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Published in: European Journal of Nutrition 6/2009

01-09-2009 | Original Contribution

Tachyphylaxis effects on postprandial oxidative stress and mitochondrial-related gene expression in overweight subjects after a period of energy restriction

Authors: Ana B. Crujeiras, Dolores Parra, Estíbaliz Goyenechea, Itziar Abete, J. Alfredo Martínez

Published in: European Journal of Nutrition | Issue 6/2009

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Abstract

Background

Postprandially induced oxidative stress can cause damage to mitochondrial components and initiate cellular degradative processes; which are related to obesity comorbidities.

Aim of the study

This trial sought to determine whether weight loss induced by caloric restriction provides antioxidant protection to reduce the postprandial response of mitochondrial function and oxidative stress markers.

Methods

A group of overweight/obese volunteers (n = 17; 39 ±7 years, 32.5 ± 4.8 kg/m2) followed an 8-week hypocaloric diet. Volunteers provided blood samples at fasting and 2-h after a test drink (CHO: 95% E, PROT: 5% E and containing antioxidants) and these were examined for postprandial oxidative stress responses, before and after the nutritional intervention. The expression of four mitochondrial-related genes, COX15, NDUFS2, MGST2 and TNF-alfa, was measured in peripheral blood mononuclear cells (PBMC) by quantitative RT-PCR. Lipid peroxidation and nitrosative stress biomarkers, total antioxidant capacity (AOP), uric acid and glutathione peroxidase were also determined.

Results

Before nutritional treatment, the test drink induced a postprandial increase in lipid peroxidation and nitrosative stress biomarkers with a concomitant increase in the AOP. The increase in postprandial oxidative stress biomarkers was accompanied by a decrease in PBMC COX15 mRNA levels. Interestingly, after the weight loss period (−5.8 ± 2.3%), the postprandial-induced changes were lower than at the beginning of the study and involved oxidative stress biomarkers and the COX15 and MGST2 transcripts. This finding suggests the occurrence of a tachyphylactic process.

Conclusions

We demonstrate for the first time that the well-known effect of energy restriction on oxidative stress is accompanied by a tolerance mechanism on the postprandial oxidative stress response and mitochondrial function-related genes. Indeed, the COX15 and MGST2 gene expression assays in PBMC emerged as valuable nutrigenomic biomarkers of the oxidative response under energy-restriction conditions.
Literature
1.
go back to reference Abete I, Parra D, Martinez JA (2008) Energy-restricted diets based on a distinct food selection affecting the glycemic index induce different weight loss and oxidative response. Clin Nutr 27:545–551CrossRef Abete I, Parra D, Martinez JA (2008) Energy-restricted diets based on a distinct food selection affecting the glycemic index induce different weight loss and oxidative response. Clin Nutr 27:545–551CrossRef
2.
go back to reference Bergmann MM, Görman U, Mathers JC (2008) Bioethical considerations for human nutrigenomics. Annu Rev Nutr 28:447–467CrossRef Bergmann MM, Görman U, Mathers JC (2008) Bioethical considerations for human nutrigenomics. Annu Rev Nutr 28:447–467CrossRef
3.
go back to reference Block G, Dietrich M, Norkus EP, Morrow JD, Hudes M, Caan B, Packer L (2002) Factors associated with oxidative stress in human populations. Am J Epidemiol 156:274–285CrossRef Block G, Dietrich M, Norkus EP, Morrow JD, Hudes M, Caan B, Packer L (2002) Factors associated with oxidative stress in human populations. Am J Epidemiol 156:274–285CrossRef
4.
go back to reference Bo S, Gambino R, Guidi S, Silli B, Gentile L, Cassader M, Pagano GF (2005) Plasma nitrotyrosine levels, antioxidant vitamins and hyperglycaemia. Diabet Med 22:1185–1189CrossRef Bo S, Gambino R, Guidi S, Silli B, Gentile L, Cassader M, Pagano GF (2005) Plasma nitrotyrosine levels, antioxidant vitamins and hyperglycaemia. Diabet Med 22:1185–1189CrossRef
5.
go back to reference Bonnard C, Durand A, Peyrol S, Chanseaume E, Chauvin MA, Morio B, Vidal H, Rieusset J (2008) Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest 118:789–800 Bonnard C, Durand A, Peyrol S, Chanseaume E, Chauvin MA, Morio B, Vidal H, Rieusset J (2008) Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest 118:789–800
6.
go back to reference Cadenas E, Davies KJ (2000) Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29:222–230CrossRef Cadenas E, Davies KJ (2000) Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29:222–230CrossRef
7.
go back to reference Crujeiras AB, Parra D, Abete I, Martinez JA (2007) A hypocaloric diet enriched in legumes specifically mitigates lipid peroxidation in obese subjects. Free Radic Res 41:498–506CrossRef Crujeiras AB, Parra D, Abete I, Martinez JA (2007) A hypocaloric diet enriched in legumes specifically mitigates lipid peroxidation in obese subjects. Free Radic Res 41:498–506CrossRef
8.
go back to reference Crujeiras AB, Parra D, Goyenechea E, Abete I, González-Muniesa P, Martínez JA (2008) Energy restriction in obese subjects impact differently two mitochondrial function markers. J Physiol Biochem 64:211–220CrossRef Crujeiras AB, Parra D, Goyenechea E, Abete I, González-Muniesa P, Martínez JA (2008) Energy restriction in obese subjects impact differently two mitochondrial function markers. J Physiol Biochem 64:211–220CrossRef
9.
go back to reference Crujeiras AB, Parra D, Goyenechea E, Martínez JA (2008) Sirtuin gene expression in human mononuclear cells is modulated by caloric restriction. Eur J Clin Invest 38:672–678CrossRef Crujeiras AB, Parra D, Goyenechea E, Martínez JA (2008) Sirtuin gene expression in human mononuclear cells is modulated by caloric restriction. Eur J Clin Invest 38:672–678CrossRef
10.
go back to reference Crujeiras AB, Parra D, Milagro FI, Goyenechea E, Larrarte E, Margareto J, Martinez JA (2008) Differential expression of oxidative stress and inflammation related genes in peripheral blood mononuclear cells in response to a low-calorie diet: a nutrigenomics study. OMICS 12:251–261CrossRef Crujeiras AB, Parra D, Milagro FI, Goyenechea E, Larrarte E, Margareto J, Martinez JA (2008) Differential expression of oxidative stress and inflammation related genes in peripheral blood mononuclear cells in response to a low-calorie diet: a nutrigenomics study. OMICS 12:251–261CrossRef
11.
go back to reference Crujeiras AB, Parra MD, Rodriguez MC, Martinez de Morentin BE, Martinez JA (2006) A role for fruit content in energy-restricted diets in improving antioxidant status in obese women during weight loss. Nutrition 22:593–599CrossRef Crujeiras AB, Parra MD, Rodriguez MC, Martinez de Morentin BE, Martinez JA (2006) A role for fruit content in energy-restricted diets in improving antioxidant status in obese women during weight loss. Nutrition 22:593–599CrossRef
12.
go back to reference Chung HY, Sung B, Jung KJ, Zou Y, Yu BP (2006) The molecular inflammatory process in aging. Antioxid Redox Signal 8:572–581CrossRef Chung HY, Sung B, Jung KJ, Zou Y, Yu BP (2006) The molecular inflammatory process in aging. Antioxid Redox Signal 8:572–581CrossRef
13.
go back to reference Dandona P, Aljada A, Chaudhuri A, Mohanty P, Garg R (2005) Metabolic syndrome: a comprehensive perspective based on interactions between obesity, diabetes, and inflammation. Circulation 111:1448–1454CrossRef Dandona P, Aljada A, Chaudhuri A, Mohanty P, Garg R (2005) Metabolic syndrome: a comprehensive perspective based on interactions between obesity, diabetes, and inflammation. Circulation 111:1448–1454CrossRef
14.
go back to reference Dandona P, Mohanty P, Ghanim H, Aljada A, Browne R, Hamouda W, Prabhala A, Afzal A, Garg R (2001) The suppressive effect of dietary restriction and weight loss in the obese on the generation of reactive oxygen species by leukocytes, lipid peroxidation, and protein carbonylation. J Clin Endocrinol Metab 86:355–362CrossRef Dandona P, Mohanty P, Ghanim H, Aljada A, Browne R, Hamouda W, Prabhala A, Afzal A, Garg R (2001) The suppressive effect of dietary restriction and weight loss in the obese on the generation of reactive oxygen species by leukocytes, lipid peroxidation, and protein carbonylation. J Clin Endocrinol Metab 86:355–362CrossRef
15.
go back to reference Fenster CP, Darley-Usmar VM, Landar AL, Gower BA, Weinsier RL, Hunter GR, Patel RP (2004) Weight loss and race modulate nitric oxide metabolism in overweight women. Free Radic Biol Med 37:695–702CrossRef Fenster CP, Darley-Usmar VM, Landar AL, Gower BA, Weinsier RL, Hunter GR, Patel RP (2004) Weight loss and race modulate nitric oxide metabolism in overweight women. Free Radic Biol Med 37:695–702CrossRef
16.
go back to reference Kadenbach B, Huttemann M, Arnold S, Lee I, Bender E (2000) Mitochondrial energy metabolism is regulated via nuclear-coded subunits of cytochrome c oxidase. Free Radic Biol Med 29:211–221CrossRef Kadenbach B, Huttemann M, Arnold S, Lee I, Bender E (2000) Mitochondrial energy metabolism is regulated via nuclear-coded subunits of cytochrome c oxidase. Free Radic Biol Med 29:211–221CrossRef
17.
go back to reference Kay CD, Holub BJ (2003) The postprandial effects of dietary antioxidants in humans. Curr Atheroscler Rep 5:452–458CrossRef Kay CD, Holub BJ (2003) The postprandial effects of dietary antioxidants in humans. Curr Atheroscler Rep 5:452–458CrossRef
18.
go back to reference Labayen I, Diez N, Parra D, Gonzalez A, Martinez JA (2004) Basal and postprandial substrate oxidation rates in obese women receiving two test meals with different protein content. Clin Nutr 23:571–578CrossRef Labayen I, Diez N, Parra D, Gonzalez A, Martinez JA (2004) Basal and postprandial substrate oxidation rates in obese women receiving two test meals with different protein content. Clin Nutr 23:571–578CrossRef
19.
go back to reference Li X, Liu Z, Luo C, Jia H, Sun L, Hou B, Shen W, Packer L, Cotman CW, Liu J (2008) Lipoamide protects RPE cells from oxidative stress and mitochondrial dysfunction. Free Radic Biol Med 44:1465–1474CrossRef Li X, Liu Z, Luo C, Jia H, Sun L, Hou B, Shen W, Packer L, Cotman CW, Liu J (2008) Lipoamide protects RPE cells from oxidative stress and mitochondrial dysfunction. Free Radic Biol Med 44:1465–1474CrossRef
20.
go back to reference Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408CrossRef Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408CrossRef
21.
go back to reference Marti A, Martinez-Gonzalez MA, Martinez JA (2008) Interaction between genes and lifestyle factors on obesity. Proc Nutr Soc 67:1–8CrossRef Marti A, Martinez-Gonzalez MA, Martinez JA (2008) Interaction between genes and lifestyle factors on obesity. Proc Nutr Soc 67:1–8CrossRef
22.
go back to reference Martinez JA (2006) Mitochondrial oxidative stress and inflammation: an slalom to obesity and insulin resistance. J Physiol Biochem 62:303–306 Martinez JA (2006) Mitochondrial oxidative stress and inflammation: an slalom to obesity and insulin resistance. J Physiol Biochem 62:303–306
23.
go back to reference Matsuzawa-Nagata N, Takamura T, Ando H, Nakamura S, Kurita S, Misu H, Ota T, Yokoyama M, Honda M, Miyamoto K, Kaneko S (2008) Increased oxidative stress precedes the onset of high-fat diet-induced insulin resistance and obesity. Metabolism 57:1071–1077CrossRef Matsuzawa-Nagata N, Takamura T, Ando H, Nakamura S, Kurita S, Misu H, Ota T, Yokoyama M, Honda M, Miyamoto K, Kaneko S (2008) Increased oxidative stress precedes the onset of high-fat diet-induced insulin resistance and obesity. Metabolism 57:1071–1077CrossRef
24.
go back to reference Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419CrossRef Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419CrossRef
25.
go back to reference Mera RTH, Prasad C (1998) How to calculate sample size for an experiment: a case-based description. Nutr Neurosci 1:87–91 Mera RTH, Prasad C (1998) How to calculate sample size for an experiment: a case-based description. Nutr Neurosci 1:87–91
26.
go back to reference Milagro FI, Campion J, Martinez JA (2007) 11-beta Hydroxysteroid dehydrogenase type 2 expression in white adipose tissue is strongly correlated with adiposity. J Steroid Biochem Mol Biol 104:81–84CrossRef Milagro FI, Campion J, Martinez JA (2007) 11-beta Hydroxysteroid dehydrogenase type 2 expression in white adipose tissue is strongly correlated with adiposity. J Steroid Biochem Mol Biol 104:81–84CrossRef
27.
go back to reference Mohanty P, Ghanim H, Hamouda W, Aljada A, Garg R, Dandona P (2002) Both lipid and protein intakes stimulate increased generation of reactive oxygen species by polymorphonuclear leukocytes and mononuclear cells. Am J Clin Nutr 75:767–772 Mohanty P, Ghanim H, Hamouda W, Aljada A, Garg R, Dandona P (2002) Both lipid and protein intakes stimulate increased generation of reactive oxygen species by polymorphonuclear leukocytes and mononuclear cells. Am J Clin Nutr 75:767–772
28.
go back to reference Mohanty P, Hamouda W, Garg R, Aljada A, Ghanim H, Dandona P (2000) Glucose challenge stimulates reactive oxygen species (ROS) generation by leucocytes. J Clin Endocrinol Metab 85:2970–2973CrossRef Mohanty P, Hamouda W, Garg R, Aljada A, Ghanim H, Dandona P (2000) Glucose challenge stimulates reactive oxygen species (ROS) generation by leucocytes. J Clin Endocrinol Metab 85:2970–2973CrossRef
29.
go back to reference Natella F, Ghiselli A, Guidi A, Ursini F, Scaccini C (2001) Red wine mitigates the postprandial increase of LDL susceptibility to oxidation. Free Radic Biol Med 30:1036–1044CrossRef Natella F, Ghiselli A, Guidi A, Ursini F, Scaccini C (2001) Red wine mitigates the postprandial increase of LDL susceptibility to oxidation. Free Radic Biol Med 30:1036–1044CrossRef
30.
go back to reference OMS-WHO (2000) Obesity: preventing and managing the global epidemic. Report of WHO consultation. Word Health Organ Tech Resp Ser 894:1–253 OMS-WHO (2000) Obesity: preventing and managing the global epidemic. Report of WHO consultation. Word Health Organ Tech Resp Ser 894:1–253
31.
go back to reference Patel C, Ghanim H, Ravishankar S, Sia CL, Viswanathan P, Mohanty P, Dandona P (2007) Prolonged reactive oxygen species generation and nuclear factor-kappaB activation after a high-fat, high-carbohydrate meal in the obese. J Clin Endocrinol Metab 92:4476–4479CrossRef Patel C, Ghanim H, Ravishankar S, Sia CL, Viswanathan P, Mohanty P, Dandona P (2007) Prolonged reactive oxygen species generation and nuclear factor-kappaB activation after a high-fat, high-carbohydrate meal in the obese. J Clin Endocrinol Metab 92:4476–4479CrossRef
32.
go back to reference Perez de Obanos MP, Lopez-Zabalza MJ, Arriazu E, Modol T, Prieto J, Herraiz MT, Iraburu MJ (2007) Reactive oxygen species (ROS) mediate the effects of leucine on translation regulation and type I collagen production in hepatic stellate cells. Biochim Biophys Acta 1773:1681–1688CrossRef Perez de Obanos MP, Lopez-Zabalza MJ, Arriazu E, Modol T, Prieto J, Herraiz MT, Iraburu MJ (2007) Reactive oxygen species (ROS) mediate the effects of leucine on translation regulation and type I collagen production in hepatic stellate cells. Biochim Biophys Acta 1773:1681–1688CrossRef
33.
go back to reference Valerio A, Cardile A, Cozzi V, Bracale R, Tedesco L, Pisconti A, Palomba L, Cantoni O, Clementi E, Moncada S, Carruba MO, Nisoli E (2006) TNF-alpha downregulates eNOS expression and mitochondrial biogenesis in fat and muscle of obese rodents. J Clin Invest 116:2791–2798 Valerio A, Cardile A, Cozzi V, Bracale R, Tedesco L, Pisconti A, Palomba L, Cantoni O, Clementi E, Moncada S, Carruba MO, Nisoli E (2006) TNF-alpha downregulates eNOS expression and mitochondrial biogenesis in fat and muscle of obese rodents. J Clin Invest 116:2791–2798
34.
go back to reference Vincent HK, Taylor AG (2006) Biomarkers and potential mechanisms of obesity-induced oxidant stress in humans. Int J Obes (Lond) 30:400–418CrossRef Vincent HK, Taylor AG (2006) Biomarkers and potential mechanisms of obesity-induced oxidant stress in humans. Int J Obes (Lond) 30:400–418CrossRef
35.
go back to reference Wiswedel I, Hirsch D, Kropf S, Gruening M, Pfister E, Schewe T, Sies H (2004) Flavanol-rich cocoa drink lowers plasma F(2)-isoprostane concentrations in humans. Free Radic Biol Med 37:411–421CrossRef Wiswedel I, Hirsch D, Kropf S, Gruening M, Pfister E, Schewe T, Sies H (2004) Flavanol-rich cocoa drink lowers plasma F(2)-isoprostane concentrations in humans. Free Radic Biol Med 37:411–421CrossRef
36.
go back to reference Zhao G, Etherton TD, Martin KR, Gillies PJ, West SG, Kris-Etherton PM (2007) Dietary alpha-linolenic acid inhibits proinflammatory cytokine production by peripheral blood mononuclear cells in hypercholesterolemic subjects. Am J Clin Nutr 85:385–391 Zhao G, Etherton TD, Martin KR, Gillies PJ, West SG, Kris-Etherton PM (2007) Dietary alpha-linolenic acid inhibits proinflammatory cytokine production by peripheral blood mononuclear cells in hypercholesterolemic subjects. Am J Clin Nutr 85:385–391
Metadata
Title
Tachyphylaxis effects on postprandial oxidative stress and mitochondrial-related gene expression in overweight subjects after a period of energy restriction
Authors
Ana B. Crujeiras
Dolores Parra
Estíbaliz Goyenechea
Itziar Abete
J. Alfredo Martínez
Publication date
01-09-2009
Publisher
D. Steinkopff-Verlag
Published in
European Journal of Nutrition / Issue 6/2009
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-009-0019-9

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