Effects of unweighting and clenbuterol on myosin
light and heavy chains in fast and slow muscles of rat
Laurence
Stevens1,
Carole
Firinga1,
Bärbel
Gohlsch2,
Bruno
Bastide1,
Yvonne
Mounier1, and
Dirk
Pette2
1 Laboratoire de Plasticité Neuromusculaire,
Université des Sciences et Technologies de Lille, F-59655
Villeneuve d'Ascq, France; and 2 Faculty of Biology, University
of Constance, D-78457 Constance, Germany
 |
ABSTRACT |
To investigate the plasticity
of slow and fast muscles undergoing slow-to-fast transition, rat soleus
(SOL), gastrocnemius (GAS), and extensor digitorum longus (EDL) muscles
were exposed for 14 days to 1) unweighting by hindlimb
suspension (HU), or 2) treatment with the
2-adrenergic agonist clenbuterol (CB), or 3)
a combination of both (HU-CB). In general, HU elicited atrophy, CB
induced hypertrophy, and HU-CB partially counteracted the HU-induced atrophy. Analyses of myosin heavy (MHC) and light chain (MLC) isoforms
revealed HU- and CB-induced slow-to-fast transitions in SOL (increases
of MHCIIa with small amounts of MHCIId and MHCIIb) and the
upregulation of the slow MHCIa isoform. The HU- and CB-induced changes
in GAS consisted of increases in MHCIId and MHCIIb
("fast-to-faster transitions"). Changes in the MLC composition of
SOL and GAS consisted of slow-to-fast transitions and mainly
encompassed an exchange of MLC1s with MLC1f. In addition, MLC3f was
elevated whenever MHCIId and MHCIIb isoforms were increased. Because
the EDL is predominantly composed of type IID and IIB fibers, HU, CB,
and HU-CB had no significant effect on the MHC and MLC patterns.
extensor digitorum longus; gastrocnemius; hindlimb suspension; myosin; slow-to-fast transition; soleus
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INTRODUCTION |
SKELETAL MUSCLE HAS THE
CAPACITY to change its phenotype, not only in response to altered
functional demands, but also under the influence of specific growth
factors and hormones. As shown in numerous studies, increased
neuromuscular activity and loading both elicit fast-to-slow transitions
and decreased neuromuscular activity, and unloading causes transitions
in the reverse direction (22). Recently, the effects of
mechanical unloading by hindlimb unweighting (HU) on the expression of
myosin heavy chain (MHC) isoforms were investigated in rat soleus (SOL)
muscle (30). In agreement with previous studies (e.g., 5, 8, 31), pronounced atrophy and slow-to-fast transitions in the MHC
isoform pattern were observed. These transitions in MHC protein
isoforms were preceded by corresponding changes at the mRNA level
(28).
Clenbuterol (CB), a
2-adrenergic agonist, is known to
induce muscle hypertrophy (9, 15, 33) and has been shown
to counteract unloading-induced atrophy (1, 23, 33).
Moreover, several studies have established that CB additionally induces slow-to-fast transitions in rat SOL muscle (7, 19, 23). Taking into account these effects, it could be expected that CB not
only counteracts atrophy under conditions of unweighting but also
enhances slow-to-fast transitions under the same conditions.
The validity of these assumptions was investigated in the present study
on the effects of unweighting, CB treatment, and a combination of both
on three different rat muscles, SOL, extensor digitorum longus (EDL),
and the red portion of the gastrocnemius (GAS) muscle. It was of
interest to determine the extent of the adaptive responses of these
muscles because of their different fiber type composition and their
different functions. The slow SOL as well as the fast GAS are
antigravity muscles. The EDL is also fast, but is a nonpostural muscle.
Adult male rats were exposed to one of the following conditions: CB
treatment for 14 days, unweighting by hindlimb suspension for 14 days,
and CB treatment combined HU for 14 days. Control and experimental
muscles were investigated for changes in weight and myosin composition.
The analysis of myosin composition encompassed electrophoretic studies
of both the MHC and myosin light chain (MLC) isoforms.
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MATERIALS AND METHODS |
Animals and muscles.
Adult male Wistar rats (initial body wt ~260 g) were randomly divided
into four groups: control, CB-treated, hindlimb unweighted (HU), and CB
combined with hindlimb unweighting (HU-CB). The animal experiments, as
well as the animal maintenance conditions, were approved by the French
Ministries of Agriculture and Education (veterinary service of health
and animal protection, authorization no. 03805). HU for 14 days was
performed as previously described (29). CB (Sigma, St.
Louis, MO) was administered via the drinking water (30 mg/l) for 14 days (23). It was freshly prepared every day. At the end
of treatment, the animals were anesthetized by intraperitoneal
injection of ethylcarbamate, killed by exsanguination, and EDL,
GAS (red portion), and SOL muscles were dissected, blotted, and weighed
(Table 1). Thereafter, the muscles were
frozen in liquid N2 and stored at
70°C until analyzed.
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Table 1.
Comparison of body and muscle weights among the different groups for
soleus, gastrocnemius, and extensor digitorum longus muscles
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MHC and MLC electrophoresis.
Frozen muscle tissue was pulverized under liquid N2 in a
small steel mortar (21). MLC isoforms were separated by
one-dimensional electrophoresis according to Laemmli (16)
using the protocol of Salviati et al. (25). The positions
of the fast and slow MLC isoforms were identified on the gels by their
apparent molecular masses. Immunoblotting with an antibody that
recognized slow and fast troponin C isoforms (17) was used
to delineate the separate bands of MLC2f and troponin Cslow
(Fig. 1).

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Fig. 1.
One-dimensional separation of myofibrillar proteins from
rat soleus (SOL) and gastrocnemius (GAS) muscles in a 10-20% SDS
polyacrylamide gradient gel (silver stained). The position of the slow
(MLC1s, MLC2s) and the fast (MLC1f, MLC2f, MLC3f) myosin light chains
is indicated. The identity of bands representing fast and slow troponin
C subunits TnCf and TnCs was proved by immunoblotting.
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MHC isoforms were analyzed on a glycerol-containing 7% SDS
polyacrylamide gel as previously described (13). The gels
were silver stained (20) and evaluated by integrating
densitometry. At least two measurements were performed on each sample.
Statistical analyses.
Data are presented as means ± SD. After one-way analysis of
variance (ANOVA), Student's t-test was used as a post hoc
test to establish intergroup comparisons. The acceptable level of
significance was set at P < 0.05.
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RESULTS |
Changes in body and muscle mass.
CB did not affect body mass, however, rats exposed to HU and HU-CB lost
weight (Table 1). As judged from absolute and relative muscle masses,
CB induced hypertrophy, especially in the two fast muscles (EDL, GAS),
and to a lesser extent in slow SOL muscle. In contrast, HU induced
atrophy, which was greatest in SOL muscle, and less in the two fast
muscles (Table 1). CB treatment during HU alleviated the atrophic
response, thus partially counteracting the HU-induced atrophy. This
effect was greatest in the EDL, whereas compared with the control,
muscle mass was maintained. SOL muscle, with an almost 60% weight loss
after 14 days of HU, exhibited a smaller loss in mass. There was
~30% more muscle mass following HU-CB compared with HU alone.
Effects on MHC isoforms.
CB treatment, HU, and HU-CB elicited marked changes in the MHC
isoform pattern of SOL muscle (Fig.
2, Table
2). Generally, these changes consisted of
slow-to-fast transitions increasing in the order CB < HU < HU-CB. CB markedly elevated the relative concentration of MHCIIa at the
expense of MHCI and, in addition, induced low amounts of MHCIId and
MHCIIb. Under the HU condition, the relative concentration of MHCIIa
was less elevated than with CB, whereas MHCIId attained higher levels.
This shift toward the faster isoform indicated a more extensive
slow-to-fast transition by unweighting than by CB. The HU-CB condition
was characterized by a stronger shift toward the faster isoforms,
especially in view of the additional increases in MHCIId and MHCIIb.
The three fast isoforms together accounted for ~35% of the total MHC
complement, reaching relative concentrations of ~14%, ~12%, and
~7%, for MHCIIa, MHCIId, and MHCIIb, respectively. An additional
effect of HU and HU-CB on SOL was the appearance of small amounts of
the previously characterized slow MHCIa isoform (11) (see
Fig. 2). MHCIa was not detected in control and CB SOL muscles but
attained relative concentrations of ~5% and ~1.5% under
conditions of HU and HU-CB, respectively.

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Fig. 2.
Electrophoretic separation of slow and fast myosin heavy chain
(MHC) isoforms in extracts from rat SOL (top) and GAS
(bottom) muscles exposed to different experimental
conditions: Cont, control; CB, clenbuterol; HU, hindlimb unweighting;
HU-CB, hindlimb unweighting combined with CB treatment. The
electrophoretic separations of SOL and GAS muscle extracts were
performed on same gels. The order of the lanes at bottom was
changed to match the order of the lanes at top.
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Except for slight decreases in the relative concentration of MHCI, CB,
HU, and HU-CB remained without effects on the MHC complement of EDL
muscle (Table 3). This contrasted with
the conspicuous changes seen in the red GAS (Table
4). Its predominantly fast fiber
population responded with shifts toward faster MHC isoforms to the
various experimental conditions. These changes were less pronounced
than in SOL muscle. CB tended to increase MHCIIb, most likely at the
expense of MHCIIa, as this isoform was reduced, and MHCIId was
unaltered. Similar changes were observed after HU where, in addition to
the MHCIIa to MHCIIb shift, MHCI tended to decrease. HU-CB did not
induce additional changes.
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Table 3.
Effects of CB, HU, and HU-CB on percentage distribution of MHC isoforms
in rat extensor digitorum longus muscle
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Table 4.
Effects of CB, HU, and HU-CB on percentage distribution of MHC isoforms
in rat gastrocnemius muscle (red portion)
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Effects on MLCs.
Similar to the effects on the MHC complement, the changes in MLCs
reflected slow-to-fast transitions and were greater in the slow
compared with the fast muscles (Table 5).
In SOL, CB induced decreases in the slow isoforms of the alkali (MLC1s)
and regulatory (MLC2s) light chains with concomitant increases in the
relative concentrations of the corresponding fast isoforms, MLC1f/MLC3f and MLC2f. HU had a slightly different effect with a reduction in the
relative concentration in MLC1s and an increase in MLC1f and MLC3f, but
little change in the regulatory light chains. The changes in MLC
composition of SOL by HU-CB were restricted to a partial exchange of
MLC1s with MLC1f.
Effects of CB and HU on the light chain pattern of fast muscle were
only observed in the deep GAS (Table 6).
On the whole, they also consisted of slow-to-fast transitions. CB
treatment decreased MLC1s and increased MLC1f. As for the regulatory
light chain, this transition did not reach statistical significance. A
similar exchange was observed in the unweighted GAS where, in addition
to the elevation of MLC1f, an increase was also evident for MLC3f. GAS
muscle exposed to CB and HU was characterized by a partial exchange of
MLC1s with MLC1f and a pronounced increase in MLC3f.
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Table 6.
Effects of CB, HU, and HU-CB on percentage distribution of MLC
isoforms in rat gastrocnemius muscle (red portion)
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DISCUSSION |
Our results on the effects of CB with regard to muscle hypertrophy
and a tempering of HU-induced muscle atrophy are in agreement with
similar data in the literature (1). We also confirm that differences exist between the adaptive responses of fast and slow muscles following unweighting and CB treatment. In addition, our results show different responses of the two fast-twitch muscles under
study. According to the present investigation, CB induces a greater
hypertrophic effect in GAS than in EDL. Moreover, although both muscles
respond to unweighting with similar losses in mass (~30%), CB
treatment counteracts the HU-induced atrophy more efficiently in EDL
than in GAS. This difference may be related to the higher content of
type I fibers in GAS than in EDL (see differences in MHC isoform
composition in Tables 3 and 4). According to the literature (7,
15) and the present results, CB appears to have a greater
hypertrophic effect on type II fibers than on type I fibers. It is not
unexpected, therefore, that CB counteracts the HU-induced atrophy more
efficiently in the EDL compared with the GAS.
As judged from the MHC analyses, CB elicits exchanges of slow with
faster isoforms in both slow and fast muscles. These findings add to
our understanding of muscle plasticity. In SOL muscle, the slow-to-fast
transition in MHC isoforms occurs mainly in the direction of MHCI
to MHCIIa, with the induction of small amounts of MHCIId and MHCIIb. In
the fast GAS muscle, the changes in MHC isoforms may be described as
"fast-to-faster" transitions, consisting mainly of a decrease in
MHCIIa accompanied by an increase in MHCIIb. The relative concentration
of MHCIId was unaltered under these conditions. This could point to
a direct transition from MHCIIa to MHCIIb, but might also result from a
two-step transition, i.e., MHCIIa
MHCIId
MHCIIb, with
MHCIId as an intermediate between MHCIIa and MHCIIb. In
this case, the relative concentration of MHCIId would appear
unaltered. A direct MHCIIa-to-MHCIIb transition would result in
hybrid fibers displaying coexistence of MHCIIa with MHCIIb without
MHCIId. Although no single fiber studies were performed in the present
study, we favor the two-step transition model and based our assumption
on single fiber analyses performed on unweighted, slow-to-fast
transforming rat SOL muscle. In these muscles, fibers with coexisting
MHCIIa and MHCIIb were not detected, but fibers with the following MHC
combinations could be delineated: MHCI + MHCIIa, MHCI + MHCIIa + MHCIId, as well as MHCI + MHCIIa + MHCIId + MHCIIb (28).
The changes in MHC isoforms in unweighted muscles are qualitatively
similar and in the same direction as those elicited by CB. However,
HU-induced slow-to-fast transitions appear to be more extensive than
those induced by CB treatment alone. Thus HU causes transitions that
extend to MHCIId and also to MHCIIb. The combination of HU and CB
further enhances the slow-to-fast transition with even higher increases
in MHCIId and MHCIIb compared with HU alone.
Interestingly, SOL muscle expresses small amounts of MHCIa, an
additional slow isoform (10), under the conditions of HU and HU-CB. We assume that MHCI
, another slow isoform, is also elevated under the conditions of HU and of HU-CB, because mRNA and immunohistochemical studies have recently demonstrated its upregulation in unweighted rat SOL muscle (30). Because of
the comigration of MHCI
and MHCI, electrophoretic separation of
these two isoforms is difficult. As such, elevations in MHCI
may
therefore be hidden within the bulky MHCI band.
The changes in the MHC isoform pattern of unweighted GAS muscle also
appear to fit this general scheme of slow-to-fast transitions. According to the predominantly fast phenotype of this muscle, slow-to-fast transitions are, for the most part, confined to the fast
fiber types and consist mainly of IIA
IID
IIB (i.e., fast-to-faster transitions). In fact, the MHC isoform pattern of GAS
exposed to HU displays increases in the relative concentration of
MHCIIb, and similar changes occur under the influence of CB. The
similar effects induced by CB and HU in the MHC isoform pattern of GAS
muscle suggest that these changes represent maximally attainable responses under these conditions. It is not unexpected, therefore, that
the combined actions of HU and CB do not lead to additional fast-to-faster transitions, i.e., greater amounts of MHCIId and MHCIIb.
In contrast to reports in the literature (9, 14, 24), we
noted significant changes in MLC expression under the conditions of HU,
CB, and HU-CB. In general, these alterations amounted to partial
exchanges of the slow MLC isoforms with their fast counterparts. These
slow-to-fast transitions appear to be greater for essential (alkali)
light chains compared with regulatory light chains. Disproportionate slow-to-fast transitions of essential and regulatory light chains undoubtedly lead to the appearance of hybrid myosins (e.g., both fast
and slow MLC isoforms in combination with fast MHC isoforms) (2,
26, 27). Such hybrid fibers have been previously observed in
muscles undergoing fast-to-slow transitions (18). Higher apparent affinities of the fast MLC3f for MHCIId and MHCIIb instead of
MHCIIa (32) may explain why increases in MLC3f are
observed in the present study under conditions that lead to significant increases in MHCIId and MHCIIb.
In summary, SOL muscle is capable of changing its phenotype from slow
to fast. HU, CB treatment, and the combination of both (HU-CB) all
cause the upregulation of the fast MHCIIa and, in addition, the
induction of considerable amounts of the faster MHCIId and fastest
MHCIIb isoforms. These data lend support to the concept of muscle
plasticity spanning from one end to the other along the spectrum of
fiber types. According to the previously established time courses of
induction and increases in fast MHC isoforms in unweighted SOL muscle
(30), it seems that the changes observed in the present
study could occur as progressive slow-to-fast transitions in the order
of MHCI
MHCIIa
MHCIId
MHCIIb. The changes in MHC isoform
expression observed under the same conditions in the GAS muscle might
be interpreted as fast-to-faster transitions, probably in the order of
MHCIIa
MHCIId
MHCIIb. These changes in MHC composition are
accompanied in both muscles by similar transitions in MLC expression.
Together, these slow-to-fast changes occur in the same order
established in independent studies on MHC-based fiber types for
contractile properties, myosin ATPase activity, tension cost, and ATP
phosphorylation potential (3, 4, 6, 12).
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ACKNOWLEDGEMENTS |
This study was supported by Association Française contre les
Myopathies Grant 7109, Fonds Européen de Développement
Régional Grant F007, and Deutsche Forschungsgemeinschaft Grant Pe
62/25-3.
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FOOTNOTES |
Addresses for reprint requests and other correspondence: L. Stevens, Laboratoire de Plasticité Neuromusculaire,
Université des Sciences et Technologies de Lille, F-59655
Villeneuve d' Ascq, France (E-mail: laurence.stevens{at}univ-lille1.fr);
and D. Pette, Fachbereich Biologie, Universität Konstanz, D-78547
Konstanz, Germany (E-mail: dirk.pette{at}uni-konstanz.de).
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.
Received 2 February 2000; accepted in final form 13 June 2000.
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