1 Departments of Medicine, This study tested
the hypothesis that increasing the protein content of isocaloric meals
increases the rate of myofibrillar synthesis in muscle of healthy
subjects over 60 yr old and enhances the stimulation of myofibrillar
synthesis induced by resistance exercise. Myofibrillar synthesis of
sedentary and exercised quadriceps muscle was determined by
incorporation of
L-[1-13C]leucine.
During the tracer infusion, subjects consumed meals with a low (7% of
energy, n = 6)-, normal (14%,
n = 6)-, or high (28%,
n = 6)-protein content. In sedentary
muscle, the mean (± SE) myofibrillar synthesis was 1.56 ± 0.13%/day in the low-protein group, 1.73 ± 0.11 %/day in the
normal-protein group, and 1.76 ± 0.10%/day in the high-protein
group (P = 0.42). Myofibrillar synthesis was faster in exercised muscle (mean 27%,
P < 10
muscle protein synthesis; amino acid concentrations; nutrition
MYOFIBRILLAR SYNTHESIS is ~30% slower in human
muscle over 60 yr old than in young adult muscle (37-39). Because
protein synthesis is necessary to maintain protein mass and protein
quality, this slowing of myofibrillar protein synthesis could
contribute to the diminished muscle mass and function in old age. The
most effective strategy for stimulating myofibrillar protein synthesis,
muscle bulk, and muscle strength is resistance training. This type of training can stimulate protein synthesis in both young and old human
muscle (3, 4, 7, 11, 29, 40, 41). Anecdotally, many athletes involved
in strength training claim that ingestion of large amounts of protein
enhances the hypertrophic response. There is some experimental evidence
to support this claim (14), but the effect of protein intake on
myofibrillar protein synthesis has not been examined. Although it is
known that feeding stimulates myofibrillar protein synthesis (39), the
relative importance of energy and protein intake in determining the
response to feeding is uncertain. In the present study, we tested the
hypothesis that myofibrillar synthesis in untrained muscle and the
stimulation of myofibrillar synthesis by resistance exercise are
proportional to protein intake when energy intake is constant.
Subjects
ABSTRACT
Top
Abstract
Introduction
Methods
Results
Discussion
References
6) in all groups (2.10 ± 0.14 %/day in low protein; 2.18 ± 0.10 %/day in normal
protein; 2.11 ± 0.09 %/day in high protein;
P = 0.84). The stimulation of
myofibrillar synthesis by exercise was not significantly different
among low-protein [0.54 ± 0.12 %/day (37 ± 9%)],
normal-protein [0.46 ± 0.08 %/day (28 ± 5%)], and
high-protein groups [0.34 ± 0.04 %/day (20 ± 3%);
P = 0.31]. We conclude that
high-protein meals do not enhance the stimulation of myofibrillar
protein synthesis induced by resistance exercise.
INTRODUCTION
Top
Abstract
Introduction
Methods
Results
Discussion
References
METHODS
Top
Abstract
Introduction
Methods
Results
Discussion
References
Procedures
Exercise protocol. The subjects exercised the quadriceps muscles of one leg (usually the right leg) on a Universal (Cedar Rapids, IA) knee extension machine. On day 1, the one repetition maximum (1RM) was determined. Subjects performed 4 sets of 10 repetitions, with brief rests between sets, at ~80% of the 1RM on days 1 and 4. On day 6 they performed 5 sets of 10 repetitions. The exercises were done between 1500 and 1530 on day 6, so that the muscle biopsies at the end of the protein synthesis determination were taken ~23 h after the final exercise session. Subjects were asked not to perform any strenuous activities involving the other leg but otherwise to continue with their normal activities and diet.
Feeding protocol. Subjects went to the University of Rochester General Clinical Research Center immediately after exercising on day 6. There they received a standard meal containing 10 kcal/kg body weight, with 10-15% of energy from protein. The meal was consumed before 2100, after which subjects were not fed until the protein synthesis determination was started on day 7.
Starting at 0700 on day 7, subjects consumed liquid meals every 30 min until the end of the study. The energy content of each meal was 6% of the Harris-Benedict daily basal metabolic rate (based on height, weight, and age) or ~4% of the daily energy requirement for weight maintenance. Thus each subject consumed ~60% of his or her daily energy requirement by the time the final muscle biopsy was taken. The subjects were divided into three groups of six (3 men and women in each group) according to the level of protein in the meals (as % of energy): 7%, 14%, or 28%. In a typical 80-kg subject consuming 2,800 kcal/day, the 14% protein level corresponds to a protein intake of 1.2 g · kg
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Protein synthesis determination. At 0800, a priming dose of L-[1-13C]leucine (Mass Trace, Woburn, MA) was given intravenously, followed by a 6.5-h intravenous infusion of this tracer. The priming dose was always 70% of the amount infused each hour during the continuous infusion. The continuous infusion was varied from 84 to 196 mg/h, depending on the size of the subject and the amount of protein fed, to produce similar plasma [13C]leucine enrichments in all subjects.
Plasma samples were obtained immediately before the start of the tracer infusion (time 0) and at 0.25, 0.5, 1, 2, 3, 4, 5, and 6 h after start of the infusion. Note that time 0 in Figs. 1 and 2 is 1 h after the start of meal feeding. Isotopic enrichment of plasma leucine andData analysis. Results are presented as means ± SE. The statistical significance of the effect of exercise, the level of protein intake, and their interaction on myofibrillar synthesis was determined by analysis of variance (NCSS 6.0; NCSS, Kaysville, UT). Other variables were measured only for descriptive purposes, so no hypothesis testing was performed for these variables.
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RESULTS |
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Average insulin concentrations during the tracer infusion were ~200-300 pmol/l in all groups, but mean insulin levels were ~70% higher in the high-protein group than in the other groups during the last 2 h of feeding (Fig. 1). Amino acid concentrations generally were proportional to the level of protein intake, as expected (Fig. 1). Because the HPLC column did not allow adequate resolution of some of the amino acids, results are not given for all of the amino acids. Leucine, isoleucine, valine, tyrosine, phenylalanine, and lysine concentrations were markedly affected by the level of protein intake. However, glycine and alanine concentrations were only marginally affected by the level of protein intake.
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Figure 2 shows the isotopic enrichments of plasma leucine and plasma KIC throughout the tracer infusion, and of muscle tissue free leucine and leucine extracted from myofibrillar proteins at the end of the tracer infusion. We were generally successful in our goal of keeping plasma leucine and KIC enrichments approximately the same in all subjects. The mean plasma leucine enrichments were 8-10%, and the mean KIC enrichments were 6-8%. As expected, KIC enrichment was closer to leucine enrichment in subjects with the highest protein intake. In subjects fed the low-protein and normal-protein meals, the free leucine enrichment in muscle at the end of the tracer infusion was only slightly less than the plasma KIC enrichment and was ~10% higher in the exercised muscle than in the sedentary muscle. In subjects fed the high-protein meals, the free leucine enrichment was the same in sedentary and exercised muscle and was nearly identical to the plasma leucine and KIC enrichments at the end of the infusion. Tracer enrichment of the leucine extracted from myofibrillar proteins was greater in the exercised muscle than in the sedentary muscle in all subjects.
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Mean myofibrillar protein synthesis rates are shown in Fig.
3. There was no evidence for an effect of
the level of protein intake on the rate of myofibrillar protein
synthesis either in sedentary muscle
(P = 0.42) or in exercised muscle
(P = 0.84). The exercised muscle had a
faster synthesis rate than the sedentary muscle in every subject, with
an average increase of 27% for all diet groups combined
(P < 106). Men and women had
similar fractional rates of myofibrillar synthesis in both sedentary
(1.75 ± 0.10%/day in men; 1.61 ± 0.06%/day in women,
P = 0.29) and exercised muscles (2.18 ± 0.10%/day in men; 2.08 ± 0.07%/day in women,
P = 0.43). The exercise-induced increase in myofibrillar synthesis tended to be greater in the subjects
fed the low-protein meals (37 ± 9%) than in those fed normal-protein meals (28 ± 5%) or high-protein meals (20 ± 3%), but the trend did not approach statistical significance
(P = 0.31). There was no difference
between men and women in the failure of increasing protein intake to
enhance the response to exercise (P = 0.14 for diet × gender × exercise interaction). However, the power to detect a significant gender influence on the interaction between diet and exercise was low (~25% to detect a 1 SD difference between men and women in the effect of diet on the response to exercise).
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DISCUSSION |
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The present study confirms previous reports that muscle protein
synthesis increases after resistance exercise (3, 4, 7, 11, 29, 40,
41). The magnitude of the effect of resistance exercise on muscle
protein synthesis has been quite variable and probably depends on the
intensity of the exercise more than any other factor. In studies done
the day after a resistance exercise session, the percent increase in
muscle protein synthesis ranged from 2% (not statistically
significant) to over 100% (7, 29, 38, 40). The stimulation of muscle
protein synthesis after resistance exercises persists for 24 h. In
subjects who had been performing resistance exercises for several
years, the average increase in muscle protein synthesis after a
resistance exercise session was 50% 4 h after the exercise,
109% 24 h after exercise, and only 14% (not statistically
significant) 36 h after exercise (7, 22). In young subjects who had not
previously engaged in resistance training, a single resistance exercise
session increased mean muscle protein synthesis 112% after 3 h, 65%
after 24 h, and 34% after 48 h (29). The 27% stimulation of
myofibrillar protein synthesis in the present study, after only three
exercise sessions, was greater than the nonsignificant 10% mean
increase observed in age-matched subjects after 3 mo of training in our previous study (38). However, the subjects in the present study performed twice as many repetitions (5 sets of 10 repetitions) the day
before protein synthesis was measured than the subjects in the previous
study (3 sets of 8 repetitions).
The major problem in determining protein synthesis rates in muscle is the uncertainty about the tracer enrichment of the aminoacyl-tRNA, the immediate precursor for incorporation of the tracer into proteins. Insufficient tissue is obtained by needle biopsy to directly measure this enrichment, so surrogate markers must be used. The plasma enrichment of KIC is a good index of leucyl-tRNA enrichment in resting muscle in postabsorptive dogs, pigs, and humans (1, 13, 34), but the effect of resistance exercise on the relation between intramuscular leucyl-tRNA enrichment and plasma KIC enrichment has not been studied. Recently it was reported that the tissue fluid free leucine enrichment is a good index of leucyl-tRNA enrichment in human muscle under various feeding conditions (17), but the effect of exercise was not specifically tested. We found that, for all diet groups combined, the mean enrichment of free leucine in the exercised muscle was 7% higher than that of the sedentary muscle (95% confidence interval of 0-13%). Thus we might have overestimated the effect of exercise on myofibrillar synthesis by using the same precursor enrichment (plasma KIC) for both sedentary and exercised muscle. Nevertheless, if the tissue free leucine enrichment at the end of the tracer infusion is an accurate index of leucyl-tRNA enrichment throughout the infusion, there was a significant increase of myofibrillar protein synthesis in the exercised muscle.
Even though older subjects have a slower rate of protein synthesis in untrained muscle than young adults (11, 30, 37-39, 41), there is no evidence that muscle protein synthesis is stimulated less by exercise in older muscle. To the contrary, some data (11, 41) suggest that the increase in protein synthesis after resistance exercises is greater in older muscle, at least in the early stages of training. Nevertheless, we observed that myofibrillar protein synthesis remained significantly slower in muscles of older subjects than in muscles of young adults after 3 mo of resistance training (38). These results prompted us to examine whether myofibrillar protein synthesis could be enhanced in older subjects in either sedentary or exercised muscles. Several lines of evidence suggested that increasing the protein intake might stimulate myofibrillar protein synthesis. Acute elevations of amino acid concentrations increase muscle protein synthesis in vitro (9, 16, 21) and in vivo (2, 4, 24, 31, 34). In fasting dogs, amino acid infusion markedly increases hindlimb protein synthesis (mostly muscle), whereas dextrose infusion is ineffective (5). Whole body protein synthesis and turnover in humans are more rapid in subjects consuming a high-protein diet than in those on a normal-protein diet (27, 28), an effect that is more pronounced in strength athletes (32). Increasing protein intake makes nitrogen balance more positive in both young and old subjects, including those performing resistance exercises (6, 8, 15, 27, 28, 32). It has been suggested that the minimum requirement for protein intake in persons performing heavy resistance exercises is about twice that of sedentary persons (14, 32).
Contrary to our hypothesis, there was no evidence that the stimulation of myofibrillar synthesis by resistance exercise was enhanced by increasing the protein intake over the range of 7-28% of energy intake as protein. This conclusion is based on the assumption that any differences in leucyl-tRNA 13C enrichment between sedentary and exercised muscles were not influenced by the level of protein intake. Although we could not measure leucyl-tRNA enrichment directly, the tissue free leucine enrichment may provide a good index. With the low-protein and normal-protein meals, the ratio of free leucine enrichment in exercised muscle to free leucine enrichment in sedentary muscle was ~1.1, whereas it was 1.0 with the high-protein meals. Thus the trend (which was not statistically significant) toward less stimulation of myofibrillar synthesis by exercise in the high-protein group might be explained by a slight overestimate of the exercise effect in the low-protein and normal-protein groups. Because free leucine enrichment in exercised and sedentary muscle was the same in the high-protein group, the exercise effect in this group is most likely to be quantitatively accurate. The high-protein feeding produces a situation similar to the flooding dose method, in which high doses of tracer are infused to equalize the tracer enrichment in all of the free amino acid pools (10). Future studies of the factors regulating the effect of exercise on muscle protein synthesis could use high-protein meals to minimize uncertainty about the tracer enrichment of the aminoacyl-tRNA.
We cannot exclude the possibility that protein intake would have influenced myofibrillar synthesis immediately after exercise. Biolo et al. (4) found that, in young subjects, the increase in muscle protein synthesis immediately after resistance exercises was >200% when amino acids were infused. This response was more than twice the stimulation in postabsorptive subjects in a similar study by the same group (3). The present study differed from that of Biolo et al. not only in examining protein synthesis after a longer postexercise delay, but also in the age of the subjects, provision of ordinary meals instead of intravenous amino acids, and examination of myofibrillar synthesis instead of total mixed muscle protein synthesis. Thus it is not particularly surprising that we did not verify that elevated amino acid levels enhance the stimulation of muscle protein synthesis by resistance exercise. The possibility that older subjects may not respond to the combination of exercise and high amino acid levels as much as young subjects is intriguing. The slower protein synthesis in older muscle seems to be caused by slower translation of mRNA, with no decline in total RNA or mRNA concentrations (35). The effects of both exercise and amino acids on protein synthesis are mediated, at least in part, by increased translation (7, 16). Thus the reduced translational efficiency in older muscle may prevent myofibrillar synthesis rates from exceeding the values observed in the present study.
It would be premature to conclude from our results that a high-protein
intake could not enhance the increase in muscle mass induced by
resistance training, because muscle mass is also determined by the rate
of muscle protein breakdown. There is some evidence that high levels of
branched-chain amino acids reduce the rate of protein breakdown in
human skeletal muscle in vivo (19, 20, 25). Whereas mixed muscle
protein breakdown increases immediately after resistance exercises in
postabsorptive subjects (3), it does not increase when subjects are
given an amino acid infusion (4). However, there is no evidence that a
high-protein diet inhibits the increase in the total daily degradation
of myofibrillar proteins induced by resistance training, as reflected
by 3-methylhistidine excretion in urine (6, 12). Campbell et
al. (6) reported that a high-protein diet (1.62 g · kg1 · day
1)
did not enhance the effect of resistance training on nitrogen balance
or muscle mass in healthy older subjects relative to effects observed
at the minimum recommended intake (0.8 g · kg
1 · day
1
), even though nitrogen balance was more positive on a high-protein diet both before and after training. Meredith et al. (23) reported that
a protein-containing supplement enhanced the hypertrophic response to
resistance exercises in older subjects. The supplement increased
overall energy intake as well as protein intake, so it is not possible
to evaluate the specific effect of protein in that study. The protein
requirement for muscle growth during resistance training is likely to
be higher when energy intake is low, and lower when energy intake is
high.
The present study confirms our previous finding (39) that feeding
increases myofibrillar protein synthesis. The myofibrillar synthesis
rate of ~1.7%/day in sedentary muscle is ~70% faster than the
rate in postabsorptive subjects of similar age in our previous studies
(37, 38). On the basis of data of Ljungqvist et al. (17), the ratio of
muscle tissue free leucine enrichment to plasma KIC enrichment is
~0.68 in postabsorptive subjects. In the present study this ratio
ranged from 0.88 to 1, depending on the protein intake. Thus about
one-half of the apparent effect of feeding could be an artifact of
assuming that the relation between plasma KIC enrichment and muscle
leucyl-tRNA enrichment is the same in postabsorptive and fed subjects,
but there still is a substantial effect of feeding. A recent abstract
indicated that meals did not increase muscle protein synthesis when the aminoacyl-tRNA enrichment was used to determine the rate of protein synthesis, but energy intake (1.26 kcal · kg1 · h
1)
was only ~55% of the energy intake of subjects in the present study
(18). In that study, muscle protein synthesis tended to decrease
(~10%) when the meals were pure carbohydrate and tended to increase
(~10%) when they contained protein, but the differences were not
statistically significant. Another study, using the phenylalanine disposal method to determine protein synthesis, confirmed that meals
with a high energy content (3.75 kcal · kg
1 · h
1,
22% of energy as protein) increase muscle (forearm) protein synthesis
(33).
It is somewhat surprising that the high-protein meals did not increase protein synthesis in the sedentary muscle more than the low-protein meals did, because raising levels of amino acids, without providing other energy sources, increase muscle protein synthesis in humans (2, 4, 31). Apparently, the level of energy intake used in the present study was adequate to maximize myofibrillar synthesis in sedentary muscle even when amino acid levels were not increased (low-protein group). Even though the plasma amino acid levels in the low-protein group were not elevated above values we usually observe in postabsorptive subjects, it is very likely that the flux of amino acids into the muscle was stimulated by the elevated insulin concentrations.
The present findings should not be generalized to long-term changes in dietary protein intake or to individuals consuming inadequate amounts of energy. It is important to note that the low-protein meals were given to subjects who were well nourished before the study. Chronic consumption of a low-protein diet, resulting in abnormally low levels of essential amino acids, could result in a reduced rate of muscle protein synthesis. Further research is needed to define the extent to which dietary protein intake can influence muscle protein metabolism.
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ACKNOWLEDGEMENTS |
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We thank the staff of the University of Rochester General Clinical Research Center for their technical assistance.
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FOOTNOTES |
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This research was supported by National Institutes of Health (NIH) Grants AG-13070, AG-10463, and RR-00044. Dr. Thornton was the recipient of an NIH Clinical Investigator Development Award during the conduct of this study.
Address for reprint requests: S. Welle, Monroe Community Hospital, 435 East Henrietta Rd., Rochester, NY 14620.
Received 18 August 1997; accepted in final form 16 January 1998.
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REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
1.
Baumann, P. Q.,
W. S. Stirewalt,
B. D. O'Rourke,
D. Howard,
and
K. S. Nair.
Precursor pools of protein synthesis: a stable isotope study in a swine model.
Am. J. Physiol.
267 (Endocrinol. Metab. 30):
E203-E209,
1994
2.
Bennet, W. M.,
A. A. Connacher,
C. M. Scrimgeour,
K. Smith,
and
M. J. Rennie.
Increase in anterior tibialis muscle protein synthesis in healthy man during mixed amino acid infusion: studies of incorporation of [1-13C]leucine.
Clin. Sci. (Colch.)
76:
447-454,
1989[Medline].
3.
Biolo, G.,
S. P. Maggi,
B. D. Williams,
K. D. Tipton,
and
R. R. Wolfe.
Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans.
Am. J. Physiol.
268 (Endocrinol. Metab. 31):
E514-E520,
1995
4.
Biolo, G.,
K. D. Tipton,
S. Klein,
and
R. R. Wolfe.
An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein.
Am. J. Physiol.
273 (Endocrinol. Metab. 36):
E122-E129,
1997
5.
Borel, M. J.,
P. E. Williams,
K. Jabbour,
J. C. Hibbard,
and
P. J. Flakoll.
Maintaining muscle protein anabolism after a metabolic stress: role of dextrose vs. amino acid availability.
Am. J. Physiol.
272 (Endocrinol. Metab. 35):
E36-E44,
1997[Abstract].
6.
Campbell, W. W.,
M. C. Crim,
V. R. Young,
L. J. Joseph,
and
W. J. Evans.
Effects of resistance training and dietary protein intake on protein metabolism in older adults.
Am. J. Physiol.
268 (Endocrinol. Metab. 31):
E1143-E1153,
1995
7.
Chesley, A.,
J. D. MacDougall,
M. A. Tarnopolsky,
S. A. Atkinson,
and
K. Smith.
Changes in human muscle protein synthesis after resistance exercise.
J. Appl. Physiol.
73:
1383-1388,
1992
8.
Fern, E. B.,
R. N. Bielinski,
and
Y. Schutz.
Effects of exaggerated amino acid and protein supply in man.
Experientia
47:
168-172,
1991[Medline].
9.
Fulks, R. M.,
J. B. Li,
and
A. L. Goldberg.
Effects of insulin, glucose, and amino acids on protein turnover in rat diaphragm.
J. Biol. Chem.
250:
290-298,
1975[Abstract].
10.
Garlick, P. J.,
M. A. McNurlan,
P. Essén,
and
J. Wernerman.
Measurement of tissue protein synthesis rates in vivo: a critical analysis of contrasting methods.
Am. J. Physiol.
266 (Endocrinol. Metab. 29):
E287-E297,
1994
11.
Hasten, D. L.,
J. Y. Pak,
J. R. Crowley,
and
K. E. Yarasheski.
Effects of resistance exercise on muscle protein synthesis in young, late middle-aged, and old men and women (Abstract).
FASEB J.
11:
A291,
1997.
12.
Hickson, J. F.,
and
K. Hinkelmann.
Exercise and protein intake effects on urinary 3-methylhistidine excretion.
Am. J. Clin. Nutr.
41:
246-253,
1985[Abstract].
13.
Horber, F. F.,
C. M. Horber-Feyder,
S. Krayer,
W. F. Schwenk,
and
M. W. Haymond.
Plasma reciprocal pool specific activity predicts that of intracellular free leucine for protein synthesis.
Am. J. Physiol.
257 (Endocrinol. Metab. 20):
E385-E399,
1989
14.
Lemon, P. W. R.
Is increased dietary protein necessary or beneficial for individuals with a physically active lifestyle?
Nutr. Rev.
54:
S169-S175,
1996[Medline].
15.
Lemon, P. W. R.,
M. A. Tarnopolsky,
J. D. MacDougall,
and
S. A. Atkinson.
Protein requirements and muscle mass/strength changes during intensive training in novice bodybuilders.
J. Appl. Physiol.
73:
767-775,
1992[Medline].
16.
Li, J. B.,
and
L. S. Jefferson.
Influence of amino acid availability on protein turnover in perfused skeletal muscle.
Biochim. Biophys. Acta
544:
351-359,
1978[Medline].
17.
Ljungqvist, O. H.,
M. Persson,
G. C. Ford,
and
K. S. Nair.
Functional heterogeneity of leucine pools in human skeletal muscle.
Am. J. Physiol.
273 (Endocrinol. Metab. 36):
E564-E570,
1997
18.
Ljungqvist, O. H.,
M. Persson,
J. Schimke,
G. C. Ford,
and
K. S. Nair.
Effect of meal-induced insulin on muscle protein synthesis: measurement using amino acyl tRNA (Abstract).
Diabetes
45:
103A,
1996.
19.
Louard, R. J.,
E. J. Barrett,
and
R. A. Gelfand.
Effect of infused branched-chain amino acids on muscle and whole-body amino acid metabolism in man.
Clin. Sci. (Colch.)
79:
457-466,
1990[Medline].
20.
Louard, R. J.,
E. J. Barrett,
and
R. A. Gelfand.
Overnight branched-chain amino acid infusion causes sustained suppression of muscle proteolysis.
Metabolism
44:
424-429,
1995[Medline].
21.
Lundholm, K.,
and
T. Schersten.
Leucine incorporation into proteins and cathepsin-D activity in human skeletal muscles. The influence of the age of the subject.
Exp. Gerontol.
10:
155-159,
1975[Medline].
22.
MacDougall, J. D.,
M. J. Gibala,
M. A. Tarnopolsky,
J. R. MacDonald,
S. A. Interisano,
and
K. E. Yarasheski.
The time course for elevated muscle protein synthesis following heavy resistance exercise.
Can. J. Appl. Physiol.
20:
480-486,
1995[Medline].
23.
Meredith, C. N.,
W. R. Frontera,
K. P. O'Reilly,
and
W. J. Evans.
Body composition in elderly men: effect of dietary modification during strength training.
J. Am. Ger. Soc.
40:
155-162,
1992[Medline].
24.
Mosoni, L.,
M.-L. Houlier,
P. P. Mirand,
G. Bayle,
and
J. Grizard.
Effect of amino acids alone or with insulin on muscle and liver protein synthesis in adult and old rats.
Am. J. Physiol.
264 (Endocrinol. Metab. 27):
E614-E620,
1993
25.
Nair, K. S.,
R. G. Schwartz,
and
S. Welle.
Leucine as a regulator of whole body and skeletal muscle protein metabolism in humans.
Am. J. Physiol.
263 (Endocrinol. Metab. 26):
E928-E934,
1992[Medline].
26.
National Research Council Food and Nutrition Board.
Recommended Dietary Allowances. Washington, DC: National Academy of Science Press, 1989.
27.
Pannemans, D. L. E.,
D. Halliday,
and
K. R. Westerterp.
Whole-body protein turnover in elderly men and women: responses to two protein intakes.
Am. J. Clin. Nutr.
61:
33-38,
1995[Abstract].
28.
Pannemans, D. L. E.,
D. Halliday,
K. R. Westerterp,
and
A. D. M. Kester.
Effect of variable protein intake on whole-body protein turnover in young men and women.
Am. J. Clin. Nutr.
61:
69-74,
1995[Abstract].
29.
Phillips, S. M.,
K. D. Tipton,
A. A. Aarsland,
S. E. Wolf,
and
R. R. Wolfe.
Mixed muscle protein synthesis and breakdown after resistance exercise in humans.
Am. J. Physiol.
273 (Endocrinol. Metab. 36):
E99-E107,
1997
30.
Rooyackers, O. E.,
D. B. Adey,
P. A. Ades,
and
K. S. Nair.
Effect of age on in vivo rates of mitochondrial protein synthesis in human skeletal muscle.
Proc. Natl. Acad. Sci. USA
93:
15364-15369,
1996
31.
Svanberg, E.,
A.-C. Möller-Loswick,
D. E. Matthews,
U. Körner,
M. Andersson,
and
K. Lundholm.
Effects of amino acids on synthesis and degradation of skeletal muscle proteins in humans.
Am. J. Physiol.
271 (Endocrinol. Metab. 34):
E718-E724,
1996
32.
Tarnopolsky, M. A.,
S. A. Atkinson,
J. D. MacDougall,
A. Chesley,
S. Phillips,
and
H. P. Schwarcz.
Evaluation of protein requirements for trained strength athletes.
J. Appl. Physiol.
73:
1986-1995,
1992
33.
Tessari, P.,
M. Zanetti,
R. Barazzoni,
M. Vettore,
and
F. Michielan.
Mechanisms of postprandial protein accretion in human skeletal muscle. Insight from leucine and phenylalanine forearm kinetics.
J. Clin. Invest.
98:
1361-1372,
1996
34.
Watt, P. W.,
Y. Lindsay,
C. M. Scrimgeour,
P. A. F. Chien,
J. N. A. Gibson,
D. J. Taylor,
and
M. J. Rennie.
Isolation of aminoacyl-tRNA and its labeling with stable-isotope tracers: Use in studies of human tissue protein synthesis.
Proc. Natl. Acad. Sci. USA
88:
5892-5896,
1991[Abstract].
35.
Welle, S.,
K. Bhatt,
and
C. Thornton.
Polyadenylated RNA, actin mRNA, and myosin heavy chain mRNA in young and old human skeletal muscle.
Am. J. Physiol.
270 (Endocrinol. Metab. 33):
E224-E229,
1996
36.
Welle, S.,
R. Jozefowicz,
and
M. Statt.
Failure of dehydroepiandrosterone to influence energy and protein metabolism in humans.
J. Clin. Endocrinol. Metab.
71:
1259-1264,
1990[Abstract].
37.
Welle, S.,
C. Thornton,
R. Jozefowicz,
and
M. Statt.
Myofibrillar protein synthesis in young and old men.
Am. J. Physiol.
264 (Endocrinol. Metab. 27):
E693-E698,
1993
38.
Welle, S.,
C. Thornton,
and
M. Statt.
Myofibrillar protein synthesis in young and old human subjects after three months of resistance training.
Am. J. Physiol.
268 (Endocrinol. Metab. 31):
E422-E427,
1995
39.
Welle, S.,
C. Thornton,
M. Statt,
and
B. McHenry.
Postprandial myofibrillar and whole body protein synthesis in young and old human subjects.
Am. J. Physiol.
267 (Endocrinol. Metab. 30):
E599-E604,
1994
40.
Yarasheski, K. E.,
J. A. Campbell,
K. Smith,
M. J. Rennie,
J. O. Holloszy,
and
D. M. Bier.
Effect of growth hormone and resistance exercise on muscle growth in young men.
Am. J. Physiol.
262 (Endocrinol. Metab. 25):
E261-E267,
1992
41.
Yarasheski, K. E.,
J. J. Zachwieja,
and
D. M. Bier.
Acute effects of resistance exercise on muscle protein synthesis rate in young and elderly men and women.
Am. J. Physiol.
265 (Endocrinol. Metab. 28):
E210-E214,
1993