Preliminary experiments on mechanical stretch‐induced activation of skeletal muscle satellite cells <i>in vivo</i>

Sakata, Tomowa; Tatsumi, Ryuichi; Yamada, Michiko; Shiratsuchi, Sei Ichi; Okamoto, Shinpei; Mizunoya, Wataru; Hattori, Akihito; Ikeuchi, Yoshihide

doi:10.1111/j.1740-0929.2006.00380.x

Cited by 10 publications

(12 citation statements)

References 29 publications

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“…This phenomenon is relevant to satellite cells in living skeletal muscle as revealed by an in vivo muscle stretch model (16,27). These experiments also show that release of HGF is blocked if nitric oxide synthase (NOS) is inhibited by N G -nitro-L-arginine methyl ester (L-NAME), and HGF can be liberated when unstretched satellite cells are incubated in sodium nitroprusside (SNP), a NO donor.…”

Section: Rementioning

confidence: 72%

A role for calcium-calmodulin in regulating nitric oxide production during skeletal muscle satellite cell activation

Tatsumi¹,

Wuollet²,

Tabata³

et al. 2009

American Journal of Physiology-Cell Physiology

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RE.A role for calcium-calmodulin in regulating nitric oxide production during skeletal muscle satellite cell activation. Am J Physiol Cell Physiol 296: C922-C929, 2009. First published January 21, 2009 doi:10.1152/ajpcell.00471.2008.-When skeletal muscle is stretched or injured, myogenic satellite cells are activated to enter the cell cycle. This process depends on nitric oxide (NO) production by NO synthase (NOS), matrix metalloproteinase activation, release of hepatocyte growth factor (HGF) from the extracellular matrix, and presentation of HGF to the c-met receptor as demonstrated by a primary culture and in vivo assays. We now add evidence that calcium-calmodulin is involved in the satellite cell activation cascade in vitro. Conditioned medium from cultures that were treated with a calcium ionophore (A23187, ionomycin) for 2 h activated cultured satellite cells and contained active HGF, similar to the effect of mechanical stretch or NO donor treatments. The response was abolished by addition of calmodulin inhibitors (calmidazolium, W-13, W-12) or a NOS inhibitor N G -nitro-L-arginine methyl ester hydrochloride but not by its less inactive enantiomer N G -nitro-Darginine methyl ester hydrochloride. Satellite cells were also shown to express functional calmodulin protein having a calcium-binding activity at 12 h postplating, which is the time at which the calcium ionophore was added in this study and the stretch treatment was applied in our previous experiments. Therefore, results from these experiments provide an additional insight that calcium-calmodulin mediates HGF release from the matrix and that this step in the activation pathway is upstream from NO synthesis. muscle regeneration; stretch-activation SKELETAL MUSCLE SATELLITE cells are resident myogenic stem cells normally found in a quiescent state in adult skeletal muscles. When muscle is injured, overused, or mechanically stretched, these cells are activated to enter the cell cycle, divide, differentiate, and fuse with muscle fibers to repair damaged regions and to enhance hypertrophy of muscle fibers (reviewed in Refs. 7,10,17). Therefore, mechanical changes in muscle can initiate events that lead to satellite cell activation, although the mechanism has not been clearly delineated.Of all growth factors studied thus far, only hepatocyte growth factor (HGF) provides a signal that can activate quiescent satellite cells in primary culture and in vivo (1,20). HGF is a heparin-binding protein localized in the extracellular domain of uninjured skeletal muscle fibers, and its predominant form is the active heterodimer of the 60-kDa ␣-chain and 30-kDa ␤-chain (25). The intracellular signaling receptor for HGF is the c-met proto-oncogene, and its message and protein have been found in quiescent and activated satellite cells (1,8,20). Thus release of HGF from its sequestration and subsequent presentation to the c-met receptor may be a critical aspect of the activation of quiescent satellite cells.In previous works, we employed a FlexerCell system (Flexcell Int...

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Section: Rementioning

confidence: 72%

A role for calcium-calmodulin in regulating nitric oxide production during skeletal muscle satellite cell activation

Tatsumi¹,

Wuollet²,

Tabata³

et al. 2009

American Journal of Physiology-Cell Physiology

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“…TIMP-1 was also shown to have no effect on NOS activity, as monitored by NO x (NO2 and NO3) assay of stretchconditioned media. This observation suggests that MMPs activate steps downstream of NO synthesis in this pathway (Yamada et al 2006).…”

Section: Involvement Of Matrix Metalloproteinasesmentioning

confidence: 92%

“…These results, however, left open the question as to whether this was an artificial cell culture phenomenon or a reflection of the physiological response of muscle to mechanical insults. In order to clarify this issue, we developed an in vivo model to apply mechanical stretch to upper hind limb muscles of adult male rats, and examined for the presence of an intracellular cascade to link between mechanical perturbation, NO synthesis, HGF release and satellite cell activation in vivo (Sakata et al . 2006; Tatsumi et al .…”

Section: Stretch Activation Of Satellite Cellsmentioning

confidence: 99%

“…In an effort to understand the downstream events from NO synthesis, subsequent experiments were designed to test the hypothesis that matrix metalloproteinases (MMPs) are involved in HGF release (Yamada et al 2006(Yamada et al , 2008. MMPs were considered reasonable candidates for this process in which an NO-activated enzyme could shed proteoglycans and associated HGF by cleaving the core proteins or glycosaminoglycan chains.…”

Section: Involvement Of Matrix Metalloproteinasesmentioning

confidence: 99%

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Mechano‐biology of skeletal muscle hypertrophy and regeneration: Possible mechanism of stretch‐induced activation of resident myogenic stem cells

Tatsumi

2010

Animal Science Journal

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119

108

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In undamaged postnatal muscle fibers with normal contraction and relaxation activities, quiescent satellite cells of resident myogenic stem cells are interposed between the overlying external lamina and the sarcolemma of a subjacent mature muscle fiber. When muscle is injured, exercised, overused or mechanically stretched, these cells are activated to enter the cell proliferation cycle, divide, differentiate, and fuse with the adjacent muscle fiber, and are responsible for regeneration and work-induced hypertrophy of muscle fibers. Therefore, a mechanism must exist to translate mechanical changes in muscle tissue into chemical signals that can activate satellite cells. Recent studies of satellite cells or single muscle fibers in culture and in vivo demonstrated the essential role of hepatocyte growth factor (HGF) and nitric oxide (NO) radical in the activation pathway. These experiments have also reported that mechanically stretching satellite cells or living skeletal muscles triggers the activation by rapid release of HGF from its extracellular tethering and the subsequent presentation to the receptor c-met. HGF release has been shown to rely on calcium-calmodulin formation and NO radical production in satellite cells and/or muscle fibers in response to the mechanical perturbation, and depend on the subsequent up-regulation of matrix metalloproteinase (MMP) activity. These results indicate that the activation mechanism is a cascade of events including calcium ion influx, calcium-calmodulin formation, NO synthase activation, NO radical production, MMP activation, HGF release and binding to c-met. Better understanding of 'mechano-biology' on the satellite cell activation is essential for designing procedures that could enhance muscle growth and repair activities in meat-animal agriculture and also in neuromuscular disease and aging in humans.

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“…These results, however, left open the question as to whether this was an artificial cell culture phenomenon or an accurate reflection of the physiological response of muscle to mechanical insults. In order to clarify this issue, we developed an in vivo model to apply mechanical stretch to the upper hind limb muscles of adult male rats, and examined for the presence of an intracellular cascade to link mechanical perturbation, NO synthesis, HGF release and satellite cell activation (Sakata et al 2006;Tatsumi et al 2006b). This in vivo stretch system used the weight of the hind portion of rats to stretch inside muscles (vastus, adductor and gracilis muscles) of the left hind limb.…”

Section: In Vivo Studymentioning

confidence: 99%

Mechano‐biology of resident myogenic stem cells: Molecular mechanism of stretch‐induced activation of satellite cells

Tatsumi

Allen

2008

Animal Science Journal

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Satellite cells, resident myogenic stem cells found between the basement membrane and the sarcolemma in postnatal skeletal muscle, are normally quiescent in adult muscles. But when muscle is injured, exercised, overused or mechanically stretched, these cells are activated to enter the cell cycle, divide, differentiate, and fuse with the adjacent muscle fiber. In this way, satellite cells are responsible for regeneration and work‐induced hypertrophy of muscle fibers. Therefore, a mechanism must exist to translate mechanical changes in muscle tissue into chemical signals that can activate satellite cells. This mechanism has not been clearly delineated. Recent in vivo studies and studies of satellite cells and single muscle fibers in culture demonstrated the essential role of hepatocyte growth factor (HGF) and nitric oxide (NO) radical in the activation pathway. These experiments also showed that mechanically stretching cultured satellite cells or living skeletal muscles stimulates satellite cell activation. This is achieved by rapid release of HGF from its tethering in the extracellular matrix and its presentation to the c‐met receptor. HGF release has been shown to depend on NO radical production by nitric oxide synthase (NOS) in satellite cells and/or muscle fibers, and relies on the subsequent upregulation of matrix metalloproteinase (MMP) activity (possibly achieved by its nitrosylation). These results suggest that the activation mechanism is a cascade of molecular events including calcium‐calmodulin formation, NOS activation, NO radical production, MMP activation, HGF release and HGF binding to c‐met. An understanding the ‘mechano‐biology’ of satellite cell activation is essential when planning procedures that could enhance muscle growth and repair. This is particularly important for meat‐animal agriculture and in human health, disease and aging.

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Preliminary experiments on mechanical stretch‐induced activation of skeletal muscle satellite cells in vivo

Cited by 10 publications

References 29 publications

A role for calcium-calmodulin in regulating nitric oxide production during skeletal muscle satellite cell activation

A role for calcium-calmodulin in regulating nitric oxide production during skeletal muscle satellite cell activation

Mechano‐biology of skeletal muscle hypertrophy and regeneration: Possible mechanism of stretch‐induced activation of resident myogenic stem cells

Mechano‐biology of resident myogenic stem cells: Molecular mechanism of stretch‐induced activation of satellite cells

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