Vol. 94, Issue 1, 185-192, January 2003
Increased wheel-running activity in the genetically skeletal
muscle fast-twitch fiber-dominant rats
Masataka
Suwa1,
Hiroshi
Nakano2,
Yasuki
Higaki3,
Tomohiro
Nakamura4,
Shigeru
Katsuta5, and
Shuzo
Kumagai1
1 Institute of Health Science, Kyushu University,
Kasuga, Fukuoka 816-8580; 2 Department of Human
Development, Nakamura Gakuen University, Jonan-ku, Fukuoka 814-0198;
3 Department of Preventive Medicine, Saga Medical
School, Saga 849-8501; 4 Department of General
Education, Osaka Institute of Technology, Asahi-ku, Osaka 535-8585; and
5 Graduate School of Integrated Science and Art,
University of East Asia, Shimonoseki, Yamaguchi 751-8503, Japan
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ABSTRACT |
The purpose of the present
study was to investigate whether genetic differences in muscle
histochemical characteristics were related to the voluntary
wheel-running activity level by using genetically fast-twitch
fiber-dominant rats (FFDR) and control rats (CR). The rats were divided
into four groups; sedentary CR (Sed-CR), wheel-running CR (WR-CR),
sedentary FFDR (Sed-FFDR), and wheel-running FFDR (WR-FFDR). Wheel
access was started at age 9 wk and lasted for 7 days. The FFDR showed a
lower percentage of type I fibers of the deep portion of gastrocnemius
and soleus muscles and a higher percentage of both type IIX fibers of
the gastrocnemius muscle and type IIA fibers of the soleus muscle compared with CR. A higher capillary density and smaller fiber cross-sectional area were also observed in FFDR. The daily running distance in WR-FFDR was higher than in WR-CR for each 7 days. The total
running distance for 7 days in WR-FFDR was 3.2-fold higher than in
WR-CR. On day 7 of the 7-day test, the total number of
active 1-min intervals for 24 h, the average rpm when they were
active, and the maximum rpm for any single 1-min period in the WR-FFDR
were significantly higher than in the WR-CR (1.5-, 2.9-, and 2.0-fold,
respectively). These results suggest that mechanical or physiological
muscle characteristics may thus affect the wheel-running activity level.
activity pattern; capillary density; selection breeding; muscle
fiber-type composition; wheel cage
| |
INTRODUCTION |
HABITUAL PHYSICAL
ACTIVITY is one of the most important factors for health-related
physical fitness and the prevention of cardiovascular diseases
(23). Habitual activity levels appear to be genetically
heritable in humans (29), rats (33), and mice
(27, 46). Wheel running has been widely used for analyzing the voluntary physical activity levels in various animals for over a
century (39). Individual variations in wheel-running activity in rats are substantial (32). Wheel running is a
relatively high-intensity activity (32) and causes several
physiological modifications, including an increase in the maximal
O2 uptake (21, 47), changes in the muscle
enzyme activity (18, 32), an increase in the glucose
transporter 4 content (14), vascular adaptations
(36), and alterations in the muscle fiber and myosin heavy
chain composition (2, 5, 19, 52).
Skeletal muscle fibers are roughly categorized as slow-twitch type I
and fast-twitch type II fibers. Type II fibers are further subclassified into type IIA and IIX fibers in human muscle and into
type IIA, IIX, and IIB fibers in rodent muscle (34). The muscle fiber composition varies considerably in the human vastus lateralis and gastrocnemius (4, 11) and the rat
gastrocnemius (24, 44). The muscle fiber composition is
affected by genetic factors in humans (40), rats
(24, 44), and mice (25) as well as by
environmental factors (40). The muscle fiber composition is related to various types of physical performance, including isokinetic strength (49, 50), fatigability
(50), maximal O2 uptake (4), and
running speed (8). Recently, transgenic Drosophila expressing only an embryonic myosin heavy chain
(51) and myosin heavy chain IIX or IIB null mice
(17) showed a lesser physical activity level than wild
type. These reports raise the possibility that the muscle fiber
composition also affects the habitual physical activity level.
Using selective breeding, we developed fast-twitch fiber-dominant rats
(FFDR), which genetically possess a higher percentage of type II fibers
in several skeletal muscles than the control rats (CR) obtained by
random breeding (43-45). We considered that this
animal model might help us to elucidate the relationships between
inherited muscle characteristics and habitual physical activity levels.
In the present study, we subjected CR and FFDR to spontaneous wheel
running to examine whether or not genetic differences in muscle
fiber-type composition were related to voluntary wheel-running activity.
| |
METHODS |
Animals.
To obtain FFDR and CR, we performed both selective and random mating of
rats, respectively. The breeding methods have been described by Suwa et
al. (44). In brief, the initial generation in the
selective breeding was randomly chosen from a base population that was
produced by the random mating of three strains, Wistar-Imamichi, Fischer 344, and Donryu. The rats were examined by histochemical analysis at age 9 wk. On the basis of the histochemical analysis, 5 males and 10 females with the highest percentage of type II fibers in
the deep portion of gastrocnemius muscle were selected and mated. These
procedures were repeated until the eighth generation. This selected
cohort was FFDR. On the other hand, 5 males and 10 females randomly
chosen from the base population were also repeatedly bred until the
eighth generation. This random mating cohort was CR. The inbreeding
coefficient for each generation is shown in Fig.
1. The distribution of type II fibers of
gastrocnemius muscle at the base population was 45.5%, and it
increased to 61.8% by selection breeding until the seventh generation
for a high percentage of type II fibers in the FFDR (44).
The percentage of type II fibers in the soleus, vastus intermedius,
adductor longus, and biceps brachii muscles as well as the deep portion of the gastrocnemius in FFDR was higher than in CR. On the other hand,
no significant differences were observed in the plantaris, extensor
digitorum longus, rectus abdominis, diaphragm, or palmaris longus
muscles (45). These rats were weaned at age 3 wk and housed two or three per cage before the experiment. Wheel running was
started at age 9 wk and lasted for 7 days. Male rats (CR: n = 17, FFDR: n = 17) at 9 wk age with
a body weight of 250-300 g were used for this experiment.
The CR and FFDR were divided into sedentary or wheel-running exercise
groups consisting of sedentary CR (Sed-CR; n = 6),
wheel-running CR (WR-CR; n = 11), sedentary FFDR
(Sed-FFDR; n = 6), and wheel-running FFDR (WR-FFDR; n = 11). Food and water were provided ad libitum. All
animals were housed in a temperature- (22 ± 2°C) and
humidity-controlled (60 ± 5%) room with a 12-h light (0700 to
1900) and 12-h dark (1900 to 0700) cycle. All experimental
procedures were approved by the University Committee for the Use of
Animals in Research and were in strict accordance with the American
Physiological Society's Guiding Principles in the Care and Use of
Animals.
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Fig. 1.
Inbreeding coefficients of the control line [control rat
(CR)] and selected line [fast-twitch fiber-dominant rat (FFDR)] for
8 generations of breeding. Values are means ± SE.
* P < 0.05 vs. control line.
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Voluntary wheel running.
Voluntary wheel running was measured on activity wheels
(1.07-m-circumference, 10-cm-wide running surface of 10-mm mesh wire; Shinano Instruments, Tokyo, Japan) for 7 days. The measurements were
started at 0900. Standard housing cages (40 × 13 × 17 cm deep) were attached to one side of the wheels. Attached to each wheel
was a photocell counter, which was interfaced to an MS DOS-compatible personal computer. Customized software from Neuroscience (Tokyo, Japan)
measured the number of revolutions for each wheel. The number of
revolutions per day was measured for 7 days. In addition, on day
7, the revolutions per hour, the number of 1-min intervals during
which any activity occurred (no. 1-min intervals/24 h), the average
number of rpm, and the maximum rpm occurring during any 1-min interval
were measured.
The sedentary rats were housed two per cage (42 × 25 × 20 cm deep) for 7 days with a metal top and wood shavings as bedding.
Muscle analysis.
After finishing the experimental period, the rats were immediately
weighed and anesthetized with pentobarbital sodium (60 mg/kg body wt
ip). The gastrocnemius and soleus muscles of one leg were rapidly
dissected. Muscle transverse sections (7 µm) were cut from each
muscle by using a cryostat maintained at 
20°C, and the sections
were then mounted on a cover glass. Myosin ATPase was demonstrated by
using previously described procedures. In brief, consecutive serial
sections were processed using three different pretreatments,
preincubation at pH 4.3 (12), 4.6 (12), and
10.4 (15). The muscle fibers were identified as type I, IIA, IIX, IIB, and IIC fibers on the basis of the myosin ATPase staining intensity (13). A composite photomontage of each
ATPase preparation was made by using micrographs, and then each fiber was identified and counted by using a hand counter. Next, the muscle
fiber composition was determined by evaluating >500 fibers in each
section in the deep and superficial portions of the gastrocnemius muscle and all countable fibers in the soleus muscle. Other photographs of artifact-free 1.085-mm2 areas were used for determining
the fiber cross-sectional area (CSA). The measurement system was
composed of an image scanner (model ES-2000, Epson, Nagano, Japan)
connected to a Macintosh computer. The software used for analyzing the
images was NIH Image 1.62 (National Institutes of Health, Bethesda,
MD). More than 150 fibers were measured in each section.
To visualize the capillaries, another cross section (7 µm) was
also cut. The section was fixed with 100 mM PBS buffer containing 4%
formaldehyde for 4 min at room temperature, and then myosin ATPase
(preincubation at pH 10.3) (28) was demonstrated. The stained sections were photographed, and then the artifact-free 0.271-mm2 areas were analyzed and the capillary density
(capillaries/mm2) and capillary-to-fiber ratio
(capillaries/fibers) were determined in each section.
Statistical analysis.
To compare the findings including the body weight, inbreeding
coefficient, muscle and heart weight, fiber composition, fiber CSA,
capillary density, and capillary-to-fiber ratio, we used the two-way
ANOVA (rat strain × exercise state). A Tukey-Kramer's post hoc
test was performed if the ANOVA indicated a significant difference. To
compare the total running distance each day during the 7-day test and
each hour on day 7, we used the two-way repeated-measures ANOVA (rat strain × time). A Tukey-Kramer's post hoc test was performed if any significant interactions were detected by ANOVA. To
compare the total running distance for 7 days and 1-min intervals/24 h,
and the mean and maximum rpm on day 7, the unpaired
Student's t-test was used. A value P < 0.05 was considered to be significant.
| |
RESULTS |
Body composition.
Table 1 indicates the body composition
data. No significant differences in the body weight among the
four groups were observed. The absolute and relative values of the
gastrocnemius muscle weight in Sed- and WR-FFDR were significantly
lower than in the Sed- and WR-CR, respectively (P < 0.05). In the soleus weight, the relative value of WR-FFDR was
significantly higher than that of Sed-FFDR and WR-CR (P < 0.05), whereas the absolute weight was not significantly different
among the four groups. No significant differences were observed in the
absolute or relative heart weights.
Muscle fiber composition.
In the deep portion of the gastrocnemius muscle, as shown in Fig.
2 (a and b) and
Table 2, the percentage of type I fibers in Sed- and WR-FFDR was significantly lower and the percentage of type
IIX fibers was significantly higher than in Sed- and WR-CR, respectively (P < 0.05). No significant differences
among the four groups were observed in the percentage of type IIA or
IIC fibers. In the superficial portion of the gastrocnemius muscle, no
significant differences in the fiber-type composition were observed
(Table 2). In the soleus muscle, as shown in Fig. 2 (c and
d) and Table 2, the percentage of type I fibers in Sed- and
WR-FFDR was significantly lower and the percentage of type IIA fibers
was significantly higher than in the Sed- and WR-CR, respectively
(P < 0.05). No significant differences among the four
groups were observed in the percentage of type IIC fibers.
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Fig. 2.
Representative transverse sections of the deep portion of the
gastrocnemius muscle in the wheel-running CR (WR-CR; a) and
wheel-running FFDR (WR-FFDR; B) and in the soleus muscle in
the WR-CR (c) and WR-FFDR (d). a and
b: Myosin ATPase preincubation at pH 4.6. Light,
intermediate, and dark fibers are type IIA, IIX, and I, respectively.
c and d: Myosin ATPase preincubation at pH 10.4. Light and dark fibers are type I and II, respectively. Bar, 200 µm.
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Fiber CSA.
The CSAs of type I and IIX fibers of the deep portion of the
gastrocnemius muscle in Sed-FFDR were significantly lower than in
Sed-CR (P < 0.05; Table 2). The CSAs of the type IIX
and IIB fibers of the superficial portion of the gastrocnemius muscle in Sed- and WR-FFDR were significantly lower than in Sed- and WR-CR,
respectively (P < 0.05; Table 2). No significant
differences in the fiber CSA were observed in the soleus muscle (Table
2).
Capillary density and capillary-to-fiber ratio.
The capillary density in the Sed- and WR-FFDR of the deep portion of
the gastrocnemius muscle was significantly higher than in Sed- and
WR-CR, respectively (Table 2; P < 0.05), whereas the
superficial portion of the gastrocnemius and soleus muscles in WR-FFDR
were significantly higher than in WR-CR (Table 2; P < 0.05). Figure 3 indicates the
histochemical staining technique for visualizing capillaries in WR-CR
(a) and WR-FFDR (b). No significant differences
were observed in the capillary-to-fiber ratio (Table 2).
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Fig. 3.
Representative transverse sections of the superficial portion of
the gastrocnemius muscle in the WR-CR (a) and WR-FFDR
(b) stained by ATPase preincubation at pH 10.3 after
fixation with 4% formaldehyde. This staining can visualize both
capillaries and fiber type. Light and weakly stained fibers are type
IIB and IIX, respectively. Bar, 100 µm.
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Wheel-running activity levels.
Figure 4A indicates the
running distance per day for 7 days. The running distance per day for
each 7 days in WR-FFDR was significantly higher than in WR-CR
(P < 0.05). WR-FFDR showed a significant increase in
the daily running distance, but WR-CR did not, on the basis of the
finding of one-way repeated-measures ANOVA (P < 0.05).
As shown in Fig. 4B, the total running distance for 7 days
in WR-FFDR was 3.2-fold higher than in WR-CR (P < 0.05).
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Fig. 4.
Average daily (A) and 7-day total (B) running
distances in the WR-CR and WR-FFDR. Values are means ± SE.
* P < 0.05 vs. WR-CR.
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Figure 5 indicates the running distance
per hour on day 7 of the 7-day test. In the dark period, the
running distance per hour of the WR-FFDR was significantly higher than
in WR-CR except for 2100-2200, 0400-0500, and 0600-0700
(P < 0.05). On the other hand, in the light period,
the activity levels were very low and no significant differences were
observed between the groups.
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Fig. 5.
Activity pattern during 24-h periods on day 7 of a 7-day
test. Values are means ± SE. * P < 0.05 vs.
WR-CR.
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Table 3 indicates the voluntary
wheel-running behavior on day 7 of the 7-day test. The total
running distance in WR-FFDR was significantly higher than in WR-CR
(P < 0.05). The total number of active 1-min intervals
for 24 h, which is an index of the total running time, was
1.5-fold higher in WR-FFDR than in WR-CR (P < 0.05).
The average rpm when they were active and maximum rpm in any single
1-min period, which are the indexes of running speed, were
significantly higher in WR-FFDR than in WR-CR (2.9- and 2.0-fold, respectively, P < 0.05).
| |
DISCUSSION |
Wheel running requires high endurance and speed
(32). Rats given access to running wheels repeatedly run
at a speed close to or exceeding that at which their aerobic capacity
is reached (38). Intuition suggests that a more
advantageous physiological capacity regarding running endurance and/or
speed may result in an increased wheel-running activity level. Indeed,
mice obtained by selection breeding for high level wheel-running
activity showed a higher maximal O2 uptake and
mitochondrial pyruvate dehydrogenase activity than control mice
(18, 47). We consider that the muscle fiber composition
also affects the wheel-running activity level because it might be one
of the determinants of physical fitness (4, 8, 49, 50). In
this study, we demonstrated that FFDR, which were shown in this study
to possess a higher percentage of type II fibers and capillary density
and a smaller fiber CSA than CR (Table 2) as well as a higher oxidative
enzyme activity in our previous study (42), spontaneously
ran longer distances than CR. Furthermore, FFDR ran longer and at a
higher wheel velocity than CR.
Recently, Harrison et al. (17) indicated that myosin
heavy chain IIX or IIB null mice showed lower level of wheel-running activity than wild-type mice. This report supports our notion that the
inherited difference in the muscle fiber composition affects the
voluntary wheel-running activity level. However, myosin heavy chain
null mice are characterized by their histopathology in the hindlimb
muscles (1, 3, 35). Moreover, the function of the
diaphragm muscle in myosin heavy chain null mice decreased (1). Presumably, the reduced wheel-running activity level
of myosin heavy chain null mice may be due to their muscle pathology and/or a reduced ventilatory capacity as well as an altered muscle fiber composition. Therefore, further analysis is needed to investigate how genetic differences in the muscle fiber composition affect the
physical activity level with the use of an animal model not obtained by
transgene techniques. In FFDR, produced by selection breeding, the
percentage of type IIX fibers of the deep portion of the gastrocnemius
muscle and the percentage of type IIA fibers of soleus muscle were
genetically higher than in CR with a concomitant decrease in the
percentage of type I fibers. In rat muscle, the contraction velocity
and power output of type IIA and IIX fibers were higher than in type I
fiber (6, 9). In addition, the type IIA and IIX rat muscle
fibers both showed a higher glycolytic and oxidative potential than
type I fiber (30). Taken together, it is speculated that
the higher percentage of type IIA and/or IIX fibers with a concomitant
decrease in the percentage of type I fibers are beneficial for wheel
running in rats. It is thus possible that the higher voluntary wheel
running in FFDR is accompanied by a higher percentage of type IIA
and/or IIX fibers. In contrast to our results, the muscle fiber
composition in the medial portion of the gastrocnemius muscle of mice
with genetically higher wheel-running activity was not different from
the control mice (53). The reason for this disagreement
between the results of the previous study (53) and the
present study is unclear. One possibility is as follows: some of the
genes enhancing the voluntary activity also affect the muscle fiber
composition, whereas the other genes do not, and the FFDR inherited at
least some of the former genes, whereas the mice with a genetically
higher activity level (53) inherited only the latter genes.
Theoretically, selective breeding for one phenotype should cause
changes in the allele frequencies of all genes related to the phenotype
under selection and allele frequencies of the genes not associated with
the selected phenotype should remain unchanged except for genetic
drift, but genetic drift might not be important. Selection for a single
trait often results in correlated changes in other traits
(10). Our laboratory previously indicated that FFDR had a
higher percentage of type II fibers in the soleus, adductor longus,
vastus intermedius, and biceps brachii muscles than did CR (43,
45). In addition, in this study, the muscles of the FFDR
showed a higher capillary density, smaller fiber CSA, and greater
voluntary wheel-running activity level than did CR. Such results
suggest that some of the genes that influence the fiber composition of
the deep portion of the gastrocnemius muscle also affect such traits.
The FFDR showed a higher capillary density and smaller fiber CSA,
and these phenomena might be caused by pleiotropic gene action. The
higher capillary density may enhance the muscle vascular transport
capacity, which is described by the maximal ability to deliver
substrates and O2 to and remove metabolic waste products from tissues during exercise (22, 37). Smaller fiber CSAs may also be advantageous for high-intensity endurance exercise because
it is considered to facilitate O2 diffusion in cells. It is
therefore possible that higher capillary density and/or smaller fiber
CSA also affect the wheel-running behavior of FFDR.
In our previous observations, FFDR showed a higher activity of
mitochondrial oxidative enzymes than did CR (42). It is
noteworthy that mice with a genetically higher wheel-running level have
also been shown to have a significantly higher mitochondrial pyruvate dehydrogenase activity than control mice (18).
Furthermore, the activity of other mitochondrial oxidative enzymes in
these mice also tends to be higher than in control mice
(18). The muscle oxidative enzyme activities were also
significantly affected by genetic factors (7, 16, 41). On
the basis of these data, it is speculated that high levels of
wheel-running activity may require a high level of muscle aerobic
capacity, and thus genetically correlated responses have been observed
between such phenotypes.
Our present study indicates that the genetic variations in
skeletal muscle characteristics may affect the variations in
spontaneous activity in rats. The muscle characteristics, which are at
least partially genetically determined (24, 25, 40, 44),
are also associated with various physical performances in humans
(4, 8, 49, 50) and mice (1). There are many
reports concerning the genetic effects on physical performance in
humans (7, 16, 31, 41, 48) and animals (20,
26). In addition, there are significant genetic effects on
habitual physical activity level in humans (29) and
animals (27, 33, 46). On the basis of these observations,
it is possible that the individual variations in the habitual physical
activity level as well as forced exercise performances in humans are in
part determined by genetic variations in the skeletal muscle
characteristics. However, further studies are called for to clarify
such causality.
In summary, we demonstrated that FFDR showed a higher voluntary
physical activity than CR. In addition, a higher percentage of type IIA
or IIX fibers and capillary density and smaller fiber CSA were observed
in FFDR than in CR. It is speculated that such muscle characteristics,
including fiber contractile or metabolic profiles of FFDR, may fit the
mechanical or physiological demands of wheel running.
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ACKNOWLEDGEMENTS |
This study was supported by a research grant from the Japanese
Ministry of Education, Science and Culture (no. 11558002) to S. Kumagai.
| |
FOOTNOTES |
Address for reprint requests and other correspondence: S. Kumagai, Institute of Health Science, Kyushu Univ., Kasuga, Fukuoka 816-8580, Japan (E-mail:
shuzo{at}ihs.kyushu-u.ac.jp).
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. Section 1734 solely to indicate this fact.
September 6, 2002;10.1152/japplphysiol.00295.2002
Received 5 April 2002; accepted in final form 2 September 2002.
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REFERENCES |
1.
Acakpo-Satchivi, LJR,
Edelmann W,
Sartorius C,
Lu BD,
Wahr PA,
Watkins SC,
Metzger JM,
Leinwand LA,
and
Kucherlapati R.
Growth and muscle defects in mice lacking adult myosin heavy chain genes.
J Cell Biol
139:
1219-1228,
1997[Abstract/Free Full Text].
2.
Allen, DL,
Harrison BC,
Maass A,
Bell ML,
Byrnes WC,
and
Leinwand LA.
Cardiac and skeletal muscle adaptations to voluntary wheel running in the mouse.
J Appl Physiol
90:
1900-1908,
2001[Abstract/Free Full Text].
3.
Allen, DL,
Harrison BC,
Sartorius C,
Byrnes WC,
and
Leinwand LA.
Mutation of the type IIB myosin heavy chain gene results in muscle fiber loss and compensatory hypertrophy.
Am J Physiol Cell Physiol
280:
C637-C645,
2001[Abstract/Free Full Text].
4.
Bergh, U,
Thorstensson A,
Sjödin B,
Hulten B,
Piehl K,
and
Karlsson J.
Maximal oxygen uptake and muscle fiber types in trained and untrained humans.
Med Sci Sports
10:
151-154,
1978[ISI][Medline].
5.
Bigard, AX,
Sanchez H,
Birot O,
and
Serrurier B.
Myosin heavy chain composition of skeletal muscles in young rats growing under hypobaric hypoxia conditions.
J Appl Physiol
88:
479-486,
2000[Abstract/Free Full Text].
6.
Bottinelli, R,
Betto R,
Schiaffino S,
and
Reggiani C.
Unloaded shortening velocity and myosin heavy chain and alkali light chain isoform composition in rat skeletal muscle fibres.
J Physiol
478:
341-349,
1994[Abstract/Free Full Text].
7.
Bouchard, C,
Simoneau JA,
Lortie G,
Boulay MR,
Marcotte M,
and
Thibault MC.
Genetic effects in human skeletal muscle fiber type distribution and enzyme activities.
Can J Physiol Pharmacol
64:
1245-1251,
1986[ISI][Medline].
8.
Farrell, PA,
Wilmore JH,
Coyle EF,
Billing JE,
and
Costill DL.
Plasma lactate accumulation and distance running performances.
Med Sci Sports
11:
338-344,
1978.
9.
Galler, S,
Schmitt TL,
and
Pette D.
Stretch activation, unloaded shortening velocity, and myosin heavy chain isoforms of rat skeletal muscle fibres.
J Physiol
478:
513-521,
1994[Abstract/Free Full Text].
10.
Garland, T, Jr,
and
Carter PA.
Evolutionary physiology.
Annu Rev Physiol
56:
579-621,
1994[ISI][Medline].
11.
Gollnick, PD,
Armstrong RB,
Saubert CW, IV,
Piehl K,
and
Saltin B.
Enzyme activity and fiber composition in skeletal muscle of untrained and trained men.
J Appl Physiol
33:
312-319,
1972[Free Full Text].
12.
Gollnick, PD,
Parsons D,
and
Orkley CR.
Differentiation of fiber types in skeletal muscle from the sequential in activation of myofibrillar actomyosin ATPase during acid preincubation.
Histochemistry
77:
543-555,
1983[ISI][Medline].
13.
Gorza, L.
Identification of a novel type 2 fiber population in mammalian skeletal muscle by combined use of histochemical myosin ATPase and anti-myosin monoclonal antibodies.
J Histochem Cytochem
38:
257-265,
1990[Abstract].
14.
Gulve, EA,
Rodnick KJ,
Henriksen EJ,
and
Holloszy JO.
Effects of wheel running on glucose transporter (GLUT4) concentration in skeletal muscle of young adult and old rats.
Mech Ageing Dev
67:
187-200,
1993[ISI][Medline].
15.
Guth, L,
and
Samaha FJ.
Procedure for the histochemical demonstration of actomyosin ATPase.
Exp Neurol
28:
365-367,
1970[ISI][Medline].
16.
Hamel, P,
Simoneau JA,
Lortie G,
Boulay MR,
and
Bouchard C.
Heredity and muscle adaptation to endurance training.
Med Sci Sports Exerc
18:
690-696,
1986.
17.
Harrison, BC,
Bell ML,
Allen DL,
Byrnes WC,
and
Leinwand LA.
Skeletal muscle adaptations in response to voluntary wheel running in myosin heavy chain null mice.
J Appl Physiol
92:
313-322,
2002[Abstract/Free Full Text].
18.
Houle-Leroy, P,
Garland T, Jr,
Swallow JG,
and
Guderley H.
Effects of voluntary activity and genetic selection on muscle metabolic capacities in house mice Mus domesticus.
J Appl Physiol
89:
1608-1616,
2000[Abstract/Free Full Text].
19.
Ishihara, A,
Inoue N,
and
Katsuta S.
The relationship of voluntary running to fibre type composition, fibre area and capillary supply in rat soleus and plantaris muscles.
Eur J Appl Physiol
62:
211-215,
1990.
20.
Koch, LG,
Meredith TA,
Fraker TD,
Metting PJ,
and
Britton SL.
Heritability of treadmill running endurance in rats.
Am J Physiol Regul Integr Comp Physiol
275:
R1455-R1460,
1998[Abstract/Free Full Text].
21.
Lambert, MI,
and
Noakes TD.
Spontaneous running increases 
O2 max and running performance in rats.
J Appl Physiol
68:
400-403,
1990[Abstract/Free Full Text].
22.
Laughlin, MH,
and
Ripperger J.
Vascular transport capacity of hindlimb muscles of exercise-trained rats.
J Appl Physiol
62:
438-443,
1987[Abstract/Free Full Text].
23.
Leon, AS.
Physical Activity and Cardiovascular Health. Chicago, IL: Human Kinetics, 1997.
24.
Nakamura, T,
Masui S,
Wada M,
Katoh H,
Mikami H,
and
Katsuta S.
Heredity of muscle fibre composition estimated from a selection experiment in rats.
Eur J Appl Physiol
66:
85-89,
1993.
25.
Nimmo, MA,
Wilson RH,
and
Snow DH.
The inheritance of skeletal muscle fibre composition in mice.
Comp Biochem Physiol A
81:
109-115,
1985.
26.
Oki, H,
Sasaki Y,
and
Willham RL.
Genetic parameter estimates for racing time by restricted maximum likelihood in the thoroughbred horse of Japan.
J Anim Breed Genet
122:
146-150,
1995.
27.
Oliverio, A,
Castellano C,
and
Messeri P.
Genetic analysis of avoidance, maze, and wheel-running behaviors in the mouse.
J Comp Physiol Psychol
79:
459-473,
1972[ISI][Medline].
28.
Padykula, HA,
and
Herman E.
The specificity of the histochemical method for adenosine triphosphatase.
J Histochem Cytochem
3:
170-195,
1955[Abstract].
29.
Perusse, L,
Tremblay A,
LeBlanc C,
and
Bouchard C.
Genetic and environmental influences on level habitual physical activity and exercise participation.
Am J Epidemiol
129:
1012-1022,
1989[Abstract/Free Full Text].
30.
Rivero, JLL,
Talmadge RJ,
and
Edgerton VR.
Interrelationships of myofibrillar ATPase activity and metabolic properties of myosin heavy chain-based fibre types in rat skeletal muscle.
Histochem Cell Biol
111:
277-287,
1999[ISI][Medline].
31.
Rodas, G,
Calvo M,
Estruch A,
Garrido E,
Ercilla G,
Arcas A,
Segura R,
and
Ventura JL.
Heritability of running economy: a study made on twin brothers.
Eur J Appl Physiol
77:
511-516,
1998.
32.
Rodnick, KJ,
Reaven GM,
Haskell WL,
Sims CR,
and
Mondon CE.
Variations in running activity and enzymatic adaptations in voluntary running rats.
J Appl Physiol
66:
1250-1257,
1989[Abstract/Free Full Text].
33.
Rundquist, EA.
Inheritance of spontaneous activity in rats.
J Comp Physiol Psychol
16:
415-438,
1933.
34.
Sant'Ana Pereira, JAA,
Ennion S,
Sargeant AJ,
Moorman AFM,
and
Goldspink G.
Comparison of the molecular, antigenic and ATPase determinants of fast myosin heavy chains in rat and human: a single-fibre study.
Pflügers Arch
435:
151-163,
1997[ISI][Medline].
35.
Sartorius, CA,
Lu BD,
Acakpo-Satchivi L,
Jacobsen RP,
Allen DL,
Harrison BC,
Byrnes WC,
and
Leinwand LA.
Myosin heavy chains IIa and IId are functionally distinct in the mouse.
J Cell Biol
141:
943-953,
1998[Abstract/Free Full Text].
36.
Sexton, WL.
Vascular adaptations in rat hindlimb skeletal muscle after voluntary running-wheel exercise.
J Appl Physiol
79:
287-295,
1995[Abstract/Free Full Text].
37.
Sexton, WL,
and
Laughlin MH.
Influence of exercise intensity on distribution of vascular adaptation in skeletal muscle.
Am J Physiol Heart Circ Physiol
266:
H483-H490,
1994[Abstract/Free Full Text].
38.
Shepherd, RE,
and
Gollnick PD.
Oxygen uptake of rats at different work intensities.
Pflügers Arch
362:
219-222,
1976[ISI][Medline].
39.
Sherwin, CM.
Voluntary wheel running: a review and a novel interpretation.
Anim Behav
56:
11-27,
1998[ISI][Medline].
40.
Simoneau, JA,
and
Bouchard C.
Genetic determinism of fiber type proportion in human skeletal muscle.
FASEB J
9:
1091-1095,
1995[Abstract].
41.
Simoneau, JA,
Lortie G,
Boulay MR,
Marcotte M,
Thibault MC,
and
Bouchard C.
Inheritance of human skeletal muscle and anaerobic capacity adaptation to high-intensity intermittent training.
Int J Sports Med
7:
167-171,
1986[ISI][Medline].
42.
Suwa, M,
Kumagai S,
Higaki Y,
Nakamura T,
and
Katsuta S.
Dietary obesity-resistance and muscle oxidative enzyme activities of the fast-twitch fibre dominant rat.
Int J Obes
26:
830-837,
2002[ISI][Medline].
43.
Suwa, M,
Miyazaki T,
Nakamura T,
Sasaki S,
Ohmori H,
and
Katsuta S.
Hereditary dominance of fast-twitch fibers in skeletal muscles and relation of thyroid hormone under physiological conditions in rats.
Acta Anat (Basel)
162:
40-45,
1998[ISI][Medline].
44.
Suwa, M,
Nakamura T,
and
Katsuta S.
Heredity of muscle fiber composition and correlated response of the synergistic muscle in rats.
Am J Physiol Regul Integr Comp Physiol
271:
R432-R436,
1996[Abstract/Free Full Text].
45.
Suwa, M,
Nakamura T,
and
Katsuta S.
Muscle fibre number is a possible determinant of muscle fibre composition in rats.
Acta Physiol Scand
167:
267-272,
1999[ISI][Medline].
46.
Swallow, JG,
Carter PA,
and
Garland T, Jr.
Artificial selection for increased wheel-running behavior in house mice.
Behav Genet
28:
227-237,
1998[ISI][Medline].
47.
Swallow, JG,
Garland T, Jr,
Carter PA,
Zan WZ,
and
Sieck GC.
Effects of voluntary activity and genetic selection on aerobic capacity in house mice (Mus domesticus).
J Appl Physiol
84:
69-76,
1998[Abstract/Free Full Text].
48.
Thomis, MAI,
Beunen GP,
Van Leemputte M,
Maes HH,
Blimkie CJ,
Claessens AL,
Marchal G,
Willems E,
and
Vlietinck RF.
Inheritance of static and dynamic arm strength and some of its determinants.
Acta Physiol Scand
163:
59-71,
1998[ISI][Medline].
49.
Thorstensson, A,
Grimby G,
and
Karlsson J.
Force-velocity relations and fiber composition in human knee extensor muscles.
J Appl Physiol
40:
12-16,
1976[Abstract/Free Full Text].
50.
Thorstensson, A,
and
Karlsson J.
Fatigability and fibre composition of human skeletal muscle.
Acta Physiol Scand
98:
328-322,
1976.
51.
Wells, L,
Edwards KA,
and
Bernstein SI.
Myosin heavy chain isoforms regulate muscle function but not myofibril assembly.
EMBO J
15:
4454-4459,
1996[ISI][Medline].
52.
Wernig, A,
Irintchev A,
and
Weisshaupt P.
Muscle injury, cross-sectional area and fibre type distribution in mouse soleus after intermittent wheel running.
J Physiol
428:
639-652,
1990[Abstract/Free Full Text].
53.
Zhan, WZ,
Swallow JG,
Garland T, Jr,
Proctor DN,
Carter PA,
and
Sieck GC.
Effects of genetic selection and voluntary activity on the medial gastrocnemius muscle in house mice.
J Appl Physiol
87:
2327-2333,
1999.
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