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Department of Veterinary Biomedical Sciences, College of Veterinary Medicine, University of Missouri, Columbia, Missouri 65211
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
McAllister, Richard M., Brian L. Reiter, John F. Amann, and
M. Harold Laughlin. Skeletal muscle biochemical adaptations to
exercise training in miniature swine. J. Appl.
Physiol. 82(6): 1862-1868, 1997.
The primary
purpose of this study was to test the hypothesis that endurance
exercise training induces increased oxidative capacity in porcine
skeletal muscle. To test this hypothesis, female miniature swine were
either trained by treadmill running 5 days/wk over 16-20 wk (Trn;
n = 35) or pen confined (Sed;
n = 33). Myocardial
hypertrophy, lower heart rates during submaximal stages of a maximal
treadmill running test, and increased running time to exhaustion during
that test were indicative of training efficacy. A variety of skeletal
muscles were sampled and subsequently assayed for the enzymes citrate
synthase (CS), 3-hydroxyacyl-CoA dehydrogenase, and lactate
dehydrogenase and for antioxidant enzymes. Fiber type composition of a
representative muscle was also determined histochemically. The largest
increase in CS activity (62%) was found in the gluteus maximus muscle
(Sed, 14.7 ± 1.1 µmol · min
1 · g1;
Trn, 23.9 ± 1.0; P < 0.0005).
Muscles exhibiting increased CS activity, however, were located
primarily in the forelimb; ankle and knee extensor and respiratory
muscles were unchanged with training. Only two muscles exhibited higher
3-hydroxyacyl-CoA dehydrogenase activity in Trn compared with Sed.
Lactate dehydrogenase activity was unchanged with training, as were
activities of antioxidant enzymes. Histochemical analysis of the
triceps brachii muscle (long head) revealed lower type IIB fiber
numbers in Trn (Sed, 42 ± 6%; Trn, 10 ± 4;
P < 0.01) and greater type IID/X
fiber numbers (Sed, 11 ± 2; Trn, 22 ± 3;
P < 0.025). These findings
indicate that porcine skeletal muscle adapts to endurance exercise
training in a manner similar to muscle of humans and other animal
models, with increased oxidative capacity. Specific
muscles exhibiting these adaptations, however, differ between the
miniature swine and other species.
citrate synthase; oxidative capacity; INTRODUCTION THE MINIATURE SWINE is an animal model that is
increasingly used in biomedical research. In recent years, it has been
used in studies of the effects of endurance exercise training on the heart (34) and its circulation (8, 25, 26). The miniature swine is well
suited for such studies because its heart is of the same relative size
as that of humans and the coronary circulation is similar in the two
species (35). In addition, the cardiovascular response to acute
exercise in swine resembles that in humans (3, 35). Studies from our
laboratory (25, 26) and from those of others (8, 34) have found that
miniature swine exhibit adaptations to endurance exercise training that
are similar to those in humans, including myocardial hypertrophy,
bradycardia at an absolute submaximal exercise intensity, and increased
maximal cardiac output and oxygen consumption. Thus, from
a cardiovascular viewpoint, the miniature swine appears to be a good
model for exercise training studies.
Although cardiovascular adaptations to training have been documented in
swine, it is uncertain whether porcine skeletal muscle adapts to
endurance-type training with increased potential for oxidative
metabolism. Breisch and colleagues (8) found that the increase in
maximal oxygen consumption exhibited by swine after a period of
training was entirely accounted for by increased maximal cardiac
output. Although these investigators did not obtain a measure of
skeletal muscle oxidative capacity in their study, unchanged maximal
systemic arteriovenous oxygen difference may have been indicative of
unchanged muscle oxidative capacity. This interpretation, however,
presumes that a consequence of increased skeletal muscle oxidative
capacity is increased oxygen extraction during exercise. Alternatively,
an increase in muscle oxidative capacity may be manifested in other
ways, such as altered patterns of energy metabolism during submaximal
exercise intensities (cf. Refs. 20, 30).
It is also uncertain which skeletal muscles experience the greatest
relative increases in activity during treadmill running in swine.
Although glycogen depletion and electromyographic recording techniques
have not been employed to determine muscle recruitment, the regional
blood flow response to exercise, another indicator of recruitment, has
been determined in miniature swine (3). Blood flows to fore- and
hindlimb musculature are elevated severalfold during treadmill running;
nonetheless, elevations in blood flow have been found to vary widely
among individual muscles (3). These blood flow data suggest that
forelimb muscles provide a greater contribution to locomotion in swine
than do muscles of the hindlimb. An increase in oxidative capacity of a
muscle after a period of exercise training is also thought to reflect
recruitment of that muscle during training bouts (cf. Refs. 20, 30).
Thus the primary purpose of this study was to test the hypotheses that endurance exercise training induces increased skeletal muscle oxidative
capacity in miniature swine and that this adaptation is more apparent
in muscles of the forelimb than those of the hindlimb. We tested these
hypotheses by determining the activities of marker enzymes for primary
energy-generating pathways in a wide variety of skeletal muscles from
sedentary and trained swine. Muscles were selected to represent a wide
range of recruitment during exercise, as suggested by blood flow
responses to treadmill running (3).
Several studies, conducted in rodent models, have shown increases in
antioxidant enzyme activities with endurance exercise training (21, 22,
29). It has been suggested that increased antioxidant enzyme activities
in skeletal muscle of trained animals may be linked to increased
oxidative capacity (21, 29). Thus a secondary purpose of this study was
to determine whether activities of antioxidant enzymes in porcine
skeletal muscle change in concert with oxidative capacity.
METHODS 
-oxidation; antioxidant
enzymes; fiber type composition
10% of bulk food provided).
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70°C until enzymatic
analyses were conducted. Additionally, samples of triceps brachii (long
head) were obtained for histochemical determination of fiber type
composition. These samples were frozen by immersion in isopentane cooled to 160°C in liquid nitrogen and stored at
70°C until histochemical analysis was done.
Enzymatic assays.
Marker enzymes for primary energy-yielding pathways of metabolism were
assayed. Citrate synthase (CS) was selected as a marker enzyme for the
tricarboxylic acid cycle and was assayed according to the method of
Srere (31). 3-Hydroxyacyl-CoA dehydrogenase (HADH), a marker enzyme for
-oxidation, was assayed by the method of Bass and co-workers (4).
Lactate dehydrogenase (LDH), a marker enzyme for the glycolytic
pathway, was assayed according to the method of Bergmeyer and Bernt
(6). These assays were either colorimetric (CS) or NADH-linked (HADH,
LDH) in nature and were conducted in a spectrophotometer (Beckman) at
30°C. Maximal enzyme activities were expressed as micromoles per
minute per gram wet weight.
Antioxidant enzymes were also assayed spectrophotometrically.
Glutathione peroxidase (GP) activity was determined using the method of
Flohe and Gunzler (14). This NADPH-linked assay was conducted at 30°C. Maximal activity was expressed as micromoles per
minute per gram wet weight. Superoxide dismutase (SOD) activity was
determined at room temperature by using the colorimetric method of
Marklund and Marklund (23). SOD activity was expressed as U per gram
wet weight, where 1 U refers to the enzyme amount causing 50%
inhibition of pyrogallol autoxidation (23).
Histochemical analysis.
Fiber type composition of the long head of triceps brachii muscle was
determined as described previously (1). Briefly, transverse sections of
frozen muscle, 5 µm thick, were cut in a cryostat (American
Optical). Serial sections from each muscle were stained for
myofibrillar actomyosin ATPase (mATPase) by using preincubation pH
values of 9.8, 4.6, and 4.3. An additional section was stained for
NADH-tetrazolium reductase (NADH-TR). A minimum of five randomly
selected microscopic fields from each muscle were analyzed. Sections
stained for mATPase were used to distinguish types I, IIA, and IIB-D/X,
and sections stained for NADH-TR were used to differentiate types IIB
and IID/X (1, 19). Determination of cross-sectional area of classified
fibers was performed by using an image analysis system (Olympus Cue 2),
as described previously (18).
Statistical analysis.
All data are presented as means ± SE. A paired
t-test (32) was used to compare
running times to exhaustion between pre- and posttraining for both Sed
and Trn. Two-way analysis of variance (repeated measures on both
factors) was used to compare heart rates pre- and posttraining for both
Sed and Trn, with the Tukey test used for post hoc analysis (32). An
unpaired t-test (32) was used to
compare heart weight-to-body weight ratios and enzyme activities. Fiber
type composition between Sed and Trn was compared by using the
nonparametric Kruskal-Wallis test (32). For all analyses,
P < 0.05 was considered significant.
RESULTS
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1 · g1,
n = 6; Trn, 7.86 ± 0.29, n = 6; NS) and external obliques (Sed, 8.13 ± 0.49, n = 6; Trn, 9.01 ± 0.73, n = 6; NS) muscles. Table 5 also presents SOD activity for muscles in Sed and Trn. Similar to GP,
training did not increase SOD activity in any muscle examined.
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Value for
trained significantly less than corresponding value for sedentary,
P < 0.01.
DISCUSSION
The results of this study indicate that porcine skeletal muscle adapts to endurance exercise training with an increase in oxidative capacity. This adaptation occurs primarily in forelimb musculature, whereas hindlimb and respiratory muscles generally are unchanged in character. This adaptation in porcine forelimb muscles is similar to that previously reported to occur in skeletal muscles of humans and other animal models (e.g., rat) in response to exercise training. Furthermore, this adaptation complements cardiovascular adaptations to exercise training previously observed in swine (8, 25, 26, 34).
Enzymes of energy-yielding pathways. Skeletal muscle from swine in the sedentary state appears to differ in some respects from that of other animals. CS activity was rather homogeneous among the muscles that we examined (Table 2). For example, in various heads of the triceps brachii muscle, activity of this oxidative enzyme exhibited a narrow range of ~14-16 µmol · min1 · g1.
This lack of variability exists in a group of muscles that vary considerably in fiber type composition (3), ranging from >90% slow
oxidative (type I) fibers in the medial head to ~50% fast glycolytic
(type IIB) fibers in the lateral head. In contrast, rodent muscles
composed primarily of type I and type IIB fibers differ three- to
fourfold in CS activity (cf. Refs. 20, 30). In the various heads of the
triceps brachii muscle, HADH and LDH activities varied more widely and
in an inverse manner; i.e., when the former was high, the latter was
low and vice versa (Tables 3 and 4). Skeletal muscles of other species
with greater potential for -oxidation also have lower glycolytic
potential (cf. Refs. 20, 30). Furthermore, activities of these enzymes
in various heads of the triceps brachii muscle were consistent with
fiber type composition data reported here (Fig. 1) and those previously reported for another strain of miniature swine (3). The medial head of
triceps brachii (>90% slow oxidative, or type I, fibers) exhibited
relatively high potential for -oxidation and relatively low
potential for glycolysis, whereas the long and lateral heads, containing many fast glycolytic (type IIB) fibers (~50%), exhibited approximately threefold greater glycolytic potential and lesser potential for oxidation of fatty acids compared with the medial head.
In response to endurance exercise training, CS activity increased in
many of the muscles examined, most notably those of the forelimb. The
magnitude of this change in forelimb muscles was generally <50%,
which is quantitatively similar to that recently reported for human
muscle from previously sedentary individuals subjected to a period of
training (7, 9, 10, 36). Rodent skeletal muscles typically exhibit
greater increases (i.e., 50-100%) in CS activity (cf. Refs. 20,
30). Curiously, the activity of HADH, another oxidative-type enzyme,
was similar between Sed and Trn swine in most muscles. A lack of change
in the activity of this marker enzyme for -oxidation has also been
reported for skeletal muscle from humans after training (7, 9, 36), although another study found ~40% increases associated with
endurance-type training (10). The two muscles (i.e., deltoid, gluteus
maximus) that did exhibit higher HADH activities in Trn animals in the present study were elevated by a similar magnitude as that reported by
Coggan and colleagues (10). Similar to CS, training induces larger
increases (~100%) in enzymes of -oxidation in rodent skeletal muscle (24). As has been found with endurance exercise training in a
variety of species (cf. Refs. 20, 30), skeletal muscle LDH activity was
unchanged with training. Thus forelimb skeletal muscle of Trn miniature
swine was changed in that potential for oxidative metabolism, estimated
by CS activity, was greater. The longer running time to exhaustion in
trained swine (Table 1) may reflect this benefit of endurance exercise
training.
Unchanged CS activity in ankle and knee extensor and respiratory
muscles merits consideration. Because ankle and knee joints of
miniature swine appear to be in chronically extended positions, it may
be that treadmill exercise training does not represent a sufficient
stimulus for biochemical adaptations in extensor muscles crossing these
joints. Our findings in ankle and knee extensor muscles emphasize the
need to be cautious when findings are applied among different species.
While increased CS activity is characteristic of ankle and knee
extensors of trained rodents (cf. Refs. 20, 30), it is clear from our
data (Table 2) and those of others from dogs (27) that this is not a
universal feature of trained animals. In the case of dogs, however,
muscle oxidative capacity is relatively high in the sedentary state. This may make training-induced augmentation of this metabolic characteristic unnecessary. Previous findings have also been mixed regarding effects of endurance exercise training on respiratory muscles. While some studies have found increased oxidative capacity in
muscles such as the diaphragm and external obliques (e.g., Ref. 17),
others have not demonstrated a training-induced increase in oxidative
capacity (e.g., Ref. 15). Our results indicate that the exercise
training program employed provided an insufficient stimulus for
induction of increased oxidative capacity in porcine respiratory
muscles.
Antioxidant enzymes.
Activity of the antioxidant enzyme GP in porcine muscle resembles that
reported for rat fast-twitch, extensor-type muscles, but values for SOD
activity in porcine muscle are lower than previously reported values
for rat muscle (21, 22, 29). Our data indicate that antioxidant enzyme
activities in porcine skeletal muscle do not increase in response to
exercise training, contrary to what has been reported for rats. Several
groups have reported that activities of GP (21, 22, 29) and SOD (22,
29) are increased after endurance-type training. Lack of adaptation of
antioxidant enzymes to training in the present study may be due to an
inadequate training stimulus, although the cardiorespiratory adaptations exhibited by Trn swine (Table 1) argue against this possibility. Alternatively, unchanged antioxidant enzyme activities may
be due to the presence of female reproductive hormones, which confer
antioxidant activity and may make upregulation of these enzymes
unnecessary. This gender effect has previously been observed in
sexually mature female rats (cf. Refs. 22, 33).
Fiber type composition.
Fiber type composition of the long head of triceps brachii muscle in
Sed miniature swine was similar to that previously reported for this
head of the same muscle in another strain of miniature swine (3). We
selected this specific muscle for histochemical analysis because
preliminary data indicated that it exhibited a large increase (~50%;
Table 2) in oxidative capacity with training. Because changes in
contractile character, specifically mATPase activity, have been
reported to be associated with large changes in oxidative capacity (cf.
Ref. 28), we hypothesized that a fast-to-slower transition in muscle
contractile character would occur in this muscle. Histochemically
determined fiber type composition, an indicator of contractile
character, was different in Trn animals compared with their Sed
counterparts. Skeletal muscle from Trn animals was composed of
significantly less type IIB fibers and greater numbers of type IID/X
fibers. Indeed, we were unable to identify any type IIB fibers in
muscle from two of the Trn swine examined. Apparent transformation of
type IIB into type IIA fibers has been reported for humans (2, 5, 10)
and rats (13, 16) after endurance exercise training. Although type IIA
fiber numbers were similar for Sed and Trn swine, it is possible that decreased type IIB and increased type IID/X fiber numbers are indicative of a type IIB-to-type IID/X fiber transformation. With identification of the IID/X fiber type (cf. Ref. 11), and the recent
demonstration of a type IIB
type IID/Xtype
IIAtype I muscle fiber transformation sequence in response to
chronic low-frequency stimulation (12), it is possible that a similar
transformation sequence occurred in triceps brachii of Trn swine. To
the best of our knowledge, this is the first time that type IID/X
fibers have been identified histochemically in an animal model
subjected to a period of locomotory exercise training. Increased type
IID/X fiber number is consistent with our biochemical data indicating increased oxidative capacity in the long head of triceps brachii because the contractile character of this fiber type is associated with
greater oxidative capacity (11). Sharply reduced numbers of type IIB
fibers, along with greater numbers of more highly oxidative type IID/X
fibers (Fig. 1), would be advantageous for prolonged exercise
performance and may have contributed to the longer running time to
exhaustion exhibited by swine after the period of endurance-type
training. It must emphasized, however, that we examined only one
forelimb muscle. These fiber compositional changes would need to be
present throughout forelimb musculature to contribute to greater
endurance.
Summary.
Porcine forelimb skeletal muscle adapts to endurance exercise training
in a manner similar to that previously reported for muscle in humans
and rodents, with an increase in oxidative capacity. In
contrast, hindlimb muscle does not exhibit increased oxidative capacity
after exercise training in swine. Additionally, and unlike findings
from studies involving rodents, antioxidant capacity of porcine muscle
is unchanged with training. Apparent conversion of type IIB fibers into
type D/X fibers with training, previously observed after chronic
electrical stimulation, is also exhibited by porcine skeletal muscle.
Combined with previous findings concerning cardiovascular function, our
findings indicate that the miniature swine is an appropriate model for
studies of the effects of endurance exercise training on the heart and
skeletal muscle.
ACKNOWLEDGEMENTS
The authors acknowledge the important technical contributions of Donna Baumgartner, Chuck Fraga, Tammy Knox, Tammy Strawn, and Pam Thorne to this study. Also acknowledged are the efforts of the many veterinary medical students who participated in the training of animals used in these experiments.
FOOTNOTES
Address for reprint requests: M. H. Laughlin, Dept. of Veterinary Biomedical Sciences, E102, Vet. Med. Bldg., Univ. of Missouri, Columbia, MO 65211.
Received 28 August 1996; accepted in final form 3 February 1997.
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 M. P. Massett and B. C. Berk Strain-dependent differences in responses to exercise training in inbred and hybrid mice Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2005; 288(4): R1006 - R1013. [Abstract] [Full Text] [PDF]
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 E. J. Clowes, F. X. Aherne, and V. E. Baracos Skeletal muscle protein mobilization during the progression of lactation Am J Physiol Endocrinol Metab, March 1, 2005; 288(3): E564 - E572. [Abstract] [Full Text] [PDF]
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