Skeletal myogenic potential of human and mouse neural stem cells (original) (raw)

Nature Neuroscience volume 3, pages 986–991 (2000)Cite this article

Abstract

Distinct cell lineages established early in development are usually maintained throughout adulthood. Thus, adult stem cells have been thought to generate differentiated cells specific to the tissue in which they reside. This view has been challenged; for example, neural stem cells can generate cells that normally originate from a different germ layer. Here we show that acutely isolated and clonally derived neural stem cells from mice and humans could produce skeletal myotubes in vitro and in vivo, the latter following transplantation into adult animals. Myogenic conversion in vitro required direct exposure to myoblasts, and was blocked if neural cells were clustered. Thus, a community effect between neural cells may override such myogenic induction. We conclude that neural stem cells, which generate neurons, glia and blood cells, can also produce skeletal muscle cells, and can undergo various patterns of differentiation depending on exposure to appropriate epigenetic signals in mature tissues.

This is a preview of subscription content, access via your institution

Access options

Subscribe to this journal

Receive 12 print issues and online access

$209.00 per year

only $17.42 per issue

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Additional access options:

Similar content being viewed by others

References

  1. Faust, C & Magnuson, T. Genetic control of gastrulation in the mouse. Curr. Opin. Genet. Dev. 3, 491–498 (1993).
    Article CAS PubMed Google Scholar
  2. Fuchs, E. & Segre, J. A. Stem cells: a new lease on life. Cell 100, 143–155 (2000).
    Article CAS PubMed Google Scholar
  3. Reynolds, B. A. & Weiss, S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707–1710 (1992).
    Article CAS PubMed Google Scholar
  4. Bjornson, C. R. R., Rietze, R. L., Reynolds, B. A., Magli, M. C. & Vescovi, A. L. Turning brain into blood: adult neural stem cells adopt a hematopoietic fate in vivo. Science 283, 534–537 (1999).
    Article CAS PubMed Google Scholar
  5. Clarke, D. et al. Generalized potential of adult neural stem cells. Science 288, 1660–1663 (2000).
    Article CAS PubMed Google Scholar
  6. Ferrari, G. et al. Muscle regeneration by bone-marrow-derived myogenic progenitor. Science 279, 1528–1530 (1998).
    Article CAS PubMed Google Scholar
  7. Gussoni, E. et al. Laminin expression in the mdx mouse restored by stem cell transplantation. Nature 401, 390–394 (1999).
    CAS PubMed Google Scholar
  8. Jackson, K. A, Mi, T. & Goodell, M. A. Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc. Natl. Acad. Sci. USA 96, 14482–14486 (1999).
    Article CAS PubMed PubMed Central Google Scholar
  9. Petersen, B. E. et al. Bone marrow as a potential source of hepatic oval cells. Science 284, 1168–1170 (1999).
    Article CAS PubMed Google Scholar
  10. Kopen, G. C., Prockop, D. J. & Phinney, D. G. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc. Natl. Acad. Sci. USA 96, 10711–10716 (1999).
    Article CAS PubMed PubMed Central Google Scholar
  11. Johansson, C. B. et al. Identification of a neural stem cell in the adult mammalian central nervous system Cell 96, 25–34 (1999).
    Article CAS PubMed Google Scholar
  12. Doetsch, F., Caille, I., Lim, D. A., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703–716 (1999).
    Article CAS PubMed Google Scholar
  13. Kelly, R., Alonso, S. Tajbakhsh, S., Cossu, G. & Buckingham, M. Myosin light chain 3F regulatory sequences confer regionalised cardiac and skeletal muscle expression in transgenic mice. J. Cell Biol. 129, 383–396 (1995).
    Article CAS PubMed Google Scholar
  14. Patapoutian, A. et al. Disruption of the mouse MRF4 gene identifies multiple waves of myogenesis in the myotome. Development 121, 3347–3358 (1995).
    CAS PubMed Google Scholar
  15. Tajbakhsh, S. et al. A population of myogenic cells derived from the mouse neural tube. Neuron 13, 813–821 (1994).
    Article CAS PubMed Google Scholar
  16. Daubas, P. et al. Myf5 is a novel early axonal in the mouse brain and is subjected to post-transcriptional regulation in neurons. Development 127, 319–331 (2000).
    CAS PubMed Google Scholar
  17. McKay, R. Stem cells in the central nervous system. Science 276, 66–71 (1997).
    Article CAS PubMed Google Scholar
  18. Loeffler, M. & Potten, C. S. in Stem Cells (ed. Potten, C. S.) 1–27 (Academic, Cambridge, 1997).
    Book Google Scholar
  19. Temple, S. & Alvarez-Buylla, A. Stem cells in the adult mammalian central nervous system. Curr. Opin. Neurobiol. 9, 135–141 (1999).
    Article CAS PubMed Google Scholar
  20. Gritti, A. et al. Epidermal growth factor and fibroblast growth factor act as redundant mitogenic regulators for the same multipotent stem cell population from the adult mouse subventricular region. J. Neurosci. 19, 3287–3297 (1999).
    Article CAS PubMed PubMed Central Google Scholar
  21. Beauchamp, J. R., Morgan, J. E., Pagel, C. N. & Partridge, T. A. Dynamics of myoblast transplantation reveal a discrete minority of precursors with stem cell-like properties as the myogenic source. J. Cell Biol. 144, 1113–1122 (1999).
    Article CAS PubMed PubMed Central Google Scholar
  22. Johansson, C. B., Svensson, M., Wallstedt, L., Janson, A. M. & Frisen, J. Neural stem cells in the adult human brain. Exp. Cell Res. 253, 733–736 (1999).
    Article CAS PubMed Google Scholar
  23. Vescovi, A. L. et al. Isolation and cloning of multipotential stem cells from the embryonic human CNS and establishment of transplantable human neural stem cell lines by epigenetic stimulation. Exp. Neurol. 156, 71–83 (1999).
    Article CAS PubMed Google Scholar
  24. Eguchi, G. & Kodama, R. Transdifferentiation. Curr. Opin. Cell Biol. 5, 1023–1028 (1993).
    Article CAS PubMed Google Scholar
  25. Beresford, W. A. Direct transdifferentiation: can cells change their phenotype without dividing? Cell Differ. Dev. 29, 81–93 (1990).
    Article CAS PubMed Google Scholar
  26. Moore, M. A. “Turning brain into blood”—Clinical applications of stem-cell research in neurobiology and hematology. N. Engl. J. Med. 341, 605–607 (1999).
    Article CAS PubMed Google Scholar

Download references

Acknowledgements

This work was supported by the EEC (Grants QLRT000894, QLRT-1999-31471), the Italian Telethon Foundation, the Spinal Cord Society (MN) (A.L.V.) and the Fondazione Pasteur-Cenci Bolognetti (G.C.). We thank Don Ward for help with the English.

Author information

Authors and Affiliations

  1. National Neurological Institute, C. Besta, Via Celoria 11, Milan, I-20133, Italy
    Rossella Galli, Marina Mora & Angelo L. Vescovi
  2. Stem Cell Research Institute, H. S. Raffaele, Via Olgettina 58, Milan, I-20133, Italy
    Rossella Galli, Ugo Borello, Angela Gritti, Roberta Fiocco, Giulio Cossu & Angelo L. Vescovi
  3. Fondazione Pasteur-Cenci Bolognetti, Dept. of Histology and Medical Embryology University of Rome, La Sapienza, Via A. Scarpa 14, Rome, I-00161, Italy
    Ugo Borello, M. Giulia Minasi & Marcello Coletta
  4. Department of Biochemistry, University of Washington, Box 357350, Seattle, 98195-7350, Washington, USA
    Christopher Bjornson & Giulio Cossu
  5. Dept. of Experimental Medicine, University of Pavia, Via Forlanini 8, Pavia, I-27100, Italy
    M. Gabriella Cusella De Angelis

Authors

  1. Rossella Galli
    You can also search for this author inPubMed Google Scholar
  2. Ugo Borello
    You can also search for this author inPubMed Google Scholar
  3. Angela Gritti
    You can also search for this author inPubMed Google Scholar
  4. M. Giulia Minasi
    You can also search for this author inPubMed Google Scholar
  5. Christopher Bjornson
    You can also search for this author inPubMed Google Scholar
  6. Marcello Coletta
    You can also search for this author inPubMed Google Scholar
  7. Marina Mora
    You can also search for this author inPubMed Google Scholar
  8. M. Gabriella Cusella De Angelis
    You can also search for this author inPubMed Google Scholar
  9. Roberta Fiocco
    You can also search for this author inPubMed Google Scholar
  10. Giulio Cossu
    You can also search for this author inPubMed Google Scholar
  11. Angelo L. Vescovi
    You can also search for this author inPubMed Google Scholar

Corresponding authors

Correspondence toGiulio Cossu or Angelo L. Vescovi.

Rights and permissions

About this article

Cite this article

Galli, R., Borello, U., Gritti, A. et al. Skeletal myogenic potential of human and mouse neural stem cells.Nat Neurosci 3, 986–991 (2000). https://doi.org/10.1038/79924

Download citation

This article is cited by