Possible implication of satellite cells in regenerative motoneuritogenesis: HGF upregulates neural chemorepellent Sema3A during myogenic differentiation

Ryuichi Tatsumi, Yoriko Sankoda, Judy E. Anderson, Yusuke Sato, Wataru Mizunoya, Naomi Shimizu, Takahiro Suzuki, Michiko Yamada, Robert P. Rhoads, Yoshihide Ikeuchi, Ronald E. Allen

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Abstract

Regenerative coordination and remodeling of the intramuscular motoneuron network and neuromuscular connections are critical for restoring skeletal muscle function and physiological properties. The regulatory mechanisms of such coordination remain unclear, although both attractive and repulsive axon guidance molecules may be involved in the signaling pathway. Here we show that expression of a neural secreted chemorepellent semaphorin 3A (Sema3A) is remarkably upregulated in satellite cells of resident myogenic stem cells that are positioned beneath the basal lamina of mature muscle fibers, when treated with hepatocyte growth factor (HGF), established as an essential cue in muscle fiber growth and regeneration. When satellite cells were treated with HGF in primary cultures of cells or muscle fibers, Sema3A message and protein were upregulated as revealed by reverse transcriptionpolymerase chain reaction and immunochemical studies. Other growth factors had no inductive effect except for a slight effect of epidermal growth factor treatment. Sema3A upregulation was HGF dose dependent with a maximum (about 7- to 8-fold units relative to the control) at 10-25 ng/ml and occurred exclusively at the early-differentiation stage, as characterized by the level of myogenin expression and proliferation (bromodeoxyuridine incorporation) of the cells. Neutralizing antibody to the HGF-specific receptor, c-met, did not abolish the HGF response, indicating that c-met may not mediate the Sema3A expression signaling. Finally, in vivo Sema3A was upregulated in the differentiation phase of satellite cells isolated from muscle regenerating following crush injury. Overall, the data highlight a heretofore unexplored and active role for satellite cells as a key source of Sema3A expression triggered by HGF, hence suggesting that regenerative activity toward motor innervation may importantly reside in satellite cells and could be a crucial contributor during postnatal myogenesis.

Original languageEnglish
JournalAmerican Journal of Physiology - Cell Physiology
Volume297
Issue number2
DOIs
Publication statusPublished - Aug 1 2009

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Semaphorin-3A
Hepatocyte Growth Factor
Up-Regulation
Muscles
Skeletal Muscle Satellite Cells
Proto-Oncogene Proteins c-met
Myogenin
Primary Cell Culture
Muscle Development
Motor Neurons
Bromodeoxyuridine
Neutralizing Antibodies
Epidermal Growth Factor
Basement Membrane
Muscle Cells
Cues
Regeneration
Intercellular Signaling Peptides and Proteins
Skeletal Muscle
Motor Activity

All Science Journal Classification (ASJC) codes

  • Physiology
  • Cell Biology

Cite this

Possible implication of satellite cells in regenerative motoneuritogenesis : HGF upregulates neural chemorepellent Sema3A during myogenic differentiation. / Tatsumi, Ryuichi; Sankoda, Yoriko; Anderson, Judy E.; Sato, Yusuke; Mizunoya, Wataru; Shimizu, Naomi; Suzuki, Takahiro; Yamada, Michiko; Rhoads, Robert P.; Ikeuchi, Yoshihide; Allen, Ronald E.

In: American Journal of Physiology - Cell Physiology, Vol. 297, No. 2, 01.08.2009.

Research output: Contribution to journalArticle

Tatsumi, Ryuichi ; Sankoda, Yoriko ; Anderson, Judy E. ; Sato, Yusuke ; Mizunoya, Wataru ; Shimizu, Naomi ; Suzuki, Takahiro ; Yamada, Michiko ; Rhoads, Robert P. ; Ikeuchi, Yoshihide ; Allen, Ronald E. / Possible implication of satellite cells in regenerative motoneuritogenesis : HGF upregulates neural chemorepellent Sema3A during myogenic differentiation. In: American Journal of Physiology - Cell Physiology. 2009 ; Vol. 297, No. 2.
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AU - Anderson, Judy E.

AU - Sato, Yusuke

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AU - Shimizu, Naomi

AU - Suzuki, Takahiro

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AU - Allen, Ronald E.

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AB - Regenerative coordination and remodeling of the intramuscular motoneuron network and neuromuscular connections are critical for restoring skeletal muscle function and physiological properties. The regulatory mechanisms of such coordination remain unclear, although both attractive and repulsive axon guidance molecules may be involved in the signaling pathway. Here we show that expression of a neural secreted chemorepellent semaphorin 3A (Sema3A) is remarkably upregulated in satellite cells of resident myogenic stem cells that are positioned beneath the basal lamina of mature muscle fibers, when treated with hepatocyte growth factor (HGF), established as an essential cue in muscle fiber growth and regeneration. When satellite cells were treated with HGF in primary cultures of cells or muscle fibers, Sema3A message and protein were upregulated as revealed by reverse transcriptionpolymerase chain reaction and immunochemical studies. Other growth factors had no inductive effect except for a slight effect of epidermal growth factor treatment. Sema3A upregulation was HGF dose dependent with a maximum (about 7- to 8-fold units relative to the control) at 10-25 ng/ml and occurred exclusively at the early-differentiation stage, as characterized by the level of myogenin expression and proliferation (bromodeoxyuridine incorporation) of the cells. Neutralizing antibody to the HGF-specific receptor, c-met, did not abolish the HGF response, indicating that c-met may not mediate the Sema3A expression signaling. Finally, in vivo Sema3A was upregulated in the differentiation phase of satellite cells isolated from muscle regenerating following crush injury. Overall, the data highlight a heretofore unexplored and active role for satellite cells as a key source of Sema3A expression triggered by HGF, hence suggesting that regenerative activity toward motor innervation may importantly reside in satellite cells and could be a crucial contributor during postnatal myogenesis.

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