Rat soleus muscle ultrastructure after hindlimb suspension

Desplanches, Dominique; Kayar, Susan R.; Semporé, B.; Flandrois, R; Hoppeler, Hans

doi:10.1152/jappl.1990.69.2.504

Cited by 78 publications

(63 citation statements)

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“…To our knowledge, this is the first study to show that decrements in skeletal muscle mitochondria, caused by denervation, can be attenuated by prior chronic stimulation. Furthermore, we were not overly surprised by the preferential reduction in SS mitochondria in response to denervation, as this subfraction has been shown to have a heightened sensitivity to alterations in muscular activity (11,16).…”

Section: Discussionmentioning

confidence: 80%

Effect of prior chronic contractile activity on mitochondrial function and apoptotic protein expression in denervated muscle

O'Leary

Hood²

2008

Journal of Applied Physiology

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O'Leary MF, Hood DA. Effect of prior chronic contractile activity on mitochondrial function and apoptotic protein expression in denervated muscle. J Appl Physiol 105: 114 -120, 2008. First published May 1, 2008 doi:10.1152/japplphysiol.00724.2007.-Skeletal muscle is highly adaptable in response to increases and decreases in contractile activity. The purpose of this study was to determine whether the preconditioning of skeletal muscle has a protective effect against subsequent denervation-induced apoptotic protein expression. To investigate this, we chronically stimulated the tibialis anterior and extensor digitorum longus muscles for 7 days (10 Hz, 3 h/day) before 7 days of denervation. Denervation reduced total cytochrome-c oxidase activity by 39%, which was likely a consequence of a decrease in subsarcolemmal (SS) mitochondria. This decrease in the SS subfraction was prevented by prior chronic stimulation and, as a result, maintained total mitochondrial content at control levels. The expression of Bax was elevated 2.2-fold by denervation, and prior chronic stimulation did not attenuate this increase. This produced a increase in the Bax-to-Bcl-2 ratio, indicating greater muscle apoptotic susceptibility. Denervation also decreased state 3 respiration in SS and intermyofibrillar mitochondria and elevated state 4 reactive oxygen species production within both mitochondrial subfractions. These changes were not prevented by prior chronic stimulation. Furthermore, the antioxidant protein MnSOD was also reduced by denervation, whereas Beclin-1 was markedly elevated. This suggests that autophagic cell death could also play a significant part in denervationinduced muscle atrophy. Thus, despite prior chronic stimulation, denervation increases the apoptotic susceptibility of skeletal muscle by altering the Bax-to-Bcl-2 ratio, by increasing reactive oxygen species production, and by reducing the expression of MnSOD. Whether a more extensive stimulation paradigm would be more effective in attenuating apoptosis before muscle disuse remains to be determined. mitochondrial biogenesis; muscle atrophy; reactive oxygen species; autophagy; protein degradation SKELETAL MUSCLE IS AN ADAPTABLE tissue that exhibits a remarkable range of plasticity in response to different levels of contractile activity (15). In particular, chronic contractile activity is known to alter the expression of a variety of proteins from the nuclear and mitochondrial genomes (15). These changes in protein expression result in an increase in mitochondrial volume and density (6, 16). In skeletal muscle, two distinct subfractions of mitochondria exist that are characterized by their anatomic localization. Subsarcolemmal (SS) mitochondria are located just beneath the sarcolemmal membrane, whereas intermyofibrillar (IMF) mitochondria are intertwined between skeletal muscle myofibrils (8). SS and IMF mitochondrial subfractions are significantly increased in response to chronic contractile activity. However, SS mitochondria are more sensitive to endurance training a...

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Section: Discussionmentioning

confidence: 80%

Effect of prior chronic contractile activity on mitochondrial function and apoptotic protein expression in denervated muscle

O'Leary

Hood²

2008

Journal of Applied Physiology

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“…diameter (16,36). Desplanches et al (7) reported that hindlimb suspension of rats for 5 wk resulted in a decrease of 37% in the C/F ratio but an increase of 48% in capillary density. HU causes atrophy of skeletal muscle fibers, reducing the muscle mass (7,28).…”

Section: Discussionmentioning

confidence: 99%

“…Desplanches et al (7) reported that hindlimb suspension of rats for 5 wk resulted in a decrease of 37% in the C/F ratio but an increase of 48% in capillary density. HU causes atrophy of skeletal muscle fibers, reducing the muscle mass (7,28). If the degree of muscle atrophy is greater than that of capillary regression, the capillary density should increase despite the decrease in the C/F ratio.…”

Section: Discussionmentioning

confidence: 99%

Regression of capillary network in atrophied soleus muscle induced by hindlimb unweighting

Fujino¹,

Kohzuki²,

Takeda³

et al. 2005

Journal of Applied Physiology

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Little is known about the mechanisms responsible for the adaptation and changes in the capillary network of hindlimb unweighting (HU)-induced atrophied skeletal muscle, especially the coupling between functional and structural alterations of intercapillary anastomoses and tortuosity of capillaries. We hypothesized that muscle atrophy by HU leads to the apoptotic regression of the capillaries and intercapillary anastomoses with their functional alteration in hemodynamics. To clarify the three-dimensional architecture of the capillary network, contrast medium-injected rat soleus muscles were visualized clearly using a confocal laser scanning microscope, and sections were stained by terminal deoxynucleotidyltransferase-mediated dUTP nick-end labeling (TUNEL) and with anti-von Willebrand factor. In vivo, the red blood cell velocity of soleus muscle capillaries were determined with a pencil-lens intravital microscope brought into direct contact with the soleus surface. After HU, the total muscle mass, myofibril protein mass, and slow-type myosin heavy chain content were significantly lower. The number of capillaries paralleling muscle fiber and red blood cells velocity were higher in atrophied soleus. However, the mean capillary volume and capillary luminal diameter were significantly smaller after HU than in the age-matched control group. In addition, we found that the number of anastomoses and the tortuosity were significantly lower and TUNEL-positive endothelial cells were observed in atrophied soleus muscles, especially the anastomoses and/or tortuous capillaries. These results indicate that muscle atrophy by HU generates structural alterations in the capillary network, and apoptosis appears to occur in the endothelial cell of the muscle capillaries. intercapllary anastomosis; tortuosity; capillary volume; capillary lumen; erythrocyte velocity; disuse atrophy; endothelial terminal deoxynucleotidyltransferase-mediated dUTP nick-end labeling SKELETAL MUSCLE CAPILLARIES run tortuously along muscle fibers in the relaxed resting state (2,4,18,20,33). These capillaries are connected with anastomoses, which run orthogonally to muscle fiber direction like parallel rungs of ladder (12, 33). Capillary-to-fiber (C/F) ratio is frequently used to evaluate O 2 supply capacity in skeletal muscle (27). In fact, the C/F ratio is higher in rat soleus muscle, which mainly contains slow oxidative fibers (type I), than in extensor digitorum longus, which is predominantly comprised of fast glycolytic fibers (type IIb) (1, 8, 13). C/F ratio was increased by the augmentation of muscle activity, e.g., exercise or electrical stimulation (9,14,20,25), and was decreased by disuse (14, 31, 33). Histological sections from earlier studies of capillary remodeling in skeletal muscle with disuse atrophy demonstrate a decrease in capillary luminal diameter (16,36) and in the C/F ratio (13, 31, 32) despite an increase in capillary density (13,31,32).Although the regression of anastomoses in atrophied skeletal muscle has not been well studied, it wa...

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“…Previous studies have reported decreases in number of mitochondria as well as the appearance of mitochondrial swelling in HU rats [4,18]. In contrast, the levels of citrate synthase activity, as well as the levels of -hydroxyacyl CoA dehydrogenase, increased in the gastrocnemius, semitendinosus and cardiac muscles in hibernating golden-mantled ground squirrels or loading rats [17,27].…”

Section: Discussionmentioning

confidence: 79%

A Low Temperature Environment Delays the Changes in Muscle Fiber Type Composition Induced by Unloading

Nagano

Suzaki

Nagano

et al. 2005

Acta Histochem. Cytochem

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The present study examined whether low-temperature (LT) could reduce experimentally-induced atrophy of the skeletal muscle in non-hibernating mammals, as judged by muscle wet-weight, cross-sectional area of muscle fibers, ratio of muscle fiber types, and number of apoptotic myofibers in the soleus muscle of rat. Hindlimb unloading (HU) was carried out for either one or two weeks (1W or 2W, respectively) at room temperature (HU-1W and HU-2W groups) or LT (10C, HULT-1W and HULT-2W groups). Other animals were allowed to move freely at either room temperature (CON-1W and CON-2W groups) or LT (LT-1W and LT-2W groups). Total caloric intake was increased in LT rats compared with the CON, HULT and HU rats. Body weight, muscle wet-weight and cross-sectional area were significantly decreased in HU and HULT rats compared with CON and/or LT rats. Type-I fiber composition in HULT-2W was not significantly reduced compared with those of CON-2W and LT-2W, but that of HU-2W was significantly reduced compared with the other groups. A small number of caspase-3-activated myofibers appeared in HULT-2W and HU-2W, but not in CON-2W and LT-2W. Thus, our results indicate that LT retards the change in the ratio of type-I and type-II fibers, but does not prevent decreases in muscle size and mass, or apoptosis of myofibers.

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Rat soleus muscle ultrastructure after hindlimb suspension

Cited by 78 publications

References 0 publications

Effect of prior chronic contractile activity on mitochondrial function and apoptotic protein expression in denervated muscle

Effect of prior chronic contractile activity on mitochondrial function and apoptotic protein expression in denervated muscle

Regression of capillary network in atrophied soleus muscle induced by hindlimb unweighting

A Low Temperature Environment Delays the Changes in Muscle Fiber Type Composition Induced by Unloading

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