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A common somitic origin for embryonic muscle progenitors and satellite cells

Nature volume 435, pages 954–958 (2005)Cite this article

Abstract

In the embryo and in the adult, skeletal muscle growth is dependent on the proliferation and the differentiation of muscle progenitors present within muscle masses. Despite the importance of these progenitors, their embryonic origin is unclear1,2. Here we use electroporation of green fluorescent protein in chick somites3, video confocal microscopy analysis of cell movements, and quail–chick grafting experiments to show that the dorsal compartment of the somite, the dermomyotome, is the origin of a population of muscle progenitors that contribute to the growth of trunk muscles during embryonic and fetal life. Furthermore, long-term lineage analyses indicate that satellite cells, which are known progenitors of adult skeletal muscles4, derive from the same dermomyotome cell population. We conclude that embryonic muscle progenitors and satellite cells share a common origin that can be traced back to the dermomyotome.

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Figure 1: The EMT of the dermomyotome triggers the emergence of a BrdU-positive cell population in the myotome.
Figure 2: Direct translocation of dermomyotome cells into the primary myotome.
Figure 3: Dermomyotome-derived cells contribute to embryonic muscle growth.
Figure 4: Satellite cells are derived from the dermomyotome.

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References

  1. Morgan, J. E. & Partridge, T. A. Muscle satellite cells. Int. J. Biochem. Cell Biol. 35, 1151–1156 (2003)

    Article  CAS  Google Scholar 

  2. Parker, M. H., Seale, P. & Rudnicki, M. A. Looking back to the embryo: defining transcriptional networks in adult myogenesis. Nature Rev. Genet. 4, 497–507 (2003)

    Article  CAS  Google Scholar 

  3. Scaal, M., Gros, J., Lesbros, C. & Marcelle, C. In ovo electroporation of avian somites. Dev. Dyn. 229, 643–650 (2004)

    Article  CAS  Google Scholar 

  4. Mauro, A. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9, 493–495 (1961)

    Article  CAS  Google Scholar 

  5. Gros, J., Scaal, M. & Marcelle, C. A two-step mechanism for myotome formation in chick. Dev. Cell 6, 875–882 (2004)

    Article  CAS  Google Scholar 

  6. Christ, B. & Ordahl, C. P. Early stages of chick somite development. Anat. Embryol. (Berl.) 191, 381–396 (1995)

    Article  CAS  Google Scholar 

  7. Scaal, M. & Christ, B. Formation and differentiation of the avian dermomyotome. Anat. Embryol. (Berl.) 208, 411–424 (2004)

    Article  Google Scholar 

  8. Hauschka, S. in Myology (eds Engel, A. & Franzini-Armstrong, C.) 3–74 (McGraw-Hill, New York, 1994)

    Google Scholar 

  9. Seale, P., Asakura, A. & Rudnicki, M. A. The potential of muscle stem cells. Dev. Cell 1, 333–342 (2001)

    Article  CAS  Google Scholar 

  10. Armand, O., Boutineau, A. M., Mauger, A., Pautou, M. P. & Kieny, M. Origin of satellite cells in avian skeletal muscles. Arch. Anat. Microsc. Morphol. Exp. 72, 163–181 (1983)

    CAS  Google Scholar 

  11. De Angelis, L. et al. Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration. J. Cell Biol. 147, 869–878 (1999)

    Article  CAS  Google Scholar 

  12. Ferrari, G. et al. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279, 1528–1530 (1998)

    Article  ADS  CAS  Google Scholar 

  13. Gussoni, E. et al. Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401, 390–394 (1999)

    ADS  CAS  Google Scholar 

  14. Tosney, K. W., Dehnbostel, D. B. & Erickson, C. A. Neural crest cells prefer the myotome's basal lamina over the sclerotome as a substratum. Dev. Biol. 163, 389–406 (1994)

    Article  CAS  Google Scholar 

  15. Olivera-Martinez, I., Coltey, M., Dhouailly, D. & Pourquié, O. Mediolateral somitic origin of ribs and dermis determined by quail-chick chimeras. Development 127, 4611–4617 (2000)

    CAS  Google Scholar 

  16. Huang, R. & Christ, B. Origin of the epaxial and hypaxial myotome in avian embryos. Anat. Embryol. (Berl.) 202, 369–374 (2000)

    Article  CAS  Google Scholar 

  17. Feldman, J. L. & Stockdale, F. E. Temporal appearance of satellite cells during myogenesis. Dev. Biol. 153, 217–226 (1992)

    Article  CAS  Google Scholar 

  18. Hartley, R. S., Bandman, E. & Yablonka-Reuveni, Z. Skeletal muscle satellite cells appear during late chicken embryogenesis. Dev. Biol. 153, 206–216 (1992)

    Article  CAS  Google Scholar 

  19. Bischoff, R. in Myology (eds Engel, A. & Franzini-Armstrong, C.) 97–119 (McGraw-Hill, New York, 1994)

    Google Scholar 

  20. Sherwood, R. I. et al. Isolation of adult mouse myogenic progenitors: functional heterogeneity of cells within and engrafting skeletal muscle. Cell 119, 543–554 (2004)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank K. Tosney for discussions on the process of dermomyotome EMT, and O. Pourquié, T. Lecuit, S. Kerridge and U. Rothbächer for comments on the manuscript. We acknowledge the help of C. Moretti and P. Weber from the Institute's Imaging Facility and of the Zeiss team. This study was funded by grants from the Actions Concertées Incitatives, the Association Française contre les Myopathies and by the EEU 6th Framework Programme Network of Excellence MYORES. J.G. and M.M. are Fellows from the Ministère de la Recherche et des Technologies.

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Authors and Affiliations

  1. Laboratoire de Génétique et de Physiologie du Développement, Developmental Biology Institute of Marseille, CNRS UMR 6545, Université de la Méditerranée, Campus de Luminy, case 907, 13288, Marseille, Cedex 09, France

    Jérôme Gros, Marie Manceau, Virginie Thomé & Christophe Marcelle

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  1. Jérôme Gros
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  2. Marie Manceau
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  3. Virginie Thomé
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  4. Christophe Marcelle
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Correspondence to Christophe Marcelle.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Legends

Legends to accompany the Supplementary Figures and Supplementary Video. (DOC 23 kb)

Supplementary Video S1

This movie is a time-lapse confocal analysis showing the direct translocation of dermomyotome cells into the myotome. (MOV 7295 kb)

Supplementary Figure S1

Contribution of dermomyotome-derived cells to embryonic muscle growth. (JPG 151 kb)

Supplementary Figure S2

Dermomyotome borders do not significantly contribute to muscle growth. (JPG 79 kb)

Supplementary Figure S3

Satellite cells observed in the muscle masses at E18 derive from the dermomyotome of the manuscript. (JPG 89 kb)

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Gros, J., Manceau, M., Thomé, V. et al. A common somitic origin for embryonic muscle progenitors and satellite cells. Nature 435, 954–958 (2005). https://doi.org/10.1038/nature03572

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