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Protective effects of tomato extract with elevated β-carotene levels on oxidative stress in ARPE-19 cells

Published online by Cambridge University Press:  08 March 2007

Gurunadh R. Chichili ,
Donatus Nohr ,
Jürgen Frank ,
Andrea Flaccus ,
Paul D. Fraser ,
Eugenia M. A. Enfissi  and
Hans K. Biesalski
Gurunadh R. Chichili
Affiliation:
Institute of Biological Chemistry and Nutrition, University of Hohenheim, Garbenstrasse 30, University of Hohenheim, D-70599 Stuttgart, Germany
Donatus Nohr
Affiliation:
Institute of Biological Chemistry and Nutrition, University of Hohenheim, Garbenstrasse 30, University of Hohenheim, D-70599 Stuttgart, Germany
Jürgen Frank
Affiliation:
Institute of Biological Chemistry and Nutrition, University of Hohenheim, Garbenstrasse 30, University of Hohenheim, D-70599 Stuttgart, Germany
Andrea Flaccus
Affiliation:
Institute of Biological Chemistry and Nutrition, University of Hohenheim, Garbenstrasse 30, University of Hohenheim, D-70599 Stuttgart, Germany
Paul D. Fraser
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 OEX, UK
Eugenia M. A. Enfissi
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 OEX, UK
Hans K. Biesalski*
Affiliation:
Institute of Biological Chemistry and Nutrition, University of Hohenheim, Garbenstrasse 30, University of Hohenheim, D-70599 Stuttgart, Germany
*
*Corresponding author: Professor H. K. Biesalski, fax +49 711 459 3822, email [email protected]
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Abstract

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Epidemiological studies show that dietary products rich in carotenoids delay the progression of age-related macular degeneration. Experimental evidence from cellular studies on the antioxidant actions of carotenoids in the retinal pigment epithelium is still, however, fragmentary. The present study examined the uptake and protective potential of dietary carotenoids from tomato on the human retinal pigment epithelial cell line ARPE-19. ARPE-19 cells were incubated in medium supplemented with tomato extract containing high levels of ß-carotene, lycopene and traces of lutein. The cellular uptake of carotenoids was analysed by reverse-phase HPLC. Oxidative stress was induced by treatment with 1 mm-H2O2. Nitrotyrosine was detected by immunocytochemistry, and oxidised proteins (protein carbonyls) were measured by a quantitative ELISA method. Lipid peroxidation was assessed by quantifying thiobarbituric acid reactive substances. ARPE-19 cells preferentially accumulated lutein and ß-carotene rather than lycopene. Nitrotyrosine formation was considerably reduced in cells incubated with tomato extract compared with controls after H2O2 treatment. Protein carbonyls were reduced by 30 % (P=0·015), and the formation of thiobarbituric acid-reactive substances was reduced by 140 % (P=0·003) in cells incubated with tomato extract. The present study provides the experimental evidence for protective effects of dietary tomatoes rich in carotenoids on oxidative stress in the retinal pigment epithelium.

Keywords

ß-caroteneOxidative stressRetinaAMDRetinal pigment epitheliumTomatoCarotenoids
Type
Research Article
Information
British Journal of Nutrition , Volume 96 , Issue 4 , October 2006 , pp. 643 - 649
Copyright
Copyright © The Nutrition Society 2006

References

Abushita, AA, Hebshi, EA, Daood, HG & Biacs, PA (1997) Determination of antioxidant vitamins in tomatoes. Food Chem 60, 207–212.CrossRefGoogle Scholar
Age-Related, Eye, Disease, Study & Research, Group (2001) A randomized, placebo controlled, clinical trial of high-dose supplementation with vitamins C and E, beta-carotene, and zinc for age-related macular degeneration and vision loss. Arch Ophthalmol 119, 1417–1436.Google Scholar
Beatty, S, Koh, H, Phil, M, Henson, D & Boulton, M (2000) The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv Ophthalmol 45, 115–134.CrossRefGoogle ScholarPubMed
Beckman, JS (1996) Oxidative damage and tyrosine nitration from peroxynitrite. Chem Res Toxicol 9, 836–844.CrossRefGoogle ScholarPubMed
Beecher, GR (1998) Nutrient content of tomatoes and tomato products. Proc Soc Exp Biol Med 218, 98–100.CrossRefGoogle ScholarPubMed
Bernstein, PS, Khachik, F, Carvalho, LS, Muir, GJ, Zhao, DY & Katz, NB (2001) Identification and quantitation of carotenoids and their metabolites in the tissues of the human eye. Exp Eye Res 72, 215–223.CrossRefGoogle ScholarPubMed
Buss, H, Chan, BH, Sluis, TP, Domigan, NM & Winterbourn, CC (1997) Protein carbonyl measurements by a sensitive ELISA method. Free Radic Biol Med 23, 361–366.CrossRefGoogle ScholarPubMed
Cantrell, A, McGarvey, DJ, Truscott, TG, Rancan, F & Bohm, F (2003) Singlet oxygen quenching by dietary carotenoids in a model membrane environment. Arch Biochem Biophys 412, 47–54.CrossRefGoogle Scholar
Chichili, GR, Nohr, D, Schaffer, M, Von Lintig, J & Biesalski, HK (2005) Beta-carotene conversion into vitamin A by retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 46, 3562–3569.CrossRefGoogle ScholarPubMed
Davies, MJ, Fu, S, Wang, H & Dean, RT (1999) Stable markers of oxidant damage to proteins and their application in the study of human disease. Free Radic Biol Med 27, 1151–1163.CrossRefGoogle Scholar
Giovannucci, E (1999) Tomatoes, tomato-based products, lycopene, and cancer: review of the epidemiologic literature. J Natl Cancer Inst 91, 317–331.CrossRefGoogle ScholarPubMed
Glickman, RD (2002) Phototoxicity to the retina: mechanisms of damage. Int J Toxicol 21, 473–490.CrossRefGoogle Scholar
Goldberg, J, Flowerdew, G, Smith, E, Brody, JA & Tso, MO (1988) Factors associated with age-related macular degeneration. An analysis of data from the first National Health and Nutrition Examination Survey. Am J Epidemiol 128, 700–710.CrossRefGoogle ScholarPubMed
Gross, J (1987) Pigments in Fruits. New York: Academic Press.Google Scholar
Ham, WT, Jr, Mueller, HA, Ruffolo, JJ, Jr, Millen, JE, Cleary, SF, Guerry, RK, Guerry, D 3rd (1984) Basic mechanisms underlying the production of photochemical lesions in the mammalian retina. Curr Eye Res 3, 165–174.CrossRefGoogle ScholarPubMed
Hawkins, BS, Bird, A, Klein, R & West, KS (1999) Epidemiology of age-related macular degeneration. Mol Vis 5, 26–32.Google ScholarPubMed
Hirayama, O, Nakamura, K, Hamada, S & Kobayasi, Y (1994) Singlet oxygen quenching ability of naturally occurring carotenoids. Lipids 29, 149–150.CrossRefGoogle ScholarPubMed
Hogg, R & Chakravarthy, U (2004) AMD and micronutrient antioxidants. Curr Eye Res 29, 387–401.CrossRefGoogle ScholarPubMed
Jentzsch, AM, Bachman, H, Furst, P & Biesalski, HK (1996) Improved analysis of malondialdehyde in human body fluids. Free Radic Biol Med 20, 251–256.CrossRefGoogle ScholarPubMed
Jouni, ZE & Wells, MA (1996) Purification and partial characterization of a lutein-binding protein from the midgut of the silkworm Bombyx mori. J Biol Chem 271, 14722–14726.CrossRefGoogle ScholarPubMed
Krinsky, NI (1998) Antioxidant functions of carotenoids. Free Radic Biol Med 7, 617–635.CrossRefGoogle Scholar
Krinsky, NI & Deneke, SM (1982) The interaction of oxygen and oxy-radicals with carotenoids. J Natl Cancer Inst 69, 205–210.Google ScholarPubMed
Kikugawa, K, Hiramoto, K, Tomiyama, S & Asano, Y (1997) Beta-carotene effectively scavenges toxic nitrogen oxides: nitrogen dioxide and peroxynitrous acid. FEBS Letts 404, 175–178.CrossRefGoogle ScholarPubMed
Kikugawa, K, Hiramoto, K, Tomiyama, S & Nakauchi, K (1999) Effect of beta-carotene on the transformation of tyrosine by nitrogen dioxide and peroxynitrous acid. Free Radic Res 30, 37–43.CrossRefGoogle ScholarPubMed
Lee, BM, Lee, SK & Kim, HS (1998) Inhibition of oxidative DNA damage, 8-OHdG, and carbonyl contents in smokers treated with antioxidants (vitamin E, vitamin C, beta-carotene and red ginseng). Cancer Lett 132, 219–227.CrossRefGoogle ScholarPubMed
Mayne, ST (1996) Beta-carotene, carotenoids, and disease prevention in humans. FASEB J 10, 690–701.CrossRefGoogle ScholarPubMed
Miyagi, M, Sakaguchi, H, Darrow, RM, Yan, L, West, KA, Aulak, KS, Stuehr, DJ, Hollyfield, JG, Organisciak, DT & Crabb, JW (2002) Evidence that light modulates protein nitration in rat retina. Mol Cell Proteomics 1, 293–303.CrossRefGoogle ScholarPubMed
Natarajan, N, Shambaugh, GE 3rd Elseth KM Haines GK Radosevich JA (1994) Adaptation of the diphenylamine (DPA) assay to a 96-well plate tissue culture format and comparison with the MTT assay. Biotechniques 17, 166–171.Google ScholarPubMed
Nomura, AM, Ziegler, RG, Stemmermann, GN, Chyou, PH & Craft, NE (1997) Serum micronutrients and upper aerodigestive tract cancer. Cancer Epidemiol Biomarker Prev 6, 407–412.Google ScholarPubMed
Paetau, I, Rao, D, Wiley, ER, Brown, ED & Clevidence, BA (1999) Carotenoids in human buccal mucosa cells after 4 wk of supplementation with tomato juice or lycopene supplements. Am J Clin Nutr 70, 490–494.CrossRefGoogle ScholarPubMed
Raffo, A, Leonardi, C, Fogliano, V, Ambrosino, P, Salucci, M, Gennaro, L, Bugianesi, R, Giuffrida, F & Quaglia, G (2002) Nutritional value of cherry tomatoes Lycopersicon esculentum Cv. (Naomi F1) harvested at different ripening stages. J Agric Food Chem 50, 6550–6556.CrossRefGoogle ScholarPubMed
Rao, MN, Ghosh, P & Lakshman, MR (1997) Purification and partial characterization of a cellular carotenoid-binding protein from ferret liver. J Biol Chem 272, 24455–24460.CrossRefGoogle ScholarPubMed
Roberts, JE (2001) Ocular phototoxicity. J Photochem Photobiol B 64, 136–143.CrossRefGoogle ScholarPubMed
Roemer, S, Fraser, PD, Kiano, JW, Shipton, CA, Mills, PB, Drake, R, Schuch, W & Bramley, PM (2000) Elevation of the provitamin A content of transgenic tomato plants. Nat Biotechnol 18, 666–669.CrossRefGoogle Scholar
Seddon, JM, Ajani, UA, Sperduto, RD, for, the, Eye, Disease, Case-control, Study Group (1994) Dietary carotenoids, vitamins A, C and E, and advanced age related macular degeneration. J Am Med Assoc 272, 1413–1420.CrossRefGoogle Scholar
Snodderly, DM (1995) Evidence for protection against age-related macular degeneration by carotenoids and antioxidant vitamins. Am J Clin Nutr 62, 1448S–1461S.CrossRefGoogle ScholarPubMed
Tonucci, LH, Holden, JM, Beecher, GR, Khachik, F, Davis, CS & Mulokozi, G (1995) Carotenoid content of thermally processed tomato-based food products. J Agric Food Chem 43, 579–586.CrossRefGoogle Scholar
Tso, MO (1989) Experiments on visual cells by nature and man: in search of treatment for photoreceptor degeneration. Invest Ophthalmol Vis Sci 30, 2430–2454.Google ScholarPubMed
Van den Langenberg, GM, Mares-Perlman, JA, Klein, R, Klein, BE, Brady, WE & Palta, M (1998) Associations between antioxidant and zinc intake and the 5-year incidence of age-related maculopathy in the Beaver Dam Eye Study. Am J Epidemiol 148, 204–214.CrossRefGoogle Scholar
van het, Hof, KH, de, Boer, BC, Tijburg, LB, Lucius, BR, Zijp, I, West, CE, Hautvast, JG & Weststrate, JA (2000) Carotenoid bioavailability in humans from tomatoes processed in different ways determined from the carotenoid response in the triglyceride-rich lipoprotein fraction of plasma after a single consumption and in plasma after four days of consumption. J Nutr 130, 1189–1196.Google Scholar
Van Leeuwen, R, Boekhoorn, S, Vingerling, JR, Witteman, JC, Klaver, CC, Hofman, A, de Jong, PT (2005) Dietary intake of antioxidants and risk of age-related macular degeneration. JAMA 294, 3101–3107.CrossRefGoogle ScholarPubMed
Wamer, WG, Wei, RR, Matusik, JE, Kornhauser, A & Dunkel, VC (1993) β-Carotene uptake, metabolism, and distribution in BALB/c 3T3 cells. Nutr Cancer 19, 31–41.CrossRefGoogle ScholarPubMed
Willcox, JK, Catignani, GL & Lazarus, S (2003) Tomatoes and cardiovascular health. Crit Rev Food Sci Nutr 43, 1–18.CrossRefGoogle ScholarPubMed
Winkler, BS, Boulton, ME, Gottsch, JD & Sternberg, P (1999) Oxidative damage and age-related macular degeneration. Mol Vis 5, 32Google ScholarPubMed
Yemelyanov, AY, Katz, NB & Bernstein, P (2001) Ligand-binding characterization of xanthophylls carotenoids to solubilized membrane proteins from human retina. Exp Eye Res 72, 381–392.CrossRefGoogle ScholarPubMed