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Département de Physiologie Systémique, Institut de Médecine Aésopatiale du Service de Santé des Acmées, 91223 Brétigny sur Orge cedex; and Laboratoire de Biologie Physicochimique, Unité de Recherche Associée, Centre National de la Recherche Scientifique 1131, Université Paris Sud, 91405 Orsay, France
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Bigard, Xavier A., Chantal Janmot, Danièle Merino,
Françoise Lienhard, Yannick C. Guezennec, and Anne D'Albis.
Endurance training affects myosin heavy chain phenotype in
regenerating fast-twitch muscle. J. Appl.
Physiol. 81(6): 2658-2665, 1996.
The aim of this
study was to analyze the effects of treadmill training (2 h/day, 5 days/wk, 30 m/min, 7% grade for 5 wk) on the expression of myosin
heavy chain (MHC) isoforms during and after regeneration of a
fast-twitch white muscle [extensor digitorum longus (EDL)]. Male Wistar rats were randomly assigned to a sedentary
(n = 10) or an endurance-trained (ET;
n = 10) group. EDL muscle degeneration and regeneration were induced by two subcutaneous injections of a snake
toxin. Five days after induction of muscle injury, animals were trained
over a 5-wk period. It was verified that ~40 days after venom
treatment, central nuclei were present in the treated EDL muscles from
sedentary and ET rats. The changes in the expression of MHCs in EDL
muscles were detected by using a combination of biochemical and
immunocytochemical approaches. Compared with contralateral nondegenerated muscles, relative concentrations of types I, IIa, and
IIx MHC isoforms in ET rats were greater in regenerated EDL muscles
(146%, P < 0.05; 76%,
P < 0.01; 87%,
P < 0.01, respectively). Their elevation corresponded to a decrease
in the relative concentration of type IIb MHC (
36%,
P < 0.01). Although type I accounted
for only 3.2% of total myosin in regenerated muscles from the ET
group, the cytochemical analysis showed that the proportion of positive staining with the slow MHC antibody was markedly greater in regenerated muscles than in contralateral ones. Collectively, these results demonstrate that the regenerated EDL muscle is sensitive to endurance training and suggest that the training-induced shift in MHC isoforms observed in these muscles resulted from an additive effect of regeneration and repeated exercise.
rat skeletal muscle; treadmill running; immunohistochemistry; myosin heavy chain isoforms; extensor digitorum longus muscle
regeneration
INTRODUCTION DURING DEVELOPMENT, muscle fibers are formed by the
fusion of myoblasts to give rise to myotubes that mature into
myofibers. Fetal muscle fiber formation results from a biphasic
mechanism. Early myogenic cells fuse to form multinucleated primary
myotubes that serve as a scaffold around which secondary generations of mononuclear cells fuse to form secondary myotubes (28). It is thus
clear that adult muscle fibers in mammals originate from at least two
populations of myotubes (26, 30). During late fetal development, a
population of myogenic cells gives rise to the mononucleate satellite
cells (34). These cells, located within the basal lamina of adult
fibers, are the source of new myofibers, either during muscle growth
(2) or during regenerative muscle development (1, 7).
Myosin, the major protein of the thick filament, exists in many
distinct isozymes, as a result of the combination of several isoforms
of both heavy and light chains (27). Myosin heavy chain (MHC) isoforms
have myosin adenosinetriphosphatase activities that correlate with the
speed of muscle fiber shortening (4). Therefore, the MHC profile has
been used as a phenotypic marker for functional aspects of muscle
fibers. Several developmental and adult isoforms of MHCs have been
identified in limb muscles (27). It has been suggested that MHC
transitions occurring during the development of mammalian muscles are
determined by both the heterogeneity of early myoblasts and
environmental factors, including neuronal influences and hormonal
signals (20-22, 30). At least two types of primary myotubes, slow
primaries and fast primaries, and two types of secondary myotubes have
been distinguished in developing mammalian muscles (21). During
development, slow primaries express embryonic and slow MHC isoforms but
no fetal isoform (6, 12, 21, 22). A transition from embryonic to slow
MHC occurs in primary slow myofibers, while secondary generation
myofibers undergo an embryonic-to-neonatal transition and subsequently
a neonatal to either adult fast or slow myosin transition (12, 22, 30).
In adult skeletal muscle, the expression of MHC isoforms is determined
by factors such as neural activity patterns and hormonal and mechanical
factors. However, experiments on denervated adult rat extensor
digitorum longus (EDL) muscles showed that fibers arising from slow
primary myotubes do not lose their identity and reexpress slow myosin
after neural influence has been suppressed (21). These data suggested
that the adult muscle phenotype resulted not only from environmental
factors (i.e. mechanical-, nerve- or hormone-dependent mechanisms) but also from its developmental heterogeneity.
Satellite cells (also termed adult myoblasts) are activated in response
to degeneration, proliferate, and fuse to form myotubes that mature to
adult muscle fibers (1). Although regeneration generally reproduces
many of the events that characterize normal development, there are
differences between fetal and postnatal myofiber formation that involve
different populations of myoblasts and myotubes and regeneration giving
rise to a muscle comprising a homogeneous population of fibers deriving
from satellite cells (9, 35). Specific neural activity and
thyroid hormones have been shown to exert important modifying effects
on the establishment of fast and slow phenotypes in regenerating
muscles (10, 11, 14, 35). In addition, postural load is an important
component in the induction of slow MHCs in regenerating muscle (5).
Moreover, with respect to myosin isoform content, it has been
previously demonstrated that regenerated myofibers are more homogeneous
than are control fibers to neural activity (35) and changes in
mechanical load (5).
Endurance training has been shown to elicit a shift in histochemically
determined fiber types in some skeletal muscles of rats (17). A
fast-to-slow shift in either the isomyosin distribution (16, 18) or MHC
isoforms (32) has been observed in rats after exercise training.
However, the results of these studies clearly demonstrate that the
training-induced changes in myosin expression in skeletal muscles are
of limited extent. When endurance training induced a significant
reduction in the relative content of the fast (16) or type IIb MHC (32)
in fast-twitch red muscles, the reverse increase in the slow isoform of
myosin was either inconsistent (16) or lacking (32). Moreover,
endurance training had only little impact on myosin expression in
fast-twitch white muscles such as the white region of the medial
gastrocnemius or the vastus lateralis (16) or on fiber type transition
in the EDL (17). It has been suggested that the apparently lower
responsiveness of fast-twitch white muscles to endurance training could
be related to their weak recruitment during locomotor activity.
However, the role of the developmental heterogeneity of skeletal muscle fibers in MHC expression in fast-twitch white muscle has never been
evaluated during endurance training.
The aim of this study was to analyze the expression of MHC isoforms in
regenerating EDL muscles submitted to increased functional demand by
endurance training. We tested the following hypotheses: 1) endurance training causes a
fast-to-slow transition in MHC isoforms in regenerating EDL muscles,
and 2) the effects of endurance training on the shift in the relative distribution of the MHC isoforms
are more marked in regenerating than in control EDL muscles.
MATERIALS AND METHODS
160°C) by liquid nitrogen. All samples were stored at 80°C until histochemical and
biochemical analyses were performed. The two muscles (i.e., injected
with toxin and contralateral) from each animal were then
processed for histochemical and biochemical
investigations.
In the present study, the heterogeneity of muscle tissue was assessed
by using immunohistochemical detection of fast and slow MHCs within
single muscle fibers and by biochemical analysis of the MHC isoforms in
the whole muscle. A combination of these two complementary techniques
has been selected to analyze the expression of contractile proteins in
skeletal muscle.
Histology and immunohistochemistry.
Transverse sections (16 µm thick) were cut on a cryostat maintained
at 20°C and were stained with hematoxylin and eosin. Three
mouse monoclonal antibodies directed against different MHC isoforms
were used. A skeletal myosin antibody that reacted with rat fast
neonatal and types IIa, IIb and IIx MHC isoforms, but not with slow
myosin, was obtained from Sigma Chemical (M4276, St. Louis, MO); this
antibody is referred to as a fast MHC antibody. A monoclonal antibody
specifically reacting with rat slow MHC (type I MHC) was purchased from
Novocastra (NCL-MHCS, Newcastle upon Tyne, UK). Finally, an antibody
referred to as RNMY2/9D2 reacted with both embryonic and neonatal MHC
isoforms but not with any of the adult isoforms. This antibody was
purchased from Novocastra (NCL-MHCD).
Serial transverse cryostat sections were incubated with appropriate
dilutions of primary antibody for 1 h in a humidified chamber at
37°C. After three washings with phosphate-buffered saline (PBS),
sections were treated with a rhodamine-labeled secondary antibody
(T2402, Sigma Chemical) for 30 min in a humidified chamber at 37°C.
After washings with PBS, sections were mounted in glycerol and viewed
with a fluorescence microscope fitted for epifluorescent illumination.
Analysis of MHCs.
EDL muscles were subjected to the analysis of MHC isoforms by sodium
dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) according
to the method described by Talmadge and Roy (33) and adapted by Janmot
and d'Albis (23). Frozen muscles were minced with scissors in 9 volumes of a solution containing 20 mM NaCl, 5 mM sodium phosphate, and
1 mM ethylene glycol-bis(
-aminoethyl ether)-N,N,N
,N-tetraacetic
acid (EGTA) (pH 6.5). Myosin was then extracted with 3 volumes of 100 mM sodium pyrophosphate, 5 mM EGTA, and 1 mM dithiothreitol (pH 8.5).
After 30 min of gentle shaking, the mixture was centrifuged at 12,000 g for 10 min, and the supernatant
containing myosin was diluted twice with glycerol and stored at
20°C. Five-microliter samples of this myofibril solution
were added to 35 µl of denaturing buffer and heated at 100°C for
3 min. Separating gels contained 30% glycerol, 8% acrylamide-bis (50:1), 0.2 M tris(hydroxymethyl)aminomethane (Tris), 0.1 M glycine, and 0.4% SDS. Stacking gels contained 30% glycerol, 4%
acrylamide-bis (50:1), 70 mM Tris, 4 mM EDTA, and 0.4% SDS. An aliquot
of the sample (5-10 µl) was subjected to SDS-PAGE analysis. Gels
were run at constant voltage (70 V) for ~28 h and then were stained with Coomassie blue. The relative amounts of the different MHCs were
measured by using a densitometer equipped with an integrator.
Whole muscle citrate synthase activity.
A 10-mg sample of muscle was homogenized at 4°C in 1 ml of 0.3 mM
phosphate buffer containing 0.05% bovine serum albumin (pH 7.7).
Citrate synthase (CS) activity (EC 4.1.3.7) was determined on this
homogenate by using NAD/NADH spectroscopic assays derived from the
technique of Lowry and Passonneau (25). This enzyme was chosen as a
marker of muscle oxidative capacity. CS activity was expressed in
micromoles substrate utilized per minute per milligram of muscle
weight.
Plasma thyroid hormone determination.
A 5-ml blood sample was obtained from the abdominal aorta for
determination of free 3,5,3-triiodothyronine
(T3). Blood samples were
centrifuged at 3,500 revolutions/min at 4°C, and the plasma supernatant was frozen and stored at 20°C until analyzed.
Plasma T3 concentrations were
determined by using a commercial radioimmunoassay kit (OCFH07-FT3, CIS
bio international, Gif-sur-Yvette, France).
Statistical procedures.
All data are presented as means ± SE. Endurance training and muscle
regeneration effects were determined by a two-way analysis of variance.
When appropriate, a Student's unpaired
t-test was used to determine
differences between S and ET groups. In addition, a one-tailed
Student's t-test was used to assess
differences between values for EDL regenerated muscles and their
respective control values recorded in contralateral muscles.
Significance was established at P < 0.05 after adjustment by using the Bonferroni correction.
RESULTS
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MHC distribution. A representative polyacrylamide gel showing the separation of MHC isoforms in EDL muscle is shown in Fig. 2. As shown in Table 2, endurance exercise had only little impact on the MHC profile of nondegenerated control muscles. The slight but significant increase in type I MHC (P < 0.05) was associated with a trend toward an increase in type IIx MHC (29%) and a decrease in type IIb MHC (
10%).
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25%;
P < 0.05).
In the ET group, regenerated muscles showed a greater percentage of
type I MHC (P < 0.05) and a smaller
percentage of type IIb MHC (P < 0.05) than did those in the S group. This was associated with a trend
toward increase in type IIa and type IIx MHCs, in comparison with S
animals (48 and 26%, respectively).
The relative concentrations of types I, IIa, and IIx MHC isoforms in ET
rats were greater in regenerated EDL muscles than in contralateral
muscles (P < 0.05, P < 0.01, P < 0.01, respectively). This
elevation corresponded to a decrease in the relative concentration of
type IIb MHC (P < 0.01).
Compared with untreated muscles from the S group, the type IIb MHC of
regenerated muscles from the ET group decreased by 42%. This likely
resulted from an additive effect of muscle regeneration (25%)
and endurance training (10%; see above). Compared
with untreated muscles from S animals, regenerated muscles from ET rats
showed a 141% increase in the relative content of type IIx isoform and
a 158% increase in the relative content of type IIa isoform. Although
the relative content of slow type I MHC was 10-fold that found in S
rats, this isoform represented only ~3% of the MHC isoform profile.
Immunohistochemistry.
Qualitative analysis of MHC expression in S rats showed that, in
regenerated muscles, most fibers were stained with the fast MHC
antibody (Fig.
3C) and
that a minority of fibers were stained with the antibody against slow
MHC (Fig. 3D). Some fibers reacting with the fast MHC also reacted positively with the slow MHC antibody. The proportion of myofibers reacting with the slow MHC antibody was
slightly higher in regenerated EDL muscles than in control nondegenerated ones (Fig. 3, B and
D).
After 5 wk of running training, the nondegenerated muscles behaved like EDL muscles in ET rats. A small proportion of fibers reacted positively with the slow MHC antibody while a majority of fibers were uniformly stained with the antibody against fast MHC isoforms (Fig. 4, A and B). At ~40 days of regeneration, many fibers reacted with the slow MHC antibody, but the staining with this antibody was heterogeneous in intensity (Fig. 4D). Many fibers were clearly stained with both slow and fast MHC antibodies (Fig. 4, C and D). In some regenerated muscles, the pattern of myosin expression within fibers, as detected by using this cytochemical approach, was clearly in contrast with that expected in such a fast-twitch white muscle, even in ET rats (Fig. 4, E and F).
No reactivity was seen with the antibody against the embryonic and neonatal MHCs in either the S or ET groups (data not shown). Muscle CS activity. In the present study, it was verified that the training program resulted in an increase in the activity of CS, a respiratory enzyme frequently used as a training marker (P < 0.02; Table 3). CS activity was found to increase by 22% in untreated muscles. The enhanced activity of this mitochondria marker is consistent with adaptive responses to running training recorded in such fast-twitch white muscles (3). On the other hand, no significant effect of muscle regeneration was detected in CS activity.
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DISCUSSION
Endurance exercise training is known to promote a transition in the MHC profile of fast-twitch muscles to a slower phenotype in adult rats (32). In the present study, the changes in EDL muscle MHC phenotype were detected by using a combination of biochemical and immunocytochemical approaches. The major findings of this study are that 1) a switch from IIb to IIa MHC expression, with a drastic increase in type IIx MHC, occurs as a result of regeneration in EDL muscles from sedentary rats; 2) endurance training causes a shift from type IIb to types IIx and IIa MHC isoforms in fast muscle during regeneration; 3) the training-induced shift in fast MHCs toward slower isoforms mainly resulted from an additive effect of endurance training and muscle regeneration; and 4) although the training-induced increase in the proportion of type I MHC was quantitatively limited in EDL regenerated muscles, slow MHC staining was seen in a great number of fibers.
The expression of specific adult MHC isoforms during development is regulated by a myogenic component that stems from the heterogeneity of myoblasts and is sensitive to a number of exogeneous factors, including neural activity patterns (14, 35) and hormones (11, 13, 29). As has been previously shown, snake toxins possessing phospholipase A2 activity induce extensive degeneration of myofibers by a direct toxic effect, followed by a complete regenerative process (8). In adult mammalian muscles, many aspects of regeneration parallel the events that characterize normal development (35). Previous data suggested that venom-induced degeneration did not result in functional denervation and that regenerating muscles received neural input (5). This was in accordance with a previous report demonstrating that the functional reinnervation was restored in 97% of fibers 10 days after the injection of toxin (19). On the other hand, results of the present study provided evidence that the thyroid hormonal status was unaltered by endurance-exercise training. It is thus suggested that regenerating fibers receive neural input as early as 4-5 days after muscle damage (19) and that the shifts observed in the relative distribution of MHCs were not associated with changes in the thyroid status.
The present findings demonstrate that an increase in the content of
type IIx MHC occurred in regenerated EDL muscles in S rats. Because MHC
transitions appear to follow an obligatory pathway in the order type I
IIa IIx IIb (31), this finding may be interpreted as
1) an overall shift in the
expression of fast MHC isoforms from IIb toward slower isoforms,
related to the high responsiveness of regenerated myofibers to the
ambulatory activity of the rat, or
2) a specific upregulation of the
type IIx MHC gene. The concomitant increase in the type IIa and
decrease in the type IIb isoform appear to be consistent with the first
hypothesis. Because type IIx fibers containing type IIx MHC have a
relatively rich mitochondrial content and belong to motor units
characterized by a higher resistance to fatigue than that of type IIb
motor units (31), changes in physiological and biochemical properties of the regenerated muscles are expected. Moreover, the distribution study of myosin expression within fibers demonstrated that the slow
isoform was more frequently detected in regenerated myofibers than in
nondegenerated fibers. Taken together, these results support the
concept that the ambulatory activity of the rat exerts a significant influence on the pattern of myosin expression during regeneration, even
in fast-twitch white muscle.
Data exist to support the concept that endurance exercise alters the myosin distribution in some adult skeletal muscles of mammals, both in native and heavy chains (16, 18, 32). However, the pattern of myosin expression is not, or is only little, altered in the fast-twitch white muscles such as the white medial gastrocnemius and the white vastus lateralis (16). These data are consistent with the lack of significant change in the percent distribution of fiber types in EDL muscles from ET rats (17). It has been thus suggested that fast white muscles are insensitive to the specific stimuli of chronic endurance exercise in the rat. This could be related to the lack of recruitment of these muscles during the pattern of locomotion imposed on the rat and/or to the ontogenic heterogeneity of myofibers. This latter hypothesis was investigated in the present experiment by comparing the effects of endurance training on normal EDL muscles arising from several distinct classes of myotubes with those recorded after the EDL muscles have regenerated from a homogeneous population of satellite cells.
Running conditioning initiated 4-5 days after the EDL muscles were treated with venom toxin resulted in a shift in the distribution of MHC isoforms in comparison with regenerated muscles from S rats. This indicates that regenerated muscles are responsive to endurance training. The mechanisms by which endurance running exerts modifying effects on muscle fiber phenotypes are not clearly defined but are probably related to increased neuromuscular activity, stretch, and metabolic factors. The results from the present study based on both quantitative and qualitative data strongly suggest that the maturation of regenerated muscle, as reflected by the pattern of MHC distribution, is sensitive to increased neuromuscular activity. With use of a different experimental model of muscle regeneration, it was shown that the ablation of synergistic muscle, a model known to increase muscle work, did not alter the fiber type composition of nerve-implant soleus grafts (15). These results disagree with our data, and this discrepancy probably reflects the differences in regenerative models, types of alterations in neuromuscular activity, and MHC profile of selected muscles.
One of the main findings of the present study was that the training-induced shift in MHCs toward slower isoforms was more marked in regenerated than in control EDL muscles compared with untreated muscles from S rats. This was evidenced by the biochemical quantitative approach and especially by the immunohistochemical analysis of MHC expression. The analysis of the percent changes in the relative proportions of fast MHCs suggests that the increased expression of types IIa and IIx MHCs in regenerated muscles from ET rats resulted, at least in part, from an additive effect of muscle regeneration and chronic exercise. The present study demonstrates that endurance training decreased by ~40% the proportion of the fastest MHC isoform and increased twofold those of types IIa and IIx MHCs. However, because regenerated EDL muscles from ET rats contained very little slow type I MHC, it appears that the transition in the MHC profile had a limited extent. It remains to be seen whether increasing the duration of the running program leads to an increase in type I MHC accumulation in regenerated muscle of trained rats.
Although type I MHC contributed to only 3.2% of total myosin in regenerated muscles from ET rats, the immunohistochemical investigation of MHC expression clearly demonstrated that this isoform was detected in ~20-40% of myofibers (Fig. 4, E and F). This finding suggests that endurance training induces an increase in the number of regenerated fibers expressing type I MHC. Quantitative and qualitative results are not inconsistent but are clearly complementary. Because even low amounts of a given MHC isoform are detectable by immunohistochemical analysis, determination of the relative content of MHCs gives complementary results on the functional plasticity of EDL muscles to endurance training. Collectively, data from biochemical and cytochemical approaches reflect an increased capacity of type I MHC expression in regenerated muscles, with this isoform being expressed in a large number of fibers. This interpretation is consistent with the increased number of fibers coexpressing fast and slow MHC isoforms in regenerated muscles, as compared with contralateral muscles.
Early dynamic activity resulted in damage in muscle grafts leading to an impairment in muscle growth (15). In contrast, results of the present study demonstrated that regenerated muscles had a higher wet mass than did control muscles in both S and ET animals. As shown in Fig. 1, the size of fibers was similar in regenerated and untreated muscles. Because the histological analysis did not detect any sign of enlargement of the interstitial space, an increase in fiber number, in comparison with left-side muscles, could partly explain the difference in muscle mass. It has been shown that, in contrast to muscle grafts, numerous inflammatory cells and macrophages were present in venom-treated muscles. These cellular events may promote the release of growth factors and the proliferation of satellite cells, respectively (24). Whether these events lead to an increase in fiber number in regenerated muscles in comparison with untreated muscles remains to be clarified.
In summary, the present findings clearly show that endurance training exerts a significant impact on the pattern of MHC expression in a fast-twitch white muscle during regeneration. Under our experimental conditions, the shift in MHC isoforms recorded in regenerated muscles from trained rats resulted from an additive effect of endurance training and muscle regeneration. Because endurance training led to changes in the phenotypic expression of MHC isoforms within a fast-twitch muscle comprising a majority of fibers deriving from satellite cells, this finding raises questions about its unresponsiveness to repeated exercise in rats.
ACKNOWLEDGEMENTS
We thank D. Freund for preparation of the English translation of this manuscript.
FOOTNOTES
Address for reprint requests: A. X. Bigard, Unité de Bioénergétique, Centre de Recherches du Service de Santé des Armées, BP 87, 38702 La Tronche cedex, France.
Received 16 April 1996; accepted in final form 13 August 1996.
REFERENCES
| 1. | Allbrook, D. Skeletal muscle regeneration. Muscle Nerve 4: 234-245, 1981. |
| 2. | Allen, R. E., and L. L. Rankin. Regulation of satellite cells during skeletal muscle growth and development. Proc. Soc. Exp. Biol. Med. 194: 81-86, 1990. |
| 3. | Baldwin, K. M., D. A. Cooke, and W. G. Cheadle. Time course adaptations in cardiac and skeletal muscle to different running programs. J. Appl. Physiol. 42: 267-272, 1977. |
| 4. | Bárány, M. ATPase activity of myosin correlated with speed of muscle shortening. J. Gen. Physiol. 50: 197-218, 1967. |
| 5. | Bigard, A. X., D. Merino, B. Serrurier, F. Lienhard, C. Y. Guezennec, K. J. Bockhold, and R. G. Whalen. Role of weight-bearing function on the expression of myosin isoforms during regeneration of rat soleus muscles. Am. J. Physiol. 270 (Cell Physiol. 39): C763-C771, 1996. |
| 6. | Butler-Browne, G. S., and R. G. Whalen. Myosin isozyme transitions occurring during the postnatal development of the rat soleus muscle. Dev. Biol. 102: 324-334, 1984. |
| 7. | Church, J. C. T., R. F. X. Noronha, and D. B. Allbrook. Satellite cells and skeletal muscle regeneration. Br. J. Surg. 53: 638-642, 1966. |
| 8. | Couteaux, R., J. C. Mira, and A. d'Albis. Regeneration of muscles after cardiotoxin injury. Biol. Cell 62: 171-182, 1988. |
| 9. | D'Albis, A., R. Couteaux, C. Janmot, and J. C. Mira. Myosin isoform transitions in regeneration of fast and slow muscles during postnatal development of the rat. Dev. Biol. 135: 320-325, 1989. |
| 10. | D'Albis, A., R. Couteaux, C. Janmot, A. Roulet, and J. C. Mura. Regeneration after cardiotoxin injury of innervated and denervated slow and fast muscles of mammals. Myosin isoform analysis. Eur. J. Biochem. 174: 103-110, 1988. |
| 11. | D'Albis, A., M. Lenfant-Guyot, C. Janmot, C. Chanoine, J. Weinman, and C. Gallien. Regulation by thyroid hormones of terminal differentiation in the skeletal dorsal muscle. I. Neonatal mouse. Dev. Biol. 123: 25-32, 1987. |
| 12. | DeNardi, C., S. Ausoni, P. Moretti, L. Gorza, M. Velleca, M. Buckingham, and S. Schiaffino. Type 2X-myosin heavy chain is coded by a muscle fiber type-specific and developmentally regulated gene. J. Cell Biol. 123: 823-835, 1993. |
| 13. | Devor, S. T., and T. P. White. Myosin heavy chain phenotype in regenerating skeletal muscle is affected by thyroid hormone. Med. Sci. Sports Exercise 27: 674-681, 1995. |
| 14. | Esser, K., P. Gunning, and E. Hardeman. Nerve-dependent and -independent patterns of mRNA expression in regenerating skeletal muscle. Dev. Biol. 159: 173-183, 1993. |
| 15. | Esser, K. A., and T. P. White. Prior running reduces hypertrophic growth of skeletal muscle grafts. J. Appl. Physiol. 69: 451-455, 1990. |
| 16. | Fitzsimons, D. P., G. M. Diffee, R. E. Herrick, and K. M. Baldwin. Effects of endurance training on isomyosin patterns in fast- and slow-twitch skeletal muscles. J. Appl. Physiol. 68: 1950-1955, 1990. |
| 17. | Green, H. J., G. A. Klug, H. Reichmann, U. Seedorf, W. Wiehrer, and D. Pette. Exercise-induced fibre type transitions with regard to myosin, parvalbumin, and sarcoplasmic reticulum in muscles of the rat. Pfluegers Arch. 400: 432-438, 1984. |
| 18. | Gregory, P., R. B. Low, and W. S. Stirewalt. Changes in skeletal-muscle myosin isozymes with hypertrophy and exercise. Biochem. J. 238: 55-63, 1986. |
| 19. | Grubb, B. D., J. B. Harris, and I. S. Schofield. Neuromuscular transmission at newly formed neuromuscular junctions in the regenerating soleus muscle of the rat. J. Physiol. Lond. 441: 405-421, 1991. |
| 20. | Gunning, P., and E. Hardeman. Multiple mechanisms regulate muscle fiber diversity. FASEB J. 5: 3064-3070, 1991. |
| 21. | Hoh, J. F. Y. Myogenic regulation of mammalian skeletal muscle fibres. News Physiol. Sci. 6: 1-6, 1991. |
| 22. | Hughes, S. M., M. Cho, I. Karsch-Mizrachi, M. Travis, L. Silberstein, L. A. Leinwand, and H. M. Blau. Three slow myosin heavy chains sequentially expressed in developing mammalian skeletal muscle. Dev. Biol. 158: 183-199, 1993. |
| 23. | Janmot, C., and A. d'Albis. Electrophoretic separation of developmental and adult rabbit skeletal muscle myosin heavy chain isoforms: example of application to muscle denervation study. FEBS Lett. 353: 13-15, 1994. |
| 24. | Lefaucheur, J. P., and A. Sebille. The cellular events of injured muscle regeneration depend on the nature of the injury. Neuromusc. Disord. 5: 501-509, 1995. |
| 25. | Lowry, O. H., and J. W. Passonneau. A Flexible System of Enzymatic Analysis (1st ed.). New York: Academic, 1972. |
| 26. | Ontell, M., D. Bourke, and D. Hughes. Cytoarchitecture of the fetal murine soleus muscle. Am. J. Anat. 181: 267-278, 1988. |
| 27. | Pette, D., and S. Staron. Cellular and molecular diversities of mammalian skeletal muscle fibers. Rev. Physiol. Biochem. Pharmacol. 116: 1-76, 1990. |
| 28. | Rubinstein, N. A., and A. M. Kelly. Development of muscle fiber specialization in the rat hindlimb. J. Cell Biol. 90: 128-144, 1981. |
| 29. | Russell, S. D., N. A. Cambon, B. Nadal-Ginard, and R. G. Whalen. Thyroid hormone induces a nerve-dependent precocious expression of fast myosin heavy chain mRNA in rat hindlimb skeletal muscle. J. Biol. Chem. 263: 6370-6374, 1988. |
| 30. | Russell, S. D., N. A. Cambon, and R. G. Whalen. Two types of neonatal-to-adult fast myosin heavy chain transitions in rat hindlimb muscle fibers. Dev. Biol. 157: 359-370, 1993. |
| 31. | Schiaffino, S., and C. Reggiani. Myosin isoforms in mammalian skeletal muscle. J. Appl. Physiol. 77: 493-501, 1994. |
| 32. | Sullivan, V. K., S. K. Powers, D. S. Criswell, N. Tumer, J. S. Larochelle, and D. Lowenthal. Myosin heavy chain composition in young and old rat skeletal muscle: effects of endurance training. J. Appl. Physiol. 78: 2115-2120, 1995. |
| 33. | Talmadge, R. J., and R. R. Roy. Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J. Appl. Physiol. 75: 2337-2340, 1993. |
| 34. | Vivarelli, E., W. E. Brown, R. G. Whalen, and G. Cossu. The expression of slow myosin during mammalian somitogenesis and limb bud differentiation. J. Cell Biol. 107: 2191-2197, 1988. |
| 35. | Whalen, R. G., J. B. Harris, G. S. Butler-Browne, and S. Sesodia. Expression of myosin isoforms during notexin-induced regeneration of rat soleus muscles. Dev. Biol. 141: 24-40, 1990. |
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