Table of Contents
Advances in Biology
Volume 2014, Article ID 612471, 16 pages
http://dx.doi.org/10.1155/2014/612471
Review Article

The Basis of Muscle Regeneration

1Institute Pasteur Cenci-Bolognetti, DAHFMO-Unit of Histology and Medical Embryology, IIM, Sapienza University of Rome, Via A. Scarpa 16, 00161 Rome, Italy
2Center for Life Nano Science@Sapienza, Italian Institute of Technology, Viale Regina Elena 291, 00161 Rome, Italy
3Edith Cowan University, Perth, WA 6027, Australia

Received 27 March 2014; Revised 28 May 2014; Accepted 18 June 2014; Published 9 July 2014

Academic Editor: Shihuan Kuang

Copyright © 2014 Antonio Musarò. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. P. Brockes, “Amphibian limb regeneration: rebuilding a complex structure,” Science, vol. 276, no. 5309, pp. 81–87, 1997. View at Publisher · View at Google Scholar · View at Scopus
  2. E. M. Tanaka, “Regeneration: if they can do it, why can't we?” Cell, vol. 113, no. 5, pp. 559–562, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. L. E. Iten and S. V. Bryant, “Forelimb regeneration from different levels of amputation in the newt, Notophthalmus viridescens: length, rate, and stages,” Wilhelm Roux's Archives of Developmental Biology, vol. 173, no. 4, pp. 263–282, 1973. View at Publisher · View at Google Scholar · View at Scopus
  4. E. M. Tanaka, A. A. F. Gann, P. B. Gates, and J. P. Brockes, “Newt myotubes reenter the cell cycle by phosphorylation of the retinoblastoma protein,” Journal of Cell Biology, vol. 136, no. 1, pp. 155–165, 1997. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Kragl, D. Knapp, E. Nacu et al., “Cells keep a memory of their tissue origin during axolotl limb regeneration,” Nature, vol. 460, no. 7251, pp. 60–65, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Tajbakhsh and G. Cossu, “Establishing myogenic identity during somitogenesis,” Current Opinion in Genetics and Development, vol. 7, no. 5, pp. 634–641, 1997. View at Publisher · View at Google Scholar · View at Scopus
  7. T. J. Hawke and D. J. Garry, “Myogenic satellite cells: physiology to molecular biology,” Journal of Applied Physiology, vol. 91, no. 2, pp. 534–551, 2001. View at Google Scholar · View at Scopus
  8. S. B. P. Chargé and M. A. Rudnicki, “Cellular and molecular regulation of muscle regeneration,” Physiological Reviews, vol. 84, no. 1, pp. 209–238, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Goulding, A. Lumsden, and A. J. Paquette, “Regulation of Pax-3 expression in the dermomyotome and its role in muscle development,” Development, vol. 120, no. 4, pp. 957–971, 1994. View at Google Scholar · View at Scopus
  10. B. A. Williams and C. P. Ordahl, “Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification,” Development, vol. 120, no. 4, pp. 785–796, 1994. View at Google Scholar · View at Scopus
  11. E. Bober, T. Franz, H. Arnold, P. Gruss, and P. Tremblay, “Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells,” Development, vol. 120, no. 3, pp. 603–612, 1994. View at Google Scholar · View at Scopus
  12. G. Daston, E. Lamar, M. Olivier, and M. Goulding, “Pax-3 is necessary for migration but not differentiation of limb muscle precursors in the mouse,” Development, vol. 122, no. 3, pp. 1017–1027, 1996. View at Google Scholar · View at Scopus
  13. P. Tremblay, S. Dietrich, M. Mericskay, F. R. Schubert, Z. Li, and D. Paulin, “A crucial role for Pax3 in the development of the hypaxial musculature and the long-range migration of muscle precursors,” Developmental Biology, vol. 203, no. 1, pp. 49–61, 1998. View at Publisher · View at Google Scholar · View at Scopus
  14. B. Jostes, C. Walther, and P. Gruss, “The murine paired box gene, Pax7, is expressed specifically during the development of the nervous and muscular system,” Mechanisms of Development, vol. 33, no. 1, pp. 27–37, 1990. View at Publisher · View at Google Scholar · View at Scopus
  15. P. Seale, L. A. Sabourin, A. Girgis-Gabardo, A. Mansouri, P. Gruss, and M. A. Rudnicki, “Pax7 is required for the specification of myogenic satellite cells,” Cell, vol. 102, no. 6, pp. 777–786, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Mansouri, A. Stoykova, M. Torres, and P. Gruss, “Dysgenesis of cephalic neural crest derivatives in Pax7-/-mutant mice,” Development, vol. 122, no. 3, pp. 831–838, 1996. View at Google Scholar · View at Scopus
  17. J. A. Epstein, D. N. Shapiro, J. Cheng, P. Y. P. Lam, and R. L. Maas, “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, vol. 93, no. 9, pp. 4213–4218, 1996. View at Publisher · View at Google Scholar · View at Scopus
  18. F. Bladt, D. Riethmacher, S. Isenmann, A. Aguzzi, and C. Birchmeier, “Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud,” Nature, vol. 376, no. 6543, pp. 768–771, 1995. View at Publisher · View at Google Scholar · View at Scopus
  19. S. J. Tapscott, “The circuitry of a master switch: myod and the regulation of skeletal muscle gene transcription,” Development, vol. 132, no. 12, pp. 2685–2695, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. C. A. Berkes and S. J. Tapscott, “MyoD and the transcriptional control of myogenesis,” Seminars in Cell and Developmental Biology, vol. 16, no. 4-5, pp. 585–595, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Tajbakhsh, E. Bober, C. Babinet, S. Pournin, H. Arnold, and M. Buckingham, “Gene targeting the myf-5 locus with nlacZ reveals expression of this myogenic factor in mature skeletal muscle fibres as well as early embryonic muscle,” Developmental Dynamics, vol. 206, pp. 291–300, 1996. View at Publisher · View at Google Scholar
  22. M.-O. Ott, E. Bober, G. Lyons, H. Arnold, and M. Buckingham, “Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo,” Development, vol. 111, no. 4, pp. 1097–1107, 1991. View at Google Scholar · View at Scopus
  23. R. Spörle, T. Günther, M. Struwe, and K. Schughart, “Severe defects in the formation of epaxial musculature in open brain (opb) mutant mouse embryos,” Development, vol. 122, no. 1, pp. 79–86, 1996. View at Google Scholar · View at Scopus
  24. M. Buckingham, “Making muscle in mammals,” Trends in Genetics, vol. 8, no. 4, pp. 144–149, 1992. View at Publisher · View at Google Scholar · View at Scopus
  25. D. Sassoon, G. Lyons, W. E. Wright et al., “Expression of two myogenic regulatory factors myogenin and MyoD1 during mouse embryogenesis,” Nature, vol. 341, no. 6240, pp. 303–307, 1989. View at Publisher · View at Google Scholar · View at Scopus
  26. M. A. Rudnicki, P. N. J. Schnegelsberg, R. H. Stead, T. Braun, H. H. Arnold, and R. Jaenisch, “MyoD or Myf-5 is required for the formation of skeletal muscle,” Cell, vol. 75, no. 7, pp. 1351–1359, 1993. View at Publisher · View at Google Scholar · View at Scopus
  27. P. Hasty, A. Bradley, J. H. Morris et al., “Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene,” Nature, vol. 364, no. 6437, pp. 501–506, 1993. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Nabeshima, K. Hanaoka, M. Hayasaka et al., “Myogenin gene disruption results in perinatal lethality because of severe muscle defect,” Nature, vol. 364, no. 6437, pp. 532–535, 1993. View at Publisher · View at Google Scholar · View at Scopus
  29. L. Kassar-Duchossoy, B. Gayraud-Morel, D. Gomès et al., “Mrf4 determines skeletal muscle identity in Myf5: Myod double-mutant mice,” Nature, vol. 431, pp. 466–471, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Musaro, M. G. C. de Angelis, A. Germani, C. Ciccareli, M. Molinaro, and B. M. Zani, “Enhanced expression of myogenic regulatory genes in aging skeletal muscle,” Experimental Cell Research, vol. 221, no. 1, pp. 241–248, 1995. View at Publisher · View at Google Scholar · View at Scopus
  31. E. I. Dedkov, T. Y. Kostrominova, A. B. Borisov, and B. M. Carlson, “MyoD and myogenin protein expression in skeletal muscles of senile rats,” Cell and Tissue Research, vol. 311, no. 3, pp. 401–416, 2003. View at Google Scholar · View at Scopus
  32. D. Palacios and P. L. Puri, “The epigenetic network regulating muscle development and regeneration,” Journal of Cellular Physiology, vol. 207, no. 1, pp. 1–11, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. E. A. Miska, E. Langley, D. Wolf, C. Karlsson, J. Pines, and T. Kouzarides, “Differential localization of HDAC4 orchestrates muscle differentiation,” Nucleic Acids Research, vol. 29, no. 16, pp. 3439–3447, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Haberland, R. L. Montgomery, and E. N. Olson, “The many roles of histone deacetylases in development and physiology: implications for disease and therapy,” Nature Reviews Genetics, vol. 10, no. 1, pp. 32–42, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. T. E. Callis, Z. Deng, J.-F. Chen, and D.-Z. Wang, “Muscling through the microRNA world,” Experimental Biology and Medicine, vol. 233, no. 2, pp. 131–138, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. E. van Rooij, N. Liu, and E. N. Olson, “MicroRNAs flex their muscles,” Trends in Genetics, vol. 24, no. 4, pp. 159–166, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. A. H. Williams, N. Liu, E. van Rooij, and E. N. Olson, “MicroRNA control of muscle development and disease,” Current Opinion in Cell Biology, vol. 21, no. 3, pp. 461–469, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. D. P. Bartel, “MicroRNAs: genomics, biogenesis, mechanism, and function,” Cell, vol. 116, no. 2, pp. 281–297, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. N. S. Asli, M. E. Pitulescu, and M. Kessel, “MicroRNAs in organogenesis and disease,” Current Molecular Medicine, vol. 8, no. 8, pp. 698–710, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. J. F. Chen, E. M. Mandel, J. M. Thomson et al., “The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation,” Nature Genetics, vol. 38, no. 2, pp. 228–233, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. R. Couteaux, J. Mira, and A. d'Albis, “Regeneration of muscles after cardiotoxin injury. I. Cytological aspects,” Biology of the Cell, vol. 62, no. 2, pp. 171–182, 1988. View at Publisher · View at Google Scholar · View at Scopus
  42. A. d'Albis, R. Couteaux, C. Janmot, A. Roulet, and J. C. Mira, “Regeneration after cardiotoxin injury of innervated and denervated slow and fast muscles of mammals. Myosin isoform analysis,” European Journal of Biochemistry, vol. 174, no. 1, pp. 103–110, 1988. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Musarò, K. McCullagh, A. Paul et al., “Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle,” Nature Genetics, vol. 27, no. 2, pp. 195–200, 2001. View at Publisher · View at Google Scholar · View at Scopus
  44. L. Pelosi, C. Giacinti, C. Nardis et al., “Local expression of IGF-1 accelerates muscle regeneration by rapidly modulating inflammatory cytokines and chemokines,” The FASEB Journal, vol. 21, no. 7, pp. 1393–1402, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. R. Matsuda, A. Nishikawa, and H. Tanaka, “Visualization of dystrophic muscle fibers in Mdx mouse by vital staining with Evans blue: evidence of apoptosis in dystrophin-deficient muscle,” The Journal of Biochemistry, vol. 118, no. 5, pp. 959–964, 1995. View at Publisher · View at Google Scholar · View at Scopus
  46. M. D. Grounds, “Phagocytosis of necrotic muscle in muscle isografts is influenced by the strain, age, and sex of host mice,” Journal of Pathology, vol. 153, no. 1, pp. 71–82, 1987. View at Publisher · View at Google Scholar · View at Scopus
  47. J. G. Tidball and M. Wehling-Henricks, “Macrophages promote muscle membrane repair and muscle fibre growth and regeneration during modified muscle loading in mice in vivo,” Journal of Physiology, vol. 578, no. 1, pp. 327–336, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Summan, G. L. Warren, R. R. Mercer et al., “Macrophages and skeletal muscle regeneration: a clodronate-containing liposome depletion study,” The American Journal of Physiology: Regulatory Integrative and Comparative Physiology, vol. 290, no. 6, pp. R1488–R1495, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. J. G. Tidball, “Inflammatory processes in muscle injury and repair,” The American Journal of Physiology: Regulatory Integrative and Comparative Physiology, vol. 288, no. 2, pp. R345–R353, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. C. F. P. Teixeira, S. R. Zamunér, J. P. Zuliani et al., “Neutrophils do not contribute to local tissue damage, but play a key role in skeletal muscle regeneration, in mice injected with Bothrops asper snake venom,” Muscle and Nerve, vol. 28, no. 4, pp. 449–459, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. R. A. Fielding, T. J. Manfredi, W. Ding, M. A. Fiatarone, W. J. Evans, and J. G. Cannon, “Acute phase response in exercise III. Neutrophil and IL-1β accumulation in skeletal muscle,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 265, no. 1, part 2, pp. R166–R172, 1993. View at Google Scholar · View at Scopus
  52. A. N. Belcastro, G. D. Arthur, T. A. Albisser, and D. A. Raj, “Heart, liver, and skeletal muscle myeloperoxidase activity during exercise,” Journal of Applied Physiology, vol. 80, no. 4, pp. 1331–1335, 1996. View at Google Scholar · View at Scopus
  53. T. K. Kishimoto and R. Rothlein, “Integrins, ICAMs, and selectins: role and regulation of adhesion molecules in neutrophil recruitment to inflammatory sites,” Advances in Pharmacology, vol. 25, pp. 117–169, 1994. View at Google Scholar · View at Scopus
  54. W. A. Muller, “Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response,” Trends in Immunology, vol. 24, no. 6, pp. 327–334, 2003. View at Google Scholar · View at Scopus
  55. B. Walzog and P. Gaehtgens, “Adhesion molecules: the path to a new understanding of acute inflammation,” News in Physiological Sciences, vol. 15, no. 3, pp. 107–113, 2000. View at Google Scholar · View at Scopus
  56. M. Sixt, R. Hallmann, O. Wendler, K. Scharffetter-Kochanek, and L. M. Sorokin, “Cell adhesion and migration properties of β2-integrin negative polymorphonuclear granulocytes on defined extracellular matrix molecules: relevance for leukocyte extravasation,” The Journal of Biological Chemistry, vol. 276, no. 22, pp. 18878–18887, 2001. View at Publisher · View at Google Scholar · View at Scopus
  57. F. X. Pizza, J. M. Peterson, J. H. Baas, and T. J. Koh, “Neutrophils contribute to muscle injury and impair its resolution after lengthening contractions in mice,” Journal of Physiology, vol. 562, no. 3, pp. 899–913, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. B. A. St. Pierre and J. G. Tidball, “Differential response of macrophage subpopulations to soleus muscle reloading after rat hindlimb suspension,” Journal of Applied Physiology, vol. 77, no. 1, pp. 290–297, 1994. View at Google Scholar · View at Scopus
  59. L. Arnold, A. Henry, F. Poron et al., “Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis,” Journal of Experimental Medicine, vol. 204, no. 5, pp. 1057–1069, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Saclier, S. Cuvellier, M. Magnan, R. Mounier, and B. Chazaud, “Monocyte/macrophage interactions with myogenic precursor cells during skeletal muscle regeneration,” The FEBS Journal, vol. 280, no. 17, pp. 4118–4130, 2013. View at Publisher · View at Google Scholar · View at Scopus
  61. I. S. McLennan, “Resident macrophages (ED2- and ED3-positive) do not phagocytose degenerating rat skeletal muscle fibres,” Cell and Tissue Research, vol. 272, no. 1, pp. 193–196, 1993. View at Publisher · View at Google Scholar · View at Scopus
  62. H. Honda, H. Kimura, and A. Rostami, “Demonstration and phenotypic characterization of resident macrophages in rat skeletal muscle,” Immunology, vol. 70, no. 2, pp. 272–277, 1990. View at Google Scholar · View at Scopus
  63. A. Pimorady-Esfahani, M. D. Grounds, and P. G. McMenamin, “Macrophages and dendritic cells in normal and regenerating murine skeletal muscle,” Muscle Nerve, vol. 20, pp. 158–166, 1997. View at Google Scholar
  64. T. Varga, R. Mounier, P. Gogolak, S. Poliska, B. Chazaud, and L. Nagy, “Tissue LyC6- macrophages are generated in the absence of circulating LyC6- monocytes and Nur77 in a model of muscle regeneration,” Journal of Immunology, vol. 191, no. 11, pp. 5695–5701, 2013. View at Google Scholar
  65. F. Geissmann, S. Jung, and D. R. Littman, “Blood monocytes consist of two principal subsets with distinct migratory properties,” Immunity, vol. 19, no. 1, pp. 71–82, 2003. View at Publisher · View at Google Scholar · View at Scopus
  66. F. Geissmann, C. Auffray, R. Palframan et al., “Blood monocytes: distinct subsets, how they relate to dendritic cells, and their possible roles in the regulation of T-cell responses,” Immunology and Cell Biology, vol. 86, no. 5, pp. 398–408, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. B. Chazaud, M. Brigitte, H. Yacoub-Youssef et al., “Dual and beneficial roles of macrophages during skeletal muscle regeneration,” Exercise and Sport Sciences Reviews, vol. 37, no. 1, pp. 18–22, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. R. D. Stout, C. Jiang, B. Matta, I. Tietzel, S. K. Watkins, and J. Suttles, “Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences,” The Journal of Immunology, vol. 175, no. 1, pp. 342–349, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Mantovani, A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati, “The chemokine system in diverse forms of macrophage activation and polarization,” Trends in Immunology, vol. 25, no. 12, pp. 677–686, 2004. View at Publisher · View at Google Scholar · View at Scopus
  70. S. S. Rabinowitz and S. Gordon, “Macrosialin, a macrophage-restricted membrane sialoprotein differentially glycosylated in response to inflammatory stimuli,” Journal of Experimental Medicine, vol. 174, no. 4, pp. 827–836, 1991. View at Publisher · View at Google Scholar · View at Scopus
  71. M. P. Ramprasad, W. Fischer, J. L. Witztum, G. R. Sambrano, O. Quehenberger, and D. Steinberg, “The 94- to 97-kDa mouse macrophage membrane protein that recognizes oxidized low density lipoprotein and phosphatidylserine-rich liposomes is identical to macrosialin, the mouse homologue of human CD68,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 21, pp. 9580–9584, 1995. View at Publisher · View at Google Scholar · View at Scopus
  72. B. B. Krippendorf and D. A. Riley, “Distinguishing unloading-versus reloading-induced changes in rat soleus muscle,” Muscle & Nerve, vol. 16, no. 1, pp. 99–108, 1993. View at Publisher · View at Google Scholar · View at Scopus
  73. B. Deng, M. Wehling-Henricks, S. A. Villalta, Y. Wang, and J. G. Tidball, “IL-10 triggers changes in macrophage phenotype that promote muscle growth and regeneration,” Journal of Immunology, vol. 189, no. 7, pp. 3669–3680, 2012. View at Publisher · View at Google Scholar · View at Scopus
  74. T. Lawrence and G. Natoli, “Transcriptional regulation of macrophage polarization: enabling diversity with identity,” Nature Reviews Immunology, vol. 11, no. 11, pp. 750–761, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. R. Mounier, M. Théret, L. Arnold et al., “AMPKα1 regulates macrophage skewing at the time of resolution of inflammation during skeletal muscle regeneration,” Cell Metabolism, vol. 18, no. 2, pp. 251–264, 2013. View at Publisher · View at Google Scholar · View at Scopus
  76. D. Sag, D. Carling, R. D. Stout, and J. Suttles, “Adenosine 5′-monophosphate-activated protein kinase promotes macrophage polarization to an anti-inflammatory functional phenotype,” Journal of Immunology, vol. 181, no. 12, pp. 8633–8641, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. V. Krishnan and B. C. Yaden, “Macrofinancing efficient remodeling of damaged muscle tissue,” Cell Metabolism, vol. 18, no. 2, pp. 149–151, 2013. View at Publisher · View at Google Scholar · View at Scopus
  78. Y. Bordon, “Macrophages: metabolic master prompts a change of tack,” Nature Reviews Immunology, vol. 13, p. 706, 2013. View at Google Scholar
  79. O. Takeuch and S. Akira, “Epigenetic control of macrophage polarization,” European Journal of Immunology, vol. 41, no. 9, pp. 2490–2493, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. S. Banerjee, H. Cui, N. Xie et al., “miR-125a-5p regulates differential activation of macrophages and inflammation,” The Journal of Biological Chemistry, vol. 288, no. 49, pp. 35428–35436, 2013. View at Publisher · View at Google Scholar
  81. S. Banerjee, N. Xie, H. Cui et al., “MicroRNA let-7c regulates macrophage polarization,” Journal of Immunology, vol. 190, no. 12, pp. 6542–6549, 2013. View at Publisher · View at Google Scholar · View at Scopus
  82. J. G. Tidball and S. A. Villalta, “Regulatory interactions between muscle and the immune system during muscle regeneration,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 298, no. 5, pp. R1173–R1187, 2010. View at Publisher · View at Google Scholar · View at Scopus
  83. S. A. Villalta, H. X. Nguyen, B. Deng, T. Gotoh, and J. G. Tidbal, “Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy,” Human Molecular Genetics, vol. 18, no. 3, pp. 482–496, 2009. View at Publisher · View at Google Scholar · View at Scopus
  84. M. R. Douglas, K. E. Morrison, M. Salmon, and C. D. Buckley, “Why does inflammation persist: a dominant role for the stromal microenvironment?” Expert Reviews in Molecular Medicine, vol. 4, no. 25, pp. 1–18, 2002. View at Google Scholar · View at Scopus
  85. A. Mauro, “Satellite cell of skeletal muscle fibers,” The Journal of Biophysical and Biochemical Cytology, vol. 9, pp. 493–495, 1961. View at Google Scholar
  86. J. Scharner and P. S. Zammit, “The muscle satellite cell at 50: the formative years,” Skeletal Muscle, vol. 1, no. 1, article 28, 2011. View at Publisher · View at Google Scholar · View at Scopus
  87. B. Gayraud-Morel, F. Chrétien, and S. Tajbakhsh, “Skeletal muscle as a paradigm for regenerative biology and medicine,” Regenerative Medicine, vol. 4, no. 2, pp. 293–319, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. P. S. Zammit, J. P. Golding, Y. Nagata, V. Hudon, T. A. Partridge, and J. R. Beauchamp, “Muscle satellite cells adopt divergent fates: a mechanism for self-renewal?” The Journal of Cell Biology, vol. 166, no. 3, pp. 347–357, 2004. View at Publisher · View at Google Scholar · View at Scopus
  89. R. Tatsumi, J. E. Anderson, C. J. Nevoret, O. Halevy, and R. E. Allen, “HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells,” Developmental Biology, vol. 194, no. 1, pp. 114–128, 1998. View at Publisher · View at Google Scholar · View at Scopus
  90. A. Irintchev, M. Zeschnigk, A. Starzinski-Powitz, and A. Wernig, “Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles,” Developmental Dynamics, vol. 199, no. 4, pp. 326–337, 1994. View at Publisher · View at Google Scholar · View at Scopus
  91. D. J. Garry, Q. Yang, R. Bassel-Duby, and R. S. Williams, “Persistent expression of MNF identifies myogenic stem cells in postnatal muscles,” Developmental Biology, vol. 188, no. 2, pp. 280–294, 1997. View at Publisher · View at Google Scholar · View at Scopus
  92. G. Mechtersheimer, M. Staudter, and P. Moller, “Expression of the natural killer (NK) cell-associated antigen CD56(Leu- 19), which is identical to the 140-kDa isoform of N-CAM, in neural and skeletal muscle cells and tumors derived therefrom,” Annals of the New York Academy of Sciences, vol. 650, pp. 311–316, 1992. View at Publisher · View at Google Scholar · View at Scopus
  93. D. D. Cornelison, M. S. Filla, H. M. Stanley, A. C. Rapraeger, and B. B. Olwin, “Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration,” Developmental Biology, vol. 239, no. 1, pp. 79–94, 2001. View at Publisher · View at Google Scholar · View at Scopus
  94. J. R. Beauchamp, L. Heslop, D. S. W. Yu et al., “Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells,” Journal of Cell Biology, vol. 151, no. 6, pp. 1221–1234, 2000. View at Publisher · View at Google Scholar · View at Scopus
  95. D. Volonte, Y. Liu, and F. Galbiati, “The modulation of caveolin-1 expression controls satellite cell activation during muscle repair,” FASEB Journal, vol. 19, no. 2, pp. 237–239, 2005. View at Publisher · View at Google Scholar · View at Scopus
  96. K. Schmidt, G. Glaser, A. Wernig, M. Wegner, and O. Rosorius, “Sox8 is a specific marker for muscle satellite cells and inhibits myogenesis,” The Journal of Biological Chemistry, vol. 278, no. 32, pp. 29769–29775, 2003. View at Publisher · View at Google Scholar · View at Scopus
  97. H. J. Lee, W. Göring, M. Ochs et al., “Sox15 is required for skeletal muscle regeneration,” Molecular and Cellular Biology, vol. 24, no. 19, pp. 8428–8436, 2004. View at Publisher · View at Google Scholar · View at Scopus
  98. T. L. Jesse, R. LaChance, M. F. Iademarco, and D. C. Dean, “Interferon regulatory factor-2 is a transcriptional activator in muscle where it regulates expression of vascular cell adhesion molecule-1,” Journal of Cell Biology, vol. 140, no. 5, pp. 1265–1276, 1998. View at Publisher · View at Google Scholar · View at Scopus
  99. V. F. Gnocchi, R. B. White, Y. Ono, J. A. Ellis, and P. S. Zammit, “Further characterisation of the molecular signature of quiescent and activated mouse muscle satellite cells,” PLoS ONE, vol. 4, no. 4, Article ID e5205, 2009. View at Publisher · View at Google Scholar · View at Scopus
  100. R. I. Sherwood, J. L. Christensen, I. M. Conboy et al., “Isolation of adult mouse myogenic progenitors: functional heterogeneity of cells within and engrafting skeletal muscle,” Cell, vol. 119, no. 4, pp. 543–554, 2004. View at Publisher · View at Google Scholar · View at Scopus
  101. S. Fukada, A. Uezumi, M. Ikemoto et al., “Molecular signature of quiescent satellite cells in adult skeletal muscle,” Stem Cells, vol. 25, no. 10, pp. 2448–2459, 2007. View at Publisher · View at Google Scholar · View at Scopus
  102. S. Fukada, M. Yamaguchi, H. Kokubo et al., “Hesr1 and Hesr3 are essential to generate undifferentiated quiescent satellite cells and to maintain satellite cell numbers,” Development, vol. 138, no. 21, pp. 4609–4619, 2011. View at Publisher · View at Google Scholar · View at Scopus
  103. F. Relaix, D. Montarras, S. Zaffran et al., “Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells,” Journal of Cell Biology, vol. 172, no. 1, pp. 91–102, 2006. View at Publisher · View at Google Scholar · View at Scopus
  104. M. Buckingham, “Skeletal muscle progenitor cells and the role of Pax genes,” Comptes Rendus—Biologies, vol. 330, no. 6-7, pp. 530–533, 2007. View at Publisher · View at Google Scholar · View at Scopus
  105. S. Creuzet, L. Lescaudron, Z. Li, and J. Fontaine-Pérus, “MyoD, myogenin, and desmin-nls-lacZ transgene emphasize the distinct patterns of satellite cell activation in growth and regeneration,” Experimental Cell Research, vol. 243, no. 2, pp. 241–253, 1998. View at Publisher · View at Google Scholar · View at Scopus
  106. Z. Yablonka-Reuveni and A. J. Rivera, “Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers,” Developmental Biology, vol. 164, no. 2, pp. 588–603, 1994. View at Publisher · View at Google Scholar · View at Scopus
  107. P. S. Zammit, T. A. Partridge, and Z. Yablonka-Reuveni, “The skeletal muscle satellite cell: the stem cell that came in from the cold,” Journal of Histochemistry & Cytochemistry, vol. 54, no. 11, pp. 1177–1191, 2006. View at Publisher · View at Google Scholar · View at Scopus
  108. K. Day, G. Shefer, A. Shearer, and Z. Yablonka-Reuveni, “The depletion of skeletal muscle satellite cells with age is concomitant with reduced capacity of single progenitors to produce reserve progeny,” Developmental Biology, vol. 340, no. 2, pp. 330–343, 2010. View at Publisher · View at Google Scholar · View at Scopus
  109. Z. Yablonka-Reuveni, M. A. Rudnicki, A. J. Rivera, M. Primig, J. E. Anderson, and P. Natanson, “The transition from proliferation to differentiation is delayed in satellite cells from mice lacking MyoD,” Developmental Biology, vol. 210, no. 2, pp. 440–455, 1999. View at Publisher · View at Google Scholar · View at Scopus
  110. L. Boldrin, F. Muntoni, and J. E. Morgan, “Are human and mouse satellite cells really the same?” Journal of Histochemistry and Cytochemistry, vol. 58, no. 11, pp. 941–955, 2010. View at Publisher · View at Google Scholar · View at Scopus
  111. K. Day, G. Shefer, J. B. Richardson, G. Enikolopov, and Z. Yablonka-Reuveni, “Nestin-GFP reporter expression defines the quiescent state of skeletal muscle satellite cells,” Developmental Biology, vol. 304, no. 1, pp. 246–259, 2007. View at Publisher · View at Google Scholar · View at Scopus
  112. Y. Nagata, H. Kobayashi, M. Umeda et al., “Sphingomyelin levels in the plasma membrane correlate with the activation state of muscle satellite cells,” Journal of Histochemistry and Cytochemistry, vol. 54, no. 4, pp. 375–384, 2006. View at Publisher · View at Google Scholar · View at Scopus
  113. F. Relaix and P. S. Zammit, “Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage,” Development, vol. 139, no. 16, pp. 2845–2856, 2012. View at Publisher · View at Google Scholar · View at Scopus
  114. Z. Yablonka-Reuveni, K. Day, A. Vine, and G. Shefer, “Defining the transcriptional signature of skeletal muscle stem cells,” Journal of Animal Science, vol. 86, supplement 14, pp. E207–E216, 2008. View at Google Scholar · View at Scopus
  115. I. M. Conboy and T. A. Rando, “The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis,” Developmental Cell, vol. 3, no. 3, pp. 397–409, 2002. View at Publisher · View at Google Scholar · View at Scopus
  116. S. Kuang, K. Kuroda, F. Le Grand, and M. A. Rudnicki, “Asymmetric self-renewal and commitment of satellite stem cells in muscle,” Cell, vol. 129, no. 5, pp. 999–1010, 2007. View at Publisher · View at Google Scholar · View at Scopus
  117. K. Schuster-Gossler, R. Cordes, and A. Gossler, “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, vol. 104, no. 2, pp. 537–542, 2007. View at Publisher · View at Google Scholar · View at Scopus
  118. C. R. R. Bjornson, T. H. Cheung, L. Liu, P. V. Tripathi, K. M. Steeper, and T. A. Rando, “Notch signaling is necessary to maintain quiescence in adult muscle stem cells,” Stem Cells, vol. 30, no. 2, pp. 232–242, 2012. View at Publisher · View at Google Scholar · View at Scopus
  119. P. Mourikis, R. Sambasivan, D. Castel, P. Rocheteau, V. Bizzarro, and S. Tajbakhsh, “A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state,” Stem Cells, vol. 30, no. 2, pp. 243–252, 2012. View at Publisher · View at Google Scholar · View at Scopus
  120. Y. Wen, P. Bi, W. Liu, A. Asakura, C. Keller, and S. Kuang, “Constitutive Notch Activation Upregulates Pax7 and promotes the self-renewal of skeletal muscle satellite cells,” Molecular and Cellular Biology, vol. 32, no. 12, pp. 2300–2311, 2012. View at Publisher · View at Google Scholar · View at Scopus
  121. R. M. George, S. Biressi, B. J. Beres et al., “Numb-deficient satellite cells have regeneration and proliferation defects,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, pp. 18549–18554, 2013. View at Publisher · View at Google Scholar
  122. A. S. Brack, I. M. Conboy, M. J. Conboy, J. Shen, and T. A. Rando, “A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis,” Cell Stem Cell, vol. 2, no. 1, pp. 50–59, 2008. View at Publisher · View at Google Scholar · View at Scopus
  123. A. J. Wagers, “Wnt not, waste not,” Cell Stem Cell, vol. 2, no. 1, pp. 6–7, 2008. View at Publisher · View at Google Scholar · View at Scopus
  124. Z. Yan, S. Choi, X. Liu et al., “Highly coordinated gene regulation in mouse skeletal muscle regeneration,” The Journal of Biological Chemistry, vol. 278, no. 10, pp. 8826–8836, 2003. View at Publisher · View at Google Scholar · View at Scopus
  125. L. Giordani and P. L. Puri, “Epigenetic control of skeletal muscle regeneration: integrating genetic determinants and environmental changes,” FEBS Journal, vol. 280, no. 17, pp. 4014–4025, 2013. View at Publisher · View at Google Scholar · View at Scopus
  126. D. Cacchiarelli, J. Martone, E. Girardi et al., “MicroRNAs involved in molecular circuitries relevant for the duchenne muscular dystrophy pathogenesis are controlled by the dystrophin/nNOS pathway,” Cell Metabolism, vol. 12, no. 4, pp. 341–351, 2010. View at Publisher · View at Google Scholar · View at Scopus
  127. T. H. Cheung, N. L. Quach, G. W. Charville et al., “Maintenance of muscle stem-cell quiescence by microRNA-489,” Nature, vol. 482, no. 7386, pp. 524–528, 2012. View at Publisher · View at Google Scholar · View at Scopus
  128. R. Bischoff, “The satellite cell and muscle regeneration,” in Myology, A. G. Engel and C. Franzini-Armstrong, Eds., pp. 97–118, McGraw-Hill, New York, NY, USA, 1994. View at Google Scholar
  129. E. Schultz and B. H. Lipton, “Skeletal muscle satellite cells: changes in proliferation potential as a function of age,” Mechanisms of Ageing and Development, vol. 20, no. 4, pp. 377–383, 1982. View at Publisher · View at Google Scholar · View at Scopus
  130. M. D. Grounds and J. K. McGeachie, “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, vol. 250, no. 3, pp. 563–569, 1987. View at Publisher · View at Google Scholar · View at Scopus
  131. F. P. Moss and C. P. Leblond, “Satellite cells as the source of nuclei in muscles of growing rats,” Anatomical Record, vol. 170, no. 4, pp. 421–435, 1971. View at Publisher · View at Google Scholar · View at Scopus
  132. E. Schultz, “Satellite cell proliferative compartments in growing skeletal muscles,” Developmental Biology, vol. 175, no. 1, pp. 84–94, 1996. View at Publisher · View at Google Scholar · View at Scopus
  133. P. Rocheteau, B. Gayraud-Morel, I. Siegl-Cachedenier, M. A. Blasco, and S. Tajbakhsh, “A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division,” Cell, vol. 148, no. 1-2, pp. 112–125, 2012. View at Publisher · View at Google Scholar · View at Scopus
  134. S. Günther, J. Kim, S. Kostin, C. Lepper, C. Fan, and T. Braun, “Myf5-positive satellite cells contribute to Pax7-dependent long-term maintenance of adult muscle stem cells,” Cell Stem Cell, vol. 13, pp. 590–601, 2013. View at Publisher · View at Google Scholar · View at Scopus
  135. S. Oustanina, G. Hause, and T. Braun, “Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification,” EMBO Journal, vol. 23, no. 16, pp. 3430–3439, 2004. View at Publisher · View at Google Scholar · View at Scopus
  136. C. Lepper, S. J. Conway, and C. M. Fan, “Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements,” Nature, vol. 460, no. 7255, pp. 627–631, 2009. View at Publisher · View at Google Scholar · View at Scopus
  137. J. von Maltzahn, A. E. Jones, R. J. Parks, and M. A. Rudnicki, “Pax7 is critical for the normal function of satellite cells in adult skeletal muscle,” Proceedings of the National Academy of Sciences of the USA, vol. 110, no. 41, pp. 16474–16479, 2013. View at Publisher · View at Google Scholar
  138. G. Messina, S. Biressi, and G. Cossu, “Non muscle stem cells and muscle regeneration,” in Skeletal Muscle Repair and Regeneration, S. Schiaffino and T. Partridge, Eds., Advances in Muscle Research, pp. 65–84, Springer, Dordrecht, The Netherlands, 2008. View at Google Scholar
  139. L. de Angelis, L. Berghella, M. Coletta et al., “Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration,” Journal of Cell Biology, vol. 147, no. 4, pp. 869–877, 1999. View at Publisher · View at Google Scholar · View at Scopus
  140. S. Kuang, S. B. Chargé, P. Seale, M. Huh, and M. A. Rudnicki, “Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis,” Journal of Cell Biology, vol. 172, no. 1, pp. 103–113, 2006. View at Publisher · View at Google Scholar · View at Scopus
  141. A. Polesskaya, P. Seale, and M. A. Rudnicki, “Wnt signaling induces the myogenic specification of resident CD45+ adult stem cells during muscle regeneration,” Cell, vol. 113, no. 7, pp. 841–852, 2003. View at Publisher · View at Google Scholar · View at Scopus
  142. T. Tamaki, A. Akatsuka, K. Ando et al., “Identification of myogenic-endothelial progenitor cells in the interstitial spaces of skeletal muscle,” The Journal of Cell Biology, vol. 157, no. 4, pp. 571–577, 2002. View at Publisher · View at Google Scholar · View at Scopus
  143. K. J. Mitchell, A. Pannérec, B. Cadot et al., “Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development,” Nature Cell Biology, vol. 12, no. 3, pp. 257–266, 2010. View at Publisher · View at Google Scholar · View at Scopus
  144. M. C. Valero, H. D. Huntsman, J. Liu, K. Zou, and M. D. Boppart, “Eccentric exercise facilitates mesenchymal stem cell appearance in skeletal muscle,” PLoS ONE, vol. 7, no. 1, Article ID e29760, 2012. View at Publisher · View at Google Scholar · View at Scopus
  145. M. N. Wosczyna, A. A. Biswas, C. A. Cogswell, and D. J. Goldhamer, “Multipotent progenitors resident in the skeletal muscle interstitium exhibit robust BMP-dependent osteogenic activity and mediate heterotopic ossification,” Journal of Bone and Mineral Research, vol. 27, no. 5, pp. 1004–1017, 2012. View at Publisher · View at Google Scholar · View at Scopus
  146. A. Asakura, P. Seale, A. Girgis-Gabardo, and M. A. Rudnicki, “Myogenic specification of side population cells in skeletal muscle,” Journal of Cell Biology, vol. 159, no. 1, pp. 123–134, 2002. View at Publisher · View at Google Scholar · View at Scopus
  147. E. Gussoni, Y. Soneoka, C. D. Strickland et al., “Dystrophin expression in the mdx mouse restored by stem cell transplantation,” Nature, vol. 401, no. 6751, pp. 390–394, 1999. View at Publisher · View at Google Scholar · View at Scopus
  148. A. Uezumi, T. Ito, D. Morikawa et al., “Fibrosis and adipogenesis originate from a common mesenchymal progenitor in skeletal muscle,” Journal of Cell Science, vol. 124, no. 21, pp. 3654–3664, 2011. View at Publisher · View at Google Scholar · View at Scopus
  149. A. Uezumi, S. Fukada, N. Yamamoto, S. Takeda, and K. Tsuchida, “Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle,” Nature Cell Biology, vol. 12, no. 2, pp. 143–152, 2010. View at Publisher · View at Google Scholar · View at Scopus
  150. S. E. Mutsaers, J. E. Bishop, G. McGrouther, and G. J. Laurent, “Mechanisms of tissue repair: from wound healing to fibrosis,” The International Journal of Biochemistry & Cell Biology, vol. 29, no. 1, pp. 5–17, 1997. View at Publisher · View at Google Scholar · View at Scopus
  151. A. W. Joe, L. Yi, A. Natarajan et al., “Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis,” Nature Cell Biology, vol. 12, no. 2, pp. 153–163, 2010. View at Publisher · View at Google Scholar · View at Scopus
  152. M. D. Grounds, “Complexity of extracellular matrix and skeletal muscle regeneration,” in Skeletal Muscle Repair and Regeneration, S. Schiaffino and T. Partridge, Eds., Advances in Muscle Research, pp. 269–301, Springer, Amsterdam, The Netherlands, 2008. View at Google Scholar
  153. C. J. Mann, E. Perdiguero, Y. Kharraz et al., “Aberrant repair and fibrosis development in skeletal muscle,” Skeletal Muscle, vol. 1, no. 1, article 21, 2011. View at Publisher · View at Google Scholar · View at Scopus
  154. G. Lluri, G. D. Langlois, B. McClellan, P. D. Soloway, and D. M. Jaworski, “Tissue inhibitor of metalloproteinase-2 (TIMP-2) regulates neuromuscular junction development via a beta1 integrin-mediated mechanism,” Journal of Neurobiology, vol. 66, no. 12, pp. 1365–1377, 2006. View at Publisher · View at Google Scholar · View at Scopus
  155. Y. Li, W. Foster, B. M. Deasy et al., “Transforming growth factor–β1 induces the differentiation of myogenic cells into fibrotic cells in injured skeletal muscle: a key event in muscle fibrogenesis,” The American Journal of Pathology, vol. 164, no. 3, pp. 1007–1019, 2004. View at Publisher · View at Google Scholar · View at Scopus
  156. P. E. Mozdziak, P. M. Pulvermacher, and E. Schultz, “Muscle regeneration during hindlimb unloading results in a reduction in muscle size after reloading,” Journal of Applied Physiology, vol. 91, no. 1, pp. 183–190, 2001. View at Google Scholar · View at Scopus
  157. P. O. Mitchell and G. K. Pavlath, “Skeletal muscle atrophy leads to loss and dysfunction of muscle precursor cells,” American Journal of Physiology: Cell Physiology, vol. 287, no. 6, pp. C1753–C1762, 2004. View at Publisher · View at Google Scholar · View at Scopus
  158. C. R. Slater and S. Schiaffino, “Skeletal muscle repair and regeneration,” in Advances in Muscle Research, S. Schiaffino and T. Partridge, Eds., pp. 303–334, Springer, Amsterdam, The Netherlands, 2008. View at Google Scholar
  159. S. Sartore, L. Gorza, and S. Schiaffino, “Fetal myosin heavy chains in regenerating muscle,” Nature, vol. 298, no. 5871, pp. 294–296, 1982. View at Publisher · View at Google Scholar · View at Scopus
  160. R. G. Whalen, J. B. Harris, G. S. Butler-Browne, and S. Sesodia, “Expression of myosin isoforms during notexin-induced regeneration of rat soleus muscles,” Developmental Biology, vol. 141, no. 1, pp. 24–40, 1990. View at Publisher · View at Google Scholar · View at Scopus
  161. K. Esser, P. Gunning, and E. Hardeman, “Nerve-dependent and -independent patterns of mRNA expression in regenerating skeletal muscle,” Developmental Biology, vol. 159, no. 1, pp. 173–183, 1993. View at Publisher · View at Google Scholar · View at Scopus
  162. M. Vinciguerra, A. Musaro, and N. Rosenthal, “Regulation of muscle atrophy in aging and disease,” Advances in Experimental Medicine and Biology, vol. 694, pp. 211–233, 2010. View at Publisher · View at Google Scholar · View at Scopus
  163. B. M. Scicchitano, E. Rizzuto, and A. Musarò, “Counteracting muscle wasting in aging and neuromuscular diseases: the critical role of IGF-1,” Aging, vol. 1, no. 5, pp. 451–457, 2009. View at Google Scholar · View at Scopus
  164. S. Carosio, M. G. Berardinelli, M. Aucello, and A. Musarò, “Impact of ageing on muscle cell regeneration,” Ageing Research Reviews, vol. 10, no. 1, pp. 35–42, 2011. View at Publisher · View at Google Scholar · View at Scopus
  165. A. L. Serrano, C. J. Mann, B. Vidal, E. Ardite, E. Perdiguero, and P. Muñoz-Cánoves, “Cellular and molecular mechanisms regulating fibrosis in skeletal muscle repair and disease,” Current Topics in Developmental Biology, vol. 96, pp. 167–201, 2011. View at Publisher · View at Google Scholar · View at Scopus
  166. B. M. Carlson and J. A. Faulkner, “Muscle transplantation between young and old rats: age of host determines recovery,” The American Journal of Physiology: Cell Physiology, vol. 256, no. 6, pp. C1262–C1266, 1989. View at Google Scholar · View at Scopus
  167. B. M. Carlson, E. I. Dedkov, A. B. Borisov, and J. A. Faulkner, “Skeletal muscle regeneration in very old rats,” Journals of Gerontology A Biological Sciences and Medical Sciences, vol. 56, no. 5, pp. B224–B233, 2001. View at Publisher · View at Google Scholar · View at Scopus
  168. I. M. Conboy, M. J. Conboy, A. J. Wagers, E. R. Girma, I. L. Weismann, and T. A. Rando, “Rejuvenation of aged progenitor cells by exposure to a young systemic environment,” Nature, vol. 433, no. 7027, pp. 760–764, 2005. View at Publisher · View at Google Scholar · View at Scopus
  169. M. Le Bihan, A. Bigot, S. S. Jensen et al., “In-depth analysis of the secretome identifies three major independent secretory pathways in differentiating human myoblasts,” Journal of Proteomics, vol. 77, pp. 344–356, 2012. View at Publisher · View at Google Scholar · View at Scopus
  170. M. Bencze, E. Negroni, D. Vallese et al., “Proinflammatory macrophages enhance the regenerative capacity of human myoblasts by modifying their kinetics of proliferation and differentiation,” Molecular Therapy, vol. 20, no. 11, pp. 2168–2179, 2012. View at Publisher · View at Google Scholar · View at Scopus
  171. L. Barberi, B. M. Scicchitano, M. De Rossi et al., “Age-dependent alteration in muscle regeneration: the critical role of tissue niche,” Biogerontology, vol. 14, no. 3, pp. 273–292, 2013. View at Publisher · View at Google Scholar · View at Scopus
  172. P. Paliwal, N. Pishesha, D. Wijaya, and I. M. Conboy, “Age dependent increase in the levels of osteopontin inhibits skeletal muscle regeneration,” Aging, vol. 4, no. 8, pp. 553–566, 2012. View at Google Scholar · View at Scopus
  173. A. Hirata, S. Masuda, T. Tamura et al., “Expression profiling of cytokines and related genes in regenerating skeletal muscle after cardiotoxin injection: a role for osteopontin,” The American Journal of Pathology, vol. 163, no. 1, pp. 203–215, 2003. View at Publisher · View at Google Scholar · View at Scopus
  174. K. Uaesoontrachoon, H. Yoo, E. M. Tudor, R. N. Pike, E. J. Mackie, and C. N. Pagel, “Osteopontin and skeletal muscle myoblasts: association with muscle regeneration and regulation of myoblast function in vitro,” International Journal of Biochemistry and Cell Biology, vol. 40, no. 10, pp. 2303–2314, 2008. View at Publisher · View at Google Scholar · View at Scopus
  175. S. A. Vetrone, E. Montecino-Rodriguez, E. Kudryashova et al., “Osteopontin promotes fibrosis in dystrophic mouse muscle by modulating immune cell subsets and intramuscular TGF-beta,” Journal of Clinical Investigation, vol. 119, no. 6, pp. 1583–1594, 2009. View at Publisher · View at Google Scholar · View at Scopus
  176. E. R. Barton, L. Morris, A. Musaro, N. Rosenthal, and H. Lee Sweeney, “Muscle-specific expression of insulin-like growth factor I counters muscle decline in mdx mice,” Journal of Cell Biology, vol. 157, no. 1, pp. 137–147, 2002. View at Publisher · View at Google Scholar · View at Scopus
  177. M. Wehling, M. J. Spencer, and J. G. Tidball, “A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice,” Journal of Cell Biology, vol. 155, no. 1, pp. 123–131, 2001. View at Publisher · View at Google Scholar · View at Scopus
  178. S. A. Villalta, C. Rinaldi, B. Deng, G. Liu, B. Fedor, and J. G. Tidball, “Interleukin-10 reduces the pathology of mdx muscular dystrophy by deactivating M1 macrophages and modulating macrophage phenotype,” Human Molecular Genetics, vol. 20, no. 4, pp. 790–805, 2011. View at Publisher · View at Google Scholar · View at Scopus
  179. P. Sousa-Victor, S. Gutarra, L. García-Prat et al., “Geriatric muscle stem cells switch reversible quiescence into senescence,” Nature, vol. 506, pp. 316–321, 2014. View at Publisher · View at Google Scholar
  180. B. D. Cosgrove, P. M. Gilbert, E. Porpiglia et al., “Rejuvenation of the muscle stem cell population restores strength to injured aged muscles,” Nature Medicine, vol. 20, pp. 255–264, 2014. View at Google Scholar
  181. M. Li and J. C. Izpisua Belmonte, “Ageing: genetic rejuvenation of old muscle,” Nature, vol. 506, pp. 304–305, 2014. View at Publisher · View at Google Scholar
  182. M. A. Rudnicki, T. Braun, S. Hinuma, and R. Jaenisch, “Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development,” Cell, vol. 71, no. 3, pp. 383–390, 1992. View at Publisher · View at Google Scholar · View at Scopus
  183. L. A. Sabourin, A. Girgis-Gabardo, P. Scale, A. Asakura, and M. A. Rudnicki, “Reduced differentiation potential of primary MyoD-/- myogenic cells derived from adult skeletal muscle,” Journal of Cell Biology, vol. 144, no. 4, pp. 631–643, 1999. View at Publisher · View at Google Scholar · View at Scopus
  184. D. D. Cornelison, B. B. Olwin, M. A. Rudnicki, and B. J. Wold, “MyoD-/- satellite cells in single-fiber culture are differentiation defective and MRF4 deficient,” Developmental Biology, vol. 224, no. 2, pp. 122–137, 2000. View at Publisher · View at Google Scholar · View at Scopus
  185. T. Braun, M. A. Rudnicki, H.-. Arnold, and R. Jaenisch, “Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death,” Cell, vol. 71, no. 3, pp. 369–382, 1992. View at Publisher · View at Google Scholar · View at Scopus
  186. S. Tajbakhsh, D. Rocancourt, G. Cossu, and M. Buckingham, “Redefining the genetic hierarchies controlling skeletal myogenesis: pax- 3 and Myf-5 act upstream of MyoD,” Cell, vol. 89, no. 1, pp. 127–138, 1997. View at Publisher · View at Google Scholar · View at Scopus
  187. A. Kaul, M. Köster, H. Neuhaus, and T. Braun, “Myf-5 revisited: loss of early myotome formation does not lead to a rib phenotype in homozygous Myf-5 mutant mice,” Cell, vol. 102, no. 1, pp. 17–19, 2000. View at Publisher · View at Google Scholar · View at Scopus
  188. J. M. Venuti, J. H. Morris, J. L. Vivian, E. N. Olson, and W. H. Klein, “Myogenin is required for late but not early aspects of myogenesis during mouse development,” Journal of Cell Biology, vol. 128, no. 4, pp. 563–576, 1995. View at Publisher · View at Google Scholar · View at Scopus
  189. J. R. Knapp, J. K. Davie, A. Myer, E. Meadows, E. N. Olson, and W. H. Klein, “Loss of myogenin in postnatal life leads to normal skeletal muscle but reduced body size,” Development, vol. 133, no. 4, pp. 601–610, 2006. View at Publisher · View at Google Scholar · View at Scopus
  190. J. L. Vivian, E. N. Olson, and W. H. Klein, “Thoracic skeletal defects in myogenin- and MRF4-deficient mice correlate with early defects in myotome and intercostal musculature,” Developmental Biology, vol. 224, no. 1, pp. 29–41, 2000. View at Publisher · View at Google Scholar · View at Scopus
  191. A. L. Thompson, G. Filatov, C. Chen et al., “A selective role for MRF4 ininnervated adult skeletal muscle: Na(V) 1.4 Na+ channel expression is reduced in MRF4-null mice,” Gene Expression, vol. 12, pp. 289–303, 2005. View at Google Scholar