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PubMed2004

Development of whole-body and skeletal muscle insulin resistance after one day of hindlimb suspension.

Hindlimb suspension (HS) of rats is a model of simulated weightlessness and induces dynamic alterations in insulin action. In the present study, the effect of acute (1-day) HS on whole-body glucose tolerance and insulin action on skeletal muscle glucose transport was assessed in juvenile, female Sprague-Dawley rats. Compared to weight-bearing control rats, 1-day HS animals displayed significantly decreased glucose tolerance and diminished whole-body insulin sensitivity. Glucose transport activity in the 1-day unweighted soleus muscle was significantly decreased (P <.05) compared to weight-bearing control muscles both in the absence and presence of insulin (2 mU/mL). Insulin-mediated glucose transport activity in the extensor digitorum longus (EDL) muscles also tended (P =.09) to be lower. There was no change in the protein expression of insulin receptor beta-subunit (IR-beta), insulin receptor substrate-1 (IRS-1), IRS-2, the p85 subunit of phosphatidylinositol-3 kinase (PI3-kinase), Akt, and glucose transporter protein 4 (GLUT-4). The activities of these proteins were also unchanged, as insulin-stimulated IR-beta tyrosine phosphorylation, IRS-1 tyrosine phosphorylation, IRS-1-associated p85, and Akt serine phosphorylation were similar to controls. However, basal Akt phosphorylation was significantly depressed (P <.05) in the 1-day HS soleus. In addition, the protein expression and basal phosphorylation of the stress-activated p38 mitogen-activated protein kinase (p38 MAPK) were significantly elevated (P <.05) in the 1-day unweighted soleus. These results indicate that the development of insulin resistance in the 1-day unweighted soleus is not due to impaired functionality of elements involved in the IR/IRS-1/PI3-kinase/Akt signaling pathway. However, activation of p38 MAPK may play a role in this response.

Animals↗
PubMed1987

Size and metabolic properties of fibers in rat fast-twitch muscles after hindlimb suspension.

Hindlimb suspension (HS) results in whole muscle atrophic and metabolic changes that vary in magnitude in different hindlimb muscles. The present study was designed to investigate these effects in single fibers. Fiber type and size and the activities of two metabolic marker enzymes were determined in a deep (close to the bone) and a superficial (away from the bone) region of the medial gastrocnemius (MG) and the tibialis anterior (TA) of control (CON) and 28-day HS adult female rats. Fibers were classified as dark or light adenosinetriphosphatase (ATPase) based on their qualitative staining reaction for myosin ATPase following alkaline preincubation. Fiber area and succinate dehydrogenase (SDH) and alpha-glycerophosphate dehydrogenase (GPD) activities were determined in tissue sections by use of an image analysis system. After 28 days of HS, the mean body weights of the CON and HS were similar. MG atrophied 28%, whereas TA weight was maintained in the HS. Both dark and light ATPase fibers in the deep region of the MG had smaller cross-sectional areas following HS, with the atrophic response being approximately twice as great in the light ATPase fibers. No significant changes in fiber type composition in either muscle or in fiber sizes in the superficial region of the MG or in either region of the TA were observed. Mean SDH activities of both fiber types were significantly lower in the MG and TA following HS. In contrast, mean GPD activities were either increased or maintained in light and dark ATPase fibers of both muscles in HS. Changes in SDH and GPD activity could not be directly linked to changes in fiber cross-sectional area. In summary, these data suggest an independence of the mechanisms determining muscle fiber size and metabolic adaptations associated with HS.

Adenosine Triphosphatases↗
PubMed1992

Ventral horn cell responses to spaceflight and hindlimb suspension.

Spaceflight or hindlimb suspension results in a loss of mass and alterations of the metabolic and contractile protein profiles of skeletal muscles toward that resembling faster muscles. Given the influence of motoneurons on muscle properties, ventral horn cells of the lumbosacral enlargement of the spinal cord were studied to determine whether similar adaptations were present. Three groups of rats (5 per group) were studied: control, 14-day spaceflight, and 14-day hindlimb suspension. Spinal cords were quick-frozen, and the succinate dehydrogenase (SDH) activity and cross-sectional area of the soma of ventral horn cells were measured using a computer-enhanced image-processing system. Briefly, the optical density for SDH activity was determined after 8 min of incubation in a medium that gave a steady-state enzymatic reaction. Soma sizes were determined in cells with a visible nucleus. Although there were no significant differences among the three groups in mean cross-sectional area and SDH activity, the population distributions of both variables shifted significantly. In the flight rats, there was a shift toward smaller cells. Compared with control, the population distribution of SDH activities in the flight rats shifted toward higher activities, whereas the distribution shifted toward lower activities in the suspended rats. When considering the interactive effects within individual cells, there was a higher percentage of small cells with high SDH activities in the flight than in the control or suspended rats. These contrasting effects of spaceflight and hindlimb suspension suggest that the changes observed in ventral horn cells were due to factors other than simply the absence of weight support.

Animals↗
PubMed1993

Central and peripheral norepinephrine turnover after hindlimb suspension in the rat.

After a 9-d hindlimb suspension, the turnover rate of norepinephrine (NE) in rats was determined in A1, A2 (rostral and caudal), A5 and A6 cell groups, as well as in peripheral target organs (heart and kidneys). The NE turnover rate decreased after hindlimb suspension respectively in caudal A2 (67.5%, p < 0.001), rostral A2 (63%, p < 0.001) and in A5 cell groups (62.5%, p < 0.001), but remained unchanged in A1 and A6 regions. The peripheral sympathetic outflow response was selectively modified: in suspended rats, the NE turnover was mainly decreased in atria (79%, p < 0.001) and in ventricles (44%, p < 0.001); there were no biochemical changes in kidneys. It was concluded that a 9-d hindlimb suspension: 1) impaired the noradrenergic neuron activity of A2 and A5 cell groups, which are involved in the central cardiovascular regulation, and particularly in the baroreceptor reflex mechanism; and 2) mainly altered the cardiac NE turnover and induced a selective response of peripheral target organs.

Animals↗
PubMed1999

Myogenin, MyoD, and myosin heavy chain isoform expression following hindlimb suspension.

BACKGROUND: Myogenin expression is associated with a slow myofiber phenotype, and MyoD expression is associated with a fast myofiber phenotype. Hindlimb suspension (HS) will induce muscular atrophy, and a transition from a slow to fast myofiber phenotype in the rat soleus. HYPOTHESIS: Hindlimb suspension will induce myofiber atrophy, and a slow to fast myofiber type transition with corresponding changes in myogenin and MyoD expression. METHODS: Myofiber phenotype was evaluated by electrophoretically separating the myosin heavy chain isoforms. Myogenin expression was evaluated by Northern analysis, while MyoD expression was evaluated by Northern analysis and semiquantitative RT-PCR. RESULT: After 28 d of hindlimb suspension, there was significantly (p < 0.05) less myosin heavy chain Type IIA, and more (p < 0.05) myosin heavy chain Type IIX in the soleus muscles of hindlimb suspended rats compared with soleus muscles from weight-bearing (WB) rats. Although there was a shift to a faster myosin heavy chain phenotype in soleus muscles from hindlimb suspended rats, there was no change in myogenin expression, and MyoD expression was undetectable by Northern analysis. Semi-quantitative RT-PCR revealed an up-regulation of MyoD expression following 14 d of hindlimb suspension. CONCLUSIONS: Myogenin expression levels do not change during the slow to fast myofiber phenotypic transition that occurs during hindlimb suspension; MyoD expression appears to increase at the same time as the phenotypic transition. Thus, MyoD expression or the Myogenin: MyoD mRNA ratio may be important in the phenotypic transition. Neither myogenin nor MyoD appear to play a critical role in the muscular atrophy that occurs during weightlessness.

Animals↗
PubMed1997

Effect of a 14-day hindlimb suspension on cytosolic Ca2+ concentration in rat portal vein myocytes.

Effects of a 14-day hindlimb suspension were examined on increases in cytosolic Ca2+ concentration ([Ca2+]i) evoked by vasoactive compounds and on Ca2+ channels in rat portal vein myocytes. The maximal increases in [Ca2+]i elicited by caffeine, norepinephrine, and angiotensin II were reduced by 30-50% in suspended rats, and complete recovery was obtained 4 days after suspension removal. In contrast, voltage-gated Ca2+ channels were unaffected by hindlimb suspension. Using both confocal microscopy and the patch-clamp technique, we measured local increases in [Ca2+]i which corresponded to activation of a small number of ryanodine-sensitive Ca(2+)-release channels (Ca2+ sparks) and D-myo-inositol 1,4,5-trisphosphate [Ins(1,4,5)P3]-gated Ca2+ channels. After hindlimb suspension, these local Ca2+ events, as well as the Ca2+ sensitivity of ryanodine-sensitive Ca2+ release channels, remained unchanged. In contrast, the propagated Ca2+ responses (Ca2+ waves) were significantly reduced in parallel with a noticeable inhibition of [3H]ryanodine binding to vascular membranes. Taken together, these results suggest that inhibition of the vasoconstrictor-induced increases in [Ca2+]i during long-term suspension may be related to a reduction of the number of functional ryanodine-sensitive and Ins(1,4,5)P3-gated channels in the sarcoplasmic reticulum of rat portal vein myocytes.

Angiotensin II↗
PubMed1998

Hindlimb suspension induces the expression of multiple myosin heavy chain isoforms in single fibres of the rat soleus muscle.

To examine the expression patterns of myosin heavy chain (MHC) isoforms in single fibres of the soleus muscle following weightlessness, 10-week-old male Wistar rats were subjected to hindlimb suspension for 4 weeks. Hindlimb suspension resulted in reduced body weight and absolute and relative mass of the soleus muscle compared with controls (P < 0.01). A total of 975, 892 and 1098 single fibres from pre-suspended controls, age-matched controls and suspension groups, respectively, were subjected to MHC analyses using SDS-PAGE. Single fibres containing only MHC I decreased (87.9 vs. 67.9%, P < 0.05) and single fibres containing only MHC IIa disappeared after hindlimb suspension. On the contrary, single fibres containing multiple type II MHC isoforms were observed as follows: 10.1% single fibres contained MHCs IIa and IId; 14.1% contained MHCs I, IIa and IId; and some (1.4%) expressed the MHC IIb isoform with MHCs IIa and IId. The relative content (%) of each MHC isoform in MHC hybrid single fibres was calculated using densitometer scanning. The MHCs IIa and IId hybrid single fibres contained the same amount of MHC IIa (51.3 +/- 6.3%) and MHC IId (48.7 +/- 6.3%). In the MHCs I, IIa and IId hybrid single fibres, the percentage of MHC IIa was distributed in a wide range (approximately 80%), whereas the percentage of MHC IId was a relatively low range (approximately 40%), and the relative content of MHC I was inversely correlated with that of MHC IIa and MHC IId, respectively. The fibre type composition of suspended soleus muscle, analysed by histochemical myosin ATPase staining, was changed, with a decrease in the percentage of type I fibres and an increase in that of type IIA fibres. Our results indicate that hindlimb suspension induces multiple type II MHC expression in the soleus single fibres and suggest that the single fibres containing multiple type II MHC isoforms should be classified into type IIA.

Adenosine Triphosphatases↗
PubMed2003

Effects of gravitational loading on rat soleus muscle fibers following hindlimb suspension.

Effects of 16 days of hindlimb suspension and 16 days of ambulation recovery at 1-G or 2-G environment on the characteristics of soleus muscle fibers were studied in male Wistar Hannover rats. The mean cross-sectional area and myonuclear number in isolated single fibers at the termination of suspension were approximately 30% and 25% of the controls, respectively. Satellite cells were distributed evenly throughout the fiber length in the control. However, the number of satellite cells distributed at the middle of the fiber was less in the unloaded rats immediately after the termination of suspension. Both the numbers of quiescent and mitotic active satellite cell per fiber were approximately 57% less immediately after the termination of suspension than controls. The number of satellite cells at the end of fibers was increased first during the early phase of reloading. Subsequently, the number at the middle was gradually increased. The myonuclear number per fiber was also less (approximately 25%) in the unloaded than the age-matched control at the termination of suspension, but was increased following the recovery. Although the mean in vivo sarcomere length of the soleus muscle was shortened in response to plantarflexion of ankle joint, the length at the certain ankle joint angle was increased after 16 days of suspension due to sarcomere remodeling. The length at the proximal and distal, rather than the middle, portion of the fiber was stretched in both reloaded and control rats in response to dorsiflexion of the ankle joint. But it was noted that the magnitude of stretch was greater in the unloaded rats. It is suggested that the fiber end is more stimulated rapidly than the middle portion by the load applied to the muscle during the ambulation recovery.

Animals↗
PubMed1991

Myofibrillar disruption in the rabbit soleus muscle after one-week hindlimb suspension.

Relevant muscle- and species-specific differences may be found in the reaction of muscles to hindlimb suspension. This problem has been studied in 5 rabbits following a one-week hindlimb suspension, and in 5 ground-based controls. The soleus and the tibialis were prepared for light and transmission electron microscopy. In suspension the animals occasionally extended and flexed the hindlimbs, but, when standing still, their hindfeet were plantar-flexed to an angle of 180 degrees. In this position the length of the soleus was determined to be 35% less than in controls, whereas that of the tibialis was 30% more. Histologically, the tibialis fibers usually exhibited a preserved sarcomeric pattern, whereas soleus fibers displayed a regular sequence of areas of shortened sarcomeres, alternating with areas of myofibrillar disruption. These findings demonstrated that hindlimb suspension induces a focal breakdown of the soleus myofibrils, probably dependent on the reduced longitudinal tension of the suspended soleus and its phasic contractions against no load. It is conceivable that similar factors could also be responsible for soleus muscle atrophy induced by hypogravity as well as by other clinical conditions during which a stressful plantar flexion of the feet occurs against no load.

Animals↗
PubMed2003

Changes of bone morphology in response to hindlimb suspension of rats.

Effects of chronic hindlimb suspension or exposure to 2-G from postnatal day 4 to month 3 followed by ambulation recovery on the floor on the morphology of hindlimb bones were investigated in rats. The dorsi-flexion of the ankle was inhibited in the suspended group and such phenomena were not recovered at all. The mean weight and length of femur, tibia, and fibula were less than the cage controls at the end of suspension, but gradually increased during recovery. However, they were still less than those of the age-matched controls even after 3-month recovery. External bending of shaft and rotation of distal end of tibia were observed in the suspended group and these phenomena were not recovered at all. These morphological changes caused the inhibition of dorsi-flexion of ankle joints. The electromyogram activities of ankle plantar-flexors, soleus, plantaris, lateral gastrocnemius, were inhibited and those of dorsi-flexor, tibialis anterior, were increased during suspension. Typical changes in bone morphology were not induced by exposure to 2-G. It was suggested that gravitational unloading during developing period causes irreversible inhibition of normal bone growth. It was also indicated that the suspension-related changes in bone morphology may be caused by abnormal mechanical stress due to the altered mobilization of hindlimb muscles.

Animals↗
PubMed1988

Adaptation of bone and tendon to prolonged hindlimb suspension in rats.

The rat hindlimb suspension model was used to ascertain the importance of ground reaction forces in maintaining bone and tendon homeostasis. Young female Sprague-Dawley rats were randomly assigned to either a suspended or a nonsuspended group. After 28 days, femur bones and patellar tendons were obtained for morphological and biochemical analyses. Prolonged suspension induced a significant change in the geometric configuration of the femur middiaphysis by increasing the minimum diameter (12%) without any significant alterations in cortical area, density, mineral, and collagen concentrations. Femur wet weight, length, DNA, and uronic acid concentrations of suspended animals were not significantly different from bones of nonsuspended rats. However, the collagen and proteoglycan concentrations in patellar tendons of suspended rats were 28% lower than the concentrations of matrix proteins in tissues obtained from nonsuspended animals. These data suggest that elimination of ground reaction forces induces alterations in tendon composition and femur diaphyseal shape by changing regional rates in bone remodeling and localized tendon strain. Therefore it appears that ground reaction forces are an important factor in the maintenance of cortical bone and patellar tendon homeostasis during weight-bearing conditions.

Adaptation, Physiological↗
PubMed2002

Peripheral vascular responses to heat stress after hindlimb suspension.

PURPOSE: The purpose of this study was to determine whether hindlimb suspension (which simulates the effects of microgravity) results in impaired hemodynamic responses to heat stress or alterations in mesenteric small artery sympathetic nerve innervation. METHODS: Over 28 d, 16 male Sprague-Dawley rats were hindlimb-suspended, and 13 control rats were housed in the same type of cage. After the treatment, mean arterial pressure (MAP), colonic temperature (Tcol), and superior mesenteric and iliac artery resistances (using Doppler flowmetry) were measured during heat stress [exposure to 42 degrees C until the endpoint of 80 mm Hg blood pressure was reached (75 +/- 9 min); endpoint Tcore = 43.6 +/- 0.2] while rats were anesthetized (sodium pentobarbital, 50 mg x kg(-1) BW). RESULTS: Hindlimb-suspended and control rats exhibited similar increases in Tcol, MAP, and superior mesenteric artery resistance, and similar decreases in iliac resistance during heat stress (endpoint was a fall in MAP below 80 mm Hg). Tyrosine hydroxylase immunostaining indicated similar sympathetic nerve innervation in small mesenteric arteries from both groups. CONCLUSION: Hindlimb suspension does not alter the hemodynamic or thermoregulatory responses to heat stress in the anesthetized rat or mesenteric sympathetic nerve innervation, suggesting that this sympathetic pathway is intact.

Animals↗
PubMed1997

Effects of acute and chronic hindlimb suspension on sensitivity and responsiveness to insulin in the rat soleus muscle.

The effects of acute (24 h) and chronic (5 weeks) hindlimb suspension on insulin-stimulated glucose utilization by the rat soleus muscle were studied in vitro. Hindlimb suspension resulted in an enhancement of basal glucose transport, lactate production, and glycogen synthesis. An increase in the sensitivity of these processes to insulin occurred as early as 24 h and persisted for 5 weeks of the muscle unloading. An increased responsiveness to insulin was found only for glucose transport after 24 h. The present data do not support the concept that the enhanced glucose utilization and improved muscle insulin sensitivity during hindlimb suspension are related to muscle atrophy, which is not observed in the early stage of muscle unweighting.

Animals↗
PubMed2002

Effects of hindlimb suspension on soleus muscle fibers and their spinal motoneurons in Wistar Hannover rats.

Cross-sectional areas and succinate dehydrogenase (SDH) activities of soleus muscle fibers and their spinal motoneurons in male Wistar Hannover rats were determined after 16 days of hindlimb suspension. A decreased percentage of type I fibers and an increased percentage of type I+II fibers were observed after hindlimb suspension. Cross-sectional areas of all types of fibers were smaller in the hindlimb suspended than control rats. SDH activities of all types of fibers did not change after hindlimb suspension. Numbers, cross-sectional areas, or SDH activities of spinal motoneurons did not change after hindlimb suspension. It is suggested that spinal motoneurons innervating the rat soleus muscle are not affected by decreased neuromuscular activity on Earth and that gravity itself is important for maintaining of spinal motoneuron metabolic properties.

Journal Article↗
PubMed1989

Ultrastructural and metabolic profiles on single muscle fibers of different types after hindlimb suspension in rats.

The relationships between ultrastructural and metabolic profiles in different types of single muscle fiber after hindlimb suspension in rats were examined. Glycolytic (lactate dehydrogenase, LDH; phosphofructokinase, PFK) and oxidative (succinate dehydrogenase, SDH; malate dehydrogenase, MDH) enzyme activities in extensor digitorum longus (EDL) and soleus (SOL) muscles were measured. Relative mitochondrial and lipid droplet volumes were also measured in single muscle fiber of different types. Glycolytic enzyme activity in EDL muscle and oxidative enzyme activity in soleus muscle decreased following suspension for 2 weeks. LDH and PFK activities in fast-twitch (FG, fast-twitch glycolytic; FOG, fast-twitch oxidative glycolytic) fibers and oxidative enzymes in FOG and FG fibers decreased following suspension. Relative mitochondrial volume decreased significantly in all types (SO, slow-twitch oxidative; FOG, and FG) of fibers following suspension. The mitochondrial volume in SO fiber of the control group was significantly (p less than 0.01) higher than that of suspended group; however, SDH and MDH activities were not different between the control and suspended groups. The structural and metabolic changes following hindlimb suspension were influenced by different factors, respectively. Changes in ultrastructural and metabolic profiles in response to the hindlimb suspension differed according to the type of fibers.

Animals↗
PubMed1998

Hindlimb suspension reduces muscle regeneration.

Exposure of juvenile skeletal muscle to a weightless environment reduces growth and satellite cell mitotic activity. However, the effect of a weightless environment on the satellite cell population during muscle repair remains unknown. Muscle injury was induced in rat soleus muscles using the myotoxic snake venom, notexin. Rats were placed into hindlimb-suspended or weightbearing groups for 10 days following injury. Cellular proliferation during regeneration was evaluated using 5-bromo-2'-deoxyuridine (BrdU) immunohistochemistry and image analysis. Hindlimb suspension reduced (P < 0.05) regenerated muscle mass, regenerated myofiber diameter, uninjured muscle mass, and uninjured myofiber diameter compared to weightbearing rats. Hindlimb suspension reduced (P < 0.05) BrdU labeling in uninjured soleus muscles compared to weight-bearing muscles. However, hindlimb suspension did not abolish muscle regeneration because myofibers formed in the injured soleus muscles of hindlimb-suspended rats, and BrdU labeling was equivalent (P > 0.10) on myofiber segments isolated from the soleus muscles of hindlimb-suspended and weightbearing rats following injury. Thus, hindlimb suspension (weightlessness) does not suppress satellite cell mitotic activity in regenerating muscles before myofiber formation, but reduces growth of the newly formed myofibers.

Animals↗
PubMed1994

Changes in fibre-type composition and myosin heavy-chain IId isoform in rat soleus muscle during recovery period after hindlimb suspension.

We examined the changes in myosin heavy-chain (HC) isoforms and fibre-type composition in rat soleus muscle using both myosin adenosine triphosphatase staining and sodium dodecyl sulphate/polyacrylamide gel electrophoresis (SDS-PAGE) analyses during the recovery period after 4 weeks of hindlimb suspension. Although there was no change in type IIc fibres after the suspension, an increase in this type of fibres was observed during the 1- to 4-week recovery period. The increase in type IIc fibres was considered to be due to a shift from type IIa to IIc fibres. The SDS-PAGE analysis revealed the presence of the HC IId isoform, which was not observed in the control muscle, after a 4-week hindlimb suspension. The HC IId isoform gradually decreased over 3 weeks of recovery and disappeared in the 4th week of recovery after the suspension. These results suggest that the hypogravity conditions induced by hindlimb suspension stimulated the synthesis of the HC IId isoform, whereas an increase in mechanical load to the muscle accelerated the degradation of the HC IId isoform and the synthesis of type IIc fibres during the recovery period after hindlimb suspension.

Animals↗
PubMed1995

Review of spaceflight and hindlimb suspension unloading induced sarcomere damage and repair.

Hindlimb suspension unloading (HSU) and spaceflight microgravity induce atrophy of the slow adductor longus muscle fibers which, following reloading, exhibit eccentric contraction (EC)-like lesions (abnormal widening of sarcomeres with A band disruption and excessively wavy, extracted Z lines). These lesions are similar morphologically to those produced in normal muscles after strenuous eccentric exercise. It appears that atrophic muscles exhibit increased susceptibility to eccentric damage because lesions are produced during nonstressful voluntary movements upon return to weightbearing. The EC-like lesions are absent in the unweighted conditions, but appear in HSU rats 15-60 minutes after reloading and in space-flown rates about 4 hrs after landing. By 12 hours, many EC-like lesioned sarcomeres are fully covered by longitudinal patches of Z line-like material which increases in density by 48 hours, producing the so-called "Z line streaming" morphology. In this case, Z line streaming is indicative of rapid repair of damaged sarcomeres rather than the onset of sarcomere breakdown. Immunoelectron microscopy is necessary to determine the composition of this dense material. By 9 days of reloading at 1 gravity, sarcomeres have regained normal structure, except for very rare persistence of faint Z patches. The morphological data indicate that Z patches serve at least two functions: 1) to permit contractile force to be transmitted across the damaged sarcomeres and 2) to provide a scaffold upon which sarcomeres are reconstructed in an active functional muscle.

Animals↗