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Defects in mitochondrial efficiency and H2O2 emissions in obese women are restored to a lean phenotype with aerobic exercise training.

ABSTRACT: The notion that mitochondria contribute to obesity-induced insulin resistance is highly debated. Therefore, we determined whether obese (BMI 33 kg/m(2)), insulin-resistant women with polycystic ovary syndrome had aberrant skeletal muscle mitochondrial physiology compared with lean, insulin-sensitive women (BMI 23 kg/m(2)). Maximal whole-body and mitochondrial oxygen consumption were not different between obese and lean women. However, obese women exhibited lower mitochondrial coupling and phosphorylation efficiency and elevated mitochondrial H2O2 (mtH2O2) emissions compared with lean women. We further evaluated the impact of 12 weeks of aerobic exercise on obesity-related impairments in insulin sensitivity and mitochondrial energetics in the fasted state and after a high-fat mixed meal. Exercise training reversed obesity-related mitochondrial derangements as evidenced by enhanced mitochondrial bioenergetics efficiency and decreased mtH2O2 production. A concomitant increase in catalase antioxidant activity and decreased DNA oxidative damage indicate improved cellular redox status and a potential mechanism contributing to improved insulin sensitivity. mtH2O2 emissions were refractory to a high-fat meal at baseline, but after exercise, mtH2O2 emissions increased after the meal, which resembles previous findings in lean individuals. We demonstrate that obese women exhibit impaired mitochondrial bioenergetics in the form of decreased efficiency and impaired mtH2O2 emissions, while exercise effectively restores mitochondrial physiology toward that of lean, insulin-sensitive individuals.

SUBMITTER: Konopka AR

PROVIDER: S-EPMC4439568 | biostudies-literature | 2015 Jun

REPOSITORIES: biostudies-literature

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Defects in mitochondrial efficiency and H2O2 emissions in obese women are restored to a lean phenotype with aerobic exercise training.

Konopka Adam R AR Asante Albert A Lanza Ian R IR Robinson Matthew M MM Johnson Matthew L ML Dalla Man Chiara C Cobelli Claudio C Amols Mark H MH Irving Brian A BA Nair K S KS

Diabetes 20150120 6

The notion that mitochondria contribute to obesity-induced insulin resistance is highly debated. Therefore, we determined whether obese (BMI 33 kg/m(2)), insulin-resistant women with polycystic ovary syndrome had aberrant skeletal muscle mitochondrial physiology compared with lean, insulin-sensitive women (BMI 23 kg/m(2)). Maximal whole-body and mitochondrial oxygen consumption were not different between obese and lean women. However, obese women exhibited lower mitochondrial coupling and phosph ...[more]

PMID: 25605809

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Project description:Regular, moderate exercise modifies the gut microbiome and contributes to human metabolic and immune health. The microbiome may exert influence on host physiology through the microbial production and modification of metabolites (xenometabolites); however, this has not been extensively explored. We hypothesized that 6 weeks of supervised, aerobic exercise 3×/week (60%-75% heart rate reserve [HRR], 30-60 min) in previously sedentary, lean (n = 14) and obese (n = 10) adults would modify both the fecal and serum xenometabolome. Serum and fecal samples were collected pre- and post-6 week intervention and analyzed by liquid chromatography/tandem mass spectrometry (LC-MS/MS). Linear mixed models (LMMs) identified multiple fecal and serum xenometabolites responsive to exercise training. Further cluster and pathway analysis revealed that the most prominent xenometabolic shifts occurred within aromatic amino acid (ArAA) metabolic pathways. Fecal and serum ArAA derivatives correlated with body composition (lean mass), markers of insulin sensitivity (insulin, HOMA-IR) and cardiorespiratory fitness ( V̇O2max$$ \dot{\mathrm{V}}{\mathrm{O}}_{2\max } $$ ), both at baseline and in response to exercise training. Two serum aromatic microbial-derived amino acid metabolites that were upregulated following the exercise intervention, indole-3-lactic acid (ILA: fold change: 1.2, FDR p < 0.05) and 4-hydroxyphenyllactic acid (4-HPLA: fold change: 1.3, FDR p < 0.05), share metabolic pathways within the microbiota and were associated with body composition and markers of insulin sensitivity at baseline and in response to training. These data provide evidence of physiologically relevant shifts in microbial metabolism that occur in response to exercise training, and reinforce the view that host metabolic health influences gut microbiota population and function. Future studies should consider the microbiome and xenometabolome when investigating the health benefits of exercise.

Project description:Background and aimsTo determine the comparative efficacy of resistance, aerobic, and combined resistance plus aerobic exercise on cardiovascular disease (CVD) risk profile.MethodsThis randomized controlled trial enrolled 406 adults aged 35-70 years with overweight or obesity and elevated blood pressure. Participants were randomly assigned to resistance (n = 102), aerobic (n = 101), combined resistance plus aerobic exercise (n = 101), or no-exercise control (n = 102). All exercise participants were prescribed 1 h of time-matched supervised exercise (the combination group with 30 min of each resistance and aerobic exercise) three times per week for 1 year. The primary outcome was the change from baseline to 1 year in the standardized composite Z-score of four well-established CVD risk factors: systolic blood pressure, low-density lipoprotein (LDL) cholesterol, fasting glucose, and per cent body fat.ResultsAmong 406 participants (53% women), 381 (94%) completed 1-year follow-up. Compared with the control group, the composite Z-score decreased at 1 year, which indicates improved CVD risk profile, in the aerobic {mean difference, -0.15 [95% confidence interval (CI): -0.27 to -0.04]; P = .01} and combination [mean difference, -0.16 (95% CI: -0.27 to -0.04); P = .009] groups, but not in the resistance [mean difference, -0.02 (95% CI: -0.14 to 0.09); P = .69] group. Both aerobic and combination groups had greater reductions in the composite Z-score compared with the resistance group (both P = .03), and there was no difference between the aerobic and combination groups (P = .96). Regarding the four individual CVD risk factors, only per cent body fat decreased in all three exercise groups at 1 year, but systolic blood pressure, LDL cholesterol, and fasting glucose did not decrease in any exercise groups, compared with the control group.ConclusionsIn adults with overweight or obesity, aerobic exercise alone or combined resistance plus aerobic exercise, but not resistance exercise alone, improved composite CVD risk profile compared with the control.

Dataset Information

Defects in mitochondrial efficiency and H2O2 emissions in obese women are restored to a lean phenotype with aerobic exercise training.

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Defects in mitochondrial efficiency and H2O2 emissions in obese women are restored to a lean phenotype with aerobic exercise training.

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