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Departments of Medicine and of Cell Biology and Physiology, Washington University School of Medicine, St. Louis, Missouri 63110
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Exercise increases the expression of lipoprotein lipase (LPL) and GLUT-4 in skeletal muscle. Intense exercise increases catecholamines, and catecholamines without exercise can affect the expression of both LPL and GLUT-4. To test the hypothesis that adrenergic-receptor signaling is central to the induction of LPL and GLUT-4 by exercise, six untrained individuals [age 28 ± 4 (SD) yr, peak oxygen uptake 3.6 ± 0.3 l/min] performed two exercise bouts within 12 days. Exercise consisted of cycling at ~65% peak oxygen uptake for 60 min with (block trial) and without (control trial) adrenergic-receptor blockade. Exercise intensity was the same during the block and control trials. Plasma catecholamine concentrations were significantly higher and heart rates were significantly lower during the block trial compared with the control trial, consistent with known effects of adrenergic-receptor blockade. However, blockade did not prevent the induction of either LPL or GLUT-4 proteins assayed in biopsies of skeletal muscle. LPL was significantly increased by 170-240% and GLUT-4 was significantly increased by 32-51% at 22 h after exercise compared with before exercise during both the control and block trials. These findings provide evidence that exercise increases muscle LPL and GLUT-4 protein content via signals generated by alterations in cellular homeostasis and not by adrenergic-receptor stimulation.
catecholamines; lipid metabolism; glucose transport; 
-blocker; 
-blocker
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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CARBOHYDRATES AND FATTY ACIDS are the main fuel sources utilized during exercise and during recovery from exercise. Lipoprotein lipase (LPL), the rate-limiting factor for the metabolism of triglyceride-rich lipoproteins, and GLUT-4, the major glucose transporter of skeletal muscle, are critical for the acquisition of fatty acids and glucose during and after exercise. The uptake of substrates after exercise replenishes energy stores in preparation for the next bout of exercise and provides fuel for muscle repair and other recovery functions (15).
Exercise depletes high-energy phosphates in muscle and increases the concentration of AMP, causing activation of AMP-activated protein kinase (AMPK). Activation of AMPK probably mediates translocation of GLUT-4 into the sarcolemma with exercise (9, 20). Exercise also increases mRNA and protein levels of both GLUT-4 and LPL in skeletal muscle within 18 h after a bout of exercise (29, 31, 32). The signaling events leading to enhanced expression (probably by activation of transcription) of the GLUT-4 and LPL genes have not yet been identified. Catecholamines increase as a function of exercise intensity (6) and interact with G protein-coupled cell-surface receptors. Both catecholamines and exercise are known to increase intracellular concentrations of cAMP, a signaling molecule implicated in the expression of LPL in skeletal and cardiac muscle (3-5, 27).
Although catecholamines stimulate LPL expression in resting muscle (3-5, 27), it is unclear whether the striking rise in catecholamines seen with exercise contributes to exercise induction of LPL. It is also not known whether catecholamines increase GLUT-4 expression. In this paper, we specifically address the question of whether the increase in skeletal muscle LPL and GLUT-4 protein after exercise is caused by adrenergic-receptor stimulation during exercise. To answer this question, we measured skeletal muscle LPL and GLUT-4 protein content after a single bout of exercise performed in the presence and absence of adrenergic-receptor blockade.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Subjects. Subjects were healthy, active, but untrained individuals who regularly performed recreational physical activities. Body composition was estimated from hydrostatic weight. The study was approved by the Washington University Human Studies Committee. Informed consent was obtained from each subject.
Oxygen uptake.
A continuous cycle ergometer test was performed by each individual to
determine peak oxygen uptake
(
O2 peak). The protocol
consisted of cycling at 100, 150, and 200 W for 3 min per
exercise intensity, followed by 25 W increments every 1 min until
exhaustion. An automated on-line system was used to collect and analyze
expired air throughout the exercise test (Max-1, Physio-Dyne Instrument, Farmingdale, NY). Each subject met at least two of the
following criteria during the O2 peak
protocol: plateau in oxygen consumption with increasing work rate,
heart rate within 10 beats/min of age-predicted maximal heart rate, and
a respiratory exchange ratio exceeding 1.11.
Exercise trials. Two exercise trials, one with and one without adrenergic-receptor blockade, were completed within a 7- to 12-day period. The order of the trials was randomized. Subjects did not exercise the day before each trial.
Adrenergic-receptor blockade was achieved with the nonselective-blocker phenoxybenzamine (Dibenzyline, SmithKline Beecham Pharmaceuticals) and the nonselective -blocker propranolol (Inderal, Ayerst Laboratories). Phenoxybenzamine is an oral medication. It was not possible to obtain phentolamine, an intravenous -blocker, for this study. At the time of these experiments, phentolamine use in
the United States was limited to medical emergencies because of
manufacturing problems. As previously described (36),
-blockade with phenoxybenzamine was started 3 days before the
exercise trial at a dose of 10 mg by mouth four times per day
(day 1). The dosage was progressively increased to 20 mg
four times per day (day 2) and to 30 mg four times per day
(day 3), and then subjects ingested 40 mg 1.5 h before
the exercise bout on day 4. For -blockade (24), subjects received a primed (143 µg/kg) continuous
intravenous infusion of propranolol, beginning 30 min before the
exercise bout. At the start of exercise, the dosage was decreased to
1.4 µg · kg
1 · min1, and
infusion of propranolol was continued at this rate until 15 min after
the completion of exercise.
On each exercise day, a blood sample was obtained in the morning
after a 12-h fast. A vastus lateralis muscle biopsy was performed. Forty-five minutes later, subjects exercised for 1 h on an
electrically braked cycle ergometer at ~65%
O2 peak. Oxygen uptake was measured at
15 min-intervals during the exercise bout, and power output was
adjusted to maintain ~65% O2 peak.
After the exercise bout, subjects rested in bed for the next 22 h
in the Washington University General Clinical Research Center. Blood samples were obtained periodically from an indwelling catheter, and
muscle biopsies were performed 8 and 22 h after exercise. Diets
during the protocol were standardized and identical for the two trials.
Muscle biopsies.
Biopsies were performed as previously described
(31). After the initial biopsy, the contralateral leg was
used for the second biopsy. The third biopsy was performed 3 cm distal
to the site of the initial biopsy. The biopsies for the second trial
were performed in the same sequence as the first trial at sites 3 cm distal to the initial biopsies. Muscle samples were immediately cleansed with saline, trimmed of any visible fat, blotted dry, and
frozen in liquid nitrogen. Samples were then stored at 
80°C for
subsequent analysis. Muscle samples from all time points were analyzed
for LPL and GLUT-4 protein content by Western blotting as described
previously (30, 31). Antibody-bound protein
was visualized by using enhanced chemiluminescence (Amersham/Pharmacia Biotech). Protein bands were quantified by densitometry. Data are
expressed per protein content. As shown previously (32), acute exercise has no detectable effect on the control protein myosin
when this assay is used.
Blood sampling and analysis.
A polyethylene catheter was inserted into an antecubital vein in the
morning before the initial biopsy and kept patent with saline. Blood
samples were obtained from the subjects before the initial biopsy,
immediately before exercise, at 30 min of exercise, and just before
completion of exercise. In addition, blood samples were obtained every
30 min for the first 2.5 h after exercise and then every 1 h
for the next 6 h. Samples were subjected to centrifugation (15 min
at 2,000 g), and the supernatant was collected and stored at
80°C until subsequent analyses. Samples were analyzed for insulin
(25), catecholamines (33), leptin
(23), glucose (Sigma Chemical, St. Louis, MO), and
nonesterified fatty acids (Waco Chemicals, Dallas TX). Lipid and
lipoprotein levels were measured after a 12-h fast in accordance with
the Centers for Disease Control lipid standardization program.
Statistics. Muscle protein content of LPL and GLUT-4 as well as plasma samples were analyzed by using two-way repeated-measures analysis of variance. A Tukey post hoc test was performed when the analysis of variance revealed significant differences.
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RESULTS |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Subject characteristics are shown in Table
1. Exercise intensities during
the two trials were not significantly different (Table
2). Heart rates were significantly lower
during exercise for the block trial compared with the control trial
(Table 2). Plasma epinephrine (Fig.
1A) and norepinephrine (Fig.
1B) concentrations were significantly higher during exercise
for the block trial compared with the control trial, an expected result
because receptor blockade interferes with normal catecholamine
clearance. Lower heart rates and higher catecholamine levels during the
block trial indicate that adrenergic-receptor blockade was successful.
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Muscle LPL protein content.
Skeletal muscle biopsies were performed before and at 8 and 22 h
after the exercise bout for both trials. Muscle was assayed for LPL and
GLUT-4 protein content. The absolute amounts of muscle tissue LPL and
GLUT-4 were variable between individuals. Therefore, LPL and GLUT-4
signals for each individual were compared with signals in the
preexercise sample for each trial, and data were analyzed by
repeated-measures analysis of variance to focus on differences
associated with the intervention rather than differences between
individuals. As shown in Fig. 2,
left, LPL protein in the control trial was increased 8 h after exercise in the control trial. At 22 h after
exercise in the control trial, LPL protein was increased by 170 ± 100% (P < 0.05). The same pattern was seen in the
block trial (Fig. 2, right). At 22 h postexercise, LPL protein content was 240 ± 110% greater than baseline
(P < 0.05) even though exercise was performed in the
setting of both - and -blockade.
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Muscle GLUT-4 protein content.
GLUT-4 protein content was also elevated after exercise bouts in both
the control and block trials (Fig. 3).
GLUT-4 protein content was already elevated 8 h after exercise in
each trial. By 22 h postexercise, GLUT-4 protein content was
increased by 51 ± 16% (P < 0.05) in the control
trial and by 32 ± 6% (P < 0.05) in the block
trial compared with baseline.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Our results confirm that a single bout of exercise increases skeletal muscle LPL protein content (32). Several previous studies have reported the induction of GLUT-4 protein after 7-10 days of endurance exercise (2, 7). A prolonged, single bout of exercise is known to increase skeletal muscle GLUT-4 expression in rats (29). To the best of our knowledge, the present results represent initial data showing that a single bout of exercise also increases GLUT-4 protein in the skeletal muscle of humans.
The present results also provide insight into the mechanisms
underlying the induction of these two proteins that are critical for
normal glucose and lipid metabolism. Catecholamines increase as a
function of exercise intensity (6), and interact with G
protein-coupled adrenergic cell-surface receptors to affect numerous
metabolic pathways. Blocking adrenergic receptors by using
phenoxybenzamine (a nonspecific -blocker) and propranolol (a
nonspecific -blocker) during exercise did not prevent the induction
of LPL and GLUT-4 protein in human skeletal muscle. These results
suggest that, even in the absence of stimulation by catecholamines,
skeletal muscle can activate signaling pathways that produce a
coordinated response to ensure fuel acquisition.
At least for LPL, several lines of evidence suggest that catecholamines are involved in the response to exercise. Catecholamines increase cAMP, cAMP levels are increased as a function of exercise or in response to elevated plasma catecholamine concentrations (17, 21), and a cAMP-response element is present in the human LPL promoter (16). Urinary excretion rates of catecholamines account for >80% of the variability in human skeletal muscle LPL activity (22). Infusion of either epinephrine or isoproterenol increases skeletal muscle LPL expression in humans and rodents (3, 4, 27). Catecholamines also increase LPL activity in rat cardiac muscle (5).
The present results suggest that signaling induced by the interaction
between catecholamines and adrenergic receptors is not required for the
exercise-induced increase in LPL protein content. A previous study in
humans concluded that local contractile activity is responsible for
increased LPL activity in muscle (14), but it did not
preclude possible local effects of catecholamines released from nerves
innervating exercising muscles. By using systemic adrenergic-receptor
blockade, our data also show that catecholamines released locally as a
consequence of contractile activity do not play a critical role in LPL
induction. Taken together with a study in rats (8),
available data indicate that muscle contraction itself induces LPL. The
mediator of this effect is unknown, although cAMP is an attractive
candidate. cAMP levels are elevated during exercise even with
-blockade (17, 18).
Studies of the effects of catecholamines on GLUT-4 are less consistent.
Short-term infusion of epinephrine in rats after surgical removal of
the adrenal medulla decreases GLUT-4 transcription (13),
suggesting that catecholamines decrease GLUT-4 expression. Rats
subjected to -blockade during 6 wk of exercise training show no
increase in muscle GLUT-4, suggesting that catecholamines are necessary
for the exercise-induced increase in GLUT-4 (19). The
present results do not support this interpretation. One possible explanation for this apparent discrepancy is the fact that the rat
study measured GLUT-4 
48 h after exercise, a time point at which
adaptive changes in GLUT-4 would be reversed (12).
LPL protein content usually reflects LPL enzyme activity in skeletal muscle (31, 35). Under most circumstances, GLUT-4 protein content reflects the capacity of skeletal muscle to carry out glucose transport (10, 29, 30). Protein levels for LPL and GLUT-4 in the present study are probably elevated because of increased message levels. Previous studies by our laboratory using humans show that an increase in skeletal muscle LPL mRNA precedes an increase in LPL protein after exercise (32). Previous studies by our laboratory using rodents show that exercise induces GLUT-4 mRNA and protein (29). Others have demonstrated an increase in GLUT-4 transcription with exercise (26). Therefore, it is likely that exercise activates a transcriptional signaling pathway independent of adrenergic receptors to increase LPL and GLUT-4 protein. A critical issue is the nature of the signaling pathways that modulate activation of transcription by exercise.
AMPK, activated by energy depletion in muscle, is likely to be involved in the induction of exercise-responsive genes. Growing evidence implicates this kinase in GLUT-4 translocation (9, 20), and recent data indicate that AMPK induces GLUT-4 and hexokinase expression (11). However, the downstream mediators of AMPK are unknown. The mitogen-activated protein kinase pathway may be involved. Muscle contraction is a potent activator of this pathway (1). Mitogen-activated protein kinase may be responsible for the increased transcription of immediate-early genes in skeletal muscle after exercise (34).
Insulin-receptor signaling may also be involved in exercise responses. Skeletal muscle contraction has striking metabolic effects in the absence of insulin (28). Consistent with this notion, exercise increases skeletal muscle glucose transport in muscle-specific insulin-receptor knockout mice (37). However, insulin potentiates the exercise effect in these mice without skeletal muscle insulin receptors, suggesting that perhaps insulin receptors in nonmyocytes or insulin interacting with other receptors can affect exercise responses. In the present study, adrenergic-receptor blockade was associated with lower plasma insulin levels during exercise (Fig. 4A). Adrenergic-receptor signaling has complex effects on insulin secretion and action (38). Because lower insulin levels were seen without differences in plasma glucose (Fig. 4B), adrenergic-receptor blockade may modestly enhance insulin signaling during exercise, at least under the conditions of this experiment.
In summary, a single bout of exercise increases human skeletal muscle
LPL and GLUT-4 protein content in the setting of both - and
-adrenergic-receptor blockade. Muscle contraction itself, perhaps
acting in response to depletion of high-energy phosphate stores,
appears to mediate fuel acquisition by muscle.
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ACKNOWLEDGEMENTS |
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We appreciate the commitment of our study subjects.
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FOOTNOTES |
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This work was supported by National Institute of Health (NIH) Grants AG-14658, HL-58427, and DK-53198; by the Washington University General Clinical Research Center (MO1 RR-00036); and by the Washington University Diabetes Research and Training Center (DK-20579). J. S. Greiwe was supported by NIH Institutional National Research Service Award AG-0078.
Address for reprint requests and other correspondence: C. F. Semenkovich, Washington Univ. School of Medicine, 660 S. Euclid Ave., Box 8046, St. Louis, MO 63110 (E-mail semenkov{at}im.wustl.edu).
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.
Received 11 February 2000; accepted in final form 23 March 2000.
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METHODS
RESULTS
DISCUSSION
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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]
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G. N. Kraniou, D. Cameron-Smith, and M. Hargreaves Acute exercise and GLUT4 expression in human skeletal muscle: influence of exercise intensity J Appl Physiol, September 1, 2006; 101(3): 934 - 937. [Abstract] [Full Text] [PDF]
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F. Magkos, D. C. Wright, B. W. Patterson, B. S. Mohammed, and B. Mittendorfer Lipid metabolism response to a single, prolonged bout of endurance exercise in healthy young men Am J Physiol Endocrinol Metab, February 1, 2006; 290(2): E355 - E362. [Abstract] [Full Text] [PDF]
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 G. N. Kraniou, D. Cameron-Smith, and M. Hargreaves Effect of short-term training on GLUT-4 mRNA and protein expression in human skeletal muscle Exp Physiol, September 1, 2004; 89(5): 559 - 563. [Abstract] [Full Text] [PDF]
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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]
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J. Q. Zhang, B. Smith, M. M. Langdon, H. L. Messimer, G. Y. Sun, R. H. Cox, M. James-Kracke, and T. R. Thomas Changes in LPLa and reverse cholesterol transport variables during 24-h postexercise period Am J Physiol Endocrinol Metab, August 1, 2002; 283(2): E267 - E274. [Abstract] [Full Text] [PDF]
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F. W. Booth, M. V. Chakravarthy, S. E. Gordon, and E. E. Spangenburg Waging war on physical inactivity: using modern molecular ammunition against an ancient enemy J Appl Physiol, July 1, 2002; 93(1): 3 - 30. [Abstract] [Full Text] [PDF]
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 A. Steensberg, G. van Hall, C. Keller, T. Osada, P. Schjerling, B. Klarlund Pedersen, B. Saltin, and M. A Febbraio Muscle glycogen content and glucose uptake during exercise in humans: influence of prior exercise and dietary manipulation J. Physiol., May 15, 2002; 541(1): 273 - 281. [Abstract] [Full Text] [PDF]
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J. S. Greiwe, G. Kwon, M. L. McDaniel, and C. F. Semenkovich Leucine and insulin activate p70 S6 kinase through different pathways in human skeletal muscle Am J Physiol Endocrinol Metab, September 1, 2001; 281(3): E466 - E471. [Abstract] [Full Text] [PDF]
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G. D. Wadley, R. J. Tunstall, A. Sanigorski, G. R. Collier, M. Hargreaves, and D. Cameron-Smith Differential effects of exercise on insulin-signaling gene expression in human skeletal muscle J Appl Physiol, February 1, 2001; 90(2): 436 - 440. [Abstract] [Full Text] [PDF]
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P. Schjerling, M. Hargreaves, D. Cameron-Smith, and Y. Kraniou The Importance of Internal Controls in mRNA Quantification J Appl Physiol, January 1, 2001; 90(1): 401 - 402. [Full Text] [PDF]
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0.05 compared with control samples at the same time
point.