J Appl Physiol
91: 1512–1519, 2001.
Postexercise muscle glycogen resynthesis in obese
insulin-resistant Zucker rats
CLINTON R. BRUCE, JONG SAM LEE, AND JOHN A. HAWLEY
Exercise Metabolism Group, School of Medical Sciences, Faculty of Life Sciences,
RMIT University, Bundoora, Victoria 3083, Australia
Received 2 February 2001; accepted in final form 10 May 2001
Bruce, Clinton R., Jong Sam Lee, and John A. Haw-
ley. Postexercise muscle glycogen resynthesis in obese insu-
lin-resistant Zucker rats. J Appl Physiol 91: 1512–1519,
2001.—We determined the effect of an acute bout of swim-
ming (8 ⫻ 30 min) followed by either carbohydrate adminis-
tration (0.5 mg/g glucose ip and ad libitum access to chow;
CHO) or fasting (Fast) on postexercise glycogen resynthesis
in soleus muscle and liver from female lean (ZL) and obese
insulin-resistant (ZO) Zucker rats. Resting soleus muscle
glycogen concentration ([glycogen]) was similar between ge-
notypes and was reduced by 73 (ZL) and 63% (ZO) after
exercise (P ⬍ 0.05). Liver [glycogen] at rest was greater in ZO
than ZL (334 ⫾ 31 vs. 247 ⫾ 16 ␮mol/g wet wt; P ⬍ 0.01) and
fell by 44 and 94% after exercise (P ⬍ 0.05). The fractional
activity of glycogen synthase (active/total) increased imme-
diately after exercise (from 0.22 ⫾ 0.05 and 0.32 ⫾ 0.04 to
0.63 ⫾ 0.08 vs. 0.57 ⫾ 0.05; P ⬍ 0.01 for ZL and ZO rats,
respectively) and remained elevated above resting values
after 30 min of recovery. During this time, muscle [glycogen]
in ZO increased 68% with CHO (P ⬍ 0.05) but did not change
in Fast. Muscle [glycogen] was unchanged in ZL from post-
exercise values after both treatments. After 6 h recovery,
GLUT-4 protein concentration was increased above resting
levels by a similar extent for both genotypes in both fasted
(⬃45%) and CHO-supplemented (⬃115%) rats. Accordingly,
during this time CHO refeeding resulted in supercompensa-
tion in both genotypes (68% vs. 44% for ZL and ZO). With
CHO, liver [glycogen] was restored to resting levels in ZL but
remained at postexercise values for ZO after both treat-
ments. We conclude that the increased glucose availability
with carbohydrate refeeding after glycogen-depleting exer-
cise resulted in glycogen supercompensation, even in the face
of muscle insulin-resistance.
glycogen synthase; GLUT-4; hexokinase; insulin resistance
GLUCOSE TRANSPORT and the subsequent activation of
glycogen synthase are important steps for controlling
the rate of glycogen accumulation in insulin-sensitive
tissue such as skeletal muscle (23, 30, 32). At rest or
after exercise, the primary fate of glucose entering
muscle is conversion to glycogen (9, 16), a reaction
catalyzed by glycogen synthase (23). In the postexer-
cise glycogen-depleted state, glycogen resynthesis pro-
ceeds in a biphasic manner (11). On cessation of exer-
cise there is an increase in the permeability of muscle
Address for reprint requests and other correspondence: J. A. Haw-
ley, School of Medical Sciences, RMIT Univ., PO Box 71, Bundoora,
Victoria 3083, Australia (E-mail: john.hawley@rmit.edu.au).
1512 8750-7587/01 $5.00 Copyright © 2001 the American Physiological Society
to glucose (32) accompanied by a rapid disposal of
glucose into muscle (11). These perturbations com-
bined with the increase in the dephosphorylated (ac-
tive) form of glycogen synthase (37) result in a rapid
resynthesis of muscle glycogen lasting up to 60 min.
As the acute, insulin-independent response wears
off, there is a gradual increase in the phosphorylated
(inactive) state of glycogen synthase, an increase in
insulin sensitivity (3, 4, 11, 12), and a 10–30% slower
(insulin-dependent) period during which glycogen val-
ues return to preexercise resting levels. After exercise
there is a prolonged (up to 18 h) and persistent in-
crease in glucose uptake by skeletal muscle (16, 31, 44).
Reversal of this increase in muscle insulin sensitivity
after exercise occurs simultaneously with muscle gly-
cogen repletion and can be speeded by carbohydrate
feeding or slowed by keeping muscle glycogen content
low by fasting (44). If adequate carbohydrate is sup-
plied throughout the postexercise recovery period,
muscle glycogen stores can be supercompensated to
levels that are higher than the fed sedentary state (4).
The regulation of exercise-stimulated glycogen syn-
thesis in normal, healthy skeletal muscle has been well
documented (for review, see Ref. 17). However, far less
is known about the effects of postexercise glycogen
accumulation in muscle (and liver) that exhibits
chronic insulin resistance. Using nuclear magnetic res-
onance spectroscopy, Shulman et al. (34) provided the
first evidence that muscle glycogen synthesis was im-
paired in individuals with non-insulin-dependent dia-
betes mellitus. Subsequently, Price et al. (28) reported
that, after glycogen-lowering exercise, the insulin-in-
dependent phase of glycogen resynthesis was normal
but the insulin-dependent phase of glycogen accumu-
lation was reduced in the muscle of insulin-resistant
fasted subjects.
To the best of our knowledge, no study has investi-
gated the impact of carbohydrate refeeding on postex-
ercise glycogen accumulation in insulin-resistant mus-
cle. Although such a treatment would be unlikely to
influence the rate of glycogen resynthesis immediately
after exercise, carbohydrate administration has been
shown to reverse the increase in insulin sensitivity
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solely to indicate this fact.
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 POSTEXERCISE GLYCOGEN RESYNTHESIS
that occurs during the slower (insulin-dependent)
phase of glycogen accumulation (44). When combined
with muscle insulin-resistance, carbohydrate refeeding
might be expected to attenuate the normal rate of
glycogen accumulation during this phase. However,
such a hypothesis remains to be tested.
In the present study we used the genetically obese
Zucker rat to determine the impact of insulin resis-
tance on postexercise muscle and liver glycogen resyn-
thesis. Skeletal muscle of the obese Zucker rat exhibits
insulin resistance (18) and decreased insulin-stimu-
lated glucose uptake (5, 43) but normal contraction-
stimulated glucose uptake (2). In addition, the obese
Zucker rat remains hyperinsulinemic and hyperglyce-
mic, even during exercise (38). We hypothesized that,
compared with normal muscle, 1) the rate of glycogen
resynthesis in skeletal muscle from insulin-resistant
rats would be similar during the early, insulin-inde-
pendent phase of recovery with or without carbohy-
drate refeeding, 2) the extent of glycogen accumulation
in the slower (insulin-dependent) phase after carbohy-
drate administration would be attenuated in insulin-
resistant muscle as a result of reversal of the exercise-
induced increase in muscle insulin sensitivity, and 3)
glycogen concentrations would be restored to resting lev-
els but not supercompensated in muscle from insulin-
resistant rats fed carbohydrate throughout recovery.
METHODS
Animal care and overview of experimental design. Female
lean (fa/?; n ⫽ 40) and obese (fa/fa; n ⫽ 40) Zucker rats aged
10–11 wk and weighing ⬃177 and ⬃306 g, respectively, were
obtained from Monash University Animal Services, Victoria,
Australia. Animals were housed two per cage in an environ-
mentally controlled laboratory (temperature 22 ⫾ 1°C, rela-
tive humidity 50 ⫾ 2%) with a 12:12-h light-dark cycle (light
0700–1900). Animals were fed standard rodent chow (67.5%
carbohydrate, 11.7% fat, 20.8% protein; Barastock, Victoria,
Australia), given ad libitum access to water, and familiarized
to laboratory conditions for 1 wk before experimentation. The
Animal Experimentation Ethics Committee of RMIT Univer-
sity approved all experimental procedures.
Animals were assigned to one of six subgroups on the basis
of 1) whether they remained sedentary control (Rest) or were
exercised, 2) whether they were fasted (Fast) or received
carbohydrate (CHO) after exercise, and 3) the time of death
after exercise.
Experimental protocol. At 1700 on the day before an exper-
iment, ZL animals were restricted to 10 g and ZO animals to
12 g of chow (⬃60% of the animals’ average daily food intake
from the previous 7 days). ZL rats were randomly assigned to
one of six experimental groups: sedentary control performing
no exercise (ZL-Rest; n ⫽ 7), fasted and killed immediately
postexercise (ZL-Post; n ⫽ 7), fasted and killed 30 min post-
exercise (ZL-Fast 30; n ⫽ 6), fasted and killed 6 h postexercise
(ZL-Fast 360; n ⫽ 7), CHO supplemented and killed 30 min
postexercise (ZL-CHO 30; n ⫽ 7), and CHO supplemented and
killed 6 h postexercise (ZL-CHO 360; n ⫽ 6). ZO rats were also
assigned to sedentary control performing no exercise (ZO-Rest,
n ⫽ 7), fasted and killed immediately postexercise (ZO-Post;
n ⫽ 7), fasted and killed 30 min postexercise (ZO-Fast 30; n ⫽
6), fasted and killed 6 h postexercise (ZO-Fast 360; n ⫽ 7), CHO
supplemented and killed 30 min postexercise (ZO-CHO 30, n ⫽
J Appl Physiol • VOL 91 • OCTOBER 2001 •
1513
7), and CHO supplemented and killed 6 h postexercise (ZO-
CHO 360; n ⫽ 6).
Exercise and refeeding protocol. The exercise mode chosen
for this study was a swimming protocol, modified from the
procedures previously utilized with rats by other laboratories
(4, 12). Before the commencement of an experiment, all
animals were familiarized to swimming for 10 min/day for 3
days. On the day of an experiment, three animals swam
together in a steel barrel measuring 60 cm in diameter and
filled to a depth of ⬃60 cm. Water temperature was main-
tained at 35 ⫾ 1°C. Rats swam for 8 ⫻ 30-min bouts sepa-
rated by 5-min rest periods during which time they were
dried and placed in their cages. In the case of the ZO animals,
a weight equal to ⬃2.5% of body mass (BM) was attached to
the base of the tail after the first 30-min exercise bout (4) to
compensate for their increased buoyancy. ZO animals swam
with the weight attached for the remaining seven exercise
bouts. Weights were selected so that during the swimming
protocol the body angles relative to the surface of the water
were similar for both the obese and lean rats (41). After the
last exercise bout, rats were dried, placed back in their cages,
and killed at the time points described previously. At the
onset of the recovery period, animals assigned to the CHO-
supplemented groups received an intraperitoneal glucose in-
jection (0.5 mg/g BM) and were subsequently allowed free
access to chow and water ad libitum. Animals in the fasted
groups were allowed only ad libitum access to water. All
postexercise food consumption was quantified.
Animal death. Approximately 5 min before the due time of
death, rats were anesthetized with an intraperitoneal injec-
tion of pentobarbital sodium (60 mg/kg BM). Then the soleus
muscle was rapidly excised and clamp frozen with tongs
cooled in liquid nitrogen. We deliberately chose to sample the
soleus (slow-twitch, oxidative fibers) because previous inves-
tigations have reported that GLUT-4 concentration is higher
in this muscle than in both the red (fast-twitch oxidative) and
white gastrocnemius (fast-twitch, glycolytic), whereas there
are no differences in GLUT-4 content between ZL and ZO
rats (2). Furthermore, total hexokinase activity is also simi-
lar between genotypes (33). In addition to the soleus, the liver
was also removed. At this time a blood sample (⬃2 ml) was
obtained from the femoral artery.
Blood biochemistry. Whole blood (⬃2 ml) was transferred
to an EDTA-administered tube and was spun in a centrifuge
at 12,000 rpm for 3 min. The plasma was immediately ana-
lyzed in duplicate for plasma glucose and plasma lactate
concentration using an automated analyzer (Yellow Springs
Instruments 2300 stat plus glucose and L-lactate analyzer,
Yellow Springs, OH). The remaining plasma was stored at
⫺80°C and was subsequently analyzed for plasma free fatty
acid (FFA) concentration by using an enzymatic colorimetric
method (NEFA C test kit, Wako, Richmond, VA) and for
plasma insulin concentration by radioimmunoassay using a
commercially available kit (Phadeseph, insulin RIA, Phar-
macia & Upjohn Diagnostics, Uppsala, Sweden).
Tissue glycogen determination. Tissue glycogen content
was assayed as previously described (22). Skeletal muscle
and liver samples were placed in 2 N HCl and incubated at
100°C for 2 h. After neutralization with 0.66 N NaOH, the
liberated glucose units were assayed fluorometrically, and
glycogen content was expressed as micromoles of glucosyl
units liberated per gram wet muscle weight (␮mol/g wet wt).
Measurement of GLUT-4 protein content. Portions of the
soleus muscle (⬃15 mg) were homogenized for 30 s in 1.0 ml
of ice cold buffer (20 mM HEPES, 1 mM EDTA, 250 mM
sucrose, pH 7.4) by using a motor-driven homogenizer (Ys-
tral, HD Scientific, NSW, Australia). Homogenates were
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1514 POSTEXERCISE GLYCOGEN RESYNTHESIS

heated for 10 min at 90°C, vortexed, and spun at 7,000 g for

10 min at 4°C. Supernatants were removed, and protein
content was determined by use of a commercially available
kit (Micro BCA protein assay reagent kit, Pierce, Rockford,
IL). The supernatant was diluted with Laemmli sample
buffer and stored at ⫺80°C until subsequent analysis. Ali-
quots of muscle homogenates containing 5 ␮g protein were
separated by SDS-PAGE (12.5% resolving gel), transferred to
polyvinylidenedifluoride membranes (MSI, 0.45 ␮m, Osmon-
ics), and blocked for 2 h with 5% nonfat milk. Membranes
were incubated overnight at 4°C in a polyclonal antibody
specific for GLUT-4. Membranes were washed in 0.05% Tris-
buffered saline Tween, incubated for 1 h with secondary
antibody conjugated to horseradish peroxidase, and washed
again in 0.05% Tris-buffered saline Tween. Proteins were
visualized by enhanced chemiluminescence (NEN Life Sci-
ence Products, Boston, MA) and quantified by densitometry.
Hexokinase and glycogen synthase activity. Soleus muscle
was homogenized (1:50 dilution) in 50% glycerol, 20 mM
phosphate buffer (pH 7.4), 5 mM 2-mercaptoethanol, 0.5 mM
EDTA, and 0.02% bovine serum albumin. Hexokinase activ-
ity was assayed fluorometrically at 25°C by measuring the
rate of production of reduced NADP (14). Glycogen synthase
activity was assayed by using the same homogenate as for
hexokinase activity, as previously described (14). Glycogen
synthase activity was measured in the absence (active form)
or presence of 10 mM (total activity) glucose-6-phosphate.
Glycogen synthase activity is reported as fractional activity
of the enzyme (active/total), with total activity expressed as
␮mol 䡠 g wet wt⫺1 䡠 min⫺1.
Statistical analyses. Analysis of differences between the
two treatments (Fast or CHO) within a genotype was per-
formed using a paired t-test. An unpaired t-test was used to
assess differences between ZL and ZO animals. All other
differences were determined by using a one-way ANOVA
with Tukey’s post hoc analysis. Significance was accepted
when P ⬍ 0.05. All data are presented as means ⫾ SE.

RESULTS

Postexercise food intake. Food consumption was sim-

ilar between ZL and ZO rats after both 30 (0.7 ⫾ 0.2 vs.
0.5 ⫾ 0.2 g) and 360 min (5.6 ⫾ 0.7 vs. 5.2 ⫾ 0.8 g) of
refeeding.
Muscle glycogen. Figure 1A displays the muscle gly-
cogen content for ZL and ZO animals at rest and at
various time points after exercise for the two treatment
interventions. Resting muscle glycogen contents were
not significantly different between genotypes, although
they tended to be higher in ZO rats (38.2 ⫾ 4.3 vs.
29.4 ⫾ 1.5 ␮mol/g wet wt). Exercise resulted in a
significant reduction in muscle glycogen content in
both genotypes (ZL 73% vs. ZO 63%; P ⬍ 0.01). In ZL
rats, CHO or Fast had little effect on muscle glycogen
resynthesis in the 30-min period after exercise (Fig.
1A). Likewise, muscle glycogen content was similar 30
min after exercise in ZO-Fast. However, CHO in-
creased muscle glycogen content 68% (from 14.3 ⫾ 1.2
to 24.1 ⫾ 2.5 ␮mol/g wet wt; P ⬍ 0.05) above postex-
ercise values in ZO rats. At this time, glycogen content
in ZO was significantly higher for both Fast and CHO
compared with ZL under the same conditions (Fig. 1A;
P ⬍ 0.01). After 360 min and in the absence of CHO,
muscle glycogen content for ZL rats remained 56%
below resting values; at the same time point, glycogen
J Appl Physiol • VOL
Fig. 1. Muscle and liver glycogen content in lean (ZL; solid bars) and
obese (ZO; open bars) Zucker rats. Soleus muscle (A) and liver (B)
were obtained from sedentary rats (Rest), exercised rats fasted and
killed immediately postexercise (Post), and fasted (Fast) and carbo-
hydrate-supplemented (CHO) rats killed after 30 min or 360 min of
recovery. Results are expressed as ␮mol/g wet wt. Values are
means ⫾ SE. *P ⬍ 0.05 vs. Rest for each genotype. †P ⬍ 0.05 vs. Post
for each genotype. §P ⬍ 0.05 vs. Fast at same time point for each
genotype.
content in the ZO rats had been restored to that of
Rest. CHO refeeding in ZL rats during 360 min of
recovery resulted in muscle glycogen supercompensa-
tion such that glycogen content was increased 68%
above resting levels (29.4 ⫾ 1.5 vs. 49.5 ⫾ 4.0 ␮mol/g
wet wt; P ⬍ 0.01). Under the same conditions, muscle
glycogen content was supercompensated by 44% in ZO
animals (38.2 ⫾ 4.3 vs. 55.0 ⫾ 2.8 ␮mol/g wet wt) with
no differences in the final glycogen content between
genotypes.
Liver glycogen content. Figure 1B displays the liver
glycogen content for both genotypes at rest and at
various time points after exercise for the two treatment
interventions. Liver glycogen content at rest was 35%
higher in ZO than ZL rats (334 ⫾ 31 vs. 247 ⫾ 16
91 • OCTOBER 2001 • www.jap.org
 POSTEXERCISE GLYCOGEN RESYNTHESIS
␮mol/g wet wt; P ⬍ 0.01). Exercise resulted in a signif-
icant reduction in liver glycogen content in both groups
(Fig. 1B), although the degree of depletion was more
marked in ZL compared with ZO rats (94 vs. 44%; P ⬍
0.01). Accordingly, liver glycogen utilization during the
exercise bout was greater in ZL than ZO rats (146 ⫾ 44
vs. 233 ⫾ 1 ␮mol/g wet wt; P ⬍ 0.01).
Liver glycogen content in ZL-Fast rats did not in-
crease above Post levels after 30 or 360 min of recovery.
However, after 360 min of CHO refeeding, liver glyco-
gen content was restored to resting values in this
genotype (Fig. 1B). Liver glycogen content in the ZO
rats was unchanged from Post values at all time points
after exercise regardless of whether or not CHO was
administered. With the exception of the 360-min value
with CHO refeeding, liver glycogen content was higher
in ZO compared with ZL rats at all time points during
recovery from exercise (P ⬍ 0.01; Fig. 1B). Although
liver glycogen content after 360 min recovery with
CHO was comparable between genotypes, it still re-
mained 38% lower than Rest levels in ZO rats.
GLUT-4 protein content. Figure 2 displays the
GLUT-4 protein concentration for both genotypes at
rest and at various time points after exercise for the
two treatment interventions. Resting GLUT-4 protein
concentration was similar between ZL and ZO rats.
There was little increase in GLUT-4 protein concentra-
tion immediately postexercise or after 30 min of recov-
ery for both genotypes regardless of refeeding regimen
(Fig. 2). GLUT-4 protein concentration was increased
⬃45% after 360 min of recovery for both genotypes in
fasted rats. However, with CHO refeeding, GLUT-4
protein concentration was increased ⬃115% above
resting values for both genotypes.
Hexokinase and glycogen synthase activity. Table 1
shows the activities of hexokinase and glycogen syn-
thase for both genotypes at rest and at various time
points after exercise for the two treatment interven-
Fig. 2. Effect of carbohydrate supplementation and fasting on
GLUT-4 protein of the soleus muscle. Representative immunoblots
showing GLUT-4 protein appear above each treatment group. Soleus
muscle was obtained from Rest, Post, and Fast and CHO rats killed
after 30 min or 360 min of recovery. Equal amounts of protein (5 ␮g)
from each muscle sample were loaded on a gel and immunoblotted as
described in METHODS. Samples are expressed as percentage of heart
standard (5 ␮g). Values are means ⫾ SE. *P ⬍ 0.05 vs. Rest for each
genotype. †P ⬍ 0.05 vs. Post for each genotype. §P ⬍ 0.05 vs. Fast at
same time point for each genotype.
J Appl Physiol • VOL 91 • OCTOBER 2001 •
1515
Table 1. Enzyme activities in soleus muscle
Glycogen synthase,
Hexokinase, ␮mol 䡠 g⫺1 䡠 min⫺1 active/total
Lean Obese Lean Obese
Rest 4.29 ⫾ 0.32 3.18 ⫾ 0.42 0.22 ⫾ 0.05 0.32 ⫾ 0.04
Post 3.55 ⫾ 0.30* 3.60 ⫾ 0.20 0.63 ⫾ 0.08* 0.57 ⫾ 0.05*
Fast 30 3.17 ⫾ 0.23* 3.68 ⫾ 0.29 0.59 ⫾ 0.06* 0.67 ⫾ 0.08*
CHO 30 3.32 ⫾ 0.27 3.85 ⫾ 0.17 0.71 ⫾ 0.05* 0.75 ⫾ 0.07*‡
Fast 360 3.98 ⫾ 0.45 4.20 ⫾ 0.43* 0.41 ⫾ 0.04* 0.35 ⫾ 0.02†
CHO 360 3.95 ⫾ 0.30 3.70 ⫾ 0.30 0.21 ⫾ 0.05‡§ 0.27 ⫾ 0.02‡§
Values are means ⫾ SE. A portion of soleus muscle was homoge-
nized and analyzed for hexokinase activity while glycogen synthase
activity was measured in the absence (active) or presence of 10 mM
glucose-6-phosphate (total). Glycogen synthase activity is reported
as fractional activity of the enzyme (active/total). Rest, sedentary
control animals; Post, animals killed immediately postexercise;
CHO, animals received an intraperitoneal glucose injection (0.5 mg/g
body wt) and free access to chow and H2O; Fast, access to H2O only;
30 and 360, no. of minutes postexercise when animals were killed.
* P ⬍ 0.01 vs. Rest for each genotype. † P ⬍ 0.05 and ‡ P ⬍ 0.01 vs.
Post for each genotype. § P ⬍ 0.05 vs. Fast at same time point for
each genotype.
tions. Hexokinase activity was similar at rest between
genotypes. Exercise was associated with a decrease in
hexokinase activity in fasted ZL rats, an effect that
persisted for the first 30 min of recovery (Table 1).
However, hexokinase activity was not different from
Rest or Post levels in ZO rats after 30 min of recovery
for either Fast or CHO. After 360 min, hexokinase
activity was significantly greater than Rest levels in
ZO-fasted but not in CHO-fed animals.
The fractional activity of glycogen synthase was sim-
ilar between genotypes at rest. Immediately after ex-
ercise, glycogen synthase activity was significantly in-
creased in both genotypes. Throughout 360 min of
recovery, glycogen synthase activity remained elevated
for fasted ZL rats (Table 1). However, glycogen syn-
thase activity had returned to Rest values after 360
min of CHO refeeding in ZL animals (Table 1). In the
ZO rats, glycogen synthase activity remained elevated
for the first 30 min of recovery for both treatments but
was back to Rest values after 360 min of either CHO or
Fast (Table 1).
Concentrations of plasma metabolites. Table 2 shows
the concentrations of plasma glucose, plasma lactate,
plasma insulin, and plasma FFA at rest and at various
time points after exercise after the two treatment in-
terventions. Resting plasma glucose concentrations
were similar between genotypes. However, in ZL rats,
exercise was associated with a significant reduction in
plasma glucose concentration, an effect that persisted
throughout 360 min of recovery (Table 2). On the other
hand, after 30 min CHO refeeding, plasma glucose
concentration was greater in ZL compared with Fast
and was still higher than Post values after 360 min of
CHO. Postexercise plasma glucose concentrations in
ZO rats were similar to Rest concentrations (Table 2).
However, apart from CHO 360, plasma glucose concen-
tration was greater in ZO than ZL animals (Table 2).
After 360 min of CHO refeeding, plasma glucose con-
centration was similar for both genotypes.
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1516 POSTEXERCISE GLYCOGEN RESYNTHESIS
Table 2. Concentrations of plasma metabolites
Glucose, mmol/l Lactate, mmol/l
Lean Obese Lean Obese
Rest 8.8 ⫾ 0.1 9.3 ⫾ 0.3 1.7 ⫾ 0.2 4.1 ⫾ 0.2‡
Post 5.3 ⫾ 0.7* 10.3 ⫾ 0.7‡ 2.4 ⫾ 0.7 5.0 ⫾ 0.8‡
Fast 30 5.2 ⫾ 0.4* 10.3 ⫾ 0.8‡ 1.5 ⫾ 0.4 3.4 ⫾ 0.3‡
CHO 30 7.6 ⫾ 0.7§ 11.9 ⫾ 0.9*‡ 1.3 ⫾ 0.2 2.9 ⫾ 0.4*‡
Fast 360 6.3 ⫾ 0.1* 9.0 ⫾ 0.6‡ 1.0 ⫾ 0.1 4.0 ⫾ 0.1‡
CHO 360 7.7 ⫾ 0.3†§ 8.0 ⫾ 0.4 2.4 ⫾ 0.5 4.2 ⫾ 0.2‡
Values are means ⫾ SE. Plasma glucose, lactate, insulin, and free fatty acid (FFA) concentrations were measured in lean and obese Zucker
rats as described in METHODS. * P ⬍ 0.05 vs. Rest for each genotype. † P ⬍ 0.05 vs. Post for each genotype. ‡ P ⬍ 0.05 vs. lean group under
identical conditions. § P ⬍ 0.05 vs. Fast at same time point for each genotype.
Resting plasma lactate concentration was signifi-
cantly greater in ZO compared with ZL rats. Although
exercise had little effect on plasma lactate concentra-
tions in either genotype (Table 2), plasma lactate was
significantly higher in obese animals at all time points,
regardless of the treatment intervention. Only after 30
min of CHO refeeding was plasma lactate lower than
Rest for ZO rats.
As would be expected, resting plasma insulin concen-
trations were significantly greater in ZO compared
with ZL rats and remained higher at all time points
regardless of treatment intervention (Table 2). On the
other hand, exercise was associated with a significant
reduction in plasma insulin concentrations in the ZL
rats such that, at all time points, concentrations were
lower than Rest levels. After 360 min of CHO refeed-
ing, plasma insulin concentration was greater than for
Post in ZL rats.
Plasma FFA concentrations were significantly
greater in ZO compared with ZL rats at rest. Exercise
was associated with a significant elevation in plasma
FFA concentration in ZL rats compared with resting
values (Table 2). Although there was a slight decrease
in plasma FFA concentration in ZO rats immediately
after exercise, this was not significant. Plasma FFA
concentrations in ZO rats remained between 1.2 and
1.4 mmol/l during the postexercise recovery period,
regardless of dietary intervention. On the other hand,
plasma FFA concentration was significantly greater 30
and 360 min after exercise in ZL rats irrespective of
whether CHO was administered or not (Table 2). Only
after 360 min of CHO refeeding was plasma FFA con-
centration back to Rest values in this genotype.
DISCUSSION
The pattern of glycogen resynthesis in normal mus-
cle after its depletion by exercise is biphasic (29, 37),
with an initial rapid (insulin-independent) phase of
synthesis, followed by a slower rate of glycogen accu-
mulation that requires the presence of insulin. In this
second phase and in the absence of carbohydrate sup-
plementation, glycogen levels are eventually restored
to basal concentrations, but if carbohydrate refeeding
takes place after exercise and is continued during re-
covery, muscle glycogen levels are increased above
normal, so-called glycogen supercompensation (4).
J Appl Physiol • VOL 91 • OCTOBER 2001 •
Insulin, ␮U/ml FFA, mmol/l
Lean Obese Lean Obese
13.1 ⫾ 0.4 48.8 ⫾ 6.2‡ 0.4 ⫾ 0.1 1.6 ⫾ 0.3‡
4.6 ⫾ 1.0* 38.2 ⫾ 5.1‡ 1.0 ⫾ 0.1* 1.4 ⫾ 0.1‡
2.6 ⫾ 0.6* 46.9 ⫾ 9.9‡ 0.9 ⫾ 0.1* 1.3 ⫾ 0.2‡
5.5 ⫾ 1.3* 55.2 ⫾ 10.8‡ 1.0 ⫾ 0.1* 1.2 ⫾ 0.1‡
3.3 ⫾ 0.5* 61.1 ⫾ 13.0‡ 0.9 ⫾ 0.1* 1.4 ⫾ 0.1‡
9.9 ⫾ 1.1*†§ 55.0 ⫾ 4.7‡ 0.5 ⫾ 0.1†§ 1.4 ⫾ 0.1‡
On the basis of the results of previous investigations
performed on insulin-resistant fasting animals (1, 10,
36), it is difficult to predict whether carbohydrate
refeeding during recovery from prolonged, strenuous
exercise would have an effect on skeletal muscle glyco-
gen resynthesis. However, in light of the finding that
contraction-stimulated glucose uptake is normal in in-
sulin-resistant muscle of the obese Zucker rat (2), we
originally proposed that the rate of glycogen accumu-
lation would be similar for both obese and lean animals
during the insulin-independent phase of recovery with
or without carbohydrate refeeding. In agreement with
our hypothesis, the first finding of the present study
was that insulin resistance had little effect on the
immediate (30 min) rate of postexercise glycogen re-
synthesis in obese fasted animals. Previous investiga-
tions have found a normal (1, 10, 36) or a reduced (13,
36) rate of postexercise glycogen resynthesis in diabetic
fasted animals. However, these results need to be re-
conciled with the fact that in those studies (1, 10, 13,
36) diabetes was induced with streptozotocin, an agent
that is known to be associated with a fall in GLUT-4
levels (7), a reduced insulin-responsiveness (19, 25),
and a fall in contraction-stimulated muscle glucose
uptake (24, 27, 42).
Perhaps of more significance was our finding of little
or no repletion of muscle glycogen after 30 min of
carbohydrate refeeding in lean rats. Such an observa-
tion is difficult to explain in light of the fact that
carbohydrate supplementation had restored blood glu-
cose concentration to resting values, whereas fasting
animals were still hypoglycemic at this time. However,
in agreement with our results, Terjung et al. (37) also
reported no net glycogen accumulation after 30 min in
the soleus muscle of rats swum to exhaustion and fed
glucose immediately after exercise. These workers re-
ported that the highest rates of glycogen resynthesis
after glucose administration were found between 30
and 60 min postexercise (37). In the present study,
animals were killed 30 and 360 min after exercise: it
may well be that, because of our early and late sam-
pling times, we failed to detect the most rapid phase of
glycogen resynthesis. We also considered the possibil-
ity that the lack of glycogen resynthesis in lean ani-
mals may have been because they consumed less food
during the early phase of recovery. Such a theory
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 POSTEXERCISE GLYCOGEN RESYNTHESIS
would be consistent with our observations that, com-
pared with obese rats, lean animals tended to be more
fatigued and lethargic when placed back in their cages.
However, analysis of food records revealed that both
lean and obese rats consumed similar amounts of chow
during the first 30 min (⬃0.6 g) and also after 360 min
(⬃5.5 g) of recovery. Because postexercise lactate levels
were consistently elevated in obese compared with lean
animals, one cannot discount the possibility that lac-
tate provided a major carbon source for muscle glyco-
gen resynthesis during recovery, as has been recently
suggested (10). On the other hand, despite higher rest-
ing and postexercise concentrations of plasma FFA in
obese compared with lean rats (Table 2), there was no
evidence of diminished glycogen deposition.
On the basis of impaired rates of insulin-dependent
glycogen synthesis in muscle from insulin-resistant
fasting humans recovering from exercise (28), along
with the observed reversal of the exercise-induced in-
crease in permeability to sugar when fed carbohydrate
(44), we hypothesized that the extent of glycogen accu-
mulation in muscle from obese animals would be at-
tenuated in the slower (insulin-dependent) phase after
carbohydrate administration. Furthermore, because
glycogen supercompensation takes place throughout
this slower portion of recovery (11), we also proposed
that glycogen concentration would only be restored to
resting (preexercise) levels and not supercompensated
in muscle from insulin-resistant rats fed carbohydrate.
However, contrary to our expectations, we found that
carbohydrate refeeding accelerated glycogen accumu-
lation in muscle of obese compared with lean animals
(Fig. 1A) and consequently resulted in supercompensa-
tion after 360 min of recovery. These data strongly
suggest that, with the increased carbohydrate avail-
ability, there was a persistent increase in glucose up-
take associated with glycogen-depleting exercise, even
in the face of muscle insulin resistance. Although the
degree of supercompensation was greater in skeletal
muscle from lean than from insulin-resistant rats (68
vs. 44%), there were no differences in the final glycogen
content between genotypes because of the slightly
higher resting glycogen content in the obese animals.
To the best of our knowledge, this is the first study to
report glycogen supercompensation in skeletal muscle
from untrained insulin-resistant rats. Our findings
raise interesting questions regarding the control of
muscle glycogen synthesis in insulin-resistant tissue.
Both glucose transport (30, 35) and glycogen syn-
thase activation (23) have been implicated to be major
rate-limiting steps for glycogen synthesis in skeletal
muscle. Being downstream of GLUT-4 and hexokinase
in the metabolic pathway, glycogen synthase is depen-
dent on glucose transport to provide substrate for sub-
sequent glycogen synthesis. Glucose transport would
be expected to exert control over the glycogen synthesis
pathway if an increase in the transport capacity in-
duced a proportional increase of flux through the path-
way. A limitation of the present study was that we did
not obtain measures of glucose transport. However,
Brozinick et al. (2) previously reported that both basal
J Appl Physiol • VOL
1517
and the maximum contraction-stimulated glucose up-
take is not impaired in insulin-resistant muscle of the
obese Zucker rat.
Alternatively, it has been proposed that the level of
skeletal muscle GLUT-4 protein serves to set or limit
the upper level of glycogen accumulation (20, 21). In
this regard, Kuo et al. (21) have recently reported that
an acute bout of prolonged swimming induced a 43%
increase in GLUT-4 protein concentration above rest-
ing control values in fasted rats. They also found that
carbohydrate supplementation in the postexercise re-
covery period further enhanced GLUT-4 protein con-
centration and reported a significant positive correla-
tion between the level of muscle GLUT-4 protein and
subsequent glycogen accumulation after carbohydrate
refeeding (21). In close agreement with the results of
Kuo et al. (21), we found that exercise alone resulted in
a ⬃45% increase in GLUT-4 protein concentration in
fasted animals. Exercise plus carbohydrate supple-
mentation, however, increased soleus GLUT-4 protein
concentration ⬃115% above rest in both genotypes.
Accordingly, during this time carbohydrate refeeding
resulted in glycogen supercompensation in both lean
and obese rats. These data strongly suggest that if
glycogen levels are lowered by similar amounts during
exercise and sufficient carbohydrate is available, gly-
cogen resynthesis will be stimulated to the same extent
in both normal and insulin-resistant muscle.
Because hexokinase expression and activity (39) and
glycogen synthase expression (40) have been reported
to be decreased in patients with type II diabetes, we
wished to quantify the activities of both hexokinase
and glycogen synthase in an attempt to determine
their role in subsequent glycogen resynthesis. In con-
trast to the finding of a reduced hexokinase activity in
skeletal muscle from humans with type II diabetes
(39), we found that hexokinase activity was similar
between normal and insulin-resistant rats and also
between fed and fasted animals (Table 1). On the basis
of this finding, one might reasonably predict the same
flux through the glucose transporter-hexokinase step
(35) that would result in comparable activation of gly-
cogen synthase (26). Indeed, the activity of glycogen
synthase was remarkably similar between genotypes
before and after exercise (Table 1). A dissociation be-
tween glycogen synthase activity and the subsequent
rate of glycogen resynthesis has been previously dem-
onstrated by Price et al. (29). These workers reported a
10-fold drop in the rate of glycogen synthesis between
the early (first 30 min) and late (⬎1 h) period of
recovery after exercise with only minor (⬍twofold)
changes in the fractional activity of glycogen synthase.
In agreement with previous reports (9), we found
that muscle contraction and glycogen depletion re-
sulted in an increase in the fractional activity of glyco-
gen synthase. Accompanying postexercise glycogen re-
synthesis was a concomitant inactivation of glycogen
synthase: it is well known that glycogen plays an
important role in regulating its own synthesis, with
glycogen synthase activity varying inversely with gly-
cogen concentration (6) and glucose transport being
91 • OCTOBER 2001 • www.jap.org
1518 POSTEXERCISE GLYCOGEN RESYNTHESIS
significantly higher in muscles in which glycogen con-
tent is kept low (9, 15).
Although the major focus of the present study was to
determine the pattern of glycogen accumulation in
insulin-resistant skeletal muscle, we also determined
the time-course changes in liver glycogen repletion
after exercise with and without carbohydrate refeed-
ing. In agreement with other studies (10), the level of
hepatic glycogen before exercise was substantially
higher in the insulin-resistant compared with the lean
animals, but whereas exercise only resulted in a mild
(⬃50%) loss of liver glycogen in insulin-resistant ani-
mals, there was an almost complete depletion in lean
animals. This latter observation concurs with the re-
sults of others (1, 8), but the finding of only a mild
exercise-induced decrease in hepatic glycogen stores in
insulin-resistant rats contrasts with the recent find-
ings of Ferreira et al. (10), who reported that strepto-
zotocin-induced diabetic animals had a more marked
fall in glycogen concentration than control animals
after exercise. The most likely reason for such a dis-
crepancy is the animals in the study of Ferreira et al.
were fasted for 24 h before their high-intensity short-
term (⬃3 min) exercise protocol.
The pattern of postexercise liver glycogen accumula-
tion deviated markedly between genotypes. Hepatic
glycogen concentration in lean animals remained sup-
pressed throughout recovery and only returned to rest-
ing levels after 360 min of CHO refeeding. On the other
hand, liver glycogen stores in obese insulin-resistant
rats showed little fluctuation throughout the recovery
period. In agreement with the results of a previous
study (8), there was preferential resynthesis of muscle
compared with liver glycogen in lean rats after ex-
hausting exercise.
In conclusion, this is the first study to show that the
increased glucose availability with carbohydrate
refeeding after an acute bout of glycogen-depleting
exercise resulted in muscle (but not liver) glycogen
supercompensation in both untrained lean and obese
insulin-resistant Zucker rats. For this reason, frequent
exercise bouts of sufficient intensity and/or duration to
markedly deplete muscle glycogen stores may benefit
those individuals with a genetic predisposition for the
development of insulin resistance.
We are grateful to S. Potocnik for providing the GLUT-4 antibod-
ies used in this study.
This study was supported by an RMIT Faculty of Life Sciences
Research Grant to J. A. Hawley.
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