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.
Subscribe to Journal
Get full journal access for 1 year
only $3.83 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Morgan, J. E. & Partridge, T. A. Muscle satellite cells. Int. J. Biochem. Cell Biol. 35, 1151–1156 (2003)
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)
Scaal, M., Gros, J., Lesbros, C. & Marcelle, C. In ovo electroporation of avian somites. Dev. Dyn. 229, 643–650 (2004)
Mauro, A. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9, 493–495 (1961)
Gros, J., Scaal, M. & Marcelle, C. A two-step mechanism for myotome formation in chick. Dev. Cell 6, 875–882 (2004)
Christ, B. & Ordahl, C. P. Early stages of chick somite development. Anat. Embryol. (Berl.) 191, 381–396 (1995)
Scaal, M. & Christ, B. Formation and differentiation of the avian dermomyotome. Anat. Embryol. (Berl.) 208, 411–424 (2004)
Hauschka, S. in Myology (eds Engel, A. & Franzini-Armstrong, C.) 3–74 (McGraw-Hill, New York, 1994)
Seale, P., Asakura, A. & Rudnicki, M. A. The potential of muscle stem cells. Dev. Cell 1, 333–342 (2001)
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)
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)
Ferrari, G. et al. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279, 1528–1530 (1998)
Gussoni, E. et al. Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401, 390–394 (1999)
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)
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)
Huang, R. & Christ, B. Origin of the epaxial and hypaxial myotome in avian embryos. Anat. Embryol. (Berl.) 202, 369–374 (2000)
Feldman, J. L. & Stockdale, F. E. Temporal appearance of satellite cells during myogenesis. Dev. Biol. 153, 217–226 (1992)
Hartley, R. S., Bandman, E. & Yablonka-Reuveni, Z. Skeletal muscle satellite cells appear during late chicken embryogenesis. Dev. Biol. 153, 206–216 (1992)
Bischoff, R. in Myology (eds Engel, A. & Franzini-Armstrong, C.) 97–119 (McGraw-Hill, New York, 1994)
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)
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.
The authors declare that they have no competing financial interests.
Legends to accompany the Supplementary Figures and Supplementary Video. (DOC 23 kb)
This movie is a time-lapse confocal analysis showing the direct translocation of dermomyotome cells into the myotome. (MOV 7295 kb)
Contribution of dermomyotome-derived cells to embryonic muscle growth. (JPG 151 kb)
Dermomyotome borders do not significantly contribute to muscle growth. (JPG 79 kb)
Satellite cells observed in the muscle masses at E18 derive from the dermomyotome of the manuscript. (JPG 89 kb)
About this article
Cite this article
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
WIREs Developmental Biology (2020)
Poor maternal nutrition during gestation in sheep alters prenatal muscle growth and development in offspring
Journal of Animal Science (2020)
Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms (2020)
Stem Cells International (2019)