Subcellular localization-dependent decrements in skeletal muscle glycogen and mitochondria content following short-term disuse in young and old men

2010 ◽  
Vol 299 (6) ◽  
pp. E1053-E1060 ◽  
Author(s):  
Joachim Nielsen ◽  
Charlotte Suetta ◽  
Lars G. Hvid ◽  
Henrik D. Schrøder ◽  
Per Aagaard ◽  
...  

Previous studies have shown that skeletal muscle glycogen and mitochondria are distributed in distinct subcellular localizations, but the role and regulation of these subcellular localizations are unclear. In the present study, we used transmission electron microscopy to investigate the effect of disuse and aging on human skeletal muscle glycogen and mitochondria content in subsarcolemmal (SS), intermyofibrillar (IMF), and intramyofibrillar (intra) localizations. Five young (∼23 yr) and five old (∼66 yr) recreationally active men had their quadriceps muscle immobilized for 2 wk by whole leg casting. Biopsies were obtained from m. vastus lateralis before and after the immobilization period. Immobilization induced a decrement of intra glycogen content by 54% ( P < 0.001) in both age groups and in two ultrastructurally distinct fiber types, whereas the content of IMF and SS glycogen remained unchanged. A localization-dependent decrease ( P = 0.03) in mitochondria content following immobilization was found in both age groups, where SS mitochondria decreased by 33% ( P = 0.02), superficial IMF mitochondria decreased by 20% ( P = 0.05), and central IMF mitochondria remained unchanged. In conclusion, our findings demonstrate a localization-dependent adaptation to immobilization in glycogen and mitochondria content of skeletal muscles of both young and old individuals. Specifically, this suggests that short-term disuse preferentially affects glycogen particles located inside the myofibrils and that mitochondria volume plasticity can be dependent on the distance to the fiber border.

1989 ◽  
Vol 66 (1) ◽  
pp. 72-78 ◽  
Author(s):  
L. Martineau ◽  
I. Jacobs

The effects of intramuscular glycogen availability on human temperature regulation were studied in eight seminude subjects immersed in 18 degrees C water for 90 min or until rectal temperature (Tre) decreased to 35.5 degrees C. Each subject was immersed three times over a 3-wk period. Each immersion followed 2.5 days of a specific dietary and/or exercise regimen designed to elicit low (L), normal (N), or high (H) glycogen levels in large skeletal muscle groups. Muscle glycogen concentration was determined in biopsies taken from the vastus lateralis muscle before and after each immersion. Intramuscular glycogen concentration before the immersion was significantly different among the L, N, and H trials (P less than 0.01), averaging 247 +/- 15, 406 +/- 23, and 548 +/- 42 (SE) mmol glucose units.kg dry muscle-1, respectively. The calculated metabolic heat production during the first 30 min of immersion was significantly lower during L compared with N or H (P less than 0.05). The rate at which Tre decreased was more rapid during the L immersion than either N or H (P less than 0.05), and the time during the immersion at which Tre first began to decrease also appeared sooner during L than N or H. The results suggest that low skeletal muscle glycogen levels are associated with more rapid body cooling during water immersion in humans. Higher than normal muscle glycogen levels, however, do not increase cold tolerance.


1974 ◽  
Vol 52 (1) ◽  
pp. 119-122 ◽  
Author(s):  
A. W. Taylor ◽  
J. Stothart ◽  
M. A. Booth ◽  
R. Thayer ◽  
S. Rao

Sixteen healthy male subjects classified as sedentary (8) or active (8), exercised to exhaustion on a bicycle ergometer at a load requiring 70% of their maximal aerobic capacity. Biopsy samples of the vastus lateralis muscle were taken at rest and at the time of fatigue. A 12 week training program increased skeletal muscle glycogen content and branching enzyme activities twofold. The exhaustive submaximal exercise reduced the glycogen levels of the trained group to values similar to the fatigue levels of the non-trained subjects. Skeletal muscle glycogen branching enzyme activities decreased with submaximal exercise to fatigue in all groups. Maximal exercise to fatigue resulted in small increases in the activities of the enzyme. The results of the present study and a previous study (Taylor et al. 1972. Can. J. Physiol. Pharmacol. 50, 411–415) indicate that the activities of the glycogen synthesizing enzymes are highly correlated with the skeletal muscle resting glycogen concentration and the relative fitness of the subjects.


1982 ◽  
Vol 60 (5) ◽  
pp. 634-637 ◽  
Author(s):  
James L. Poland ◽  
Jerry W. Poland ◽  
Richard N. Honey

Though glucocorticoids were previously implicated in the support of myocardial glycogen supercompensation after exercise, it was unclear why skeletal muscle glycogen did not simultaneously supercompensate since it was also exposed to the exercise-induced glucocorticoid increases. The current study shows that glucocorticoids differentially affect cardiac and skeletal muscle glycogen. Following dexamethasone administration (400 μg i.p.) myocardial glycogen peaked at 6 h while glycogen in the soleus, red vastus lateralis, and white vastus lateralis increased more slowly and reached the highest values 17 h postinjection. Concurrently, blood glucose, insulin, and glucagon remained at control levels. Liver glycogen increased within 2 h and continued to rise with a peak value at 17 h. Plasma free fatty acid (FFA) levels increased and remained high throughout the 26-h experimental period. High FFA levels inhibit glycogenolysis and thus could be partially responsible for glucocorticoid-induced glycogen increases. It is postulated that glycogen supercompensation does not readily occur in skeletal muscles after exercise because of the brevity of the corticosterone and FFA increases and the slowness of the skeletal muscle glycogen response to glucocorticoids.


1994 ◽  
Vol 76 (6) ◽  
pp. 2586-2593 ◽  
Author(s):  
J. Cadefau ◽  
H. J. Green ◽  
R. Cusso ◽  
M. Ball-Burnett ◽  
G. Jamieson

To examine whether the metabolic adaptations to short-term training are expressed over a range of submaximal levels of mitochondrial respiration, seven untrained male subjects [maximal O2 uptake (VO2max) = 45.9 +/- 1.9 (SE) ml.kg-1.min-1] performed a progressive three-stage protocol of cycle exercise at 60% (20 min), 79% (20 min), and 92% (11 min) of pretraining VO2max before and after training. Training consisted of 5–6 days of cycling for 2 h/day at 65% VO2max. Muscle tissue rapidly obtained from the vastus lateralis by needle biopsy indicated that training blunted (P < 0.05) the increase in lactate observed at 60% (23.4 +/- 6.5 vs. 12.4 +/- 2.9 mmol/kg dry wt), 79% (48.9 +/- 5.1 vs. 25.6 +/- 5.2 mmol/kg dry wt), and 92% (68.3 +/- 6.4 vs. 41.5 +/- 6.5 mmol/kg dry wt) of VO2max. Training also resulted in a higher phosphocreatine and lower creatine and P(i) concentrations at both 79% (P < 0.05) and 92% (P < 0.05) of VO2max and higher muscle glycogen levels (P < 0.05). These changes were accompanied by small but significant reductions (P < 0.05) in O2 uptake at the two higher exercise intensities. Given that the lactate-to-pyruvate ratio and the calculated free ADP and AMP were also reduced (P < 0.05), it would appear that short-term training results in a tighter metabolic control over a range of mitochondrial respiratory rates.


1999 ◽  
Vol 86 (2) ◽  
pp. 474-478 ◽  
Author(s):  
Sven Asp ◽  
Jens R. Daugaard ◽  
Thomas Rohde ◽  
Kristi Adamo ◽  
Terry Graham

Muscle glycogen remains subnormal several days after muscle damaging exercise. The aims of this study were to investigate how muscle acid-soluble macroglycogen (MG) and acid-insoluble proglycogen (PG) pools are restored after a competitive marathon and also to determine whether glycogen accumulates differently in the various muscle fiber types. Six well-trained marathon runners participated in the study, and muscle biopsies were obtained from the vastus lateralis of the quadriceps muscle before, immediately after, and 1, 2, and 7 days ( days 1, 2, and 7, respectively) after the marathon. During the race, 56 ± 3.8% of muscle glycogen was utilized, and a greater fraction of MG (72 ± 3.7%) was utilized compared with PG (34 ± 6.5%). On day 2, muscle glycogen and MG values remained lower than prerace values, despite a carbohydrate-rich diet, but they had both returned to prerace levels on day 7. The PG concentration was lower on day 1 compared with before the race, whereas there were no significant differences between the prerace PG concentration and the concentrations on days 2 and 7. On day 2 the glycogen concentration was particularly low in the type I fibers, indicating that local processes are important for the accumulation pattern. We conclude that a greater fraction of human muscle MG than of PG is utilized during a marathon and that accumulation of MG is particularly delayed after the prolonged exercise bout. Furthermore, factors produced locally appear important for the glycogen accumulation pattern.


1999 ◽  
Vol 77 (4) ◽  
pp. 300-304 ◽  
Author(s):  
A Ramamani ◽  
M M Aruldhas ◽  
P Govindarajulu

Although reports on sex steroids have implicated them as promoting protein synthesis and also providing extra strength to the skeletal muscle, it remains unclear whether sex steroids affect glycogen metabolism to provide energy for skeletal muscle functions, since glycogen metabolism is one of the pathways that provides energy for the skeletal muscle contraction and relaxation cycle. The purpose of the current study was to show that testosterone and estradiol act differentially on skeletal muscles from different regions, differentially with reference to glycogen metabolism. To study this hypothesis, healthy mature male Wistar rats (90-120 days of age, weighing about 180-200 g) were castrated (a bilateral orchidectomy was performed to test the significance of skeletal muscle glycogen metabolism in the absence of testosterone). One group of castrated rats was supplemented with testosterone (100 µg/100 g body weight, i.m., for 30 days from day 31 postcastration onwards). To test whether estradiol has any effect on male skeletal muscle glycogen metabolism 17beta-estradiol (5 µg/100 g body weight, i.m., for 30 days from day 31 postcastration onwards) was administered to orchidectomized rats. To test whether these sex steroids have any differential effect on skeletal muscles from different regions, skeletal muscles from the temporal region (temporalis), muscle of mastication (masseter), forearm muscle (triceps and biceps), thigh muscle (vastus lateralis and gracilis), and calf muscle (gastrocnemius and soleus) were considered. Castration enhanced blood glucose levels and decreased glycogen stores in skeletal muscle from head, jaw, forearm, thigh, and leg regions. This was accompanied by diminished activity of glycogen synthetase and enhanced activity of muscle phosphorylase. Following testosterone supplementation to castrated rats, a normal pattern of all these parameters was maintained. Estradiol administration to castrated rats did not bring about any significant alteration in any of the parameters. The data obtained suggest a stimulatory effect of testosterone on skeletal muscle glycogenesis and an inhibitory effect on glycogenolysis. Estradiol did not play any significant role in the skeletal muscle glycogen metabolism of male rats.Key words: testosterone, estradiol, skeletal muscle, glycogen metabolism.


1976 ◽  
Vol 231 (2) ◽  
pp. 614-618 ◽  
Author(s):  
RK Conlee ◽  
MJ Rennie ◽  
WW Winder

To test whether skeletal muscle glycogen concentration is related to food consumption, glycogen content was determined in red (R) and white (W) vastus lateralis and in soleus (S) muscles from six groups of ad libitum-fed rats killed at 4-h intervals and from 24-h-fasted animals killed at 0800 and 1600 h. The animal quarters were illuminated between 0700 and 1900 h. Glycogen values exhibited a peak at 0800 h and a nadir at 2000 h. These changes bore no relationship to blood glucose and lactate or plasma free fatty acids, glucagon, insulin, and corticosterone concentrations. Fasting resulted in reductions of glycogen content of 49% (S), 47% (R), and 29% (W) in animals killed at 0800h, but at 1600h changes were only 23% (RY), 17% (W), and 8% (S). The smaller changes at 1600 h were apparently due to lower glycogen levels in the tissues of the fed animals. It was concluded that skeletal muscle exhibits a diurnal variation in glycogen content, and that, contrary to accepted belief, fating significantly alters muscle glycogen concentration.


2002 ◽  
Vol 36 (1) ◽  
pp. 22-29 ◽  
Author(s):  
Corinne Lang ◽  
Markus Schäfer ◽  
Laszlo Varga ◽  
Arthur Zimmermann ◽  
Stephan Krähenbühl ◽  
...  

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