Skip Navigation LinksHome > January 1996 - Volume 28 - Issue 1 > Dystrophin, vinculin, and aciculin in skeletal muscle subjec...
Medicine & Science in Sports & Exercise:
Basic Sciences/Regulartory Physiology: Original Investigations

Dystrophin, vinculin, and aciculin in skeletal muscle subject to chronic use and disuse

REZVANI, MOJGAN; ORNATSKY, OLGA I.; CONNOR, MICHAEL K.; EISENBERG, HERBERT A.; HOOD, DAVID A.

Free Access
Article Outline
Collapse Box

Author Information

Department of Biology and School of Physical Education, York University, North York, Ontario, CANADA M3J 1P3

Submitted for publication January 1995.

Accepted for publication June 1995.

We are grateful to Dr. R.G. Worton, Genetics Dept., The Hospital for Sick Children, Toronto, Canada, for the original donation of a dystrophin antibody, to M.A. Glukhova, currently at the Laboratoire de Physiopathologie du Développement, Ecole Normale Supérieure, Paris, France, for the donation of anti-vinculin/M-vinculin VIIF9 monoclonal antibodies, and to Dr. A. Belkin, Dept. of Cell Biology and Anatomy, University of North Carolina at Chapel Hill, USA, for providing the anti-aciculin 60/63 kDa XIVF8 monoclonal antibody. This work was supported by the Natural Sciences and Engineering Research Council of Canada, the Canadian Space Agency, and the Heart and Stroke Foundation of Ontario.

Address for correspondence: Dr. David A. Hood, Department of Biology, York University, 4700 Keele St., North York, Ont., Canada M3J 1P3.

Collapse Box

Abstract

Dystrophin is a subsarcolemmal protein that interacts with cytoskeletal actin and a glycoprotein complex in the plasma membrane. One potential function of dystrophin is its ability to stabilize the sarcolemmal membrane during muscle contraction. We hypothesized 1) that chronic muscle use and disuse would alter the expression of dystrophin as a compensatory mechanism designed to prevent muscle damage, and 2) that other subsarcolemmal cytoskeletal proteins (vinculin, M-vinculin, aciculin 60/63 kDa) that colocalize with dystrophin in muscle adherens junctions would be changed in parallel. Chronic muscle use induced by voluntary running or 10-Hz chronic stimulation did not alter dystrophin levels in rat muscle. In contrast, muscle disuse induced by 6 d of microgravity, or 7 and 21 d of denervation, increased dystrophin levels by 1.8-, 1.9- and 3.2-fold, respectively. Thus, this increase in dystrophin levels appears to be dependent on the duration of muscle disuse, independent of the presence of the nerve. Denervation also induced 3.3-fold increases in vinculin and aciculin 60 kDa, in parallel with dystrophin. However, in contrast to its effects on dystrophin, chronic stimulation increased the levels of vinculin and aciculin 60 kDa by 3.4- and 6.4-fold, respectively. Thus, both the removal and the augmentation of muscle activity resulted in increases of these two cytoskeletal proteins. The data indicate that the concentrations of these proteins are independently regulated. They further indicate that chronic muscle use is not a stimulus for the induction of dystrophin levels, suggesting that normal levels are sufficient for the protective effect on the sarcolemma that dystrophin may confer. The results reveal an interesting area of muscle plasticity, and the adaptation observed may have profound implications for the structure and function of skeletal muscle responding to changes in contractile activity.

Dystrophin is a large protein of 427 kDa that is expressed at its highest level in normal skeletal muscle (18). This protein is altered or absent in skeletal muscle of patients with Becker and Duchenne muscular dystrophies, leading to progressive skeletal muscle deterioration. Dystrophin is localized at the cytoplasmic surface of the subsarcolemmal membrane of skeletal muscle fibers, and in conjugation with surface glycoproteins, forms a scaffold thought to play an important role in maintaining skeletal muscle architecture and the integrity of the sarcolemma between the contractile apparatus and the extracellular matrix(6). Skeletal muscle possesses extensive and highly specialized subsarcolemmal adherens junctions, such as neuromuscular and myotendinous junctions, as well as costameres which are myofibril-to-sarcolemma attachment sites. These junctions represent membrane-microfilament contact zones that appear to be involved in the uniform transmission of contraction forces, as well as the lateral association of myofibrils with the sarcolemma (31). Several proteins of adherens junctions, namely vinculin, meta-vinculin, talin, aciculin,α-actinin, and integrin(s), are found in skeletal muscle and appear to mediate a linkage between actin filaments and the plasma membrane(1,2,7,9). Immunofluorescent studies have also localized dystrophin to costameres, of which vinculin is an ubiquitous marker (28). Aciculin, a newly identified cytoskeletal component of adherens junctions, is particularly enriched in the myotendinous junction (1,2), where dystrophin is also found (3). Thus, the cytoskeletal proteins dystrophin, vinculin and aciculin appear to be intimately related to the maintenance of adherens junctions in skeletal muscle.

The effects of chronic muscle use and disuse on the muscle phenotype has been well established for myofibrillar proteins and Z-line proteins(26,30), as well as those involved in the function of the sarcoplasmic reticulum and in energy metabolism(13,14,27). Less well established are the effects of chronic muscle use and disuse on structural proteins such as those of the cytoskeleton. In the mdx mouse, an animal model in which dystrophin is lacking in skeletal muscle, a chronic functional overload results in muscle deterioration (4,22) and an increased susceptibility to contraction-induced sarcolemmal rupture(25). Thus, it seems reasonable to hypothesize that chronic exercise of normal muscle possessing dystrophin might result in the induction of this protein as a compensatory mechanism designed to subvert muscle damage. The present study was designed to evaluate changes in the levels of dystrophin and other related cytoskeletal proteins (vinculin and aciculin) in different models of skeletal muscle use and disuse.

Back to Top | Article Outline

METHODS

Animals

Male Sprague-Dawley rats (Charles River, Canada) were used. They were housed individually with a 12:12-h light-dark cycle. All procedures used were in accordance with the guiding principles in the care and use of animals of the Canadian Council on Animal Care, and the American College of Sports Medicine.

Back to Top | Article Outline
Voluntary Running

Individual rats were placed in cages adjoining a running wheel. As found in other studies (29), animals had to be moderately food restricted to attain running distances in which a training effect could be expected. Thus, each runner (R) was matched with a food restricted sedentary(S) animal, as well as a free-eating sedentary (FS) animal (N = 7/group). Animal weight was monitored regularly, and running distances were measured using a revolution counter and converted to km distances attained per day. The animals used in the present study ran an average of 9.6 ± 1.0 km·d-1. At the end of 8 wk, animals were anesthetized and the red gastrocnemius muscle was removed and frozen for further processing. This tissue was selected because it was expected to be recruited during this moderately intense exercise condition.

Back to Top | Article Outline
Chronic Stimulation

The surgical procedure was carried out as described previously(32,33). The left tibialis anterior (TA) muscle(N = 5 rats) was stimulated at 10 Hz, 24 h·d-1. The contralateral muscle served as a nonstimulated control. After 10 d, muscles were excised and frozen as above. Chronic stimulation for this period of time results in an approximate 15% decline in muscle mass(32).

Back to Top | Article Outline
Spaceflight

Frozen forelimb muscles (triceps and biceps brachii) of six rats which were subject to 6 d of microgravity during the spaceflight of the NASA shuttle“Endeavour” in January 1993 were obtained. Identical tissues from control animals (N = 6) subject to normal gravity conditions were also excised simultaneously.

Back to Top | Article Outline
Denervation

The surgical procedure for the induction of denervation was described previously (34). Tibialis anterior muscles were denervated for 7 or 21 d (N = 4-6 rats), after which tissues were removed and frozen. Sham-operated animals served as controls. This treatment period resulted in approximately 36% and 64% declines in muscle mass, respectively (5).

Back to Top | Article Outline
Tissue Sampling and Extraction

Muscle tissues were stored at -80°C. Muscles were subsequently powdered using a stainless steel mortar which was precooled to the temperature of liquid N2. Samples of muscle powder (10-15 mg) were suspended in a 20-fold (w/v) dilution of 0.1 M KH2PO4/Na2PO4 buffer (pH 7.2) containing 2 mM EDTA for the measurement of cytochrome c oxidase activity (12). Muscle powders were also used to generate tissue extracts in the same buffer using a 40-fold dilution(15) for total protein measurements(19) and for application to gradient gels for electrophoresis.

Back to Top | Article Outline
Gradient Gel Electrophoresis

A 3-12% gradient polyacrylamide gel was used for the separation of dystrophin. Extracts of samples containing 150 μg of total protein were combined with an equal volume of sample buffer (10% glycerol (v/v), 2.3% SDS(v/v), 62.5 mM Tris-HCl (pH 6.8), 5% mercaptoethanol (v/v)) containing bromphenol blue, denatured 5 min at 95°C, and applied to the gel. A 4-10% gradient polyacrylamide gel and a 3% stacking gel were used for the separation of aciculin from samples containing 100 μg of total protein. Vinculin was separated on 4-15% gradient polyacrylamide gels with a 3% stacking gel. In this case, 50 μg of total protein/lane were applied to the gel. All separations were achieved using low voltage (40-50 V) overnight.

Back to Top | Article Outline
Immunoblot Analyses

Proteins were transferred from the gel onto Hybond-C Super nitrocellulose membrane (Amersham, Canada) for 1.5-2 h using an ISS semi-dry electroblotter. The transfer buffer used for dystrophin electroblotting was prepared according to Otter et al. (24), while that used for vinculin and aciculin analyses was made according to Harlow and Lane(10). Membranes were incubated with a primary monoclonal antibody directed against dystrophin (donated by Dr. R. G. Worton, or Novocastra NCL-Dys2, Newcastle upon Tyne, U.K.) diluted to 1:300 for 3 h at room temperature. The affinity-purified monoclonal antibody specific for aciculin 60/63 kDa (XIVF8, Ref. 1) was diluted to 1:200, and incubated with the membrane for 2 h at room temperature. Vinculin and meta-vinculin (M-vinculin) were detected by using a hybridoma supernate(VIIF9) at room temperature for 2 h as well. Primary antibodies were revealed with sheep anti-mouse IgG alkaline phosphatase-coupled secondary antibody(Sigma, St. Louis) diluted to 1:1000. The reaction was detected using a 5-15 min incubation with nitro-blue-tetrazolium and 5-bromo-4-chloro-3-indolyl phosphate. Incubation times were chosen such that signals were within the linear range of the laser densitometry detection system (Zeineh SL-504-XL, Fullerton, CA). Scanning was performed using a vertical line through the midpoint of the sample signal. Relative values were expressed as the ratio of treated samples over control.

Back to Top | Article Outline
Statistics

Absolute values of integration peaks obtained via laser densitometry were compared using Student's t-test for paired or unpaired samples, as appropriate. All values are reported as means ± SEM, and values in brackets in the tables refer to the number of animals analyzed.

Back to Top | Article Outline

RESULTS

The effects of the two chronic muscle use and disuse models on cytochrome c oxidase activity are illustrated in Table 1. As expected, 10 d of chronic stimulation was much more effective than voluntary locomotion for 8 wk in producing adaptive changes within the muscle. Of the muscle disuse models, denervation for 21 d led to a slightly greater reduction in mitochondrial content compared to 6 d of microgravity conditions. This analysis was performed to indicate the extent of the adaptive changes evident in the muscles under the experimental situations employed, as done previously(5,16,34).

Table 1
Table 1
Image Tools

The protein levels of dystrophin, vinculin and aciculin are shown as representative blots in Figs. 1-4, and quantified as a larger sample size in Table 2. Dystrophin levels were not altered by voluntary running (Fig. 1). The ratio of dystrophin levels in muscle of running animals relative to sedentary weight matched controls was 1.59 ± 0.63 (N = 7). The greater stimulus of chronic stimulation also resulted in no significant change in dystrophin levels (Fig. 2, Table 2). In contrast, muscle disuse imposed by microgravity conditions resulted in values which were 1.82 ± 0.21-fold (N = 6) above those in control animals (P < 0.05; Fig. 3). Denervation (21 d) led to a greater than three-fold increase in dystrophin levels within the muscle (Fig. 4, Table 2). Because the two muscle disuse models were divergent in duration (6 vs 21 d) and with respect to the presence (microgravity) or absence (denervation) of the nerve, we subsequently investigated dystrophin levels in 7-d denervated muscle, which approximated the duration of the microgravity condition. Dystrophin levels were increased 1.9 ±0.2 fold (N = 4; P < 0.05, immunoblot not shown) under these conditions, similar to the results of the microgravity treatment.

Table 2
Table 2
Image Tools
Figure 1-Immunoblot ...
Figure 1-Immunoblot ...
Image Tools
Figure 2-Immunoblot ...
Figure 2-Immunoblot ...
Image Tools
Figure 3-Immunoblot ...
Figure 3-Immunoblot ...
Image Tools
Figure 4-Immunoblot ...
Figure 4-Immunoblot ...
Image Tools

Two distinct cytoskeletal proteins are detectable on the blots probed with the vinculin antibody. These are the closely related proteins M-vinculin (150 kDa) and vinculin (130 kDa). Vinculin levels were markedly increased by both chronic stimulation and denervation to values which were greater than three-fold above nontreated control levels. Changes in vinculin levels appear to occur partly at the expense of reductions in M-vinculin levels, since these decreased by approximately 25-50% as a result of these treatments(Figs. 2 and 4, Table 2)

Aciculin exists in two different isoforms with relative molecular weights of 63 kDa and 60 kDa. Aciculin 60 kDa was markedly increased to six-fold higher levels in stimulated as compared with control tibialis anterior muscles. In contrast, aciculin 63 kDa levels were unchanged in stimulated as compared to control muscles (Fig. 2). This latter protein was not detectable in 21 d denervated muscles, but a 3.3-fold increase in aciculin 60 kDa was observed in this condition of muscle disuse(Fig. 4, Table 2).

Back to Top | Article Outline

DISCUSSION

The purpose of this study was to investigate the adaptability of cytoskeletal proteins in skeletal muscle subject to conditions of chronic muscle use or disuse. While much attention has been focused on changes in proteins of the myofibrils, sarcoplasmic reticulum, and mitochondria (for reviews, see (13,14,26,27), little is known regarding alterations in the gene expression of muscle cell structural proteins under conditions of altered muscle contractile activity. The cytoskeletal proteins chosen for the present work appear to be intimately associated, and are involved in the maintenance of subsarcolemmal adherens junctions in muscle cells (7). For example, dystrophin colocalizes with β-spectrin (28) and its N-terminal end binds F-actin (20) in subsarcolemmal domains within muscle cells. Vinculin is also present in the same structural complexes as dystrophin and β-spectrin (28). The C-terminus of dystrophin appears to be attached to a large sarcolemmal oligomeric complex consisting mainly of glycoproteins, called the dystrophin-glycoprotein complex(21). This complex acts as a link between intracellular proteins such as actin, and extracellular matrix proteins such as laminin(6). This lattice of proteins may serve to stabilize the plasma membrane during muscle contraction (20). Aciculin is a newly discovered protein of adherens junctions, and its role within muscle is unknown. However, it appears to be concentrated in similar areas as dystrophin, and it also interacts with actin filaments(1,2). Because these proteins colocalize at adherens junctions, it was hypothesized that levels of these may change similarly under conditions of muscle adaptation. Our results reveal that this was not the case. For example, while dystrophin was unaltered under conditions of chronic muscle use, both aciculin and vinculin were markedly increased by contractile activity. However, they did not increase in parallel, indicating independent regulation of these two proteins under conditions of chronic muscle use. In contrast, these three proteins exhibited a coordinated three-fold increase following 21 d of denervation. Muscle disuse imposed for a shorter time period in the continuing presence (microgravity conditions for 6 d) or absence (denervation for 7 d) of the nerve resulted in similar 1.8- and 1.9-fold increases in dystrophin levels. These data suggest that the duration of muscle disuse is more important than the presence or absence of the nerve in modifying dystrophin levels in muscle.

In contrast, muscle use imposed by running or 10 d of chronic stimulation had no impact on the dystrophin levels in muscle. A similar lack of effect of chronic stimulation has recently been reported in the dog(23). However, it is known that dog muscle reacts very differently to chronic stimulation (17) than do other species such as the rat or the rabbit (15,16), and therefore we felt that it was important to clarify the role of chronic contractile activity, either through voluntary running or chronic stimulation, on dystrophin levels in the rat. Thus, despite the apparent role of dystrophin in protecting the sarcolemma during the stresses of muscle contraction(25), sufficient levels of this protein may be present within normal muscle without the need for invoking cellular mechanisms of protein induction in response to contractile activity. It is unlikely that the increase in dystrophin levels which we observed under conditions of chronic muscle disuse would be of any benefit to muscular dystrophy patients possessing a defective dystrophin gene. However, it may be of benefit for muscle cell structure and function in those normal individuals forced into conditions of muscle disuse (i.e., immobilization, denervation).

Dystrophin levels have been shown to exist at a higher concentration in slow-twitch, compared with fast-twitch muscle (11). Based upon this observation, we expected that denervation might increase the level of dystrophin in muscle, since this treatment results in a muscle with slower contractile properties (34). Our results indicate that changes in dystrophin levels are associated with the transformation to a slower phenotype. In support of this, chronic stimulation does not result in a fast-to-slow transformation in rat skeletal muscle (27), and we did not find an increase in dystrophin levels as a result of this treatment.

The increases in protein levels observed are likely due either to alterations in the expression of genes that encode these proteins, or to decreased rates of protein turnover. Although it is possible that increases in the degradation of other proteins in atrophying muscle could result in an increase in the concentration of cytoskeletal proteins, the large increases of greater than 3- to 6-fold cannot be entirely accounted for by the decreases in muscle mass observed. Further, even though aciculin, vinculin, and M-vinculin are highly expressed in vascular smooth muscle(1,9), it seems unlikely that the increases in concentration noted could be due solely to changes in skeletal muscle vascularity. This is because any increase in vascularity brought about by the treatment would be expected to enhance the measured levels of all three proteins. However, M-vinculin tended to decrease in response to both denervation and stimulation, rather than increase. Since vinculin and M-vinculin appear to arise from alternative splicing of the same primary transcript (8), the results potentially illustrate an interesting example of splicing regulation. Thus, it seems appropriate to suggest that these experimental conditions are useful for the study of the regulation of the expression and turnover of cytoskeletal proteins in muscle. The changes observed are large and rapid, and reveal a new area of muscle phenotypic plasticity, which could have important implications for muscle cell structure and function.

Back to Top | Article Outline

REFERENCES

1. Belkin, A. M., I. V. Klimanskaya, M. E. Lulashev, K. Lilley, D. R. Critchley, and V. E. Koteliansky. A novel phosphoglucomutase-related protein is concentrated in adherens junctions of muscle and nonmuscle cell. J. Cell Sci. 107:159-173, 1994.

2. Belkin, A. M. and K. Burridge. Expression and localization of the phosphoglucomutase-related cytoskeletal protein, aciculin, in skeletal muscle. J. Cell Sci. 107:1993-2003, 1994.

3. Byers, T. J., L. M. Kunkel, and S. C. Watkins. The subcellular distribution of dystrophin in mouse skeletal, cardiac, and smooth muscle. J. Cell Biol. 115:411-421, 1991.

4. Dick, J. and G. Vrbova. Progressive deterioration of muscle in mdx mice induced by overload. Clin. Sci. 84:145-150, 1993.

5. Eisenberg, H. A. and D. A. Hood. Blood flow, mitochondria, and performance in skeletal muscle after denervation and reinnervation. J. Appl. Physiol. 76:859-866, 1994.

6. Ervasti, J. M. and K. P. Campbell. A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell Biol. 122:809-823, 1993.

7. Geiger, B. and D. Ginsburg. The cytoplasmic domain of adherenstype junctions. Cell Motil. Cytoskeleton 20:1-6, 1991.

8. Gimona, M., J. V. Small, M. Moeremans, J. Van Damme, M. Puype, and J. Vandekerckhove. Porcine vinculin and metavinculin differ by a 68-residue insert located close to the carboxy-terminal part of the molecule.EMBO J. 7:2329-2334, 1988.

9. Glukhova, M. A., A. E. Kabakov, A. M. Belkin, et al. Metavinculin distribution in adult human tissues and cultured cells.FEBS Lett. 207:139-141, 1986.

10. Harlow, E. and D. Lane. Antibodies. A Laboratory Manual., Cold Spring Harbor NY: Cold Spring Harbor Laboratories, 1988, pp. 471-510.

11. Ho-Kim, M.-A. and P. A. Rogers. Quantitative analysis of dystrophin in fast- and slow-twitch mammalian skeletal muscle. FEBS Lett. 304:187-191, 1992.

12. Hood, D. A. Co-ordinate expression of cytochrome c oxidase subunit III and VIc mRNAs in rat tissues. Biochem. J. 269:503-506, 1990.

13. Hood, D. A., A. Balaban, M. K. Connor, et al. Mitochondrial biogenesis in striated muscle. Can. J. Appl. Physiol. 19:12-48, 1994.

14. Hood, D. A., R. Kelton, and M. L. Nishio. Mitochondrial adaptation to chronic muscle use: effect to iron deficiency. Comp. Biochem. Physiol. 101:597-605, 1992.

15. Hood, D. A. and D. Pette. Chronic long-term electrostimulation creates a unique metabolic enzyme profile in rabbit fast-twitch muscle. FEBS Lett. 247:427-474, 1989.

16. Hood, D. A., R. Zak, and D. Pette. Chronic stimulation of rat skeletal muscle induces coordinate increases in mitochondrial and nuclear mRNAs of cytochrome-c-oxidase subunits. Eur. J. Biochem. 179:275-280, 1989.

17. Ianuzzo, C. D., N. Hamilton, P. J. O'Brien, C. Desrosiers, and R. Chiu. Biochemical transformation of canine skeletal muscle for use in cardiac-assist devices. J. Appl. Physiol. 68:1481-1485, 1990.

18. Lansman, B. J. and A. Franco, Jr. What does dystrophin do in normal muscle? J. Muscle Res. Cell Motil. 12:409-411, 1991.

19. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193:265-275, 1951.

20. Luna, E. J. and A. L. Hitt. Cytoskeleton-plasma membrane interactions. Science 258:955-964, 1992.

21. Matsumura, K. and K. P. Campbell. Dystrophin-glycoprotein complex: its role in the molecular pathogenesis of muscular dystrophies. Muscle Nerve 17:2-15, 1994.

22. Moens, P., P. H. W. W. Baatsen, and G. Marechal. Increased susceptibility of EDL muscles from mdx mice to damage induced by contractions with stretch. J. Muscle Res. Cell Motil. 14:446-451, 1993.

23. Ohlendieck, K., F. N. Briggs, K. F. Lee, A. W. Wechsler, and K. P. Campbell. Analysis of excitation-contraction-coupling component in chronically stimulated canine skeletal muscle. Eur. J. Biochem. 202:739-747, 1991.

24. Otter, T., S. M. King, and G. B. Witman. A two-step procedure for efficient electrotransfer of both high-molecular-weight(>400,000) and low-molecular-weight (<20,000) proteins. Anal. Biochem. 162:370-377, 1987.

25. Petrof, B. J., J. B. Shrager, H. H. Stedman, A. M. Kelly, and H. L. Sweeney. Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc. Natl. Acad. Sci. USA 90:3710-3714, 1993.

26. Pette, D. and R. S. Staron. Cellular and molecular diversity of mammalian skeletal muscle fibers. Rev. Physiol. Biochem. Pharmacol. 116:1-76, 1990.

27. Pette, D. and G. Vrbova. Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation. Rev. Physiol. Biochem. Pharmacol. 120:115-202, 1992.

28. Porter, G. A., G. M. Dmytrenko, J. C. Winkelmann, and R. J. Bloch. Dystrophin colocalizes with β-spectrin in distict subsarcolemmal domains in mammalian skeletal muscle. J. Cell Biol. 117:997-1005, 1992.

29. Russell, J. C., W. F. Epling, D. Pierce, R. M. Amy, and D. P. Boer. Induction of prolonged voluntary running by rats. J. Appl. Physiol. 63:2549-2553, 1987.

30. Schachat, F., R. S. Williams, and C. A. Schnurr. Coordinate changes in fast thin filament and Z-line protein expression in the early response to chronic stimulation. J. Biol. Chem. 263:13975-13978, 1988.

31. Schliwa, M. The cytoskeleton. Cell Biol. Monogr. 13:210-229, 1986.

32. Takahashi, M. and D. A. Hood. Chronic stimulation-induced changes in mitochondria and performance in rat skeletal muscle. J. Appl. Physiol. 74:934-941, 1993.

33. Takahashi, M., A. Rana, and D. A. Hood. Portable electrical stimulator for use in small animals. J. Appl. Physiol. 74:942-945, 1993.

34. Wicks, K. L. and D. A. Hood. Mitochondrial adaptations in denervated muscle: relationship to muscle performance. Am. J. Physiol. 260 (Cell Physiol. 29):C841-C850, 1991.

CYTOSKELETON; CHRONIC STIMULATION; SPACE FLIGHT; DENERVATION; VOLUNTARY RUNNING; ADHERENS JUNCTIONS; MICROGRAVITY; SARCOLEMMA

Cited By:

This article has been cited 14 time(s).

American Journal of Physiology-Regulatory Integrative and Comparative Physiology
Cytoskeletal protein contents before and after hindlimb suspension in a fast and slow rat skeletal muscle
Chopard, A; Pons, F; Marini, JF
American Journal of Physiology-Regulatory Integrative and Comparative Physiology, 280(2): R323-R330.

Biochemical and Biophysical Research Communications
Increased expression of the nicotinic acetylcholine receptor in stimulated muscle
O'Reilly, C; Pette, D; Ohlendieck, K
Biochemical and Biophysical Research Communications, 300(2): 585-591.
10.1016/S0006-291X(02)02898-X
CrossRef
American Journal of Physiology-Cell Physiology
Early functional and biochemical adaptations to low-frequency stimulation of rabbit fast-twitch muscle
Hicks, A; Ohlendieck, K; Gopel, SO; Pette, D
American Journal of Physiology-Cell Physiology, 273(1): C297-C305.

Muscle & Nerve
Membrane skeleton of innervated and denervated fast- and slow-twitch muscle
Williams, MW; Resneck, WG; Bloch, RJ
Muscle & Nerve, 23(4): 590-599.

Canadian Journal of Applied Physiology-Revue Canadienne De Physiologie Appliquee
Apoptosis in heart and skeletal muscle
Primeau, AJ; Adhihetty, PJ; Hood, DA
Canadian Journal of Applied Physiology-Revue Canadienne De Physiologie Appliquee, 27(4): 349-395.

Pflugers Archiv-European Journal of Physiology
Vinculin and meta-vinculin in fast and slow rat skeletal muscle before and after hindlimb suspension
Chopard, A; Pons, F; Marini, JF
Pflugers Archiv-European Journal of Physiology, 444(5): 627-633.
10.1007/s00424-002-0872-3
CrossRef
American Journal of Physiology-Cell Physiology
Dystrophin-glycoprotein complex and Ras and Rho GTPase signaling are altered in muscle atrophy
Chockalingam, PS; Cholera, R; Oak, SA; Zheng, Y; Jarrett, HW; Thomason, DB
American Journal of Physiology-Cell Physiology, 283(2): C500-C511.
10.1152/ajpcell.00529.2001
CrossRef
Biologicheskie Membrany
Influence of rat hind limb suspension on sarcolemmal dystrophin and permeability of sarcolemma to macromolecules
Gasnikova, NM; Shenkman, BS
Biologicheskie Membrany, 23(6): 461-469.

Brain Research Reviews
Brain dystrophin, neurogenetics and mental retardation
Mehler, MF
Brain Research Reviews, 32(1): 277-307.

Journal of Muscle Research and Cell Motility
Function induced modifications of gene expression: an alternative approach to gene therapy of Duchenne muscular dystrophy
Vrbova, G
Journal of Muscle Research and Cell Motility, 25(2): 187-192.

Respiration
Distribution of costameric proteins in the diaphragm of patients with chronic obstructive pulmonary disease
Wijnhoven, JH; Hafmans, T; Dekhuijzen, PNR
Respiration, 73(4): 529-537.
10.1159/000091270
CrossRef
Industrial Health
Effects of static load on the weight and protein content in the leg muscles of the mouse: a simulation of prolonged standing in the workplace
Ueno, S; Yokoyama, K; Okuno, M; Wang, RS; Fujioka, Y; Kobayashi, Y
Industrial Health, 42(4): 401-407.

Pflugers Archiv-European Journal of Physiology
The disruption of myofibre structures in rat skeletal muscle after forced lengthening contractions
Komulainen, J; Takala, TES; Kuipers, H; Hesselink, MKC
Pflugers Archiv-European Journal of Physiology, 436(5): 735-741.

Journal of Muscle Research and Cell Motility
Repeated bout effect on the cytoskeletal proteins titin, desmin, and dystrophin in rat skeletal muscle
Lehti, TM; Kalliokoski, R; Komulainen, J
Journal of Muscle Research and Cell Motility, 28(1): 39-47.
10.1007/s10974-007-9102-0
CrossRef
Back to Top | Article Outline

©1996The American College of Sports Medicine

Login

Article Tools

Images

Share

Search for Similar Articles
You may search for similar articles that contain these same keywords or you may modify the keyword list to augment your search.

Connect With Us