Histochemical Responses of Human Soleus Muscle Fibers to Long-Term Bedrest with or without Countermeasures.

Ohira, Yoshinobu; Yoshinaga, Tetsutaro; Nonaka, Ikuya; Ohara, Makoto; Yoshioka, Toshitada; Yamashita-Goto, Katsumasa; Izumi, Ryutaro; Yasukawa, K; Sekiguchi, Chiharu; Шенкман, Борис; Kozlovskaya, I. B.

doi:10.2170/jjphysiol.50.41

Cited by 42 publications

(43 citation statements)

References 15 publications

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“…Exposure to microgravity or hind limb unloading of rodents causes passive shortening of soleus muscle due to ankle plantarflexion (20,39,59), which reduces the mechanical stress (20) and neural activity (19,20,39,43). Even though it is well-reported that muscles composed predominantly of slowtwitch fibers are more susceptible to unloading-related atrophy (6,41,42,(45)(46)(47)59), atrophy in soleus muscle of mice composed of fast-twitch fibers mainly was also observed in all types of mice, as was reported elsewhere (40,48,55). The unloading-related decreases in fiber length and sarcomere number may be associated with the remodeling of muscle fibers and sarcomeres, as was reported before (20,59).…”

Section: Responses To Unloadingsupporting

confidence: 55%

“…For example, chronic unloading of muscles by bedrest in humans (45,46,64) and hind limb suspension and actual spaceflight in animals (6, 40 -42, 47, 59) result in muscle fiber atrophy and a shift toward a faster myosin heavy chain profile, particularly in antigravity muscles composed predominantly of slow-twitch fibers, such as the soleus (6,42,(45)(46)(47) and adductor longus (41,59). Muscle fiber atrophy and the shift toward a faster myosin heavy chain profile are reversed in response to muscle reloading (41,45,46,59). The muscular response to reloading appears to be closely related to intramuscular stimuli that are activated by mechanical loading (20,21,41,47,59) and/or muscle activation with reloading (1,12,20,22,41).…”

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confidence: 99%

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Macrophage deficiency in osteopetrotic (op/op) mice inhibits activation of satellite cells and prevents hypertrophy in single soleus fibers

Ohira

Wang

Ito

et al. 2015

American Journal of Physiology-Cell Physiology

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Effects of macrophage on the responses of soleus fiber size to hind limb unloading and reloading were studied in osteopetrotic homozygous (op/op) mice with inactivated mutation of macrophage colony-stimulating factor (M-CSF) gene and in wild-type (ϩ/ϩ) and heterozygous (ϩ/op) mice. The basal levels of mitotically active and quiescent satellite cell (Ϫ46 and Ϫ39% vs. ϩ/ϩ, and Ϫ40 and Ϫ30% vs. ϩ/op) and myonuclear number (Ϫ29% vs. ϩ/ϩ and Ϫ28% vs. ϩ/op) in fibers of op/op mice were significantly less than controls. Fiber length and sarcomere number in op/op were also less than ϩ/ϩ (Ϫ22%) and ϩ/op (Ϫ21%) mice. Similar trend was noted in fiber cross-sectional area (CSA, Ϫ15% vs. ϩ/ϩ, P ϭ 0.06, and Ϫ14% vs. ϩ/op, P ϭ 0.07). The sizes of myonuclear domain, cytoplasmic volume per myonucleus, were identical in all types of mice. The CSA, length, and the whole number of sarcomeres, myonuclei, and mitotically active and quiescent satellite cells, as well as myonuclear domain, in single muscle fibers were decreased after 10 days of unloading in all types of mice, although all of these parameters in ϩ/ϩ and ϩ/op mice were increased toward the control values after 10 days of reloading. However, none of these levels in op/op mice were recovered. Data suggest that M-CSF and/or macrophages are important to activate satellite cells, which cause increase of myonuclear number during fiber hypertrophy. However, it is unclear why their responses to general growth and reloading after unloading are different. myonuclei; muscle fiber size; osteopetrotic mice; satellite cells; unloading and reloading SKELETAL MUSCLES ARE COMPOSED of multinucleated muscle fibers and have an extensive capacity for morphological and functional adaptation. For example, chronic unloading of muscles by bedrest in humans (45,46,64) and hind limb suspension and actual spaceflight in animals (6, 40 -42, 47, 59) result in muscle fiber atrophy and a shift toward a faster myosin heavy chain profile, particularly in antigravity muscles composed predominantly of slow-twitch fibers, such as the soleus (6,42,(45)(46)(47) and adductor longus (41, 59). Muscle fiber atrophy and the shift toward a faster myosin heavy chain profile are reversed in response to muscle reloading (41,45,46,59). The muscular response to reloading appears to be closely related to intramuscular stimuli that are activated by mechanical loading (20,21,41,47,59) and/or muscle activation with reloading (1,12,20,22,41).Macrophage colony-stimulating factor (M-CSF, CSF-1) is a cytokine that influences hematopoietic stem cells to differentiate into macrophages and other cell types (54). Deficiency of macrophages has been well-reported in osteopetrotic (op/op) mutant mice with inactivating mutation of M-CSF gene, which results in the absence of certain macrophage and in osteopetrosis, following a lack of osteoclasts (60, 63). Tidball and Wehling-Henricks (58) reported important roles of macrophages in the repair of muscle fiber membrane, regeneration, and regrowth after unloading-related atrophy in mouse s...

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Section: Responses To Unloadingsupporting

confidence: 55%

mentioning

confidence: 99%

Macrophage deficiency in osteopetrotic (op/op) mice inhibits activation of satellite cells and prevents hypertrophy in single soleus fibers

Ohira

Wang

Ito

et al. 2015

American Journal of Physiology-Cell Physiology

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“…The ex-pression of IId MHC (most likely analogous to IIx) has also been observed in the rat soleus of 21-and 28-d suspended rats [67]. A similar tendency in fiber type transformation was also seen in the human vastus lateralis muscle after 11 d of spaceflight [77,78] and in the soleus after 4 months of bedrest associated with fiber atrophy [79,80].…”

Section: Fiber Phenotypementioning

confidence: 67%

Neuromuscular Adaptation to Microgravity Environment.

Ohira

2000

JJP

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The pattern of muscle activity influences the morphological, metabolic, and contractile properties of skeletal muscles. For example, the metabolic capacity of muscles is affected specifically by the type of exercise training [1][2][3]. Increased activity or over-loading by removing the synergists causes a compensatory hypertrophy [4][5][6][7][8][9][10][11]. Hypertrophy is also induced by the stretching of matured muscles in vivo [12,13] and cultured myotubes and fibroblasts [14][15][16][17]. Exercise-induced metabolic adaptation of muscles is lost when exercise training is stopped [18]. Further, muscle atrophy is induced by denervation [10,19], spinal cord transection [20], joint immobilization [21][22][23], tenotomy [24,25], spaceflight [26][27][28][29], and/or hindlimb suspension [29][30][31][32]. Most of these models are generally presumed to be models of reduced neuromuscular activity. But the level of use may not be the only factor involved in the atrophic process.There is a close association in the physiological, biochemical, and morphological properties between a motoneuron and the muscle fibers it innervates [1]. Studies to support this view are those in which chronic electrical stimulation at low frequency (1-10 Hz) changes the properties of fast-twitch muscles toward those of slow-twitch muscles [33][34][35][36][37][38].Some of the characteristics of muscle fibers are also altered following cross-innervation [39][40][41][42]. Buller et al. [40] suggested that the neural influence on muscle could be due to neurotrophic effect as well as via nerve impulses. Muscular Responses to Gravitational Unloading Morphological propertiesGravitational unloading by exposure to weightlessness [26][27][28][29][43][44][45][46][47] and/or its simulation model, hindlimb suspension [29][30][31][32][48][49][50][51][52][53][54][55][56], causes rapid atrophy in muscles, such as soleus and adductor longus, that are composed predominantly of slow fibers. The cross-sectional areas (CSAs) of both slow-and fasttwitch fibers of rats were less after 14 d of spaceflight and hindlimb suspension than those in the agematched controls [29]. But the degree of atrophy was greater in slow-than fast-twitch fibers [28,29]. Therefore, muscles composed of predominantly slow fibers are more susceptible to atrophy [26,28, 47]. The weights of fast-twitch ankle dorsi-flexors, such as the tibialis anterior (TA) and extensor digitorum longus (EDL), are also generally less after unloading than those of age-matched controls [31, 57]. But these were Japanese Journal of Physiology, 50, 303-314, 2000 Key words: atrophy, fiber-type transformation, contractile properties, neural responses, microgravity.Abstract: Morphological and/or functional characteristics of skeletal muscles have a greater adaptability in response to changes in environmental stimuli. For example, an atrophy associated with a shift of fiber characteristics toward fast-twitch type is a common adaptation of antigravity muscle to a microgravity environment. Neuromuscular responses and ...

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“…A similar reduction occurred after a 17-day bed rest (17). During bed rest, the feet tend to plantarflex (16). Physical therapists apply foot boards daily to chronically bedridden patients to prevent continuous plantarflexion, which unabated leads to shortening contracture of the plantarflexors.…”

Section: Ajp-cell Physiolmentioning

confidence: 85%

Skeletal muscle fiber atrophy: altered thin filament density changes slow fiber force and shortening velocity

Riley¹,

Bain²,

Romatowski³

et al. 2005

American Journal of Physiology-Cell Physiology

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Single skinned fibers from soleus and adductor longus (AL) muscles of weight-bearing control rats and rats after 14-day hindlimb suspension unloading (HSU) were studied physiologically and ultrastructurally to investigate how slow fibers increase shortening velocity (V 0) without fast myosin. We hypothesized that unloading and shortening of soleus during HSU reduces densities of thin filaments, generating wider myofilament separations that increase V 0 and decrease specific tension (kN/m 2 ). During HSU, plantarflexion shortened soleus working length 23%. AL length was unchanged. Both muscles atrophied as shown by reductions in fiber cross-sectional area. For AL, the 60% atrophy accounted fully for the 58% decrease in absolute tension (mN). In the soleus, the 67% decline in absolute tension resulted from 58% atrophy plus a 17% reduction in specific tension. Soleus fibers exhibited a 25% reduction in thin filaments, whereas there was no change in AL thin filament density. Loss of thin filaments is consistent with reduced cross bridge formation, explaining the fall in specific tension. V 0 increased 27% in soleus but was unchanged in AL. The V 0 of control and HSU fibers was inversely correlated (R ϭ Ϫ0.83) with thin filament density and directly correlated (R ϭ 0.78) with thick-to-thin filament spacing distance in a nonlinear fashion. These data indicate that reduction in thin filament density contributes to an increased V 0 in slow fibers. Osmotically compacting myofilaments with 5% dextran returned density, spacing, and specific tension and slowed V 0 to near-control levels and provided evidence for myofilament spacing modulating tension and V 0. rat; soleus; adductor longus; fiber length; electron microscopy; hindlimb suspension unloading WE OBSERVED PREVIOUSLY (17-19, 26, 28, 29) that 17-day spaceflight and bed rest produced disproportionate losses (ϳ25%) of thin filaments and commensurate increases in the shortening velocities of slow fibers in human soleus muscles. Unexpectedly, the elevated velocity of shortening (V 0 ) was not explained by fast myosin heavy chain expression. We concluded that decreased thin filament densities increase the average spacing distance between thick and thin fibers, resulting in an increased rate of cross-bridge cycling, although changes in other myofibrillar proteins may have been involved in generating faster shortening. The present study was undertaken to determine whether similar changes in V 0 and myofilament densities occur in the fibers of unloaded rat soleus and adductor longus (AL) muscles, to establish a model and examine potential mechanism(s). In rats, atrophy of soleus and AL during hindlimb suspension unloading (HSU) is similar in degree, but soleus exhibits decreased myofilament density with a moth-eaten appearance of myofibrils on day 12 (20). The foci of disrupted myofibrils were called central corelike lesions (CCLs). CCLs did not occur in the AL muscles. Foot drop posture and the resulting shortening of the soleus in the pendant hindlimb were postulated to c...

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Histochemical Responses of Human Soleus Muscle Fibers to Long-Term Bedrest with or without Countermeasures.

Cited by 42 publications

References 15 publications

Macrophage deficiency in osteopetrotic (op/op) mice inhibits activation of satellite cells and prevents hypertrophy in single soleus fibers

Macrophage deficiency in osteopetrotic (op/op) mice inhibits activation of satellite cells and prevents hypertrophy in single soleus fibers

Neuromuscular Adaptation to Microgravity Environment.

Skeletal muscle fiber atrophy: altered thin filament density changes slow fiber force and shortening velocity

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