Molecular Signature of Quiescent Satellite Cells in Adult Skeletal Muscle

Fukada, So‐ichiro; Uezumi, Akiyoshi; Ikemoto, Madoka; Masuda, S.; Segawa, Masashi; Tanimura, Naoki; Yamamoto, Hiroshi; Miyagoe-Suzuki, Yuko; Takeda, Shin’ichi

doi:10.1634/stemcells.2007-0019

Cited by 418 publications

(415 citation statements)

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“…Eleven of these Pax3/7-inducible genes have been observed previously to be induced by Pax7 in C2C12 cells (McKinnell et al, 2008) (Supplemental Table 1). In addition, 28 of the genes we identified were shown previously to be expressed at higher levels in quiescent versus activated satellite cells (Fukada et al, 2007) (Supplemental Table 1), correlating with the greater level of expression of Pax7 in quiescent versus activated satellite cells ( Figure 1A). The HLH inhibitor Id3 was one of the genes most highly induced by Pax7 in C2C12 cells cultured in low serum, showing a 33-fold induction and a high absolute level of expression (3168 U).…”

Section: Identification Of Pax3/7 Transcriptional Targets In C2c12 Cellssupporting

confidence: 54%

“…In this light, it is interesting that quiescent satellite cells express relatively robust levels of both Id2 and Id3 (this study) and several members of the hairy/enhancer of split family, including Heyl (Fukada et al, 2007), Hes1 and Hey1 (Wagers,unpublished observations). It is possible that high-level expression of Id2 and Id3 in quiescent satellite cells acts to either block the activity of Myf5 that is readily expressed (at least at the RNA level) in at least 90% of quiescent satellite cells (Kuang et al, 2007) or to maintain the expression of the Notchinduced transcriptional repressors Hes1, Hey1, and/or Heyl, which in turn may block expression of MyoD and Myf5.…”

Section: Discussionmentioning

confidence: 81%

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Id3 Is a Direct Transcriptional Target of Pax7 in Quiescent Satellite Cells

Kumar

Shadrach

Wagers

et al. 2009

MBoC

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INTRODUCTIONPax3 and Pax7 are two closely related transcription factors that are expressed in the dermomyotome, and they have been shown to be essential for generation of all fetal trunk musculature . Pax3/7-expressing dermomyotomal cells have recently been shown to give rise to skeletal muscle progenitors, termed satellite cells, in the adult (Gros et al., 2005;Kassar-Duchossoy et al., 2005;Relaix et al., 2005;Schienda et al., 2006). Satellite cells are a small population of myogenic progenitors that reside between the sarcolemma and basal lamina of the muscle fiber, and they play a crucial role in postnatal muscle growth and regeneration (reviewed in Zammit et al., 2006). Following skeletal muscle injury or exercise-induced activation, the normally quiescent Pax7-expressing satellite cells proliferate extensively and up-regulate expression of MyoD (Smith et al., 2001;Yan et al., 2003;Montarras et al., 2005) and Myf-5 (Conboy and Rando, 2002;Yan et al., 2003), before differentiation into skeletal muscle.Pax3 and Pax7 are members of the Pax transcription factor family and contain both paired (PD) and homeodomain (HD) DNA binding motifs. Pax3 and Pax7 can bind to DNA sequences containing either a consensus paired domain binding site (GTCAC A/G C/G A/T T/C) or a homeodomain binding site (ATTA) (Chalepakis et al., 1994;Chalepakis and Gruss, 1995). Pax3 and Pax7 activate MyoD expression (Maroto et al., 1997;Tajbakhsh et al., 1997;Relaix et al., 2003Relaix et al., , 2004, and recently Pax3 has been shown to directly bind sequences that regulate the expression of either MyoD in C2C12 cells (Hu et al., 2008) or Myf-5 during development of hypaxial muscle (Bajard et al., 2006). Although it is clear that Pax3/7 can directly induce the expression of Myf5 (Bajard et al., 2006), MyoD (Hu et al., 2008), and fibroblast growth factor receptor 4 (Lagha et al., 2008), other relevant targets for Pax3/7 in satellite cells have yet to be identified. To identify potential targets for Pax3/7 in satellite cells, we examined the transcriptional profile of genes induced by these transcription factors in the C2C12 muscle cell line. Of the genes identified, we found that a subset were also expressed in quiescent satellite cells and therefore they could potentially be direct targets of Pax7 in these cells. In this report, we focus on two such putative Pax3/7 transcriptional targets, inhibitor of DNA binding (Id) 2 and Id3, which we found to be expressed in quiescent satellite cells. We report that Pax3/7 can drive expression of both Id2 and Id3 in C2C12 cells under low serum conditions, that the Id3 promoter contains a conserved Pax3/7 binding site, and that Pax3/7 can activate expression of a reporter construct driven by the Id3 promoter. In addition, we demonstrate that Pax7 is normally bound to the Id3 promoter in quiescent satellite cells and that short hairpin RNA (shRNA)-mediated knockdown of Pax7 expression in cultured satellite cells Abbreviations used: C1R, complement component 1 R subunit; ChIP, chromatin immunoprecipitation; CS...

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Section: Identification Of Pax3/7 Transcriptional Targets In C2c12 Cellssupporting

confidence: 54%

Section: Discussionmentioning

confidence: 81%

Id3 Is a Direct Transcriptional Target of Pax7 in Quiescent Satellite Cells

Kumar

Shadrach

Wagers

et al. 2009

MBoC

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“…In muscle development, no detailed expression analysis of teneurin family members, except for Ten‐4, has been reported. However, in a genome‐wide expression analysis by microarray, Ten‐3 is expressed in quiescent satellite cells, and an attenuation of its expression level is observed in activated satellite cells 21. This expression pattern of Ten‐3 is similar to that of Ten‐4.…”

Section: Discussionmentioning

confidence: 80%

“…A genome‐wide gene expression analysis revealed that a specific expression of Ten‐4 is detected in quiescent satellite cells, and that the expression is diminished in activated satellite cells, similar to that of calcitonin receptor, a marker for quiescent satellite cells 21. Analysis of Ten‐4 expression pattern by immunostaining showed that all the quiescent satellite cells expressed Ten‐4 at the neonatal stage, while the calcitonin receptor was expressed only in part of the cells 22.…”

Section: Discussionmentioning

confidence: 99%

Muscle Satellite Cell Protein Teneurin-4 Regulates Differentiation During Muscle Regeneration

et al. 2015

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Satellite cells are maintained in an undifferentiated quiescent state, but during muscle regeneration they acquire an activated stage, and initiate to proliferate and differentiate as myoblasts. The transmembrane protein teneurin‐4 (Ten‐4) is specifically expressed in the quiescent satellite cells; however, its cellular and molecular functions remain unknown. We therefore aimed to elucidate the function of Ten‐4 in muscle satellite cells. In the tibialis anterior (TA) muscle of Ten‐4‐deficient mice, the number and the size of myofibers, as well as the population of satellite cells, were reduced with/without induction of muscle regeneration. Furthermore, we found an accelerated activation of satellite cells in the regenerated Ten‐4‐deficient TA muscle. The cell culture analysis using primary satellite cells showed that Ten‐4 suppressed the progression of myogenic differentiation. Together, our findings revealed that Ten‐4 functions as a crucial player in maintaining the quiescence of muscle satellite cells. Stem Cells 2015;33:3017–3027

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“…Si, jusqu'à récemment, l'expression de la dystrophine et des protéines du complexe dystroglycane (DGC) était restreinte aux fibres musculaires, l'analyse par puce à ADN a révélé que les cellules satellites expriment également la plupart des composants du DGC [7,8]. Les cellules satellites expriment ainsi la protéine dystroglycane (Dag1) qui joue un rôle clé dans leur bon fonctionnement [9].…”

Section: Rôle Du Complexe Dystroglycane Dans Les Cellules Satellitesunclassified