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Effects of energy restriction and fish oil supplementation on renal guanidino levels and antioxidant defences in aged lupus-prone B/W mice

Published online by Cambridge University Press:  08 March 2007

You Jung Kim ,
Takako Yokozawa  and
Hae Young Chung
You Jung Kim
Affiliation:
Department of Cosmetology, Pusan Women's College, Pusanjin-Gu, Pusan, Korea
Takako Yokozawa
Affiliation:
Institute of Natural Medicine, Toyama Medical and Pharmaceutical University, 2630 Sugitani, Toyama 930-0194, Japan
Hae Young Chung*
Affiliation:
Department of Pharmacy, Longevity Life Science and Technology Institutes, Aging Tissue Bank, Pusan National University, Kumjeong-Gu, Pusan, Korea
*
*Corresponding author: Dr Hae Young Chung, fax +82 51 510 2821, email hyjung@pusan.ac.kr
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Abstract

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Energy restriction (ER) and dietary fish oil (FO) are known to reduce the severity of glomerulonephritis and increase the lifespan of lupus-prone (NZB×NZW) F1 (B/W) mice. In the present study, mice were fed either ad libitum or energy-restricted (a 40 % lower energy intake than the diet ad libitum), semi-purified diets containing 5 % maize oil or 5 % fish oil supplementation. To estimate the renal damage associated with oxidative stress, the total amounts of reactive oxygen species (ROS), cyclooxygenase-derived ROS and levels of guanidino compounds were measured. Additionally, we assessed the putative action of ER and FO on several key antioxidant enzymes measured in the kidney post-mitochondrial fraction. Results showed that the age-related increase in creatinine level was significantly reduced by ER and FO in old mice. In contrast, arginine and guanidino acetic acid levels showed a decrease with age but were increased by ER and FO. The GSH:GSSG ratio showed a significant decrease with age, whereas ER and FO feeding prevented the decrease. The age-related decrease in antioxidant scavenging superoxide dismutase, catalase and glutathione peroxidase activities were all reversed by ER and FO. The moderately decreased glutathione reductase and glutathione-S-transferase activities with age were significantly increased by ER and FO. Furthermore, the increased total ROS and cyclooxygenase-derived ROS levels were effectively reduced by ER and FO. In conclusion, our data strongly indicate that ER and FO maintain antioxidant status and GSH:GSSG ratio, thereby protecting against renal deterioration from oxidative insults during ageing.

Keywords

Energy restrictionDietary fish oilGSH:GSSG ratioGuanidino compoundsAntioxidant enzymesOxidative stress
Type
Research Article
Information
British Journal of Nutrition , Volume 93 , Issue 6 , June 2005 , pp. 835 - 844
Copyright
Copyright © The Nutrition Society 2005

References

Aebi, H (1984) Catalase in vitro. Methods Enzymol 105, 121–126.CrossRefGoogle ScholarPubMed
Ali, SFLeBel, CP & Bondy, SC (1992) Reactive oxygen species formation as a biomarker of methylmercury and trimethyltin neurotoxicity. Neurotoxicology 13, 637–648.Google ScholarPubMed
Astorg, P (2004) Dietary N-6 and N-3 polyunsaturated fatty acids and prostate cancer risk: a review of epidemiological and experimental evidence. Cancer Causes Control 15, 367–386.CrossRefGoogle Scholar
Baylis, C & Schmidt, R (1996) The aging glomerulus. Semin Nephrol 16, 265–276.Google ScholarPubMed
Calder, PC (1997) n-3 polyunsaturated fatty acids and cytokine production in health and disease. Ann Nutr Metab 41, 203–234.CrossRefGoogle ScholarPubMed
Cardinali, DP, Garcia, AP, Cano, P & Esquifino, AI (2004) Melatonin role in experimental arthritis. Curr Drug Targets Immune Endocr Metabol Disord 4, 1–10.CrossRefGoogle ScholarPubMed
Chandrasekar, B & Fernandes, G (1994) Decreased pro-inflammatory cytokines and increased antioxidant enzyme gene expression by omega-3 lipids in murine lupus nephritis. Biochem Biophys Res Commun 200, 893–898.CrossRefGoogle ScholarPubMed
Chung, HY, Kim, HJ, Kim, KW, Choi, JS & Yu, BP (2002) Molecular inflammation hypothesis of aging based on the anti-aging mechanism of calorie restriction. Microsc Res Tech 59, 264–272.CrossRefGoogle ScholarPubMed
Chung, HY, Kim, HJ, Kim, JW & Yu, BP (2001) The inflammation hypothesis of aging: molecular modulation by calorie restriction. Ann N Y Acad Sci 928, 327–335.CrossRefGoogle ScholarPubMed
Clark, WF & Parbtani, A (1994) Omega-3 fatty acid supplementation in clinical and experimental lupus nephritis. Am J Kidney D, is 23, 644–647.CrossRefGoogle ScholarPubMed
Fernandes, G (1994) Dietary lipids and risk of autoimmune disease. Clin Immunol Immunopathol 72, 193–197.CrossRefGoogle ScholarPubMed
Fernandes, G, Chandrasekar, B, Luan, X & Troyer, DA (1996) Modulation of antioxidant enzymes and programmed cell death by n-3 fatty acids. Lipids 31, S91–S96.CrossRefGoogle ScholarPubMed
Guarnieri, G, Antonione, R & Biolo, G (2003) Mechanisms of malnutrition in uremia. J Ren Nutr 13, 153–157.CrossRefGoogle ScholarPubMed
Habig, WH, Pabst, MJ & Jakoby, WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249, 7130–7139.CrossRefGoogle ScholarPubMed
Higashidate, S, Maekubo, T, Saito, M, Senda, M & Hoshino, T (1984) Rapid and highly sensitive method for the determination of guanidino compounds in body fluids. Bunseki kagaku 33, 366–370.CrossRefGoogle Scholar
Hu, FB, Cho, E, Rexrode, KM, Albert, CM & Manson, JE (2003) Fish and long-chain omega-3 fatty acid intake and risk of coronary heart disease and total mortality in diabetic women. Circulation 107, 1852–1857 Epub 2003 Mar 31.CrossRefGoogle ScholarPubMed
Jolly, CA, Muthukumar, A, Avula, CP, Troyer, D & Fernandes, G (2001a) Life span is prolonged in food-restricted autoimmune-prone (NZB×NZW)F(1) mice fed a diet enriched with (n-3) fatty acids. J Nutr 131, 2753–2760.CrossRefGoogle Scholar
Jolly, CA, Muthukumar, AReddy, Avula CP & Fernandes, G (2001b) Maintenance of NF-kappaB activation in T-lymphocytes and a naive T-cell population in autoimmune-prone (NZB/NZW)F(1) mice by feeding a food-restricted diet enriched with n-3 fatty acids. Cell Immunol 213, 122–133.CrossRefGoogle Scholar
Judex, S, Wohl, GR, Wolff, RB, Leng, W, Gillis, AM & Zernicke, RF (2000) Dietary fish oil supplementation adversely affects cortical bone morphology and biomechanics in growing rabbits. Calcif Tissue Int 66, 443–448.CrossRefGoogle Scholar
Kim, HJ, Jung, KJ, Yu, BP, Cho, CG, Choi, JS & Chung, HY (2002) Modulation of redox-sensitive transcription factors by calorie restriction during aging. Mech Ageing Dev 123, 1589–1595.CrossRefGoogle ScholarPubMed
Kono, DH & Theofilopoulos, AN (2000) Genetics of systemic autoimmunity in mouse models of lupus. Int Rev Immunol 19, 367–387.CrossRefGoogle ScholarPubMed
Kubo, C, Johnson, BC, Day, NK & Good, RA (1984) Calorie source, calorie restriction, immunity and aging of (NZB/NZW)F1 Mice. J Nutr 114, 1884–1899.CrossRefGoogle ScholarPubMed
Levillain, O, Marescau, B, Possemiers, I, Al Banchaabouchi, M & De Deyn, PP (2001) Influence of 72 % injury in one kidney on several organs involved in guanidino compound metabolism: a time course study. Pflugers Arch 442, 558–569.CrossRefGoogle ScholarPubMed
Lowry, OH, Rosebrough, NJ & Farr, AL (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193, 265–275.CrossRefGoogle ScholarPubMed
McCord, JM & Fridovich, I (1988) Superoxide dismutase: the first twenty years (1968–1988). Free Radic Biol Med 5, 363–369.CrossRefGoogle ScholarPubMed
Morrow, WJ, Ohashi, Y, Hall, J, Pribnow, J, Hirose, S, Shirai, T & Levy, JA (1985) Dietary fat and immune function. Antibody responses, lymphocytes and accessory cell function in (NZB/NZW)F1 mice. J Immunol 135, 3857–3863.CrossRefGoogle Scholar
Motojima, M, Hosokawa, A, Yamato, H, Muraki, T & Yoshioka, T (2003) Uremic toxins of organic anions up-regulate PAI-1 expression by induction of NF-kappaB and free radical in proximal tubular cells. Kidney Int 63, 1671–1680.CrossRefGoogle ScholarPubMed
Muthukumar, AR, Jolly, CA, Zaman, K & Fernandes, G (2000) Calorie restriction decreases proinflammatory cytokines and polymeric Ig receptor expression in the submandibular glands of autoimmune prone (NZB×NZW)F1 mice. J Clin Immunol 20, 354–361.CrossRefGoogle Scholar
Muthukumar, A, Zaman, K, Lawrence, R, Barnes, JL & Fernandes, G (2003) Food restriction and fish oil suppress atherogenic risk factors in lupus-prone (NZB×NZW) F1 mice. J Clin Immunol 23, 23–33.CrossRefGoogle Scholar
Nohara, Y, Usui, T, Kinoshita, T & Watanabe, M (2002) Generation of superoxide anions during the reaction of guanidino compounds with methylglyoxal. Chem Pharm Bull 50, 179–184.CrossRefGoogle ScholarPubMed
Okudaira, H, Terada, E, Fukuda, K, Ito, T, Gohda, A, Nomura, T, Kudo, K, Ogita, T & Miyamoto, T (1984) Treatment of NZB/W F1 mice with NZW splenic T cells or with serum of mice experiencing the graft-versus-host reaction: suppression of ongoing anti-double-stranded (ds) DNA antibody formation and improvement of renal function. Clin Immunol Immunopathol 32, 359–367.CrossRefGoogle ScholarPubMed
Pandey, A & Katiyar, SS (1996) Inactivation of yeast glutathione reductase by O-phthalaldehyde. J Enzyme Inhib 11, 141–149.CrossRefGoogle ScholarPubMed
Patel, J, Manjappa, N, Bhat, R, Mehrotra, P, Bhaskaran, M & Singhal, PC (2003) Role of oxidative stress and heme oxygenase activity in morphine-induced glomerular epithelial cell growth. Am J Physiol Renal Physiol 285, F861–F869.CrossRefGoogle ScholarPubMed
Pey, A, Saborido, A, Blazquez, I, Delgado, J & Megias, A (2003) Effects of prolonged stanozolol treatment on antioxidant enzyme activities, oxidative stress markers, and heat shock protein HSP72 levels in rat liver. J Steroid Biochem Mol Biol 87, 269–277.CrossRefGoogle ScholarPubMed
Reddy, Avula CP, Lawrence, RA, Zaman, K & Fernandes, G (2002) Inhibition of intracellular peroxides and apoptosis of lymphocytes in lupus-prone B/W mice by dietary n-6 and n-3 lipids with calorie restriction. J Clin Immunol 22, 206–219.CrossRefGoogle Scholar
Sailaja, YR, Baskar, R & Saralakumari, D (2003) The antioxidant status during maturation of reticulocytes to erythrocytes in type 2 diabetics. Free Radic Biol Med 35, 133–139.CrossRefGoogle ScholarPubMed
Satoh, M, Hayashi, H, Watanabe, M, Ueda, K, Yamato, H, Yoshioka, T & Motojima, M (2003) Uremic toxins overload accelerates renal damage in a rat model of chronic renal failure. Nephron Exp Nephrol 95, e111–e118.CrossRefGoogle Scholar
Sethi, S (2002) Inhibition of leukocyte-endothelial interactions by oxidized omega-3 fatty acids: a novel mechanism for the anti-inflammatory effects of omega-3 fatty acids in fish oil. Redox Rep 7, 369–378.CrossRefGoogle ScholarPubMed
Shainkin, R, Berkenstadt, Y, Giat, Y & Berlyne, GM (1975) An automated technique for the analysis of plasma guanidino acids, and some findings in chronic renal disease. Clin Chim Acta 60, 45–50.CrossRefGoogle ScholarPubMed
Tappel, AL, Tappel, AA & Fraga, CG (1989) Application of simulation modeling to lipid peroxidation processes. Free Radic Biol Med 7, 361–368.CrossRefGoogle ScholarPubMed
Troyer, DA, Chandrasekar, B, Barnes, JL & Fernandes, G (1997) Calorie restriction decreases platelet-derived growth factor (PDGF)-A and thrombin receptor mRNA expression in autoimmune murine lupus nephritis. Clin Exp Immunol 108, 58–62.CrossRefGoogle ScholarPubMed
Vanholder, R (2003) Uremic toxins. Nephrologie 24, 373–376.Google ScholarPubMed