British Journal of Nutrition

Human and Clinical Nutrition

Antioxidant enzymes induced by repeated intake of excess energy in the form of high-fat, high-carbohydrate meals are not sufficient to block oxidative stress in healthy lean individuals

Sangbin Lima1, Hyeran Wona1, Yeonghwan Kima1, Miran Janga1, K. R. Jyothia1, Youngseol Kima3, Paresh Dandonaa1a2, Joohun Haa1 and Sung Soo Kima1 c1

a1 Department of Biochemistry and Molecular Biology (BK21 Project), Medical Research Center for Bioreaction to Reactive Oxygen Species and Biomedical Science Institute, School of Medicine, Kyung Hee University, No. 1 Hoegi-dong, Dongdaemun-gu, Seoul 130-701, South Korea

a2 Division of Endocrinology, Diabetes and Metabolism, State University of New York at Buffalo and Kaleida Health, 3 Gates Circle, Buffalo, NY 14209, USA

a3 Department of Endocrinology and Metabolism, School of Medicine, Kyung Hee University, No. 1 Hoegi-dong, Dongdaemun-gu, Seoul 130-701, South Korea

Abstract

It has been reported that high-fat, high-carbohydrate (HFHC) meals increase oxidative stress and inflammation. We examined whether repeated intake of excess energy in the form of HFHC meals alters reactive oxygen species (ROS) generation and the expression levels of antioxidant enzymes and mitochondrial proteins in mononuclear cells, and to determine whether this is associated with insulin resistance. We recruited healthy lean individuals (n 10). The individuals were divided into two groups: one group (n 5) ingested 10878·4 kJ/d (2600 kcal/d; 55–70 % carbohydrate, 9·5–16 % fat, 7–20 % protein) recommended by the Dietary Reference Intake for Koreans for 4 d and the other group (n 5) ingested a HFHC meal containing 14 644 kJ/d (3500 kcal/d). Then, measurements of blood insulin and glucose levels, together with suppressor of cytokine signalling-3 (SOCS-3) expression levels, were performed in both groups. Also, cellular and mitochondrial ROS levels as well as malondialdehyde (MDA) levels were measured. Expression levels of cytosolic and mitochondrial antioxidant enzymes, and mitochondrial complex proteins were analysed. Repeated intake of HFHC meals induced an increase in homeostasis model of assessment-insulin resistance (HOMA-IR), together with an increase in SOCS-3 expression levels. While a single intake of the HFHC meal increased cytosolic and mitochondrial ROS, repeated intake of HFHC meals reduced them and increased the levels of MDA, cytosolic and mitochondrial antioxidant enzymes, and several mitochondrial complex proteins. Repeated intake of HFHC meals induced cellular antioxidant mechanisms, which in turn increased lipid peroxidation (MDA) and SOCS-3 expression levels, induced hyperinsulinaemia and increased HOMA-IR, an index of insulin resistance. In conclusion, excess energy added to a diet can generate detrimental effects in a short period.

(Received October 12 2010)

(Revised March 14 2011)

(Accepted March 14 2011)

(Online publication June 08 2011)

Correspondence:

c1 Corresponding author: S. S. Kim, fax +82 2 959 8168, email sgskim@khu.ac.kr

Footnotes

Abbreviations: COX, cyclo-oxygenase subunit; HFHC, high fat, high carbohydrate; HOMA-IR, homeostasis model of assessment-insulin resistance; KDRI, Dietary Reference Intake for Koreans; mETC, mitochondrial electron transport chain; MNC, mononuclear cells; ND1, NADH dehydrogenase 1; NDUFB, NADH dehydrogenase [ubiquinone] 1β sub-complex subunit; ONOO, peroxynitrite; Prx, peroxiredoxin; Rieske Fe-S, cytochrome bc1 complex subunit; ROS, reactive oxygen species; SDHB, succinate dehydrogenase complex subunit B; SOCS-3, suppressor of cytokine signalling-3; SOD, superoxide dismutase; TBA, thiobarbituric acid; TFAM, mitochondrial transcription factor A

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