Growth and differentiation potential of main- and side-population cells derived from murine skeletal muscle

Tamaki, Toru; Akatsuka, Akira; Okada, Yoshinori; Matsuzaki, Yuji; Okano, Hideyuki; Kimura, Minoru

doi:10.1016/s0014-4827(03)00376-8

Cited by 76 publications

(149 citation statements)

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“…The Desmin ϩ clones were dispersed and plated on collagencoated glass coverslips in GM for 24 h to adhere and proliferate, or in differentiation medium (DM; see Materials and Methods) for 72 h to induce myogenic differentiation. Immunocytochemistry revealed that, of the five clones analyzed, all of them grown for 12 h in GM were positive for MyoD ( Figure 1A), the markers of myogenic lineage-committed myoblasts (Kablar et al, 1999;Jankowski et al, 2002;Tamaki et al, 2003), but were negative for Nestin ( Figure 1B), a muscle-derived NSC marker (Romero-Ramos et al, 2002). They also were negative for CD34 ( Figure 1B) and CD45 ( Figure 1B), the markers of muscle-derived CD45 ϩ /CD34 ϩ SP cells/MDSCs (Asakura et al, 2002;Jankowski et al, 2002;Qu-Petersen et al, 2002;Tamaki et al, 2003).…”

Section: Myogenic Lineage-committed Myoblast Clonesmentioning

confidence: 99%

“…Adult skeletal myoblasts have long been considered as myogenic lineage-committed cells with either self-renewing or differentiating into multinucleated myotubes in vitro (Jankowski et al, 2002;Tamaki et al, 2003). Myoblast fate is critically dependent on the myogenic regulatory factors (MRFs): MyoD, Myf5, myogenin, and Mrf4, which have a well-defined role in orchestrating skeletal muscle development and differentiation.…”

Section: Introductionmentioning

confidence: 99%

“…Especially, the recent reports have shown that ectopic expression of msx1 in C2C12 myotubes can induce dedifferentiation of the myotubes to produce multipotent mononucleated cells (Odelberg et al, 2000), and a 2,6-disubstituted purine, reversine, can also induce dedifferentiation of C2C12 myoblasts to become mesenchymal progenitor cells (Chen et al, 2004). However, the C2C12 myogenic line may be heterogeneous because there is this novel evidence for a resident subset of cells with side population (SP) phenotype in the C2C12 line (Benchaouir et al, 2004), whereas SP cells themselves are growth-arrested and delayed in their ability to differentiate with behaving as multipotent stem cells (Zhou et al, 2001;Jankowski et al, 2002;Tamaki et al, 2003). In addition, whether human skeletal myoblasts can dedifferentiate is unclear.…”

Section: Introductionmentioning

confidence: 99%

“…To exclude the presence of fibroblasts and mesenchymal stem cells (MSCs) in the myoblast clones, NIH3T3 and human MSCs were also cultured in the same myoblast GM or DM to determine the myogenic specificity of these cells. Furthermore, the Nestin ϩ NSCs (neural stem cells) and CD45 ϩ /CD34 ϩ HSCs (hemopoietic stem cells), which were used as the positive control of the immunocytochemical analysis with anti-Nestin, anti-CD34, and anti-CD45 antibodies to exclude the presence of previously reported progenitor/stem cells isolated from adult skeletal muscle, such as Nestin ϩ neuronal differentiation of stem cells (Romero-Ramos et al, 2002), and CD45 ϩ /CD34 ϩ SP cells/MDSCs (Asakura et al, 2002;Jankowski et al, 2002;Qu-Petersen et al, 2002;Tamaki et al, 2003) were plated onto the collagen-coated glass coverslips for 12 h to adhere. The control human MSCs and HSCs were gifts from Professor XiaoDan Guo and Xiaoxia Jiang, Ph.D., whereas NSCs of adult rat were isolated as previously described (Xu et al, 2003).…”

mentioning

confidence: 99%

“…These clones were subjected to immunocytochemical analysis by staining with Desmin, a marker of myogenic lineage-committed myoblasts. Only the Desmin ϩ clones were allowed to further propagated and five of these clones were analyzed.To characterize the Desmin ϩ clones better, we analyzed them for production of markers associated with other progenitor/stem cells which have been isolated and identified from adult skeletal muscle, such as muscle satellite cells (Jankowski et al, 2002), the precursor cells of myoblasts, SP (side population) cells (Asakura et al, 2002;Jankowski et al, 2002;Tamaki et al, 2003), MDSCs (muscle-derived stem) cells (Jankowski et al, 2002;Qu-Petersen et al, 2002), and NSCs (neural stem cells; Romero-Ramos et al, 2002). The Desmin ϩ clones were dispersed and plated on collagencoated glass coverslips in GM for 24 h to adhere and proliferate, or in differentiation medium (DM; see Materials and Methods) for 72 h to induce myogenic differentiation.…”

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confidence: 99%

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Dedifferentiation of Adult Human Myoblasts Induced by Ciliary Neurotrophic Factor In Vitro

Chen

Mao

Liu³

et al. 2005

MBoC

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Ciliary neurotrophic factor (CNTF) is primarily known for its important cellular effects within the nervous system. However, recent studies indicate that its receptor can be highly expressed in denervated skeletal muscle. Here, we investigated the direct effect of CNTF on skeletal myoblasts of adult human. Surprisingly, we found that CNTF induced the myogenic lineage-committed myoblasts at a clonal level to dedifferentiate into multipotent progenitor cells-they not only could proliferate for over 20 passages with the expression absence of myogenic specific factors Myf5 and MyoD, but they were also capable of differentiating into new phenotypes, mainly neurons, glial cells, smooth muscle cells, and adipocytes. These "progenitor cells" retained their myogenic memory and were capable of redifferentiating into myotubes. Furthermore, CNTF could activate the p44/p42 MAPK and down-regulate the expression of myogenic regulatory factors (MRFs). Finally, PD98059, a specific inhibitor of p44/p42 MAPK pathway, was able to abolish the effects of CNTF on both myoblast fate and MRF expression. Our results demonstrate the myogenic lineage-committed human myoblasts can dedifferentiate at a clonal level and CNTF is a novel regulator of skeletal myoblast dedifferentiation via p44/p42 MAPK pathway. INTRODUCTIONAdult skeletal myoblasts have long been considered as myogenic lineage-committed cells with either self-renewing or differentiating into multinucleated myotubes in vitro (Jankowski et al., 2002;Tamaki et al., 2003). Myoblast fate is critically dependent on the myogenic regulatory factors (MRFs): MyoD, Myf5, myogenin, and Mrf4, which have a well-defined role in orchestrating skeletal muscle development and differentiation. Gene targeting in mice has illustrated the essential role for MRFs: Myf5 and MyoD is critical to establishing the myogenic cell lineage and producing committed, undifferentiated myoblasts (Kablar et al., 1999), whereas myogenin has an important role in initiating differentiation (Hasty et al., 1993); Mrf4 regulates terminal differentiation and myofiber maintenance (Patapoutian et al., 1995). Gene targeting in mice has illustrated the essential role for Myf5 and MyoD in myoblast fates. In MyoDϪ/Ϫ and/or Myf5Ϫ/Ϫ knockout mice, muscle precursors acquire nonmuscle cell fates (Kablar et al., 1999) and become multipotential stem cells or a progenitor compartment (Parker et al., 2003). Early histological studies indicated that muscle fibers at the amputation plane of urodele amphibians might dedifferentiate by budding off mononucleate cells from syncytial muscle cells (Echeverri and Tanaka, 2002). Recent studies suggest that dedifferentiation may be also possible in mammalian system (Odelberg et al., 2000;Tsai et al., 2002;Chen et al., 2004). Especially, the recent reports have shown that ectopic expression of msx1 in C2C12 myotubes can induce dedifferentiation of the myotubes to produce multipotent mononucleated cells (Odelberg et al., 2000), and a 2,6-disubstituted purine, reversine, can also induce dedifferentia...

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Section: Myogenic Lineage-committed Myoblast Clonesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Dedifferentiation of Adult Human Myoblasts Induced by Ciliary Neurotrophic Factor In Vitro

Chen

Mao

Liu³

et al. 2005

MBoC

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Cancer Stem Cell Side Populations

Balicki

Beaulieu

2008

Cancer Stem Cells

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Defining the heterogeneity of skeletal muscle‐derived side and main population cells isolated immediately ex vivo

Kallestad¹,

McLoon²

2009

Journal Cellular Physiology

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Myoblast transfer therapy for Duchenne muscular dystrophy (DMD) largely fails due to cell death and inability of transplanted cells to engraft in diseased muscles. One method attempting to enrich for cell subpopulations is the Hoechst 33342 dye exclusion assay, yielding a side population (SP) thought to be progenitor enriched and a main population (MP). However, in vitro and transplant studies yielded inconsistent results relative to downstream progeny. Cell surface markers expressed by skeletal muscle-derived MP and SP cells have not been fully characterized directly ex vivo. Using flow cytometry, MP and SP cells were characterized based on their expression of several well-accepted progenitor cell antigens. Both the MP and SP populations are heterogeneous and overlapping in the cells they contain. The percentages of cells in each population vary with species and specific muscle examined. MP and SP populations contain both satellite and multipotent progenitor cells, based on expression of CD34, Sca-1, Pax7, and M-cadherin. Thus, isolation using this procedure cannot be used to predict downstream differentiation outcomes, and explains the conflicting literature on these cells. Hoechst dye also results in significant mortality of sorted cells. As defined subpopulations are easily obtained using flow cytometry, sorting immediately ex vivo based on accepted myogenic precursor cell markers will yield superior results in terms of cell homogeneity for transplantation therapy.Skeletal muscle possesses a remarkable ability to remodel and repair after injury and in disease. The repair process is mainly accomplished through activation of satellite cells along the myofibers, which differentiate and fuse into damaged areas. Although the satellite cell was described nearly 50 years ago (Mauro, 1961), the genotype and maintenance of these regenerative cells are not well understood. In dystrophic and sarcopenic muscles, the satellite cell pool becomes exhausted leading to severe and permanent muscle degeneration Renault et al., 2000). Many investigations have sought a method of replacing the satellite cell population through transplantation. Adult-derived myoblasts have been investigated for their therapeutic potential in the treatment of dystrophies, but unfortunately, this approach has been largely unsuccessful due to relatively rapid death of the majority of the transplanted cells Miller et al., 1997;Skuk et al., 2002). In part, this is due to immune rejection of the transplanted cells (Watt, 1990;Rando and Blau, 1994). However, immune system rejection only partly explains the failure of myoblast therapy, as even transplantation between monozygotic twin girl carriers of the Duchenne muscular dystrophy (DMD) gene does not result in long-term survival of the transplanted cells (Tremblay et al., 1993). In addition, transplanted myoblasts do not disperse very well within treated muscles (Lipton and Schultz, 1979;Morgan et al., 1987; Huard et al., 1994), and their expansion in vitro is limited by replicative senescence (K...

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Growth and differentiation potential of main- and side-population cells derived from murine skeletal muscle

Cited by 76 publications

References 19 publications

Dedifferentiation of Adult Human Myoblasts Induced by Ciliary Neurotrophic Factor In Vitro

Dedifferentiation of Adult Human Myoblasts Induced by Ciliary Neurotrophic Factor In Vitro

Cancer Stem Cell Side Populations

Defining the heterogeneity of skeletal muscle‐derived side and main population cells isolated immediately ex vivo

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