Basic nutritional investigationHigh-fat diets rich in ω-3 or ω-6 polyunsaturated fatty acids have distinct effects on lipid profiles and lipid peroxidation in mice selected for either high body weight or leanness
Introduction
Oxidative stress characterizes an imbalance between the systemic appearance of reactive oxygen species (ROS) and the ability of a biological system to readily detoxify the reactive intermediate products or to repair the resulting damage. Oxidative stress induced by high-fat diets (HFDs) and the resulting lipid peroxidation combined with the formation of lipid peroxides have been associated with a range of diseases, such as type 2 diabetes mellitus, arteriosclerosis, Alzheimer's disease, and cancer [1], [2]. Furthermore, the amount of dietary fat intake and the composition of the dietary fat can influence the onset and/or progression of cardiovascular disease and other health outcomes [3]. There is compelling evidence for the benefits of dietary ω-3 long-chain polyunsaturated fatty acid (ω-3 PUFA) on inflammation and metabolic and cardiovascular health. Urgent attention is therefore needed to advance the knowledge of how fatty-acid compositions of our diets influence long-term health. The trends in Western diets, combined with a shift toward higher intake of vegetable oils rich in ω-6 PUFA, have resulted in an overall increase in total fat intake [4], [5]. Dietary and de novo synthesized ω-3 and ω-6 PUFA in body tissues are highly susceptible to lipid peroxidation by ROS originating from endogenous or exogenous sources. Although antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GPx) reduce the cellular damage caused by common free radicals in the body, the activity of these antioxidant enzymes is significantly diminished as adipose tissue increases [6]. Furthermore, high ROS production and a decrease in antioxidant capacity lead to damage of biomolecules directly or initiate chain reactions, in which ROS are passed from one molecule to another, resulting in extensive damage to lipids and proteins and thus impairing normal cell structure and function [6], [7], [8]. Mice from long-term selection lines offer unique models for studying influences of genetic factors in determining specific dietary effects on oxidative stress induced by HFDs and tissue lipid peroxidation. Increased formation of ROS has been observed in various tissues from mice fed HFD [9], [10]. Additionally, some studies have shown that high-fat and high-cholesterol–containing diets also promote oxidative stress in mice through formation of lipid peroxides [10], [11]. Mice lines with distinct biological traits, that is, the high body weight (DU6) obesity-prone mice and the high treadmill performance (DUhTP) lean mice, were generated by long-term selection from a common genetic pool of outbred mice (DUK) [12], [13], [14]. Recently, we described the metabolic responses to an HFD rich in either ω-3 or ω-6 PUFA on the insulin-signaling pathways in liver, muscle, and abdominal adipose tissue in DU6 and DUhTP mice [15]. The specific metabolic responses in body tissues to an HFD enriched with either ω-3 or ω-6 PUFA differed markedly between the two selection lines despite similar calorie intake.
The aim of this study was to investigate lipid peroxidation and fatty-acid profiles of muscle tissue and the responses to HFDs rich in either ω-3 or ω-6 PUFA in DU6 obesity-prone mice and DUhTP lean mice with distinct biological traits and compare them with the unselected control DUK line. We hypothesize that a higher overall antioxidant capacity in muscle tissue of obesity-prone DU6 mice may ameliorate the ROS formation in response to an ω-3 PUFA-rich HFD compared with the response observed in lean DUhTP mice. The work presented here advances the understanding of metabolic responses to HFDs rich in ω-3 and ω-6 PUFA and will show whether dietary changes influence muscle lipid peroxidation that could, in turn, influence long-term health outcomes.
Section snippets
Materials
Animals: Ninety male mice of different long-term selected lines and three dietary treatments were used in this study. A portion of this mice experiment investigating different endocrine and metabolic responses of ω-3 and ω-6 PUFA-rich HFDs has been described previously [15]. The study was conducted at the Mouse Laboratory of the Leibniz Institute for Farm Animal Biology in Dummerstorf, Germany. Thirty DU6 obesity-prone mice were selected for high body weight at day 42 of life for 128
Oxidative stability of muscle homogenates
For evaluating the stability of quadriceps femoris muscle samples against stimulated lipid peroxidation, the determination of thiobarbituric acid reactive substances (TBARS) was used. Lipid peroxidation can be induced and enhanced by employing systems containing pro-oxidants like Fe2+/ascorbate. The possibility of a muscle homogenate to slow the formation of peroxidative degradation products in such systems is an indication of its antioxidant capacity. The TBARS assay procedure was described
Results
All animals were fed an HFD rich in either ω-3 or ω-6 PUFA or a standard chow diet during the entire experimental period from day 29 to 87 of life (58 d). The extent of lipid peroxidation measured by the TBARS in M. quadriceps femoris (consisting of rectus femoris, vastus medialis, v. intermedius, and v. lateralis) of DU6, DUhT,P and DUK mice was influenced by both the selected mice lines and the dietary treatment (Table 2, Fig. 1). Figure 1 shows the TBARS as an indicator of lipid peroxidation
Discussion
The present study describes lipid peroxidation and fatty-acid concentrations in quadriceps femoris muscle of mice selected for either DU6 obesity-prone mice, or DUhTP lean mice, and unselected (DUK) control mice, fed high fat diets rich in ω-3 or ω-6 PUFA compared with a standard chow diet. The degree of lipid peroxidation in the muscle of mice fed ω-3 and ω-6 PUFA-rich HFDs in the present study was influenced by both the different selection lines and the type of HFD. Surprisingly, the
Acknowledgments
Acknowledgment is made to the staff of the Mouse Laboratory, Leibniz Institute for Farm Animal Biology, for conducting the mice feeding experiment (U. Renne, M. Langhammer, and staff) and B. Jentz and M. Dahm of the Department of Muscle Biology and Growth, Leibniz Institute for Farm Animal Biology, who collected samples and collaborated in the sample preparation, GC, and spectrophotometric measurements. B.H. Breier was supported by the Health Research Council of New Zealand and the National
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K. Nuernberg (KN), D. Dannenberger (DD), B. Breier (BB), G. Nuernberg (GN), and K. Huber (KH) participated in the formulation and design of the diet experiment. U. Renne (UR) and M. Langhammer (ML) participated in production of different mice lines and conducted the high-fat diet feeding experiment, including sampling. DD and KN performed the fatty-acid analysis and lipid peroxidation assays. GN performed the statistical analysis of the data. DD, KH, KN, and BH developed the manuscript in its final form. All authors read and approved the final version of the manuscript.