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Origin and hierarchy of basal lamina-forming and -non-forming myogenic cells in mouse skeletal muscle in relation to adhesive capacity and Pax7 expression in vitro

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Abstract

As a novel approach to distinguish skeletal myogenic cell populations, basal lamina (BL) formation of myogenic cells was examined in the mouse compensatory enlarged plantaris muscles in vivo and in fiber-bundle cultures in vitro. MyoD+ myogenic cells located inside the regenerative muscle fiber BL were laminin− but interstitial MyoD+ cells were laminin+. This was also confirmed by electron microscopy as structural BL formation. Similar trends were observed in the fiber-bundle cultures including satellite cells and interstitial myogenic cells and laminin+ myogenic cells predominantly showed non-adhesive (non-Ad) behavior with Pax7−, whereas laminin− cells were adhesive (Ad) with Pax7+. Moreover, non-Ad/laminin+ and Ad/laminin− myotubes were also observed and the former type showed spontaneous contractions, while the latter type did not. The origin and hierarchy of Ad/Pax7+/laminin− and non-Ad/Pax7−/laminin+ myogenic cells were also examined using skeletal muscle interstitium-derived CD34+/45− (Sk-34) and CD34−/45− (Sk-DN) multipotent stem cells, which were composed of non-committed myogenic cells with a few (<1%) Pax7+ cells in the Sk-DN cells at fresh isolation. Both cell types were separated by Ad/non-Ad capacity in repetitive culture. As expected, both Ad/Pax7+/laminin− and non-Ad/Pax7−/laminin+ myogenic cells consistently appeared in the Ad and non-Ad cell culture. However, Ad/Pax7+/laminin− cells were repeatedly detected in the non-Ad cell culture, while the opposite phenomenon did not occur. This indicates that the source of non-Ad/ Pax7−/laminin+ myogenic cells was present in the Sk-34 and Sk-DN stem cells and they were able to produce Ad/ Pax7+/ laminin− myogenic cells during myogenesis as primary myoblasts and situated hierarchically upstream of the latter cells.

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Authors and Affiliations

  1. Muscle Physiology and Cell Biology Unit, Department of Regenerative Medicine, Division of Basic Clinical Science, Tokai University School of Medicine, 143 Shimokasuya, Isehara, Kanagawa, 259-1193, Japan

    Tetsuro Tamaki, Kayoko Tono, Yoshiyasu Uchiyama, Yoshinori Okada, Maki Masuda, Shuichi Soeda, Masahiro Nitta & Akira Akatsuka

  2. Department of Orthopedics, Tokai University School of Medicine, 143 Shimokasuya, Isehara, Kanagawa, 259-1143, Japan

    Yoshiyasu Uchiyama

  3. Teaching & Research Support Center, Tokai University School of Medicine, 143 Shimokasuya, Isehara, Kanagawa, 259-1143, Japan

    Yoshinori Okada & Akira Akatsuka

  4. Department of Urology, Tokai University School of Medicine, 143 Shimokasuya, Isehara, Kanagawa, 259-1143, Japan

    Shuichi Soeda & Masahiro Nitta

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  1. Tetsuro Tamaki
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  2. Kayoko Tono
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  3. Yoshiyasu Uchiyama
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  4. Yoshinori Okada
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  5. Maki Masuda
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  8. Akira Akatsuka
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Correspondence to Tetsuro Tamaki.

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Supplemental Figure 1

Characteristics of C2C12 mouse myoblast cell line. C2C12 cells were purchased from RIKEN Cell Bank (Ibaragi, Japan). Double-labeling for MyoD and laminin (a) and myogenin and laminin (b) showed that MyoD+ and/or myogenin+ myogenic cells were adhesive in culture and mostly spindle-shaped but laminin- (a and b). Electron microscopy also indicated no basal lamina structure with a few contractile components in single C2C12 cells (c) and their myotubes (d). These characteristics correspond to the Ad/Pax7+ myogenic cells in Sk-34 and Sk-DN cell cultures (see Figs. 2 and 4). Bars in a and b = 10 μm, c and d = 2 μm (TIFF 3865 kb) (GIF 243 kb)

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Tamaki, T., Tono, K., Uchiyama, Y. et al. Origin and hierarchy of basal lamina-forming and -non-forming myogenic cells in mouse skeletal muscle in relation to adhesive capacity and Pax7 expression in vitro. Cell Tissue Res 344, 147–168 (2011). https://doi.org/10.1007/s00441-010-1127-9

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