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Obesity is associated with a higher incidence of a of diseases, including diabetes, cardiovascular disease, and cancer. Consumption of fast food, trans fatty acids TFAsand fructose—combined with increasing portion sizes and decreased physical activity—has been implicated as a potential contributing factor in the obesity crisis.
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Reductions in insulin sensitivity in conjunction with muscle mitochondrial dysfunction have been reported to occur in many conditions including aging. The objective was to determine whether insulin resistance and mitochondrial dysfunction are directly related to chronological age or are related to age-related changes in body composition.
Twelve young lean, 12 young obese, 12 elderly lean, and 12 elderly obese sedentary adults were studied. Insulin sensitivity was measured by a hyperinsulinemic-euglycemic clamp, and skeletal muscle mitochondrial ATP production rates MAPRs were measured in freshly isolated mitochondria obtained from vastus lateralis biopsy samples using the luciferase reaction. Obese participants, independent of age, had reduced insulin sensitivity based on lower rates of glucose infusion during a hyperinsulinemic-euglycemic clamp.
In contrast, age had no independent effect on insulin sensitivity. However, the elderly participants had lower muscle MAPRs than the young participants, independent of obesity. Elderly participants also had higher levels inflammatory cytokines and total adiponectin. In addition, higher muscle MAPRs were also noted in men than in women, whereas glucose infusion rates were higher in women. The demonstrate that age-related reductions in insulin sensitivity are likely due to an age-related increase in adiposity rather than a consequence of advanced chronological age.
The also indicate that an age-related decrease in muscle mitochondrial function is neither related to adiposity nor insulin sensitivity.
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Of interest, a higher mitochondrial ATP production capacity was noted in the men, whereas the women were more insulin sensitive, demonstrating further dissociation between insulin sensitivity and muscle mitochondrial function. As the population ages, the prevalence of several chronic health problems such as obesity, type 2 diabetes, and cardiovascular disease has risen.
Insulin resistance is recognized as a key factor contributing to the development of both type 2 diabetes and its related cardiometabolic disorders 12. Insulin resistance and impaired glucose tolerance are commonly observed phenomena among elderly adults.
For example, the glucose excursion postprandially is substantially greater and remains elevated longer in nondiabetic elderly adults than in nondiabetic younger adults, which is indicative of age-related declines in insulin sensitivity and glucose tolerance 3.
Age, obesity, and sex effects on insulin sensitivity and skeletal muscle mitochondrial function
Aging is associated with detrimental changes in body composition, which persists even when elderly adults are matched to younger adults for BMI 4. Adiposity, in particular abdominal adiposity, is well accepted as a determinant of insulin resistance and therefore may be a key mediator for the development of age-related insulin resistance. Aging is also associated with reductions in skeletal muscle mitochondrial function. In particular, skeletal muscle mitochondrial ATP production rates MAPRs in elderly people are reduced in vivo in the resting state 8 as well as in vitro in the maximally stimulated state 3.
These age-related reductions in MAPRs have also been associated with concomitant reductions in skeletal muscle mitochondrial enzyme activities 9protein synthesis and expression 310and mtDNA abundance in humans 311 and rodents Of interest, insulin resistance is closely associated with skeletal muscle mitochondrial dysfunction in some 351314 but not in all conditions 15 This close association between muscle mitochondrial dysfunction and insulin resistance has led to the hypothesis that mitochondrial dysfunction could be the basis of insulin resistance 5.
Another equally plausible hypothesis is that insulin resistance causes muscle mitochondrial dysfunction 16 In support of the later hypothesis is the demonstration that, in type 2 diabetic people, muscle MAPR fails to increase in response to physiologically high insulin levels, unlike in nondiabetic people However, it should be recognized that the association between insulin resistance and mitochondrial dysfunction are not consistent.
Furthermore, a recent report also indicated that while a low-calorie diet substantially enhanced insulin sensitivity e. In contrast, in rats, a high-fat diet caused insulin resistance while enhancing mitochondrial biogenesis Together, the from the above studies indicate that the close association between insulin sensitivity and muscle mitochondrial function can be uncoupled, arguing against the hypothesis that insulin resistance causes muscle mitochondrial dysfunction or vice versa.
Age is not only associated with insulin resistance and muscle mitochondrial dysfunction but is also associated with changes in Fat asians sex in Rochester Minnesota composition, which likely contribute to the development of age-related insulin resistance We therefore sought to determine whether the changes in insulin sensitivity and muscle mitochondrial function are secondary to age-related changes in body composition rather than being directly related to chronological age.
We studied 48 lean and obese, young and elderly men and women. Insulin sensitivity was measured using hyperinsulinemic-euglycemic clamp and skeletal muscle mitochondrial function by measuring MAPRs from freshly prepared mitochondria obtained from muscle biopsy samples. The studies demonstrated the impact of not only age and body weight, but also sex on insulin sensitivity and muscle mitochondrial function in humans. There were six men and six women in each group. Participants underwent an initial screening that included a medical history, physical examination, resting electrocardiogram, incremental treadmill test, and biochemical tests of renal, hepatic, hematologic, and metabolic function.
Participants with evidence of diabetes, cardiovascular disease, thyroid dysfunction, or a history of alcohol or substance abuse were excluded. Activity levels were confirmed with a leisure-time activity questionnaire. The study was approved by the institutional review board of the Mayo Foundation, and all participants gave written informed consent.
On a second outpatient visit, each participant underwent a dual-energy X-ray absorptiometry DPX-L; Lunar, Madison, WI examination to determine body composition and an incremental cycle ergometer exercise test to determine peak oxygen uptake peak V o 2as ly described On the evening before each study day, participants were admitted to the Mayo Center of Translational Science Activities Clinical Research Unit at and stayed overnight until the following day.
A retrograde catheter was inserted into a dorsal hand vein for sample collection, and the hand was kept in a heating pad overnight. A second intravenous catheter was placed in the contralateral forearm for infusions. After a standard dinner at and a standardized snack ata fasting state was maintained, except for water, until the end of the inpatient visit. A hyperinsulinemic-euglycemic clamp was performed infusing 1.
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Arterialized venous blood was used to measure glucose levels every 10 min with a Beckman glucose analyzer Fullerton, CA. Baseline samples from the participants were obtained at 0 h and after 3 and 8 h from the contralateral thigh. Plasma levels of amino acids were measured by an HPLC system HPfluorescence detector and cooling system with precolumn o -phthalaldehyde derivatization Total adiponectin and HMW adiponectin concentrations were measured by the human adiponectin double-antibody radioimmunoassay kit Linco Research, St.
Louis, MO. Highly sensitive C-reactive protein hsCRP concentrations were measured on the Hitachi chemistry analyzer by a polystyrene particle—enhanced immunoturbidimetric assay from DiaSorin Stillwater, MN. We measured maximal muscle MAPRs as ly described The tissue was transferred to a glass mortar and homogenized in 20 volumes of buffer A with a motor-driven Teflon pestle.
Several substrates were used to allow for the potential detection of pathway-specific differences among study groups. The SR substrate, for example, delivers electrons to complex II of the respiratory chain, whereas all other substrates used transfer energy predominately to complex I.
GM and PM rely on different transporters to enter mitochondrial and provide fuel to different points of the tricarboxylic acid TCA cycle, whereas KG enters the TCA after interconversion with glutamate.
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PCM processing uses the carnitine-palmitoyl transferase system to enter mitochondria, then undergoes fatty acid oxidation pathway before acetyl CoA units are directed to the TCA cycle. The PPKM substrate provides an energy-rich combination to provide substrates to multiple pathways. Skeletal muscle mtDNA copy s were determined as ly described 16 All data examined for departures from normality and transformations were used as needed. Analyses evaluating the main effects of age young versus elderlyBMI lean versus obeseand sex male versus female were conducted using three-way ANOVA.
Because no ificant interactions were observed, the are reported considering only the main effects. Pair-wise comparisons between groups were made using two sample t tests. Comparisons between baseline and ending values within groups were made using paired t tests. Multiple linear regression models were developed to determine the independent effects of age, BMI, and sex, after adjusting for each other, on insulin sensitivity glucose infusion rate [GIR] and MAPR. As per the study de, our young groups were younger than elderly, and our obese groups had a higher BMI than lean.
However, HMW adiponectin levels were not different between the young and elderly participants. Data are medians minimum, maximum. To convert values for glucose to milligram per deciliter, multiply by To convert values for insulin to micro-units per milliliter, divide by 6. Hyperinsulinemic-euglycemic clamp. A and B show the plasma insulin and glucose concentrations during the 8-h clamp, respectively. C shows that the GIRs required to maintain euglycemia during the 8-h clamp were higher in lean groups than in the obese groups with no effects of age.
D—F show integrated area under the curve AUC for the GIR comparing the young and elderly participants, the lean and obese participants, and men and women, respectively. When obese and lean groups were analyzed separately, we found that with all six substrates, both groups showed a ificant age-related decline in MAPR or similar trend supplementary Fig. Similar trends were also observed when the MAPR data were expressed relative to mitochondrial protein content Fig.
Mitochondrial ATP production rates. Similar trends were also observed when expressed per milligram of mitochondrial mito protein D. Insulin-induced changes in MAPRs. There was no age-related reduction in mtDNA copy s among the obese participants. In addition, there was no sex effect on mtDNA copy s data not shown Fig. Baseline mitochondrial mtDNA copy s assessed using primers and probes directed to cytochrome B normalized to 28 s. In contrast, peak V o 2 was not associated with mtDNA copy data not shown.
Association between peak V o 2 and mitochondrial ATP production rates. A and B display the relationship between peak V o 2 and mitochondrial ATP production rates assessed using the succinate plus rotenone SR and glutamate plus malate GM substrate combinations, respectively. Because no ificant interactions were observed, the are reported for the models considering only the main effects of age, BMI, and sex.
Insulin sensitivity was not associated with age after adjusting for BMI and sex. In contrast, insulin sensitivity was lower in obese compared with lean subjects after adjusting for age and sex and was lower in men compared with women after adjusting for age and BMI.
MAPR were lower in the elderly participants compared with the younger participants for five of the six substrate combinations after adjusting for BMI and sex.
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Interestingly, MAPRs were higher in men than in women after adjusting for age and sex. Since no ificant interactions were observed, the are reported for the model considering only the main effects. The current study determined the effects of age and adiposity on insulin sensitivity and mitochondrial function to further explore whether age-related mitochondrial dysfunction and insulin resistance are direct effects of chronological age or are related to adiposity.
The main findings of the current study are, first, that skeletal MAPRs were higher among the young compared with the elderly participants, independent of obesity or truncal fat.