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J Physiol (2003), 552.1, pp. 47-58
© Copyright 2003 The Physiological Society
DOI: 10.1113/jphysiol.2003.044966
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ABSTRACT |
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The purpose of this study was to determine whether there was an age-related decline in the isometric and isotonic contractile function of permeabilized slow (MHC I) and fast (MHC IIa) single muscle fibres. Vastus lateralis muscle fibres from six young men (YM; 25 ± 1 years), six young women (YW; 25 ± 1 years), six old men (OM; 80 ± 4 years) and six old women (OW; 78 ± 2 years) were studied at 15 °C for in vitro force-velocity properties, peak force and contractile velocity. Peak power was 23-28 % lower (P < 0.05) in MHC I fibres of YW compared to the other three groups. MHC IIa peak power was 25-40 % lower (P < 0.05) in OW compared to the other three groups. No difference was found in MHC I and IIa normalized peak power among any of the groups. Peak force was lower (P < 0.05) in the YW (MHC I fibres) and OW (MHC IIa fibres) compared to the other groups. Differences in peak force with ageing were negated when normalized to cell size. No age-related differences were observed in single fibre contractile velocity of MHC I and IIa fibres. These data show that YW (MHC I) and OW (MHC IIa) have lower single fibre absolute peak power and peak force compared to men; however, these differences are negated when normalized to cell size. General muscle protein concentrations (i.e. total, sarcoplasmic and myofibrillar) from the same biopsies were lower (4-9 %, P < 0.05) in the OM and OW. However, myosin and actin concentrations were not different (P > 0.05) among the four groups. These data suggest that differences in whole muscle strength and function that are often observed with ageing appear to be regulated by quantitative rather than qualitative parameters of single muscle fibre contractile function.
(Resubmitted 10 April 2003; accepted after revision 25 June 2003; first published online 1 July 2003)
Corresponding author S. Trappe: Human Performance Laboratory, Ball State University, Muncie, IN 47306, USA. Email: strappe{at}bsu.edu
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INTRODUCTION |
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Sarcopenia is a condition referring to a loss of skeletal muscle mass and strength and has been well documented in older adults (see Rogers & Evans, 1993; Dutta, 1997). Functional measurements on individual slow- and fast-twitch muscle fibres have shown impairments in the contractile properties that may explain, in part, why older men and women suffer from muscle weakness. More specifically, single fibre unloaded shortening velocity (Vo) has been reported to be reduced by 40 % in both human (Larsson et al. 1997) and rodent (Li & Larsson, 1996; Thompson & Brown, 1999) skeletal muscle. An age-related decline in the ability of slow- and fast-twitch muscle fibres to generate force has also been reported (Larsson et al. 1997; Frontera et al. 2000). Taken together, these data suggest that the intrinsic characteristics related to the cross-bridge mechanics of single fibres are altered with ageing.
While the intrinsic qualities of shortening velocity and specific force have been shown to decline with ageing, there have been no reports characterizing single muscle fibre power with ageing. Information describing the in vitro power of single muscle fibres may provide additional information to help elucidate the myocellular basis of sarcopenia. A major advantage of measuring peak power from a single fibre is that the dynamic components that contribute to isotonic muscle function are involved. Whereas previous measurements of ageing human single muscle fibre function have been reported from independent measures of contractile velocity and peak force (Larsson et al. 1997; Frontera et al. 2000), power development simultaneously employs velocity and force over a range of movement speeds and forces. Furthermore, peak power can be normalized for muscle cell size, thus providing a more detailed profile of muscle function (size, speed and force) as it relates to fibre type (slow vs. fast) with ageing.
The intent of this investigation was to characterize the isometric (peak force) and dynamic (contractile velocity and power) contractile properties with ageing in young and old men and women with similar life-long physical activity levels. While there have been other published single fibre data with ageing in humans (Larsson et al. 1997; Frontera et al. 2000; Krivickas et al. 2001), the current investigation provides the most comprehensive overview of single fibre function to date (size, force- velocity relationships, peak force, normalized force and contractile velocity) with comparisons of young and old individuals of both sexes. To our knowledge, this is also the first investigation to report single muscle fibre power with ageing. We hypothesized that older men and women would have reduced muscle cell size, peak power, peak force and contractile velocity in individual slow- and fast- muscle fibres compared to young men and women. In addition to the single fibre experiments, we also measured the concentrations of the general protein fractions and the specific skeletal muscle contractile proteins myosin and actin. We hypothesized that a reduction in single fibre function would be partially explained by a loss of myosin and actin in the older men and women. The results presented below do not support the above hypotheses.
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METHODS |
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Subjects
Twelve young (6 men, YM; 6 women, YW) and 12 old (6 men, OM; 6 women, OW) individuals were studied as part of this investigation (Table 1) following a physical examination, which included blood and urine analyses, electrocardiogram (older subjects), and an interview to document life history of physical activity. Subjects were excluded if they had any acute or chronic illness, cardiac, pulmonary, liver or kidney abnormalities, uncontrolled hypertension, insulin- or non-insulin-dependent diabetes, abnormal blood or urine chemistries, arthritis or a history of neuromuscular problems, or if they smoked cigarettes. Women taking oral contraceptives or hormone replacement therapy were included.
It was our intent to carefully screen the subjects so as to include only life-long sedentary healthy old and young individuals; therefore, we excluded individuals that had ever completed any formal exercise programmes or physical activity outside of their activities of daily living. Each subject completed a life activity and occupation form developed for the study to carefully screen for voluntary or occupation-related activities that would be considered chronic aerobic or resistance exercise type activities. The form, which was initially explained by a member of the investigative team, required each volunteer to outline a year-by-year profile of his or her lifestyle, hobbies and occupation. Each volunteer was allowed several days to complete the form at home. The form was then reviewed with the same member of the investigative team and the volunteer.
Body composition was determined using whole body air displacement plethysmography (Life Measurement Instruments, Concord, CA, USA). Prior to the screening, all potential subjects were informed of all procedures and risks associated with the experimental testing. Informed consent was obtained from each volunteer. The Institutional Review Boards of Ball State University and the University of Arkansas for Medical Sciences approved the informed consent. The study was conducted in accordance with the Declaration of Helsinki.
Whole muscle peak power and size
To document muscle power and size differences among the groups, an isokinetic test was performed to determine peak power and magnetic resonance imaging (MRI) was conducted to determine muscle cross-sectional area (CSA) of the thigh muscles (see Table 1). Muscle functional tests were completed during four different visits. The first two of these four visits were used for familiarization to the tests, while the third was used for data analysis (i.e. the data presented here) and the fourth for the determination of the reliability of these measurements. Each of these four visits was separated by at least 2 days.
Peak power measurements. Prior to peak power measurements, subjects completed light stretching of the legs and a 5 min warm-up on a bicycle ergometer (Monark Exercise AB, Sweden). Muscle function testing was performed on a Cybex Norm dynamometer (Lumenex, Ronkonkoma, NY, USA). Maximal isokinetic concentric torque was determined at 1.05, 2.09, 3.14, 4.19, 5.24, 6.28, 7.33, 8.38 and 8.73 rad s-1. At each velocity the subjects were allowed three warm-up attempts immediately followed by three maximal concentric contractions. Peak torque at each velocity was taken as the highest torque attained during either of three maximal efforts, independent of knee angle, and after correction for the effect of gravity. A 2 min rest period was given between velocities. Peak power was calculated for each subject by curve fitting the data of power (peak torque 
velocity) vs. the peak torque produced at each velocity represented as a percentage of maximal isometric torque. Some subjects were not able to generate torque at the higher velocities and/or their measured in vivo maximal shortening velocity (Vmax, data not shown) was lower than some of the higher measurement velocities. Therefore, data to develop the power curve were used if the measurement velocity was below the measured Vmax for that subject and torque production at two consecutive velocities differed by greater than 4 N m. The coefficient of variation of peak torque production for the concentric velocities that all subjects met these criteria, 1.05-5.24 rad s-1, averaged 5.3, 3.9, 4.2, 5.5 and 5.5 %, respectively, with no age, group or sex difference.
MRI measurements. Following 1 h of supine rest to control for the influence of posturally related fluid shifts on muscle size (Berg et al. 1993), MRI were obtained for each subject (T. A. Trappe et al. 2001). Subjects were supine and their heels were fixed on a non-metallic support to control joint and scan angle and to minimize compression of the legs against each other and the MRI gurney. Imaging was completed in a 1.5T GE Signa scanner (General Electric, Milwaukee, WI, USA) to determine the CSA of the total quadriceps femoris, rectus femoris (RF), vastus lateralis (VL), vastus intermedius (VI) and vastus medialis (VM). A coronal scout scan (TR/TE = 300/14 ms, field of view 48 cm, 256 160 matrix) of approximately five slices of 5 cm thickness with 5 mm spacing was completed to establish the orientation of the femur. Following the scout scan, interleaved transaxial images of 1 cm thickness (TR/TE = 2000/9.0 ms, field of view 48 cm, 256 256 matrix) were taken from the top of the greater trochanter of the femur to the articular surface of the tibia.
MR images were transferred electronically from the scanner to a personal computer (Macintosh Power PC) and analysed with NIH Image software (version 1.60) using manual planimetry. Analyses of the MR images began with the first proximal slice not containing gluteal muscle and continued distally to the last slice containing RF (Castro et al. 1999), because this region has been shown to represent the maximal CSA of the thigh (Narici et al. 1989). The average CSA (cm2) was taken as the average of all the analysed slices for an individual muscle and determined for the RF, VL, VI and VM and summed for the total quadriceps femoris.
Muscle biopsy
A muscle biopsy (Bergstrom, 1962) from the VL of the dominant leg was obtained from each subject. The biopsy area was cleaned and anaesthetized with 1 % xylocaine. Approximately 5 min later, an incision was made and a biopsy needle was inserted into the belly of the muscle for sampling. A portion of each muscle sample was sectioned longitudinally into several pieces and placed in cold skinning solution (see below) and stored at -20 °C for later analysis of single muscle fibre physiology. Following a single muscle fibre experiment, each single fibre was analysed for myosin heavy chain (MHC) composition as described below. Following each muscle biopsy, all single fibre contractile measurements were completed within a 4 week period. A separate portion of the muscle was immediately frozen and stored in liquid nitrogen (-190 °C) for later analysis of general and specific muscle protein concentrations.
Skinning, relaxing and activating solutions
The skinning solution contained (mM): 125 potassium propionate, 2.0 EGTA, 4.0 ATP, 1.0 MgCl2 and 20.0 imidazole (pH 7.0), and 50 % (v/v) glycerol. The compositions of the relaxing and activating solutions were calculated using an iterative computer program described by Fabiato & Fabiato (1979). These solutions were adjusted for temperature, pH and ionic strength using stability constants in the calculations (Godt & Lindley, 1982). Each solution contained (mM): 7.0 EGTA, 20.0 imidazole, 14.5 creatine phosphate, 1.0 free Mg2+, 4.0 free MgATP, KCl and KOH to produce an ionic strength of 180 mM and a pH of 7.0. The relaxing and activating solutions had a free [Ca2+] of pCa 9.0 and pCa 4.5, respectively (where pCa = -log [Ca2+]).
Single fibre physiology experiments
On the day of an experiment, a 2-3 mm muscle fibre segment was isolated from a muscle bundle and transferred to an experimental chamber filled with cold relaxing solution. The fibre ends were aligned in small stainless steel troughs and securely fastened in place using 4.0 monofilament posts and 10.0 suture. The troughs were attached via thin wires to a force transducer (model 400A, Cambridge Technology, Watertown, MA, USA) and a DC torque motor (model 308B, Cambridge Technology) as described by Moss (1979). The instrumentation was arranged so that the muscle fibre could be rapidly transferred back and forth between experimental chambers filled with relaxing or activating solutions. The apparatus was mounted on a microscope (Olympus BH-2, Japan) so that the fibre could be viewed (800) during an experiment. Using an eyepiece micrometer, sarcomeres along the isolated muscle segment length were adjusted to 2.5 µm. All single muscle fibre experiments were performed at 15 °C.
Unamplified force and length signals were sent to a digital oscilloscope (Nicolet 310, Madison, WI, USA) enabling muscle fibre performance to be monitored throughout data collection. Analog force and position signals were amplified (Positron Development, Dual Differential Amplifier, 300-DIF2, Ingelwood, CA, USA), converted to digital signals (National Instruments, Inc.) and transferred to a computer (Micron Electronics, Nampa, Idaho) for analysis using customized software. Servo-motor arm and isotonic force clamps were controlled using a computer interfaced force-position controller (Positron Development, Force Controller, 300-FC1).
The within fibre test/re-test variation of a single muscle fibre in our lab for the measurements of size, force-velocity relationships, peak force and contractile velocity was less than 1 %. The coefficient of variation for the force transducer and servo-mechanical lever mechanism during the 1.5 year period we examined single muscle cell function from the young and old men and women as part of this investigation was 0.5 and 0.8 %, respectively.
Single muscle fibre analysis. Individual muscle fibres were analysed for diameter, force-velocity relationships, peak force (Po) and maximal unloaded shortening velocity (Vo). Experimental procedures were identical to those previously used in our human ageing studies (S. Trappe et al. 2000, 2001b).
Single fibre diameter. A video camera (Sony CCD-IRIS, DXC-107A, Japan) connected to the microscope and interfaced to a computer allowed viewing on a computer monitor and storage of the digitized images of the muscle fibres. Fibre diameter was determined from a captured computer image taken with the fibre briefly suspended in air (< 5 s) as has been done with our previous ageing studies (S. Trappe et al. 2000, 2001b). Fibre width (diameter) was determined at three points along the segment length of the captured computer image using public domain software (NIH Image v1.61). Fibre CSA was calculated from the mean width with the assumption that the fibre forms a cylindrical cross-section when suspended in air.
Single fibre force-velocity relationship. Submaximal isotonic load clamps were performed on each fibre for determination of force-velocity parameters. Each fibre segment was fully activated in a pCa 4.5 solution and then subjected to three isotonic load steps. The circuitry of this system is essentially the same as that described by Julian & Moss (1981). Force records for a representative series of three isotonic steps are shown in Fig. 1. After the third step, the position motor imposed a slack length step of < 15 % of the original fibre length and the fibre was transferred back into relaxing solution where it was re-extended to the original fibre length. This procedure was performed at various loads so that each fibre was subjected to a total of 15-18 isotonic contractions.
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Figure 1. Representative force and length records and the resulting force-velocity relationship of a single muscle fibre from the vastus lateralis of a 93 year old male Inset, series of 3 submaximal isotonic load clamps (each step lasted 100 ms). Force and shortening velocity were determined over the final one-third of each isotonic load clamp. The filled circles represent the resulting data points from the 3 isotonic load clamps shown in the inset. The open circles represent the resulting data points for the previous isotonic load clamps. Data were fitted using the Hill equation, (P + a)(V + b) = (Po + a)/b, where P is force, V is velocity, Po is peak isometric force, and a and b are constants of force and velocity, respectively. For this muscle fibre, the Vmax was 0.80 FL s-1, power was 11.2 µN FL s-1, normalized power was 1.25 W l-1, a/Po was 0.024 and r2 was 0.98. Gel electrophoresis identified this fibre as MHC I. | ||
For the force-velocity relationships, load was expressed as P/Po, where P is the force during load clamping and Po is the peak isometric force developed prior to the submaximal load clamps. Force and shortening velocity data points derived from the isotonic contractions were fitted using the hyperbolic Hill equation (Hill, 1938). Only individual experiments in which r2 was greater than or equal to 0.98 were included for analysis.
Fibre power was calculated from the fitted force-velocity parameters (Po, Vmax and a/Po, where a is a force constant). Absolute power (µN FL s-1, where FL is fibre length) was defined as the product of force (µN) and shortening velocity (FL s-1). Normalized power (Watts per litre, W l-1) was defined as the product of normalized force (i.e. fibre force per CSA) and shortening velocity.
Single fibre Po. The output of the force and position transducers was amplified and sent to a microcomputer via a Lab-PC+ 12-bit data acquisition board (National Instruments, Inc.). Resting force was monitored and then the fibre was maximally activated in pCa 4.5 solution. Peak active force (Po) was determined in each fibre by computer subtraction of the force baseline from the peak force in the pCa 4.5 solution.
Single fibre Vo. Fibre Vo was measured by the slack test technique as described previously (Edman, 1979). The fibre was fully activated in pCa 4.5 and then rapidly released to a shorter length, such that force fell to baseline. The fibre shortened, taking up the slack, after which force began to redevelop. The fibre was then placed in relaxing solution and returned to its original length. The duration of unloaded shortening, or time between onset of slack and redevelopment of force, was determined by computer analysis. Four different activation and length steps (150, 200, 250 and 300 µm; each 
15 % of FL) were used for each fibre with the slack distance plotted as a function of the duration of unloaded shortening. Representative force records and resulting force vs. slack distance plot are shown in Fig. 2. Fibre Vo (FL s-1) was calculated by dividing the slope of the fitted line by the segment length and the data normalized to a sarcomere length of 2.5 µm. Fibre length averaged 2.33 ± 0.03 mm with an average y-intercept of 19.0 ± 3.7 µm, resulting in a fibre compliance of 0.8 %.
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Figure 2. Representative force records of a maximally Ca2+-activated single muscle fibre from the vastus lateralis of a 93 year old male A, original force recordings following slack steps of 150, 200, 250 and 300 µm. Records have been superimposed to illustrate the increasing duration to force redevelopment with increasing slack distance. B, time required to redevelop force plotted vs. imposed slack distance. Slope of this line defines fibre unloaded shortening velocity (Vo). In this example, Vo of the fibre was 0.98 FL s-1 with a y-intercept of 20.5 µm. The fibre segment studied was 2.27 mm, resulting in a compliance of 0.9 %; r2 was 0.99. Gel electrophoresis identified this fibre as MHC I. | ||
Single fibre MHC determination
Following the single muscle fibre physiology measurements, each fibre was solubilized in 80 µl of 10 % SDS sample buffer and stored at -20 °C until assayed (Giulian et al. 1983; Williamson et al. 2001). In order to determine the MHC composition, fibres were run on a Hoefer SE 600 gel electrophoresis system that consisted of a 3.5 % (w/v) acrylamide stacking gel with 5 % separating gel at 4 °C. Following gel electrophoresis, the gels were silver stained for MHC identification as described by Giulian et al. (1983). A representative MHC gel is shown in Fig. 3.
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Figure 3. Representative 5 % SDS-PAGE gel of human single muscle fibres for MHC identification Each lane represents a single muscle fibre. | ||
Muscle protein concentration determination
For each subject, a piece of muscle weighing ~10 mg was divided and weighed on a precision microbalance (Cahn 35, Orion Research, Beverly, MA, USA) at -35 °C. Each sample was homogenized in 40 volumes of cold homogenizing buffer (250 mM sucrose, 100 mM potassium chloride, 20 mM imidazole and 5 mM EDTA; pH 6.8) in a ground-glass homogenizer (Radnoti Glass Technology, Monrovia, CA, USA) (Chi et al. 1983). Samples were then centrifuged at 21 000 g for 30 min at 4 °C. The supernatant was taken as the sarcoplasmic protein fraction and the pellet was resuspended in 40 volumes of cold homogenizing buffer and taken as the myofibrillar protein fraction (Solaro et al. 1971). Aliquots of the homogenate (total protein), sarcoplasmic and myofibrillar protein fractions were measured for protein concentration using the bicinchoninic acid assay (Sigma, St Louis, MO, USA) with bovine serum albumin used as the protein standard. The amount of protein in each of the three fractions was normalized to the wet weight of each muscle sample.
MHC and actin concentration determination
MHC and actin concentrations were determined by quantitative gel electrophoresis as previously described (Tsika et al. 1987; Ingalls et al. 1998). Aliquots of the myofibrillar protein fraction were diluted with sodium dodecyl sulphate (SDS) buffer (2 % SDS, 125 mM Tris HCl (pH 6.8), 12.5 % glycerol, 5 % 2-mercaptoethanol, 0.005 % bromophenol blue) and heated at 60 °C for 4 min. Myofibrillar protein (800 ng) was separated by SDS-PAGE (Laemmli, 1970). MHC was resolved with a 4 % stacking gel and 10 % separating gel. Actin was resolved with a 4 % stacking gel and a 6-12 % gradient separating gel that were allowed to polymerize overnight. For MHC and actin, electrophoresis was performed at a constant current of 20 mA per gel in the stacking gel, and 25 mA per gel in the separating gel with a Tris-glycine electrode buffer at 4 °C (Hoeffer SE 600, Amersham Pharmacia Biotech, Piscataway, NJ, USA).
The separating gels were silver stained (Giulian et al. 1983), digitally photographed (ChemImager 5500, Alpha Innotech, San Leandro, CA, USA), and densitometry was completed using NIH Image software (version 1.60). Each gel was loaded with five standards of either MHC or actin (Sigma), a molecular mass standard (Pierce, Rockford, IL, USA), and subject samples (see Fig. 4). All standards and samples were loaded in duplicate and each gel contained samples from young and old men and women. An average of the duplicate densities was taken to represent each standard and sample. All measurements were made in blinded fashion by the same investigator. Unknown sample amounts of MHC and actin were determined from regression analysis of the standard curves on each gel. Correlation coefficients were 0.98-1.00 for both MHC and actin.
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Figure 4. Representative silver-stained gel used for MHC (10 %) and actin (6-12 % gradient) protein quantification Five standards (MHC: 1000, 800, 600, 400, 200 ng; Actin: 500, 400, 300, 200, 100 ng) were loaded in duplicate on each gel. Each gel also contained samples (800 ng myofibrillar protein) in duplicate from young and old men and women. | ||
Statistical analysis
A two-way (age and sex) nested ANOVA was used to determine whether there were differences between the YM, YW, OM and OW for each of the following variables: diameter, peak power, normalized peak power, a/Po, Po, Po/CSA, Vo and Vmax. Data from all the fibres studied for an individual were nested to represent a mean for MHC I and MHC IIa fibres. A Bonferroni post hoc test was used when significance was noted.
Given the small number of hybrid (I/IIa and IIa/IIx) fibres studied in these experiments (Table 2), they were not included in the analysis. In addition, no pure IIx fibres were identified among the fibres studied. Thus, age and sex comparisons of single muscle fibre contractile function are limited to the MHC I and IIa fibre types.
As with our previous work (S. Trappe et al. 2001b), a limited number (n = 7) of MHC IIa fibres were analysed from the older women. We attempted to study the contractile function on several of the MHC IIa fibres; however, most of these fibres (n = 16) either broke during the experiments or failed to meet the inclusion criteria (see 'Single fibre physiology experiments'). These failed fibres were later identified as MHC IIa using gel electrophoresis.
Muscle protein concentrations were compared with a two-way (age and sex) ANOVA. No significant interactions were detected; therefore, post hoc comparisons were not completed and the data were collapsed and presented as young and old. Significance was accepted at P < 0.05. Data are presented as means ± S.E.M.
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RESULTS |
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Whole muscle power and size
Whole muscle power was 45 % lower in the old compared to the young (P < 0.05; Table 1). Of the four groups, the older women had the lowest (P < 0.05) power output of the knee extensors, while the young men had the highest power output (P < 0.05). Interestingly, no differences in whole muscle power of the knee extensors were found between the young women and old men. Whole muscle size, as measured by MRI, was found to have a similar pattern to the whole muscle power output data (Table 1). The thigh muscles of the old men and women were 15 % smaller compared to those of the young men and women. By group, the old women had the smallest (P < 0.05) thigh muscles, while the young men had the largest (P < 0.05) thigh muscle CSA.
Single fibre MHC composition
The MHC profile is shown in Table 2. A total of 337 fibres were studied from the young and old men and women, with 68 % of the fibres identified as MHC I and 20 % identified as MHC IIa. Nine per cent of the fibres were identified as hybrid MHC I/IIa and 3 % as hybrid MHC IIa/IIx. In addition, no MHC IIx fibres were identified as part of the functional analysis.
Single fibre diameter
Single MHC I and IIa fibre diameter is shown in Table 3. The MHC I fibres from the YW were 13, 15 and 13 % smaller (P < 0.05) compared to those from the YM, OM and OW, respectively. No difference in MHC I fibre size was noted among the YM, OM and OW. The MHC IIa fibres of the OW were 28, 17 and 23 % smaller (P < 0.05) compared to those of the YM, YW and OM, respectively, with no other differences noted among the groups.
Single fibre power
Absolute peak power and peak power normalized for muscle cell size of the MHC I and IIa fibres for each group are shown in Table 4. MHC I peak power was ~28 % lower in the YW compared to that in the YM, OM and YW. Peak power of the MHC IIa fibres was 40, 25 and 34 % lower in the OW compared with that in the YM, YW and OM, respectively. However, when peak power was normalized to muscle cell size there was no difference in MHC I or IIa peak power among the young and old men and women.
The distribution of MHC I and MHC IIa single myofibre normalized power from the young and old men and women is shown in Fig. 5 and Fig. 6, respectively. The range for the MHC I fibres was 0.50-4.16 W l-1 for all subjects. Interestingly, the lowest (0.50) and highest (4.16) normalized power values were found in the YW. By group, the range for MHC I normalized power ( W l-1) was 0.86-2.44 in the OM, 0.65-3.42 in the YM, 0.88-3.59 in the OW and 0.50-4.16 in the YW.
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Figure 5. Normalized power (W l-1) distribution of MHC I single muscle fibres from young men and women, and old men and women Each point represents normalized power data from a single muscle fibre. | ||
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Figure 6. Normalized power (W l-1) distribution of MHC IIa single muscle fibres from young men and women, and old men and women Each point represents normalized power data from a single muscle fibre. | ||
The range for the normalized power of the MHC IIa fibres was 1.84-16.51 W l-1 for all subjects. As with the MHC I fibres, the lowest (1.84) and highest (16.51) MHC IIa normalized power values were found among the YW (different individuals for the MHC I and IIa range among the YM). For each group, the MHC IIa normalized power ( W l-1) was 4.72-14.66 in the OM, 2.81-11.90 in the YM, 5.57-14.04 in the OW and 1.84-16.51 in the YW.
The majority (~75 %) of the MHC I muscle fibres had a normalized power between 1 and 2 W l-1 for the YM, OM, and OW, whereas 54 % of the young women's fibres were between 1 and 2 W l-1. Approximately 70 % of the MHC IIa fibres had a normalized power between 6 and 12 W l-1, with the older women having the majority of their MHC IIa fibres between 6 and 12 W l-1.
The parameter a/Po, which describes the curvature of the force-velocity relationship, was similar among all groups for the MHC I fibres. The MHC IIa fibres also had a similar a/Po among all four groups. The mean a/Po for the MHC I and IIa fibres for all groups was 0.029 ± 0.003 and 0.041 ± 0.005, respectively.
Single fibre Po
Peak force for MHC I and IIa fibres is shown in Table 5. The YW had the weakest (P < 0.05) MHC I fibres by an average of 23, 29 and 27 % compared with the YM, OM and OW, respectively. No other difference in fibre Po was observed in the MHC I fibres among the groups. The MHC IIa fibres from the OW were 46, 33 and 38 % weaker (P < 0.05) compared with those from the YM, YW and OM, respectively. The MHC IIa fibres from the YW produced 20 % less (P < 0.05) peak force compared to those from the YM. No other difference was found among the groups in MHC IIa fibre Po.
When fibre force (Po) was corrected for fibre size, the YM had a lower MHC IIa Po/CSA compared to the YW, OM and OW. No other differences in fibre force per CSA for the MHC I (Figure 7) and MHC IIa (Figure 8) fibres were observed among the YM, YW, OM and OW.
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Figure 7. Scatter plot of fibre diameter and peak tension for the MHC I muscle fibres from young men (YM), old men (OM), young women (YW) and old women (OW) | ||
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Figure 8. Scatter plot of fibre diameter and peak tension for the MHC IIa muscle fibres from young men, old men, young women and old women | ||
Single fibre shortening velocity
The contractile velocity of the muscle fibres was assessed using the slack test procedure (Vo) and the force-velocity procedure (Vmax). Both of these measurements provided a measure of shortening velocity and data are shown in Table 6. No difference was found in the average Vo or Vmax of the MHC I fibres among the groups. Similarly, no difference in the average Vo and Vmax was found in the MHC IIa fibres among the young and old men and women. However, the shortening velocity (Vo and Vmax) of the MHC I fibres was slower (P < 0.05) than that of the MHC IIa fibres for each group.
Muscle protein concentrations
Muscle protein concentrations are presented in Tables 7 and 8. Total, sarcoplasmic and myofibrillar protein concentrations were not different (P > 0.05) among YM, YW, OM and OW. However, total (-4 %), sarcoplasmic (-9 %) and myofibrillar (-6 %) protein concentrations per milligram muscle wet weight were lower (P < 0.05) in the old compared to the young group. MHC and actin concentrations within the myofibrillar protein, total protein or the muscle wet weight were not different among YM, YW, OM and OW. MHC concentration was 20 and 13 % greater (P < 0.05) in the old vs. young within the myofibrillar and total protein fractions, respectively. However, actin concentration in these two protein fractions was not different (P > 0.05) between the young and old. When expressed per muscle wet weight, MHC and actin concentrations were not different (P > 0.05) between the young and the old.
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DISCUSSION |
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Our intent was to study several parameters of single muscle cell contractile function in a cohort of young and old men and women to gain a better understanding of the myocellular contribution to sarcopenia with ageing. Of primary interest was the variable of normalized power to assess single muscle fibre function since variables of strength, speed and size are involved in this measurement. To our knowledge, this is the first investigation to make direct measurements of single muscle fibre power with age in humans. The main finding from this investigation was that slow- and fast-twitch normalized muscle power did not differ among young and old men and women, suggesting that the intrinsic properties related to cross-bridge mechanics are maintained with age.
We hypothesized that single muscle fibre peak power would be reduced with age. The fact that we found no age-related differences in single fibre normalized peak power indicates that this cannot explain the age-related decline in whole muscle function in these same subjects (see Table 1) that has been documented in previous studies (Larsson et al. 1979; Young et al. 1985). This would suggest that the loss of muscle mass is the critical component that accounts for the decrease in muscle function with ageing. This reduction in muscle mass is most likely to be the result of a combination of muscle fibre atrophy and loss of fibre number that may be targeted to the fast-twitch fibres. Lexell et al. (1988) reported that VL muscle fibre number drops from ~600 000 fibres at age 20-30 years to less than 300 000 by age 80 years. This is further compounded by the fact that the fast-twitch muscle fibres occupy less of the contractile material, which is probably mediated through a reduction in the number and/or size of the fast-twitch fibres (Lexell & Downham, 1992). Data from the current study showed that the MHC IIa fibres had a 5- to 6-fold higher normalized power compared to the MHC I fibres. Thus, a smaller number of fast-twitch fibres that provide greater normalized peak power (~450 %) than slow-twitch fibres may be a major contributing factor in the loss of muscle function with age.
The similarities in peak power when normalized for cell size suggest that the mechanical components regulating the dynamic properties of the contractile proteins are not altered in slow- and fast-twitch muscle fibres with ageing. This implies that the myofibrillar proteins that regulate muscle contraction remain intact and functional in older adults. There have been reports of myofibrillar protein loss in old rats, which was hypothesized to alter the density of actin and myosin leading to a decrease in the number of cross-bridges acting in parallel and therefore reducing the force-generating capacity of muscle (Ansved & Larsson, 1990). Partially consistent with this idea, we found that the myofibrillar protein concentration was decreased with age. However, the muscle concentrations of myosin and actin were maintained with age, suggesting that proteins other than myosin and actin in the myofibrillar apparatus are compromised with ageing. The similarities in the normalized power of individual slow- and fast-twitch fibres from the young and old coupled with the myofibrillar data suggest that fibre volume may be regulated in such a way to alter the ultrastructural architecture but preserve the density of the contractile material, thereby maintaining the force-generating capacity of the remaining muscle.
In agreement with the normalized single muscle fibre power data, other aspects of contractile function were also maintained with age in the current investigation. Specifically, force per CSA and contractile velocity of the MHC I and IIa fibres were similar among the young and old men and women. Our finding of maintained single muscle fibre function with age is in conflict with previous reports from humans (Larsson et al. 1997; Frontera et al. 2000) and animals (Brooks & Faulkner, 1994; Li & Larsson, 1996; Thompson & Brown, 1999). One of our primary goals was to carefully screen subjects to minimize physical activity as a confounding variable. Previous human single muscle fibre ageing studies have studied subjects that have been engaged in moderate to heavy physical activity (Larsson et al. 1997) or had varying degrees of weekly physical activity (Frontera et al. 2000), or have not reported physical activity levels (Krivickas et al. 2001). In addition, the results reported by Larsson et al. (1997) may have been limited by the low number of young (n = 4) and old (active n = 2; inactive n = 2) men studied. As a result, differences in subject populations, the number of subjects studied and/or the physical activity level of the subjects may account for differences among the current and previous investigations.
In support of the influence of physical activity on contractile function, our lab has shown that fibre Vo is altered with various training regimens in swimmers (S. Trappe et al. 2001a) and runners (Widrick et al. 1996), and in resistance training in the elderly (S. Trappe et al. 2000). These studies and others of spaceflight (Widrick et al. 1999) and bedrest (Larsson et al. 1996; Widrick et al. 1997) in humans have all shown fibre Vo to be altered when the external load on the muscle is manipulated, suggesting that increases or decreases in physical activity can significantly alter fibre Vo. Furthermore, single muscle fibre Vo has been shown to vary considerably, even in fibres containing the same MHC isoform (Bottinelli, 2001), possibly a cellular strategy to accommodate a wide range of movements. We did not find a reduced fibre contractile velocity with age or sex. Our findings are strengthened by the fact that we had two independent measures of fibre shortening velocity (Vo and Vmax) from each fibre segment studied. While Vmax yielded slightly lower values compared to Vo, the same conclusions could be made from the two data sets.
While physical activity probably contributed to the differences in single muscle fibre function in the current investigation compared to previous reports, the underlying mechanisms by which age, physical activity, illness, etc., interact to alter a fibre's mechanical properties remain to be determined. In this regard, other aspects must also be considered. Our single muscle fibre data indicated a rather large range in functionality among the groups (see Fig. 5 and Fig. 6), which contributed to the overall similarities among the groups. Previous human ageing studies have reported single fibre contractile properties that do not appear to have the large range found in the current investigation. However, the study by Larsson et al. (1997) involved fewer fibres, which may have limited the finding of a large functional range. Furthermore, Larsson et al. (1997) reported data from freeze-dried samples, and freeze-drying has been shown to affect the contractile properties of single fibres (Larsson & Moss, 1993). Thompson & Brown (1999) found a large range in fibre Vo (0.6-3.1 FL s-1) from rodent soleus muscle, but did report a decline in fibre Vo with ageing. The fact that the soleus is primarily composed of slow-twitch fibres compared to the mixed fibre profile of the VL from subjects in the current investigation may have contributed to the differences in our results. Thus, fibre number, methodological differences among investigations, the muscle investigated and/or the species studied may have contributed to the different findings in the current investigation.
There have also been reports indicating that modifications in myosin are apparent in older animals, which may help to explain some of the force decrements with ageing (Ramamurthy et al. 2001; Lowe et al. 2001, 2002). We did not measure these aspects in this investigation. Our myosin and actin data from the current investigation indicated that the quantity is unaltered with age, thus supporting the similarities in single fibre contractile function. It is unclear what molecular modifications occur in older human muscle, if any, that can be attributed to ageing that may modify the contractile properties of human muscle. It is possible that minor modifications may occur at the level of the cross-bridge (i.e. amino acid alterations, glycation, etc.) that are not detectable in the single fibre preparation (multiple cross-bridge interactions occurring in parallel) used in this investigation.
One notable exception to our finding that single muscle fibre contractile function was maintained with age was the minimal number (n = 7) of fast-twitch fibres that were successfully studied from older women as part of this investigation. This is in agreement with our previous study on older women (S. Trappe et al. 2001b), and indicates that the structural framework of these fast-twitch fibres may be compromised with age. The MHC distribution in older women has been shown to be similar to that of old men and sedentary young men and women (Williamson et al. 2000), suggesting that the MHC IIa fibre type is present, but the current data suggest that the myofibre is not structurally sound enough to tolerate the type of repeated contractions used in the current investigation. It is possible that structural/anchoring proteins that provide stability for cell integrity are altered in these older women and contributed to the failure of these fibres when subjected to a series of maximal and submaximal contractions. Our myofibrillar data (see Tables 7 and 8) would support the theory that muscle fibres from older adults may be more susceptible to damage due to fewer structural proteins in the myofilament lattice while at the same time maintaining proteins that generate force (i.e. myosin and actin). Frontera et al. (2000) successfully studied 56 fast-twitch fibres from twelve 72 year old women. However, they only measured Po from these fast-twitch fibres, which required one to two maximal contractions. To obtain all the single fibre data for the current investigation (Po, Vo and force-velocity relationships), each fibre was subjected to 15-25 maximal and submaximal contractions. Thus, the nature of these different tests (static vs. dynamic) and the number of contractions imposed on the fibres may have contributed to the discrepancy between investigations in fast-twitch fibre success among the older women.
Also worth noting was how small the MHC IIa fibres from the older women were compared to those from the other groups (Table 3). Within each group, the MHC I and IIa fibres were similar in size for the YM, YW and OM. In the old women, however, the MHC IIa fibres were 28 % smaller than the MHC I fibres. These data suggest that there is advanced fast-twitch fibre-specific sarcopenia in older women and that the size of MHC I fibres from older women is maintained or even hypertrophied (compared to YW) with age. The reason for this finding is unknown, but a reasonable interpretation would be that old women have a decreased use of fast-twitch muscle fibres and an increased use of slow-twitch muscle fibres for normal daily movement. Previous studies have suggested that a loss of motor units may occur in older humans which could lead to a reorganization of the motor unit resulting in compensatory hypertrophy in the remaining muscle fibres (Tomlinson & Irving, 1977; Einarsson et al. 1990; Aniansson et al. 1992). Our data would support such a theory since the fast-twitch fibres from the older women were significantly smaller while the slow-twitch fibres were larger than in the young women but were similar to those of the men we investigated.
In summary, the single muscle fibre normalized power, normalized force and contractile velocity results provide evidence that the isometric and isotonic contractile properties of slow- and fast-twitch fibres are maintained with age and cannot explain the decrease in whole muscle function observed in these same individuals. Differences in skeletal muscle function related to ageing appear to be quantitative (muscle cell size and/or number) rather than qualitative (no change in single muscle fibre normalized power or contractile velocity). These data suggest that while whole muscle mass and function are reduced with ageing, the remaining muscle that older adults do have is functionally equivalent to that of young adults when corrected for cell size.
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Acknowledgements
The authors would like to thank the subjects for their participation. This investigation was supported by National institutes of Health grants R21AG15833, K01AG00831 and M01RR14288.
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