Journal of Sports Science and Medicine
Journal of Sports Science and Medicine
ISSN: 1303 - 2968   
Ios-APP Journal of Sports Science and Medicine
Androit-APP Journal of Sports Science and Medicine
Views
6248
Download
100
from September 2014
 
©Journal of Sports Science and Medicine (2009) 08, 51 - 57

Research article
Effects of voluntary wheel running on satellite cells in the rat plantaris muscle
Mitsutoshi Kurosaka1, Hisashi Naito1, , Yuji Ogura1,2, Atsushi Kojima2, Katsumasa Goto2,3, Shizuo Katamoto1
Author Information
1 Department of Exercise Physiology, Graduate School of Health and Sports Science, Juntendo University, Chiba, apan
2 Department of Physiology, St. Marianna University School of Medicine, Kawasaki, Japan
3 Laboratory of Physiology, Toyohashi SOZO University, Toyohashi, Japan

Hisashi Naito
✉ Department of Exercise Physiology, Graduate School of Health and Sports Science, Juntendo University, Chiba, 270-1695, Japan
Email: naitoh@sakura.juntendo.ac.jp
Publish Date
Received: 13-11-2008
Accepted: 03-12-2008
Published (online): 01-03-2009
Share this article
 
ABSTRACT

This study investigated the effects of voluntary wheel running on satellite cells in the rat plantaris muscle. Seventeen 5-week-old male Wistar rats were assigned to a control (n = 5) or training (n = 12) group. Each rat in the training group ran voluntarily in a running-wheel cage for 8 weeks. After the training period, the animals were anesthetized, and the plantaris muscles were removed, weighed, and analyzed immunohistochemically and biochemically. Although there were no significant differences in muscle weight or fiber area between the groups, the numbers of satellite cells and myonuclei per muscle fiber, percentage of satellite cells, and citrate synthase activity were significantly higher in the training group compared with the control group (p < 0.05). The percentage of satellite cells was also positively correlated with distance run in the training group (r = 0.61, p < 0.05). Voluntary running can induce an increase in the number of satellite cells without changing the mean fiber area in the rat plantaris muscle; this increase in satellite cell content is a function of distance run.

Key words: Endurance training, muscle damage, hypertrophy, myonuclear, Pax7.


           Key Points
  • There is no study about the effect of voluntary running on satellite cells in the rat plantaris muscle.
  • Voluntary running training causes an increase of citrate synthase activity in the rat plantaris muscle but does not affect muscle weight and mean fiber area in the rat plantaris muscle.
  • Voluntary running can induce an increase in the number of satellite cells without hypertrophy of the rat plantaris muscle.

INTRODUCTION

Skeletal muscle satellite cells are located outside the sarcolemma and under the basal lamina of the muscle fiber (Mauro, 1961). They have the ability to generate new muscle fibers or to provide new myonuclei (Schultz and McCormick, 1994). After muscle damage, satellite cells are activated and proliferate for muscle repair and regeneration (Kadi et al., 2005). Therefore, they are considered important structures for the maintenance of normal muscle function.

It is thought that satellite cells are in a non-proliferative quiescent state in the resting condition and that they are activated by intense exercise. In fact, many studies have shown increases in the number of satellite cells after resistance training leading to muscle hypertrophy (Kadi et al., 2000, 2004; Roth et al., 2001; Mackey et al., 2007). Although the exact mechanism is still unknown, the activation of satellite cells by resistance training may be attributable to exercise-induced localized ultrastructural damage, segmental fiber damage, and the release of inflammatory substances or growth factors (Kadi et al., 2005). In addition, various types of prolonged exercise training also induce the activation and proliferation of satellite cells in skeletal muscle of both humans and animals, although the functional load on skeletal muscle may not be as strong as that seen with resistance training (Appell et al., 1988; Umnova and Seene, 1991; Charifi et al., 2003). For example, it was reported that 14 weeks of intermittent cycle ergometer training at 65~95% of the VO2peak for 45 min increased the number of satellite cells in the vastus lateralis muscle in men aged 70 to 80 years, while hypertrophy was observed simultaneously in type IIA fibers (Charifi et al., 2003). Furthermore, there was a 2.5-fold increase in the number of satellite cells in rat gastrocnemius muscle after 6 weeks of treadmill running at a speed of 35 m·min -1 according to an increasing regimen, but the effect on muscle hypertrophy was not clear (Umnova and Seene, 1991). It is not known whether low-intensity exercise training, which does not result in muscle hypertrophy, can also induce the activation and proliferation of satellite cells in skeletal muscle, given sufficient exercise. In this regard, Putman et al., 1999 demonstrated that chronic low-frequency stimulation of fast-twitch muscle in the rat induced an increase in satellite cells. The low-frequency electrical stimulation can be considered as a highly standardized, reproducible protocol of maximum endurance training for muscle. However, their experimental model has not been examined under physiological conditions such as exercise training. Therefore, a suitable animal model should be used to determine whether exercise training can induce satellite cells in skeletal muscle in the absence of hypertrophy.

In animal studies, voluntary freewheel running is considered one of the most effective prolonged training models for inducing aerobic adaptation in rodent muscles, because the daily exercise duration is extremely long, although inter-individual variation is observed (Lambert and Noake, 1990). For example, 6 weeks of voluntary freewheel running increased the cytochrome oxidase activity in the plantaris muscles of the high-runner (> 11 km·day-1) group without increasing muscle weight (Rodnick et al., 1989). In addition, Ishihara et al., 1998 demonstrated that 8 weeks of voluntary wheel running in the unloaded condition did not increase the weight or fiber area of the plantaris muscle, regardless of the distance run. Therefore, unloaded voluntary running training constitutes a good model in which to study the effect of low-intensity, long-duration exercise training on satellite cells in skeletal muscle without associated muscle hypertrophy.

In the present study, we tested the hypothesis that voluntary running will increase the number of satellite cells in the rat plantaris muscle, which is a well- recruited fast-twitch muscle during running (Jasmin and Gardiner, 1987), without causing hypertrophy.

METHODS

Animals and treatment

The experimental procedures were approved by the Juntendo University Animal Care and Use Committee and followed the Japanese and American Physiological Society Animal Care Guidelines. Seventeen 5-week-old male Wistar rats were used in this study. A growing rat runs very well voluntarily, and the satellite cell frequency in a 2-month-old rat has stabilized at less than 5% of skeletal muscle nuclei during postnatal muscle growth (Charge and Rudnicki, 2004).

All animals used in this study were obtained from a licensed laboratory animal vender (Japan SLC, Shizuoka, Japan). The rats were maintained in an environmentally controlled room (22.0 ± 0.5 °C, 55.0 ± 5.0% relative humidity) under a fixed 12:12-h photoperiod cycle (lights on from 0900 to 2100). The animals were fed standard rat chow and water ad libitum. After a week of acclimation to the animal facility, the rats were assigned randomly to a control (n = 5) or training (n = 12) group. Each rat in the training group was kept individually in a stainless steel cage (19.5 × 27.5 × 3.0 cm) equipped with a unloaded running wheel (1 m·revolution-1) for 8 weeks. The wheel revolutions were counted continuously throughout the experiment, and the number of revolutions indicated by the counter attached to the wheel was recorded at the same time each day.

Immunohistochemical analysis

All animals were anesthetized with pentobarbital sodium (50 mg·kg-1) 48 h after the last training session to avoid the acute effects of training, and the plantaris muscle was removed and weighed. The plantaris muscle was studied because it is a primary ankle extensor and is activated during running (Jasmin et al., 1987). The plantaris muscles were embedded in Tissue Tek OCT compound and frozen in liquid nitrogen. Transverse 8-μm-thick sections were cut using a microtome (CM3050S, Leica, Wetzlar, Germany) at -20°C and mounted on glass slides. The numbers of myonuclei and satellite cells were counted, as described previously (Kojima et al., 2007). Briefly, immunofluorescence staining was used to detect satellite cells. Muscle cross-sections were air-dried and rinsed for 25 min in phosphate-buffered saline with Tween-20 (T-PBS, pH 7.4 and 0.1% Tween-20). T-PBS was used to rinse the sections between the incubation steps. After rinsing, the sections were fixed in 4% paraformaldehyde followed by methanol, for 15 min each. Then, the sections were boiled using microwaves (BE-S160-W, Sharp, Tokyo, Japan) for 9 min in 0.01 M citrate buffer (pH 6.0) and blocked with 1% blocking regent (Roche Diagnostics, Penzberg, Germany) in T-PBS for 30 min. The sections were incubated overnight at 4°C with mouse monoclonal anti-pax7 antibody (1:500; undiluted tissue culture supernatant of hybridoma cells was obtained from the Developmental Studies Hybridoma Bank, Iowa City, IA, USA) and rabbit polyclonal anti-laminin antibody (1:500; DAKO, Ely, UK) in the antibody solution (1% blocking regent). After rinsing, the sections were incubated for 1 h at room temperature with Cy3 anti-mouse IgG antibody (1:500; Jackson, Baltimore, MD, USA) and FITC-conjugated anti-rabbit IgG (1:200; Sigma-Aldrich, St. Louis, MO, USA) in antibody solution. Finally, the sections were stained with 4′ ,6-diamidino-2-phenylindole (DAPI; 1:10,000; Sigma-Aldrich) in T-PBS for 5 min to stain the nuclei and were mounted using Vectashield (Vector Laboratories, Burlingame, CA, USA).

A fluorescence microscope with a ×20 objective (DM5000B, Leica) was used to detect the satellite cells (Figure 1). Satellite cells, laminin, and myonuclei were visualized using N3 (546 nm), L5 (480 nm), and A4 (360 nm) fluorescence cubes, respectively. Images of the sections were obtained with a digital camera connected to the microscope and were stored on a personal computer. In each section, 10 different areas, which contained 1000~1200 fibers, 25~40 satellite cells, and 2400~3000 myonuclei, were chosen randomly for measuring myonuclei and satellite cells. The numbers of myonuclei and satellite cells per muscle fiber were calculated. For each section, the percentage of satellite cells was calculated as: [number of satellite cells/(total number of myonuclei and satellite cells)] × 100. The total area observed (sum of the 10 areas) was digitized on a computer attached to the fluorescence microscope (IM 500; Leica), and then the mean cross-sectional fiber area was determined by dividing the total area by the total number of fibers (IM 500, Leica). To determine the myonuclear domain, the mean fiber area was divided by the number of myonuclei per fiber.

Analysis of citrate synthase activity

The citrate synthase activity was determined based on the oxidative capacity, which is an index of the effect of endurance training. Muscle samples were minced and then homogenized in ice-cold homogenization buffer (100 mM potassium phosphate, 0.1 mM EDTA, pH 7.4). The homogenate was centrifuged at 400 × g for 15 min, and the enzyme activity in the supernatant was measured spectrophotometrically (U-2000; Hitachi, Tokyo, Japan) at 25°C, based on the method of Srere, 1969. The assay was performed in duplicate, and the mean measurement was used to calculate the enzyme activity. The total protein concentration in the supernatant was determined using the Bradford (1976) technique.

Statistical analysis

All data are expressed as means ± SD. The statistical significance of differences between groups was analyzed using an unpaired t-test. Pearson's product correlations were used to determine the relationship between the distance run and the citrate synthase activity and between the distance run and the percentage of satellite cells. The results were considered significant at p < 0.05.

RESULTS

Body and muscle weight

The body and muscle weights of both groups are shown in Table 1. After 8 weeks, the body weight in the training group was significantly lower than that in the control group (p < 0.05). There was no significant difference in muscle weight between the control and training groups.

Citrate synthase activity

The citrate synthase activity in both groups is shown in Table 2. The citrate synthase activity in the training group was significantly higher than that in the control group (p < 0.05). Furthermore, the citrate synthase activity was positively correlated with the distance run in the training group (r = 0.62, p < 0.05; Figure 2).

Mean muscle fiber area, myonuclei per muscle fiber, and myonuclear domain

The mean muscle fiber area, myonuclei per muscle fiber, and myonuclear domain in both groups are shown in Table 2. The mean muscle fiber area did not differ significantly between the control and training groups. The number of myonuclei per muscle fiber was significantly higher in the training group (p < 0.05), while the myonuclear domain was significantly smaller in the training group (p < 0.05).

Satellite cells per muscle fiber and the percentage of satellite cells

The satellite cells per muscle fiber and percentage of satellite cells in both groups are shown in Table 2. There were significantly more satellite cells per muscle fiber in the training group (p < 0.05), and the percentage of satellite cells was significantly higher in the training group (p < 0.05). Furthermore, the percentage of satellite cells was positively correlated with the distance run (r = 0.61, p < 0.05; Figure 3).

DISCUSSION

The effects of resistance training on satellite cells were well studied but there are a few studies about the effects of endurance training on satellite cells. A previous study in human shows that the amplitude of the increase in satellite cell number following an high intensity interval training is within the same range as that reported in response to strength training (Charifi et al., 2003). Verney et al., 2008 also demonstrat the effects of 14 weeks of concurrent lower body endurance and upper body resistance training on vastus lateralis and deltoid muscles of elderly men and they show that satellite cell pool increases similarly in both muscles, mainly in type II muscle fibers. It is very interesting that satellite cells can respond to a training intensity much lower than that used in resistance training because the power developed at VO2peak is about 25% of the maximal power (Charifi et al., 2003; Kadi et al., 2005). However, these human studies investigated effects of high intensity interval training to elderly men and the training intensity seems to have been relatively high as an endurance training. In addition, fiber area of vastus lateralis muscle which was mainly recruited by the endurance training was significantly increased although aerobic capacity was also increased.

The purpose of this study was to clarify the effect of low-intensity, long-duration exercise training on satellite cells in skeletal muscle without associated muscle hypertrophy. As expected, the voluntary running model enhanced citrate synthase activity but caused no changes in absolute muscle mass or fiber size. The main finding was that voluntary running significantly increased the number of satellite cells in the plantaris muscle and that the increase in satellite cells was positively correlated with the distance run (r = 0.61, p < 0.05). To our knowledge, this is the first study to show an increase in the number of satellite cells in rat skeletal muscle with voluntary running training without muscle hypertrophy.

Increase in satellite cells with voluntary wheel running

Many studies have shown increases in the number of satellite cells following resistance training that leads to muscle hypertrophy (Kadi and Thornell, 2000; Kadi et al., 2004; Mackey et al., 2007; Roth et al., 2001). An increase in the number of satellite cells is reported to be associated with fibroblast growth factor (Sheehan and Allen, 1999) and insulin-like growth factor-I (IGF-I) (Charge and Rudnicki, 2004). As resistance training increases IGF-I secretion, it also promotes satellite cell proliferation and fusion and causes muscle hypertrophy. However, IGF-I secretion is regulated mainly by serum testosterone and growth hormone, which are determined more by exercise intensity than exercise volume (Hawke, 2005). The purpose of prolonged endurance training, as in our study, is not to cause muscle hypertrophy, but rather to increase the oxidative capacity. Indeed, previous studies have demonstrated that voluntary wheel running did not affect the plantaris muscle mass or fiber size (Ishihara et al., 1998; Rodnick et al., 1989). In our study, the absolute muscle weight and mean muscle fiber area determined using a simple method did not differ significantly between the control and training groups, although the citrate synthase activity was increased in the training group. Therefore, the exercise intensity of voluntary wheel running training in this study was insufficient to induce muscle hypertrophy. Ishihara et al., 1998 also demonstrated that 8 weeks of voluntary running on an unloaded wheel did not increase the weight or fiber area of the plantaris muscle regardless of the distance run, whereas running on a wheel in the loaded condition did. In our study, the running wheel was unloaded, and the results were consistent with the previous study. Given that voluntary running does not result in an increase in IGF-I mRNA expression in hind limb muscles (Matsakas et al., 2004), we speculate that the increase in the number of satellite cells observed in this study was not associated with hypertrophy involving the hormonal mechanisms observed in resistance training.

Verney et al., 2008 have recently suggested that satellite cell population in the human skeletal muscle might be genetically determined. However, in our study model, the same strain, gender and age of rats were obtained from a licensed laboratory animal vender and they were randomly assigned to either a control or training group. In addition, their voluntary running activities in the training group were between about 2 and 9 km·day-1 and it was very similar to previous studies and rats in the training group would not be especially talented as high runners (Ishihara et al., 1998; Rodnick et al., 1989). Therefore, it is thought that there was no difference of genetic factors between the two groups and that the involvement of genetic factor in the regulation of satellite cell content could be ruled out in this study model.

The activation of satellite cells may also involve exercise- induced localized ultrastructural damage, segmental fiber damage, and the release of inflammatory substances or growth factors (Kadi et al., 2005). Myofiber damage leads to the release of nitric oxide, which mediates the release of active hepatocyte growth factor from the heparin sulfate chains on the extracellular matrix and surrounding myofibers (Hawke, 2005). In the present study, it is not clear whether physical activity per se or muscle injury induced by exercise training secondarily stimulated satellite cell division; nevertheless, running may markedly stimulate satellite cells.

For example, McCormick and Thomas, 1992 showed that 10 weeks of progressive treadmill running doubled the satellite cell mitotic activity and doubled the number of damaged fibers in the soleus muscle of rats. In addition, Umnova and Seene, 1991 reported that the number of satellite cells increased 2.5-fold with local muscle damage after 6 weeks of treadmill training. It has been reported that voluntary wheel running in the mouse causes eccentric contractions, damaging the hind limb muscles (Werning et al., 1990). Furthermore, regardless of strain of mice, hind limb muscles are damaged and repaired with voluntary wheel running (Irintchev and Wernig, 1987). Although we did not investigate whether the voluntary wheel running caused muscle damage, we believe that it would have occurred, as in the previous studies. Therefore, the muscle damage induced by daily voluntary running may stimulate an increase in the number of satellite cells.

Changes in domain size and endurance training

Although the fiber area did not differ between the control and training groups in this study, voluntary wheel running significantly increased the number of myonuclei. As a result, the myonuclear domain size was significantly smaller in the training group. One possible explanation for the ability of endurance training to induce an increase in the number of myonuclei is related to a change in fiber type. The number of myonuclei is influenced by fiber type: muscle fibers of slow muscle have smaller myonuclear domains than those of fast muscle (Roy et al., 1999). In the plantaris muscle of cats, slow fibers have 25 to 50% more myonuclei in a longitudinal section and a smaller average myonuclear domain size compared with fast fibers (Allen et al., 1995). Voluntary wheel running is considered one of the most effective types of exercise training to increase oxidative capacity in rodents (Rodnick et al., 1989); it can increase the percentage of fast-twitch oxidative glycolytic fibers and decrease the percentage of fast-twitch glycolytic fibers in the rat plantaris muscle (Ishihara et al., 1991). Although we did not determine muscle fiber type in the plantaris muscle, it is possible that the voluntary wheel running training in our study transformed fast-twitch glycolytic muscle fibers into slow or oxidative fibers, as in previous studies. Therefore, the increase in the number of myonuclei with endurance training could be related to changes in muscle fiber type and the concomitant increase in the oxidative capacity of fast type fibers in the plantaris muscle. Alternatively, an increase in muscle nuclei in the fast fibers may be a prerequisite for a fast-to- slow fiber transition (Putman et al., 2000).

In addition, in this study, the percentage of satellite cells was positively correlated with the distance run. Satellite cell activation occurs in response to various protocols that enhance contractile activity. Putman et al., 1999 showed that low-frequency electrical stimulation of fast-twitch muscles in the rat led to a time- dependent increase in satellite cell content and myonuclear density, although the experiment did not involve physiological conditioning such as exercise training. Briefly, they showed that the percentage of satellite cells increased from 3.8% in control muscle to 7.9, 11.5, and 13.8% in muscles stimulated for 5, 10, and 20 days, respectively, with the transformation of existing fast fibers into slower fibers. In our study, the percentage of satellite cells was positively correlated with the distance run (r = 0.61, p < 0.05; Figure 3); the greater the total distance run or time spent exercising, the greater the percentage increase in satellite cells. In addition, citrate synthase activity was significantly higher in the training group, and the increase was also a function of the distance run (r = 0.62, p < 0.05; Figure 2). Combined, these results indicate a relationship between an increase in satellite cell number and amount of exercise or muscular oxidative capacity. However, we did not determine muscle fiber types and regional differences (e.g. distal, middle, or proximal) in the plantaris muscle and did not analyze a slow type of muscle like the soleus muscle. Further investigation is required to elucidate the muscle fiber type and region specific adaptation of satellite cells with endurance training.

New myonuclei arise by the incorporation of proliferating satellite cells to maintain the myonuclear domain size, and an increase in the number of myonuclei generally occurs with increased muscle fiber area (Kadi and Thornell, 2000). Resistance training was shown to increase the muscle fiber area, yet the number of myonuclei was unchanged (Hikida et al., 1998; Kadi et al., 2004). Kadi et al., 2004 explained that until a certain limit of hypertrophy is reached, an increase in the area of muscle fibers could occur without the addition of new myonuclei. If endurance training were to result in the opposite adaptation to the phenomenon seen in resistance training, it may be possible that the satellite cells and myonuclei change first. Further investigation is required to elucidate the adaptation of satellite cells and myonuclear domain that occurs with endurance training.

CONCLUSION

The present study showed that voluntary running can induce the proliferation of satellite cells without changing the mean fiber area in the rat plantaris muscle; this increase in satellite cell content is a function of the distance run. This study found that endurance training can be used as preconditioning to increase muscle volume and to improve muscle function. Further study is necessary to clarify the mechanisms of satellite cell proliferation and differentiation following endurance training.

ACKNOWLEDGEMENTS

Our research was partly supported by Grants-in-Aid for Scientific Research (16300212 and 12480011 to H.N.) and High Technology Research Center Grants for Juntendo University from the Ministry of Education, Culture, Sports, Science, and Technology of Japan.

AUTHOR BIOGRAPHY

Journal of Sports Science and Medicine Mitsutoshi Kurosaka
Employment: Ph.D. Student, Graduate School of Health and Sports Science, Juntendo University, Japan
Degree: MSc
Research interests: Muscle hypertrophy and satellite cell.
E-mail: kuromitsumail@ybb.ne.jp
 

Journal of Sports Science and Medicine Hisashi Naito
Employment: Associate Professor, Graduate School of Health and Sports Science, Juntendo University, Japan
Degree: PhD
Research interests: Stress proteins and exercise.
E-mail: naitoh@sakura.juntendo.ac.jp
 

Journal of Sports Science and Medicine Yuji Ogura
Employment: Assistant professor, Department of Physiology, St. Marianna University School of Medicine, Japan
Degree: PhD
Research interests: Alpha-actinin-3 and stress proteins.
E-mail: yuji_ogura@marianna-u.ac.jp
 

Journal of Sports Science and Medicine Atsushi Kojima
Employment: Doctor, St. Marianna University School of Medicine Hospital, Japan
Degree: PhD
Research interests: Muscle regeneration and satellite cell.
E-mail: atsushikojima@marianna-u.ac.jp
 

Journal of Sports Science and Medicine Katsumasa Goto
Employment: Professor, Laboratory of Physiology, Toyohashi SOZO University, Japan
Degree: PhD
Research interests: Muscle hypertrophy and atrophy.
E-mail: gotok@sepia.ocn.ne.jp
 

Journal of Sports Science and Medicine Shizuo Katamoto
Employment: Professor, Graduate School of Health and Sports Science, Juntendo University, Japan
Degree: PhD
Research interests: Exercise training and aging.
E-mail: atamoto@sakura.juntendo.ac.jp
 
 
REFERENCES
Journal of Sports Science and Medicine Allen D.L., Monke S.R., Talmadge R.J., Roy R.R., Edgerton V.R. (1995) Plasticity of myonuclear number in hypertrophied and atrophied mammalian skeletal muscle fibers. Journal of Applied Physiology 78, 1969-1976.
Journal of Sports Science and Medicine Appell H.J., Forsberg S., Hollmann W. (1988) Satellite cell activation in human skeletal muscle after training: evidence for muscle fiber neoformation. International Journal of Sports Medicine 9, 297-299.
Journal of Sports Science and Medicine Bradford MM. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical biochemistry 72, 248-254.
Journal of Sports Science and Medicine Charge S.B., Rudnicki M.A. (2004) Cellular and molecular regulation of muscle regeneration. Physiological Reviews 84, 209-238.
Journal of Sports Science and Medicine Charifi N., Kadi F., Feasson L., Denis C. (2003) Effects of endurance training on satellite cell frequency in skeletal muscle of old men. Muscle & Nerve 28, 87-92.
Journal of Sports Science and Medicine Hawke T.J. (2005) Muscle stem cells and exercise training. Exercise and Sport Sciences Reviews 33, 63-68.
Journal of Sports Science and Medicine Hikida R.S., Walsh S., Barylski N., Campos G., Hgerman F.C., Staron R.S. (1998) Is hypertrophy limited in elderly muscle fibers?. A comparison of elderly and young-trained men. Basic and applied Myology 8, 419-427.
Journal of Sports Science and Medicine Irintchev A., Wernig A. (1987) Muscle damage and repair in voluntarily running mice: strain and muscle differences. Cell and Tissue Research 249, 509-521.
Journal of Sports Science and Medicine Ishihara A., Inoue N., Katsuta S. (1991) The relationship of voluntary running to fibre type composition, fibre area and capillary supply in rat soleus and plantaris muscles. European Journal of Applied Physiology and Occupational Physiology 62, 211-215.
Journal of Sports Science and Medicine Ishihara A., Roy R.R., Ohihara Y., Ibata Y., Edgerton V.R. (1998) Hypertrophy of rat plantaris muscle fibers after voluntary running with increasing loads. Journal of Applied Physiology 84, 2183-2189.
Journal of Sports Science and Medicine Jasmin B.J., Gardiner P.F. (1987) Patterns of EMG activity of rat plantaris muscle during swimming and other locomotor activities. Journal of Applied Physiology 63, 713-718.
Journal of Sports Science and Medicine Kadi F., Charifi N., Denis C., Lexell J., Andersen J.L., Schjerling P., Olsen S., Kjaer M. (2005) The behaviour of satellite cells in response to exercise: what have we learned from human studies?. Pflugers Archive 451, 319-327.
Journal of Sports Science and Medicine Kadi F., Schjerling P., Andersen L.L., Charifi N., Madsen J.L., Christensen L.R., Andersen J.L. (2004) The effects of heavy resistance training and detraining on satellite cells in human skeletal muscles. The Journal of Physiology 558, 1005-1012.
Journal of Sports Science and Medicine Kadi F., Thornell L.E. (2000) Concomitant increases in myonuclear and satellite cell content in female trapezius muscle following strength training. Histchemistry and Cell Biology 113, 99-103.
Journal of Sports Science and Medicine Kojima A., Goto K., Morioka S., Naito T., Akema T., Fujiya H., Sugiura T., Ohira Y., Beppu M., Aoki H., Yoshioka T. (2007) Heat stress facilitates the regeneration of injured skeletal muscle in rats. Journal of Orthopaedic Science 12, 74-82.
Journal of Sports Science and Medicine Lambert M.I., Noakes T.D. (1990) Spontaneous running increases VO2max and running performance in rats. Journal of Applied Physiology 68, 400-403.
Journal of Sports Science and Medicine Mackey A.L., Esmarck B., Kadi F., Koskinen S.O., Kongsgaard M., Sylvestersen A., Hansen J.J., Larsen G., Kjaer M. (2007) Enhanced satellite cell proliferation with resistance training in elderly men and women. Scandinavian Journal of Medicine & Science in Sports 117, 34-42.
Journal of Sports Science and Medicine Matsakas A., Nikolaidis M.G., Kokalas N., Mougios V., Diel P. (2004) Effect of voluntary exercise on the expression of IGF-I and androgen receptor in three rat skeletal muscles and on serum IGF-I and testosterone levels. International Journal of Sports Medicine 225, 502-508.
Journal of Sports Science and Medicine Mauro A. (1961) Satellite cell of skeletal muscle fibers. Journal of biophysical and Biochemical Cytology 99, 493-495.
Journal of Sports Science and Medicine McCormick K.M., Thomas D.P. (1992) Exercise-induced satellite cell activation in senescent soleus muscle. Journal of Applied Physiology 72, 888-893.
Journal of Sports Science and Medicine Putman C.T., Dusterhoft S., Pette D. (1999) Journal of Applied Physiology.
Journal of Sports Science and Medicine Putman C.T., Dusterhoft S., Pette D. (2000) Satellite cell proliferation in low frequency-stimulated fast muscle of hypothyroid rat. American Journal of Physiology 279, C682-690.
Journal of Sports Science and Medicine Rodnick K.J., Reaven G.M., Haskell W.L., Sims C.R., Mondon C.E. (1989) Variations in running activity and enzymatic adaptations in voluntary running rats. Journal of Applied Physiology 66, 1250-1257.
Journal of Sports Science and Medicine Roth S.M., Martel G.F., Ivey F.M., Lemmer J.T., Tracy B.L., Metter E.J., Hurley B.F., Rogers M.A. (2001) Skeletal muscle satellite cell characteristics in young and older men and women after heavy resistance strength training. Journal of Gerontlogy Series A: Biological Sciences and Medical Sciences 56, B240-247.
Journal of Sports Science and Medicine Roy R.R., Monke S.R., Allen D.L., Edgerton V.R. (1999) Journal of Applied Physiology.
Journal of Sports Science and Medicine Schultz E., McCormick K.M. (1994) Skeletal muscle satellite cells. Revies of Physiology, Biochemistry and Pharmacology 123, 213-257.
Journal of Sports Science and Medicine Sheehan S.M., Allen RE. (1999) Skeletal muscle satellite cell proliferation in response to members of the fibroblast growth factor family and hepatocyte growth factor. Journal of Cell Physiology Cell Physiology 181, 499-506.
Journal of Sports Science and Medicine Srere P. (1969) Citrate synthase. Methods in Enzymology 13, 3-13.
Journal of Sports Science and Medicine Umnova M.M., Seene T.P. (1991) The effect of increased functional load on the activation of satellite cells in the skeletal muscle of adult rats. International Journal of Sports Medicine 12, 501-504.
Journal of Sports Science and Medicine Verney J., Kadi F., Charifi N., Féasson L., Saafi M.A., Castells J., Piehl-Aulin K., Denis C. (2008) Effects of combined lower body endurance and upper body resistance training on the satellite cell pool in elderly subjects. Muscle & Nerve 38, 1147-1154.
Journal of Sports Science and Medicine Wernig A., Irintchev A., Weisshaupt P. (1990) Muscle injury, cross-sectional area and fibre type distribution in mouse soleus after intermittent wheel-running. Journal of Physiology 428, 639-652.
 
 
 
Home Issues About Authors
Contact Current Editorial board Authors instructions
Email alerts In Press Mission For Reviewers
Archive Scope
Supplements Statistics
Most Read Articles
  Most Cited Articles
 
  
 
JSSM | Copyright 2001-2020 | All rights reserved. | LEGAL NOTICES | Publisher

It is forbidden the total or partial reproduction of this web site and the published materials, the treatment of its database, any kind of transition and for any means, either electronic, mechanic or other methods, without the previous written permission of the JSSM.

This work is licensed under a Creative Commons License Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.