Skip to main content
SpringerLink
Log in

The Origin and Fate of Muscle Satellite Cells

  • Published:
Stem Cell Reviews and Reports Aims and scope Submit manuscript

Abstract

Satellite cells represent the primary population of stem cells resident in skeletal muscle. These adult muscle stem cells facilitate the postnatal growth, remodeling, and regeneration of skeletal muscle. Given the remarkable regenerative potential of satellite cells, there is great promise for treatment of muscle pathologies such as the muscular dystrophies with this cell population. Various protocols have been developed which allow for isolation, enrichment, and expansion of satellite cell derived muscle stem cells. However, isolated satellite cells have yet to translate into effective modalities for therapeutic intervention. Broadening our understanding of satellite cells and their niche requirements should improve our in vivo and ex vivo manipulation of these cells to expedite their use for regeneration of diseased muscle. This review explores the fates of satellite cells as determined by their molecular signatures, ontogeny, and niche dependent programming.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Peault, B., Rudnicki, M., Torrente, Y., et al. (2007). Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Molecular Therapy, 15(5), 867–877.

    PubMed  CAS  Google Scholar 

  2. Tapscott, S. J. (2005). The circuitry of a master switch: Myod and the regulation of skeletal muscle gene transcription. Development, 132(12), 2685–2695.

    PubMed  CAS  Google Scholar 

  3. Asakura, A., Hirai, H., Kablar, B., et al. (2007). Increased survival of muscle stem cells lacking the MyoD gene after transplantation into regenerating skeletal muscle. Proceedings of the National Academy of Sciences of the United States of America, 104(42), 16552–16557.

    PubMed  CAS  Google Scholar 

  4. Ferrari, G., Cusella-De Angelis, G., Coletta, M., et al. (1998). Muscle regeneration by bone marrow-derived myogenic progenitors. Science, 279(5356), 1528–1530.

    PubMed  CAS  Google Scholar 

  5. Goodell, M. A., Brose, K., Paradis, G., Conner, A. S., & Mulligan, R. C. (1996). Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. The Journal of Experimental Medicine, 183(4), 1797–1806.

    PubMed  CAS  Google Scholar 

  6. Gussoni, E., Soneoka, Y., Strickland, C. D., et al. (1999). Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature, 401(6751), 390–394.

    PubMed  CAS  Google Scholar 

  7. Lee, J. Y., Qu-Petersen, Z., Cao, B., et al. (2000). Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. The Journal of Cell Biology, 150(5), 1085–1100.

    PubMed  CAS  Google Scholar 

  8. Qu-Petersen, Z., Deasy, B., Jankowski, R., et al. (2002). Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. The Journal of Cell Biology, 157(5), 851–864.

    PubMed  CAS  Google Scholar 

  9. Sampaolesi, M., Blot, S., D’Antona, G., et al. (2006). Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature, 444(7119), 574–579.

    PubMed  CAS  Google Scholar 

  10. Dellavalle, A., Sampaolesi, M., Tonlorenzi, R., et al. (2007). Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nature Cell Biology, 9(3), 255–267.

    PubMed  CAS  Google Scholar 

  11. Mitchell, K. J., Pannerec, A., Cadot, B., et al. (2010). Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nature Cell Biology, 12(3), 257–266.

    PubMed  CAS  Google Scholar 

  12. Di Rocco, G., Iachininoto, M. G., Tritarelli, A., et al. (2006). Myogenic potential of adipose-tissue-derived cells. Journal of Cell Science, 119(Pt 14), 2945–2952.

    PubMed  Google Scholar 

  13. Otto, A., Collins-Hooper, H., & Patel, K. (2009). The origin, molecular regulation and therapeutic potential of myogenic stem cell populations. Journal of Anatomy, 215(5), 477–497.

    PubMed  CAS  Google Scholar 

  14. Field, E. (1960). Muscle regeneration and repair.

  15. Lewis, W., & Lewis, M. (1917). Behaviour of cross striated muscle in tissue cultures. The American Journal of Anatomy, 22, 169–194.

    Google Scholar 

  16. Katz, B. (1961). The terminations of the afferent nerve fibre in the muscle spindle of the frog. Philosophical Transactions of the Royal Society London [Biology], 243, 221–240.

    Google Scholar 

  17. Mauro, A. (1961). Satellite cell of skeletal muscle fibers. The Journal of Biophysical and Biochemical Cytology, 9, 493–495.

    PubMed  CAS  Google Scholar 

  18. Moss, F. P., & Leblond, C. P. (1971). Satellite cells as the source of nuclei in muscles of growing rats. Anatomical Record, 170(4), 421–435.

    PubMed  CAS  Google Scholar 

  19. Grounds, M. D., & McGeachie, J. K. (1987). A model of myogenesis in vivo, derived from detailed autoradiographic studies of regenerating skeletal muscle, challenges the concept of quantal mitosis. Cell and Tissue Research, 250(3), 563–569.

    PubMed  CAS  Google Scholar 

  20. Robertson, T. A., Grounds, M. D., & Papadimitriou, J. M. (1992). Elucidation of aspects of murine skeletal muscle regeneration using local and whole body irradiation. Journal of Anatomy, 181(Pt 2), 265–276.

    PubMed  Google Scholar 

  21. Kelly, R., Alonso, S., Tajbakhsh, S., Cossu, G., & Buckingham, M. (1995). Myosin light chain 3 F regulatory sequences confer regionalized cardiac and skeletal muscle expression in transgenic mice. The Journal of Cell Biology, 129(2), 383–396.

    PubMed  CAS  Google Scholar 

  22. Beauchamp, J. R., Heslop, L., Yu, D. S. W., et al. (2000). Expression of Cd34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. The Journal of Cell Biology, 151(6), 1221–1234.

    PubMed  CAS  Google Scholar 

  23. Relaix, F., Rocancourt, D., Mansouri, A., & Buckingham, M. (2005). A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature, 435(7044), 948–953.

    PubMed  CAS  Google Scholar 

  24. Seale, P., Sabourin, L. A., Girgis-Gabardo, A., Mansouri, A., Gruss, P., & Rudnicki, M. A. (2000). Pax7 is required for the specification of myogenic satellite cells. Cell, 102(6), 777–786.

    PubMed  CAS  Google Scholar 

  25. Faralli, H., Martin, E., Core, N., et al. (2011). Teashirt-3, a novel regulator of muscle differentiation, associates with BRG1-associated factor 57 (BAF57) to inhibit myogenin gene expression. Journal of Biological Chemistry, 286(26), 23498–23510.

    PubMed  CAS  Google Scholar 

  26. Cornelison, D. D., & Wold, B. J. (1997). Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Developmental Biology, 191(2), 270–283.

    PubMed  CAS  Google Scholar 

  27. Ratajczak, M. Z., Majka, M., Kucia, M., et al. (2003). Expression of functional CXCR4 by muscle satellite cells and secretion of SDF-1 by muscle-derived fibroblasts is associated with the presence of both muscle progenitors in bone marrow and hematopoietic stem/progenitor cells in muscles. Stem Cells, 21(3), 363–371.

    PubMed  CAS  Google Scholar 

  28. Holterman, C. E., Le Grand, F., Kuang, S., Seale, P., & Rudnicki, M. A. (2007). Megf10 regulates the progression of the satellite cell myogenic program. The Journal of Cell Biology, 179(5), 911–922.

    PubMed  CAS  Google Scholar 

  29. Irintchev, A., Zeschnigk, M., Starzinski-Powitz, A., & Wernig, A. (1994). Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles. The American Journal of Anatomy, 199(4), 326–337.

    CAS  Google Scholar 

  30. Volonte, D., Liu, Y., & Galbiati, F. (2005). The modulation of caveolin-1 expression controls satellite cell activation during muscle repair. The FASEB Journal, 19(2), 237–239.

    CAS  Google Scholar 

  31. Cornelison, D. D., Filla, M. S., Stanley, H. M., Rapraeger, A. C., & Olwin, B. B. (2001). Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Developmental Biology, 239(1), 79–94.

    PubMed  CAS  Google Scholar 

  32. LaBarge, M. A., & Blau, H. M. (2002). Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell, 111(4), 589–601.

    PubMed  CAS  Google Scholar 

  33. Harel, I., Nathan, E., Tirosh-Finkel, L., et al. (2009). Distinct origins and genetic programs of head muscle satellite cells. Developmental Cell, 16(6), 822–832.

    PubMed  CAS  Google Scholar 

  34. Gros, J., Manceau, M., Thome, V., & Marcelle, C. (2005). A common somitic origin for embryonic muscle progenitors and satellite cells. Nature, 435(7044), 954–958.

    PubMed  CAS  Google Scholar 

  35. Noden, D. M. (1988). Interactions and fates of avian craniofacial mesenchyme. Development, 103(Suppl), 121–140.

    PubMed  Google Scholar 

  36. Trainor, P. A., Tan, S. S., & Tam, P. P. (1994). Cranial paraxial mesoderm: regionalisation of cell fate and impact on craniofacial development in mouse embryos. Development, 120(9), 2397–2408.

    PubMed  CAS  Google Scholar 

  37. Couly, G. F., Coltey, P. M., & Le Douarin, N. M. (1992). The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development, 114(1), 1–15.

    PubMed  CAS  Google Scholar 

  38. Scaal, M., & Christ, B. (2004). Formation and differentiation of the avian dermomyotome. Anatomy and Embryology (Berlin), 208(6), 411–424.

    Google Scholar 

  39. Armand, O., Boutineau, A. M., Mauger, A., Pautou, M. P., & Kieny, M. (1983). Origin of satellite cells in avian skeletal muscles. Archives d’Anatomie Microscopique et de Morphologie Expérimentale, 72(2), 163–181.

    PubMed  CAS  Google Scholar 

  40. Sambasivan, R., & Tajbakhsh, S. (2007). Skeletal muscle stem cell birth and properties. Seminars in Cell & Developmental Biology, 18(6), 870–882.

    CAS  Google Scholar 

  41. Buckingham, M. (2001). Skeletal muscle formation in vertebrates. Current Opinion in Genetics & Development, 11(4), 440–448.

    CAS  Google Scholar 

  42. Buckingham, M. (2006). Myogenic progenitor cells and skeletal myogenesis in vertebrates. Current Opinion in Genetics & Development, 16(5), 525–532.

    CAS  Google Scholar 

  43. Pourquie, O. (2001). Vertebrate somitogenesis. Annual Review of Cell and Developmental Biology, 17, 311–350.

    PubMed  CAS  Google Scholar 

  44. Messina, G., & Cossu, G. (2009). The origin of embryonic and fetal myoblasts: a role of Pax3 and Pax7. Genes & Development, 23(8), 902–905.

    CAS  Google Scholar 

  45. Brent, A. E., Schweitzer, R., & Tabin, C. J. (2003). A somitic compartment of tendon progenitors. Cell, 113(2), 235–248.

    PubMed  CAS  Google Scholar 

  46. Hutcheson, D. A., Zhao, J., Merrell, A., Haldar, M., & Kardon, G. (2009). Embryonic and fetal limb myogenic cells are derived from developmentally distinct progenitors and have different requirements for β-catenin. Genes & Development, 23(8), 997–1013.

    CAS  Google Scholar 

  47. Feldman, J. L., & Stockdale, F. E. (1992). Temporal appearance of satellite cells during myogenesis. Developmental Biology, 153(2), 217–226.

    PubMed  CAS  Google Scholar 

  48. Kassar-Duchossoy, L., Giacone, E., Gayraud-Morel, B., Jory, Al, Gomes, D., & Tajbakhsh, S. (2005). Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes & Development, 19(12), 1426–1431.

    CAS  Google Scholar 

  49. Schienda, J., Engleka, K. A., Jun, S., et al. (2006). Somitic origin of limb muscle satellite and side population cells. Proceedings of the National Academy of Sciences of the United States of America, 103(4), 945–950.

    PubMed  CAS  Google Scholar 

  50. Biressi, S., Molinaro, M., & Cossu, G. (2007). Cellular heterogeneity during vertebrate skeletal muscle development. Developmental Biology, 308(2), 281–293.

    PubMed  CAS  Google Scholar 

  51. Biressi, S., Tagliafico, E., Lamorte, G., et al. (2007). Intrinsic phenotypic diversity of embryonic and fetal myoblasts is revealed by genome-wide gene expression analysis on purified cells. Developmental Biology, 304(2), 633–651.

    PubMed  CAS  Google Scholar 

  52. Maroto, M., Reshef, R., Münsterberg, A. E., Koester, S., Goulding, M., & Lassar, A. B. (1997). Ectopic Pax-3 activates MyoD and Myf-5 expression in embryonic mesoderm and neural tissue. Cell, 89(1), 139–148.

    PubMed  CAS  Google Scholar 

  53. Tajbakhsh, S., Rocancourt, D., Cossu, G., & Buckingham, M. (1997). Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell, 89(1), 127–138.

    PubMed  CAS  Google Scholar 

  54. Bajard, L., Relaix, Fdr, Lagha, M., Rocancourt, D., Daubas, P., & Buckingham, M. E. (2006). A novel genetic hierarchy functions during hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. Genes & Development, 20(17), 2450–2464.

    CAS  Google Scholar 

  55. Goulding, M., Lumsden, A., & Paquette, A. J. (1994). Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development, 120(4), 957–971.

    PubMed  CAS  Google Scholar 

  56. Relaix, Fdr, Montarras, D., Zaffran, Sp, et al. (2006). Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. The Journal of Cell Biology, 172(1), 91–102.

    PubMed  CAS  Google Scholar 

  57. Montarras, D., Morgan, J., Collins, C., et al. (2005). Direct isolation of satellite cells for skeletal muscle regeneration. Science, 309(5743), 2064–2067.

    PubMed  CAS  Google Scholar 

  58. Young, A. P., & Wagers, A. J. (2010). Pax3 induces differentiation of juvenile skeletal muscle stem cells without transcriptional upregulation of canonical myogenic regulatory factors. Journal of Cell Science, 123(Pt 15), 2632–2639.

    PubMed  CAS  Google Scholar 

  59. Bober, E., Franz, T., Arnold, H. H., Gruss, P., & Tremblay, P. (1994). Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development, 120(3), 603–612.

    PubMed  CAS  Google Scholar 

  60. Williams, B. A., & Ordahl, C. P. (1994). Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification. Development, 120(4), 785–796.

    PubMed  CAS  Google Scholar 

  61. Ivanova, A., Signore, M., Caro, N., Greene, N. D. E., Copp, A. J., & Martinez-Barbera, J. P. (2005). In vivo genetic ablation by Cre-mediated expression of diphtheria toxin fragment A. Genesis, 43(3), 129–135.

    PubMed  CAS  Google Scholar 

  62. Kardon, G., Heanue, T. A., & Tabin, C. J. (2002). Pax3 and Dach2 positive regulation in the developing somite. Developmental Dynamics, 224(3), 350–355.

    PubMed  CAS  Google Scholar 

  63. Sambasivan, R., Yao, R., Kissenpfennig, A., et al. (2011). Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development, 138(17), 3647–3656.

    PubMed  CAS  Google Scholar 

  64. Lepper, C., Partridge, T. A., & Fan, C. M. (2011). An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development, 138(17), 3639–3646.

    PubMed  CAS  Google Scholar 

  65. Lepper, C., Conway, S. J., & Fan, C.-M. (2009). Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature, 460(7255), 627–631.

    PubMed  CAS  Google Scholar 

  66. Lepper, C., & Fan, C.-M. (2010). Inducible lineage tracing of Pax7-descendant cells reveals embryonic origin of adult satellite cells. Genesis, 48(7), 424–436.

    PubMed  CAS  Google Scholar 

  67. De Angelis, L., Berghella, L., Coletta, M., et al. (1999). Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration. The Journal of Cell Biology, 147(4), 869–878.

    PubMed  Google Scholar 

  68. Dong, F., Sun, X., Liu, W., et al. (2006). Pitx2 promotes development of splanchnic mesoderm-derived branchiomeric muscle. Development, 133(24), 4891–4899.

    PubMed  CAS  Google Scholar 

  69. Kelly, R. G., Jerome-Majewska, L. A., & Papaioannou, V. E. (2004). The del22q11.2 candidate gene Tbx1 regulates branchiomeric myogenesis. Human Molecular Genetics, 13(22), 2829–2840.

    PubMed  CAS  Google Scholar 

  70. Rudnicki, M. A., Schnegelsberg, P. N., Stead, R. H., Braun, T., Arnold, H. H., & Jaenisch, R. (1993). MyoD or Myf-5 is required for the formation of skeletal muscle. Cell, 75(7), 1351–1359.

    PubMed  CAS  Google Scholar 

  71. Tirosh-Finkel, L., Elhanany, H., Rinon, A., & Tzahor, E. (2006). Mesoderm progenitor cells of common origin contribute to the head musculature and the cardiac outflow tract. Development, 133(10), 1943–1953.

    PubMed  CAS  Google Scholar 

  72. Tzahor, E., Kempf, H., Mootoosamy, R. C., et al. (2003). Antagonists of Wnt and BMP signaling promote the formation of vertebrate head muscle. Genes & Development, 17(24), 3087–3099.

    CAS  Google Scholar 

  73. Tzahor, E., & Lassar, A. B. (2001). Wnt signals from the neural tube block ectopic cardiogenesis. Genes & Development, 15(3), 255–260.

    CAS  Google Scholar 

  74. Porter, J. D., Israel, S., Gong, B., et al. (2006). Distinctive morphological and gene/protein expression signatures during myogenesis in novel cell lines from extraocular and hindlimb muscle. Physiological Genomics, 24(3), 264–275.

    PubMed  CAS  Google Scholar 

  75. Pavlath, G. K., Thaloor, D., Rando, T. A., Cheong, M., English, A. W., & Zheng, B. (1998). Heterogeneity among muscle precursor cells in adult skeletal muscles with differing regenerative capacities. Developmental Dynamics, 212(4), 495–508.

    PubMed  CAS  Google Scholar 

  76. Sinanan, A. C., Hunt, N. P., & Lewis, M. P. (2004). Human adult craniofacial muscle-derived cells: neural-cell adhesion-molecule (NCAM; CD56)-expressing cells appear to contain multipotential stem cells. Biotechnology and Applied Biochemistry, 40(Pt 1), 25–34.

    PubMed  CAS  Google Scholar 

  77. Emery, A. E. (2002). The muscular dystrophies. Lancet, 359(9307), 687–695.

    PubMed  CAS  Google Scholar 

  78. Noden, D. M., & Francis-West, P. (2006). The differentiation and morphogenesis of craniofacial muscles. Developmental Dynamics, 235(5), 1194–1218.

    PubMed  CAS  Google Scholar 

  79. Kitajima, S., Takagi, A., Inoue, T., & Saga, Y. (2000). MesP1 and MesP2 are essential for the development of cardiac mesoderm. Development, 127(15), 3215–3226.

    PubMed  CAS  Google Scholar 

  80. Saga, Y., Hata, N., Kobayashi, S., Magnuson, T., Seldin, M. F., & Taketo, M. M. (1996). MesP1: a novel basic helix-loop-helix protein expressed in the nascent mesodermal cells during mouse gastrulation. Development, 122(9), 2769–2778.

    PubMed  CAS  Google Scholar 

  81. Saga, Y., Miyagawa-Tomita, S., Takagi, A., Kitajima, S., Miyazaki, J., & Inoue, T. (1999). MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development, 126(15), 3437–3447.

    PubMed  CAS  Google Scholar 

  82. Sambasivan, R., Gayraud-Morel, B., Dumas, G., et al. (2009). Distinct regulatory cascades govern extraocular and pharyngeal arch muscle progenitor cell fates. Developmental Cell, 16(6), 810–821.

    PubMed  CAS  Google Scholar 

  83. Shih, H. P., Gross, M. K., & Kioussi, C. (2007). Expression pattern of the homeodomain transcription factor Pitx2 during muscle development. Gene Expression Patterns, 7(4), 441–451.

    PubMed  CAS  Google Scholar 

  84. Gage, P. J., Suh, H., & Camper, S. A. (1999). Dosage requirement of Pitx2 for development of multiple organs. Development, 126(20), 4643–4651.

    PubMed  CAS  Google Scholar 

  85. Kitamura, K., Miura, H., Miyagawa-Tomita, S., et al. (1999). Mouse Pitx2 deficiency leads to anomalies of the ventral body wall, heart, extra- and periocular mesoderm and right pulmonary isomerism. Development, 126(24), 5749–5758.

    PubMed  CAS  Google Scholar 

  86. Nathan, E., Monovich, A., Tirosh-Finkel, L., et al. (2008). The contribution of Islet1-expressing splanchnic mesoderm cells to distinct branchiomeric muscles reveals significant heterogeneity in head muscle development. Development, 135(4), 647–657.

    PubMed  CAS  Google Scholar 

  87. Marcucio, R. S., & Noden, D. M. (1999). Myotube heterogeneity in developing chick craniofacial skeletal muscles. Developmental Dynamics, 214(3), 178–194.

    PubMed  CAS  Google Scholar 

  88. Bentzinger, C. F., von Maltzahn, J., & Rudnicki, M. A. (2010). Extrinsic regulation of satellite cell specification. Stem Cell Research and Therapy, 1(3), 27.

    PubMed  Google Scholar 

  89. Collins, C. A., Olsen, I., Zammit, P. S., et al. (2005). Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell, 122(2), 289–301.

    PubMed  CAS  Google Scholar 

  90. Hall, J. K., Banks, G. B., Chamberlain, J. S., & Olwin, B. B. (2010). Prevention of muscle aging by myofiber-associated satellite cell transplantation. Science Translational Medicine, 2(57), 57ra83.

    PubMed  CAS  Google Scholar 

  91. Scadden, D. T. (2006). The stem-cell niche as an entity of action. Nature, 441(7097), 1075–1079.

    PubMed  CAS  Google Scholar 

  92. Christov, C., Chretien, F., Abou-Khalil, R., et al. (2007). Muscle satellite cells and endothelial cells: close neighbors and privileged partners. Molecular Biology of the Cell, 18(4), 1397–1409.

    PubMed  CAS  Google Scholar 

  93. Joe, A. W., Yi, L., Natarajan, A., et al. (2010). Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nature Cell Biology, 12(2), 153–163.

    PubMed  CAS  Google Scholar 

  94. Murphy, M. M., Lawson, J. A., Mathew, S. J., Hutcheson, D. A., & Kardon, G. (2011). Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development, 138(17), 3625–3637.

    PubMed  CAS  Google Scholar 

  95. Molgo, J., Colasantei, C., Adams, D. S., & Jaimovich, E. (2004). IP3 receptors and Ca2+ signals in adult skeletal muscle satellite cells in situ. Biological Research, 37(4), 635–639.

    PubMed  Google Scholar 

  96. Tatsumi, R., Liu, X., Pulido, A., et al. (2006). Satellite cell activation in stretched skeletal muscle and the role of nitric oxide and hepatocyte growth factor. American Journal of Physiology. Cell Physiology, 290(6), C1487–C1494.

    PubMed  CAS  Google Scholar 

  97. Philippou, A., Halapas, A., Maridaki, M., & Koutsilieris, M. (2007). Type I insulin-like growth factor receptor signaling in skeletal muscle regeneration and hypertrophy. Journal of Musculoskeletal and Neuronal Interactions, 7(3), 208–218.

    PubMed  CAS  Google Scholar 

  98. Abou-Khalil, R., Le Grand, F., Pallafacchina, G., et al. (2009). Autocrine and paracrine angiopoietin 1/Tie-2 signaling promotes muscle satellite cell self-renewal. Cell Stem Cell, 5(3), 298–309.

    PubMed  CAS  Google Scholar 

  99. Roe, J. A., Harper, J. M., & Buttery, P. J. (1989). Protein metabolism in ovine primary muscle cultures derived from satellite cells–effects of selected peptide hormones and growth factors. Journal of Endocrinology, 122(2), 565–571.

    PubMed  CAS  Google Scholar 

  100. Miller, K. J., Thaloor, D., Matteson, S., & Pavlath, G. K. (2000). Hepatocyte growth factor affects satellite cell activation and differentiation in regenerating skeletal muscle. American Journal of Physiology. Cell Physiology, 278(1), C174–C181.

    PubMed  CAS  Google Scholar 

  101. Wehling, M., Spencer, M. J., & Tidball, J. G. (2001). A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. The Journal of Cell Biology, 155(1), 123–131.

    PubMed  CAS  Google Scholar 

  102. Le Grand, F., Jones, A. E., Seale, V., Scimè, A., & Rudnicki, M. A. (2009). Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells. Cell Stem Cell, 4(6), 535–547.

    PubMed  Google Scholar 

  103. Brack, A. S., Conboy, I. M., Conboy, M. J., Shen, J., & Rando, T. A. (2008). A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell, 2(1), 50–59.

    PubMed  CAS  Google Scholar 

  104. Bischoff, R. (1986). Proliferation of muscle satellite cells on intact myofibers in culture. Developmental Biology, 115(1), 129–139.

    PubMed  CAS  Google Scholar 

  105. Allen, R. E., & Boxhorn, L. K. (1989). Regulation of skeletal muscle satellite cell proliferation and differentiation by transforming growth factor-beta, insulin-like growth factor I, and fibroblast growth factor. Journal of Cellular Physiology, 138(2), 311–315.

    PubMed  CAS  Google Scholar 

  106. Kuang, S., Gillespie, M. A., & Rudnicki, M. A. (2008). Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell, 2(1), 22–31.

    PubMed  CAS  Google Scholar 

  107. Bischoff, R. (1990). Interaction between satellite cells and skeletal muscle fibers. Development, 109(4), 943–952.

    PubMed  CAS  Google Scholar 

  108. Gospodarowicz, D., & Cheng, J. (1986). Heparin protects basic and acidic FGF from inactivation. Journal of Cellular Physiology, 128(3), 475–484.

    PubMed  CAS  Google Scholar 

  109. Clemmons, D. R., Elgin, R. G., Han, V. K., Casella, S. J., D’Ercole, A. J., & Van Wyk, J. J. (1986). Cultured fibroblast monolayers secrete a protein that alters the cellular binding of somatomedin-C/insulinlike growth factor I. The Journal of Clinical Investigation, 77(5), 1548–1556.

    PubMed  CAS  Google Scholar 

  110. Sporn, M. B., Roberts, A. B., Wakefield, L. M., & de Crombrugghe, B. (1987). Some recent advances in the chemistry and biology of transforming growth factor-beta. The Journal of Cell Biology, 105(3), 1039–1045.

    PubMed  CAS  Google Scholar 

  111. Shea, K. L., Xiang, W., LaPorta, V. S., et al. (2010). Sprouty1 regulates reversible quiescence of a self-renewing adult muscle stem cell pool during regeneration. Cell Stem Cell, 6(2), 117–129.

    PubMed  CAS  Google Scholar 

  112. McPherron, A. C., Lawler, A. M., & Lee, S. J. (1997). Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature, 387(6628), 83–90.

    PubMed  CAS  Google Scholar 

  113. McPherron, A. C., & Lee, S. J. (1997). Double muscling in cattle due to mutations in the myostatin gene. Proceedings of the National Academy of Sciences of the United States of America, 94(23), 12457–12461.

    PubMed  CAS  Google Scholar 

  114. Kollias, H. D., & McDermott, J. C. (2008). Transforming growth factor-beta and myostatin signaling in skeletal muscle. Journal of Applied Physiology, 104(3), 579–587.

    PubMed  CAS  Google Scholar 

  115. Yamada, M., Tatsumi, R., Yamanouchi, K., et al. (2010). High concentrations of HGF inhibit skeletal muscle satellite cell proliferation in vitro by inducing expression of myostatin: a possible mechanism for reestablishing satellite cell quiescence in vivo. American Journal of Physiology. Cell Physiology, 298(3), C465–C476.

    PubMed  CAS  Google Scholar 

  116. Amthor, H., Otto, A., Vulin, A., et al. (2009). Muscle hypertrophy driven by myostatin blockade does not require stem/precursor-cell activity. Proceedings of the National Academy of Sciences of the United States of America, 106(18), 7479–7484.

    PubMed  CAS  Google Scholar 

  117. Kuang, S., Kuroda, K., Le Grand, F., & Rudnicki, M. A. (2007). Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell, 129(5), 999–1010.

    PubMed  CAS  Google Scholar 

  118. Schuster-Gossler, K., Cordes, R., & Gossler, A. (2007). Premature myogenic differentiation and depletion of progenitor cells cause severe muscle hypotrophy in Delta1 mutants. Proceedings of the National Academy of Sciences of the United States of America, 104(2), 537–542.

    PubMed  CAS  Google Scholar 

  119. Perez-Ruiz, A., Ono, Y., Gnocchi, V. F., & Zammit, P. S. (2008). Beta-Catenin promotes self-renewal of skeletal-muscle satellite cells. Journal of Cell Science, 121(Pt 9), 1373–1382.

    PubMed  CAS  Google Scholar 

  120. van Amerongen, R., & Nusse, R. (2009). Towards an integrated view of Wnt signaling in development. Development, 136(19), 3205–3214.

    PubMed  Google Scholar 

  121. Munsterberg, A. E., Kitajewski, J., Bumcrot, D. A., McMahon, A. P., & Lassar, A. B. (1995). Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes & Development, 9(23), 2911–2922.

    CAS  Google Scholar 

  122. Tajbakhsh, S., Borello, U., Vivarelli, E., et al. (1998). Differential activation of Myf5 and MyoD by different Wnts in explants of mouse paraxial mesoderm and the later activation of myogenesis in the absence of Myf5. Development, 125(21), 4155–4162.

    PubMed  CAS  Google Scholar 

  123. Vasyutina, E., Lenhard, D. C., Wende, H., Erdmann, B., Epstein, J. A., & Birchmeier, C. (2007). RBP-J (Rbpsuh) is essential to maintain muscle progenitor cells and to generate satellite cells. Proceedings of the National Academy of Sciences of the United States of America, 104(11), 4443–4448.

    PubMed  CAS  Google Scholar 

  124. Jory, A., Le Roux, I., Gayraud-Morel, B., et al. (2009). Numb promotes an increase in skeletal muscle progenitor cells in the embryonic Somite. Stem Cells, 27(11), 2769–2780.

    PubMed  CAS  Google Scholar 

  125. Kitamoto, T., & Hanaoka, K. (2010). Notch3 null mutation in mice causes muscle hyperplasia by repetitive muscle regeneration. Stem Cells, 28(12), 2205–2216.

    PubMed  CAS  Google Scholar 

  126. Conboy, I. M., Conboy, M. J., Wagers, A. J., Girma, E. R., Weissman, I. L., & Rando, T. A. (2005). Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature, 433(7027), 760–764.

    PubMed  CAS  Google Scholar 

  127. Daston, G., Lamar, E., Olivier, M., & Goulding, M. (1996). Pax-3 is necessary for migration but not differentiation of limb muscle precursors in the mouse. Development, 122(3), 1017–1027.

    PubMed  CAS  Google Scholar 

  128. Bladt, F., Riethmacher, D., Isenmann, S., Aguzzi, A., & Birchmeier, C. (1995). Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature, 376(6543), 768–771.

    PubMed  CAS  Google Scholar 

  129. Epstein, J. A., Shapiro, D. N., Cheng, J., Lam, P. Y., & Maas, R. L. (1996). Pax3 modulates expression of the c-Met receptor during limb muscle development. Proceedings of the National Academy of Sciences of the United States of America, 93(9), 4213–4218.

    PubMed  CAS  Google Scholar 

  130. Tatsumi, R., Anderson, J. E., Nevoret, C. J., Halevy, O., & Allen, R. E. (1998). HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Developmental Biology, 194(1), 114–128.

    PubMed  CAS  Google Scholar 

  131. Sheehan, S. M., Tatsumi, R., Temm-Grove, C. J., & Allen, R. E. (2000). HGF is an autocrine growth factor for skeletal muscle satellite cells in vitro. Muscle & Nerve, 23(2), 239–245.

    CAS  Google Scholar 

  132. Jennische, E., Ekberg, S., & Matejka, G. L. (1993). Expression of hepatocyte growth factor in growing and regenerating rat skeletal muscle. American Journal of Physiology, 265(1 Pt 1), C122–C128.

    PubMed  CAS  Google Scholar 

  133. Yamada, M., Sankoda, Y., Tatsumi, R., et al. (2008). Matrix metalloproteinase-2 mediates stretch-induced activation of skeletal muscle satellite cells in a nitric oxide-dependent manner. The International Journal of Biochemistry & Cell Biology, 40(10), 2183–2191.

    CAS  Google Scholar 

  134. Podleski, T. R., Greenberg, I., Schlessinger, J., & Yamada, K. M. (1979). Fibronectin delays the fusion of L6 myoblasts. Experimental Cell Research, 122(2), 317–326.

    PubMed  CAS  Google Scholar 

  135. Foster, R. F., Thompson, J. M., & Kaufman, S. J. (1987). A laminin substrate promotes myogenesis in rat skeletal muscle cultures: analysis of replication and development using antidesmin and anti-BrdUrd monoclonal antibodies. Developmental Biology, 122(1), 11–20.

    PubMed  CAS  Google Scholar 

  136. Mu, X., Urso, M. L., Murray, K., Fu, F., & Li, Y. (2010). Relaxin regulates MMP expression and promotes satellite cell mobilization during muscle healing in both young and aged mice. American Journal of Pathology, 177(5), 2399–2410.

    PubMed  CAS  Google Scholar 

  137. Ohtake, Y., Tojo, H., & Seiki, M. (2006). Multifunctional roles of MT1-MMP in myofiber formation and morphostatic maintenance of skeletal muscle. Journal of Cell Science, 119(Pt 18), 3822–3832.

    PubMed  CAS  Google Scholar 

  138. Tatsumi, R., & Allen, R. E. (2004). Active hepatocyte growth factor is present in skeletal muscle extracellular matrix. Muscle & Nerve, 30(5), 654–658.

    CAS  Google Scholar 

  139. Powell, J. A., Molgo, J., Adams, D. S., et al. (2003). IP3 receptors and associated Ca2+ signals localize to satellite cells and to components of the neuromuscular junction in skeletal muscle. Journal of Neuroscience, 23(23), 8185–8192.

    PubMed  CAS  Google Scholar 

  140. Li, Y., Foster, W., Deasy, B. M., et al. (2004). Transforming growth factor-{beta}1 induces the differentiation of myogenic cells into fibrotic cells in injured skeletal muscle: a key event in muscle fibrogenesis. American Journal of Pathology, 164(3), 1007–1019.

    PubMed  CAS  Google Scholar 

  141. Vidal, B., Serrano, A. L., Tjwa, M., et al. (2008). Fibrinogen drives dystrophic muscle fibrosis via a TGFβ/alternative macrophage activation pathway. Genes & Development, 22(13), 1747–1752.

    CAS  Google Scholar 

  142. Mu, X., Li, Y. (2010). Conditional TGF-beta1 treatment increases stem cell-like cell population in myoblasts. J Cell Mol Med.

  143. Collins, C. A., & Partridge, T. A. (2005). Self-renewal of the adult skeletal muscle satellite cell. Cell Cycle, 4(10), 1338–1341.

    PubMed  CAS  Google Scholar 

  144. Darabi, R., Gehlbach, K., Bachoo, R. M., et al. (2008). Functional skeletal muscle regeneration from differentiating embryonic stem cells. Nature Medicine, 14(2), 134–143.

    PubMed  CAS  Google Scholar 

  145. Darabi, R., Santos, F. N., Filareto, A., et al. (2011). Assessment of the myogenic stem cell compartment following transplantation of Pax3/Pax7-induced embryonic stem cell-derived progenitors. Stem Cells, 29(5), 777–790.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Drs Florian Bentzinger, and Tetsuaki Miyake for critically reading the manuscript. Work in the Dilworth lab is funded by grants from the CIHR (FRN 93777 and 77778). SS is a recipient of an Ontario Research Fund Computational Regulomics Training Fellowship. FJD holds a Canadian Research Chair in Epigenetic Regulation of Gene Expression.

Author information

Authors and Affiliations

  1. Sprott Center for Stem Cell Research, Regenerative Medicine Program, Ottawa Hospital Research Institute, 501 Smyth Rd, Mailbox 511, Ottawa, ON, Canada, K1H 8L6

    Arif Aziz, Soji Sebastian & F. Jeffrey Dilworth

  2. Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, ON, Canada, K1H 8M5

    F. Jeffrey Dilworth

Authors
  1. Arif Aziz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Soji Sebastian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F. Jeffrey Dilworth
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to F. Jeffrey Dilworth.

Additional information

Arif Aziz and Soji Sebastian contributed equally to this work

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aziz, A., Sebastian, S. & Dilworth, F.J. The Origin and Fate of Muscle Satellite Cells. Stem Cell Rev and Rep 8, 609–622 (2012). https://doi.org/10.1007/s12015-012-9352-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12015-012-9352-0

Keywords

Search

Navigation