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Effects of Acute Exercise Combined With Calorie Restriction Initiated Late-in-Life on Insulin Signaling, Lipids, and Glucose Uptake in Skeletal Muscle From Old Rats.

ABSTRACT: We evaluated effects of calorie restriction (CR: consuming 60-65% of ad libitum [AL] intake) initiated late-in-life with or without acute exercise on insulin-stimulated glucose uptake (ISGU) of skeletal muscle by studying four groups of 26-month-old rats: sedentary-AL, sedentary-CR (8-week duration), 3 hours post-exercise (3hPEX)-AL and 3hPEX-CR. ISGU was determined in isolated epitrochlearis muscles incubated ± insulin. Muscles were assessed for signaling proteins (immunoblotting) and lipids (mass spectrometry). ISGU from sedentary-CR and 3hPEX-AL exceeded sedentary-AL; 3hPEX-CR exceeded all other groups. Akt (Ser473, Thr308) and Akt substrate of 160 kDa (AS160; Ser588, Thr642, Ser704) phosphorylation levels tracked with ISGU. Among the 477 lipids detected, 114 were altered by CR (including reductions in 15 of 25 acylcarnitines), and 27 were altered by exercise (including reductions in 18 of 22 lysophosphatidylcholines) with only six lipids overlapping between CR and exercise. ISGU significantly correlated with 23 lipids, including: acylcarnitine 20:1 (r = .683), lysophosphatidylethanolamine19:0 (r = -.662), acylcarnitine 24:0 (r = .611), and plasmenyl-phosphatidylethanolamine 37:5 (r = -.603). Muscle levels of ceramides (a lipid class previously linked to insulin resistance) were not altered by CR and/or exercise nor significantly correlated with ISGU, implicating other mechanisms (which potentially involve other lipids identified in this study) for greater ISGU and Akt and AS160 phosphorylation with these interventions.

SUBMITTER: Oki K

PROVIDER: S-EPMC7176061 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Effects of Acute Exercise Combined With Calorie Restriction Initiated Late-in-Life on Insulin Signaling, Lipids, and Glucose Uptake in Skeletal Muscle From Old Rats.

Oki Kentaro K Arias Edward B EB Kanzaki Makoto M Cartee Gregory D GD

The journals of gerontology. Series A, Biological sciences and medical sciences 20200101 2

We evaluated effects of calorie restriction (CR: consuming 60-65% of ad libitum [AL] intake) initiated late-in-life with or without acute exercise on insulin-stimulated glucose uptake (ISGU) of skeletal muscle by studying four groups of 26-month-old rats: sedentary-AL, sedentary-CR (8-week duration), 3 hours post-exercise (3hPEX)-AL and 3hPEX-CR. ISGU was determined in isolated epitrochlearis muscles incubated ± insulin. Muscles were assessed for signaling proteins (immunoblotting) and lipids (m ...[more]

PMID: 30272137

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Project description:Calorie restriction (CR) and exercise training (EX) are two critical lifestyles for the prevention and treatment of metabolic diseases, such as obesity and diabetes. Brown adipose tissue (BAT) and skeletal muscle (SkM) are two important organs to generate heat. Here we provide detailed transcriptional profiling of these two thermogenic tissues from mice treated with CR and/or EX. We demonstrate the transcriptional reprogramming of BAT and SkM according to CR, but little to EX. Consistent with this, CR induces genes encoding adipokines or myokines alteration in BAT and SkM, respectively. Deconvolution analysis implies differences of subpopulations of myogenic cells, mesothelial cells and endogenic cells in BAT, and demonstrates differences of subpopulations of satellite cells, immune cells and endothelial cells in SkM according to CR or EX. NicheNet analysis, exploring potential inter-organ communication, indicates that BAT and SkM can mutually regulate their fatty acid metabolism and thermogenesis by ligands and receptors. These data comprise an extensive resource for thermogenic tissues molecular responses to CR and/or EX in healthy state. Calorie restriction (CR) and exercise training (EX) are two critical lifestyles for the prevention and treatment of metabolic diseases, such as obesity and diabetes. Brown adipose tissue (BAT) and skeletal muscle (SkM) are two important organs to generate heat. Here we provide detailed transcriptional profiling of these two thermogenic tissues from mice treated with CR and/or EX. We demonstrate the transcriptional reprogramming of BAT and SkM according to CR, but little to EX. Consistent with this, CR induces genes encoding adipokines or myokines alteration in BAT and SkM, respectively. Deconvolution analysis implies differences of subpopulations of myogenic cells, mesothelial cells and endogenic cells in BAT, and demonstrates differences of subpopulations of satellite cells, immune cells and endothelial cells in SkM according to CR or EX. NicheNet analysis, exploring potential inter-organ communication, indicates that BAT and SkM can mutually regulate their fatty acid metabolism and thermogenesis by ligands and receptors. These data comprise an extensive resource for thermogenic tissues molecular responses to CR and/or EX in healthy state.

Project description:1. The interaction of insulin and isometric exercise on glucose uptake by skeletal muscle was studied in the isolated perfused rat hindquarter. 2. Insulin, 10 m-i.u./ml, added to the perfusate, increased glucose uptake more than 10-fold, from 0.3-0.5 to 5.2-5.4 mumol/min per 30g of muscle in hindquarters of fed and 48h-starved rats respectively. In contrast, it did not stimulate glucose uptake in hindquarters from rats in diabetic ketoacidosis. 3. In the absence of added insulin, isometric exercise, induced by sciatic-nerve stimulation, increased glucose uptake to 4 and 3.4 mumol/min per 30g of muscle in fed and starved rats respectively. It had a similar effect in rats with moderately severe diabetes, but it did not increase glucose uptake in rats with diabetic ketoacidosis or in hindquarters of fed rats that had been "washed out" with an insulin-free perfusate. Insulin, at concentrations which did not stimulate glucose uptake in resting muscle, restored the stimulatory effect of exercise in these situations. 4. The stimulation of glucose uptake by exercise was independent of blood flow and the degree of tissue hypoxia; also it could not be reproduced by perfusing resting muscle with a medium previously used in an exercise experiment. 5. At rest glucose was not detectable in muscle cell water of fed and starved rats even when perfused with insulin. In the presence of insulin, a small accumulation of glucose, 0.25 mM, was noted in the muscle of ketoacidotic diabetic rats, suggesting inhibition of glucose phosphorylation, as well as of transport. 6. During exercise, the calculated intracellular concentration of glucose in the contracting muscle increased to 1.1-1.6mM in the fed, starved and moderately diabetic groups. Insulin significantly increased the already high rates of glucose uptake by the hindquarters of these animals but it did not alter the elevated intracellular concentration of glucose. 7. In severely diabetic rats, exercise did not cause glucose to accumulate in the cell in the absence of insulin. In the presence of insulin, it increased glucose uptake to 6.1 mumol/min per 30g of muscle and intracellular glucose to 0.72 mM. 8. The data indicate that the stimulatory effect of exercise on glucose uptake requires the presence of insulin. They suggest that in the absence of insulin, glucose uptake is not enhanced by exercise owing to inhibition of glucose transport into the cell.

Dataset Information

Effects of Acute Exercise Combined With Calorie Restriction Initiated Late-in-Life on Insulin Signaling, Lipids, and Glucose Uptake in Skeletal Muscle From Old Rats.

Publications

Effects of Acute Exercise Combined With Calorie Restriction Initiated Late-in-Life on Insulin Signaling, Lipids, and Glucose Uptake in Skeletal Muscle From Old Rats.

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