 14:325 (1993).PubMedGoogle Scholar
  30. 30.
    T.C. Stadtman, Specific occurrence of selenium in enzymes and amino acid tRNAs, FASEB J. 1:375 (1987).PubMedGoogle Scholar
  31. 31.
    F.-F. Chu, J.H. Doroshow, and R.S. Esworthy, Expression, characterization and tissue distribution of a new cellular selenium-dependent glutathione peroxidase, GSHPx-GI, J. Biol. Chem. 268:2571 (1993).PubMedGoogle Scholar
  32. 32.
    R.A. Sunde, J.A. Dyer, T.V. Moran, J.K. Evenson, and M. Sugimoto, Phospholipid hydroperoxide glutathione peroxidase: full-length pig blastocyst cDNA sequence and regulation by selenium status, Biochem. Biophys. Res. Commun. 193:905 (1993).PubMedGoogle Scholar
  33. 33.
    J.G. Bergan and H.H. Draper, Absorption and metabolism of 1-14C-hydroxy octadecadienoate in the rat, Lipids 5:983 (1970).Google Scholar
  34. 34.
    G. Yang, J. Chen, Z. Wen, K. Ge, L. Zhu, X. Chen, and X. Chen, The Role of selenium in Keshan disease, Adv. Nutr. Res. 6:203 (1984).PubMedGoogle Scholar
  35. 35.
    C.D. Thompson and M.F. Jones, Selenium in human health and disease with emphasis on those aspects peculiar to New Zealand, Amer. J. Clin. Nutr. 33:303 (1980).Google Scholar
  36. 36.
    G. Yang, S. Wang, R. Zhou, and S. Sun, Endemic selenium intoxication of humans in China, Amer. J. Clin. Nutr. 37:872 (1983).PubMedGoogle Scholar
  37. 37.
    J.N. Thompson, P. Erdody, and D.C. Smith, Selenium content of food consumed by Canadians,. J. Nutr. 105:214 (1975).Google Scholar
  38. 38.
    A.V. Kozlov, D.Y. Yegorow, Y.A. Vladimirov, and O.A. Azizova, Intracellular free iron in liver tissue and liver homogenate: studies with electron paramagnetic resonance on the formation of paramagnetic complexes with desferal and nitric oxide, Free Rad. Biol. Med. 13:9 (1992).PubMedGoogle Scholar
  39. 39.
    H.H. Draper, E.J. Squires, H. Mahmoodi, J. Wu, and M. Hadley, A comparative evaluation of thiobarbituric acid methods for the determination of malondialdehyde in biological materials, Free Rad. Biol. Med. 15:353 (1993).PubMedGoogle Scholar
  40. 40.
    L.A. Witting, Lipid peroxidation in vivo, J. Amer. Oil Chem. 42:908 (1965).Google Scholar
  41. 41.
    T. Miyazawa, T. Suzuki, and K. Fujimoto, Age-dependent accumulation of phosphatidyl hydroperoxide in the brain and liver of the rat, Lipids 28:789 (1993).PubMedGoogle Scholar
  42. 42.
    H.H. Draper, Antioxidant role of vitamin E, in: Atmospheric Oxidation and Antioxidants, Vol. III, G. Scott, ed., Elsevier, Amsterdam (1993).Google Scholar
  43. 43.
    W.A. Pryor and S.S. Godber, Noninvasive measures of oxidative stress status in humans, Free Rad. Biol. Med. 10:177 (1991).PubMedGoogle Scholar
  44. 44.
    K.N. Jeejeebhoy, In vivo breath alkane as an index of lipid peroxidation, Free Rad. Biol. Med. 10:191 (1991).PubMedGoogle Scholar
  45. 45.
    L.A. Piché, P.D. Cole, M. Hadley, R. van den Bergh, and H.H. Draper, Identification of N-ε-(2-propenal)lysine as the main form of malondialdehyde in food digesta, Carcinogenesis 9:473 (1988).PubMedGoogle Scholar
  46. 46.
    S.N. Danakoti and H.H. Draper, Response of urinary malondialdehyde to factors that stimulate lipid peroxidation in vivo, Lipids 22:643 (1987).Google Scholar
  47. 47.
    K.J.A. Davies and A.L. Goldberg, Proteins damaged by oxygen radicals are rapidly degraded in extracts of red blood cells, J. Biol. Chem. 262:8227 (1987).PubMedGoogle Scholar
  48. 48.
    H.H. Draper and M. Hadley, A review of recent studies on the metabolism of exogenous and endogenous malondialdehyde, Xenobiotics 20:901 (1990).Google Scholar
  49. 49.
    S. Agarwal and H.H. Draper, Isolation of a malondialdehyde-deoxyguanosine adduct from rat liver DNA, Free Rad. Biol. Med. 13:695 (1992).PubMedGoogle Scholar
  50. 50.
    R. Adelman, R.L. Saul, and B.N. Ames, Oxidative damage to DNA: relation to species metabolic rate and life span, Proc. Natl. Acad. Sci. USA 85:2706 (1988).PubMedGoogle Scholar
  51. 51.
    M.E. Haberland, D. Fong, and L. Cheng, Malondialdehyde, modified lipoproteins, and atherosclerosis, Europ. Heart. J. 11 (Suppl. E): 100 (1990).Google Scholar
  52. 52.
    H. Esterbauer, Cytotoxicity and genotoxicity of lipid-oxidation products, Amer. J. Clin. Nutr. 57:(Suppl):7795 (1993).Google Scholar
  53. 53.
    C.C. Seltzer, Letter to the editor, New Engl. J. Med. 323:1705 (1990).Google Scholar
  54. 54.
    J.D. Morrow, K.E. Hill, R.F. Burk, T.M. Nammour, K.F. Badr, and L.J. Roberts, II, A series of prostaglandin F2-like compounds are produced in vivo in humans by a noncyclooxygenase, free radical-catalyzed mechanism, Proc. Natl. Acad. Sci. USA 87:9383 (1990).PubMedGoogle Scholar
  55. 55.
    M. Meydani, F. Natiello, B. Goldin, N. Free, M. Woods, E. Schaefer, J.B. Blumberg, and S.L. Gorbach, Effect of long-term fish oil supplementation on vitamin E status and lipid peroxidation in women,. J. Nutr. 121:484 (1991).PubMedGoogle Scholar
  56. 56.
    H.J. Kayden and M.G. Traber, Absorption, lipoprotein transport, and regulation of plasma concentrations of vitamin E in humans,. J. Lipid Res. 34:343 (1993).PubMedGoogle Scholar
  57. 57.
    M.K. Horwitt, Vitamin E and lipid metabolism in man, Amer. J. Clin.Nutr. 8:451 (1960).PubMedGoogle Scholar
  58. 58.
    M.J. Stampfer, C.H. Hennekens, J.E. Manson, G.A. Colditz, B. Rosner, and W.C. Willett, Vitamin E consumption and the risk of coronary disease in women, New Engl. J. Med. 328:1444 (1993).PubMedGoogle Scholar
  59. 59.
    D.J. Hunter, J.E. Manson, G.A. Colditz, M.J. Stampfer, B. Rosner, C.H. Hennekens, F.E. Speizer, and W.C. Willett, A prospective study of the intake of vitamins C, E and A and the risk of breast cancer, New Engl. J. Med. 329: 234 (1993).PubMedGoogle Scholar
  60. 60.
    E.B. Rim, M.J. Stampfer, A. Ascherio, E. Giovannucci, G.A. Colditz, and W.C. Willett, Vitamin E consumption and the risk of coronary heart disease in men, New Engl J. Med. 328:1450 (1993).Google Scholar
  61. 61.
    H.H. Draper, Nutrient interrelationships, in: “Vitamin E. A Comprehensive Treatise”, L.J. Machlin, ed., Marceli Dekker, New York (1980).Google Scholar
  62. 62.
    J.P. Kehrer, Free radicals as mediators of tissue inury and disease, Critical Rev. Toxicol. 23:21 (1993).Google Scholar
  63. 63.
    C.A. Rice-Evans and A.T. Diplock, Current status of antioxidant therapy, Free Rad. Biol. Med. 15:77 (1993).PubMedGoogle Scholar
  64. 64.
    T. Tihan, P. Chiba, O. Krupicka, M. Fritzer, R. Seitelbergen, and M.M. Muller, Serum lipid peroxide levels in the course of coronary by-pass surgery, Eur. J. Clin. Chem. Clin. Biochem. 30:205 (1992).PubMedGoogle Scholar
  65. 65.
    Z.W. Weitz, A.J. Birnbaum, P.A. Sobolka, E.J. Starling, and J.L. Skosey, High breath pentane concentrations during acute myocardial infarction, Lancet 337:933 (1991).PubMedGoogle Scholar
  66. 66.
    P.A. Sobolka, M.D. Brottman, Z. Weitz, A.J. Birnbaum, J. Skosey, and E.J. Zarling, Elevated breath pentane in heart failure reduced by free radical scavenger, Free Rad. Biol. Med. 14:643 (1993).Google Scholar
  67. 67.
    D.L. Gee and R.E. Litov, Lipid peroxidation and antioxidant status in burn patients, Amer. J. Clin. Nutr. 31:P–31 (1991).Google Scholar
  68. 68.
    Y.-K. Youn, C. Lalonde, and R. Demling, Oxidants and the pathophysiology of burn and smoke inhalation injury, Free Rad. Biol. Med. 12:409 (1992).Google Scholar
  69. 69.
    H.M. Berger, J.H.N. Lindeman, D. van Zoeren-Grobben, E. Houdkamp, J. Schrijver, and H.H. Kanhai, Iron overload, free radical damage, and rhesus haemolytic disease, Lancet 335:933 (1990).PubMedGoogle Scholar
  70. 70.
    I.S. Young, T.G. Trouton, J.J. Forney, D. McMaster, M.E. Callender, and E. Trimble, Antioxidant status and lipid peroxidation in hereditary haemochromatosis, Free Rad. Biol. Med. 16:393 (1994).PubMedGoogle Scholar
  71. 71.
    H.H. Draper, L. Polensek, M. Hadley, and L.G. McGirr, Urinary malondialdehyde as an indicator of lipid peroxidation in the diet and in the tissues, Lipids 19:836 (1984).PubMedGoogle Scholar
  72. 72.
    G. Paolisse, A. D’Amote, D. Giuliano, A. Ceriello, M. Varrichio, and F. D’Onofrio, Pharmacological doses of vitamin E improve insulin action in healthy subjects and non-insulin-dependent diabetic patients, Amer. J. Clin. Nutr. 57:650 (1993).Google Scholar
  73. 73.
    A.B. Baouali, H. Aube, V. Maupoil, B. Blettery, and L. Rochette, Plasma lipid peroxidation in critically ill patients: importance of mechanical ventilation, Free Rad. Biol. Med. 16:223 (1994).PubMedGoogle Scholar
  74. 74.
    W.A. Pryor, Can vitamin E protect humans against the pathological effects of ozone in smog?, Amer. J. Clin. Nutr. 53:702 (1991).PubMedGoogle Scholar
  75. 75.
    C.K. Chow, C.G. Plopper, and D.L. Dungworth, Influence of dietary vitamin E on the lungs of ozone-exposed rats, Envir. Res. 20:309 (1977).Google Scholar
  76. 76.
    S. Owen, D. Pearson, V. Suarez-Mendez, R. O’Driscoll, and A. Woodcock, Evidence of free radical action in asthma, New Engl. J. Med. 325:586 (1991).PubMedGoogle Scholar
  77. 77.
    M.M. Mathews-Roth, Beta carotene therapy for erythropoietic protoporphyria and other photosensitivity diseases, Biochimie 68:875 (1986).PubMedGoogle Scholar
  78. 78.
    G.W. Burton and K.V. Ingoici, Beta carotene: an unusual type of lipid antioxidant, Science 224: 569 (1984).PubMedGoogle Scholar
  79. 79.
    B.A. Underwood, The diet-cancer conundrum, Public Health Rev. 14:191 (1986).PubMedGoogle Scholar
  80. 80.
    J.A. Olson, Carotenoids, vitamin A and cancer, J. Nutr. 116:1127 (1986).PubMedGoogle Scholar
  81. 81.
    C. La Vecchia, S. Franceschi, A. Decarli, A. Gentile, M. Fasoli, S. Pampailona, and G. Tognoni, Dietary vitamin A and the risk of invasive cervical cancer, Int. J. Cancer 34:319 (1984).PubMedGoogle Scholar
  82. 82.
    K. Katsouyami, W. Willett, D. Trichopoulos, P. Boyle, A. Trichopoulu, S. Vasilaros, J. Papadiamantis, and B. MacMahon, Risk of breast cancer among Greek women in relation to nutrient intake, Cancer 61:181 (1988).Google Scholar
  83. 83.
    K. Gottlieb, E.J. Zarling, S. Mobarhan, P. Bowen, and S. Sugerman, β-carotene decreases markers of lipid peroxidation in healthy volunteers, Nutr. Cancer 19:207 (1993).PubMedGoogle Scholar
  84. 84.
    J.M.W. Slack, We have a morphogen!, Nature 327:553 (1987).PubMedGoogle Scholar
  85. 85.
    M.B. Sporn and A.B. Roberts, Role of retinoids in differentiation and carcinogenesis, Cancer Res. 43:3034 (1983).PubMedGoogle Scholar
  86. 86.
    J. Brockes, We may not have a morphogen, Nature 350:15 (1991).PubMedGoogle Scholar
  87. 87.
    G. Kolata, Does vitamin A prevent cancer?, Science 233:1161 (1984).Google Scholar
  88. 88.
    J.C. Bauernfeind, “The Safe Use of Vitamin A”, International Vitamin A Consultative Group, The Nutrition Foundation, Washington, D.C. (1980).Google Scholar
  89. 89.
    F.W. Rosa, A.L. Wilk, and F.O. Kelsey, Teratogen update: vitamin A congeners, Teratology 33:355 (1986).PubMedGoogle Scholar
  90. 90.
    R.C. Rose and A.M. Bode, Biology of free radical scavengers: an evaluation of ascorbate, FASEB J. 7:1135 (1993).PubMedGoogle Scholar
  91. 91.
    B. Frei, R. Stocker, and B.N. Ames, Antioxidant defenses and lipid peroxidation in human blood plasma, Proc. Natl. Acad. Sci. USA 85:9748 (1988).PubMedGoogle Scholar
  92. 92.
    A.B. Kallner, D. Harbmann, and D.H. Hornig, On the requirements of ascorbic acid in man: steady state turnover and body pool in smokers, Amer. J. Clin. Nutr. 34:1347 (1981).PubMedGoogle Scholar
  93. 93.
    A.C. Chan, K. Tran, T. Raynor, P.R. Ganz, and C.K. Chow, Regeneration of vitamin E in human platelets,. J. Biol. Chenu 266:17290 (1991).Google Scholar
  94. 94.
    G.W. Burton, U. Wronska, L. Stone, D.O. Foster, and K.U. Ingold, Biokinetics of dietary RRR-a-tocopherol in the male guinea pig at three dietary levels of vitamin C and two levels of vitamin E. Evidence that vitamin C does not “spare” vitamin E in vivo, Lipids 25:199 (1990).PubMedGoogle Scholar
  95. 95.
    L. Chen, An increase in vitamin E requirement induced by high supplementation of vitamin C in rats, Amer. J. Clin. Nutr. 34:1036 (1981).PubMedGoogle Scholar
  96. 96.
    W.A. Behrens and R. Madère, Ascorbic and dehydroascorbic acid status in rats fed diets varying in vitamin E levels, intern. J. Vit. Nutr. Res. 59:360 (1989).Google Scholar
  97. 97.
    S. England and S. Seifter, The biochemical functions of ascorbic acid, Ann. Rev. Nutr. 6:365 (1986).Google Scholar
  98. 98.
    T.M. Bray and C.G. Taylor, Enhancement of tissue glutathione for antioxidant and immune functions in malnutrition, Biochem. Pharmacol. (in press).Google Scholar
  99. 99.
    C. Huang and M. Fwu, Degree of protein deficiency affects the extent of depression of the antioxidative enzyme activities and the enhancement of tissue lipid peroxidation in rats, J. Nutr. 123:803 (1993).PubMedGoogle Scholar
  100. 100.
    C.C. Winterbourne, Superoxide as an intracellular radical sink, Free Rad. Biol. Med. 14:85 (1993).Google Scholar
  101. 101.
    T.M. Bray and C.G. Taylor, Tissue glutathione, nutrition and oxidative stress, Can. J. Physiol. Pharmacol. 71:746 (1993).PubMedGoogle Scholar
  102. 102.
    M.G.L. Hertog, E.J.M. Feskens, P.C.H. Hollman, M.B. Katan and D. Kromhout, Dietary antioxidant flavanoids and risk of coronary heart disease: the Zutphen elderlystudy, Lancet 342:1007 (1993).PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1994

Authors and Affiliations

  • Harold H. Draper
    • 1
  • William J. Bettger
    • 1
  1. 1.Department of Nutritional ScienceesUniversity of GuelphGuelphCanada

Personalised recommendations