| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Section of Applied Physiology, Department of Internal Medicine, Washington University School of Medicine, St. Louis, Missouri 63110
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Hickner, R. C., J. S. Fisher, P. A. Hansen, S. B. Racette,
C. M. Mier, M. J. Turner, and J. O. Holloszy. Muscle glycogen accumulation after endurance exercise in trained and untrained individuals. J. Appl. Physiol. 83(3):
897-903, 1997.
Muscle glycogen accumulation was determined in six
trained cyclists (Trn) and six untrained subjects (UT) at 6 and either
48 or 72 h after 2 h of cycling exercise at ~75% peak
O2 uptake
(
O2 peak), which terminated with five 1-min sprints. Subjects ate 10 g
carbohydrate · kg
1 · day1
for 48-72 h postexercise. Muscle glycogen accumulation averaged 71 ± 9 (SE) mmol/kg (Trn) and 31 ± 9 mmol/kg (UT) during the first 6 h postexercise (P < 0.01) and 79 ± 22 mmol/kg (Trn) and 60 ± 9 mmol/kg (UT) between 6 and 48 or 72 h postexercise (not significant). Muscle glycogen
concentration was 164 ± 21 mmol/kg (Trn) and 99 ± 16 mmol/kg
(UT) 48-72 h postexercise (P < 0.05). Muscle GLUT-4 content immediately postexercise was threefold
higher in Trn than in UT (P < 0.05)
and correlated with glycogen accumulation rates (r = 0.66, P < 0.05). Glycogen synthase in the
active I form was 2.5 ± 0.5, 3.3 ± 0.5, and 1.0 ± 0.3 µmol · g1 · min1
in Trn at 0, 6, and 48 or 72 h postexercise, respectively;
corresponding values were 1.2 ± 0.3, 2.7 ± 0.5, and 1.6 ± 0.3 µmol · g1 · min1
in UT (P < 0.05 at 0 h). Plasma
insulin and plasma C-peptide area under the curve were lower in Trn
than in UT over the first 6 h postexercise
(P < 0.05). Plasma creatine kinase
concentrations were 125 ± 25 IU/l (Trn) and 91 ± 9 IU/l (UT)
preexercise and 112 ± 14 IU/l (Trn) and 144 ± 22 IU/l
(UT; P < 0.05 vs.
preexercise) at 48-72 h postexercise (normal: 30-200 IU/l).
We conclude that endurance exercise training results in an increased
ability to accumulate muscle glycogen after exercise.
fiber type; GLUT-4; glycogen synthase; glycogen supercompensation
INTRODUCTION MUSCLE GLYCOGEN accumulation and supercompensation have
been extensively studied since the pioneering investigation of
Bergström and Hultman (3). However, there have been few studies
of this process in untrained individuals, and, remarkably, only one
investigation in which a direct comparison of trained and untrained
individuals was made (5). This is surprising not only in light of the
wealth of publications concerning glycogen accumulation in skeletal
muscle but also because of possible insights regarding the glycogen
accumulation process that such a comparison might provide.
Muscle glycogen accumulation has been shown to correlate with the
relative proportion of glycogen synthase in the active (I) form (4,
17). However, the amount of the glucose transporter protein (GLUT-4)
appears to be rate limiting for this process because GLUT-4 content has
been shown to determine the rate of glucose transport into muscle (33).
Untrained individuals have lower levels of GLUT-4 than trained
individuals, and the level of GLUT-4 increases with endurance exercise
training (11, 15, 31). Muscle GLUT-4 content has also been reported to
be correlated with glycogen accumulation rates over the 6 h immediately
after exercise when endurance-trained and physically active subjects are fed a high carbohydrate diet (25). However, there have been no
investigations into whether a correlation exists between muscle GLUT-4
content and muscle glycogen accumulation rates in trained and untrained
individuals.
Recently Nakatani et al. (28) have reported that exercise training that
induces an increase in muscle GLUT-4 content results in a large
increase in the rate and amount of muscle glycogen accumulation after a
glycogen-depleting bout of exercise in rats. In this context, the
purpose of the present investigation was to determine whether a similar
phenomenon is seen in humans. To this end, we compared
endurance-trained cyclists with untrained individuals with respect to
muscle glycogen accumulation rates after glycogen-depleting endurance
exercise.
METHODS
Table 1.
Subject characteristics
Group
n
Age, yr
Height, cm
Weight, kg
Body Fat,
%
LBM, kg
O2 peak, l/min
O2 peak,
ml · kg1 · min1
Trained
6
29.8 ± 2.7
178.3 ± 2.2
73.6 ± 2.9
12.9 ± 2.8
64.1 ± 3.2*
4.4 ± 0.2
59.6 ± 1.6
Untrained
6
29.2 ± 3.9
175 ± 2.7
68.8 ± 1.9
18.8 ± 2.0
55.7 ± 1.1
2.6 ± 0.2
38.3 ± 3.4
Values are means ± SE; n, no. of subjects.
O2 peak, peak
O2 uptake; LBM, lean body mass.
*
P < 0.05.
P < 0.001.
O2 peak) for 2 h,
including a 4-min rest every 30 min. Subjects then performed
five 1-min sprints at a workload that elicited 100%
O2 peak (as
determined during
O2 peak testing). A
3-min rest was allowed between sprints.
The subjects did not exercise during the 2- to 3-day period of recovery
after the glycogen-depletion exercise bouts.
Diet.
Subjects were given a controlled diet for 48 h before, and for 48 or 72 h after, exercise. Subjects ate at hours convenient to their schedule,
except during the 6 h after termination of exercise. During this time,
they ate at 0, 2, and 4 h postexercise. The preexercise diet consisted
of 37 kcal · kg body
weight1 · day1,
plus additional calories equal to estimated caloric expenditure during
exercise-training sessions for the trained individuals. The preexercise
diet consisted of 50% carbohydrate (CHO), 30% fat, and 20% protein.
The postexercise diet, consisting of 80% CHO, 7% fat, and 13%
protein, was designed to result in rapid accumulation of muscle
glycogen stores and provided 10 g CHO · kg body
wt1 · day1.
The diet during the first 6 h postexercise consisted of two-thirds of the carbohydrate for that day, supplying 1.4 g
CHO · kg body weight1 · h1.
The meals at 0, 2, and 4 h postexercise consisted of a beverage containing 75-100 g glucose/meal, cereal and milk, bagels,
raisins, jelly, fruit, and tuna.
Biopsies.
Before initiation of exercise, an incision was made in the vastus
lateralis of the quadriceps femoris muscle after administration of
local anesthesia (2% lidocaine). The biopsy site was draped with
sterile dressing and wrapped with an Ace bandage for the duration of
the exercise session. A biopsy was taken from the vastus lateralis of
the quadriceps femoris muscle immediately after the final sprint. The
biopsy sample was immediately frozen in liquid nitrogen and stored at
80°C for subsequent analysis. A biopsy was also taken from
the vastus lateralis of the quadriceps femoris muscle of the
contralateral leg 6 h after the initiation of eating (which began
within 20 min postexercise), as well as from the vastus lateralis of
the same leg 48 h (6 subjects, 3 trained and 3 untrained) or 72 h (6 subjects, 3 trained and 3 untrained) after initiation of eating. The
study was terminated at 48 h, instead of 72 h, to accommodate the
subjects' schedules because glycogen supercompensation has been shown
to occur within 48 h (3). The 48/72-h biopsies were taken from a site
at least 3 cm distal to the initial biopsy to avoid possible influences of the previous biopsy procedure on muscle glycogen (9). Muscle biopsy
samples were analyzed for glycogen (29), GLUT-4 protein (12), glycogen
synthase (30), and fiber type (6). GLUT-4 concentration was determined
only on the biopsy sample obtained immediately after
exercise.
Blood samples.
Blood samples were drawn immediately before exercise, immediately
before termination of the last 0.5 h ride, immediately after the last sprint, and every 0.5 h after initiation of eating for the
subsequent 6 h. One blood sample was also drawn at 48/72 h postexercise. Blood samples were collected in tubes containing heparin
for determination of plasma glucose by using the glucose oxidase method
(Beckman Instruments, Fullerton, CA) and creatine kinase (CK) by using
the two-site sandwich immunoassay method (Stratus II, Dade
International, Miami, FL), trasylol for determination of insulin (27)
and C peptide (23), reduced glutathione and ethylene
glycol-bis(
-aminoethyl ether)-N, N,
N
, N-tetraacetic acid for catecholamine
determination (34), perchloric acid for lactate (24) and
-hydroxybutyrate (32) analyses, and untreated test tubes for
analysis of serum free fatty acids by using an enzymatic colorometric
procedure (NEFA C kit, Waco Chemicals, Dallas, TX). Samples were
subjected to centrifugation (2,000 g for 15 min), and the supernatant was collected and stored at
80°C for subsequent analyses.
Oxygen uptake.
O2 peak was
determined in each subject at least 3 wk before the glycogen-depleting
exercise. Trained cyclists cycled at 150, 200, and 250 W
for 3 min/exercise intensity, followed by 50- or 25-W increments every
minute until exhaustion. Untrained subjects cycled at 50, 100, and 150 W for 3 min/exercise intensity, followed by 25-W increments every
minute until exhaustion. O2 and
CO2 were continuously monitored by
using a Max 1 on-line system (Fitco: Farmingdale, NY) and averaged
every 30 s for determination of oxygen uptake. Oxygen uptake was
determined for 5 min every 0.5 h during the glycogen-depleting exercise
and for 10 min every hour for 6 h after the exercise.
Body composition.
A modified hydrostatic-weighing procedure by using partial expiration
was employed as described by Kohrt et al. (22). Residual volume was
measured outside the weighing tank by using the oxygen-dilution method
described by Wilmore (36). Percent body fat was estimated by using the
formula of Brozek et al. (7).
Statistics.
Hormone and metabolite data, as well as glycogen concentration data,
were analyzed by using two-way analysis of variance with repeated
measures over time. When significance was attained, post hoc analysis
was performed by using the Student-Newman-Keuls test. Student's
t-test was used to detect differences
between groups with respect to glucose and insulin area under the
curve, lactate concentration, glycogen accumulation rates, and fiber
type. Multiple-regression analysis was performed, as well as analysis
of residuals, by using BMDP software (Los Angeles, CA).
All data are presented as means ± SE.
RESULTS
1 · 6 h1, respectively;
n = 6;
P < 0.01). Muscle glycogen
concentration at 48/72 h postexercise was greater in trained than in
untrained individuals (164 ± 21 vs. 99 ± 16 mmol/kg wet wt;
P < 0.05, n = 6), although the 30% higher rate
of glycogen accumulation between 6 and 48/72 h in trained than in
untrained individuals was not statistically different (78.7 ± 21.8 vs. 60.2 ± 9.0 mmol/kg wet wt). The muscle glycogen concentration
in the trained subjects was 146 ± 38.5 mmol/kg wet weight
(n = 3) at 48 h and 182.1 ± 20.8 mmol/kg wet weight (n = 3) at 72 h
[P = 0.46; not significant (NS)]. The glycogen values for the untrained subjects were 63.4 ± 7.2 mmol/kg wet weight (n = 3)
at 48 h and 134.4 ± 8.6 mmol/kg wet weight
(n = 3) at 72 h
(P < 0.01). Data at the specific
time points of 48 and 72 h should be interpreted with caution because of the small number of subjects in each group
(n = 3); nevertheless, it is clear
that higher levels of glycogen were attained in the trained group.
O2 peak), followed by
5 1-min sprints. Subjects consumed a diet supplying 1.4 g carbohydrate (CHO) · kg body
wt1 · h1
over initial 6 h postexercise. The diet over 48-72 h postexercise, consisting of 80% CHO, 7% fat, and 13% protein, provided 10 g CHO · kg body
wt1 · day1.
* Different from untrained subjects,
P < 0.05.
Muscle GLUT-4 content. Muscle GLUT-4 content in trained and untrained subjects is presented in Fig. 2. Muscle GLUT-4 content was threefold higher in trained than in untrained subjects (P < 0.05) and correlated with glycogen accumulation rates over the initial 6 h after exercise (Fig. 3; r = 0.66; P = 0.05; n = 12), the glycogen level attained at 48/72 h (r = 0.57, P = 0.05; n = 12), and the percentage of type I fibers (Fig. 4; r = 0.64, P < 0.05; n = 10). Data are presented for only 10 subjects in Fig. 4 because it was not possible to perform muscle fiber typing on two of the subjects due to insufficient muscle sample size.
O2 peak, followed by 5 1-min sprints. Subjects then consumed a diet supplying 1.4 g CHO · kg body
wt1 · h1
over initial 6 h postexercise. n, No.
of subjects.
Muscle glycogen synthase activity. Total muscle glycogen synthase activity was not different at 0, 6, and 48/72 h postexercise; therefore, these values were pooled. Total muscle glycogen synthase activity was higher postexercise in the trained than in the untrained subjects (6.0 ± 0.4 vs. 4.4 ± 0.3 mmol · kg
1 · min1;
P < 0.01). The percentage of
glycogen synthase in the I form at 0, 6, and 48 h postexercise was
calculated by using the values for total glycogen synthase at the
corresponding individual time points and were 40.7 ± 6.1, 55.8 ± 8.8, and 17.2 ± 3.1% in trained subjects and 26.0 ± 5.1, 59.8 ± 9.6, and 35.8 ± 6.9% in untrained subjects,
respectively. Muscle glycogen synthase I activity was higher in trained
than in untrained subjects immediately after exercise (2.5 ± 0.5 vs. 1.2 ± 0.3 mmol · kg1 · min1;
P < 0.05; Fig.
5). Glycogen synthase I activity was not
correlated with glycogen accumulation rates over the first 6 h after
exercise (r = 0.52, P = 0.08;
n = 12) but did correlate with the
percentage of type I fibers (r = 0.59, P < 0.05;
n = 10).
O2 peak,
followed by 5 1-min sprints. Subjects consumed a diet supplying 1.4 g
CHO · kg body
wt1 · h1
over initial 6 h postexercise. Diet over 48-72 h postexercise, consisting of 80% CHO, 7% fat, and 13% protein, provided 10 g CHO · kg body
wt1 · day1. * Different
from untrained subjects, P < 0.05.
Fiber type. The percentage of type I fibers was greater in trained (70.3 ± 3.7%) than in untrained (46.4 ± 3.0; P < 0.01, n = 5) subjects, and the percentage of type IIB fibers was less in trained (1.6 ± 0.7%) than in untrained (22.2 ± 3.4%; P < 0.01, n = 5) subjects. There was no difference in the IIA fiber type percent between groups. The percentage of type I fibers was correlated with the rate of glycogen accumulation over the 6 h immediately after cessation of exercise (Fig 6A; r = 0.64, P < 0.05, n = 10). This correlation improved when type I and IIA fibers were combined (Fig 6B; r = 0.72, P < 0.05, n = 10).
O2 peak, followed by 5 1-min sprints. Subjects then consumed a diet supplying 1.4 g
CHO · kg body
wt1 · h1
over initial 6 h postexercise. B:
relationship between percentage of type I and type II muscle fibers and
glycogen accumulation rates over initial 6 h postexercise. Subjects
cycled for 2 h at ~75%
O2 peak, followed by 5 1-min sprints. Subjects then consumed a diet supplying 1.4 g
CHO · kg body
wt1 · h1
over initial 6 h postexercise. n, No.
of subjects.
Hormones and metabolites. Data for plasma insulin, C peptide, and glucose are presented in Figs. 7, A and B, and 8, respectively. Areas under the curves from 0-360 min postexercise were larger in the untrained than in the trained subjects for plasma insulin (31,819 ± 9,618 vs. 9,072 ± 1,468 µU · ml
1 · 6 h1;
P < 0.05) and C peptide (4,355 ± 871 vs. 2,217 ± 144 ng · ml1 · 6 h1;
P < 0.05). There was a
correlation of r = 0.55
(P = 0.06) between the area under the
glucose curves and glycogen accumulation rate over the initial 6 h
after exercise. Plasma glucose values were significantly lower in
trained than in untrained subjects during the first 6 h of recovery
when compared by using a two-way repeated-measures analysis of variance
(Fig. 8). Plasma lactate concentrations immediately after exercise were
5.7 ± 1.3 and 6.9 ± 0.6 mM in trained and untrained subjects,
respectively (P = NS). There were no
significant differences in either norepinephrine or epinephrine
concentrations between trained and untrained subjects (data not shown).
No differences were observed in serum free fatty acid, plasma
-hydroxybutyrate, or plasma lactate concentrations between trained
and untrained subjects in the 6 h immediately after cessation of
exercise (data not shown).
141 min) and
at end of (21 min) endurance cycling exercise, as well as
immediately after final sprint (0 min) and over initial 6 h
postexercise (0-360 min). Values are means ± SE;
n = 6 subjects. Subjects cycled for 2 h at ~75% O2 peak, followed by 5 1-min sprints. Subjects then consumed a diet supplying 1.4 g CHO · kg body
wt1 · h1
over initial 6 h postexercise. B:
plasma C-peptide concentration in trained and untrained subjects
immediately before (141 min) and at end of (21 min)
endurance cycling exercise, as well as immediately after final sprint
(0 min) and over initial 6 h postexercise (0-360 min). Values are
means ± SE; n = 6 subjects.
Subjects cycled for 2 h at ~75%
O2 peak, followed by 5 1-min sprints. Subjects then consumed a diet supplying 1.4 g
CHO · kg body
wt1 · h1
over initial 6 h postexercise.
141 min) and at end of (21 min)
endurance cycling exercise, immediately after final sprint (0 min) and
over initial 6 h postexercise (0-360 min). Values are means ± SE; n = 6 subjects. Subjects cycled
for 2 h at ~75%
O2 peak, followed by 5 1-min sprints. Subjects then consumed a diet supplying 1.4 g
CHO · kg body
wt1 · h1
over initial 6 h postexercise.
CK concentration. Plasma CK concentrations were 125 ± 25 and 91 ± 9 IU/l before exercise and 112 ± 14 and 144 ± 22 IU/l at 48/72 h postexercise in trained and untrained subjects, respectively. Plasma CK values were increased in the untrained subjects 48-72 h postexercise compared with preexercise (P = 0.04); however, these values were not significantly different from those of the trained subjects and were in the normal range of 30-200 IU/l. There was no correlation between plasma CK concentration and the rate of glycogen accumulation at 6 or 48/72 hr after exercise. Oxygen uptake.
O2 peak data are
presented in Table 1. The correlation between
O2 peak and glycogen
accumulation over the initial 6 h after exercise was
r = 0.46 (P = 0.01). A
similar correlation (r = 0.46;
P = 0.01) was found
between O2 peak and
glycogen accumulation over the 48/72 h after exercise. McCoy et al.
(25) have found a correlation between
O2 peak and glycogen
accumulation over the first 6 h after exercise. In the present study,
there also appears to be a relationship between
O2 peak and
glycogen accumulation rate; however, it did not attain statistical
significance.
There was no difference in the oxygen uptake relative to
O2 peak between trained
(72.2 ± 1.3%
O2 peak) and untrained
(73.3 ± 1.9%
O2 peak) subjects
during the endurance ride. The respiratory exchange ratio during the
ride was 0.899 ± 0.014 for trained and 0.942 ± 0.247 for
untrained subjects (NS). Oxygen consumption was 0.397 ± 0.26 l/min
in trained and 0.295 ± 0.29 l/min in untrained subjects (NS) during
the 6 h after exercise. The respiratory exchange ratio was similar in
trained (0.894 ± 0.012) and untrained (0.896 ± 0.032) subjects
during the 6 h after cessation of exercise.
DISCUSSION
Nakatani et al. (28) recently reported that endurance exercise training enhances the rate of muscle glycogen accumulation in rats after exercise. The only previous study of glycogen accumulation in trained and untrained individuals was that of Blom et al. (5), who compared well-trained runners and untrained subjects after a 90- to 120-min run to exhaustion. No difference was observed between trained and untrained subjects with respect to the rates of glycogen accumulation over the first 22 h after exercise. Muscle glycogen levels were lower immediately after exercise in untrained than in trained individuals in that study, which may have resulted in a higher rate of accumulation in the untrained group than would have occurred at a higher initial glycogen level immediately after exercise. This is probably not the cause of the discrepant results between the study of Blom et al. and the present study, however, because the glycogen levels immediately after exercise in the present study were also lower in the untrained than in the trained group.
Studies on rat muscles have shown that glucose transport rates are
correlated with muscle GLUT-4 content (14, 18) and that an increase in
muscle GLUT-4 is associated with an increase in the rate of
insulin-stimulated glycogen synthesis (33). In the present study, the
rate of glycogen accumulation over the 6 h immediately after exercise
was correlated with GLUT-4 concentration, as has been demonstrated
previously by McCoy et al. (25). The data from the present study
furthermore demonstrate that the level of glycogen accumulation
attained at 48-72 h after exercise is also correlated with GLUT-4
concentration. Because the rate of glycogen accumulation and GLUT-4
content were both correlated with percentage of type I fibers in the
present study, it is possible that the difference between trained and
untrained individuals with respect to glycogen accumulation is due to
the different fiber type makeup of the two groups. This is probably not
the case, however, because a recent swimming-training study in rats also demonstrated a higher rate of glycogen accumulation in trained than in untrained rats (28). In support of this interpretation, muscle
glucose uptake was apparently higher in the trained than in the
untrained individuals, as evidenced by the lower plasma glucose despite
lower plasma insulin concentrations in the trained subjects over the 6 h immediately after exercise. There was also a strong tendency
(r= 0.55,
P = 0.06) for the rates of glycogen accumulation to be correlated with the area under the glucose curves
over the initial 6 h after exercise. The higher rate of glycogen
accumulation despite the lower prevailing plasma insulin concentrations
in the trained individuals is impressive and clearly demonstrates the
well-established finding of an enhanced insulin action on glucose
uptake in trained individuals (13, 19, 20, 26), which is probably, at
least in part, because of an increased amount of GLUT-4. The mechanisms
responsible for the increased rate of glycogen accumulation do not
involve differences in the prevailing serum free fatty acid
concentration after exercise because free fatty acid levels were very
similar in the two groups. Plasma catecholamine concentrations were
also not different, ruling out the possibility of reduced
counterregulatory action by these hormones in the trained subjects.
It is widely accepted that glycogen synthase, particularly the amount of this enzyme that is in the I form, is the major determinant of muscle glycogen accumulation after exercise (4). Glycogen synthase I activity in the present study was indeed twofold higher in trained than in untrained subjects immediately after exercise. However, the correlation between glycogen synthase I activity immediately after exercise and glycogen accumulation rates over the initial 6 h after exercise was not statistically significant (P = 0.08). In the present study, GLUT-4 content accounted for 44% of the variance in glycogen accumulation, whereas glycogen synthase I accounted for only 27% of the variance, indicating that muscle GLUT-4 content is more closely associated with glycogen accumulation rates than glycogen synthase I. Further support of the postulation that glycogen synthase is not the major determinant of glycogen accumulation rates after exercise comes from a recent study in rats by Ren et al. (33). Glycogen accumulation rates over the first 4 h after exercise were twofold higher in rats in which muscle GLUT-4 content had been elevated by means of 2 days of swimming training, despite similar glycogen synthase I activity in the swimming-trained and sedentary groups.
Numerous investigations have described the deleterious effects of muscle damage on glycogen accumulation, insulin sensitivity, and GLUT-4 in muscle (1, 8, 21, 35). Muscle damage probably did not result in reduced glycogen accumulation rates in skeletal muscle in the present study, as evidenced by the following findings: 1) exercise on a cycle ergometer has a low eccentric component; 2) the untrained subjects performed a 1-h bout of exercise on the cycle ergometer 3 wk before the glycogen depletion bout of exercise, which would have reduced muscle damage during the subsequent depletion ride (10); 3) although plasma CK values in untrained subjects were higher 48/72 h after exercise compared with preexercise values, these 48/72-h values were not significantly higher than in trained subjects, did not correlate with glycogen accumulation at these time points, and were not out of the normal range. Furthermore, Widrick et al. (35) found that muscle glycogen accumulation was not decreased over the initial 6 h, even after eccentric exercise.
There was no significant difference in accumulation rates between trained and untrained individuals between 6 and 48/72 h. The elevated muscle glycogen concentration at 48/72 h in the trained compared with untrained individuals was therefore mainly because of the difference in glycogen accumulation rates over the initial 6 h after exercise. It can thus be concluded that there was no significant difference in the slow phase of glycogen accumulation between the two groups. Whether this indicates that glycogen supercompensation is a phenomenon relative to "resting" glycogen levels and occurs in both trained and untrained individuals is not possible to determine from this study because preexercise biopsies were not obtained. The mean muscle glycogen concentration of 99 mmol/kg in untrained subjects at 48/72 h postexercise in the present study is not out of the previously reported range of values for resting muscle glycogen in untrained individuals (80-100 mmol/kg) (2, 16); however, the mean muscle glycogen concentration at 72 h postexercise for the three untrained subjects who consumed the diet for 3 days postexercise was ~130 mmol/kg.
We conclude that endurance training results in an increased ability to accumulate muscle glycogen after exercise and that this increase is associated with increased GLUT-4 content in trained muscle. This adaptation to training should be beneficial for performance of daily bouts of glycogen-depleting exercise.
ACKNOWLEDGEMENTS
The authors thank the Staff of the General Clinical Research Center and May Chen for assistance in completing this project.
FOOTNOTES
Address for reprint requests: J. O. Holloszy, Washington Univ. School of Medicine, Dept. of Internal Medicine, Section of Applied Physiology, Campus Box 8113, 4566 Scott Ave., St. Louis, MO 63110 (E-mail: apphyspc{at}im.wustl.edu).
Received 7 January 1997; accepted in final form 9 June 1997.
REFERENCES
| 1. |
Asp, S.,
S. Kristiansen,
and
E. A. Richter.
Eccentric muscle damage transiently decreases rat skeletal muscle GLUT-4 protein.
J. Appl. Physiol.
79:
1338-1345,
1995 |
| 2. | Bergström, J., L. Hermansen, E. Hultman, and B. Saltin. Diet, muscle glycogen and physical performance. Acta Physiol. Scand. 71: 140-150, 1967[Medline]. |
| 3. | Bergström, J., and E. Hultman. Muscle glycogen synthesis after exercise: an enhancing factor localized to the muscle cells in man. Nature 210: 309-310, 1966[Medline]. |
| 4. | Bergström, J., E. Hultman, and A. E. Roch-Norlund. Muscle glycogen synthetase in normal subjects. Scand. J. Clin. Lab. Invest. 29: 231-236, 1972[Medline]. |
| 5. | Blom, P. C. S., D. L. Costill, and N. K. Vollestad. Exhaustive running: inappropriate as a stimulus of muscle glycogen supercompensation. Med. Sci. Sports Exerc. 19: 398-403, 1987[Medline]. |
| 6. | Brooke, M. H., and K. K. Kaiser. Muscle fiber types: how many and what kind? Arch. Neurol. 23: 369-379, 1970[Medline]. |
| 7. | Brozek, J., F. Grande, J. T. Anderson, and A. Keys. Densitometric analysis of body composition: revision of some quantitative assumptions. Ann. NY Acad. Sci. 110: 113-140, 1963. |
| 8. |
Costill, D. L.,
D. D. Pascoe,
W. J. Fink,
R. A. Robergs,
S. I. Barr,
and
D. Pearson.
Impaired muscle glycogen resynthesis after eccentric exercise.
J. Appl. Physiol.
69:
46-50,
1990 |
| 9. |
Costill, D. L.,
D. R. Pearson,
and
W. J. Fink.
Impaired muscle glycogen storage after muscle biopsy.
J. Appl. Physiol.
64:
2245-2248,
1988 |
| 10. | Friden, J., J. Seger, M. Sjostrom, and B. Ekblom. Adaptive response in human skeletal muscle subjected to prolonged eccentric training. Int. J. Sports Med. 4: 177-183, 1983[Medline]. |
| 11. |
Gulve, E. A.,
and
R. J. Spina.
Effect of 7-10 days of cycle ergometer exercise on skeletal muscle GLUT-4 protein content.
J. Appl. Physiol.
79:
1562-1566,
1995 |
| 12. |
Hansen, P. A.,
T. J. McCarthy,
E. N. Pasia,
R. J. Spina,
and
E. A. Gulve.
Effects of ovariectomy and exercise training on muscle GLUT-4 content and glucose metabolism in rats.
J. Appl. Physiol.
80:
1605-1611,
1996 |
| 13. |
Heath, G. W.,
J. R. Gavin III,
J. M. Hinderliter,
J. M. Hagberg,
S. A. Bloomfield,
and
J. O. Holloszy.
Effects of exercise and lack of exercise on glucose tolerance and insulin sensitivity.
J. Appl. Physiol.
55:
512-517,
1983 |
| 14. |
Henriksen, E. J.,
R. E. Bourey,
K. J. Rodnick,
L. Koranyi,
M. A. Permutt,
and
J. O. Holloszy.
Glucose transporter protein content and glucose transport capacity in rat skeletal muscles.
Am. J. Physiol.
259 (Endocrinol. Metab. 22):
E593-E598,
1990 |
| 15. |
Houmard, J. A.,
P. C. Egan,
P. D. Neufer,
J. E. Friedman,
W. S. Wheeler,
R. G. Israel,
and
G. L. Dohm.
Elevated skeletal muscle glucose transporter levels in exercise-trained middle-aged men.
Am. J. Physiol.
261 (Endocrinol. Metab. 24):
E437-E443,
1991 |
| 16. | Hultman, E. Studies on muscle metabolism of glycogen and active phosphate in man with special reference to exercise and diet. Scand. J. Clin. Lab. Invest. 19: 1-63, 1967[Medline]. |
| 17. | Hultman, E., J. Bergström, and A. E. Roche-Norland. Glycogen storage in human skeletal muscle. In: Muscle Metabolism During Exercise, edited by B. Pernow, and B. Saltin. New York: Plenum, 1971, p. 273-288. |
| 18. | Kern, M., J. A. Wells, J. M. Stephens, C. W. Elton, J. E. Friedmann, E. B. Tapscott, P. H. Pekala, and G. L. Dohm. Insulin responsiveness in skeletal muscle is determined by glucose transporter (GLUT-4) protein level. Biochem. J. 270: 397-400, 1990[Medline]. |
| 19. |
King, D. S.,
G. P. Dalsky,
W. E. Clutter,
D. A. Young,
M. A. Staten,
P. E. Cryer,
and
J. O. Holloszy.
Effects of exercise and lack of exercise on insulin sensitivity and responsiveness.
J. Appl. Physiol.
64:
1942-1946,
1988 |
| 20. |
King, D. S.,
G. P. Dalsky,
M. A. Staten,
W. E. Clutter,
D. R. Van Houten,
and
J. O. Holloszy.
Insulin action and secretion in endurance-trained and untrained humans.
J. Appl. Physiol.
63:
2247-2252,
1987 |
| 21. |
Kirwan, J. P.,
R. C. Hickner,
K. E. Yarasheski,
W. M. Kohrt,
B. V. Wiethop,
and
J. O. Holloszy.
Eccentric exercise induces transient insulin resistance in healthy individuals.
J. Appl. Physiol.
72:
2197-2202,
1992 |
| 22. | Kohrt, W. M., M. T. Malley, G. P. Dalsky, and J. O. Holloszy. Body composition of healthy sedentary and trained, young and older men and women. Med. Sci. Sports Exerc. 24: 832-837, 1992[Medline]. |
| 23. | Kuzuya, H., P. M. Blix, D. L. Horwitz, D. F. Steiner, and A. H. Rubenstein. Determination of free and total insulin and C-peptide in insulin treated diabetics. Diabetes 26: 22-29, 1977[Abstract]. |
| 24. |
Lowry, O. H.,
J. V. Passoneau,
F. X. Hasselberger,
and
D. V. Shultz.
Effect of ischemia on known substrates and cofactors of the glycolytic pathway of the brain.
J. Biol. Chem.
239:
18-30,
1964 |
| 25. |
McCoy, M.,
J. Proietto,
and
M. Hargreaves.
Skeletal muscle GLUT-4 and postexercise muscle glycogen storage in humans.
J. Appl. Physiol.
80:
411-415,
1996 |
| 26. |
Mikines, K. J.,
B. Sonne,
P. A. Farrell,
B. Tronier,
and
H. Galbo.
Effect of training on the dose-response relationship for insulin action in men.
J. Appl. Physiol.
66:
695-703,
1989 |
| 27. | Morgan, D. R., and A. Lazarow. Immunoassay of insulin: two antibody system. Diabetes 12: 115-126, 1963. |
| 28. |
Nakatani, A.,
D. H. Han,
P. A. Hansen,
L. A. Nolte,
H. H. Host,
R. C. Hickner,
and
J. O. Holloszy.
Effect of endurance exercise training on muscle glycogen supercompensation in rats.
J. Appl. Physiol.
82:
711-715,
1997 |
| 29. | Passonneau, J. V., and V. R. Lauderdale. A comparison of three methods of glycogen measurement in tissue. Anal. Biochem. 60: 405-412, 1974[Medline]. |
| 30. | Passonneau, J. V., and O. H. Lowry. A collection of enzyme assays. In: Enzymatic Analysis, edited by J. V. Passonneau, and O. H. Lowry. Totowa, NJ: Humana, 1993, p. 268-270. |
| 31. |
Phillips, S. M.,
X. X. Han,
J. J. Green,
and
A. Bonen.
Increments in skeletal muscle GLUT-1 and GLUT-4 after endurance training in humans.
Am. J. Physiol.
270 (Endocrinol. Metab. 33):
E456-E462,
1996 |
| 32. | Pinter, J. K., J. A. Hayaski, and J. A. Watson. Enzymatic assay of glycerol, dihydroxyacetone and glyceraldehyde. Arch. Biochem. Biophys. 121: 404-414, 1967[Medline]. |
| 33. |
Ren, J. M.,
C. F. Semenkovich,
E. A. Gulve,
J. Gao,
and
J. O. Holloszy.
Exercise induces rapid increases in GLUT-4 expression, glucose transport capacity, and insulin-stimulated glycogen storage in muscle.
J. Biol. Chem.
269:
14396-14401,
1994 |
| 34. | Shah, S. D., W. E. Clutter, and P. E. Cryer. External and internal standards in the single isotope derivative (radioenzymatic) assay of plasma norepinephrine and epinephrine in normal human and persons with diabetes mellitus or chronic renal failure. J. Lab. Clin. Med. 106: 624-629, 1985[Medline]. |
| 35. |
Widrick, J. J.,
D. L. Costill,
G. K. McConnell,
D. E. Anderson,
D. R. Pearson,
and
J. J. Zachwieja.
Time course of glycogen accumulation after eccentric exercise.
J. Appl. Physiol.
72:
1999-2004,
1992 |
| 36. |
Wilmore, J. H.
A simplified technique for determination of residual lung volumes.
J. Appl. Physiol.
27:
96-100,
1969 |
This article has been cited by other articles:
|
|
 |
|
  D. S. Battram, J. Shearer, D. Robinson, and T. E. Graham Caffeine ingestion does not impede the resynthesis of proglycogen and macroglycogen after prolonged exercise and carbohydrate supplementation in humans J Appl Physiol, March 1, 2004; 96(3): 943 - 950. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. A. Willey and M. A. F. Singh Battling Insulin Resistance in Elderly Obese People With Type 2 Diabetes: Bring on the heavy weights Diabetes Care, May 1, 2003; 26(5): 1580 - 1588. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. O. Holloszy A forty-year memoir of research on the regulation of glucose transport into muscle Am J Physiol Endocrinol Metab, March 1, 2003; 284(3): E453 - E467. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. S. Fisher, L. A. Nolte, K. Kawanaka, D.-H. Han, T. E. Jones, and J. O. Holloszy Glucose transport rate and glycogen synthase activity both limit skeletal muscle glycogen accumulation Am J Physiol Endocrinol Metab, June 1, 2002; 282(6): E1214 - E1221. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. S. Fisher, R. E. Van Pelt, O. Zinder, M. Landt, and W. M. Kohrt Acute exercise effect on postabsorptive serum leptin J Appl Physiol, August 1, 2001; 91(2): 680 - 686. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. L. Carter, C. Rennie, and M. A. Tarnopolsky Substrate utilization during endurance exercise in men and women after endurance training Am J Physiol Endocrinol Metab, June 1, 2001; 280(6): E898 - E907. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Malenfant, A. Tremblay, E. Doucet, P. Imbeault, J.-A. Simoneau, and D. R. Joanisse Elevated intramyocellular lipid concentration in obese subjects is not reduced after diet and exercise training Am J Physiol Endocrinol Metab, April 1, 2001; 280(4): E632 - E639. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Kawanaka, L. A. Nolte, D.-H. Han, P. A. Hansen, and J. O. Holloszy Mechanisms underlying impaired GLUT-4 translocation in glycogen-supercompensated muscles of exercised rats Am J Physiol Endocrinol Metab, December 1, 2000; 279(6): E1311 - E1318. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. O. Ojuka, L. A. Nolte, and J. O. Holloszy Increased expression of GLUT-4 and hexokinase in rat epitrochlearis muscles exposed to AICAR in vitro J Appl Physiol, March 1, 2000; 88(3): 1072 - 1075. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C.-H. Kuo, D. G. Hunt, Z. Ding, and J. L. Ivy Effect of carbohydrate supplementation on postexercise GLUT-4 protein expression in skeletal muscle J Appl Physiol, December 1, 1999; 87(6): 2290 - 2295. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. W. RYDER, Y. KAWANO, D. GALUSKA, R. FAHLMAN, H. WALLBERG-HENRIKSSON, M. J. CHARRON, and J. R. ZIERATH Postexercise glucose uptake and glycogen synthesis in skeletal muscle from GLUT4-deficient mice FASEB J, December 1, 1999; 13(15): 2246 - 2256. [Abstract] [Full Text]
|
|
|
|
|
|
J. S. Greiwe, R. C. Hickner, P. A. Hansen, S. B. Racette, M. M. Chen, and J. O. Holloszy Effects of endurance exercise training on muscle glycogen accumulation in humans J Appl Physiol, July 1, 1999; 87(1): 222 - 226. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
