| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
1 Laboratory of Exercise
Physiology, This study
assessed the effects of inactivity on GLUT-4 content of human skeletal
muscle and evaluated resistance training as a countermeasure to
inactivity-related changes in GLUT-4 content in skeletal muscle. Nine
young men participated in the study. For 19 days, four control subjects
remained in a
inactivity; glucose metabolism; isometric training; vastus
lateralis muscle
SKELETAL MUSCLE is responsible for at least 80% of
insulin-stimulated glucose uptake. Glucose transport is the
rate-limiting step in skeletal muscle glucose metabolism under most
physiological conditions (19). Furthermore, maximal insulin- and
contraction-stimulated glucose transport activity is reported to be
linearly related to the content of GLUT-4 isoform of the glucose
transporter in muscle (12, 14). Therefore, the level of
GLUT-4 in skeletal muscle may be an important determinant of whole body
glucose disposal.
Previous studies demonstrated that exercise training increases GLUT-4
protein content (3, 4, 11, 16), whereas detraining reduces GLUT-4 in
skeletal muscle (17, 22, 33). Because several studies demonstrated that
inactivity, including bed rest, induces glucose intolerance (13, 18,
21, 24, 33, 34), it is reasonable to speculate that a decrease in
muscle activity may play a role in the decrease in glucose tolerance.
However, the effect of prolonged bed rest on muscle GLUT-4 in humans
has not been investigated (27). We have, therefore, examined the effect
of 19 days of bed rest on muscle GLUT-4 in young, healthy men. We also
evaluated the effect of brief resistance training as a countermeasure
to the effect of bed rest on muscle GLUT-4 and glucose tolerance.
Subjects.
Nine young men [age 22 ± 4 (SD) yr] volunteered to
participate in the study after they provided written informed consent. Subjects passed a comprehensive physical examination. The subjects were
randomly assigned to control (n = 4)
or resistance training groups (n = 5).
The protocol was approved by the Institutional Ethics Committee of the
National Aero Space Development Agency, Japan.
Bed-rest procedure.
After the last blood sampling taken for the oral glucose tolerance test
(OGTT) before bed rest, the subjects ate a light breakfast. Then, at
approximately 10:30 AM, the subjects started bed rest. For 20 days, the
subjects remained in a Muscle biopsy.
Using Bergstrom biopsy needles (2), we obtained muscle samples from the
lateral aspect of vastus lateralis (VL) muscle 4 days before the start
of bed rest (before bed rest) and in the evening of the 20th day of bed
rest (after bed rest). This time corresponded to 8 h after the last
bout of resistance training and 14 h before the end of 20 days of bed
rest. Therefore, actual exposure of the sampled muscles to bed rest is
19 days + 6-8 h.
OGTT.
Glucose tolerance was determined with a 75-g OGTT that was performed in
the morning after an overnight fast just before bed rest and during the
last hours of bed rest, as described above. This time corresponded to
~1 day after the last bout of resistance training (in other words,
12-14 h after the biopsy procedure). Blood samples were taken
immediately before and 30, 60, and 120 min after the glucose load.
Plasma glucose concentration was determined by using an enzymatic
method (10). Plasma insulin was determined by using radioimmunoassay
(26). The total areas under the curve (AUCs) for glucose and insulin
were calculated by using the trapezoidal rule.
Resistance training.
Subjects in the training group did resistance training once every
morning during the bed-rest period. The resistance training consisted
of 30 isometric maximal voluntary contractions for 3 s each; subjects
used leg-press exercise to recruit the extensor muscles of the ankle,
knee, and hip. The angle of the knee was fixed to be 90°. Pauses of
3 s were allowed between bouts of maximal contractions. The duration of
each training session was 3 min.
Measurement of GLUT-4 in muscle.
The muscle samples were minced and mixed well. Twenty milligrams of
minced muscle were homogenized in 9 ml of buffer containing 0.25 M
sucrose, 1 mM EDTA, and 10 mM Tris · HCl, pH 7.5. Homogenate was centrifuged at 175,000 g for 60 min. The pellet (the membrane fraction) was suspended in 450 µl of buffer, containing 1 mM EDTA and
10 mM Tris · HCl, pH 7.5, and was blended vigorously
in a Vortex mixer until the pellets were completely dispersed. Then this solution was solubilized by adding 50 µl of 0.35 M (10% wt/vol) SDS, mixed well in a Vortex mixer, and kept for 10 min at room temperature. This solution was transferred to a microcentrifuge tube
and centrifuged at 10,000 g for 10 min
to remove unsolubilized materials. These solubilized membranes were
used for the assay of protein concentration and the amount of glucose transporters.
Detection of GLUT-4 protein.
The solubilized membranes were incubated for 10 min at 37°C in a
solution containing 2.5% SDS, 75 mM dithiothreitol, 1.7 M (12.5%
vol/vol) glycerol, 361 mM (0.025% wt/vol) bromophenol blue, and 12.5 mM Tris · HCl, pH 7.0. SDS-PAGE was performed
according to Laemmli (20) with a 0.56 M (4% wt/vol) stacking gel and a 1.4 M (10% wt/vol) resolving gel. Immunoblotting of
electrophoresis gels was performed as described previously (5).
Proteins in gels were electrophoretically transferred to polyvinylidine
difluoride sheets in a transfer buffer. The sheets were incubated
successively with antibodies to glucose transporters for 20 h and
125I-labeled protein A for 24 h at
4°C. Autoradiography was performed with Kodak X-AR film at
Measurement of maximal voluntary isometric force.
Maximal voluntary isometric contraction torque of the knee extensors
was measured 4 days before bed rest and 2 days after the end of the
bed-rest period. The angle of the knee was fixed at 90°. Each
subject was seated at a test bench and was secured by placing
restraining straps about the hip and thigh to minimize extraneous
movement. The best performance of three trials was recorded as the
maximal value.
Determination of cross-sectional area (CSA).
CSA of thigh muscles, including VL muscle, was determined by using
magnetic resonance imaging (1) 2 days before the start of bed rest and
1 day after the end of bed rest. The subjects were imaged in a prone
position, with the knee and ankle kept at 180 and 120°,
respectively, with 180° being full extension of each joint.
Magnetic resonance imaging was performed with a 1.0-T GYROSCAN T10-NT
Powertrak 1000 (Philips Medical Systems). T1-weighted,
spin-echo, axial-plane imaging was performed with the following
variables: 450-ms TR, 20-ms TE, 256 × 172 matrix, 300-mm field of
view, 10-mm slice thickness, and 7-mm interslice gap. First, coronal
plane images were taken to identify the spina iliaca anterior superior,
which is the origin of the sartorius. Consecutive axial images were
obtained from the anterior superior iliac spine to the end of the
tibia. From the serial cross-sectional images, outlines of quadricep
femoris muscle, including VL muscle, were traced on the axial images at
50% of the femur length. Traced images were transferred to a personal
computer (Power Macintosh 8100/80 AV, Apple Computer) for calculation
of the CSA with the use of the National Institutes of Health
public-domain image software package.
Statistical procedure.
Unless otherwise stated, the differences between physiological
variables obtained before and after bed rest were evaluated by
two-tailed Student's t-test for
paired observations. When data are not distributed normally,
nonparametric analysis with the Mann-Whitney ranked sum test was used.
The AUCs for plasma glucose and insulin were analyzed with a one-tailed
t-test (11). Values are expressed as
means ± SD. Differences were considered statistically significant
if P < 0.05.
Physical characteristics of subjects.
In the period after bed rest, body mass of the subjects in the control
group (66.9 ± 11.1 vs. 65.9 ± 10.1 kg, before and after bed
rest, respectively) and training group (69.7 ± 9.8 vs. 68.3 ± 8.8 kg, before and after bed rest, respectively) appeared to be less
than that observed before bed rest, but the differences were not
statistically significant. Body height of the nine subjects increased
slightly but significantly during bed rest (172.0 ± 4.6 vs. 172.4 ± 4.3 cm before and after bed rest, respectively, P < 0.05).
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
6° head-down tilt at all times throughout bed
rest, except for showering every other day. Five training group
subjects also remained at bed rest, except during resistance training
once in the morning. The resistance training consisted of 30 isometric
maximal voluntary contractions for 3 s each; leg-press exercise was
used to recruit the extensor muscles of the ankle, knee, and hip.
Pauses (3 s) were allowed between bouts of maximal contraction. Muscle
biopsy samples were obtained from the lateral aspect of vastus
lateralis (VL) muscle before and after the bed rest. GLUT-4 content in
VL muscle of the control group was significantly decreased after bed
rest (473 ± 48 vs. 398 ± 66 counts · min
1 · µg
membrane protein1, before
and after bed rest, respectively), whereas GLUT-4 significantly increased in the training group with bed rest (510 ± 158 vs. 663 ± 189 counts · min1 · µg
membrane protein1, before
and after bed rest, respectively). The present study demonstrated that
GLUT-4 in VL muscle decreased by ~16% after 19 days of bed rest, and
isometric resistance training during bed rest induced a 30% increase
above the value of GLUT-4 before bed rest.
INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
MATERIALS AND METHODS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
6° head-down tilt at all times
throughout the study except during resistance training (once in the
morning) and showering every other day. The subjects also remained in
the supine position during the training and the transfer from head-down
tilt to the training device charge. Because this study was done in
conjunction with a joint project for studying general adaptations to
spaceflight, including cardiovascular system adaptations, the subject
remained not in a supine but in a 6° head-down position.
70°C for 4-12 h. To quantify the glucose transporters,
we cut out pieces of sheet containing the GLUT-4 protein and counted
the radioactivity in a gamma counter.
RESULTS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
7.3 ± 4.0%; P = 0.05), whereas bed rest did not significantly affect CSA of the VL
muscle of the training group (Table 1). 1. After the bed-rest period, total CSA of thigh muscles decreased in both
control and training group by 8.1 ± 1.9%
(P < 0.01) and 4.3 ± 3.6% (P < 0.05), respectively
(Table 2).
Table 1.
Changes in cross-sectional area of vastus lateralis (VL) muscle after
20 days of bed rest
Table 2.
Changes in total cross-sectional area of thigh muscles after 20 days of
bed rest
|
GLUT-4 protein concentration.
GLUT-4 content in VL muscle of the control group significantly
decreased after 19 days of bed rest (P < 0.05), whereas it significantly increased during 19 days of bed
rest plus isometric training (P < 0.01) (Fig. 1).
|
OGTTs.
Plasma glucose concentration during an OGTT after 20 days of bed rest
was not significantly different in the control group (Fig.
2 A),
whereas the AUC for plasma insulin level was higher compared with
levels before bed rest (14,038 ± 6,846 vs. 9,832 ± 4,662 µU · ml1 · 120 min1, respectively;
P < 0.05; Fig.
2 B). For the training group
subjects, 20 days of bed rest did not affect the plasma glucose level
during OGTT (Fig.
3 A).
Furthermore, in the training group, the AUC for plasma insulin levels
during the test after bed rest was also significantly higher than the
respective AUC during the test before bed rest (7,297 ± 4,088 vs.
4,427 ± 1,652 µU · ml1 · 120 min1, respectively; Fig.
3B).
|
|
| |
DISCUSSION |
|---|
|
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
The main findings of this study are that the GLUT-4 content of VL muscle was reduced after 19 days of bed rest, and brief periods of resistance training increased GLUT-4 content in the same muscle during the same duration of bed rest.
This decrease in GLUT-4 content in muscle may reduce insulin-stimulated glucose uptake, resulting in insulin-resistance in skeletal muscle during inactivity (21, 28, 32). The magnitude of the decrement in GLUT-4 was modest (~16%) but is comparable with that reported for insulin-resistant obese subjects (18% lower than that of normal subjects) (5). Furthermore, even in non-insulin-dependent diabetes mellitus patients, GLUT-4 content in skeletal muscle is not different from that in nondiabetic controls (4, 5). Therefore, the inactivity induced by bed rest is a potent physiological stimulus to induce depressed GLUT-4 expression in skeletal muscle.
There has been no previous investigation regarding the effect of resistance training on GLUT-4 content in human skeletal muscle, although endurance training has been shown to increase GLUT-4 content and to improve insulin-stimulated glucose uptake (3, 4, 11). However, because several studies have recently suggested that neurogenic factors, including motor unit activity, are the most potent stimuli to increase in GLUT-4 content (8, 23), we believe that it is also possible that intense neuromuscular activity induced during maximal voluntary isometric contractions may have a significant influence on GLUT-4 content in human skeletal muscle recruited by high-intensity short-term isometric contractions. Actually, the present investigation demonstrated that GLUT-4 content in the skeletal muscle was increased by 30% with the short bouts of resistance exercise training even during 19 days of bed rest that, by itself, depresses GLUT-4 expression. The magnitude of this increase in GLUT-4 was relatively small compared with that reported for moderate-intensity endurance training [98% increase after 7-10 days of cycle ergometer exercise training (11)]. However, because it is probable that the increase in GLUT-4 content in muscle is greater after resistance training without bed rest, it is not known whether the effect of isometric resistance training is less than that of endurance training. Therefore, it will be of interest to determine how much resistance training increases GLUT-4 content in muscle of freely living humans. Furthermore, in terms of developing an effective countermeasure to depressed expression of muscle GLUT-4 during inactivity, it is worthwhile to compare the effect of protocols that differ in intensity, frequency, and duration of isometric resistance training on GLUT-4 content in skeletal muscle.
Expression of GLUT-4 content in brown adipose tissue is enhanced by augmented sympathetic nerve activity by cold exposure (30). Furthermore, it is known that muscle sympathetic nerve activity is inhibited by both acute (25) and prolonged (31) head-down tilt. Therefore, it is possible that head-down tilt might have influenced the change in muscle GLUT-4 content observed in the present investigation. Although we believe that the relative influence of altered muscle sympathetic nerve activity on GLUT-4 content is small, the pure effect of 19 days of inactivity on GLUT-4 content in skeletal muscles will be clarified by a future study that allows subjects to rest on a flat bed for 19 days.
OGTT after bed rest showed that, compared with the OGTT before bed rest, there was no significant change in plasma glucose, and plasma insulin level during the test was marginally increased in both control and training groups. These results demonstrate that 20 days of inactivity induce mild insulin resistance. Furthermore, these results suggest that a small increase in GLUT-4 content in VL muscle of the trained subjects did not succeed in preventing a bed-rest-induced defect of whole body glucose disposal. First, the discrepancy between the change in GLUT-4 and the OGTT of the trained subjects probably results from the fact that GLUT-4 was measured in a discrete muscle bed recruited by the exercise training, whereas the OGTT reflects whole body glucose handling by the total musculature (trained and untrained) (11). Because GLUT-4 content in the control group was reduced by 16% after bed rest, it is assumable that, in the training group, GLUT-4 content was also decreased, to the same extent, in muscles that were not recruited during the training session. Second, the discrepancy between the GLUT-4 and OGTT response after bed rest in the trained subjects may be explained by the inverse response of muscle mass that affects OGTT scores. Because a further decrease in CSA of the thigh muscle was observed in the control subjects compared with in the trained subjects (Table 2), it is also assumable that, for the training group, more atrophy may have occurred in the untrained muscle than in the trained muscle during bed rest. Therefore, the results of the present investigation suggest that the effect of training-induced increase in GLUT-4 concentration in the trained muscle on whole body glucose disposal might have been overcome by the bed-rest-induced decrease in muscle volume, in both trained and nontrained muscle.
From results obtained from the present investigation, two strategies can be postulated in terms of developing better countermeasures to insulin resistance induced by bed rest. First, the resistance training should recruit as much muscle in the body as possible (for example, back muscle) for the purpose of giving a stimulus for maintaining muscle mass (7). Second, resistance training should be more intense and/or more frequent (for example, two times a day) to induce more increase in GLUT-4 content in trained muscle. The efficacy of these strategies may be proved in future studies.
Because the value of the AUC for plasma insulin of the control group before bed rest was significantly higher than that of the training group (P = 0.04), different characteristics of the two groups may have influenced the result of the present investigation. However, the insulin response of the control group during the OGTT was within the normal range. Furthermore, the content of GLUT-4 in VL muscle of the two groups was not different before bed rest. Therefore, it seems unlikely that the marginally different characteristics of the two groups affected the essential finding of the present investigation, at least regarding the GLUT-4 response during bed rest.
The CSA of thigh muscles decreased significantly in both the control and training groups after bed rest (Table 2), whereas the maximal voluntary torque of knee extension was not statistically significantly changed in either group (Table 3). This result seems to be in conflict with the general knowledge that these two variables are closely related (15). However, maximal knee extension torque of three of the four control subjects decreased by 5-33%, while one subject in the control group increased his torque marginally (3%) after bed rest. Overall, average isometric knee extension torque decreased by 16%. This value is comparable to the values reported by Funato et al. (9) in a previous bed-rest study. Therefore, we believe that the inconsistent relationship between CSA and maximal isometric torque of the knee extensors in the control group may be explained by the statistical limitation of the present study, especially the small number of the control subjects. On the other hand, it is reasonable to speculate that the trained subjects could preserve their knee extension torque during bed rest through compensating for decreased muscle CSA with increased specific tension (force per muscle CSA in N/cm2) as a result of the resistance training (9, 29).
In conclusion, the result of the present study shows that GLUT-4 concentration in VL muscle of humans decreases modestly with 19 days of bed rest and that isometric resistance training not only overcomes this effect but induces a small increase in muscle GLUT-4.
| |
ACKNOWLEDGEMENTS |
|---|
The authors thank Dr. John O. Holloszy (Washington University School of Medicine, St. Louis, MO) for a critical review of the manuscript. We also thank Dr. Osamu Ezaki (Div. of Clinical Nutrition, National Institute of Health and Nutrition, Tokyo, Japan) for providing the antibody against GLUT-4 protein. The biopsy procedure was conducted by Drs. Michael Kjaer (Muscle Research Center, University of Copenhagen, Copenhagen, Denmark) and Hitoshi Shimojo (Institute of Health and Sports Sciences, University of Tsukuba, Tsukuba City, Japan). Technical assistance of Kishiko Ogawa (National Institute of Health and Nutrition, Tokyo, Japan) for handling human subjects during bed rest is greatly appreciated.
| |
FOOTNOTES |
|---|
This study was supported by research grants from the Japan Space Utilization Promotion, Tokyo, Japan, and by Grants-in-Aid for Scientific Research 09480017 and 08680158 from the Ministry of Education, Science, Sports and Culture.
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. §1734 solely to indicate this fact.
Address for reprint requests and correspondence: I. Tabata, Laboratory of Exercise Physiology, Div. of Health Promotion, National Institute of Health and Nutrition, 1-23-1 Toyama, Shinjuku City, Tokyo 162-8636, Japan (E-mail: tabata{at}nih.go.jp).
Received 22 April 1998; accepted in final form 16 November 1998.
| |
REFERENCES |
|---|
|
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
1.
Akima, H., S. Kuno, Y. Suzuki, A. Gunji, and T. Fukunaga.
Effects of 20 days of bed rest on physiological cross-sectional
area of human thigh and leg muscles evaluated by magnetic resonance
imaging. J. Gravitational Physiol. 4, Suppl.: S15-S21, 1997.
2.
Bergstrom, J.,
L. Hermansen,
E. Hultman,
and
B. Saltin.
Diet, muscle glycogen and physical performance.
Acta Physiol. Scand.
71:
140-150,
1967[Medline].
3.
Dela, F.,
A. Handberg,
K. J. Mikines,
J. Vinten,
and
H. Galbo.
GLUT-4 and insulin receptor binding and kinase activity in trained human muscle.
J. Physiol. (Lond.)
469:
615-624,
1993
4.
Dela, F.,
T. Ploug,
A. Handberg,
L. N. Petersen,
J. J. Larsen,
K. J. Mikines,
and
H. Galbo.
Physical training increases muscle GLUT-4 protein and mRNA in patients with NIDDM.
Diabetes
43:
862-865,
1994[Abstract].
5.
Dohm, G. L.,
C. W. Elton,
J. E. Friedman,
P. F. Pilch,
W. J. Pories,
S. M. Atkinson, Jr.,
and
J. F. Caro.
Decreased expression of glucose transporter in muscle from insulin-resistant patients.
Am. J. Physiol.
260 (Endocrinol. Metab. 23):
E459-E463,
1991
6.
Ezaki, O.,
N. Fukuda,
and
H. Itakura.
Role of two types of glucose transporters in enlarged adipocytes from aged obese rats.
Diabetes
39:
1543-1549,
1990[Abstract].
7.
Ferrand, A. A.,
K. D. Tipton,
M. M. Bamman,
and
R. R. Wolfe.
Resistance exercise maintains skeletal muscle protein synthesis during bed rest.
J. Appl. Physiol.
82:
807-810,
1997
8.
Fogt, D.,
M. J. Slentz,
M. E. Tischler,
and
E. J. Henriksen.
GLUT-4 protein and citrate synthase activity in distally or proximally denervated rat soleus muscle.
Am. J. Physiol.
272 (Regulatory Integrative Comp. Physiol. 41):
R429-R432,
1997
9.
Funato, K., A. Matsuo, H. Yata, H. Akima, Y. Suzuki, A. Gunji,
and T. Fukunaga. Changes in force-velocity and power output of
upper and lower extremity musculature in young subjects following 20 days of bed rest. J. Gravitational
Physiol. 4, Suppl.:
S23-S30, 1997.
10.
Goto, Y.,
and
M. Kakizaki.
Glucose tolerance test and diagnosis of diabetes mellitus (in Japanese).
Diagnosis Treatment
66:
1993-1996,
1978.
11.
Gulve, E. A.,
and
R. 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.
Goodyear, L. J.,
P. A. King,
M. F. Hirshman,
C. M. Thompson,
E. D. Horton,
and
E. S. Horton.
Contractile activity increases plasma membrane glucose transporters in absence of insulin.
Am. J. Physiol.
258 (Endocrinol. Metab. 21):
E667-E672,
1990
13.
Heath, G. W.,
J. R. Gavin III,
J. M. Hinderliter,
J. M. Hagberg,
S. A. Bloodfield,
and
J. O. Holloszy.
Effects of exercise and lack of exercise on glucose tolerance and insulin sensitivity.
J. Appl. Physiol.
55:
628-634,
1983
14.
Henriksen, E. J.,
R. E. Bourey,
K. J. Rodnick,
L. Koranyi,
M. A. Permutt,
and
J. O. Holloszy.
Glucose transport protein content and glucose transport capacity in rat skeletal muscle.
Am. J. Physiol.
259 (Endocrinol. Metab. 22):
E593-E598,
1990
15.
Ikai, M.,
and
T. Fukunaga.
Calculation of muscle strength per unit cross-sectional area of human muscle by means of ultrasonic measurement.
Int. Z. Angew. Physiol. Einschl. Arbeitsphysiol.
26:
26-32,
1968.
16.
Kawanaka, K.,
M. Higuchi,
H. Ohmori,
S. Shimegi,
O. Ezaki,
and
S. Katsuta.
Muscle contractile activity modulates GLUT-4 protein content in the absence of insulin.
Horm. Metab. Res.
28:
75-80,
1996[Medline].
17.
Kawanaka, K.,
I. Tabata,
S. Katsuta,
and
M. Higuchi.
Changes in insulin-stimulated glucose transport and GLUT-4 protein in rat skeletal muscle after swimming training.
J. Appl. Physiol.
83:
2043-2047,
1997
18.
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
19.
Kubo, K.,
and
J. E. Foley.
Rate-limiting steps for insulin-mediated glucose uptake into perfused rat hindlimb.
Am. J. Physiol.
250 (Endocrinol. Metab. 13):
E100-E102,
1986
20.
Laemmli, U. K.
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
Nature
227:
680-685,
1970[Medline].
21.
Lipman, R. L.,
J. J. Schnure,
E. M. Bradley,
and
F. R. Lecocq.
Impairment of peripheral glucose utilization in normal subjects by prolonged bed rest.
J. Lab. Clin. Med.
76:
221-230,
1970[Medline].
22.
McCoy, M.,
J. Proietto,
and
M. Hargreaves.
Effect of detraining on GLUT-4 protein in human skeletal muscle.
J. Appl. Physiol.
77:
1532-1536,
1994
23.
Megeney, L. A.,
M. A. Prasad,
M. H. Tan,
and
A. Bonen.
Expression of the insulin-regulatable transporter GLUT-4 in muscle is influenced by neurogenic factors.
Am. J. Physiol.
266 (Endocrinol. Metab. 29):
E813-E816,
1994
24.
Mikines, K. J.,
F. Dela,
B. Tronier,
and
H. Galbo.
Effect of 7 days of bed rest on dose-response relation between plasma glucose and insulin secretion.
Am. J. Physiol.
257 (Endocrinol. Metab. 20):
E43-E48,
1989
25.
Nagaya, K.,
F. Wada,
S. Nakamitsu,
S. Sagawa,
and
K. Shiraki.
Response of the circulatory system and muscle sympathetic nerve activity to head-down tilt in humans.
Am. J. Physiol.
268 (Regulatory Integrative Comp. Physiol. 37):
R1289-R1294,
1995
26.
Nomura, T.,
R. Odagiri,
R. Idehara,
H. Akashi,
and
H. Idehara.
Clinical application of plasma IRI determination using double antibody solid phase technique RIA kit.
Clin. Endocrinol. (Oxf.)
32:
573-578,
1984.
27.
Ploug, T.,
T. Ohkuwa,
A. Handberg,
J. Vissing,
and
H. Galbo.
Effect of immobilization on glucose transport and glucose transporter expression in rat skeletal muscle.
Am. J. Physiol.
268 (Endocrinol. Metab. 31):
E980-E986,
1995
28.
Richter, E. A.,
B. Kiens,
M. Mizuno,
and
B. Saltin.
Insulin action in human thighs after one-legged immobilization.
J. Appl. Physiol.
67:
19-23,
1989
29.
Sale, D. G. Neural adaptation to resistance
training. Med. Sci. Sports Exerc. 20, Suppl.: S135-S145, 1988.
30.
Shimizu, Y.,
H. Nikami,
K. Tsukazaki,
U. F. Machado,
H. Yano,
Y. Seino,
and
M. Saito.
Increased expression of glucose transported GLUT-4 in brown adipose tissue of fasted rats after cold exposure.
Am. J. Physiol.
264 (Endocrinol. Metab. 27):
E890-E895,
1993
31.
Shoemaker, J. K.,
C. S. Hogeman,
U. A. Leuenberger,
M. D. Herr,
K. Gray,
D. H. Silber,
and
L. I. Sinoway.
Sympathetic discharge and vascular resistance after bed rest.
J. Appl. Physiol.
84:
612-617,
1998
32.
Stuart, C. A.,
R. E. Shangraw,
M. J. Prince,
E. J. Peters,
and
R. R. Wolfe.
Bed-rest-induced insulin resistance occurs primarily in muscle.
Metabolism
37:
802-806,
1988[Medline].
33.
Vukovich, M. D.,
P. J. Arciero,
W. M. Kohrt,
S. B. Racette,
P. A. Hansen,
and
J. O. Holloszy.
Changes in insulin action and GLUT-4 with 6 days of inactivity in endurance runners.
J. Appl. Physiol.
80:
240-244,
1996
34.
Yanagibori, R.,
Y. Suzuki,
K. Kawakubo,
Y. Makita,
and
A. Gunji.
Carbohydrate and lipid metabolism after 20 days of bed rest.
Acta Physiol. Scand., Suppl.
616:
51-57,
1994[Medline].
This article has been cited by other articles:
|
|
 |
|
  K. A. Burgomaster, N. M. Cermak, S. M. Phillips, C. R. Benton, A. Bonen, and M. J. Gibala Divergent response of metabolite transport proteins in human skeletal muscle after sprint interval training and detraining Am J Physiol Regulatory Integrative Comp Physiol, May 1, 2007; 292(5): R1970 - R1976. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. B Iglay, J. P Thyfault, J. W Apolzan, and W. W Campbell Resistance training and dietary protein: effects on glucose tolerance and contents of skeletal muscle insulin signaling proteins in older persons Am. J. Clinical Nutrition, April 1, 2007; 85(4): 1005 - 1013. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. M. Ferrara, A. P. Goldberg, H. K. Ortmeyer, and A. S. Ryan Effects of aerobic and resistive exercise training on glucose disposal and skeletal muscle metabolism in older men. J. Gerontol. A Biol. Sci. Med. Sci., May 1, 2006; 61(5): 480 - 487. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. K. Holten, M. Zacho, M. Gaster, C. Juel, J. F.P. Wojtaszewski, and F. Dela Strength Training Increases Insulin-Mediated Glucose Uptake, GLUT4 Content, and Insulin Signaling in Skeletal Muscle in Patients With Type 2 Diabetes Diabetes, February 1, 2004; 53(2): 294 - 305. [Abstract] [Full Text]
|
|
|
|
 |
|
 G. R. Adams, V. J. Caiozzo, and K. M. Baldwin Skeletal muscle unweighting: spaceflight and ground-based models J Appl Physiol, December 1, 2003; 95(6): 2185 - 2201. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J L Andersen, P Schjerling, L L Andersen, and F Dela Resistance training and insulin action in humans: effects of de-training J. Physiol., September 15, 2003; 551(3): 1049 - 1058. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Hamada, H. Sasaki, T. Hayashi, T. Moritani, and K. Nakao Enhancement of whole body glucose uptake during and after human skeletal muscle low-frequency electrical stimulation J Appl Physiol, June 1, 2003; 94(6): 2107 - 2112. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. Derave, B. O. Eijnde, P. Verbessem, M. Ramaekers, M. Van Leemputte, E. A. Richter, and P. Hespel Combined creatine and protein supplementation in conjunction with resistance training promotes muscle GLUT-4 content and glucose tolerance in humans J Appl Physiol, May 1, 2003; 94(5): 1910 - 1916. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Steensberg, C. P Fischer, M. Sacchetti, C. Keller, T. Osada, P. Schjerling, G. van Hall, M. A Febbraio, and B. K. Pedersen Acute interleukin-6 administration does not impair muscle glucose uptake or whole-body glucose disposal in healthy humans J. Physiol., April 15, 2003; 548(2): 631 - 638. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 W. J. Banz, M. A. Maher, W. G. Thompson, D. R. Bassett, W. Moore, M. Ashraf, D. J. Keefer, and M. B. Zemel Effects of Resistance versus Aerobic Training on Coronary Artery Disease Risk Factors Experimental Biology and Medicine, April 1, 2003; 228(4): 434 - 440. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. E. Hurlbut, M. E. Lott, A. S. Ryan, R. E. Ferrell, S. M. Roth, F. M. Ivey, G. F. Martel, J. T. Lemmer, J. L. Fleg, and B. F. Hurley Does age, sex, or ACE genotype affect glucose and insulin responses to strength training? J Appl Physiol, February 1, 2002; 92(2): 643 - 650. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Terada, T. Yokozeki, K. Kawanaka, K. Ogawa, M. Higuchi, O. Ezaki, and I. Tabata Effects of high-intensity swimming training on GLUT-4 and glucose transport activity in rat skeletal muscle J Appl Physiol, June 1, 2001; 90(6): 2019 - 2024. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. O.'t Eijnde, B. Ursø, E.A. Richter, P.L. Greenhaff, and P. Hespel Effect of Oral Creatine Supplementation on Human Muscle GLUT4 Protein Content After Immobilization Diabetes, January 1, 2001; 50(1): 18 - 23. [Abstract] [Full Text]
|
|
|
|
 |
|
 S. Blanc, S. Normand, C. Pachiaudi, J.-O. Fortrat, M. Laville, and C. Gharib Fuel Homeostasis during Physical Inactivity Induced by Bed Rest J. Clin. Endocrinol. Metab., June 1, 2000; 85(6): 2223 - 2233. [Abstract] [Full Text]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
) and after (
) 20 days of bed rest
in control subjects. B: response of
plasma insulin to 75-g oral glucose challenge before (