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Department of Physiological Science and Brain Research Institute, University of California, Los Angeles, California 90095-1761
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Roy, Roland R., Robert J. Talmadge, Kenneth Fox, Michael
Lee, Aki Ishihara, and V. Reggie Edgerton. Modulation of MHC isoforms in functionally overloaded and exercised rat plantaris fibers.
J. Appl. Physiol. 83(1): 280-290, 1997.
The effects of 1 and 10 wk of functional overload (FO) of the
rat plantaris with (FOTr) and
without daily endurance treadmill training on its myosin heavy chain
(MHC) composition were studied. After 1 and 10 wk of FO, plantaris mass
was 22 and 56% greater in FO and 37 and 94% greater, respectively, in
FOTr rats compared with
age-matched controls. At 1 wk, pure type I and pure type IIa MHC fibers
were hypertrophied in FO (39 and 44%) and
FOTr (70 and 87%) rats. By 10 wk
all fiber types comprising >5% of the fibers sampled showed a
hypertrophic response in both FO groups. One week of FO increased the
percentage of hybrid (containing both type I and type IIa MHC) fibers
and of fibers containing embryonic MHC. By 10 wk, the percentage of
pure type I MHC fibers was ~40% in both FO groups compared with 15%
in controls, and the percentage of fibers containing embryonic MHC was
similar to that in controls. Sodium dodecyl sulfate-polyacrylamide gel
electrophoresis analyses showed an increase in type I MHC and a
decrease in type IIb MHC in both FO groups at 10 wk, whereas little
change was observed at 1 wk. These data are consistent with hypertrophy
and transformation from faster to slower MHC isoforms in chronically
overloaded muscles. The additional overload imposed by daily endurance
treadmill training employed in this study (1.6 km/day; 10% incline)
results in a larger hypertrophic response but appears to have a minimal
effect on the MHC adaptations.
immunohistochemistry; gel electrophoresis; hypertrophy; fiber type
conversion; fiber size
INTRODUCTION FUNCTIONAL OVERLOAD (FO) of the rat plantaris by
removal of its major synergists results in hypertrophy and a shift in
the contractile, biochemical, and metabolic properties toward those observed in a "slower" muscle (26). The extent of these
adaptations may be related, in part, to the activity level of the rats
after surgery. For example, it appears that the amount of hypertrophy is greater in rats that are exercised on a treadmill than in rats not
exercised after FO (13, 25), although this is somewhat controversial
(3). Thus one of the mechanisms regulating muscle hypertrophy may be
the amount and/or type of activity that the overloaded muscle
experiences after ablation of its synergists. This contention is
supported by the observation that in cats, a relatively sedentary
animal, FO of the plantaris has little effect on the mass of the muscle
unless the cat is exercised. In addition, the largest amount of
hypertrophy was found when the cats were subjected to high-intensity
exercise, i.e., sprinting and jumping (26, 29).
On the basis of gel electrophoresis analyses, FO of the rat plantaris
has been shown to result in increases in the percent composition of
type I, IIa, and IIx and a decrease in type IIb myosin heavy chains
(MHCs) (8, 10, 19, 23, 37, 38). The effects of exercise on the degree
of conversion from fast to slow fibers in FO muscles, however, are
equivocal. Riedy et al. (25) reported a similar percentage of slow and
fast fibers, on the basis of myofibrillar adenosinetriphosphatase
staining, after 13 wk of FO with and without treadmill training. In
contrast, the increase in the percent composition of slow native myosin in the plantaris of FO rats that were allowed spontaneous running exercise for 11 wk was equal to the sum of the increases observed with
exercise or FO alone (14). Thus it is not presently known whether the
shift toward slower biochemical properties in a muscle responding with
elevated neuromuscular activity (12, 29) to one functional stressor can
be enhanced by imposing a second functional stressor. In other words,
can MHC expression reflecting a fast-to-slow fiber type transition in
an FO muscle be further regulated by regular endurance exercise? In
addition, the effects of FO with and without training on the expression
of MHC isoforms in plantaris muscle fibers have not been determined.
The objectives of the present study, therefore, were threefold:
1) to define the complement of MHC
isoforms in the FO plantaris by using immunohistochemical and sodium
dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE)
procedures; 2) to compare the
adaptations in the MHC isoforms and fiber size at an early (1-wk) and a
later (10-wk) stage after FO; and 3)
to determine any effects of an additional overload imposed on the FO
muscles by treadmill training.
MATERIALS AND METHODS
20°C) microcentrifuge tubes and
stored at 70°C in preparation for myofibrillar protein
isolation. Because of differences in the fiber type distribution along
the rostral-caudal axis of the highly compartmentalized rat plantaris
(Roy and Edgerton, unpublished observations) and the reported
differences in the adaptations to FO along the proximal-distal axis of
a muscle (11), fibers from a deep region (close to the bone) in the
midportion of the muscle were consistently chosen for analysis and
comparison.
SDS-PAGE.
Isolated myofibrils were prepared from whole muscle cross sections
stored in microcentrifuge tubes according to Thomason et al. (36),
except that sample volumes were reduced to 0.25 ml to accommodate the
small sample size. The protein concentration of the final myofibrillar
suspension was determined according to Bradford (5). Myofibrillar
protein was then boiled in sample buffer (20) for 2 min at a final
protein concentration of 0.25 mg/ml. MHCs were separated by SDS-PAGE
according to Talmadge and Roy (34). The SDS-PAGE gels were stained with
Coomassie blue, photographed, and scanned with a digital imaging system
densitometer (IS-1000, Alpha Innotech) for the quantification of MHC
isoforms.
Immunohistochemistry.
Immunohistochemical analysis of MHC content in individual fibers was
performed on serial sections by using a series of monoclonal antibodies
(primary antibody) specific to rat MHC isoforms (see Table
1 for monoclonal antibody specificities).
The avidin-biotin immunohistochemical procedure was used for the
localization of primary antibody binding according to the instructions
for kits PK-6102 and AK-5010 (Vector Laboratories, Burlingame CA).
Phosphate-buffered saline was used as a buffer for all immunoglobulin
G-class primary antibodies, and
tris(hydroxymethyl)aminomethane-buffered saline as the buffer for all
immunoglobulin M-class primary antibodies. A sample of ~100 fibers
that were free from artifact and showed good staining for all
antibodies was selected for single-fiber MHC composition analysis from
the deep region of each muscle. Stained cross sections were
photographed on an Olympus BH-2 microscope with a Nikon camera
attachment. A fiber showing a reaction to a specific antibody was
considered to be expressing that specific MHC isoform.
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0.05 for all analyses.
RESULTS
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0.05;
§ significantly different from same group at 1 wk,
P 0.05.
0.05;
§ significantly different from same group at 1 wk,
P 0.05.
There were only subtle changes in the fiber type distribution in the 1-wk overloaded groups, and the adaptations were similar in the trained and untrained rats (Fig. 4). There was a decrease in the percentage of fibers containing only type IIa MHC in both FO groups compared with that in Con1 wk rats. It appears that these fibers also began to express type I MHC because the percentage of fibers containing both type I and IIa MHC increased from 1% in Con1 wk rats to 8 and 6% in the FO1 wk and FOTr-1 wk groups, respectively. Compared with the Con1 wk rats, the Con10 wk rats had a higher percentage of fibers containing only type IIx MHC and a lower percentage of fibers containing both type IIa and IIx MHCs (Fig. 4). The percentage of pure type I fibers was increased from 15% in Con10 wk rats to 40 and 42% in the FO10 wk and FOTr-10 wk rats, respectively. In addition, the percentage of pure type IIa and pure type IIx fibers was decreased in both FO groups. There also was a tendency for the percentage of type IIa+IIx fibers to be increased in both FO groups (P > 0.05). Both FO10 wk groups had a higher percentage of pure type I fibers than both FO1 wk groups (Fig. 4). There was a clear tendency for the FO10 wk rats to have a smaller percentage of fibers that contained some type IIb MHC than did the FO1 wk rats, i.e., 6 and 2% for the FO10 wk and FOTr-10 wk rats vs. 16 and 15% for the FO1 wk and FOTr-1 wk groups, respectively. A small percentage of fibers (2% or less) in the control groups contained some embryonic MHC (Fig. 5). This percentage rose to 37 and 39% in the FO1 wk and FOTr-1 wk groups but was only ~1% in both FO10 wk groups. Fiber Cross-Sectional Areas (CSAs). One week of FO resulted in a 39 and 44% increase in the CSA of pure type I MHC and pure IIa MHC fibers, respectively, compared with Con1 wk rats (Fig. 6). In the FOTr-1 wk rats, the CSAs of these fiber types were elevated by 70 and 87%. In addition, there was a 27% increase in the CSA of the type IIa+IIx MHC fibers in the trained compared with Con1 wk rats.
0.05; § significantly different from same group at 1 wk,
P 0.05; 
significantly
different from FO group at same time period,
P 0.05.
The mean CSAs of all fiber types comprising >5% of the fibers sampled in both FO10 wk groups were larger than in the Con10 wk rats. The percent increase in CSA was the highest in the pure type I MHC fibers, i.e., 159 and 220% increases in the FO10 wk and FOTr-10 wk groups, respectively. The mean CSAs of type I, IIa, and IIa+IIx MHC fibers (comprising >70% of the total population of fibers in both groups) were larger in FOTr-10wk rats than in FO10 wk rats. The CSA of the fibers containing embryonic MHC was similar across groups after 1 wk of FO (Fig. 7). At 10 wk, these fibers were significantly larger in the FOTr compared with the control or FO rats.
0.05; § significantly
different from same group at 1 wk, P 0.05; significantly different from FO group at same time
period, P 0.05.
SDS-PAGE analyses. Figure 8 shows the migration patterns of the four adult rat MHCs in SDS-PAGE gels of plantaris muscle myofibrils isolated from six individual animals representing the six treatment groups. Note that in the two control animals (lanes 1 and 4), the type IIx and IIb MHC isoforms are the most prominent. After 1 wk of FO [with or without training (lanes 2 and 3)], there is a small increase in the proportion of type I MHC. After 10 wk of FO [with or without training (lanes 5 and 6)], there is a large increase in the proportion of type I MHC, and type IIb MHC is the least prominent MHC isoform.
The plantaris muscle of the Con1 wk rats was composed of 5, 11, 46, and 38% type I, IIa, IIx, and IIb MHC, respectively (Fig. 9). The only significant difference from control in either the FO1 wk or FOTr-1 wk groups was a doubling of the percent composition of type I MHC in the FO1 wk group. The Con10 wk rats had a significantly lower percentage of type IIb MHC than the Con1 wk rats. Both the FO10 wk and FOTr-10 wk groups had a higher percentage of type I and a lower percentage of type IIb MHCs than either the Con10 wk rats or their comparable group at 1 wk after surgery. In addition, the FOTr-10 wk group had a higher percentage of type IIx MHC than did the FO10 wk group.
0.05; § significantly
different from same group at 1 wk, P 0.05; significantly different from FO group at same time
period, P 0.05.
DISCUSSION
The increases in plantaris muscle weight and fiber size are consistent with previous reports (see Ref. 26 for a review). At 1 wk, the largest increases in fiber size were observed in the pure type I and pure type IIa fibers, with the changes being somewhat greater in the trained compared with the untrained rats. These data suggest that the lower-threshold slow and fast motor units (fibers) were preferentially recruited during this initial period of overload, consistent with the size principle of motor unit recruitment (15). In addition, the rats walked more plantigrade than normal during the first few days after FO [called "waddling" by Gardiner et al. (12); Roy and Edgerton, unpublished observations], resulting in a longer "yield" phase per step and presumably higher muscle forces than normal (see Ref. 29 for kinetic measurements in cats after FO of the plantaris). Activation patterns (on the basis of intramuscular electromyographic recordings) of the rat plantaris after FO also indicate higher but not maximal recruitment levels after compared with before FO (12). The greater effect on fiber CSA in the trained rats suggests that the daily training regime resulted in the recruitment of additional motor units (fibers) and had an additional effect on the overload imposed on the muscle fibers. These data also show that by 1 wk after FO the size of the fibers had increased, as shown previously (16), indicating that the hypertrophy process had begun and that the increase in muscle weight was not only a reflection of an early inflammatory response and edema associated with surgical trauma (2).
Ten weeks of overload resulted in a significant increase in the size of all fiber types comprising at least 5% of the total population of fibers compared with either the aged-matched control or the comparable 1-wk group. In general, the percent increase in fiber sizes was equal to or larger than the percent increase in muscle mass, suggesting that functional hypertrophy, i.e., an increase in contractile elements, had occurred. This contention is consistent with the increases in the maximum tetanic tension of the rat plantaris reported after 9-12 wk of FO (17, 30). However, the increase in force production is not proportional to the increase in physiological CSA, and thus the specific tension of the plantaris is decreased (~10-15%) after periods of overload ranging from 30 to 240 days (17, 29). This decrease in specific tension could be reflecting a disproportionate increase in noncontractile elements and/or a decrease in the tension-generating capability of the contractile elements. Evidence for the involvement of both of these factors has been reported. Kandarian and White (16) have reported that decreases in connective tissue protein concentration and increases in interstitial space can explain, in part, the decreased specific tension in the early, but not the late (17), stages of FO. A lower specific tension in predominantly slow (soleus; ~15 N/cm2) compared with predominantly fast (plantaris and medial gatrocnemius; ~26 and 21 N/cm2, respectively) extensor muscles has been reported (27, 30). Because one of the primary adaptations in the long-term overloaded plantaris muscle is an increase in the percentage of slow fibers, this factor could explain, at least in part, the decrease in specific tension observed in the FO10 wk rats. After 10 wk of overload, the muscles and fibers in trained rats were significantly larger than in the untrained overloaded rats, clearly demonstrating that exercise enhanced the hypertrophic response of the overloaded plantaris. These data are consistent with the 70 and 99% increase in plantaris weight after overload and overload plus treadmill exercise, respectively, reported by Riedy et al. (25).
The adaptations in the MHC isoforms were consistent with the plantaris
becoming a slower muscle (see Ref. 26 for a review). The
results are consistent with the reported increases in the percentages
of 1) type I MHC (24, 32, 33);
2) type I MHC mRNA (7, 24, 33);
3) type I fibers (4, 7);
4) slow native isomyosins (14, 38);
and 5) slow myosin light chains (24,
38), as well as a decrease in the maximum rate of shortening (18, 21,
30) after overload of the rat plantaris. Comparisons of the adaptations
observed at the fiber level in the deep region of the muscle after 1 and 10 wk of overload demonstrate the progressive nature of these
changes. For example, after 1 wk of overload the plantaris showed an
increase in the percentage of hybrid fibers, i.e., fibers that
contained both type I and some fast MHC isoform (usually type IIa) but
showed no change in pure type I fibers. By 10 wk after overload, the
percentage of pure type I fibers was almost threefold higher in both
overloaded groups compared with control. Combined with the decrease in
pure type IIa and IIx MHC fibers, these data strongly suggest that
there is a shift in MHC isoforms from type IIx to IIa to I MHC in the
deep region of the muscle after overload. Combined with the overall
decrease in type IIb MHC as reflected by gel electrophoresis of the
entire cross section of the muscle (Fig. 9), these data suggest a shift from type IIb to IIx to IIa to I MHC after 10 wk of FO. The progressive nature of these adaptations has also been observed by Crerar et al.
(7), who reported minimal changes in the percentage of slow fibers,
slow myosin protein, and 
-MHC mRNA after 7 days of FO of the rat
plantaris, whereas these values were at least twofold higher than
control after ~4 wk of FO. Although these data are suggestive of a
progression from type IIb to IIx to IIa to I MHC after FO, the
possibility still exists that some fibers did not express each of the
intermediate MHC types during the adaptation process.
The similarity in the fiber type percentage between exercised and nonexercised overloaded groups at either of the two time points indicates that the endurance training program used had little effect on the phenotypic properties of the fibers in the deep region of the overloaded plantaris. Similarly, gel analyses of the entire muscle cross section showed minimal differences in the percent MHC composition between trained and untrained overloaded muscles at either time point (Fig. 9), further substantiating that the endurance training program had a minimal effect on MHC composition of overloaded muscles. These data are consistent with the observation of no difference in the percentage of slow fibers in the plantaris after 13 wk of FO or FO plus treadmill training (25). These data, however, are in contrast to the reported additive effect of FO and voluntary exercise on the shift of the native isomyosin profile from fast to slow in the rat plantaris after 11 wk of overload of the plantaris and soleus (14). In the study of Gregory et al. (14), the rats were housed in cages having voluntary wheels, and the rats ran a minimum of 8 km/day, 7 days/wk. Thus in one 7-day period, the rats in the present study ran ~11.2 km (1.6 km/day × 7 days), whereas the rats in the Gregory et al. (14) study ran a minimum of ~56 km (8 km/day × 7 days). The differences in the MHC responses in the two studies could, therefore, be related to the total volume of exercise experienced by the FO rats.
In general, the gel analyses of whole muscle cross sections reflected adaptations in a direction similar to, although to a lesser magnitude, those observed for the immunohistochemical analyses of a sample of fibers from the deep region of the muscle. These apparent discrepancies between the gel and immunohistochemical analyses could reflect several factors. For example, although a fiber may contain multiple MHC isoforms as demonstrated immunohistochemically, the amount of newly expressed MHCs in hybrid fibers may be very small. In addition, the superficial region of the plantaris, a large proportion of the total cross section of the muscle, is composed predominantly of fast fibers that may have adapted somewhat differently to the overload stimulus. In any case, the gel analyses suggest that a shift from faster to slower MHC isoforms occurred in the superficial as well as the deep region of the muscle. In addition, a conversion from fast to slow fibers has been observed previously in both the deep (from 16 to 48%) and the superficial (from 3 to 19%) regions of the plantaris after 9-12 wk of overload (4). The changes in the percentage of total MHC observed in the present study after 10 wk of FO are consistent with the results of Fauteck and Kandarian (10) after 5 wk of FO. They found the following shifts from control to FO: 11 to 16% for type I, 14 to 24% for type IIa, 36 to 42% for type IIx, and 39 to 18% for type IIb.
The appearance of the embryonic MHC isoform in a high proportion of plantaris fibers sampled in both overloaded groups after only 1 wk of overload (~40% compared with ~2% in either control group) could reflect the reexpression of this developmental isoform in existing mature fibers or the presence of "new" fibers. On the basis of the similarity in the sizes of the fibers containing embryonic MHC and those fibers of the same type but not having this developmental MHC, the data suggest that the former possibility is more likely. Furthermore, relatively few fibers (~1%) contained embryonic MHC after 10 wk of overload, suggesting that the expression of this MHC is transient and may be related to the initial muscle fiber damage (probably due to the high forces associated with a prolonged and increased yield phase during each step) and inflammation associated with the sudden increase in the loading properties of the muscle after surgery (2). A second and more likely interpretation for the time course of the adaptations in the embryonic MHC composition is that the compensatory hypertrophy after overload is associated with an increase in the number of myonuclei to maintain a relatively constant nuclear domain (cytoplasmic volume per myonucleus). This process would involve satellite cell activation (1), cells that initially express embryonic MHC after fusion with either existing fibers or other satellite cells (9). After 10 wk of overload when the hypertrophic response has plateaued, these cells would most likely have switched to adult MHC isoform expression. The low percentage of fibers containing embryonic MHC at 10 wk after FO is consistent with the small amounts of embryonic and neonatal MHC mRNAs observed after 4 or 11 wk of overload of the plantaris (24). The contention that there were no new fibers in the FO muscles is consistent with the report of similar total fiber counts after FO with or without endurance treadmill training for 4-40 wk for FO and control plantaris muscles (13).
Perspective. FO is an excellent model for studying the effects of increased activation and loading on the plasticity of skeletal muscle (see Ref. 26 for a review). The adaptations in fiber size, MHC type, and metabolic properties all strongly indicate that a muscle becomes larger and slower after FO. These adaptations have been shown to occur in a variety of muscles (e.g., Ref. 27) and in laboratory animal models other than the rat, e.g., the cat (6, 29, 35) and mouse (28). Because of the rapid time course of these adaptations, FO appears to be an appropriate model for studying the interrelationships among fiber size, metabolic potential, and myonuclear number in hypertrophying and transforming skeletal muscle fibers. Initial results in the cat (1) and preliminary results in the rat (22) indicate that the number of myonuclei (presumably from satellite cell activation and incorporation) increases either in proportion to or at a faster rate than the increase in fiber volume after FO. Thus the increased genetic machinery provided by the additional myonuclei may be one mechanism for increasing muscle protein synthesis during hypertrophy and/or fiber transformation. That treadmill training in FO rats resulted in an enhancement of the muscle hypertrophy but no additional conversion toward slower MHCs suggests that there may be a limit to the modulation of specific protein systems in an overloaded muscle.ACKNOWLEDGEMENTS
This study was supported in part by National Institute of Neurological Disorders and Stroke Grant NS-16333.
FOOTNOTES
Address for reprint requests: R. R. Roy, Brain Research Institute, UCLA School of Medicine, Center for the Health Sciences, 10833 Le Conte Ave., Los Angeles, CA 90095-1761 (E-mail: rroy{at}physci.ucla.edu).
Received 17 July 1996; accepted in final form 13 March 1997.
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