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1 Human Biology and Nutritional Sciences, University of Guelph, Guelph, Ontario, Canada N1G 2W1 and 2 Copenhagen Muscle Research Centre, Rigshospitalet, DK-2200 Copenhagen N, Denmark
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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We examined the net catabolism of two pools of
glycogen, proglycogen (PG) and macroglycogen (MG), in human skeletal
muscle during exercise. Male subjects (n = 21) were
assigned to one of three groups. Group 1 exercised 45 min at
70% maximal O2 uptake (
O2 max) and had muscle biopsies at
rest, 15 min, and 45 min. Group 2 exercised at 85%
O2 max to exhaustion (45.4 ± 3.4 min) and had biopsies at rest, 10 min, and exhaustion. Group
3 performed three 3-min bouts of exercise at 100%
O2 max separated by 6 min of rest.
Biopsies were taken at rest and after each bout. Group 1 had
small MG and PG net glycogenolysis rates (ranging from 3.8 ± 1.0 to 2.4 ± 0.6 mmol glucosyl
units · kg
1 · min1)
that did not change over time. In group 2, the MG
glycogenolysis rate remained low and unchanged over time, whereas the
PG rate was initially elevated (11.3 ± 2.3 mmol glucosyl
units · kg1 · min1) and
declined (P 
0.05) with time. During the first 10 min, PG
concentration ([PG]) declined (P 0.05), whereas MG
concentration ([MG]) did not. Similarly, in group 3, in
both the first and the second bouts of exercise [PG] declined
(P 0.05) and [MG] did not, although by the end of the
second exercise period the [MG] was lower (P 0.05) than
the rest level. The net catabolic rates for PG in the first two
exercises were 22.6 ± 6.8 and 21.8 ± 8.2 mmol glucosyl
units · kg1 · min1, whereas
the corresponding values for MG were 17.6 ± 6.0 and 10.8 ± 5.6. The MG pool appeared to be more resistant to mobilization, and,
when activated, its catabolism was inhibited more rapidly than that of
PG. This suggests that the metabolic regulation of the two
pools must be different.
glycogen; glycogen phosphorylase; carbohydrate; metabolic compartments; repeated exercise; intermittent exercise
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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THE METABOLISM OF MUSCLE GLYCOGEN has been studied in the human for several decades. It has been clearly demonstrated (11, 12, 18) that the net rate of glycogenolysis increases with exercise intensity, and it often decreases with exercise duration. There have been a variety of early reports (23, 26, 34) that glycogen was not a uniform molecule, and it is now clear that glycogen exists in two pools that can be distinguished on the basis of their solubility in acid. Lomako, Whelan, and colleagues (3, 29) were the first to describe these two forms in detail. The acid-soluble pool has a high ratio of carbohydrate to protein, has a maximum mass of ~107 Da, and is termed macroglycogen (MG). The acid-insoluble fraction has the same complement of protein as MG but less carbohydrate, ranges up to 400 kDa, and has been termed proglycogen (PG).
Neither the physiological roles of these two forms nor their metabolic regulation has been established. Fundamental aspects such as whether PG exists as a discrete molecular form or merely represents part of a continuum of molecular sizes from the protein primer, glycogenin, through to a "mature" MG molecule are being debated (33). However, Lomako et al. (29) have suggested that PG is associated with a unique synthase (PG synthase) that is regulated differently from the synthase associated with MG. Two different reports (3, 31) have proposed that generally muscle carbohydrate "oscillates" between the PG and MG forms, implying that MG is commonly the fuel of choice. Melendez et al. (31) supported this concept on the basis of mathematical considerations of the molecules; at its theoretical maximum size, a molecule of PG contains only 6% of the carbohydrate of a MG molecule. Nevertheless, considering that 65-75% of the glycogen is in the PG form in resting human muscle (1, 2, 4), this would be a remarkable situation.
Adamo et al. (2) studied humans after glycogen-depleting exercise. In contrast to the concept that MG might be the most dynamic glycogen pool, they found that there is very little net MG formed in the first 4 h of recovery, and it appeared that initially the muscle selectively synthesized PG. Only when PG approached its normal resting concentration after 24 h was there a net MG accumulation. Ingestion of large amounts of carbohydrate stimulated the rate of PG synthesis far more than the MG synthesis rate. These findings suggest that PG is the most dynamic form of glycogen during recovery from exercise and that its synthesis is regulated differently from that of MG. The only two reports on exercised human muscle (2, 4) have examined PG and MG only at the end of prolonged, exhaustive exercise. There is no information available about the relative rates of glycogenolysis of the two pools during the time course of exercise. Similarly, the responses of PG and MG in different exercise intensities have not been examined.
The purpose of this study is to explore the changes in the two pools under varying metabolic demands, specifically to examine the net changes in the pools with different exercise intensities and durations as well as to investigate the changes that occur during repeated bouts of intense exercise. We hypothesized that the PG pool would be most affected by these metabolic challenges because the PG pool is normally the largest and appears to be more sensitive to carbohydrate ingestion and to be more rapidly restored postexercise.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The experimental protocol was approved by the University of Guelph's Human Subjects Committee. Twenty-one recreationally active men volunteered and gave their written consent as subjects for the study.
Pretrial testing.
Each subject underwent an incremental maximal O2 uptake
(O2 max) test on an electronically
braked cycle ergometer (Quinton Excalibur). This result was used to
predict the power output for the experimental trial. Subsequently, the
subject came to the laboratory on a second occasion to perform this
power output. This served both to habituate the subject to the
experimental protocol and also to confirm that the power output was correct.
Experimental design.
The subjects were randomly assigned to one of three groups
(n = 7) to exercise at either 70, 85, or 100% of
O2 max, referred to in this report
as groups 1, 2, and 3, respectively. Subject characteristics (means ± SE) for groups 1,
2, and 3 (as defined below) were age 24 ± 2.9, 22 ± 0.8, and 20 ± 0.4 yr; height 1.83 ± 0.03, 1.80 ± 0.04, and 1.77 ± 0.02 m; weight 79.9 ± 3.1, 76.6 ± 5.1, and 72.2 ± 1.3 kg; and
O2 max 56.3 ± 3.8, 58.6 ± 3.8, and 55.3 ± 1.6 ml · kg1 · min1,
respectively. After the pretrial testing, all subjects abstained from
exercise for 48 h before testing and reported to the laboratory 2-4 h after a light meal.
O2 max, had muscle
biopsies taken after 15 and 45 min of exercise, and group 2,
who exercised at 85% O2 max, had
muscle biopsies taken after 10 min of exercise and at exhaustion. The
third group performed three 3-min bouts of exercise requiring 100%
O2 max with each exercise separated by
6 min of rest. Muscle biopsies were obtained immediately after each
exercise period. Pulmonary measures of
O2 and respiratory exchange ratio (RER)
(Applied Electrochemical S-3A O2 analyzer and Sensormedics
LB-2 CO2 analyzer) were made periodically during the
exercises. In the trial at 70%
O2 max (group 1), the actual mean pulmonary O2 was
67.9 ± 0.5%
O2 max. For the 85%
O2 max (group 2), the value
was 85.0 ± 2.4%, and, for the three exercise bouts of
group 3, it was 89 ± 1, 100 ± 1.3, and 100 ± 2.5% of O2 max for exercise
bouts 1, 2, and 3, respectively. The data
for the first exercise period for group 3 were significantly
(P 0.05) less than for the subsequent two bouts. In
group 2, the mean time for exhaustion was 45.4 ± 3.4 min.
Analysis.
Muscle samples were rapidly frozen in liquid N2 and then
stored at 
80°C until analyzed. The samples were freeze-dried and dissected free of visible blood and connective tissue. A 1.5- to 3.0-mg
portion was extracted after the MG and PG isolation method
(1) based on solubility in perchloric acid. This was followed by enzymatic measurement of glucosyl units (1,
10). In the assay for MG, all glucose and fructose forms are
measured together with the glucose derived from the MG. Normally, the
concentration of these is very small relative to the MG concentration;
however, during intense exercise, the hexose monophosphate (HMP)
concentration could create an important error in the MG determination.
Thus, for the samples of group 3, the HMP (glucose
1-phosphate, glucose 6-phosphate, and fructose 6-phosphate) and glucose
were assayed (10) in the acid-soluble (or MG) extraction,
and this was subtracted from the total value to derive MG.
Subsequently, the PG and MG data were reported as millimoles glucosyl
units per kilogram dry weight. The concentration of HMP in group
3 rose from a resting level of 4.0 ± 0.6 mmol/kg to
15.2 ± 4.6, 15.4 ± 4.4, and 25.1 ± 5.3 mmol/kg after
the three exercise periods. Thus ignoring the HMP in such extreme
exercise conditions could create an error of up to 27% in MG.
Calculations and statistical analysis. The total glycogen (Gt) in each sample was calculated as the sum of MG and PG. The fraction of Gt that was PG was also calculated. For MG, PG, and Gt, the difference between concentrations in consecutive samples was calculated and expressed as the net rate per minute. When a MG molecule undergoes glycogenolysis, it is not known whether this proceeds only until a PG molecule results or whether all of the glucosyl units are liberated. If the former occurs, MG catabolism would supply molecules to the PG pool, whereas the latter would mean that a PG was transiently formed and then catabolized. The calculation of net PG glycogenolytic rate in this study does not consider this issue and hence is a conservative estimate of the true net breakdown of PG.
Within each group, a one-way ANOVA was used to compare the Gt, PG, and MG concentrations as well as their net glycogenolysis rates within each time period. A Tukey's post hoc test was used to locate significant differences. Concentrations were only compared across groups at rest (one-way ANOVA) to examine whether the groups had similar initial concentrations of glycogen. The PG, MG, and Gt net glycogenolytic rates for the earliest data set for each group (rest to 15 min, rest to 10 min, and rest to 3 min for 70, 85, and 100%O2 max,
respectively) were also compared with a one-way ANOVA, and significant
differences were identified using a Tukey's post hoc test. Within a
given group, the changes in concentration and in net catabolic rate of
each form of glycogen were examined for changes over time with a
one-way ANOVA for repeated measures. Significance was accepted at
P 0.05, and the data cited in the text are means ±SE.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Glycogen concentrations.
The concentrations of Gt, PG, and MG for the three groups
are summarized in Table 1. There were no
differences between groups in any of the concentrations at rest, with
the one exception that the PG concentration for group 1 was
less than that of group 2 (P 0.05). The PG
concentration accounted for 66-77% of the Gt at rest
in the three groups. Within group 1 (70%
O2 max), all three measures of glycogen
decreased significantly (P 0.05) from rest at 15 min.
These measures were also lower (P 0.05) at 45 min than at 15 min of exercise. The one exception was that at 15 min
the PG concentration was not different from that at rest
(P = 0.09).
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O2 max),
both the Gt and PG concentrations were significantly lower
(P 0.05) from rest at 10 min. At exhaustion they were
lower (P 0.05) than either that at rest or that at 10 min. In contrast, the MG concentration was not different (P 
0.05) from rest at 10 min, but at exhaustion it was lower than the
concentration at rest as well as that at 10 min of exercise. The
responses of group 3 (three bouts of exercise at 100%
O2 max) also suggested that the PG pool
was more dynamic. After the first exercise bout, the MG concentration
was not lower (P 0.05) than at rest. Similarly, the
second bout of exercise did not lower the MG concentration below that
of the first exercise (P 0.05), although it was less than
the MG at rest (P 0.05). In contrast, the Gt
and PG concentrations decreased significantly (P 0.05) during the first bout, and after the second exercise they were also
significantly (P 0.05) lower than the corresponding
values either at rest or after the first exercise. At the end of the third exercise bout, Gt, PG, and MG concentrations were not
different (P 0.05) from their respective values at the
end of the second workload.
Net glycogenolytic rates within each exercise intensity.
The net rates of glycogenolysis for Gt, PG, and MG for
groups 1 and 2 are summarized in Fig.
1. For group 1, the rates were small for Gt, PG, and MG, and they did not change
significantly over time. In addition, there were no differences
(P 0.05) between the net rates for MG (3.8 ± 1.0 and 1.8 ± 0.5 mmol glucosyl
units · kg1 · min1 for
0-15 and 15-45 min, respectively) and those of PG
(corresponding data were 2.9 ± 1.1 and 2.4 ± 0.6 mmol
glucosyl
units · kg1 · min1) or that
of Gt (6.7 ± 2.0 and 4.2 ± 1.0 mmol
glucosyl
units · kg1 · min1,
respectively) within either time period.
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0.05) between 0-10 min
and 10 min to exhaustion (mean net rates were 2.3 ± 1.2 and
1.7 ± 0.3 mmol glucosyl
units · kg1 · min1,
respectively). In contrast, the net rate for PG was greater (P 0.05) than that for MG in each time period and also
decreased (P 0.05) over time. The corresponding data were
11.3 ± 2.3 and 3.7 ± 0.7 mmol glucosyl
units · kg1 · min1. The net
Gt rate also tended (P = 0.09) to decrease
over time. The net Gt rate for the first 10 min
(12.6 ± 3.2 mmol glucosyl units · kg1 · min1) was
approximately double that observed in the first 15 min for group
1 (i.e., 70% O2 max). In
group 2, the net PG rate in the first 10 min was 90% of the
net Gt rate, whereas in group 1 the net PG rate
for the first 15 min was only 43% of the net Gt rate.
The net glycogenolytic rates in the three exercise bouts at 100%
O2 max (group 3) are
summarized in Fig. 2. The net Gt rate was lower (P 0.05) in the third
exercise bout compared with the first (40.2 ±7.0 vs. 1.7 ± 6.6 mmol glucosyl
units · kg1 · min1,
respectively). The net MG rate tended (P = 0.06) to
decline between each exercise period. In fact, during the second
exercise, three subjects had a negative net MG rate, indicating a net
MG synthesis. In the third bout, five of the seven subjects had a negative value, and the mean net MG rate was 2.3 ± 2.8 mmol
glucosyl units · kg1 ·min1.
Although the difference between net MG and PG rates was not significant
(P > 0.05) at any time point, the net MG rate
decreased by 39% from the first exercise to the second (from 17.6 ± 6.0 to 10.8 ± 5.6 mmol glucosyl
units · kg1 · min1). In
contrast, the PG net rate was virtually constant (22.6 ± 6.8 and
21.8 ± 8.2 mmol glucosyl
units · kg1 · min1,
respectively) in these two exercise periods. In the second exercise period, the MG rate was <50% of the corresponding PG rate. The mean
net PG rate showed a marked drop in the third exercise, but the decline
was not significant. During this latter exercise period, four subjects
had net negative PG rates, and all of these four also had net negative
MG rates. It is interesting that, despite the high work intensity, by
the second work bout the net MG rate was reduced and was similar to
that of the net PG rate in the first 10 min at 85%
O2 max (11.3 ± 2.3 mmol glucosyl units · kg1 · min1).
Similarly, by the third exercise period, the data for net
Gt, PG, and MG rates were among the lowest measured at any
time at any exercise intensity in this study.
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Comparison of the net glycogenolytic rates among the groups during
the early phase of the exercise.
Figure 3 summarizes the initial
glycogenolytic rate data for the three groups. The initial net
Gt rate (Fig. 3) tended to increase with exercise intensity
from 6.7 ± 2.0 to 12.6 ± 3.2 to 40.2 ± 7.0 mmol
glucosyl units · kg1 · min1
in the initial phase of 70, 85, and 100%
O2 max, respectively, and the latter
was significantly (P 0.05) greater than the other two
values. Similarly, the net PG rate tended to increase with exercise
intensity, and the value at 100%
O2 max was greater (P 0.05) than that for 70% O2 max. In
contrast, the net MG rate remained low until 100%
O2 max, when it was greater
(P 0.05) than the data for 70 and 85% of
O2 max.
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O2 max tests and in the third
exercise bout at 100% O2 max. The
suppression of glycogenolysis in the third bout of exercise at 100%
O2 max was not due to low glycogen concentrations; the concentrations of PG and MG before bout
3 were equal to or even greater than those in the lower intensity exercises (Table 1). Linear regression of the resting concentration of
Gt, PG, or MG and the respective initial net glycogenolytic rates within each exercise intensity failed to show any significant relationships (data not shown).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The purpose of this study was to examine the impact of exercise intensity, duration, and repeated bouts of intense exercise on the net rates of catabolism of the two pools of muscle glycogen. The key findings were that 1) there were several situations in which exercise stimulated a significant decline in PG but not in MG; 2) the net rate of glycogenolysis was almost always greater for the PG pool; 3) although the net rates of catabolism increase with exercise intensity, this is most distinct in the PG pool; and 4) when the net rate of glycogenolysis decreases with increased duration of the exercise, this is predominantly due to deceased net rate of catabolism of the MG pool. Thus the data suggest that the two glycogen pools are differentiated not only in terms of acid solubility but also with regard to metabolic regulation. The concept that the glycogen pool generally "oscillates" between MG and PG does not appear to be true during exercise.
Previous work by Adamo et al. (2) clearly showed that
resynthesis of PG after a major depletion of muscle glycogen in humans was regulated very differently from that of MG. PG was resynthesized far faster and was much more sensitive to carbohydrate ingestion. As
such, PG appears to be an important site of anabolic regulation. The
current study offers insight into the catabolic nature of the MG and PG
pools. Alonso et al. (3) speculated that the carbohydrate
stores leave the granule retracing the steps occurring during storage,
i.e., the first glucosyl units to be mobilized would be from MG. They
proposed that the rise and fall of glycogen concentrations first occurs
by oscillations between PG and MG on the basis of their previous
observations (28) that when cultured quail embryonic
muscle was stimulated by phenylephrine, MG was degraded and PG was
generated, increasing PG concentration. Only when there was a greater
catabolic stimulus was the PG also degraded. There was no evidence of
this occurring in the present study; even at the mildest metabolic
demand (70% O2 max), the PG pool was
at least as labile as the MG and catabolism of both pools occurred
simultaneously. There was never a situation in which there was a net
decrease in MG and a rise in PG. On the other hand, there were numerous
situations in which the PG pool was catabolized to a much greater
extent than MG, such that the net MG rate deceased over time and the PG
rate did not. During the initial portion of exercise, at both
85 and 100% O2 max, there was a
significant decline in PG whereas MG did not change. In addition,
during exercise at 85% of O2 max, the
rate of PG catabolism was greater than that for MG and the former
declined with time whereas the latter did not. Although we cannot
address whether PG is a discrete entity or is a range of compounds up to a maximum carbohydrate complement, our results clearly support the
theory that the catabolism of the two pools is regulated differently and that PG is the most labile during moderate and intense exercise.
The literature is controversial regarding the range of molecular sizes of PG and MG (3, 28, 29, 33). Our data do not address this issue, and the interpretation of our results is not dependent on whether PG and MG exist as a single discrete size or exist as a range of sizes. (In fact, because the molecules are degraded during exercise, it is most likely that a range of sizes would exist.) Regardless of the molecular sizes, the present data and those of Adamo et al. (1, 2) clearly illustrate that the two fractions of glycogen found in human muscle can be separated on the basis of acid solubility. In the present study, these two fractions are catabolized at different rates during some exercise metabolic states and were shown previously (2) to be anabolized at different rates during recovery. Thus we conclude that the forms are metabolically important. The actual molecular form of these pools remains to be established.
Previously, various studies have demonstrated in cell cultures (28, 29) and muscle (21) in vitro that, in the process of glycogen synthesis, the transition from PG to MG was a point of regulation. There are also suggestions that glycogen synthase kinetics and regulation are different for MG and PG (17, 29). The present study did not address the activity of glycogen synthase or phosphorylase, but the latter system appears to be more active within the PG pool. Much of the phosphorylase enzyme system is associated with the glycogen granules (24). This binding to glycogen exerts regulatory properties on phosphorylase and its catalytic site. It is possible that the more complex nature of the larger MG molecule results in differences in this binding and hence in phosphorylase regulation. This may be a result of the higher degree of branching in MG and/or a change in the relationships among the various proteins/enzymes that are bound to the granule.
Our data are based on differences in concentration over time and thus are net PG and MG glycogenolytic rates. It is clear from various studies (5, 15, 16, 22, 27, 32) that muscle glycogen is not static but is continually being synthesized and degraded in a substrate cycle both at rest and during exercise. It is likely that such turnover occurs in both PG and MG pools, but it is not known whether the pools have similar turnover rates or whether the turnover rates of the two pools are independent from each other. The preferential catabolism of PG that we have observed could be due to regulation on either "arm" of the cycle within this pool. In other words, the phosphorylase activity could be similar for both PG and MG, but the synthase activity is greater for MG. We feel that this is unlikely because it would require that the substrate cycling in each pool would have to accelerate with exercise intensity. Although glycogen synthase activity has been shown (14, 22) to increase above resting levels during very mild, prolonged exercise, it is unlikely that such an energy- requiring process would increase proportionately to that of phosphorylase in high-intensity exercise. Furthermore, the reports (3, 17) in which PG and MG synthase activity has been studied suggest that PG synthase is more active. Thus it is most likely that the differences in glycogen catabolism are due to the phosphorylase activity.
One could argue that the differences in catabolism are due to the
differences in concentration; i.e., 66-77% of the Gt
was PG, and, thus, if the muscle glycogen phosphorylase is activated, there should be approximately three times more PG catabolized. However,
the present data demonstrate that the regulation is not so simple. The
relative rates of glycogenolysis of the two pools varied dramatically
under different exercise conditions. It does not appear that the
initial concentrations of PG and MG are important regulators of
glycogenolysis within the conditions of this study. Although the range
of PG and MG concentrations was small, linear regression of net rate of
catabolism did not demonstrate a significant relationship with their
initial concentration within any power output. Furthermore, there were
times (e.g., 70% O2 max) when the
catabolic rates of PG and MG were similar. There were circumstances
when they are very different (e.g., first 10 min at 85%
O2 max) and times when they were
similar initially (e.g., first work bout at 100%
O2 max), but later (bouts 2 and 3) they appeared to be quite different.
With increasing exercise intensity, there is a progressive recruitment of type II fibers (20, 35, 36). It is also possible that the MG of type II fibers is more labile than that of type I and thus only when these fibers are active is there a large MG catabolism. This possibility has not been studied.
We did not sample muscle before the second and third bouts of exercise for group 3, and it is possible that some glycogen resynthesis occurred during the 6 min of rest. This would potentially mask an actual catabolism during the following exercise bout. However, on the basis of the work by Adamo et al. (2), one would predict that any such resynthesis would occur in the PG pool, and it was the MG pool that showed the smallest responses. Thus this possibility is unlikely to mask decreases in MG. Furthermore, Bangsbo et al. (6, 7, 9) have repeatedly shown that there is minimal resynthesis from either blood glucose or muscle lactate during this brief time.
As others have reported (8, 13, 19, 25, 30), there was a
marked decrease in glycogenolysis with repeated bouts of intense
exercise. The present study increases the understanding of several
aspects of this phenomenon. First, unlike in some of these previous
investigations (13, 30), the power output was the same in
the repeated exercise bouts. Second, the decline in the net
Gt rate in the second work bout was due primarily to
inhibition of MG catabolism, and only in the third exercise period is
net PG catabolism reduced and contributing to the decline in net
Gt catabolism. This Gt decline is not
related to a progressively greater oxidative metabolism given
that the pulmonary O2 was the same in
the final two bouts of exercise. It does not appear that accumulations
of HMP were a key factor; although they were greater in the third bout,
they were very similar in the first two bouts. Finally, the
availability of PG and MG concentrations was not limiting; their
concentrations in exercise bout 3 were similar or perhaps
greater than in the other exercise trials.
In summary, the present study clearly illustrated in human muscle that PG and MG are different glycogen pools and are subject to differences in metabolic regulation during exercise. PG is an important site of regulation, and the PG pool is more dynamic. MG is mobilized by intense exercise and is inhibited more rapidly as exercise continues or is repeated.
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ACKNOWLEDGEMENTS |
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We gratefully acknowledge the excellent technical assistance of P. Sathasivam.
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FOOTNOTES |
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This work was supported by the National Sciences and Engineering Research Council (NSERC) of Canada and by Gatorade. I. Marchand held a NSERC scholarship, and both K. Adamo and J. Shearer held industrial NSERC scholarships in association with Gatorade.
Address for reprint requests and other correspondence: T. E. Graham, Human Biology and Nutritional Sciences, Univ. of Guelph, Guelph, Ontario, Canada N1G 2W1 (E-mail: terrygra{at}uoguelph.ca).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 19 July 2000; accepted in final form 2 October 2000.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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