Abstract
Postprandial oxidative stress is characterized by an increased susceptibility of the organism towards oxidative damage after consumption of a meal rich in lipids and/or carbohydrates. We have investigated whether the quality of dietary fat alters postprandial gene expression and protein levels involved in oxidative stress and whether the supplementation with coenzyme Q10 (CoQ) improves this situation in an elderly population. Twenty participants were randomized to receive three isocaloric diets each for 4 weeks: Mediterranean diet supplemented with CoQ (Med + CoQ diet), Mediterranean diet (Med diet), saturated fatty acid-rich diet (SFA diet). After 12-h fast, volunteers consumed a breakfast with a fat composition similar to that consumed in each of the diets. Nrf2, p22phox and p47phox, superoxide dismutase 1 and 2 (SOD1 and SOD2), glutathione peroxidase 1 (GPx1), thiorredoxin reductase (TrxR) gene expression and Kelch-like ECH associating protein 1 (Keap-1) and citoplasmic and nuclear Nrf2 protein levels were determined. Med and Med + CoQ diets induced lower Nrf2, p22phox, p47phox, SOD1, SOD2 and TrxR gene expression and higher cytoplasmic Nrf2 and Keap-1 protein levels compared to the SFA diet. Moreover, Med + CoQ diet produced lower postprandial Nrf2 gene expression and lower nuclear Nrf2 protein levels compared to the other diets and lower GPx1 gene expression than the SFA diet. Our results support the antioxidant effect of a Med diet and that exogenous CoQ supplementation has a protective effects against free radical overgeneration through the lowering of postprandial oxidative stress modifying the postprandial antioxidant protein levels and reducing the postprandial expression of antioxidant genes in peripheral blood mononuclear cells.
Abbreviations
- Apo:
-
Apolipoprotein
- CAT:
-
Catalase
- CoQ:
-
Coenzyme Q10
- GPx:
-
Gluthatione peroxidase
- H2O2 :
-
Hydrogen peroxide
- Keap-1:
-
Kelch-like ECH associating protein 1
- Med diet:
-
Mediterranean diet
- Med + CoQ diet:
-
Mediterranean supplemented with CoQ
- MUFA:
-
Monounsaturated fatty acid
- PBMCs:
-
Peripheral blood mononuclear cells
- PUFA:
-
Polyunsaturated fatty acid
- ROS:
-
Reactive oxygen species
- SFA diet:
-
Saturated fatty acid-rich diet
- SOD:
-
Superoxide dismutase
- TG:
-
Triacylglycerol
- TrxR:
-
Thiorredoxin reductase
References
Arsova-Sarafinovska A, Eken A, Matevska N, Erdem O, Sayal A, Savaser A, Banev S, Petrovski D, Dzikova S, Georgiev V et al (2009) Increased oxidative/nitrosative stress and decreased antioxidant enzyme activities in prostate cancer. Clin Biochem 42:1228–1235
Battino M, Bompadre S, Leone L, Villa RF, Gorini A (2001)Coenzymes Q9 and Q10, vitamin E and peroxidation in rats synaptic and non-synaptic occipital cerebral cortex mitochondrial during ageing. Biol Chem 382:925–931
Bjornstedt M, Hamberg M, Kumar S, Xue J, Holmgren A (1995) Human thioredoxin reductase directly reduces lipid hydroperoxides by NADPH and selenocystine strongly stimulates the reaction via catalytically generated selenols. J Biol Chem 270:11761–11764
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brandes RP, Kreuzer J (2005) Vascular NADPH oxidases: molecular mechanisms of activation. Cardiovasc Res 65:16–27
Burczynski ME, Dorner AJ (2006) Transcriptional profiling of peripheral blood cells in clinical pharmacogenomic studies. Pharmacogenomics 7:187–202
Chen C, Kong AN (2004) Dietary chemopreventive compounds and ARE/EpRE signaling. Free Radic Biol Med 36:1505–1516
Coate KC, Huggins KW (2010) Consumption of a high glycemic index diet increases abdominal adiposity but does not influence adipose tissue pro-oxidant and antioxidant gene expression in C57BL/6 mice. Nutr Res 30:141–150
Covas MI (2007) Benefits of the Mediterranean diet on cardiovascular disease. Future Cardiol 3:575–578
de Haan JB, Bladier C, Griffiths P, Kelner M, O’Shea RD, Cheung NS, Bronson RT, Silvestro MJ, Wild S, Zheng SS et al (1998) Mice with a homozygous null mutation for the most abundant glutathione peroxidase, Gpx1, show increased susceptibility to the oxidative stress-inducing agents paraquat and hydrogen peroxide. J Biol Chem 273:22528–22536
de Mello VD, Kolehmaimen M, Schwab U, Mager U, Laaksonen DE, Pulkkinen L, Niskanen L, Gylling H, Atalay M, Rauramaa R et al (2008) Effect of weight loss on cytokine messenger RNA expression in peripheral blood mononuclear cells of obese subjects with the metabolic syndrome. Metabolism 57:192–199
Dinkova-Kostova AT, Talalay P (2008) Direct and indirect antioxidant properties of inducers of cytoprotective proteins. Mol Nutr Food Res 52(Suppl 1):S128–138
Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95
Elahi MM, Kong YX, Matata BM (2009) Oxidative stress as a mediator of cardiovascular disease. Oxid Med Cell Longev 2:259–269
Estruch R, Martinez-Gonzalez MA, Corella D, Salas-Salvado J, Ruiz-Gutierrez V, Covas MI, Fiol M, Gomez-Gracia E, Lopez-Sabater MC, Vinyoles E et al (2006) Effects of a Mediterranean-style diet on cardiovascular risk factors: a randomized trial. Ann Intern Med 145:1–11
Folkers K, Brown R, Judy WV, Morita M (1993) Survival of cancer patients on therapy with coenzyme Q10. Biochem Biophys Res Commun 192:241–245
Forstermann U (2008) Oxidative stress in vascular disease: causes, defense mechanisms and potential therapies. Nat Clin Pract Cardiovasc Med 5:338–349
Grienling KK (2004) Novel NAD(P)H oxidases in the cardiovascular system. Heart 90:491–493
Gutierrez-Mariscal FM, Perez-Martinez P, Delgado-Lista J, Yubero-Serrano EM, Camargo A, Delgado-Casado N, Cruz-Teno C, Santos-Gonzalez M, Rodriguez-Cantalejo F, Castaño JP, et al (2011). Mediterranean diet supplemented with coenzyme Q10 induces postprandial changes in p53 in response to oxidative DNA damage in elderly subjects. Age (Dordr) (in press)
Harman D (2009) Origin and evolution of the free radical theory of aging: a brief personal history, 1954–2009. Biogerontology 10:773–81
Human Nutrition Information Service, Department of Agriculture (1987) Composition of foods. US Government Printing Office, Washington, DC
Jimenez-Gomez Y, Lopez-Miranda J, Blanco-Colio JM, Marin C, Perez-Martinez P, Ruano J, Paniagua JA, Rodriguez F, Egido J, Perez-Jimenez F (2009) Olive oil and walnut breakfasts reduce the postprandial inflammatory response in mononuclear cells compared with a butter breakfast in healthy men. Atherosclerosis 204:e70–6
Kaikkonen J, Tuomainen TP, Nyyssonen K, Salonen JT (2002) Coenzyme Q10: absorption, antioxidative properties, determinants, and plasma levels. Free Radic Res 36:389–397
Kobayashi M, Yamamoto M (2005) Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid Redox Signal 7:385–394
Lombard DB, Chua KF, Mostoslavsky R, Franco S, Gostissa M, Alt FW (2005) DNA repair, genome stability, and aging. Cell 120:497–512
Mass K, Chan S, Parker J, Slater A, Moore J, Olsen N, Aune TM (2002) Cutting edge: molecular portrait of human autoimmune disease. J Immunol 169:5–9
Mates JM, Perez-Gomez C, Nuñez de Castro I (1999) Antioxidant enzymes and human diseases. Clin Biochem 32:595–603
Muller T, Buttner T, Gholipour AF, Kuhn W (2003) Coenzyme Q10 supplementation provides mild symptomatic benefit in patients with Parkinson's disease. Neurosci Lett 341:201–204
Nguyen T, Sherratt PJ, Nioi P, Yang CS, Pickett CB (2005) Nrf2 controls constitutive and inducible expression of ARE-driven genes through a dynamic pathway involving nucleocytoplasmic shuttling by Keap1. J Biol Chem 280:32485–32492
Nordberg J, Arner ES (2001) Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med 31:1287–1312
Quiles JL, Ochoa JJ, Battino M, Gutierrez-Rios P, Nepomuceno EA, Frías ML, Huertas JR, Mataix J (2005) Life-long supplementation with a low dosage of coenzyme Q10 in the rat: effects on antioxidant status and DNA damage. Biofactors 25:73–86
Quinzii CM, Lopez LC, Naini A, DiMauro S, Hirano M (2008) Human CoQ10 deficiencies. Biofactors 32:113–118
Rao G, Xia E, Richardson A (1990) Effect of age on the expression of antioxidant enzymes in male Fischer F344 rats. Mech Ageing Dev 53:49–60
Stachowska E, Wesolowska T, Olszewska M, Safranow K, Millo B, Domanski L, Jakubowska K, Ciechanowski K, Chlubek D (2005) Elements of Mediterranean diet improve oxidative status in blood of kidney graft recipients. Br J Nutr 93:345–352
Trichopoulou A, Costacou T, Bamia C, Trichopoulos D (2003) Adherence to a Mediterranean diet and survival in a Greek population. N Engl J Med 348:2599–2608
Varela G (1980) Tablas de composición de alimentos. (Food composition tables). Instituto de Nutrición CSIC, Madrid
Visioli F, Galli C (2001) The role of antioxidants in the Mediterranean diet. Lipids 36(Suppl):S49–52
Wang YP, Cheng ML, Zhang BF, Mu M, Wu J (2010) Effects of blueberry on hepatic fibrosis and transcription factor Nrf2 in rats. World J Gastroenterol 16:2657–2663
Xu W, Hellerbrand C, Kohler UA, Bugnon P, Kan YW, Werner S, Beyer TA (2008) The Nrf2 transcription factor protects from toxin-induced liver injury and fibrosis. Lab Invest 88:1068–1078
Yubero-Serrano EM, Delgado-Casado N, Delgado-Lista J, Perez-Martinez P, Tasset-Cuevas I, Santos-Gonzalez M, Caballero J, Garcia-Rios A, Marin C, Gutierrez-Mariscal FM, et al (2010). Postprandial antioxidant effect of the Mediterranean diet supplemented with coenzyme Q(10) in elderly men and women. Age (Dordr) (in press)
Zhang DD (2006) Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab Rev 38:769–789
Zhong L, Holmgren A (2000) Essential role of selenium in the catalytic activities of mammalian thioredoxin reductase revealed by characterization of recombinant enzymes with selenocysteine mutations. J Biol Chem 275:18121–18128
Acknowledgements
Supported in part by research grants from the Ministerio de Ciencia e Innovación (AGL 2004-07907, AGL2006-01979, AGL2009-12270 to JL-M and FIS PI10/01041 to PP-M), Consejería de Innovación, Ciencia y Empresa, Junta de Andalucía (P06-CTS-01425 to JL-M, CTS5015 to FP-J); Consejería de Salud, Junta de Andalucía (06/128, 07/43, PI0193/2009 to JL-M, 06/129 to FP-J, PI-0252/09 to JD-L, and PI-0058/10 to PP-M), and Kaneka Corporation (Japan) by the production of CoQ and placebo capsules. The CIBEROBN is an initiative of the Instituto de Salud Carlos III, Madrid, Spain.
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Yubero-Serrano, E.M., Gonzalez-Guardia, L., Rangel-Zuñiga, O. et al. Postprandial antioxidant gene expression is modified by Mediterranean diet supplemented with coenzyme Q10 in elderly men and women. AGE 35, 159–170 (2013). https://doi.org/10.1007/s11357-011-9331-4
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DOI: https://doi.org/10.1007/s11357-011-9331-4