The Role of Neural and Mechanical Influences in Maintaining Normal Fast and Slow Muscle Properties

Ohira, Yoshinobu; Yoshinaga, Tetsutaro; Ohara, Makoto; Kawano, Fuminori; Wang, Xiao Dong; Higo, Yoko; Terada, Masahiro; Matsuoka, Yoshikazu; Roy, Roland R.; Edgerton, V. Reggie

doi:10.1159/000093963

Cited by 47 publications

(44 citation statements)

References 59 publications

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“…Twelve-week-old male Wistar rats (Nihon CLEA) with a mean body weight of ϳ340 g were randomly separated into pre-(n ϭ 5) and postexperimental control (n ϭ 8), synergist-ablated (n ϭ 11), sham-operated control (n ϭ 8), deafferentated (n ϭ 8), synergist-ablated plus deafferentated (n ϭ 8), and hindlimb-unloaded (n ϭ 8) groups. The denervation model has been used to inhibit neural activity (16,28,30). However, denervation leads to a limb paralysis and plantarflexion-related passive shortening of ankle dorsiflexors that also inhibits the mechanical load to muscles.…”

Section: Methodsmentioning

confidence: 99%

“…However, denervation leads to a limb paralysis and plantarflexion-related passive shortening of ankle dorsiflexors that also inhibits the mechanical load to muscles. Furthermore, hindlimb unloading-related atrophy of soleus muscle was not advanced by additional treatment with denervation (28). Therefore, the group with denervation alone was not included in the present study.…”

Section: Methodsmentioning

confidence: 99%

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Role(s) of nucleoli and phosphorylation of ribosomal protein S6 and/or HSP27 in the regulation of muscle mass

Kawano

Matsuoka²,

Oke³

et al. 2007

American Journal of Physiology-Cell Physiology

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Effects of 14 days of hindlimb unloading or synergist ablation-related overloading with or without deafferentation on the fiber cross-sectional area, myonuclear number, size, and domain, the number of nucleoli in a single myonucleus, and the levels in the phosphorylation of the ribosomal protein S6 (S6) and 27-kDa heat shock protein (HSP27) were studied in rat soleus. Hypertrophy of fibers (ϩ24%), associated with increased nucleolar number (from 1-2 to 3-5) within a myonucleus and myonuclear domain (ϩ27%) compared with the preexperimental level, was induced by synergist ablation. Such phenomena were associated with increased levels of phosphorylated S6 (ϩ84%) and HSP27 (ϩ28%). Fiber atrophy (Ϫ52%), associated with decreased number (Ϫ31%) and domain size (Ϫ28%) of myonuclei and phosphorylation of S6 (Ϫ98%) and HSP27 (Ϫ63%), and with increased myonuclear size (ϩ19%) and ubiquitination of myosin heavy chain (ϩ33%, P Ͼ 0.05), was observed after unloading, which inhibited the mechanical load. Responses to deafferentation, which inhibited electromyogram level (Ϫ47%), were basically similar to those caused by hindlimb unloading, although the magnitudes were minor. The deafferentation-related responses were prevented and nucleolar number was even increased (ϩ18%) by addition of synergist ablation, even though the integrated electromyogram level was still 30% less than controls. It is suggested that the load-dependent maintenance or upregulation of the nucleolar number and/or phosphorylation of S6 and HSP27 plays the important role(s) in the regulation of muscle mass. It was also indicated that such regulation was not necessarily associated with the neural activity. rat soleus muscle; functional overload; deafferentation; 27-kDa heat shock protein; ubiquitination of myosin heavy chain

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Role(s) of nucleoli and phosphorylation of ribosomal protein S6 and/or HSP27 in the regulation of muscle mass

Kawano

Matsuoka²,

Oke³

et al. 2007

American Journal of Physiology-Cell Physiology

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“…The PI-labeled nuclei were counted in the entire single fiber. Myonuclear domain size [Allen et al, 1996Roy et al, 1999;McCarter and Steinhardt, 2000;Ohira et al, 2001Ohira et al, , 2006Wang et al, 2006;Kawano et al, 2008] was also calculated by multiplying the fiber CSA and the fiber length and then dividing by the myonuclear number per fiber. The CSA of the myonuclei (at least 30 myonuclei in each fiber) was also measured.…”

Section: Confocal Microscopymentioning

confidence: 99%

Myonucleus-Related Properties in Soleus Muscle Fibers of <i>mdx</i> Mice

Terada

Lan

Kawano

et al. 2009

Cells Tissues Organs

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Distribution and total number of myonuclei in single soleus muscle fibers, sampled from tendon to tendon, were analyzed in mdx and wild-type (WT) mice. Apoptotic myonuclei and the microscopic structure around the myonuclei were also analyzed. Three types of muscle fibers of mdx mice with myonuclear distribution at either central, peripheral, or both central and peripheral regions were observed in the longitudinal analyses. All of the myonuclei were located at the peripheral region in WT mice. The total number of myonuclei counted in the whole length of fibers with peripheral myonuclei only was 17% less in mdx than in WT mice (p < 0.05). But the total myonuclear numbers in mdx mouse fibers with different distribution (peripheral vs. central) of myonuclei were identical, and the peripheral nucleus was noted where the central nucleus was missing. Myonuclei located between the center and peripheral regions were also seen in the cross-sectional analyses of muscle fibers. The cross-sectional area and length of fibers, sarcomere number, myonuclear size, myosin heavy chain expression, satellite cell number and neuromuscular junction were identical between each type of fiber. Apoptosis was not detected in any myonuclei located either in central or peripheral regions of muscle fibers. Thus, it was suggested that apoptosis-related loss of central myonuclei and regeneration-related new accretion at the peripheral region is not the cause of different distribution of myonuclei seen in muscle fibers in mdx mice. However, it was speculated that cross-sectional migration of myonuclei from central to peripheral regions may be induced in response to regeneration, because the total myonuclear numbers in fibers with different distribution of myonuclei were identical, and the peripheral nucleus was noted where the central nucleus was missing. Further, myonuclei located between the center and peripheral regions were also seen. However, the question remains as to how or why nuclei might migrate to the periphery in a regenerating muscle fiber, since there was no microscopic evidence of any structural changes around the myonuclei that may be responsible for the movement of the nucleus.

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“…In contrast, the fast-type innervation pattern maintains different fast isoforms (MHCIIA, IIX, and IIB). However, denervation or muscle inactivity has a similar effect on fastisoform expression, inducing slow-to-fast shift with a concomitant increase in hybrid fibers in slow-type muscles (Ohira et al 2006;Patterson et al 2006). Cross-reinnervation studies have also proved the plasticity of muscles by adapting the fiber phenotype to the properties of the newly innervating motoneurons (Vrbová et al 1995).…”

mentioning

confidence: 99%

Regeneration of Reinnervated Rat Soleus Muscle Is Accompanied by Fiber Transition Toward a Faster Phenotype

Mendler

Pintér

Kiricsi

et al. 2007

J Histochem Cytochem.

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S U M M A R Y The functional recovery of skeletal muscles after peripheral nerve transection and microsurgical repair is generally incomplete. Several reinnervation abnormalities have been described even after nerve reconstruction surgery. Less is known, however, about the regenerative capacity of reinnervated muscles. Previously, we detected remarkable morphological and motor endplate alterations after inducing muscle necrosis and subsequent regeneration in the reinnervated rat soleus muscle. In the present study, we comparatively analyzed the morphometric properties of different fiber populations, as well as the expression pattern of myosin heavy chain isoforms at both immunohistochemical and mRNA levels in reinnervated versus reinnervated-regenerated muscles. A dramatic slow-tofast fiber type transition was found in reinnervated soleus, and a further change toward the fast phenotype was observed in reinnervated-regenerated muscles. These findings suggest that the (fast) pattern of reinnervation plays a dominant role in the specification of fiber phenotype during regeneration, which can contribute to the long-lasting functional impairment of the reinnervated muscle. Moreover, because the fast II fibers (and selectively, a certain population of the fast IIB fibers) showed better recovery than did the slow type I fibers, the faster phenotype of the reinnervated-regenerated muscle seems to be actively maintained by selective yet undefined cues. (J Histochem Cytochem 56:111-123, 2008)

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The Role of Neural and Mechanical Influences in Maintaining Normal Fast and Slow Muscle Properties

Cited by 47 publications

References 59 publications

Role(s) of nucleoli and phosphorylation of ribosomal protein S6 and/or HSP27 in the regulation of muscle mass

Role(s) of nucleoli and phosphorylation of ribosomal protein S6 and/or HSP27 in the regulation of muscle mass

Myonucleus-Related Properties in Soleus Muscle Fibers of <i>mdx</i> Mice

Regeneration of Reinnervated Rat Soleus Muscle Is Accompanied by Fiber Transition Toward a Faster Phenotype

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