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Effect of dietary supplementation with carotenoids on xenobiotic metabolizing enzymes in the liver, lung, kidney and small intestine of the rat

Published online by Cambridge University Press:  09 March 2007

Christopher Jewell  and
Nora M. O'Brien
Christopher Jewell
Affiliation:
Department of Nutrition National Food Biotechnology Centre, University College, Cork, Ireland
Nora M. O'Brien*
Affiliation:
Department of Nutrition National Food Biotechnology Centre, University College, Cork, Ireland
*
*Corresponding author: Dr Nora O'Brien, fax + 353 21 270244, email [email protected]
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Abstract

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The effect of 16 d intake of 300 mg carotenoids/kg diet (β-carotene (βC), bixin (BX), lycopene (LY), lutein (LU), canthaxanthin (CX) or astaxanthin (AX)) on xenobiotic metabolizing enzymes in the liver, lung, kidney and small intestine of male Wistar rats was assessed. A control group received the basal diet (AIN-76) without carotenoids and a positive control group for enzyme induction received 3-methylcholanthrene (3-MC) at 666 mg/kg diet. Cytochrome P450 activity was assessed using the substrates ethoxyresorufin for P450 1A1, methoxyresorufin for P450 1A2, pentoxyresorufin for P450 2B1/2 and benzyloxyresorufin for P450 types 1A1/2, 2B1/2 and 3A. Glutathione-S-transferase (EC 2.5.1.18) and reduced glutathione status were assessed. Carotenoid uptake by the tissues was also determined. 3-MC and the carotenoids BX, CX and AX led to significant increases compared with control in liver, lung and kidney ethoxyresorufin-O-deethylation. Methoxyresorufin-O-demethylation activity was significantly increased in liver and lung by BX, CX and AX but only CX and AX significantly increased activity in kidney. Pentoxyresorufin-O-depentylation and benzyloxyresorufin-O-dearylation increased in liver of 3-MC-, BX-, CX- and AX-treated rats, but to a much lesser degree than for the other two substrates. Benzyloxyresorufin-O-dearylation in lung was significantly decreased by all carotenoids. Activities of any of the measured enzymes in the small intestine were undetectable in all treatment groups except the 3-MC group. Glutathione status was unaffected by any of the treatments. This is the first study identifying the carotenoids BX, CX and AX as inducers of rat lung and kidney xenobiotic metabolizing enzymes.

Keywords

Cytochrome P450Enzyme inductionCarotenoids
Type
Research Article
Information
British Journal of Nutrition , Volume 81 , Issue 3 , March 1999 , pp. 235 - 242
Copyright
Copyright © The Nutrition Society 1999

References

Alam, BS, Alam, SQ, Bendich, A & Shapiro, SS (1989) Effect of dietary lipids on hepatic and plasma beta-carotene and vitamin A levels in rats fed beta-carotene. Nutrition and Cancer 12, 57–60.CrossRefGoogle ScholarPubMed
Alam, BS, Brown, LR & Alam, SQ (1990) Influence of dietary fats and vitamin E on plasma and hepatic vitamin A and beta-carotene levels in rats fed excess beta-carotene. Nutrition and Cancer 14, 111–116.CrossRefGoogle ScholarPubMed
American Institute of Nutrition (1977) Report of the American Institute of Nutrition ad hoc committee on standards for nutritional studies. American Journal of Nutrition 107, 1340–1348.CrossRefGoogle Scholar
Ash, M & Ash, I (1995) Handbook of Food Additives. Aldershot: Gower Publishing Limited.Google Scholar
Astorg, P (1988) Testing diets low in alpha-linolenic acid in growing, gestating and lactating female rats. Nutrition Reports International 38, 823–831.Google Scholar
Astorg, P, Gradelet, S, Leclerc, J, Canivenc, MC & Siess, MH (1994) Effects of b-carotene and canthaxanthin on liver xenobiotic-metabolizing enzymes in the rat. Food and Chemical Toxicology 32, 735–742.CrossRefGoogle Scholar
Astorg, P, Gradelet, S, Leclerc, J & Siess, MH (1997) Effects of provitamin A or non-provitamin A carotenoids on liver xenobiotic-metabolizing enzymes in mice. Nutrition and Cancer 27, 245–249.CrossRefGoogle ScholarPubMed
Batieha, AM, Armenian, HK, Norkus, EP, Morris, JS, Spate, VE & Comstock, GW (1993) Serum micronutrients and the subsequent risk of cervical cancer in a population-based nested case–control study. Cancer Epidemiology, Biomarkers and Prevention 2, 335–339.Google Scholar
Blakely, SR, Grundel, E, Jenkins, HY & Mitchell, GV (1990) Alterations in b-carotene and vitamin E status in rats fed b-carotene and excess vitamin A. Nutrition Research 10, 1035–1044.CrossRefGoogle Scholar
Burke, MD, Thompson, S, Elcombe, CR, Halpert, J, Haaparanta, T & Mayer, RT (1985) Ethoxy- pentoxy- and benzyloxyphenoxazones and homologues: a series of substrates to distinguish between different induced cytochrome P450. Biochemical Pharmacology 34, 3337–3345.CrossRefGoogle Scholar
Cotgreave, IA & Moldéus, P (1986) Methodologies for the application of monobromobimane to the simultaneous analysis of soluble and protein thiol components of biological systems. Journal of Biochemical and Biophysical Methods 13, 231–246.CrossRefGoogle Scholar
Craft, NE & Wise, SA (1992) Optimisation of an isocratic high performance liquid chromatographic separation of carotenoids. Journal of Chromatography 589, 171–176.CrossRefGoogle Scholar
Edes, TE, Thornton, W Jr & Shah, J (1989) b-Carotene and aryl hydrocarbon hydroxylase in the rat: an effect of b-carotene independent of vitamin A activity. Journal of Nutrition 119, 769–799.CrossRefGoogle Scholar
Giovannucci, E, Ascherio, A, Rimm, EB, Stampfer, MJ, Colditz, GA & Willett, WC (1995) Intake of carotenoids and retinol in relation to risk of prostate cancer. Journal of the National Cancer Institute 87, 1767–1776.CrossRefGoogle ScholarPubMed
Gradelet, S, Astorg, P, Le Bon, AM, Berges, R & Suschetet, M (1997) Modulation of aflatoxin B1 carcinogenicity, genotoxicity and metabolism in rat liver by dietary carotenoids: evidence for a protective effect of CYP1A inducers. Cancer Letters 114, 221–223.CrossRefGoogle ScholarPubMed
Gradelet, S, Astorg, P, Leclerc, J, Chevalier, J, Vernevaut, MF & Siess, MH (1996 a) Effects of canthaxanthin, astaxanthin, lycopene and lutein on liver xenobiotic metabolizing enzymes in the rat. Xenobiotica 26, 49–63.CrossRefGoogle ScholarPubMed
Gradelet, S, Leclerc, J, Siess, MH & Astorg, P (1996 b) b-Apo-8-carotenal, but not b-carotene, is a strong inducer of liver cytochromes P450 1A1 and 1A2 in rat. Xenobiotica 26, 909–919.CrossRefGoogle ScholarPubMed
Habig, WH, Pabst, MJ & Jakoby, WB (1974) Glutathione S-transferases. Journal of Biological Chemistry 249, 7130–7139.CrossRefGoogle ScholarPubMed
Heinonen, OP & Albanes, D (1994) Alpha-tocopherol, beta-carotene prevention study group. The effect of vitamin E and beta-carotene on the incidence of lung cancer and other cancers in male smokers. New England Journal of Medicine 330, 1029–1035.Google Scholar
Hughes, DA, Wright, AJ, Finglas, PM, Peerless, AC, Bailey, AL, Astley, SB, Pinder, AC & Southon, S (1997) The effect of beta-carotene supplementation on the immune function of blood monocytes from healthy male nonsmokers. Journal of Laboratory and Clinical Medicine 129, 309–317.CrossRefGoogle ScholarPubMed
Krinsky, NI (1991) Effects of carotenoids in cellular and animal systems. American Journal of Clinical Nutrition 53, 238–246.CrossRefGoogle ScholarPubMed
LaChance, P (1988) Dietary intake of carotenes and the carotene gap. Clinical Nutrition 7, 118–122.Google Scholar
Manorama, R, Chinnasamy, N & Rukmini, C (1993) Effect of red palm oil on some hepatic drug metabolizing enzymes in rats. Food and Chemical Toxicology 31, 583–588.CrossRefGoogle ScholarPubMed
Mathews-Roth, MM, Welankiwar, S, Sehgal, PK, Lausen, NC, Russett, M & Krinsky, NI (1990) Distribution of [14C]canthaxanthin and [14C]lycopene in rats and monkeys. Journal of Nutrition 120, 1205–1213.CrossRefGoogle ScholarPubMed
Omenn, GS, Goodman, GE, Thornquist, MD, Balmes, J, Cullen, MR, Glass, A, Keogh, JP, Meyskens, FL Jr, Valanis, B, Williams, JH, Barnhart, S, Cherniack, MG, Brodkin, CA & Hammar, S (1996) Risk factors for lung cancer and for intervention effects in CARET, the beta-carotene and retinol efficacy trial. Journal of the National Cancer Institute 88, 1550–1559.CrossRefGoogle ScholarPubMed
Rock, CL, Jacob, RA & Bowen, PE (1996) Update on the biological characteristics of the antioxidant micronutrients: vitamin C, vitamin E and the carotenoids. Journal of the American Dietetic Association 96, 693–702.CrossRefGoogle ScholarPubMed
Santos, MS, Meydani, SN, Leka, L, Wu, D, Fotouhi, N, Meydani, M, Hennekens, CH & Gaziano, JM (1996) Natural killer cell activity in elderly men is enhanced by beta-carotene supplementation. American Journal of Clinical Nutrition 64, 772–777.CrossRefGoogle ScholarPubMed
Smith, PK, Krohn, RI, Hermanson, GT, Mallia, AK, Gartner, FH, Provenzano, MD, Fujimoto, FK, Goeke, NM, Olsen, BJ & Klenk, DC (1985) Measurement of protein using bicinchoninic acid. Analytical Chemistry 150, 76–85.Google ScholarPubMed
Stahl, W & Sies, H (1996) Lycopene: a biologically important carotenoid for humans?. Archives of Biochemistry and Biophysics 336, 1–9.CrossRefGoogle ScholarPubMed
Steinmetz, KA & Potter, JD (1996) Vegetables, fruit and cancer prevention: a review. Journal of the American Dietetic Association 96, 1027–1039.CrossRefGoogle ScholarPubMed
Toma, S, Losardo, PL, Vincent, M & Palumbo, R (1995) Effectiveness of beta-carotene in cancer chemoprevention. European Journal of Cancer Prevention 4, 213–224.CrossRefGoogle ScholarPubMed
Van Poppel, G, Poulsen, H, Loft, S & Verhagen, H (1995) Influence of beta-carotene on oxidative DNA damage in male smokers. Journal of the National Cancer Institute 87, 310–311.CrossRefGoogle ScholarPubMed
Zhang, LX, Cooney, RV & Bertram, JS (1992) Carotenoids up-regulate connexin-43 gene expression independent of their provitamin A or antioxidant properties. Cancer Research 52, 5707–5712.Google ScholarPubMed
Ziegler, RG, Colavito, EA, Hartge, P, McAdams, MJ, Schoenberg, JB, Mason, TJ & Fraumeni, JF (1996) Importance of alpha-carotene, beta-carotene and other phytochemicals in the etiology of lung cancer. Journal of the National Cancer Institute 88, 612–615.CrossRefGoogle ScholarPubMed