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1 Department of Physiology, St. Marianna University School of Medicine, Miyamae, Kawasaki City, Kanagawa 216-8511; 2 School of Health and Sport Sciences, Osaka University, Osaka 560-0043; and 3 Aomori University of Health and Welfare, Aomori 030-8505, Japan
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Responses of the properties of
connectin molecules in the slow-twitch soleus (Sol) and fast-twitch
extensor digitorum longus muscles of rats to 3 days of unloading with
or without 3-day reloading were investigated. The wet weight (relative
to body wt) of Sol, not of extensor digitorum longus, in the unloaded
group was significantly less than in the age-matched control
(P < 0.05). Immunoelectron microscopic analyses showed
that a monoclonal antibody against connectin (SM1) bound to the I-band
region close to the edge of the A band at resting length and moved
reversibly away from the Z line as the muscle fibers were stretched. In
Sol, the displacement of the SM1-bound dense spots in response to
stretching decreased after hindlimb suspension. There were no changes
in the molecular weights and the percent distributions of 
- and
-connectin in both muscles after hindlimb suspension. A significant
increment of percent -connectin in Sol was observed after 3 days of
reloading after hindlimb suspension (P < 0.05). It is
suggested that the elasticity of connectin filaments in the I-band
region of the atrophied Sol fibers was reduced relative to that of the
control fibers. The lack of the elasticity in atrophied muscle fibers may cause a decrease in contractile function.
fast and slow muscles of rat; hindlimb suspension
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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CONNECTIN (TITIN), a giant structural protein with a molecular mass of ~3,000 kDa, is generally considered to be elastic in nature and could account for some of the elastic properties of skeletal muscle fibers (9, 26). The connectin molecule links the thick filament to the Z line and is responsible for positioning of the thick filament at the center of a sarcomere and for generating resting tension after stretching (13, 29, 40). It is reported that the connectin molecule in slow-twitch fibers is larger than that in fast-twitch fibers, and the difference in the elastic properties between slow and fast muscle fibers is related to the difference in connectin molecules (11, 12, 40). However, it is not fully understood how the connectin molecule responds to transformation of fiber phenotype.
It is reported that -connectin (titin 2) is the proteolytic product
of the mother molecule, -connectin (titin 1) (15, 22,
27). The protease, which is responsible for splitting a pure
connectin molecule (-connectin) into -connectin, is partially inhibited by 1 mM E64c (an inhibitor for a thiol protease) or leupeptin
and is thought to be a thiol protease such as calpain (13,
21). However, the physiological role of -connectin is still unclear.
Unloading causes a striking atrophy of skeletal muscle, especially of the antigravity muscle such as the soleus (Sol) (1, 2). Such a morphological adaptation is generally associated with the slow-to-fast transformation of muscle fiber phenotype. Changes in the expression of contractile proteins, such as myosin heavy chain and troponin, in slow-twitch muscle has been reported (1, 30, 31, 34). It is generally considered that muscular atrophy is caused by both the activation of proteolysis and the inhibition of the synthesis of muscular proteins (3, 38). However, it is unclear how the changes in proteolysis caused by unloading and reloading affect the characteristics of connectin. It is also not known how the elasticity of muscle fibers, which may be closely associated with the altered characteristics of connectin, is influenced.
Our laboratory previously reported (39) that the percent
distribution of - and -connectin in Sol was stable after 14 days of hindlimb suspension, although atrophy of muscle fibers was induced.
It is speculated that such phenomena might be related to the phenomenon
that the rate of atrophy or protein breakdown slows at ~14 days,
although a marked loss of muscular protein is induced after only a few
days of hindlimb unloading (2, 3). However, it is still
unclear how the profiles of connectin are influenced when Sol atrophies
at a higher rate. Thus the present study was carried out to examine our
working hypothesis that the profiles of connectin molecules are altered
drastically when the muscle proteins turnover at a higher rate.
Three-day hindlimb suspension followed by 3-day reloading, which may
cause muscle fiber damage and change in connectin profiles, was
performed in rats. The response of muscle fiber elasticity to unloading
and/or reloading was also investigated.
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Animals and treatments. This study was performed following the Guiding Principles for the Care and Use of Animals Approved by the Council of the Physiological Society of Japan. Male Wistar rats, 10 wk of age, were used. Rats were randomly divided into three groups: 1) control group (n = 5), 2) hindlimb-suspended group (n = 5) subjected to 3 days of hindlimb suspension, and 3) recovery group (n = 5) subjected to 3 days of hindlimb suspension followed by 3 days of ambulation recovery. Rats were anesthetized with pentobarbital sodium (5 mg/100 g body wt ip) and killed by decapitation. Immediately after decapitation, the Sol and extensor digitorum longus (EDL) muscles were dissected and weighed.
A portion of each muscle (cut cross sectionally) was solubilized in 3 ml of SDS-DTT buffer consisting of 5 mM ethylenediaminetetraacetic acid, 10% SDS, 50 mM DTT, and 0.1 M Tris · HCl (pH 8.8), boiled for 3 min, and clarified by centrifugation for 20 min at 13,000 g at 20°C (19, 28). Then, the supernatant was mixed with 10 µl of 50% glycerol solution (50% glycerol, 0.1% bromophenol blue) at a 1:1 ratio and used for SDS-PAGE. For immunoelectron microscopic study, single muscle fibers were dissected from each muscle in relaxing solution, which consisted of 10 mM EGTA, 3.5 mM MgATP, 15 mM phosphocreatine, 0.3 mM DTT, 1.5 mM Mg2+, and 20 mM piperazine-N,N'-bis(2-ethanesulfonic acid) (PIPES) with pH 7.0 at 20°C. The ionic strength was adjusted to 0.2 M with potassium methansulfonate.SDS-PAGE.
SDS-PAGE was carried out by using 3-6% polyacrylamide
[bisacrylamide/acrylamide, 1:20 (wt/wt)] slab gel (60 × 85 × 1 mm) containing 0.5% SDS at a constant current (10 mA) for 60 min,
as was described by Itoh et al. (17). The proteins on the
gels were visualized by silver staining with Bio-Rad Silver Stain Plus
(Bio-Rad, Hercules, CA) and were analyzed by using NIH Image software
(National Institutes of Health). The molecular weights of - and
-connectin were estimated by the densitometric scanning of the bands.
Immunoelectron microscopy. A single muscle fiber, dissected from each muscle, was tied to a platinum bar and treated with a skinning solution consisted of 10 mM EGTA, 3.5 mM MgATP, 1.5 mM Mg2+, 20 mM PIPES, and 1% (vol/vol) Triton X-100 with pH 7.0 (20°C). The skinned single fiber was fixed to a platinum bar at different sarcomere lengths by using laser diffraction patterns. After the skinning procedure, muscle fibers were fixed with formaldehyde and treated with a monoclonal antibody (SM1) (14, 17) for connectin for 12 h at 4°C. The SM1 was kindly donated by Dr. K. Maruyama, the President of Chiba University. Although it has been reported that SM1, which is a monoclonal antibody against connectin, was obtained by using crude human myosin as the antigen, it turned out that SM1 specifically reacts with connectin among myofibrillar protein (17, 33). The specificity of SM1 has been investigated in skeletal muscles (14).
After antibody treatment, fibers were washed with phosphate buffer (0.15 M NaCl, 20 mM NaPO4, 0.1% NaN3, pH 7.2), and treated with anti-mouse IgG for 12 h at 4°C. Then, fibers were washed with phosphate buffer and finally fixed with OsO4 in 100 mM phosphate buffer (9, 10, 17, 29). Postfixed fibers were dehydrated at room temperature and embedded in Epon 812. Thin sections of the embedded fibers were cut on the microtome and then observed under a JOEL 1200EX electron microscope (Nihon Denshi, Kyoto, Japan). The minimum distance between the edge (close to the Z line) of the SM1 binding site and the edge (close to the A band) of Z line (Z-S distance) in the sarcomere was measured on the electronmicrographs at the magnifications of ×5,000 and ×10,000.Statistical analysis. All values are expresses as means ± SD. Statistical significance was analyzed by using analysis of variance followed by Scheffé's post hoc test. The significance was accepted at P < 0.05.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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After the 3 days of hindlimb suspension, the wet weight of Sol
relative to body weight was significantly less than that in the
age-matched control (Table 1,
P < 0.05). However, the weight of EDL was not
different between two groups.
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In both Sol (Fig. 1) and EDL (Fig.
2), the SM1 bound to the
I-band region close to the edges of the A band at resting length. At
resting fiber length, there was no change in the distance between the
binding site of SM1 and the Z line (Z-S distance) for both muscles
after 3 days of hindlimb suspension. As the muscle fibers were
stretched, the Z-S distance was extended. In Sol, the magnitude of
displacement of the SM1-bound dense spots from the Z line (Z-S distance) in response to stretching decreased after hindlimb suspension (Figs. 1 and 3). According to the
analyses of the relationship between Z-S distance and the half
sarcomere length, the extension of half sarcomere length by 100 nm
caused the extension of Z-S distance by 47 nm in the control and by 35 nm in the hindlimb-suspended group, respectively. The Z-S-to-half
sarcomere length ratio of the control Sol (0.34 ± 0.02, n = 37) was significantly greater than that of
suspended Sol (0.28 ± 0.02, n = 53, P < 0.05). These results indicate that the region of
Z-S in suspended Sol was less extensible than that in the control Sol.
However, hindlimb suspension had no effects on Z-S distance in response
to stretching of EDL fibers (Fig. 4).
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Figure 5 illustrates the representative
SDS-PAGE pattern of connectin molecules. Connectin molecules in both
EDL and Sol displayed double connectin bands. It has been considered
that the upper connectin band is -connectin and the lower one is
-connectin. A subtle difference in the mobility of - and
-connectin was observed between fast EDL and slow Sol. However, the
molecular weights of - and -connectin, estimated from the
mobility, in both muscles did not change after unloading and/or
reloading.
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Figure 6 showed the percent composition
of connectin molecules in each group. There were no changes in the
percent compositions of - and -connectin in both muscles after
hindlimb suspension. However, a significant increment of -connectin,
associated with an insignificant decrease of -connectin, was
observed in Sol after 3 days of ambulation recovery from hindlimb
suspension (P < 0.05). In EDL, there was no
significant change in the composition of - and -connectin
molecules after hindlimb suspension and ambulation recovery.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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In a muscle sarcomere, connectin molecules span from the M line to the Z line and anchor the thick filament to the Z line. Connectin molecule in skeletal muscle contains three segments [tandem immunoglobulin (Ig), N2-A, and one that, which is rich in proline, glutamate, valine, and lysine residues (PEVK)] in the I-band region (25). It has been considered that the extensibility of the I-band region is mainly dependent on the PEVK segment and Ig-like domain (tandem Ig domain), which is serially linked to PEVK segment (12, 25, 26). The elastic nature of a connectin molecule is dependent on the I-band region in physiological condition. When the sarcomeres are stretched, tandem Ig segments are first straightened with little increase in tension. Further extension leads to unfolding of the PEVK segment, which is folded at the resting sarcomere length (12). In addition, the extensible region of the N2-A (4 Ig domains and a 106-residue unique sequence) or the N2-B element (3 Ig domains and a 572-residue unique sequence) is found in Z-line-linked tandem Ig domain in skeletal and cardiac muscles (25).
The connectin molecule in slow-twitch fibers is larger than that in
fast-twitch fibers, and the difference in the elastic properties
between slow and fast muscle fibers is related to the difference in
connectin molecules (11, 12, 40). Greater mobility of -
and -connectin was observed in fast muscle compared with slow
muscle, as was reported elsewhere (11, 39). It is suggested that the large differences in resting tension between Sol and
EDL may be due to the different molecular size of each connectin
(11, 12). It has been reported that muscles that express
larger connectin isoforms tend to initiate passive tension at a longer
sarcomere length, and therefore, the passive tension development at a
certain sarcomere length is less than that in muscles with smaller
connectin (40), suggesting that slow muscle is more
elastic than fast muscle.
It has been reported that a monoclonal antibody for connectin, SM1, binds to the I-band region ~0.3 and 0.1 µm away from the Z line and the edges of the A band, respectively, at a resting sarcomere length of ~2.4 µm (12). In the present study, SM1 also bound to the I-band region ~0.3 µm away from the Z line at resting sarcomere length in the control and suspended Sol. However, the extensibility of the I-band region from the Z line to SM1 binding site (Z-S distance) in Sol, but not in EDL, decreased after hindlimb suspension.
Recently, it has been reported that hindlimb unloading caused a
decrease in the content of connectin protein (37) and that the sizes of - and -connectin and connectin antibody localization were altered (18). These observations suggest that
connectin in atrophied muscle may have some alterations in the
molecular composition. However, none of the molecular weights,
estimated from the mobility in the electrophoresis, and the percent
distributions of - and -connectin in the unloaded group were
different from those in the age-matched control. Kasper and Xun
(18) and Toursel et al. (37) also observed
that 14 days of hindlimb unloading had no effect on the expression of
connectin molecules.
In atrophied Sol, the decrease in contractile protein contents (1-3), the depression of the isometric force generation (1, 41-43), Ca2+ sensitivity of myofilaments (41-43), and the increment of both maximal shortening velocities (41-43) are observed. The expressions of contractile proteins (1, 4, 30, 31, 34), regulatory proteins (4), sarcoplasmic reticulum Ca2+-pump protein (32), and metabolic proteins (5, 8, 44) are shifted from slow to fast type in slow-twitch muscles after unloading. In the present study, however, unloading by hindlimb suspension did not induce any change in the expression of connectin molecules. These observations suggest that the regulation system of the expression of muscular elastic protein might be different from that of other muscular proteins.
-Connectin is considered to be easily degraded into -connectin
and a 1,200-kDa subfragment (20, 35). This degradation of
-connectin molecule is induced by the binding of Ca2+ to
-connectin (35) and/or calpain (20).
Increased intracellular Ca2+ concentration may activate
calpain, and then -connectin may be degraded to -connectin. In
the present study, however, the percent composition of - and
-connectin did not change after hindlimb suspension. These
observations suggest that the proteolysis by calpain may not be
activated in the atrophied muscles. Muscular atrophy, in the present
study, may be induced by a non-Ca2+-activated proteolysis
system, such as ubiquitin-proteasome and/or by the decreased synthesis
of structural proteins.
Fiber damage is induced in response to reloading after unloading
(6, 7, 23, 24, 36). Eccentric contraction-like lesions,
such as an abnormal widening of sarcomeres with A-band disruption and
excessively wavy and/or extracted Z line, are reported (23,
24). The reloading after unloading caused an increased percentage of -connectin in Sol but not in EDL. These observations suggest that the reloading on atrophied muscle may activate
proteolysis, associated with calpain, for example, and then
-connectin may be degraded to -connectin. It has been reported
that 1 day of reloading after 14 days of hindlimb suspension increased
the resting intracellular Ca2+ concentration by 24%
(16).
Recently, Farges et al. (6) reported that increased
cathepsin B activity and mRNA encoding cathepsin B, L, H, and C were observed in rat gastrocnemius muscle at 48 h after traumatic
injury, suggesting that muscle proteolysis by inflammatory cells after local trauma appears to be the major participant in protein catabolism. It was also studied whether inflammatory cell concentrations correlate with muscle impairment during reloading periods after 10 days of
hindlimb suspension of rats (7, 36). For example, the density of neutrophils and ED1+ macrophages was
significantly increased by 16.5- and 9.8-fold, respectively, after
1 day of reloading, although ED2+ macrophage concentration
was not increased until 3 days of reloading. Thus it is suggested that
the digestion of necrotic fibers by macrophages may also influence the
degradation of connectin. However, the precise mechanism responsible
for the elevation of -connectin expression by reloading is still
unclear, because the changes in the ultrastructure and the permeability
of plasma membranes were not investigated in the present study. The
increase in the percent of -connectin after reloading also suggests
that the elasticity in reloaded Sol may be altered. However, the role
of -connectin molecule in a living skeletal muscle cell is still unknown.
Higuchi (9) reported that the disordering of the regular structure in a sarcomere was induced by the digestion of connectin and caused depression of the active force generation. The function of connectin is to keep the position of the thick filaments at the center of a sarcomere (26). One of the causes for the decrease in force generation after unloading may be related to the changes in the elastic properties of connectin filaments. However, it is still unclear how the decreased elasticity in the I-band region affects the contractile properties of muscles.
In conclusion, the elasticity of connectin filaments in the I-band
region of atrophied Sol fibers was reduced after 3 days of hindlimb
suspension. But the molecular weights or percent distributions of -
and -connectin were not affected, although degradation of - to
-connectin was noted after 3 days of reloading. It is also unknown
whether the properties of PEVK and/or tandem Ig segments were altered
or not. Thus the mechanism responsible for the reduction of elasticity
in atrophied muscle fibers is still unclear. The decreased elasticity
in atrophied muscle fibers may, in part, play a role in the decrement
of contractile function.
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ACKNOWLEDGEMENTS |
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The authors thank Drs. K. Maruyama, and S. Kimura from Department of Biology, Faculty of Science, Chiba University, for supplying the SM1 antibody and technical assistance to this study.
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FOOTNOTES |
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This study was supported, in part, by a grant from Japan Space Forum (to T. Yoshioka, K. Goto, and Y. Ohira) and a Grant-in-Aid for Encouragement of Young Scientists from Japan Society for the Promotion of Science (to K. Goto).
Address for reprint requests and other correspondence: Y. Ohira, School of Health and Sport Sciences, Osaka Univ., Toyonaka City, Osaka 560-0043, Japan (E-mail: ohira{at}space.hss.osaka-u.ac.jp).
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.
First published October 11, 2002;10.1152/japplphysiol.00408.2002
Received 10 May 2002; accepted in final form 3 September 2002.
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REFERENCES |
|---|
|
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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|---|
1.
Baldwin, KM.
Effects of altered loading states on muscle plasticity: what have we learned from rodents?
Med Sci Sports Exerc
28:
S101-S106,
1996.
2.
Booth, FW.
Time course of muscular atrophy during immobilization of hindlimbs in rats.
J Appl Physiol
43:
656-661,
1977.
3.
Booth, FW.
Effect of limb immobilization on skeletal muscle.
J Appl Physiol
52:
1113-1118,
1982.
4.
Campione, M,
Ausoni S,
Guezennec CY,
and
Schiaffino S.
Myosin and troponin changes in rat soleus muscle after hindlimb suspension.
J Appl Physiol
74:
1156-1160,
1993.
5.
Chi, MMY,
Choksi R,
Nemeth P,
Krasnov I,
Ilyina-Kakueva E,
Manchester JK,
and
Lowry OH.
Effects of microgravity and tail suspension on enzyme of individual soleus and tibialis anterior fibers.
J Appl Physiol
43:
66-73,
1992.
6.
Farges, MC,
Balcerzak D,
Fisher BD,
Attaix D,
Bechet D,
Ferrara M,
and
Baracos VE.
Increased muscle proteolysis after local trauma mainly reflects macrophage-associated lysosomal proteolysis.
Am J Physiol Endocrinol Metab
282:
E326-E335,
2002.
7.
Frenette, J,
St-Pierre M,
Cote CH,
Mylona E,
and
Pizza FX.
Muscle impairment occurs rapidly and precedes inflammatory cell accumulation after mechanical loading.
Am J Physiol Regul Integr Comp Physiol
282:
R351-R357,
2002.
8.
Grichko, VP,
Heywood-Cooksey A,
Kidd KR,
and
Fitts RH.
Substrate profile in rat soleus muscle fibers after hindlimb unloading and fatigue.
J Appl Physiol
88:
473-478,
2000.
9.
Higuchi, H.
Changes in contractile properties with selective digestion of connectin (titin) in skinned fibers of frog skeletal muscle.
J Biol Chem
111:
291-295,
1992.
10.
Higuchi, H,
Suzuki T,
Kimura S,
Yoshioka T,
Maruyama K,
and
Umazume Y.
Localization and elesticity of connectin (titin) filaments in skinned frog muscle fibres subjected to partial depolymerization of thick filaments.
J Muscle Res Cell Motil
13:
285-294,
1992.
11.
Horowits, R.
Passive force generation and titin isoforms in mammalian skeletal muscle.
Biophys J
61:
392-398,
1992.
12.
Horowits, R.
The physiological role of titin in striated muscle.
Rev Physiol Biochem Pharmacol
138:
57-96,
1999.
13.
Horowitz, R,
Kempner ES,
Bisher ME,
and
Podolsky RJ.
A physiological role for titin and nebulin in skeletal muscle.
Nature
323:
160-164,
1986.
14.
Horowits, R,
Maruyama K,
and
Podolsky RJ.
Elastic behavior of connectin filaments during thick filament movement in activated skeletal muscle.
J Cell Biol
109:
2169-2176,
1989.
15.
Hu, DH,
Kimura S,
Kawashima S,
and
Maruyama K.
Calcium activated neutral protease quickly converts -connectin to -connectin.
Zool Sci
6:
797-800,
1989.
16.
Ingalls, CP,
Warren GL,
and
Armstrong RB.
Intracellular Ca2+ transients in mouse soleus muscle after hindlimb unloading and reloading.
J Appl Physiol
87:
386-390,
1999.
17.
Itoh, Y,
Suzuki T,
Kimura S,
Ohashi K,
Higuchi H,
Sawada H,
Shimizu T,
Shibata M,
and
Maruyama K.
Extensible and less-extensible domains of connectin filaments in stretched vertebrate skeletal muscle sarcomeres as detected by immunofluorescence and immunoelectron microscopy using monoclonal antibodies.
J Biochem (Tokyo)
104:
504-508,
1988.
18.
Kasper, CE,
and
Xun L.
Expression of titin in skeletal muscle varies with hind-limb unloading.
Biol Res Nurs
2:
107-115,
2000.
19.
Kawamura, Y,
Ohtani Y,
and
Maruyama K.
Biodiversity of the localization of the epitopes to connectin antibodies in the sarcomeres of lamprey, electric ray, and horce mackerel skeletal muscles.
Tissue Cell
26:
677-685,
1994.
20.
Kim, K,
Homma Y,
Ikeuchi Y,
and
Suzuki A.
Effect of high hydrostatic pressure on the conversion of -connectin to -connectin.
J Biochem (Tokyo)
114:
463-467,
1993.
21.
Kimura, S,
Maki S,
and
Maruyama K.
The role of a thiol protease in the proteolysis of connectin in rabbit skeletal muscle myofibrils.
Biomed Res (Tokyo) 14, Suppl
2:
89-92,
1993.
22.
Kimura, S,
Matsuura T,
Ohtsuka S,
Nakauchi Y,
Matsuno A,
and
Maruyama K.
Characterization of localization of -connectin (titin 1): an elastic protein isolated from rabbit skeletal muscle.
J Muscle Res Cell Motil
13:
39-47,
1992.
23.
Krippendorf, BB,
and
Riley DA.
Distinguishing unloading versus reloading-induced changes in rat soleus muscle.
Muscle Nerve
16:
99-108,
1993.
24.
Krippendorf, BB,
and
Riley DA.
Temporal changes in sarcomere lesions of rat adductor longus muscles during hindlimb reloading.
Anat Rec
238:
304-310,
1994.
25.
Labeit, S,
and
Kolmerer B.
Titin: giants proteins in charge of muscle ultrastructure and elasticity.
Science
270:
293-296,
1995.
26.
Maruyama, K.
Connectin/titin, giant elastic protein of muscle.
FASEB J
11:
341-345,
1997.
27.
Maruyama, K.
Comparative aspects of muscle elastic proteins.
Rev Physiol Biochem Pharmacol
138:
1-18,
1999.
28.
Maruyama, K,
Matsuno A,
Higuchi H,
Shimaoka S,
Kimura S,
and
Shimizu T.
Behaviour of connectin (titin) and nebulin in skinned muscle fibres released after extreme stretch as revealed by immunoelectron microscopy.
J Muscle Res Cell Motil
10:
350-359,
1989.
29.
Maruyama, K,
Yoshioka T,
Higuchi H,
Ohashi K,
Kimura S,
and
Natori R.
Connectin filaments link thick filaments and Z-line in frog skeletal muscles as revealed by immunoelectron microscopy.
J Cell Biol
101:
2167-2172,
1985.
30.
Ohira, Y,
Yoshinaga T,
Nonaka I,
Ohara M,
Yoshioka T,
Yamashita-Goto K,
Izumi R,
Yasukawa K,
Sekiguchi C,
Shenkman BS,
and
Kozlovskaya IB.
Histochemical responses of human soleus muscle fibers to long-term bedrest with or without countermeasure.
Jpn J Physiol
50:
41-47,
2000.
31.
Ohira, Y,
Yoshinaga T,
Ohara M,
Nonaka I,
Yoshioka T,
Yamashita-Goto K,
Shenkman BS,
Kozlovskaya IB,
Roy RR,
and
Edgerton VR.
Myonuclear domain and myosin phenotype in human soleus after bed rest with or without loading.
J Appl Physiol
87:
1776-1785,
1999.
32.
Peters, DG,
Mitchel-Felton H,
and
Kandarian SC.
Unloading induces transcriptional activation of the sarco(endo)plasmic reticulum Ca2+-ATPase 1 gene in muscle.
Am J Physiol Cell Physiol
276:
C1218-C1225,
1999.
33.
Shimizu, T,
Matsumura K,
Itoh Y,
Mannen T,
and
Maruyama K.
An immunological homology between neurofilament and muscle elastic filament: a monoclonal antibody cross-reacts with neurofilament subunits and connectin.
Biomed Res (Tokyo)
9:
227-233,
1988.
34.
Stevens, L,
Sultan KR,
Peuker H,
Gohlsch B,
Mounier Y,
and
Pette D.
Time-dependent changes in myosin heavy chain mRNA and protein isoforms in unloaded soleus muscle of rat.
Am J Physiol Cell Physiol
277:
C1044-C1049,
1999.
35.
Takahashi, K,
Hattori A,
Tatsumi R,
and
Takai K.
Calcium-induced spilitting of connectin filaments into -connectin and 1,200-kDa subfragment.
J Biochem (Tokyo)
111:
778-782,
1992.
36.
Tidball, JG,
Berchenko E,
and
Frenette J.
Macrophage invasion does not contribute to muscle membrane injury during inflammation.
J Leukoc Biol
65:
492-498,
1999.
37.
Toursel, T,
Stevens L,
Granzier H,
and
Mounier Y.
Passive tension of rat skeletal soleus muscle fibers: effects of unloading conditions.
J Appl Physiol
92:
1465-1472,
2002.
38.
Tucker, KR,
Seider MJ,
and
Booth FW.
Protein synthesis rates in atrophied gastrocnemius muscles after limb immobilization.
J Appl Physiol
51:
73-77,
1981.
39.
Uchida, H,
Fujita K,
Yamashita-Goto K,
and
Yoshioka T.
Muscular factors on the elasticity of skeletal muscles in rats.
Jpn J Phys Fitness Sports Med
46:
635,
1997.
40.
Wang, K,
McCarter R,
Wright J,
Beverly J,
and
Ramirez-Mitchell R.
Regulation of skeletal muscle stiffness and elasticity by titin isoforms: A test of the segmental extension model of resting tension.
Proc Natl Acad Sci USA
88:
7101-7105,
1991.
41.
Widrick, JJ,
Knuth ST,
Norenberg KM,
Romatowski JG,
Bain JLW,
Riley DA,
Karhanek M,
Trappe SW,
Trappe TA,
Costill DL,
and
Fitts RH.
Effect of a 17 day spaceflight on contractile properties of human soleus muscle fibres.
J Physiol
516:
915-930,
1999.
42.
Yamashita, K,
and
Yoshioka T.
Shortening velocity and calcium sensitivity of single fibers from hinlimb suspended muscle in rats.
Jpn J Aerospace Environ Med
30:
71-80,
1993.
43.
Yamashita-Goto, K,
Okuyama R,
Honda M,
Kawasaki K,
Fujita K,
Yamada T,
Nonaka I,
Ohira Y,
and
Yoshioka T.
Maximal and submaximal forces of slow fibers in human soleus after bed rest.
J Appl Physiol
91:
417-424,
2001.
44.
Yoshioka, T,
Takekura H,
and
Yamashita K.
Effect of endurance training on disuse muscle atrophy induced by body suspension in rats. A structural and biochemical study.
Med Sport Sci
37:
150-161,
1992.
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