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1 Laboratoire de Plasticité Neuromusculaire, Université des Sciences et Technologies de Lille I, Bat SN4, F-59655 Villeneuve d'Ascq Cedex, France; and 2 Department of Veterinary and Comparative Anatomy, Pharmacology and Physiology, Washington State University, Pullman, Washington 99164
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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In this work we studied changes in passive elastic properties of rat soleus muscle fibers subjected to 14 days of hindlimb unloading (HU). For this purpose, we investigated the titin isoform expression in soleus muscles, passive tension-fiber strain relationships of single fibers, and the effects of the thick filament depolymerization on passive tension development. The myosin heavy chain composition was also measured for all fibers studied. Despite a slow-to-fast transformation of the soleus muscles on the basis of their myosin heavy chain content, no modification in the titin isoform expression was detected after 14 days of HU. However, the passive tension-fiber strain relationships revealed that passive tension of both slow and fast HU soleus fibers increased less steeply with sarcomere length than that of control fibers. Gel analysis suggested that this result could be explained by a decrease in the amount of titin in soleus muscle after HU. Furthermore, the thick filament depolymerization was found to similarly decrease passive tension in control and HU soleus fibers. Taken together, these results suggested that HU did not change titin isoform expression in the soleus muscle, but rather modified muscle stiffness by decreasing the amount of titin.
depolymerization; hindlimb unloading, myosin heavy chain; titin
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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RAT HINDLIMB UNLOADING (HU) is a well-developed model to elicit muscle atrophy, especially of the slow postural soleus muscle (27). Muscle atrophy is accompanied by a slow-to-fast transformation of the soleus muscle, characterized by a decrease in the expression of the slow myosin heavy chain (MHC) I isoform, concomitant with a rise in the expression of the fast MHC IIa and the appearance of the MHC IId/x and MHC IIb (1, 2, 6, 23, 26). These transitions at the molecular level have been found to modify the contractile properties of the soleus muscle fibers such as the calcium-activated properties (8, 25, 29), the maximal shortening velocity (19, 20, 29), as well as the elastic properties of the maximally activated muscle fibers (21, 29, 35).
In addition to the calcium-dependent contractile properties, skeletal muscle fibers develop passive tension when they are passively stretched beyond their slack length. The passive properties of the skeletal muscle fibers lie in the properties of titin, a filamentous protein found in striated muscle (18, 30, 32), which extends from the Z-line to the M-line of the sarcomere. Furthermore, only the I-band titin segment has been found to develop passive tension when sarcomeres are stretched, whereas the A-band titin segment is strongly attached to the thick filament (9, 33, 34). Recent investigations on skeletal and cardiac muscles indicate that I-band titin consists of three main segments: a "PEVK" segment rich in proline (P), glutamate (E), valine (V), and lysine (K) residues; tandem immunoglobulin (Ig) segments flanking the PEVK segment; and the N2A/N2B segment. The N2A segment is found in skeletal muscle, whereas the N2B is found exclusively in cardiac muscle, which also expresses the N2A segment (3, 16). Both segments are expressed in muscle type-specific length variants and act as mechanically distinct molecular spring segments (16). The tissue-specific expression of tandem Ig, PEVK, and N2A/2B spring elements results in specific exon-skipping events from a single titin gene (7). This molecular basis of titin expression provides an understanding of the diversity in passive mechanical properties of myofibrils (7). Moreover, this elastic protein appears to contribute to the structural and mechanical stability of the sarcomere during calcium activation (13, 14). The titin filament keeps the thick filament in a centered position into the sarcomere and avoids misalignments that can affect the sarcomere functioning during calcium activation.
The expression of muscle-specific variants of titin seems to be closely related to the functional activity of the sarcomere. Because no studies have determined titin elastic properties under disuse conditions, we investigated the passive elastic properties of soleus muscle fibers from rats subjected to 14 days of HU. Titin expression was analyzed on SDS-PAGE. The passive elastic properties (passive tension-fiber strain curves) were determined on single muscle fibers, stretched stepwise to their elastic limit. To determine any modifications in the A-band region of titin, fibers were submitted to a partial depolymerization of the thick filaments by using a high-concentration KCl solution (12). Skeletal muscle fibers were identified on the basis of their MHC content.
Our results indicated that, after HU, changes in the shape of the passive tension-fiber strain curves for soleus fibers were observed without a change in titin isoform expression.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Animals. Adult male Wistar rats weighing 280-300 g were randomly divided into two groups: a control group (n = 5) and a 14-day HU group (n = 8) using the previously described HU model (25). In this model, the rats are able to move freely on their forelimbs and have full access to food and water. The rats were individually caged on a 12:12-h light/dark daily cycle at 23°C room temperature. The experiments were conducted under authorization from both the Ministry of Agriculture and the Ministry of Education (veterinary service of health and animal protection, authorization no. 03805).
Muscle processing.
Animals were anesthetized with an intraperitoneal injection of
pentobarbital sodium (30 mg/kg body wt). For each control and HU
animal, the soleus muscles were quickly removed from the hindlimbs. One
soleus muscle was randomly frozen in liquid nitrogen and stored at
80°C until electrophoretic analysis. The second soleus muscle was
chemically skinned in an EGTA skinning solution (see
Solutions) for 24 h at 4°C and stored in a 50%
glycerol skinning solution at 20°C for 2 wk (22). The
fast extensor digitorum longus (EDL) muscles of the control animals
were also removed and stored at 80°C as described above. EDL
muscles were used as SDS-PAGE controls for the three fast MHC IIa,
IId/x, and IIb isoforms. After the surgical operation, animals were
euthanized with an overdose of pentobarbital sodium. The same protocol
as described above was applied to obtain soleus and psoas muscles from
New Zealand White rabbits (n = 2). Fibers from rabbit
muscles were used to validate (see RESULTS) our passive
tension protocol described below.
Mechanics. Single muscle fibers were dissected from the skinned biopsies with use of a binocular microscope. Fibers were mounted between the arm of a feedback-controlled stepping motor (Cambridge Technology, model 6350) and a hook attached to a strain gauge (AE801, AME, Horten, Norway; resonance frequency in air 5.33 kHz) by gluing each end with cellulose polyacetate dissolved in acetone. Fibers were then bathed in relaxing solution (see Solutions). Their slack sarcomere length (SLs) was measured by the light diffraction of a He-Ne laser beam (Melles-Griot; 632 nm wavelength, 10 mW output). The position of the first-order diffraction line was collected on a 512-element photodiode array (TSL 218, Texas Instruments, Dallas, TX) that was scanned electronically every 1 ms. The median position of the first-order intensity distribution was converted into a voltage proportional to the sarcomere length using a nonlinear amplifier. Special attention was given to the manner by which the SLs was determined. After being mounted, fibers were shortened until they clearly buckled and were kept in this state for 10 min. The fibers were then stretched slowly, and the length at which sarcomere length just started to increase was taken as the slack length. Moreover, fibers with a diffuse diffraction pattern suggesting disrupted sarcomeres were discarded.
Passive tension, motor position, and sarcomere length signals were recorded on a chart recorder (Gould; model 40-8474-02) and digitized and stored on floppy disk for further analysis. The slack length (Ls) and the diameter of the fiber segments were determined with a micrometer through a high-magnifying (×80) binocular microscope. All the experiments were performed at 19 ± 1°C.Passive tension determination. The slack fibers were bathed for 10 min in relaxing solution containing Brij (2% wt/vol) and Triton X-100 (1% vol/vol). This procedure was repeated two times to obtain an optimal skinning protocol. Fibers were then washed three times with the washing solution (see Solutions) and returned to relaxing solution.
To ensure a stable slack length throughout the mechanical protocol and to improve fiber attachments, fibers were stretched to a sarcomere length of 2.6 µm and maximally activated in a pCa 4.2 solution (pCa =log [Ca2+], where brackets denote
concentration). Subsequently, they were returned to relaxing solution
for 10 min and released to their original SLs.
Passive tension was measured by subjecting fibers to a
stretch-and-release cycle. To obtain reproducible results, the
stretches and releases were generated by a computer-controlled stepping motor to impose an identical stretch-release protocol. For a given stretch-release cycle (Fig. 1), the fiber
was slowly stretched stepwise in intervals of 10% of its slack fiber
length (Ls) over 15 s. During stretching,
tension rose to a peak. At the end of each stretch, fiber length was
held constant for 3 min to allow relaxation and tension to decay
exponentially to a plateau, taken as the passive tension level (Fig. 1,
inset A). After a series of stretches to 140% of
Ls, the fiber was released stepwise in the same
way. Upon each release, the tension decreased and then rose slightly to
another plateau value. The passive tension decreased quickly with
shortening so the fiber became slack before the release was completed
(Fig. 1). For each experiment, we have drawn the relation between the
fiber length and the sarcomere length (Fig. 1, inset B). The
linear relation obtained (r 
0.98) was used as a control
to verify the rigid attachment of the fiber to the mechanical
apparatus.
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Thick filament depolymerization. The passive elastic properties of the muscle fibers were determined also after partial depolymerization of the thick filaments (12). Fiber passive properties were first characterized by a stepwise stretch-release protocol to 70% of Ls. This maximal fiber stretch was chosen to not stretch the fiber beyond its yield sarcomere length (its elastic limit). Fibers were then relaxed at their SLs for 10 min and directly stretched to a sarcomere length of 3.0 µm to minimize the thick and thin filament overlap and enhance the depolymerization procedure. A maximal tension was elicited by applying the maximally activating pCa 4.2 solution. After relaxation, fibers were bathed to 20 min in the 540 mM KCl solution to partially depolymerize the thick filaments. The depolymerization was completed by washing fibers twice with the KCl solution and then with the relaxing solution. Depolymerization of the thick filaments was indicated by the complete reduction in active tension during activation in pCa 4.2 solution. Fibers were then returned to their initial SLs and allowed to relax for 10 min. The fibers then were submitted to the complete stretch-release cycle to 140% of Ls.
MHC isoform determination.
After the passive tension measurements, each fiber was solubilized in
Laemli buffer (62.5 mM Tris, pH 6.8, 2% wt/vol SDS, 10% vol/vol
glycerol, 55 vol/vol 2-mercaptoethanol, and 0.02% wt/vol bromphenol
blue) and then stored at 80°C until electrophoretic analysis. The
fiber samples were used to determine the MHC composition by SDS-PAGE on
a 7.5% slab gel (31). All results presented in this work
are from muscle fibers for which both the passive tension properties
and the MHC composition had been determined. Some fibers were discarded
because only partial data had been obtained. In addition to
single-fiber characterization, we also determined the MHC profile of
each muscle to verify that HU caused the expected MHC transformations.
Titin isoform determination. After the MHC determination of whole muscles, control and transformed muscle samples were electrophoresed on a 2-12% SDS-polyacrylamide gradient gel according to the method of Granzier and Wang (10). Human soleus muscle was used as a titin molecular mass marker. After electrophoresis, gels were stained with Coomassie blue, and a quantitative densitometry was performed to determine the amount of titin relative to that of MHC (for details, see Ref. 3). Briefly, to ensure that results were obtained in the linear range of SDS-PAGE and scanner systems, a loading range of each sample was electrophoresed on the same gel. The optical density (OD) of titin and MHC isoform signals were determined, and the OD results of all lanes were plotted vs. their loadings. A slope of linear range of this relation was determined for titin and MHC, and the slope ratios were taken as a measure of the relative amount of titin in the samples (3).
Solutions. The solutions were prepared (22) with a final ionic strength of 200 mM and a pH of 7.00 ± 0.02. The following solutions were used for the experimental procedure: a washing solution composed of ATP (2.5 mM), MOPS (20 mM), potassium propionate (185 mM), and magnesium acetate (2.5 mM). The relaxing or skinning solution was composed of ATP (2.5 mM), MOPS (20 mM), potassium propionate (170 mM), magnesium acetate (2.5 mM), and K2EGTA (5 mM). The pCa 4.2 activating solution consisted of ATP (2.5 mM), MOPS (10 mM), potassium propionate (170 mM), magnesium acetate (2.5 mM), and free Ca2+ buffered with 5 mM EGTA (CaEGTA and K2EGTA mixed in adequate proportions to obtain the pCa 4.2 value).
The depolymerization solution was composed of MOPS (20 mM), magnesium acetate (2.5 mM), K2EGTA (5 mM), and KCl (540 mM). The final ionic strength was 570 mM, and the pH was 7.00 ± 0.02. To prevent titin degradation, the skinning, storage, relaxing, and depolymerization solutions contained protease inhibitors leupeptin (20 µg/ml), aprotinin (5 µg/ml), and pepstatin A (1 µg/ml).Statistical analysis. The data are presented as means ± SE. The results were analyzed statistically by using a one-way ANOVA. Student's t-test was used to estimate differences among means, the acceptable level of significance being set at P < 0.05.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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MHC composition of whole muscles and fiber type identification. A preliminary SDS-PAGE analysis was performed on whole muscles to verify the soleus muscle transformation after 14 days of HU (data not shown). The control soleus muscles (n = 5) were found to express MHC I (69.95 ± 2.90%) and MHC IIa (30.05 ± 2.70%) isoforms. After HU, soleus muscles (n = 8) showed a decrease in MHC I and MHC IIa isoform expressions to 48.56 ± 2.76 and 20.65 ± 1.26% of the total MHC content, respectively. This change in MHC distribution pattern was concomitant with the appearance of fast MHC IId/x (18.57 ± 1.67%) and MHC IIb (12.12 ± 3.33%) isoforms not expressed in control muscles.
Single fibers submitted to the analysis of their passive elastic properties were identified by SDS-PAGE according to their MHC content. All the studied control soleus fibers (n = 13) were found to be slow, expressing only or predominantly MHC I isoform (with a small amount of MHC IIa in the later case). After HU, two fiber populations were identified in the soleus: a population of slow fibers (HU slow, n = 15), which expressed only or predominantly MHC I isoform as described above, and a population of fast fibers (HU fast, n = 13). This fast fiber population included hybrid fast fibers that coexpressed predominantly fast MHC isoforms with minimal MHC I and pure fast fibers containing a mixed proportion of MHC IIa, IId/x, and IIb isoforms. These observed fiber populations have been already described in previous works (23, 26, 29).Titin isoform in rat soleus muscles.
Skeletal titin isoform expression was analyzed in whole soleus muscles
of control (n = 5) and HU (n = 5) rats
(Fig. 2A). Control rat soleus
contained only a single T1 titin band at the top of the gel. After HU,
no difference in titin mobility was found compared with control soleus.
Furthermore, when control and HU samples were coelectrophoresed, titin
bands of the two samples comigrated and revealed no difference in titin
molecular mass between the two samples.
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Passive tension in skeletal muscle fibers.
Preliminary experiments were performed with rabbit soleus and psoas
muscle fibers to reproduce data already described and validate our
experimental procedure. These results are illustrated in the
inset of Fig. 3A.
As the fibers were stretched stepwise beyond their
SLs, passive tension increased exponentially
until the yield sarcomere length (SLy) was
reached. Additional stretches beyond SLy caused
tension to increase further. Rabbit psoas and soleus muscle fibers
displayed different passive tension levels. For psoas muscle fibers,
passive tension increased more steeply as a function of sarcomere
length than for soleus fibers. Thus psoas fibers have a lower
SLy value (3.82 ± 0.07 µm) than soleus fibers (4.40 ± 0.05 µm).
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1) where
L is the fiber length for a given stretch and
Ls the slack fiber length. After HU, both slow
and fast fibers displayed lower passive tension-fiber strain curves
compared with control fibers (Fig. 3B). The exponential
phase of the passive tension-fiber strain curves (fiber strain range
from 0.0 to 0.7) was fitted by an equation described by Elden
(5) to analyze the elastic properties of the tendon:
= E · 
2. In this equation,
describes the passive tension normalized to the cross-sectional
area of the fiber (kN/m2), E is the complex
Young's modulus that reflects the steepness of the curve, and is
the fiber strain (L/Ls 1).
The passive tension-fiber strain curves were analyzed according to this
equation. The analysis indicated that the initial increase in passive
tension of HU fibers rose less steeply than in control fibers, and the effect was more pronounced for the fibers that became fast after HU
(Table 1). However, the slow and fast HU soleus fibers did not show
different yield point values (SLy strain)
compared with the control (Table 1).
Thick-filament depolymerization.
The mechanical properties of the A-band segment of titin were evaluated
by submitting fibers to thick-filament depolymerization. For each
fiber, the depolymerization procedure was assessed by SDS-PAGE
electrophoresis. Because actin is not significantly removed by this
high-salt extraction procedure (12), it was used as a
calibration standard for the densitometric analysis of the MHC content.
For this purpose, after dissection one part of each fiber was directly
stored in Laemli buffer for subsequent densitometric analysis. Thus the
pre- and postdepolymerization MHC-actin ratio were compared for each
group (control or HU). This ratio permitted the evaluation of the
degree of depolymerization (Table 2). For control and HU fiber groups, a homogeneous depolymerization of the
A-band of 53-55% was obtained. Passive tension levels of control soleus fibers (Fig. 4A) were
smaller after KCl depolymerization and increased less steeply with
fiber strain than in pretreated fibers, as shown by the lower complex
Young's modulus value found after KCl treatment (Table 2). Similar
results were obtained on the slow and fast soleus fibers after HU (Fig.
4, B and C, respectively). These findings
suggested no change in titin filament length and/or extensibility in
the A-band segment.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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In this work, we investigated the effect of HU on the passive elastic properties of rat soleus muscle fibers, which have been shown by several authors to be related mainly to titin isoform expression (11, 18, 30, 32). To our knowledge, this is the first study of the changes in passive properties of single muscle fibers in response to muscle atrophy. This study has shown that titin isoform expression of soleus muscle did not change after 14 days of HU. However, HU soleus muscle fibers displayed lower passive tension-fiber strain relationships than control fibers. This indicates that changes in passive tension can occur without changes in titin isoform expression.
MHC and titin expression in rat soleus after unloading. As shown by numerous studies (1, 2, 4, 6, 23, 26), HU of rat soleus muscle induced slow-to-fast transitions in the phenotype of this muscle. These transitions are well illustrated by a decrease in the slow MHC I content concomitant with the appearance of the MHC IIb and IId/x isoforms.
SDS-PAGE analysis revealed that both control and HU soleus muscles expressed only one major titin T1 band. No additional band or degradation was seen. Moreover, this experiment showed that titin T1 band from both control and HU soleus have the same migration level. This assumption is supported also by the coelectrophoresis of control and HU samples, which revealed no difference in titin molecular mass between the two samples. Because we observed pronounced changes in the MHC expression pattern of the soleus muscles after HU, we expected concomitant changes in titin isoform expression in the transformed soleus. However, this was not the case (Fig. 2). Instead, the quantitative densitometric analysis of titin in control and HU soleus muscles revealed that the expression level of titin decreases in the soleus after HU. Thus only the relative quantity of titin changes in rat soleus muscles after HU and not the isoform type.Passive tension in single muscle fibers. The passive tension was found to increase more steeply with sarcomere stretch in rabbit psoas than in rabbit soleus muscles. It resulted in a yield point value (SLy) of 3.82 ± 0.07 µm for psoas fibers and 4.40 ± 0.05 µm for soleus fibers. These SLy values on rabbit muscle fibers are in accordance with those previously found in the literature (9, 11, 17, 33, 34), lending confidence to our experimental procedure.
For control rat soleus fibers, the SLy value deduced from the passive tension curves was 4.11 ± 0.04 µm and is equivalent to the observed yield point of 4.2 µm measured by Linke et al. (17). After HU, slow and fast soleus fibers were found to have the same SLy strain values as control fibers. With the assumption that the SLy value is determined by the titin isoform (9, 11, 15, 17, 33, 34), this result is consistent with the electrophoretic data, which showed no change in titin isoform of soleus muscles after HU. However, compared with control, HU fibers displayed a decrease in passive tension levels and in complex Young's modulus. Indeed, the decrease after HU in muscle fiber stiffness related to the fiber diameter (kN/m2) could result in a reduction in the relative amount of titin protein. Consequently, we also studied the ratio of titin relative to the MHC (Fig. 2B) and found that this ratio is reduced in HU. Therefore, even if the titin/MHC ratio was underestimated in HU animals as MHC content has been shown to decrease after HU (28), it is likely that the decrease in muscle fiber stiffness after HU can be explain by a loss of titin content in soleus after HU. Recently, unloading condition was found to modify the turnover of the protein of the myofilament, as suggested by the increase in the number of short, thin filaments on human soleus muscles after spaceflight (24). This phenomenon may support the idea that HU induced titin filament modifications within the sarcomere and may impair its elastic properties. Under physiological conditions, the titin segment located in the A-band of the sarcomere is anchored to the thick filament and does not contribute to the passive tension generation when sarcomeres are stretched. However, this A-band segment can be recruited after the dislocation of anchorage to the thick filament and thus participated in the passive tension generation (33). Control fibers after KCl depolymerization displayed a decrease in passive tension levels as well as in their complex Young's modulus compared with their tension before treatment. This passive tension drop might result from the extension of an additional titin segment newly recruited from the A-band after depolymerization. After HU, slow and fast posttreated fibers display a decrease in their passive tension levels as well as in their complex Young's modulus similar to the trends in control fibers. This result suggests that the part of titin located in the A-band does not show any modification after HU. In conclusion, this study is the first to investigate titin isoform expression and passive mechanical properties of muscle fibers after HU. Our data suggest that no change occurs in soleus titin isoform expression after HU. However, the decrease in titin-MHC ratio gives rise to a significant decrease in passive tension levels of soleus fibers after HU. Further studies will be required to further analyze the passive mechanical properties of muscles under disuse conditions and elucidate their functional significance.| |
ACKNOWLEDGEMENTS |
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This work was supported by grants from the Centre National d'Etudes Spatiales (CNES, no. 99-3027), the Conseil Regional de la Region Nord Pas-de-Calais (France), and the Fonds Européen de Developpement Economique Regional (FEDER, no. F-007).
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FOOTNOTES |
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Address for reprint requests and other correspondence: L. Stevens, Laboratoire de Plasticité Neuromusculaire, Université des Sciences et Technologies de Lille I, Bat SN4, F-59655 Villeneuve d'Ascq Cedex, France (E-mail: laurence.stevens{at}univ-lille1.fr).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
10.1152/japplphysiol.00621.2001
Received 15 June 2001; accepted in final form 4 December 2001.
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METHODS
RESULTS
DISCUSSION
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) and psoas (
) muscle fibers.
Values are means ± SE. B: passive tension-fiber strain
curves from control, HU slow, and HU fast soleus muscle fibers. Values
are means ± SE.
