The Journal of Nutritional Biochemistry
Volume 18, Issue 8 , Pages 509-518 , August 2007

Dietary zinc restriction in rats alters antioxidant status and increases plasma F2 isoprostanes

  • Richard S. Bruno

      Affiliations

    • Department of Nutritional Sciences, University of Connecticut, Storrs, CT 06269, USA
    • Linus Pauling Institute, Oregon State University, Corvallis, OR 97331, USA
    • ,
  • Yang Song

      Affiliations

    • Department of Nutrition and Exercise Sciences, Oregon State University, Corvallis, OR 97331, USA
    • ,
  • Scott W. Leonard

      Affiliations

    • Linus Pauling Institute, Oregon State University, Corvallis, OR 97331, USA
    • ,
  • Debbie J. Mustacich

      Affiliations

    • Linus Pauling Institute, Oregon State University, Corvallis, OR 97331, USA
    • ,
  • Alan W. Taylor

      Affiliations

    • Linus Pauling Institute, Oregon State University, Corvallis, OR 97331, USA
    • ,
  • Maret G. Traber

      Affiliations

    • Linus Pauling Institute, Oregon State University, Corvallis, OR 97331, USA
    • Department of Nutrition and Exercise Sciences, Oregon State University, Corvallis, OR 97331, USA
    • ,
  • Emily Ho

      Affiliations

    • Linus Pauling Institute, Oregon State University, Corvallis, OR 97331, USA
    • Department of Nutrition and Exercise Sciences, Oregon State University, Corvallis, OR 97331, USA
    • Corresponding Author InformationCorresponding author. Department of Nutrition and Exercise Sciences, Oregon State University, Corvallis, OR 97331, USA. Tel.: +1 541 737 9559; fax: +1 541 737 6914.

Received 6 May 2006 ,Revised 25 August 2006 ,Accepted 27 September 2006.

References 

  1. Powell SR. The antioxidant properties of zinc. J Nutr. 2000;130:1447S–1454S
  2. Bray TM, Bettger WJ. The physiological role of zinc as an antioxidant. Free Radic Biol Med. 1990;8:281–291
  3. Olin KL, Shigenaga MK, Ames BN, Golub MS, Gershwin ME, Hendrickx AG, et al. Maternal dietary zinc influences DNA strand break and 8-hydroxy-2′-deoxyguanosine levels in infant rhesus monkey liver. Proc Soc Exp Biol Med. 1993;203:461–466
  4. Centers for Disease Control and Prevention (CDC) , National Center for Health Statistics (NCHS) . National Health and Nutrition Examination Survey Questionnaire (or Examination Protocol, or Laboratory Protocol). Hyattsville (MD): U.S. Department of Health and Human Services, Centers for Disease Control and Prevention; 2001–2002;[http://www.cdc.gov/nchs/about/major/nhanes/nhanes01-02.htm]
  5. Oteiza PI, Olin KL, Fraga CG, Keen CL. Zinc deficiency causes oxidative damage to proteins, lipids and DNA in rat testes. J Nutr. 1995;125:823–829
  6. Castro L, Freeman BA. Reactive oxygen species in human health and disease. Nutrition. 2001;17:161, 3–5.
  7. Taylor CG, Bettger WJ, Bray TM. Effect of dietary zinc or copper deficiency on the primary free radical defense system in rats. J Nutr. 1988;118:613–621
  8. Ho E, Quan N, Tsai YH, Lai W, Bray TM. Dietary zinc supplementation inhibits NFkappaB activation and protects against chemically induced diabetes in CD1 mice. Exp Biol Med (Maywood). 2001;226:103–111
  9. Ho E, Courtemanche C, Ames BN. Zinc deficiency induces oxidative DNA damage and increases p53 expression in human lung fibroblasts. J Nutr. 2003;133:2543–2548
  10. Ho E, Ames BN. Low intracellular zinc induces oxidative DNA damage, disrupts p53, NFkappaB, and AP1 DNA binding, and affects DNA repair in a rat glioma cell line. Proc Natl Acad Sci U S A. 2002;99:16770–16775
  11. Oteiza PI, Clegg MS, Zago MP, Keen CL. Zinc deficiency induces oxidative stress and AP-1 activation in 3T3 cells. Free Radic Biol Med. 2000;28:1091–1099
  12. Oteiza PL, Olin KL, Fraga CG, Keen CL. Oxidant defense systems in testes from zinc-deficient rats. Proc Soc Exp Biol Med. 1996;213:85–91
  13. Burke JP, Owens K, Fenton MR. Effect of a zinc-deficient diet on mitochondrial and microsomal lipid composition in TEPC-183 plasmacytoma. Biochem Med Metab Biol. 1987;37:148–156
  14. Bray TM, Kubow S, Bettger WJ. Effect of dietary zinc on endogenous free radical production in rat lung microsomes. J Nutr. 1986;116:1054–1060
  15. Reeves PG, Nielsen FH, Fahey GC. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition Ad Hoc Writing Committee on the Reformulation of the AIN-76A Rodent Diet. J Nutr. 1993;123:1939–1951
  16. Verbanac D, Milin C, Domitrovic R, Giacometti J, Pantovic R, Ciganj Z. Determination of standard zinc values in the intact tissues of mice by ICP spectrometry. Biol Trace Elem Res. 1997;57:91–96
  17. Taylor AW, Bruno RS, Frei B, Traber MG. Benefits of prolonged gradient separation for high-performance liquid chromatography–tandem mass spectrometry quantitation of plasma total 15-series F-isoprostanes. Anal Biochem. 2006;350:41–51
  18. Benzie IF, Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem. 1996;239:70–76
  19. Podda M, Weber C, Traber MG, Packer L. Simultaneous determination of tissue tocopherols, tocotrienols, ubiquinols, and ubiquinones. J Lipid Res. 1996;37:893–901
  20. Leonard SW, Bruno RS, Paterson E, Schock BC, Atkinson J, Bray TM, et al. 5-nitro-gamma-tocopherol increases in human plasma exposed to cigarette smoke in vitro and in vivo. Free Radic Biol Med. 2003;35:1560–1567
  21. Lodge JK, Traber MG, Elsner A, Brigelius-Flohe R. A rapid method for the extraction and determination of vitamin E metabolites in human urine. J Lipid Res. 2000;41:148–154
  22. Himmelfarb J, Kane J, McMonagle E, Zaltas E, Bobzin S, Boddupalli S, et al. Alpha and gamma tocopherol metabolism in healthy subjects and patients with end-stage renal disease. Kidney Int. 2003;64:978–991
  23. Leonard SW, Gumpricht E, Devereaux MW, Sokol RJ, Traber MG. Quantitation of rat liver vitamin E metabolites by LC-MS during high-dose vitamin E administration. J Lipid Res. 2005;46:1068–1075
  24. Frei B, England L, Ames BN. Ascorbate is an outstanding antioxidant in human blood plasma. Proc Natl Acad Sci U S A. 1989;86:6377–6381
  25. Bruno RS, Ramakrishnan R, Montine TJ, Bray TM, Traber MG. {alpha}-Tocopherol disappearance is faster in cigarette smokers and is inversely related to their ascorbic acid status. Am J Clin Nutr. 2005;81:95–103
  26. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193:265–275
  27. Terasawa Y, Cases SJ, Wong JS, Jamil H, Jothi S, Traber MG, et al. Apolipoprotein B-related gene expression and ultrastructural characteristics of lipoprotein secretion in mouse yolk sac during embryonic development. J Lipid Res. 1999;40:1967–1977
  28. Hambidge M. Biomarkers of trace mineral intake and status. J Nutr. 2003;133(Suppl 3):948S–955S
  29. Yin H, Porter NA, Morrow JD. Separation and identification of F(2)-isoprostane regioisomers and diastereomers by novel liquid chromatographic/mass spectrometric methods. J Chromatogr B Analyt Technol Biomed Life Sci. 2005;827:157–164
  30. tom Dieck H, Doring F, Fuchs D, Roth HP, Daniel H. Transcriptome and proteome analysis identifies the pathways that increase hepatic lipid accumulation in zinc-deficient rats. J Nutr. 2005;135:199–205
  31. Eder K, Kirchgessner M. Activities of liver microsomal fatty acid desaturases in zinc-deficient rats force-fed diets with a coconut oil/safflower oil mixture of linseed oil. Biol Trace Elem Res. 1995;48:215–229
  32. Eder K, Kirchgessner M. Zinc deficiency and the desaturation of linoleic acid in rats force-fed fat-free diets. Biol Trace Elem Res. 1996;54:173–183
  33. Kudo N, Nakagawa Y, Waku K. The effect of cadmium on the composition and metabolism of hepatic fatty acids in zinc-adequate and zinc-deficient rats. Toxicol Lett. 1990;50:203–212
  34. Kudo N, Nakagawa Y, Waku K. Effects of zinc deficiency on the fatty acid composition and metabolism in rats fed a fat-free diet. Biol Trace Elem Res. 1990;24:49–60
  35. Ho E. Zinc deficiency, DNA damage and cancer risk. J Nutr Biochem. 2004;15:572–578
  36. Brigelius-Flohe R, Traber MG. Vitamin E: function and metabolism. Faseb J. 1999;13:1145–1155
  37. Traber MG, Burton GW, Hamilton RL. Vitamin E trafficking. Ann N Y Acad Sci. 2004;1031:1–12
  38. Qian J, Morley S, Wilson K, Nava P, Atkinson J, Manor D. Intracellular trafficking of vitamin E in hepatocytes: the role of tocopherol transfer protein. J Lipid Res. 2005;46:2072–2082
  39. Birringer M, Drogan D, Brigelius-Flohe R. Tocopherols are metabolized in HepG2 cells by side chain omega-oxidation and consecutive beta-oxidation. Free Radic Biol Med. 2001;31:226–232
  40. Traber MG, Siddens LK, Leonard SW, Schock B, Gohil K, Krueger SK, et al. Alpha-tocopherol modulates Cyp3a expression, increases gamma-CEHC production, and limits tissue gamma-tocopherol accumulation in mice fed high gamma-tocopherol diets. Free Radic Biol Med. 2005;38:773–785
  41. Sontag TJ, Parker RS. Cytochrome P450 omega-hydroxylase pathway of tocopherol catabolism. Novel mechanism of regulation of vitamin E status. J Biol Chem. 2002;277:25290–25296
  42. Parker RS, Sontag TJ, Swanson JE. Cytochrome P4503A-dependent metabolism of tocopherols and inhibition by sesamin. Biochem Biophys Res Commun. 2000;277:531–534
  43. Lasker JM, Chen WB, Wolf I, Bloswick BP, Wilson PD, Powell PK. Formation of 20-hydroxyeicosatetraenoic acid, a vasoactive and natriuretic eicosanoid, in human kidney. Role of Cyp4F2 and Cyp4A11. J Biol Chem. 2000;275:4118–4126
  44. Kim SH, Keen CL. Influence of dietary carbohydrate on zinc-deficiency-induced changes in oxidative defense mechanisms and tissue oxidative damage in rats. Biol Trace Elem Res. 1999;70:81–96
  45. Gentili A. Advanced imaging of gout. Semin Musculoskelet Radiol. 2003;7:165–174
  46. Hooper DC, Scott GS, Zborek A, Mikheeva T, Kean RB, Koprowski H, et al. Uric acid, a peroxynitrite scavenger, inhibits CNS inflammation, blood-CNS barrier permeability changes, and tissue damage in a mouse model of multiple sclerosis. Faseb J. 2000;14:691–698
  47. Hooper DC, Spitsin S, Kean RB, Champion JM, Dickson GM, Chaudhry I, et al. Uric acid, a natural scavenger of peroxynitrite, in experimental allergic encephalomyelitis and multiple sclerosis. Proc Natl Acad Sci U S A. 1998;95:675–680
  48. Scott GS, Hooper DC. The role of uric acid in protection against peroxynitrite-mediated pathology. Med Hypotheses. 2001;56:95–100
  49. Polidori MC, Pratico D, Savino K, Rokach J, Stahl W, Mecocci P. Increased F2 isoprostane plasma levels in patients with congestive heart failure are correlated with antioxidant status and disease severity. J Card Fail. 2004;10:334–338
  50. Kim WK, Patterson PH. Effect of minerals on activity of microbial uricase to reduce ammonia volatilization in poultry manure. Poult Sci. 2003;82:223–231
  51. Milatovic D, VanRollins M, Li K, Montine KS, Montine TJ. Suppression of murine cerebral F2-isoprostanes and F4-neuroprostanes from excitotoxicity and innate immune response in vivo by alpha- or gamma-tocopherol. J Chromatogr B Analyt Technol Biomed Life Sci. 2005;827:88–93
  52. Mastaloudis A, Morrow JD, Hopkins DW, Devaraj S, Traber MG. Antioxidant supplementation prevents exercise-induced lipid peroxidation, but not inflammation, in ultramarathon runners. Free Radic Biol Med. 2004;36:1329–1341
  53. Leonard SW, Bruno RS, Ramakrishnan R, Bray T, Traber MG. Cigarette smoking increases human vitamin E requirements as estimated by plasma deuterium-labeled CEHC. Ann N Y Acad Sci. 2004;1031:357–360
  54. Bruno RS, Leonard SW, Li J, Bray TM, Traber MG. Lower plasma alpha-carboxyethyl-hydroxychroman after deuterium-labeled alpha-tocopherol supplementation suggests decreased vitamin E metabolism in smokers. Am J Clin Nutr. 2005;81:1052–1059
  55. Bruno RS, Leonard SW, Atkinson J, Montine TJ, Ramakrishnan R, Bray TM, et al. Faster plasma vitamin E disappearance in smokers is normalized by vitamin C supplementation. Free Radic Biol Med. 2006;40:689
  56. Noh SK, Koo SI. Feeding of a low-zinc diet lowers the tissue concentrations of alpha-tocopherol in adult rats. Biol Trace Elem Res. 2001;81:153–168
  57. Kim ES, Noh SK, Koo SI. Marginal zinc deficiency lowers the lymphatic absorption of alpha-tocopherol in rats. J Nutr. 1998;128:265–270
  58. Traber MG. Vitamin E, nuclear receptors and xenobiotic metabolism. Arch Biochem Biophys. 2004;423:6–11
  59. Fernandez MA, O'Dell BL. Effect of zinc deficiency on plasma glutathione in the rat. Proc Soc Exp Biol Med. 1983;173:564–567
  60. Mills BJ, Lindeman RD, Lang CA. Effect of zinc deficiency on blood glutathione levels. J Nutr. 1981;111:1098–1102
  61. Mills BJ, Lindeman RD, Lang CA. Differences in blood glutathione levels of tumor-implanted or zinc-deficient rats. J Nutr. 1981;111:1586–1592

☆ Financial support for this investigation was provided to E.H. (USDA2005-35200-15439, Oregon AES (OR00735), M.G.T. (NIH DK 59576) and the Environmental Health Science Center at Oregon State University (NIEHS P30 ES00210).

PII: S0955-2863(06)00226-9

doi: 10.1016/j.jnutbio.2006.09.001

The Journal of Nutritional Biochemistry
Volume 18, Issue 8 , Pages 509-518 , August 2007

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