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J Appl Physiol 86: 881-886, 1999;
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Vol. 86, Issue 3, 881-886, March 1999

Age-related changes in contractile properties of single skeletal fibers from the soleus muscle

LaDora V. Thompson1 and Marybeth Brown2

1 Program in Physical Therapy, Department of Physical Medicine and Rehabilitation, School of Medicine, University of Minnesota, Minneapolis, Minnesota 55455; and 2 Program of Physical Therapy, Washington University School of Medicine, St. Louis, Missouri 63108


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES

Peak absolute force, specific tension (peak absolute force per cross-sectional area), cross-sectional area, maximal unloaded shortening velocity (Vo; determined by the slack test), and myosin heavy chain (MHC) isoform compositions were determined in 124 single skeletal fibers from the soleus muscle of 12-, 24-, 30-, 36-, and 37-mo-old Fischer 344 Brown Norway F1 Hybrid rats. All fibers expressed the type I MHC isoform. The mean Vo remained unchanged from 12 to 24 mo but did decrease significantly from the 24- to 30-mo time period (from 1.71 ± 0.13 to 0.85 ± 0.09 fiber lengths/s). Fiber cross-sectional area remained constant until 36 mo of age, at which time there was a 20% decrease from the values at 12 mo of age (from 5,558 ± 232 to 4,339 ± 280 µm2). A significant decrease in peak absolute force of single fibers occurred between 12 and 24 mo of age (from 51 ± 2 × 10-5 to 35 ± 2 × 10-5 N) and then remained constant until 36 mo, when another 43% decrease occurred. Like peak absolute force, the specific tension decreased significantly between 12 and 24 mo by 20%, and another 32% decline was observed at 37 mo. Thus, by 24 mo, there was a dissociation between the loss of fiber cross-sectional area and force. The results suggest time-specific changes of the contractile properties with aging that are independent of each other. Underlying mechanisms responsible for the time-dependent and contractile property-specific changes are unknown. Age-related changes in the molecular dynamics of myosin may be the underlying mechanism for altered force production. The presence of more than one beta /slow MHC isoform may be the mechanism for the altered Vo with age.

peak absolute force; maximal unloaded shortening velocity; specific tension; myosin heavy chain; fiber diameter


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES

AGING IS ASSOCIATED with a progressive loss of motor function, a slowing of muscle movements, and a decline in muscle strength (6, 16, 28). These age-related changes in the skeletal muscle system are considered to be factors contributing to falls in the elderly, which in return result in a loss of independence (11).

There are inconsistent results among age-related changes in the force-generating capacity of individual skeletal muscle fibers and single skeletal muscle fiber maximal unloaded shortening velocity (Vo) (16, 28). For example, the force-generating capacity has been reported to change and not change, and Vo has been reported to increase, decrease, or not change with age (5, 9, 12, 17, 19). The reasons for these inconsistencies are not known. The inconsistencies may in part be explained by differences between species with various life spans, specific muscles evaluated, and methodological limitations of the various experimental approaches used in the previous studies. The varied reports in the age-induced alterations of contractile properties may be related to an asynchronous temporal pattern of change of the contractile properties over the life span of the animal and a difference in the extent of change.

Recently, the National Institute on Aging has identified the Fischer 344 Brown Norway F1 Hybrid as a rodent model for age-related studies of skeletal muscle function because this strain ages with minimal disease (20, 30). Thus research studies using this strain may yield more consistent age-related changes in muscle function. The single permeabilized (skinned)-fiber preparation allows for quantification of actomyosin cross-bridge interactions in an intact myofilament lattice under controlled levels of calcium activation. This preparation may provide insight into age-related changes in contractile properties.

To better address some of the inconsistencies observed in previous studies of aging in skeletal muscle, an in-depth examination of one muscle at multiple ages has been undertaken. Specifically, the present study was undertaken to determine the effects of aging on the cross-sectional area, force-generating capacity characteristics, and Vo of single permeabilized fibers. The study reports only the type I myosin heavy chain (MHC) fibers with myosin light chains [MLC slow 1s (MLC1s) and MLC slow 2s (MLC2s)] from the soleus. Five age groups of the Fischer 344 Brown Norway F1 Hybrid rat were chosen to represent the adult life span and to evaluate contractile function characteristics over the life span. Because force production is related to the amount of contractile protein present, we hypothesized that the extent of change (percent decline) in single-fiber cross-sectional area would be associated with a comparable decrease in the force production of the single cells. Last, because whole-muscle movements are slower with age, we hypothesized that the Vo of individual cells would be slower with age.


    MATERIALS AND METHODS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES

Animals. Twenty specific-pathogen-free male Fischer 344 Brown Norway F1 Hybrid rats were purchased from the aging colony maintained by the National Institutes on Aging. The ages selected are from mature rats (12 mo) and represent multiple time points during the aging spectrum. Because 31 mo of age represents 50% mortality for the Fischer 344 Brown Norway F1 Hybrid rats, the 12- and 24-mo-old ages represent young adult and adult animals, respectively. The 30-mo-old age represents the older adult animal. The 36- and 37-mo-old ages were selected because the functional mobility of the ages declines at this age (unpublished observations). There were three to five animals per age group. The animals were housed in pathogen-free environment with food and water given ad libitum. The animals were observed for 3-4 wk to make sure body weights were stable. The animal care protocol was approved by the Institutional Animal Care and Use Committee.

Single-fiber preparation and solutions. The permeabilized (skinned) fiber preparation was used to ensure that any differences detected in the force-generating capacity and in the Vo values were due to differences in the contractile proteins and not in metabolic or ionic conditions within the fibers. The skinned fibers were prepared by using a procedure similar to that described earlier (1, 23, 29). Bundles of fibers were dissected from the soleus muscles of pentobarbital sodium-anesthetized 12-, 24-, 30-, 36-, and 37-mo-old male rats. The bundles were placed in a glycerinating solution at -20°C containing 126 mM K-propionate, 2 mM EGTA, 4 mM ATP, 1 mM MgCl2, 20 mM imidazole (pH 7.0), and 50% glycerol (vol/vol).

Single-fiber segments were teased from the bundles, and the fiber segments were mounted between the output shaft of a force transducer (sensitivity 2 mV/mg; model 400A, Cambridge Technology) and the lever arm of a servo-controlled galvanometer (model 300H, Cambridge Technology); the fibers were attached by using tweezers. The fiber segments were submerged in a relaxing solution (pH 7.0) containing the following (in mM): 7.0 mM EGTA, 5.4 mM MgCl2, 20 imidazole (pH 7.0), 14.5 mM creatine phosphate, and 4.7 mM ATP, as well as CaCl2 to achieve pCa (-log[Ca2+]) 9.0, where [Ca2+] is calcium concentration. The relaxing solution contained enough KCl to achieve an ionic strength of 180 mM. For activation (maximum force development), sufficient calcium was added to bring the pCa to 4.5 in the activating solution. The activating solution (pH 7.0) contained the following (in mM): 7.0 EGTA, 5.4 MgCl2, 20 imidazole (pH 7.0), 14.5 creatine phosphate, 4.7 ATP; CaCl2 to achieve pCa (-log[Ca]) 4.5; and enough KCl to achieve an ionic strength of 180 mM.

Determination of contractile properties. The permeabilized fiber preparation was mounted on the stage of an inverted microscope (Nikon) equipped with ×600 magnification and a calibrated eyepiece micrometer. This magnification allowed for resolution of individual sarcomeres (2.5 µm). With use of the calibrated eyepiece micrometer, the distance between the force transducer and the servo-controlled galvanometer was adjusted such that the single-fiber sarcomere length was 2.5 µm (1, 23, 29).

Mechanical experiments were performed at 15°C. This temperature allowed for accurate determination of maximal velocity of shortening (1, 23, 29). Fiber cross-sectional areas were estimated by rotating the fiber under the microscope and measuring the diameter at three places along the fiber. The cross-sectional area was then determined by assuming the fiber possessed a circular fiber geometry (1, 23, 29).

As a determination of the maximal velocity of shortening, the Vo was estimated by using the slack test (1, 23, 29). This procedure consisted of imposing slack releases of varying lengths (5, 7.5, 10, and 12.5% total fiber length) and measuring the time interval beginning with the force falling to zero and ending with the onset of force redevelopment. For each release, the magnitude of the release was then plotted vs. the time elapsed before the redevelopment of tension. The Vo was derived from the slope of the resulting linear relationship. All fiber data used were fit with the least squares method, and the resulting Pearson's R values were in all cases >0.98.

MHC and MLC determination for fiber typing. The use of the same fiber for mechanical experiments and subsequent MHC and MLC analyses was a key element in this work permitting an unambiguous analysis of the correlation between contractile properties and myosin type of a fiber. After mechanical measurements, the fiber was removed from the experimental chamber and solubilized in 10 µl of 1% SDS sample buffer containing 6 mg/ml EDTA, 0.06 M Tris, 1% SDS, 2 mg/ml bromphenol blue, 15% glycerol, and 5% beta -mercaptoethanol. Approximately 0.5 nl of fiber volume was electrophoresed on gels consisting of 3% (wt/vol) acrylamide stacking gel and a 5% separating gel for MHC analysis. To determine MLC expression, 1 nl of fiber volume was loaded on a gel consisting of a 3.5% acrylamide stacking gel and a 12% acrylamide separating gel. To evaluate the MHC (type I) and MLC (MLC1s and MLC2s), each gel had three lanes of purified standards. The gel was silver-stained, and subsequently the protein mobility of each individual fiber was compared with the protein mobility of the standards (23). The standards for MHC type I, type IIa, and type IIb and for MLC (MLC1s and MLC2s) were prepared by myosin purification techniques (23, 24, 26).

The fibers were typed according to the results of the gel analyses and matched with the mechanical data. Only those fibers were used that gave acceptable mechanical results (isometric force maintained within 5%; Vo maintained within 10%; mean sarcomere length maintained within 5%) and yielded an unambiguous gel pattern. Of the 134 fibers evaluated, 125 fibers met the aforementioned criteria and were composed of MHC type I and MLC (MLC1s and MLC2s). The study reports five to nine fibers per animal. In the final analyses, 31 fibers were investigated from the 12-mo-old animals, 27 fibers from the 24-mo-old animals, 20 fibers from the 30-mo-old animals, 19 fibers from the 36-mo-old animals, and 27 fibers from the 37-mo-old animals. There were individual fibers coexpressing MHC type IIa isoform and MHC type I isoform, but the findings are not reported in this study.

Statistical analysis. Means ± SE were calculated from individual data values by descriptive statistics. The ANOVA was used for comparisons between the means by contractile property of the different age groups. Differences were judged significant at P <=  0.05 with the Tukey post hoc analysis.


    RESULTS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES

Table 1 shows the body weights, soleus muscle wet weights, and soleus muscle wet weight-to-body weight ratio (relative soleus weight). With age there was a 32% increase in body weight with animals between the ages of 12 and 30 mo. The soleus muscle wet weight did not change between 12 and 30 mo of age; however, a significant difference of 26% was observed after 30 mo of age. The relative soleus wet weight declined 33% from 12 to 37 mo of age.

                              
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  		Table 1.   Animal characteristics

Contractile property data values of single permeabilized soleus fibers classified according to type I MHC isoform composition and MLC1s and MLC2s isoforms from 12- to 37-mo-old animals are shown in Table 2. Significant changes in specific tension (Po) were already present at 24 mo, whereas a significant decline in Vo was not observed until 30 mo.

                              
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  		Table 2.   Single MHC type I fiber contractile properties from the soleus

Single-fiber cross-sectional area did not differ significantly among 12-, 24-, and 30-mo-old animals. Fiber cross-sectional area remained constant until 36 mo of age, at which time there was a 20% difference from 12 mo of age (Table 2).

A significant change in peak absolute force of single fibers occurred earlier in the life span than did the change in cross-sectional area (Table 2). Between the 12- and 24-mo periods, there was a 31% decrease in single-fiber peak absolute force. The force did not remain constant until the 36-mo period according to Table 2. This decline in single-fiber force represented a 50% difference from the 12- and 36-mo-old animals.

Like the peak absolute force, the Po changed significantly between 12 and 24 mo of age by 20%. This force then remained constant until 36 mo, when another 32% decline was observed (Table 2).

The mean Vo did not change significantly from the 12- to 24-mo periods, but it did change by 50% between 24 and 30 mo of age. Figure 1 shows the frequency distributions for the single permeabilized fiber Vo values from the present study. The frequency distribution reveals that 22-26% of the fibers investigated from 12- or 24-mo-old animals had Vo values below 1.0 fiber lengths (fl)/s. This same percentage of fibers had Vo values above 2.1 fl/s. In contrast, 47% of the single-fiber Vo values from 30- or 36-mo-old animals were below 1.0 fl/s. Interestingly, there were not any fibers with Vo values above 2.1 fl/s. In 37-mo-old animals, 15% of the fibers investigated had Vo values above 2.1 fl/s and 67% of the fibers Vo had values below 1.0 fl/s.


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  		Fig. 1.   Distributions of maximal unloaded shortening velocity values from soleus skeletal muscle fibers of 12- (A), 24- (B), 30- (C), 36- (D), and 37-mo-old (E) Fischer 344 Brown Norway F1 Hybrid rats. Fibers were classified according to myosin heavy chain isoforms as myosin heavy chain type I. fl, Fiber lengths.


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES

In the present study, cross-sectional area, peak absolute force, Po, and Vo were evaluated in single permeabilized soleus fibers, a preparation that allows quantification of actomyosin cross-bridge interactions in an intact myofilament lattice under controlled levels of calcium activation. Subsequent electrophoresis of each fiber relates these contractile properties to MHC and MLC isoform expression. One major observation in this study was the age-related decline in the contractile properties in single soleus type I MHC fibers with MLC (MLC1s and MLC2s), but the extent of change and the temporal pattern of change varied between the contractile properties.

Previous studies have investigated age-related changes in Vo of whole-limb slow-twitch muscles and have reported that Vo is slightly diminished or unaltered (5, 12, 19, 25, 26). However, Vo evaluated at the whole-muscle level may be influenced by the connective tissue or protein heterogeneity between cells of multicellular preparations (8, 21). At the whole-muscle level, a muscle is composed of slow-twitch and fast-twitch fibers. The slow-twitch fibers have slow myosin isoforms with slower cycling cross-bridges than do fast-twitch fibers with fast myosin isoforms (24, 27). Thus the slow-twitch fibers may act as an internal drag on the fast-twitch fibers, resulting in a slower whole-muscle Vo (7). It has been hypothesized that with age there is fiber-type transformation (fast to slow), thus providing a mechanism for altered Vo at the whole-muscle level with age (28).

Another possibility for the slowing of whole-muscle Vo with age may be related to changes in connective tissue (29). The reported increase in connective tissue with age would also provide an increase in the internal drag to all the fiber types within the muscle (29). Subsequently, the whole-muscle Vo would be slower.

At the single-cell level the influence of hetereogeneity of fiber types and the increase in connective tissue can be minimized. The present study reports the slowing of Vo with age in an experimental preparation where connective tissue is not a factor and the single fiber has homogeneous myosin isoforms. The findings characterize a specific temporal pattern of change and a specific extent of change of Vo over the life span of the animal. For example, the Vo is maintained until 24 mo of age in the Fischer 344 Brown Norway F1 Hybrid and then significantly declines by 50% by 30 mo of age. Thirty-one months of age of this rat strain represents 50% mortality (20).

Single-fiber Vo is thought to reflect the maximum speed of actin and myosin interaction and correlates with the myofibrillar ATPase activity or MHC isoform (3). All the single fibers in the present study were homogenous concerning their MHC isoform compositions (type I MHC isoform). Thus the age-related slowing of Vo observed in the single fibers of this study may be related to differences in MHC type I subtypes that have yet to be characterized. Recently, it has been hypothesized that additional MHC type I isoforms may exist in single skeletal muscle fibers previously considered to be homogeneous with regard to their MHC isoform composition (10, 14, 24). This hypothesis has been suggested because there are large variations in Vo within groups of fibers presumed homogenous in MHC content (4, 27). There appeared to be large variations in Vo of the single fibers from 12-, 24-, and 37-mo-old animals. For example, in the present study, there was a population of type I MHC fibers in older animals with slower Vo than that observed in younger animals (<1.0 fl/s). As well, there was a population of type I MHC in the young animals with faster Vo values (>2.1 fl/s) than those observed in old age (12-mo-old animals compared with the 36-mo-old animals). The findings suggest the presence of an undetected MHC type I isoform that may comigrate with the detected MHC type I isoform. Thus aging may induce expression of an alternative slow MHC type I isoform. Such an alternative MHC type I isoform could be responsible for the decrease in Vo.

It is known that a change in the relationship between myofilament geometry may also contribute to the change in Vo (22). In the present study, the force-generating capacity of the individual cells decreases between the period of 12 and 24 mo, indicating alterations in the contractile proteins. These alterations in the contractile proteins may contribute to a change in the myofilament geometry that subsequently results in altered maximal shortening velocity (13, 18, 27).

There are mixed reports about the effects of aging on Po, with some investigators reporting a decrease, no change, and an increase (5, 9, 12, 15). Studies of permeabilized slow-twitch fibers have not always revealed any decline in Po (9, 19). Eddinger et al. (9) reported an increase in Po in single permeabilized fibers from soleus muscles of 30-mo-old rats, but this study reports a small number of single fibers from the soleus (n = 7) on which Po was measured. Li and Larsson report a small difference in Po in type I MHC fibers between young and old animals, whereas in single human skeletal muscle cells with MHC type I they report a decline (17, 19). Our data show a significant difference in the Po values of single permeabilized fibers with age and that the inconsistencies in the reported literature may be related to the time course of change in Po. Thus the age of the animal along the total life span of the animal may play an important role when Po is evaluated.

This study and the other two studies cited above (9, 19) evaluated Po with the permeabilized fiber preparation. It is known that the permeabilized fiber preparation swells in the skinning solution. The previous studies and this study have not corrected for fiber swelling and thus have made the assumption that all fibers swell to the same extent no matter the age of the animal tissue. It is possible that the extent of swelling is not homogenous over the age groups from which the tissues are taken. Variable swelling may compound the interpretation of Po measurements in the permeabilized fibers. We believe that the decline in Po is not the result of experimental artifact (swelling) because of the extent of change observed in absolute force. The absolute force (N) significantly declined between 12 and 36 mo of age (50%).

We hypothesized that a decline in single-fiber force-generating capacity would be associated with a decline in single-fiber cross-sectional area. This study reports a greater decline in the force-generating capacity of single cells (50%) compared with the decline in single-fiber cross-sectional area (30%). These results suggest that the underlying mechanism for the decline in the force-generating capacity may in part be related to a loss of contractile material. However, the loss of contractile material does not explain the total decline in the force-generating capacity. In very old rats, there have been reports of ultrastructural evidence of myofibrillar loss and an increase in intermyofibrillar spaces (2). These morphological changes can potentially alter the density packing of the actin and myosin or the number of cross bridges in the strong-binding force-generating step of the cross-bridge cycle. These alterations would influence the force-generating capacity of skeletal muscle cells and need to be investigated to identify other mechanisms responsible for the decline in force.

Fiber cross-sectional area remained relatively constant throughout the aging process until 36 mo, at which time a significant decrease in fiber cross-sectional area occurred. We hypothesized that the loss in whole-muscle mass would be associated with a decrease in single-fiber cross-sectional area. Our results are consistent with this hypothesis and indicate that the fiber cross-sectional area plays a role in whole-muscle mass atrophy (28).

In conclusion, the present study determined the contractile properties of single MHC type I fibers from the soleus muscle in 12-, 24-, 30-, 36-, and 37-mo-old Fischer 344 Brown Norway F1 Hybrid rats. The results showed that Vo decreased between the 24- and 30-mo age period, whereas single-fiber cross-sectional area decreased at 37 mo of age. The force-generating capacity of the individual cells decreased between 12 and 24 mo of age and then again at 37 mo. The results from investigating the five different time points during the life span of the Fischer 344 Brown Norway F1 Hybrid rat suggest time-specific changes of the contractile properties that are independent of each other. Underlying mechanisms responsible for the time-dependent and contractile property-specific changes are unknown.


    ACKNOWLEDGEMENTS

We are grateful to Janice Shoeman, Susan Toyli, and Scott Johnson for technical assistance.


    FOOTNOTES

This work was supported by a grant from the American Heart Association, Minnesota Affiliate, to L. Thompson and by National Institute on Aging Grant AG-600585 to M. Brown.

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. §1734 solely to indicate this fact.

Address for reprint requests: L. V. Thompson, Program in Physical Therapy, Dept. of Physical Medicine and Rehabilitation, School of Medicine, Univ. of Minnesota, UMHC Box 388, Minneapolis, MN 55455 (E-mail: thomp067{at}tc.umn.edu).

Received 20 April 1998; accepted in final form 28 October 1998.


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ABSTRACT
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DISCUSSION
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