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Department of Human Nutrition, Kansas State University, Manhattan, KS 66506-1407 and * Department of Community Health Sciences, King Saud University, Riyadh 11433, Saudi Arabia
3To whom correspondence should be addressed.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • dietary protein • muscular growth • functional overload • rats
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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), it is
highly plastic when forced to assume a greater mechanical load. For
example, muscle growth occurs as a result of weight-lifting
exercise (Garner et al. 1991
, Wong and Booth 1988
), weighted stretch (Antonio and Gonyea 1993b
, Gollnick et al. 1983
) or the
addition of load in various experimental models (Caiozzo et al. 1992
, Haddad et al. 1998
, Watt et al. 1982
). In the functional overload model, muscles are forced to
grow after tenotomy or removal of synergist muscles (Ianuzzo et al. 1991
, Noble et al. 1984
, Sugiura et al. 1993
, Tsika et al. 1987a
, 1987b
and 1987c
).
As a result, they exhibit an increase in muscle mass, total protein and
myofibrillar protein (Noble et al. 1984
, Tsika et al. 1987a
), and shifts in myosin isoform expression from fast
to slow (Ianuzzo et al. 1991
, Sugiura et al. 1993
, Tsika et al. 1987c
). These responses have
been attributed to the added weight-bearing stress imposed on the
muscles (Tsika et al. 1987b
), because when hindlimbs are
unweighted, changes in muscle size and myosin isoform distribution are
minimized (Tsika et al. 1987b
and 1987c
).
The primary objective of our study is to examine dietary protein
effects on growth of functionally overloaded muscle in rats. Dietary
protein effects on skeletal muscle have been studied in normally
growing animals (Hill et al. 1970
, Laurent et al. 1984
, Millward and Waterlow 1978
, Smith et al. 1982
). However effects during protocols designed
specifically to enhance muscular growth are largely unknown. Because
skeletal muscle is a major reservoir of nitrogen, a study of factors
that both initiate and regulate its growth is warranted. Furthermore,
protein supplementation is commonly practiced by humans to enhance
muscular growth during weight-training programs (Applegate and Grivetti 1997
, Grunewald and Bailey 1993
,
Kreider 1999
).
In this investigation, we examined the effects of three levels of protein intake (7, 17.5 or 30 g/100 g) on muscle growth induced by functional overload in rats. The two muscles selected for study were the slow-twitch soleus and fast-twitch plantaris hindlimb muscles. Dietary protein effects on overloaded muscles were examined for characteristics associated with growth such as muscle mass, total protein content, myofibrillar protein content and myosin heavy chain (MHC)4 isoform expression.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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This study was approved by the Institutional Animal Care and Use
Committee of Kansas State University and was performed according to the
guidelines of the National Institutes of Health on the experimental use
of laboratory animals (NRC 1985
).
Male Sprague-Dawley weanling rats (Harlan Sprague Dawley, Indianapolis, IN) were housed in individual plastic cages under a controlled temperature of 24°C and a 12-h light:dark cycle. When rats reached body weights of 220–240 g (8 wk of age), they were anesthetized with halothane, and the gastrocnemius muscle was removed from the left hindlimb to induce compensatory growth of the underlying plantaris and soleus muscles. The right hindlimb was sham-operated to serve as an intra-animal control.
Immediately after the surgical protocol, the rats were allocated
randomly to one of three experimental diets (Harlan Teklad, Madison,
WI) (Table 1
). Three different levels of dietary protein were tested, CON (control
or adequate protein, 17.5%), HP (high protein, 30%) or LP (low
protein, 7%). Control rats had free access to the AIN-76A diet
(AIN 1977
) (CON). The other two experimental diets were
formulated to be nutritionally similar to the CON diet except for
protein. Cellulose concentration was lower in the HP diet as a result
of dietary formulation. The Ca-P–deficient mineral mix (TD 79055) was
used in the protein-modified diets to correct for the phosphorus
contributed by the casein. When used at the levels employed in our
protein-modified diets, it supplied mineral elements (other than Ca
and P) similar to those provided by 35.0 g/kg AIN-76 mineral mix in the
control diet. Rats in all three groups had free access to food and
water. Food intake was measured daily by subtracting the amount
remaining from that given the day before.
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Analytical procedures.
Serum free fatty acids (FFA) were assayed by the colorimetric method of
Duncombe (1964)
with modifications by Noma et al. (1973)
and Laurell and Tibbling (1966)
. Blood
urea nitrogen (BUN) was measured by a colorimetric procedure (Sigma Kit
no. 535, Sigma Chemical, St. Louis, MO). Serum glucose was determined
by the glucose oxidase method (Sigma Kit no. 510). Serum albumin levels
were assayed using a colorimetric procedure (Sigma Kit no. 631). The
glycerol used to store the muscles did not interfere with the assay
procedures.
Washed myofibrils preparation.
Myofibrils were washed and prepared according to the method of
Talmadge and Roy (1993)
. Frozen muscles were minced with
scissors in 10 vol of ice-cold homogenization buffer [250 mmol/L
sucrose, 100 mmol/L KCl, 5 mmol/L EDTA, and 20 mmol/L Tris (base), pH
6.8]. The muscle minces then were homogenized by a high speed
Brinkmann Homogenizer (Sybron, Westbury, NY). Total protein was
determined on 0.1 mL of the homogenate using the Bio-Rad protein
assay (Bio-Rad Laboratories, Hercules, CA); the remainder of the
homogenate was centrifuged in 4°C at 1000 x g
for 10 min. The supernatant was discarded and the myofibril pellet was
resuspended in wash solution [175 mmol/L KCl, 20 mmol/L Tris (base), 2
mmol/L EDTA, 0.5% Triton X-100, pH 6.8 (cold)] using the same volume
as for the homogenization buffer. It then was centrifuged as above, and
the supernatant was discarded. The washing step was repeated for a
second time, and the resultant myofibril pellet was resuspended in 0.5
vol of resuspension buffer [150 mmol/L KCl, 20 mmol/L Tris (base), pH
7.0 (cold)]. The myofibril solution was used to determine myofibrillar
protein content and electrophoretic assays.
Electrophoresis.
The electrophoresis was run in a Bio-Rad Mini-Protean II Dual Slab
Cell electrophoretic system utilizing a Bio-Rad 1000/500 power
supply. Gels and running buffers were prepared as described previously
by Talmadge and Roy (1993)
. The washed myofibrils were
boiled in sample buffer [1% mercaptoethanol (v/v), 138.7 mmol/L SDS,
160 mmol/L Tris (base), 25% glycerol (v/v), 2g/L bromophenol blue]
for 1 min at a final concentration of 0.125 µg/L
immediately before loading, cooled to room temperature, and 5
µL were loaded into each well. The entire
electrophoresis apparatus was placed in the refrigerator for the period
of running (24 h) at 80 V (constant voltage). The gels then were silver
stained (Bio-Rad silver stain plus kit) because silver staining had
been used successfully on these gels before (Talmadge and Roy 1993
). This procedure provides highly repeatable, high
resolution separation of MHC protein isoforms. (Talmadge and Roy 1993
). Bands were quantified using a Hewlett-Packard 6100C
ScanJet scanner (Hewlett-Packard, Palo Alto, CA) and Sigma Gel
version1.1 software (John Dell Scientific, Chicago, IL).
Statistical analysis.
A randomized complete block design blocking for body weight and the day
of surgery was used. There were three dietary treatments, two legs
(overloaded vs. sham for each rat), and 10 rats for each dietary
treatment. The response tested was the difference between the
overloaded and sham legs. ANOVA were used followed by the
Least-Squares Means option in SAS (1982)
. Both linear and quadratic
contrast were used to detect the main effect of the diet. A
P-value of < 0.05 was considered significant.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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After 4 wk, rats fed the LP diet gained less weight (-29%) but ate
more food (+4%) and had lower feed efficiencies (-33%) than CON rats
(P < 0.05) (Table 2
). Average daily protein consumption of the LP rats was less than half
that of CON rats (P < 0.05). Rats fed the HP diets did
not differ in weight gain, feed intake, and feed efficiency from CON
rats; however, their average daily protein consumption was 69% higher
(P < 0.05).
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Rats fed the LP diet had lighter livers (-20%) and kidneys (-16%)
than CON rats fed 17.5% protein (P < 0.05); those
organs were also significantly smaller when normalized to body weight
(g/100 g body wt) (P < 0.05) (Table 3
). Absolute heart weights did not differ between LP and CON rats, but LP
rats had heavier normalized heart weights (P < 0.05).
Fat pad weights (epididymal, retroperitoneal, omental), serum albumin,
FFA and glucose concentrations did not differ between LP and CON rats.
However, LP rats had lower BUN levels (P < 0.05).
Measurements of HP rats were not different from those of CON rats
except that HP rats had heavier kidneys (+6%), higher BUN and lower
serum albumin levels (P < 0.05).
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We first examined dietary protein effects in each leg separately (sham
or overloaded). Rats fed the LP diet had smaller plantaris weights (mg)
(sham, -10%; overloaded, -11%; P < 0.05), which
contained less protein (sham, -11%; overloaded, -12%) and
myofibrillar protein (sham, -16%; overloaded, -14%; P
< 0.05) than those of CON rats (Table 4
). However, plantaris weights from both legs of LP and CON rats did not
differ when normalized to body weight (mg/100g body wt). The rats fed
the 30% HP diet had plantaris weights (absolute and normalized), total
protein, and myofibrillar protein contents that did not differ from
those of CON rats.
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. The differences in plantaris weights,
total protein and myofibrillar protein content between those muscles
did not differ among rats fed the CON, LP and HP diets. Mean values for
the three groups fell within a relatively narrow range. Overall,
overloaded plantaris muscles were heavier (+42 to +45%) and contained
more total protein (+42 to +46%) and myofibrillar protein (+40 to
+44%) than sham-operated muscles. Soleus growth.
Rats fed the LP diet had smaller soleus weights (mg) (sham, -16%;
overloaded, -16%; P < 0.05), which contained less
protein (sham, -17%; overloaded, -19%) and myofibrillar protein
(sham, -16%; overloaded, -17%) than those of CON rats (P
< 0.05) (Table 5
). When soleus weights were normalized to body weight, sham-operated
muscles were smaller for LP than CON rats (P < 0.05).
Rats fed the 30% HP diet and CON rats did not differ in soleus weights
(absolute and normalized), and contents of total protein and
myofibrillar protein.
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Myosin heavy chain isoforms.
The four MHC bands of the plantaris (I, IIa, IIx, IIb) and the two MHC
bands of the soleus (I and IIa) were resolved clearly using this
procedure (Fig. 1
). Rats fed the CON, LP and HP diets for 4 wk had similar MHC
distribution in plantaris muscles (types I, IIa, IIx, IIb) and in
soleus muscles (types I, IIa) (data not shown). The MHC distribution of
those muscles did not differ between sham-operated and overloaded
muscles.
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|
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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To our knowledge, our investigation is the first to show the effect of
dietary protein level on muscular growth during protocols designed
specifically to induce this effect. Other trials have demonstrated
dietary protein effects during endurance exercise using several
different modes of training (Luczak-Szczurek and Flisinska-Bojanowska 1997
, Tagliaferro et al. 1990
, Tsuji et al. 1975
). However, the focus of
our study was to examine effects of low or high protein feeding during
a period of stimulated rapid muscular growth.
The increases in muscle mass as a result of the loading procedure were
maintained even in rats fed the 7% LP diet, even though other indices
of growth were reduced. For example, after 4 wk, the LP rats gained
less weight and had smaller livers and kidneys than control rats, but
their loaded plantaris and soleus muscles still weighed more than
sham-operated muscles. This response suggests that the muscular
growth resulting from the overloading procedure was a high
physiological priority that could be maintained during nutritional
inadequacy. It also suggests that muscular contractile activity, as a
component of weight-bearing, was important for the maintenance of
mass in these muscles. Similar findings have been observed in other
studies involving nutritional deprivation. Mice fed a reduced amount of
food and trained to pull a cord had larger biceps brachii muscles than
untrained mice (Goldspink 1964
). Stretch exercise
applied to extensor digitorum longus muscles made them more resistant
to the effects of starvation (Goldspink 1978
). When low
protein diets were fed, skeletal muscle mass and protein were conserved
to a greater degree than were visceral organs of rats (Addis et al. 1936
, Garlick et al. 1975
).
The low protein diets fed to rats in our trial also may have been
utilized more efficiently. The lower BUN levels in LP rats suggests
that less protein was used for energy. However, energy intake was not a
limiting factor for growth in our trial because all diets were
isocaloric and rats were allowed free access to food. In fact, the
LP-fed rats consumed slightly more energy (+4%) than control rats,
but their overall weight gain and feed efficiency were still lower,
which has been observed previously for low protein diets (Mohan and Rao 1983
, Tulp et al. 1979
).
Our study also showed that high protein feeding (30% protein) did not
enhance or affect the muscular growth induced by functional overload in
plantaris or soleus muscles over that obtained by feeding the control
diet (17.5% protein). Total protein or myofibrillar protein contents
in those muscles also were not altered. The HP-fed rats had similar
voluntary energy intake, body weight gain, and liver and heart weights
compared with control rats These data suggest that additional protein
availability over that recommended for normal growth does not further
enhance muscular growth. However our rats had larger kidneys than
control rats, a finding that has been reported previously for high
protein–fed rats (Murray et al. 1993
), and higher BUN
levels. Other studies have shown that high protein intake is unlikely
to have any beneficial effect on the musculature in rats
(Laurent et al. 1984
, Taillandier et al. 1996
).
We studied dietary protein effects on plantaris and soleus muscles to
examine growth responses in two different muscle types. The soleus is a
postural, antigravity muscle comprised predominantly of slow-twitch
fibers, whereas the plantaris is a phasic muscle comprised of
fast-twitch muscles (Schiaffino and Reggiani 1996
).
The addition of functional load increased mass of both muscles.
However, this stimulated growth was not affected by level of dietary
protein for either plantaris or soleus muscle. Thus, we conclude that
the induced growth response could be maintained by two muscles that are
metabolically and functionally different during short-term protein
deficiency or excess.
We also studied dietary protein effects on MHC isoform expression in
muscle. Myosins are among the most abundant of skeletal muscle
proteins, and four distinct MHC isoforms are expressed in rodent limb
muscle (Pette and Staron 1990
). Myosin heavy chain
composition has been correlated with muscle fiber type (Oishi 1993
, Staron 1991
). Slow-twitch muscle such
as the soleus expresses type I MHC and smaller amounts of IIa, whereas
fast-twitch muscles such as the plantaris express type IIa, IIb and
IIx MHC (Demirel et al. 1999
, Sullivan et al. 1995
). Those MHC distributions were observed in the plantaris
and soleus muscles in our study.
Relatively few studies have examined diet effects on MHC isoform
contents in muscles. Taillandier et al. (1993)
found
that high protein feeding in hindlimb-suspended rats sustained
protein synthesis in slow-twitch soleus muscle. However, a later
study showed that high protein diets did not prevent the growth
reduction in fast-twitch tibialis anterior muscle in
hindlimb-suspended rats (Taillandier et al. 1996
).
In our trial, low protein or high protein feeding did not affect MHC
ratios in soleus or plantaris muscles. Therefore MHC distribution in
these muscles appears to be fairly stable and resistant to
short-term (4 wk) alterations in dietary protein intake.
Several investigators have observed MHC isoform shifts from fast to
slow in muscles forced to assume a greater load after surgical removal
of synergist muscles (Ianuzzo et al. 1991
,
Sugiura et al. 1993
, Tsika et al. 1987c
);
however, this was not observed in our study. The reason for this is not
clear, but it is possible that the sham-operated contralateral leg
was favored after surgery, thus altering its MHC gene expression and
resultant intra-animal differences. The extent of this effect could
be assessed by comparisons with an additional control group consisting
of animals having both limbs sham-operated with gastrocnemius
muscles intact, but our experimental design did not include this
treatment. We did not find any differences in MHC isoform profiles when
making intra-animal comparisons between sham-operated and
overloaded muscles or interanimal comparisons across all three diet
groups.
It is also possible that there was an expression of immature isoforms
of MHC, which were not measured in our trial. In a study employing
monoclonal antibodies, Dunn and Michel (1997)
found that
overloaded rat plantaris muscles exhibited a transient reexpression of
two embryonic MHC and the neonatal isoform in preexisting myofibers.
Future studies might be directed toward an assessment of dietary
effects on those isoforms during conditions of normal or induced
muscular growth.
Results of our study may not be applicable directly to humans who are
participating in resistance training programs to increase muscle mass
(i.e., sets and repetitions). In fact, developing a comparable protocol
for laboratory animals in an experimental setting is a challenge
(Timson 1990
). Several other methods used to induce
muscular growth in animals include the weighted/stretched avian wing
(Antonio and Gonyea 1993a
, Gollnick et al. 1983
), muscle activity initiated by electrical stimulation
(Caiozzo et al. 1992
, Garner et al. 1991
,
Wong and Booth 1988
) and various other exercise regimens
and/or mechanical devices (Haddad et al. 1998
,
Watt et al. 1982
). We selected the compensatory growth
model for our study because it has well-documented effects on
muscle growth and composition (Ianuzzo et al. 1991
,
Noble et al. 1984
, Tsika et al. 1987a
),
produces rapid gains in muscle mass over a short time and does not
require animals to do mechanical work in return for a reward such as
food. Furthermore, the intra-animal control aspect of this method
allows for the comparison of genetically identical sham-operated
and overloaded muscles exposed to the same diet.
In conclusion, the results of this study illustrate for the first time effects of dietary protein level on skeletal muscle growth induced by functional overload. We studied effects in two different overloaded muscles and examined several indices of muscle growth and MHC composition. We found that the additional growth in plantaris and soleus muscle induced by surgical removal of synergists was not affected by low protein feeding or protein excess for 4 wk.
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FOOTNOTES |
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2 Supported by the Kansas Agricultural Experiment Station, Contribution no. 99–401-J.
4 Abbreviations used: BUN, blood urea nitrogen; CON, control diet; FFA, free fatty acids; HP, high protein diet; LP, low protein diet; MHC, myosin heavy chain.
Manuscript received September 22, 1999. Initial review completed November 30, 1999. Revision accepted February 24, 2000.
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