Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-28T00:06:00.557Z Has data issue: false hasContentIssue false

Paraoxonase 1 Q192R (PON1-192) polymorphism is associated with reduced lipid peroxidation in healthy young men on a low-carotenoid diet supplemented with tomato juice

Published online by Cambridge University Press:  08 March 2007

Achim Bub*
Affiliation:
Institute of Nutritional Physiology, Federal Research Centre for Nutrition and Food, Haid-und-Neu-Str. 9, Karlsruhe, Germany
Stephan W. Barth
Affiliation:
Institute of Nutritional Physiology, Federal Research Centre for Nutrition and Food, Haid-und-Neu-Str. 9, Karlsruhe, Germany
Bernhard Watzl
Affiliation:
Institute of Nutritional Physiology, Federal Research Centre for Nutrition and Food, Haid-und-Neu-Str. 9, Karlsruhe, Germany
Karlis Briviba
Affiliation:
Institute of Nutritional Physiology, Federal Research Centre for Nutrition and Food, Haid-und-Neu-Str. 9, Karlsruhe, Germany
Gerhard Rechkemmer
Affiliation:
Department of Food and Nutrition, Center of Life Science, Technical University of Munich, Freising-Weihenstephan, Germany
*
*Corresponding author: Dr Achim Bub, fax +49 721-6625-404, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The HDL-bound enzyme paraoxonase (PON) protects LDL from oxidation and may therefore attenuate the development of atherosclerosis. We examined the effect of tomato and carrot juice consumption on PON1 activity and lipid peroxidation in healthy young volunteers with different PON1-192 genotypes (Q/R substitution at position 192). In this randomized cross-over study twenty-two healthy, non-smoking men on a low-carotenoid diet received 330 ml/d tomato juice (37·0 mg lycopene, 1·6 mg β-carotene) or carrot juice (27·1 mg β-carotene, 13·1 mg α-carotene) for 2 weeks. Intervention periods were preceded by 2-week low-carotenoid intake. We determined the PON1-192 genotype by restriction fragment length polymorphism–polymerase chain reaction (RFLP-PCR) and measured ex vivo LDL oxidation (lag time), plasma malondialdehyde and PON1 activity at the beginning and end of each intervention period. At baseline, lag time was higher (P<0·05) in QQ (111 (sd 9) min) than in QR/RR subjects (101 (sd 8) min). Neither tomato nor carrot juice consumption had significant effects on PON1 activity. However, tomato juice consumption reduced (P<0·05) plasma malondialdehyde in QR/RR (Δ: −0·073 (sd 0·11) μmol/l) as compared to QQ subjects (Δ:+0·047 (sd 0·13) μmol/l). Carrot juice had no significant effect on malondialdehyde irrespective of the PON1-192 genotype. Male volunteers with the QR/RR genotype showed an increased lipid peroxidation at baseline. Although tomato and carrot juice fail to affect PON1 activity, tomato juice intake reduced lipid peroxidation in healthy volunteers carrying the R-allele of the PON1-192 genotype and could thus contribute to CVD risk reduction in these individuals.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2005

References

Adkins, S, Gan, KN, Mody, M, La Du, BN (1993) Molecular basis for the polymorphic forms of human serum paraoxonase/arylesterase: glutamine or arginine at position 191, for the respective A or B alloenzyme. Am J Hum Genet 52, 598608.Google ScholarPubMed
Agarwal, S & Rao, AV (1998) Tomato lycopene and low density lipoprotein oxidation: a human dietary intervention study. Lipids 33, 981984.CrossRefGoogle ScholarPubMed
Altman, DG (1991) Clinical trials Practical Statistics for Medical Research, 440476 [Altman, DG, editors]. London: Chapman & Hall.Google Scholar
Aviram, M (1999) Does paraoxonase play a role in susceptibility to cardiovascular disease?. Mol Med Today 5, 381386.CrossRefGoogle ScholarPubMed
Aviram, M, Billecke, S & Sorenson, R (1998) Paraoxonase active site required for protection against LDL oxidation involves its free sulfhydryl group and is different from that required for its arylesterase/paraoxonase activities. Arterioscler Thromb Vasc Biol 18, 16171624.CrossRefGoogle ScholarPubMed
Aviram, M, Dornfeld, L, Rosenblat, M, Volkova, N, Kaplan, M, Colemann, R, Hayek, T, Presser, D & Fuhrman, B (2000) Pomegranate juice consumption reduces oxidative stress, atherogenic modifications to LDL, and platelet aggregation: studies in humans and in atherosclerotic apolipoprotein E-deficient mice. Am J Clin Nutr 71, 10621076.CrossRefGoogle ScholarPubMed
Bazzano, LA, He, J, Ogden, LG, Loria, CM, Vupputuri, S, Myers, L & Whelton, PK (2002) Fruit and vegetable intake and risk of cardiovascular disease in US adults: the first National Health and Nutrition Examination Survey Epidemiologic Follow-up Study. Am J Clin Nutr 76, 9399.CrossRefGoogle ScholarPubMed
Briviba, K, Schnäbele, K, Rechkemmer, G & Bub, A (2004) Supplementation of a diet low in carotenoids with tomato and carrot juice does not affect lipid peroxidation in plasma and feces of healthy men. J Nutr 134, 10811083.CrossRefGoogle Scholar
Bub, A, Barth, S, Watzl, B, Briviba, K, Herbert, BM, Luhrmann, PM, Neuhauser-Berthold, M & Rechkemmer, G (2002) Paraoxonase 1 Q192R (PON1-192) polymorphism is associated with reduced lipid peroxidation in R-allele-carrier but not in QQ homozygous elderly subjects on a tomato-rich diet. Eur J Nutr 41, 237243.CrossRefGoogle Scholar
Bub, A, Watzl, B, Abrahamse, L, Delincée, H, Adam, S, Wever, J, Müller, H & Rechkemmer, G (2000) Moderate intervention with carotenoid-rich vegetable products reduces lipid peroxidation in men. J Nutr 130, 22002206.CrossRefGoogle ScholarPubMed
Burkart, V, Liu, H, Bellmann, K, Wissing, D, Jäättelä, M, Cavallo, MG, Pozilli, P, Briviba, K & Kolb, H (2000) Natural resistance of human beta cells toward nitric oxide is mediated by heat shock protein 70. J Biol Chem 275, 1952119528.CrossRefGoogle ScholarPubMed
Diaz, MN, Frei, B, Vita, JA & Keaney, JF (1997) Mechanisms of disease: antioxidants and atherosclerotic heart disease. N Engl J Med 337, 408416.CrossRefGoogle Scholar
Esterbauer, H, Striegl, G, Puhl, H & Rotheneder, M (1989) Continuous monitoring of in vitro oxidation of human low density lipoprotein. Free Rad Res Commun 6, 6775.CrossRefGoogle ScholarPubMed
Frei, B, Keaney, JF, Retsky, KL & Chen, K (1996) Vitamins C and E and LDL oxidation Vitamins and Hormones—Advances in Research and Applications, Vol. 52, 134 [Litwack, G, editors]. San Diego: Academic Press.Google Scholar
Gan, KN, Smolen, A, Eckerson, HW, La Du, BN (1991) Purification of human serum paraoxonase/arylesterase. Evidence for one esterase catalyzing both activities. Drug Metab Dispos 19, 100106.Google Scholar
Humbert, R, Adler, DA, Disteche, CM, Hassett, C, Omiecinski, CJ & Furlong, CE (1993) The molecular basis of the human serum paraoxonase activity polymorphism. Nat Genet 3, 7376.Google Scholar
Jarvik, GP, Hatsukami, TS, Carlson, C, Richter, RJ, Jampsa, R, Brophy, VH, Margolin, S, Rieder, M, Nickerson, D, Schellenberg, GD, Heagerty, PJ & Furlong, CE (2003) Paraoxonase activity, but not haplotype utilizing the linkage disequilibrium structure, predicts vascular disease. Arteriosc Thromb Vasc Biol 23, 14651471.Google Scholar
Jarvik, GP, Rozek, LS, Brophy, VH, Hatsukami, TS, Richter, RJ, Schellenberg, GD & Furlong, CE (2000) Paraoxonase (PON1) phenotype is a better predictor of vascular disease than is PON1(192) or PON1(55) genotype. Arterioscler Thromb Vasc Biol 20, 24412447.CrossRefGoogle Scholar
Jialal, I & Devaraj, S (1996) Low density lipoprotein oxidation, antioxidants, and atherosclerosis: a clinical biochemistry perspective. Clin Chem 42, 498506.CrossRefGoogle ScholarPubMed
Joshipura, KJ, Hu, FB & Manson, JE (2001) The effect of fruit and vegetable intake on risk for coronary heart disease. Ann Intern Med 134, 11061114.Google Scholar
Kleemola, P, Freese, R, Jauhiainen, M, Pahlman, R, Alfthan, G & Mutanen, M (2002) Dietary determinants of serum paraoxonase activity in healthy humans. Atherosclerosis 160, 425432.CrossRefGoogle ScholarPubMed
Krinsky, NI (1998) The antioxidant and biological properties of the carotenoids. Ann NY Acad Sci 854, 443447.Google Scholar
Kudchodkar, BJ, Lacko, AG, Dory, L & Fungwe, TV (2000) Dietary fat modulates serum paraoxonase 1 activity in rats. J Nutr 130, 24272433.CrossRefGoogle ScholarPubMed
Liu, S, Lee, IM, Ajani, U, Cole, SR, Buring, JE & Manson, JE (2001) Intake of vegetables rich in carotenoids and risk of coronary heart disease in men: The Physicians' Health Study. Int J Epidemiol 30, 130135.CrossRefGoogle Scholar
Liu, S, Manson, JE, Lee, IM, Cole, SR, Hennekens, CH, Willett, WC & Buring, JE (2000) Fruit and vegetable intake and risk of cardiovascular disease: the Women's Health Study. Am J Clin Nutr 72, 922928.CrossRefGoogle ScholarPubMed
Mackness, B, Durrington, P, McElduff, P, Yarnell, J, Azam, N, Watt, M & Mackness, M (2003) Low paraoxonase activity predicts coronary events in the caerphilly prospective study. Circulation 107, 27752779.Google Scholar
Mackness, B, Mackness, MI, Arrol, S, Turkie, W & Durrington, PN (1998) Effect of the human serum paraoxonase 55 and 192 genetic polymorphisms on the protection by high density lipoprotein against low density lipoprotein oxidative modification. FEBS Lett 423, 5760.Google Scholar
Mackness, MI, Bouiller, A, Hennuyer, N, Mackness, B, Hall, M, Tailleux, A, Duriez, P, Delfly, B, Durrington, P, Fruchart, JC, Duverger, N, Caillaud, JM & Castro, G (2000) Paraoxonase activity is reduced by a pro-atherosclerotic diet in rabbits. Biochem Biophys Res Commun 269, 232236.Google Scholar
Mackness, MI, Durrington, PN & Mackness, B (2000) How high-density lipoprotein protects against the effects of lipid peroxidation. Curr Opin Lipidol 11, 383388.CrossRefGoogle ScholarPubMed
Mackness, MI, Harty, D, Bhatnagar, D, Winocour, PH, Arrol, S, Ishola, M & Durrington, PN (1991) Serum paraoxonase activity in familial hypercholesterolaemia and insulin-dependent diabetes mellitus. Atherosclerosis 86, 193199.Google Scholar
Mackness, MI, Mackness, B, Durrington, PN, Fogelman, AM, Berliner, JXLA, Navab, M, Shih, D & Fonarow, GC (1998) Paraoxonase and coronary heart disease. Curr Opin Lipidol 9, 319324.Google Scholar
Müller, H, Bub, A, Watzl, B & Rechkemmer, G (1999) Plasma concentrations of carotenoids in healthy volunteers after intervention with carotenoid-rich foods. Eur J Nutr 38, 3544.Google ScholarPubMed
Osganian, SK, Stampfer, MJ, Rimm, E, Spiegelman, D, Manson, JE & Willett, WC (2003) Dietary carotenoids and risk of coronary artery disease in women. Am J Clin Nutr 77, 13901399.CrossRefGoogle ScholarPubMed
Rantala, M, Silaste, ML, Tuominen, A, Kaikkonen, J, Salonen, JT, Alfthan, G, Aro, A, Kesäniemi, YA (2002) Dietary modifications and gene polymorphisms alter serum paraoxonase activity in healthy women. J Nutr 132, 30123017.CrossRefGoogle ScholarPubMed
Salonen, JT (2002) Clinical trials testing cardiovascular benefits of antioxidant supplementation. Free Rad Res 36, 12991306.CrossRefGoogle ScholarPubMed
Sutherland, WHF, Walker, RJ, DeJong, SA, vanRijn, AM, Phillips, V & Walker, HL (1999) Reduced postprandial serum paraoxonase activity after a meal rich in used cooking fat. Arterioscler Thromb Vasc Biol 19, 13401347.CrossRefGoogle Scholar
Tomás, M, Sentí, M, Elosua, R, Vila, J, Sala, J, Masià, R & Marrugat, J (2001) Interaction between the Gln-Arg 192 variants of the paraoxonase gene and oleic acid intake as a determinant of high-density lipoprotein cholesterol and paraoxonase activity. Eur J Pharmacol 432, 121128.CrossRefGoogle ScholarPubMed
Upston, JM, Kritharides, L & Stocker, R (2003) The role of vitamin E in atherosclerosis. Prog Lip Res 42, 405422.CrossRefGoogle ScholarPubMed
van der, Gaag, MS, van, Tol, A, Scheek, LM, James, RW, Urgert, R, Schaafsma, G & Hendriks, HFJ (1999) Daily moderate alcohol consumption increases serum paraoxonase activity; a diet-controlled, randomized intervention study in middle-aged men. Atherosclerosis 147, 405410.CrossRefGoogle Scholar
Visioli, F, Riso, P, Grande, S, Galli, C & Porrini, M (2003) Protective activity of tomato products on in vivo markers of lipid oxidation. Eur J Nutr 42, 201206.Google Scholar
Vivekananthan, DP, Penn, MS, Sapp, SK, Hsu, A & Topol, EJ (2003) Use of antioxidant vitamins for the prevention of cardiovascular disease: meta-analysis of randomised trials. Lancet 361, 20172023.CrossRefGoogle ScholarPubMed
Watzl, B, Bub, A, Briviba, K & Rechkemmer, G (2003) Supplementation of a low-carotenoid diet with tomato or carrot juice modulates immune functions in healthy men. Ann Nutr Metab 47, 255261.Google Scholar