Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Muscle-derived stem cells

Abstract

The existence of cells with stem cell-like abilities derived from various tissues can now be extended to include the skeletal muscle compartment. Although researchers have focused on the utilization of these cells with regard to their myogenic capacity, initially exploring more efficient cellular therapy treatments for muscular dystrophy, it is becoming increasingly apparent that such cells may one day be used in the treatment of non-myogenic disorders. Evidence regarding the existence and differentiation capacity of muscle-derived stem cells is discussed, along with current theories regarding their proposed position within the myogenic hierarchy.

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

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1
Figure 2

References

  1. Ham R, Veomett M. . Mechanisms of Development. CV Mosby: St Louis 1980, pp 5–107

    Google Scholar 

  2. Osawa M, Hanada K, Hamada H, Nakauchi H . Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell Science 1996 273: 242–245

    Article  CAS  Google Scholar 

  3. Rasko J et al. The flt3/flk-2 ligand: receptor distribution and action on murine haemopoietic cell survival and proliferation Leukemia 1995 9: 2058–2066

    CAS  Google Scholar 

  4. Okada S et al. In vivo and in vitro stem cell function of c-kit- and Sca-1-positive murine hematopoietic cells Blood 1992 12: 3044–3050

    Google Scholar 

  5. Mauro A . Satellite cells of skeletal muscle fibers J Biochem Biophys Cytol 1961 9: 493–498

    Article  CAS  Google Scholar 

  6. Lipton BH, Schultz E . Developmental fate of skeletal muscle satellite cells Science 1979 205: 1292–1294

    Article  CAS  Google Scholar 

  7. Cossu G et al. In vitro differentiation of satellite cells isolated from normal and dystrophic mammalian muscles. A comparison with embryonic myogenic cells Cell Differ 1980 9: 357–368

    Article  CAS  Google Scholar 

  8. Bischoff R . The satellite cell and muscle regeneration Engel AG, Franszini-Armstrong C (eds); Myogenesis McGraw-Hill 1994 pp 97–118

  9. Yablonka-Reuveni Z, Rivera AJ . Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers Dev Biol 1994 164: 588–603

    Article  CAS  Google Scholar 

  10. Cornelison D, Wold B . Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells Dev Biol 1997 191: 270–283

    Article  CAS  Google Scholar 

  11. Beauchamp J et al. Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells J Cell Biol 2000 151: 1221–1233

    Article  CAS  Google Scholar 

  12. Yoshida N et al. Cell heterogeneity upon myogenic differentiation: down-regulation of MyoD and Myf5 generates ‘reserve cells’ J Cell Sci 1998 111: 769–779

    CAS  PubMed  Google Scholar 

  13. Miller J, Schafer L, Dominov J . Seeking muscle stem cells Curr Topic Dev Biol 1999 43: 191–214

    Article  CAS  Google Scholar 

  14. Seale P, Rudnicki M . A new look at the origin, function, and ‘stem-cell’ status of muscle satellite cells Dev Biol 2000 218: 115–124

    Article  CAS  Google Scholar 

  15. Pate DW et al. Isolation and differentiation of mesenchymal stem cells from rabbit muscle Clin Res 1993 41: 374A

    Google Scholar 

  16. Young HE et al. Pluripotent mesenchymal stem cells reside within avian connective tissue matrices In Vitro Cell Dev Biol Anim 1993 29A: 723–736

    Article  CAS  Google Scholar 

  17. Rogers JJ et al. Differentiation factors induce expression of muscle, fat, cartilage, and bone in a clone of mouse pluripotent mesenchymal stem cells Am Surg 1995 61: 231–236

    CAS  PubMed  Google Scholar 

  18. Williams JT et al. Cells isolated from adult human skeletal muscle capable of differentiating into multiple mesodermal phenotypes Am Surg 1999 65: 22–26

    CAS  PubMed  Google Scholar 

  19. Young HE et al. Human pluripotent and progenitor cells display cell surface cluster differentiation markers CD10, CD13, CD56 and MHC class-I Proc Soc Exp Biol Med 1999 221: 63–71

    Article  CAS  Google Scholar 

  20. Pittenger MF et al. Multilineage potential of adult human mesenchymal stem cells Science 1999 284: 143–147

    Article  CAS  Google Scholar 

  21. Katagiri T et al. Bone morphogenic protein-2 converts differentiation pathway of C2C12 myoblasts into the osteoblast lineage J Cell Biol 1994 127: 1755–1766

    Article  CAS  Google Scholar 

  22. Lee J et al. Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing J Cell Biol 2000 150: 1085–1099

    Article  CAS  Google Scholar 

  23. Bosch P et al. Osteoprogenitor cells within skeletal muscle J Orth Res 2000 18: 933–944

    Article  CAS  Google Scholar 

  24. Musgrave DS et al. Ex vivo gene therapy to produce bone using different cell types Clin Orth 2000 378: 290–305

    Article  Google Scholar 

  25. Musgrave DS et al. Ex vivo gene therapy to produce bone using different cell types Adachi N et al. Muscle-derived cell-based ex vivo gene therapy for the treatment of full-thickness articular cartilage defects. J Rheumatol (in press)

  26. Gussoni E et al. Dystrophin expression in the mdx mouse restored by stem cell transplantation Nature 1999 401: 390–394

    CAS  Google Scholar 

  27. Jackson KA, Mi T, Goodell MA . Hematopoietic potential of stem cells isolated from murine skeletal muscle Proc Natl Acad Sci USA 1999 96: 14482–14486

    Article  CAS  Google Scholar 

  28. Seale P et al. Pax7 is required for the specification of myogenic satellite cells Cell 2000 102: 777–786

    Article  CAS  Google Scholar 

  29. Partridge TA, Beauchamp JR, Morgan JE . Conversion of mdx myofibers from dystrophin-negative to positive by injection of normal myoblasts Nature 1989 337: 176–179

    Article  CAS  Google Scholar 

  30. Beauchamp JR, Morgan JE, Pagel CN, Partridge TA . Quantitative studies of efficacy of myoblast transplantation Muscle Nerve 1994 18: (Suppl) 261

    Google Scholar 

  31. Huard J et al. Gene transfer into skeletal muscles by isogenic myoblasts Hum Gene Ther 1994 5: 949–958

    Article  CAS  Google Scholar 

  32. Fan Y, Maley M, Beilharz M, Grounds M . Rapid death of injected myoblasts in myoblast transfer therapy Muscle Nerve 1996 19: 853–860

    Article  CAS  Google Scholar 

  33. Beauchamp JR, Morgan JE, Pagel CN, Partridge TA . Dynamics of myoblast transplantation reveal a discrete minority of precursors with stem cell-like properties as the myogenic source J Cell Biol 1999 144: 1113–1122

    Article  CAS  Google Scholar 

  34. Guerette B et al. Control of inflammatory damage by anti-LFA-1: increased success of myoblast transplantation Cell Transplant 1997 6: 101–107

    CAS  PubMed  Google Scholar 

  35. Qu Z et al. Development of approaches to improve cell survival in myoblast transfer therapy J Cell Biol 1998 142: 1257–1267

    Article  CAS  Google Scholar 

  36. Cossu G, Mavilio F . Myogenic stem cells for the therapy of primary myopathies: wishful thinking or therapeutic perspective? J Clin Invest 2000 105: 1669–1674

    Article  CAS  Google Scholar 

  37. Smythe GM, Hodgetts S, Grounds M . Problems and solutions in myoblast transfer therapy J Cell Mol Med 2001 5: 33–47

    Article  CAS  Google Scholar 

  38. Hodgetts S, Beilharz M, Scalzo T, Grounds M . Why do cultured transplanted myoblasts die in vivo? DNA quantification shows enhanced survival of donor myoblasts in host mice depleted of CD4+/CD8+ or NK1.1+ cells Cell Transplant 2000 9: 489–502

    Article  CAS  Google Scholar 

  39. Torrente Y et al. Intraarterial injection of muscle-derived CD34+Sca-1+ stem cells restores dystrophin in mdx mice J Cell Biol 2001 152: 335–348

    Article  CAS  Google Scholar 

  40. Jankowski R, Haluszczak C, Trucco M, Huard J . Flow cytometric characterization of myogenic cell populations obtained via the preplate technique: potential for rapid isolation of muscle-derived stem cells Hum Gene Ther 2001 12: 619–628

    Article  CAS  Google Scholar 

  41. DeAngelis L et al. Skeletal myogenic progenitors originating from embryonic dorsal aorta co-express endothelial and myogenic markers and contribute to post-natal muscle growth and regeneration J Cell Biol 1999 147: 869–878

    Article  CAS  Google Scholar 

  42. DeAngelis L et al. Skeletal myogenic progenitors originating from embryonic dorsal aorta co-express endothelial and myogenic markers and contribute to post-natal muscle growth and regeneration Qu-Peterson Z et al. Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J Cell Biol (in press)

Download references

Acknowledgements

This work was supported in part by grants to Dr Huard from the National Institutes of Health (1P60 AR44811-01, 1PO1 AR45925-01), the Pittsburgh Tissue Engineering Initiative (PTEI), the William F and Jean W Donaldson Chair at Children's Hospital of Pittsburgh, the Muscular Dystrophy Association (USA), the Parent Project (USA), and the Orris C Hirtzel and Beatrice Dewey Hirtzel Memorial Foundation.

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Jankowski, R., Deasy, B. & Huard, J. Muscle-derived stem cells. Gene Ther 9, 642–647 (2002). https://doi.org/10.1038/sj.gt.3301719

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.gt.3301719

Keywords

  • skeletal muscle
  • stem cells
  • differentiation
  • dystrophin

This article is cited by

Search

Quick links