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BioMed Research International
Volume 2014, Article ID 957014, 21 pages
http://dx.doi.org/10.1155/2014/957014
Review Article

Cellular Players in Skeletal Muscle Regeneration

1Department of Cell Biology and Histology, School of Medicine, “Carol Davila” University of Medicine and Pharmacy, 8 Eroii Sanitari, 050474 Bucharest, Romania
2Department of Molecular Medicine and Neuroscience, “Victor Babes,” Institute of Pathology, 99-101 Splaiul Independentei, 050096 Bucharest, Romania
3Department of Neurology, Colentina Clinical Hospital (CDPC), School of Medicine, “Carol Davila” University of Medicine and Pharmacy, 19-21 Sos. Stefan cel Mare, 020125 Bucharest, Romania

Received 7 December 2013; Revised 12 January 2014; Accepted 28 January 2014; Published 23 March 2014

Academic Editor: P. Bryant Chase

Copyright © 2014 Laura Cristina Ceafalan et al. 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. Huard, Y. Li, and F. H. Fu, “Muscle injuries and repair: current trends in research,” Journal of Bone and Joint Surgery A, vol. 84, no. 5, pp. 822–832, 2002. View at Google Scholar · View at Scopus
  2. I. Stratos, R. Rotter, C. Eipel, T. Mittlmeier, and B. Vollmar, “Granulocyte-colony stimulating factor enhances muscle proliferation and strength following skeletal muscle injury in rats,” Journal of Applied Physiology, vol. 103, no. 5, pp. 1857–1863, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. 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 · View at Scopus
  4. E. Schultz, M. C. Gibson, and T. Champion, “Satellite cells are mitotically quiescent in mature mouse muscle: an EM and radioautographic study,” Journal of Experimental Zoology, vol. 206, no. 3, pp. 451–456, 1978. View at Google Scholar · View at Scopus
  5. M. Ontell, K. C. Feng, K. Klueber, R. F. Dunn, and F. Taylor, “Myosatellite cells, growth, and regeneration in murine dystrophic muscle: a quantitative study,” Anatomical Record, vol. 208, no. 2, pp. 159–174, 1984. View at Google Scholar · View at Scopus
  6. P. S. Zammit, “All muscle satellite cells are equal, but are some more equal than others?” Journal of Cell Science, vol. 121, no. 18, pp. 2975–2982, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. M. A. LaBarge and H. M. Blau, “Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury,” Cell, vol. 111, no. 4, pp. 589–601, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. 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
  9. A. Asakura, M. Komaki, and M. A. Rudnicki, “Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation,” Differentiation, vol. 68, no. 4-5, pp. 245–253, 2001. View at Google Scholar · View at Scopus
  10. 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
  11. T. Oishi, A. Uezumi, A. Kanaji et al., “Osteogenic differentiation capacity of human skeletal muscle-derived progenitor cells,” PLoS ONE, vol. 8, no. 2, Article ID e56641, 2013. View at Google Scholar
  12. 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 Google Scholar
  13. C. A. Collins, I. Olsen, P. S. Zammit et al., “Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche,” Cell, vol. 122, no. 2, pp. 289–301, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. H. Yin, F. Price, and M. A. Rudnicki, “Satellite cells and the muscle stem cell niche,” Physiological Reviews, vol. 93, no. 1, pp. 23–67, 2013. View at Google Scholar
  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 Google Scholar · View at Scopus
  16. C. Lepper, S. J. Conway, and C. 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
  17. C. Lepper, T. A. Partridge, and C. Fan, “An absolute requirement for pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration,” Development, vol. 138, no. 17, pp. 3639–3646, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Gunther, J. Kim, S. Kostin et al., “Myf5-positive satellite cells contribute to Pax7-dependent long-term maintenance of adult muscle stem cells,” Cell Stem Cell, vol. 13, no. 5, pp. 590–601, 2013. View at Google Scholar
  19. 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 United States of America, vol. 110, no. 41, pp. 16474–16479, 2013. View at Google Scholar
  20. M. Buckingham, L. Bajard, T. Chang et al., “The formation of skeletal muscle: from somite to limb,” Journal of Anatomy, vol. 202, no. 1, pp. 59–68, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. D. D. W. Cornelison and B. J. Wold, “Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells,” Developmental Biology, vol. 191, no. 2, pp. 270–283, 1997. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Meech, K. N. Gonzalez, M. Barro et al., “Barx2 is expressed in satellite cells and is required for normal muscle growth and regeneration,” Stem Cells, vol. 30, no. 2, pp. 253–265, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. 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 Google Scholar · View at Scopus
  24. M. Z. Ratajczak, M. Majka, M. Kucia et al., “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, vol. 21, no. 3, pp. 363–371, 2003. View at Google Scholar · View at Scopus
  25. R. E. Allen, S. M. Sheehan, R. G. Taylor, T. L. Kendall, and G. M. Rice, “Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro,” Journal of Cellular Physiology, vol. 165, no. 2, pp. 307–312, 1995. View at Publisher · View at Google Scholar · View at Scopus
  26. 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 Google Scholar · View at Scopus
  27. L. A. S. Alfaro, S. A. Dick, A. L. Siegel et al., “CD34 promotes satellite cell motility and entry into proliferation to facilitate efficient skeletal muscle regeneration,” Stem Cells, vol. 29, no. 12, pp. 2030–2041, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. E. Colombo, S. Romaggi, E. Medico et al., “Human neurotrophin receptor p75NTR defines differentiation-oriented skeletal muscle precursor cells: implications for muscle regeneration,” Journal of Neuropathology and Experimental Neurology, vol. 70, no. 2, pp. 133–142, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. R. Abou-Khalil, R. Mounier, and B. Chazaud, “Regulation of myogenic stem cell behavior by vessel cells: the “ménage à trois” of satellite cells, periendothelial cells and endothelial cells,” Cell Cycle, vol. 9, no. 5, pp. 892–896, 2010. View at Google Scholar · View at Scopus
  30. D. J. Burkin and S. J. Kaufman, “The α7β1 integrin in muscle development and disease,” Cell and Tissue Research, vol. 296, no. 1, pp. 183–190, 1999. View at Publisher · View at Google Scholar · View at Scopus
  31. 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
  32. D. D. W. 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
  33. C. Chiristov, F. Chrétien, R. Abou-Khalil et al., “Muscle satellite cells and endothelial cells: close neighbors and privileged partners,” Molecular Biology of the Cell, vol. 18, no. 4, pp. 1397–1409, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Lu, D. Huang, N. Saederup, I. F. Charo, R. M. Ransohoff, and L. Zhou, “Macrophages recruited via CCR2 produce insulin-like growth factor-1 to repair acute skeletal muscle injury,” The FASEB Journal, vol. 25, no. 1, pp. 358–369, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. R. W. ten Broek, S. Grefte, and J. W. von den Hoff, “Regulatory factors and cell populations involved in skeletal muscle regeneration,” Journal of Cellular Physiology, vol. 224, no. 1, pp. 7–16, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Fukada, S. Higuchi, M. Segawa et al., “Purification and cell-surface marker characterization of quiescent satellite cells from murine skeletal muscle by a novel monoclonal antibody,” Experimental Cell Research, vol. 296, no. 2, pp. 245–255, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. 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
  38. J. E. Anderson, “The satellite cell as a companion in skeletal muscle plasticity: currency, conveyance, clue, connector and colander,” Journal of Experimental Biology, vol. 209, part 12, pp. 2276–2292, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. 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
  40. M. Cerletti, S. Jurga, C. A. Witczak et al., “Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles,” Cell, vol. 134, no. 1, pp. 37–47, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. 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
  42. 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
  43. V. Moresi, A. Pristerà, B. M. Scicchitano et al., “Tumor necrosis factor-α inhibition of skeletal muscle regeneration is mediated by a caspase-dependent stem cell response,” Stem Cells, vol. 26, no. 4, pp. 997–1008, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Pannerec, L. Formicola, V. Besson, G. Marazzi, and D. A. Sassoon, “Defining skeletal muscle resident progenitors and their cell fate potentials,” Development, vol. 140, no. 14, pp. 2879–2891, 2013. View at Google Scholar
  45. X. Mu, G. Xiang, C. R. Rathbone et al., “Slow-adhering stem cells derived from injured skeletal muscle have improved regenerative capacity,” The American Journal of Pathology, vol. 179, no. 2, pp. 931–941, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. T. Tamaki, A. Akatsuka, K. Ando et al., “Identification of myogenic-endothelial progenitor cells in the interstitial spaces of skeletal muscle,” Journal of Cell Biology, vol. 157, no. 4, pp. 571–577, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. B. G. Galvez, M. Sampaolesi, S. Brunelli et al., “Complete repair of dystrophic skeletal muscle by mesoangioblasts with enhanced migration ability,” Journal of Cell Biology, vol. 174, no. 2, pp. 231–243, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Sampaolesi, S. Blot, G. D'Antona et al., “Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs,” Nature, vol. 444, no. 7119, pp. 574–579, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. K. Lolmede, L. Campana, M. Vezzoli et al., “Inflammatory and alternatively activated human macrophages attract vessel-associated stem cells, relying on separate HMGB1- and MMP-9-dependent pathways,” Journal of Leukocyte Biology, vol. 85, no. 5, pp. 779–787, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. D. Galli, A. Innocenzi, L. Staszewsky et al., “Mesoangioblasts, vessel-associated multipotent stem cells, repair the infarcted heart by multiple cellular mechanisms: a comparison with bone marrow progenitors, fibroblasts, and endothelial cells,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 25, no. 4, pp. 692–697, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. B. Zheng, B. Cao, M. Crisan et al., “Prospective identification of myogenic endothelial cells in human skeletal muscle,” Nature Biotechnology, vol. 25, no. 9, pp. 1025–1034, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Chen, M. Corselli, B. Péault, and J. Huard, “Human blood-vessel-derived stem cells for tissue repair and regeneration,” Journal of Biomedicine and Biotechnology, vol. 2012, Article ID 597439, 9 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Armulik, A. Abramsson, and C. Betsholtz, “Endothelial/pericyte interactions,” Circulation Research, vol. 97, no. 6, pp. 512–523, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. R. G. Bagley, W. Weber, C. Rouleau, and B. A. Teicher, “Pericytes and endothelial precursor cells: cellular interactions and contributions to malignancy,” Cancer Research, vol. 65, no. 21, pp. 9741–9750, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Dellavalle, M. Sampaolesi, R. Tonlorenzi et al., “Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells,” Nature Cell Biology, vol. 9, no. 3, pp. 255–267, 2007. View at Publisher · View at Google Scholar · View at Scopus
  56. M. J. Doyle, S. Zhou, K. K. Tanaka et al., “Abcg2 labels multiple cell types in skeletal muscle and participates in muscle regeneration,” Journal of Cell Biology, vol. 195, no. 1, pp. 147–163, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Crisan, S. Yap, L. Casteilla et al., “A perivascular origin for mesenchymal stem cells in multiple human organs,” Cell Stem Cell, vol. 3, no. 3, pp. 301–313, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Dellavalle, G. Maroli, D. Covarello et al., “Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells,” Nature Communications, vol. 2, no. 1, article 499, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. D. O. Traktuev, S. Merfeld-Clauss, J. Li et al., “A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks,” Circulation Research, vol. 102, no. 1, pp. 77–85, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. D. Sun, C. O. Martinez, O. Ochoa et al., “Bone marrow-derived cell regulation of skeletal muscle regeneration,” The FASEB Journal, vol. 23, no. 2, pp. 382–395, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. M. Corselli, C. W. Chen, B. Sun et al., “The tunica adventitia of human arteries and veins as a source of mesenchymal stem cells,” Stem Cells and Development, vol. 21, no. 8, pp. 1299–1308, 2012. View at Google Scholar
  62. M. W. Majesky, X. R. Dong, V. Hoglund, G. Daum, and W. M. Mahoney Jr., “The adventitia: a progenitor cell niche for the vessel wall,” Cells Tissues Organs, vol. 195, no. 1-2, pp. 73–81, 2012. View at Google Scholar · View at Scopus
  63. Y. Torrente, M. Belicchi, M. Sampaolesi et al., “Human circulating AC133+ stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle,” The Journal of Clinical Investigation, vol. 114, no. 2, pp. 182–195, 2004. View at Publisher · View at Google Scholar · View at Scopus
  64. E. Zengin, F. Chalajour, U. M. Gehling et al., “Vascular wall resident progenitor cells: a source for postnatal vasculogenesis,” Development, vol. 133, no. 8, pp. 1543–1551, 2006. View at Publisher · View at Google Scholar · View at Scopus
  65. S. E. Duff, C. Li, J. M. Garland, and S. Kumar, “CD105 is important for angiogenesis: evidence and potential applications,” The FASEB Journal, vol. 17, no. 9, pp. 984–992, 2003. View at Publisher · View at Google Scholar · View at Scopus
  66. A. Schrage, C. Loddenkemper, U. Erben et al., “Murine CD146 is widely expressed on endothelial cells and is recognized by the monoclonal antibody ME-9F1,” Histochemistry and Cell Biology, vol. 129, no. 4, pp. 441–451, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. R. A. Collins and M. D. Grounds, “The role of tumor necrosis factor-alpha (TNF-α) in skeletal muscle regeneration: studies in TNF-α(-/-) and TNF-α(-/-)/LT-α(-/-) mice,” Journal of Histochemistry and Cytochemistry, vol. 49, no. 8, pp. 989–1001, 2001. View at Google Scholar · View at Scopus
  68. O. Ochoa, D. Sun, S. M. Reyes-Reyna et al., “Delayed angiogenesis and VEGF production in CCR2-/- mice during impaired skeletal muscle regeneration,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 293, no. 2, pp. R651–R661, 2007. View at Publisher · View at Google Scholar · View at Scopus
  69. S. L. Deshmane, S. Kremlev, S. Amini, and B. E. Sawaya, “Monocyte chemoattractant protein-1 (MCP-1): an overview,” Journal of Interferon and Cytokine Research, vol. 29, no. 6, pp. 313–326, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. S. S. M. Rensen, P. A. F. M. Doevendans, and G. J. J. M. van Eys, “Regulation and characteristics of vascular smooth muscle cell phenotypic diversity,” Netherlands Heart Journal, vol. 15, no. 3, pp. 100–108, 2007. View at Google Scholar · View at Scopus
  71. C. O. Martinez, M. J. McHale, J. T. Wells et al., “Regulation of skeletal muscle regeneration by CCR2-activating chemokines is directly related to macrophage recruitment,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 299, no. 3, pp. R832–R842, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. J. K. Daniloff, G. Levi, and M. Grumet, “Altered expression of neuronal cell adhesion molecules induced by nerve injury and repair,” Journal of Cell Biology, vol. 103, no. 3, pp. 929–945, 1986. View at Google Scholar · View at Scopus
  73. D. Íková, T. Soukup, and J. Mokrý, “Nestin expression reflects formation, revascularization and reinnervation of new myofibers in regenerating rat hind limb skeletal muscles,” Cells Tissues Organs, vol. 189, no. 5, pp. 338–347, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. E. Perentes, Y. Nakagawa, G. W. Ross, C. Stanton, and L. J. Rubinstein, “Expression of epithelial membrane antigen in perineurial cells and their derivatives. An immunohistochemical study with multiple markers,” Acta Neuropathologica, vol. 75, no. 2, pp. 160–165, 1987. View at Google Scholar · View at Scopus
  75. Y.-G. Chen and T. M. Brushart, “The effect of denervated muscle and schwann cells on axon collateral sprouting,” Journal of Hand Surgery, vol. 23, no. 6, pp. 1025–1033, 1998. View at Google Scholar · View at Scopus
  76. C. Webber and D. Zochodne, “The nerve regenerative microenvironment: early behavior and partnership of axons and Schwann cells,” Experimental Neurology, vol. 223, no. 1, pp. 51–59, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. J. A. Blake and M. R. Ziman, “The characterisation of Pax3 expressant cells in adult peripheral nerve,” PLoS ONE, vol. 8, no. 3, Article ID e59184, 2013. View at Google Scholar
  78. K. Kami, Y. Morikawa, M. Sekimoto, and E. Senba, “Gene expression of receptors for IL-6, LIF, and CNTF in regenerating skeletal muscles,” Journal of Histochemistry and Cytochemistry, vol. 48, no. 9, pp. 1203–1213, 2000. View at Google Scholar · View at Scopus
  79. M. Yamamoto, N. Okui, M. Tatebe, T. Shinohara, and H. Hirata, “Regeneration of the perineurium after microsurgical resection examined with immunolabeling for tenascin-C and alpha smooth muscle actin,” Journal of Anatomy, vol. 218, no. 4, pp. 413–425, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. S. Piña-Oviedo and C. Ortiz-Hidalgo, “The normal and neoplastic perineurium: a review,” Advances in Anatomic Pathology, vol. 15, no. 3, pp. 147–164, 2008. View at Publisher · View at Google Scholar · View at Scopus
  81. T. Goodpaster, A. Legesse-Miller, M. R. Hameed, S. C. Aisner, J. Randolph-Habecker, and H. A. Coller, “An immunohistochemical method for identifying fibroblasts in formalin-fixed, paraffin-embedded tissue,” Journal of Histochemistry and Cytochemistry, vol. 56, no. 4, pp. 347–358, 2008. View at Publisher · View at Google Scholar · View at Scopus
  82. E. Alt, Y. Yan, S. Gehmert et al., “Fibroblasts share mesenchymal phenotypes with stem cells, but lack their differentiation and colony-forming potential,” Biology of the Cell, vol. 103, no. 4, pp. 197–208, 2011. View at Publisher · View at Google Scholar · View at Scopus
  83. A. W. B. 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
  84. F. Strutz, H. Okada, C. W. Lo et al., “Identification and characterization of a fibroblast marker: FSP1,” Journal of Cell Biology, vol. 130, no. 2, pp. 393–405, 1995. View at Publisher · View at Google Scholar · View at Scopus
  85. A. S. Brack, M. J. Conboy, S. Roy et al., “Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis,” Science, vol. 317, no. 5839, pp. 807–810, 2007. View at Publisher · View at Google Scholar · View at Scopus
  86. S. J. Mathew, J. M. Hansen, A. J. Merrell et al., “Connective tissue fibroblasts and Tcf4 regulate myogenesis,” Development, vol. 138, no. 2, pp. 371–384, 2011. View at Publisher · View at Google Scholar · View at Scopus
  87. M. M. Murphy, J. A. Lawson, S. J. Mathew, D. A. Hutcheson, and G. Kardon, “Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration,” Development, vol. 138, no. 17, pp. 3625–3637, 2011. View at Publisher · View at Google Scholar · View at Scopus
  88. K. K. Long, M. Montano, and G. K. Pavlath, “Sca-1 is negatively regulated by TGF-β1 in myogenic cells,” The FASEB Journal, vol. 25, no. 4, pp. 1156–1165, 2011. View at Publisher · View at Google Scholar · View at Scopus
  89. 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
  90. L. M. Popescu, E. Manole, C. S. Şerboiu et al., “Identification of telocytes in skeletal muscle interstitium: implication for muscle regeneration,” Journal of Cellular and Molecular Medicine, vol. 15, no. 6, pp. 1379–1392, 2011. View at Publisher · View at Google Scholar · View at Scopus
  91. L. C. Suciu, B. O. Popescu, S. Kostin, and L. M. Popescu, “Platelet-derived growth factor receptor-beta-positive telocytes in skeletal muscle interstitium,” Journal of Cellular and Molecular Medicine, vol. 16, no. 4, pp. 701–707, 2012. View at Google Scholar
  92. C. Sonnet, P. Lafuste, L. Arnold et al., “Human macrophages rescue myoblasts and myotubes from apoptosis through a set of adhesion molecular systems,” Journal of Cell Science, vol. 119, part 12, pp. 2497–2507, 2006. View at Publisher · View at Google Scholar · View at Scopus
  93. E. Duchesne, M. Tremblay, and C. H. Cote, “Mast cell tryptase stimulates myoblast proliferation, a mechanism relying on protease-activated receptor-2 and cyclooxygenase-2,” BMC Musculoskeletal Disorders, vol. 12, article 235, 2011. View at Publisher · View at Google Scholar · View at Scopus
  94. E. Duchesne, P. Bouchard, M. P. Roussel, and C. H. Cote, “Mast cells can regulate skeletal muscle cell proliferation by multiple mechanisms,” Muscle & Nerve, vol. 48, no. 3, pp. 403–414, 2013. View at Google Scholar
  95. Y. Kharraz, J. Guerra, C. J. Mann, A. L. Serrano, and P. Munoz-Canoves, “Macrophage plasticity and the role of inflammation in skeletal muscle repair,” Mediators of Inflammation, vol. 2013, Article ID 491497, 9 pages, 2013. View at Publisher · View at Google Scholar
  96. G. L. Warren, L. O'Farrell, M. Summan et al., “Role of CC chemokines in skeletal muscle functional restoration after injury,” American Journal of Physiology—Cell Physiology, vol. 286, no. 5, pp. C1031–C1036, 2004. View at Publisher · View at Google Scholar · View at Scopus
  97. H. X. Nguyen, A. J. Lusis, and J. G. Tidball, “Null mutation of myeloperoxidase in mice prevents mechanical activation of neutrophil lysis of muscle cell membranes in vitro and in vivo,” Journal of Physiology, vol. 565, part 2, pp. 403–413, 2005. View at Publisher · View at Google Scholar · View at Scopus
  98. L. Yahiaoui, D. Gvozdic, G. Danialou, M. Mack, and B. J. Petrof, “CC family chemokines directly regulate myoblast responses to skeletal muscle injury,” Journal of Physiology, vol. 586, no. 16, pp. 3991–4004, 2008. View at Publisher · View at Google Scholar · View at Scopus
  99. 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
  100. 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?” Journal of Cell Biology, vol. 166, no. 3, pp. 347–357, 2004. View at Publisher · View at Google Scholar · View at Scopus
  101. J. G. Tidball and S. A. Villalta, “Regulatory interactions between muscle and the immune system during muscle regeneration,” 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
  102. F. le Grand and M. A. Rudnicki, “Skeletal muscle satellite cells and adult myogenesis,” Current Opinion in Cell Biology, vol. 19, no. 6, pp. 628–633, 2007. View at Publisher · View at Google Scholar · View at Scopus
  103. R. de Mori, S. Straino, A. di Carlo et al., “Multiple effects of high mobility group box protein 1 in skeletal muscle regeneration,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 27, no. 11, pp. 2377–2383, 2007. View at Publisher · View at Google Scholar · View at Scopus
  104. Y. Li, “TNF-α is a mitogen in skeletal muscle,” American Journal of Physiology—Cell Physiology, vol. 285, no. 2, pp. C370–C376, 2003. View at Google Scholar · View at Scopus
  105. M. Hara, S. Yuasa, K. Shimoji et al., “G-CSF influences mouse skeletal muscle development and regeneration by stimulating myoblast proliferation,” Journal of Experimental Medicine, vol. 208, no. 4, pp. 715–727, 2011. View at Publisher · View at Google Scholar · View at Scopus
  106. 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
  107. 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
  108. K. K. Tanaka, J. K. Hall, A. A. Troy, D. D. W. Cornelison, S. M. Majka, and B. B. Olwin, “Syndecan-4-expressing muscle progenitor cells in the SP engraft as satellite cells during muscle regeneration,” Cell Stem Cell, vol. 4, no. 3, pp. 217–225, 2009. View at Publisher · View at Google Scholar · View at Scopus
  109. 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
  110. C. A. Rossi, M. Pozzobon, A. Ditadi et al., “Clonal characterization of rat muscle satellite cells: proliferation, metabolism and differentiation define an intrinsic heterogeneity,” PLoS ONE, vol. 5, no. 1, Article ID e8523, 2010. View at Publisher · View at Google Scholar · View at Scopus
  111. 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
  112. Z. Qu-Petersen, B. Deasy, R. Jankowski et al., “Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration,” Journal of Cell Biology, vol. 157, no. 5, pp. 851–864, 2002. View at Publisher · View at Google Scholar · View at Scopus
  113. D. Danieli-Betto, S. Peron, E. Germinario et al., “Sphingosine 1-phosphate signaling is involved in skeletal muscle regeneration,” American Journal of Physiology—Cell Physiology, vol. 298, no. 3, pp. C550–C558, 2010. View at Publisher · View at Google Scholar · View at Scopus
  114. G. Ferrari, G. Cusella-De Angelis, M. Coletta et al., “Muscle regeneration by bone marrow-derived myogenic progenitors,” Science, vol. 279, no. 5356, pp. 1528–1530, 1998. View at Publisher · View at Google Scholar · View at Scopus
  115. R. Palumbo, M. Sampaolesi, F. de Marchis et al., “Extracellular HMGB1, a signal of tissue damage, induces mesoangioblast migration and proliferation,” Journal of Cell Biology, vol. 164, no. 3, pp. 441–449, 2004. View at Publisher · View at Google Scholar · View at Scopus
  116. L. Bosurgi, G. Corna, M. Vezzoli et al., “Transplanted mesoangioblasts require macrophage IL-10 for survival in a mouse model of muscle injury,” The Journal of Immunology, vol. 188, no. 12, pp. 6267–6277, 2012. View at Google Scholar
  117. H. Kawada and M. Ogawa, “Bone marrow origin of hematopoietic progenitors and stem cells in murine muscle,” Blood, vol. 98, no. 7, pp. 2008–2013, 2001. View at Publisher · View at Google Scholar · View at Scopus
  118. T. Tamaki, Y. Uchiyama, Y. Okada et al., “Functional recovery of damaged skeletal muscle through synchronized vasculogenesis, myogenesis, and neurogenesis by muscle-derived stem cells,” Circulation, vol. 112, no. 18, pp. 2857–2866, 2005. View at Publisher · View at Google Scholar · View at Scopus
  119. D. Tilki, H. Hohn, B. Ergün, S. Rafii, and S. Ergün, “Emerging biology of vascular wall progenitor cells in health and disease,” Trends in Molecular Medicine, vol. 15, no. 11, pp. 501–509, 2009. View at Publisher · View at Google Scholar · View at Scopus
  120. P. Campagnolo, D. Cesselli, A. Al Haj Zen et al., “Human adult vena saphena contains perivascular progenitor cells endowed with clonogenic and proangiogenic potential,” Circulation, vol. 121, no. 15, pp. 1735–1745, 2010. View at Publisher · View at Google Scholar · View at Scopus
  121. C. Farrington-Rock, N. J. Crofts, M. J. Doherty, B. A. Ashton, C. Griffin-Jones, and A. E. Canfield, “Chondrogenic and adipogenic potential of microvascular pericytes,” Circulation, vol. 110, no. 15, pp. 2226–2232, 2004. View at Publisher · View at Google Scholar · View at Scopus
  122. G. Paul, I. Özen, N. S. Christophersen et al., “The adult human brain harbors multipotent perivascular mesenchymal stem cells,” PLoS ONE, vol. 7, no. 4, Article ID e35577, 2012. View at Publisher · View at Google Scholar · View at Scopus
  123. I. H. Conboy, M. J. Conboy, G. M. Smythe, and T. A. Rando, “Notch-mediated restoration of regenerative potential to aged muscle,” Science, vol. 302, no. 5650, pp. 1575–1577, 2003. View at Publisher · View at Google Scholar · View at Scopus
  124. B. Chazaud, C. Sonnet, P. Lafuste et al., “Satellite cells attract monocytes and use macrophages as a support to escape apoptosis and enhance muscle growth,” Journal of Cell Biology, vol. 163, no. 5, pp. 1133–1143, 2003. View at Publisher · View at Google Scholar · View at Scopus
  125. R. Mounier, F. Chrétien, and B. Chazaud, “Blood vessels and the satellite cell niche,” Current Topics in Developmental Biology, vol. 96, pp. 121–138, 2011. View at Publisher · View at Google Scholar · View at Scopus
  126. A. Pacilli and G. Pasquinelli, “Vascular wall resident progenitor cells. A review,” Experimental Cell Research, vol. 315, no. 6, pp. 901–914, 2009. View at Publisher · View at Google Scholar · View at Scopus
  127. J. N. Passman, X. R. Dong, S. Wu et al., “A sonic hedgehog signaling domain in the arterial adventitia supports resident Sca1+ smooth muscle progenitor cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 27, pp. 9349–9354, 2008. View at Publisher · View at Google Scholar · View at Scopus
  128. J. G. Tidball, “Inflammatory processes in muscle injury and repair,” 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
  129. 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
  130. 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
  131. L. Bosurgi, A. A. Manfredi, and P. Rovere-Querini, “Macrophages in injured skeletal muscle: a perpetuum mobile causing and limiting fibrosis, prompting or restricting resolution and regeneration,” Frontiers in Immunology, vol. 2, article 62, 2011. View at Google Scholar
  132. G. L. Warren, T. Hulderman, N. Jensen et al., “Physiological role of tumor necrosis factor alpha in traumatic muscle injury,” The FASEB Journal, vol. 16, no. 12, pp. 1630–1632, 2002. View at Google Scholar · View at Scopus
  133. S. Chen, E. Gerken, Y. Zhang et al., “Role of TNF-α signaling in regeneration of cardiotoxin-injured muscle,” American Journal of Physiology—Cell Physiology, vol. 289, no. 5, pp. C1179–C1187, 2005. View at Publisher · View at Google Scholar · View at Scopus
  134. R. C. J. Langen, J. L. J. van der Velden, A. M. W. J. Schols, M. C. J. M. Kelders, E. F. M. Wouters, and Y. M. W. Janssen-Heininger, “Tumor necrosis factor-alpha inhibits myogenic differentiation through MyoD protein destabilization,” The FASEB Journal, vol. 18, no. 2, pp. 227–237, 2004. View at Publisher · View at Google Scholar · View at Scopus
  135. S. Chen, B. Jin, and Y. Li, “TNF-α regulates myogenesis and muscle regeneration by activating p38 MAPK,” American Journal of Physiology—Cell Physiology, vol. 292, no. 5, pp. C1660–C1671, 2007. View at Publisher · View at Google Scholar · View at Scopus
  136. B. Baeza-Raja and P. Muñoz-Cánoves, “p38 MAPK-induced nuclear factor-kappaB activity is required for skeletal muscle differentiation: role of interleukin-6,” Molecular Biology of the Cell, vol. 15, no. 4, pp. 2013–2026, 2004. View at Publisher · View at Google Scholar · View at Scopus
  137. M. Cheng, M. Nguyen, G. Fantuzzi, and T. J. Koh, “Endogenous interferon-γ is required for efficient skeletal muscle regeneration,” American Journal of Physiology—Cell Physiology, vol. 294, no. 5, pp. C1183–C1191, 2008. View at Publisher · View at Google Scholar · View at Scopus
  138. J. Ma, Q. Wang, T. Fei, J. J. Han, and Y. Chen, “MCP-1 mediates TGF-β-induced angiogenesis by stimulating vascular smooth muscle cell migration,” Blood, vol. 109, no. 3, pp. 987–994, 2007. View at Publisher · View at Google Scholar · View at Scopus
  139. P. K. Shireman, V. Contreras-Shannon, O. Ochoa, B. P. Karia, J. E. Michalek, and L. M. McManus, “MCP-1 deficiency causes altered inflammation with impaired skeletal muscle regeneration,” Journal of Leukocyte Biology, vol. 81, no. 3, pp. 775–785, 2007. View at Publisher · View at Google Scholar · View at Scopus
  140. K. H. Hong, J. Ryu, and K. H. Han, “Monocyte chemoattractant protein-1-induced angiogenesis is mediated by vascular endothelial growth factor-A,” Blood, vol. 105, no. 4, pp. 1405–1407, 2005. View at Publisher · View at Google Scholar · View at Scopus
  141. 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
  142. M. L. Novak, S. C. Bryer, M. Cheng et al., “Macrophage-specific expression of urokinase-type plasminogen activator promotes skeletal muscle regeneration,” The Journal of Immunology, vol. 187, no. 3, pp. 1448–1457, 2011. View at Publisher · View at Google Scholar · View at Scopus
  143. T. H. Sisson, M. Nguyen, B. Yu, M. L. Novak, R. H. Simon, and T. J. Koh, “Urokinase-type plasminogen activator increases hepatocyte growth factor activity required for skeletal muscle regeneration,” Blood, vol. 114, no. 24, pp. 5052–5061, 2009. View at Publisher · View at Google Scholar · View at Scopus
  144. M. S. Rodeheffer, “Tipping the scale: muscle versus fat,” Nature Cell Biology, vol. 12, no. 2, pp. 102–104, 2010. View at Publisher · View at Google Scholar · View at Scopus
  145. A. L. Moyer and K. R. Wagner, “Regeneration versus fibrosis in skeletal muscle,” Current Opinion in Rheumatology, vol. 23, no. 6, pp. 568–573, 2011. View at Publisher · View at Google Scholar · View at Scopus
  146. A. M. Czerwinska, W. Streminska, M. A. Ciemerych, and I. Grabowska, “Mouse gastrocnemius muscle regeneration after mechanical or cardiotoxin injury,” Folia Histochemica et Cytobiologica, vol. 50, no. 1, pp. 144–153, 2012. View at Publisher · View at Google Scholar · View at Scopus
  147. Z. Zhou, C. P. Cornelius, M. Eichner, and A. Bornemann, “Reinnervation-induced alterations in rat skeletal muscle,” Neurobiology of Disease, vol. 23, no. 3, pp. 595–602, 2006. View at Publisher · View at Google Scholar · View at Scopus
  148. K. Hiatt, D. Lewis, M. Shew, K. Bijangi-Vishehsaraei, and S. Halum, “Ciliary neurotrophic factor (CNTF) promotes skeletal muscle progenitor cell (MPC) viability via the phosphatidylinositol 3-kinase-Akt pathway,” Journal of Tissue Engineering and Regenerative Medicine, 2012. View at Publisher · View at Google Scholar
  149. N. Lee, R. P. Spearry, K. M. Leahy et al., “Muscle ciliary neurotrophic factor receptor alpha promotes axonal regeneration and functional recovery following peripheral nerve lesion,” Journal of Comparative Neurology, vol. 521, no. 13, pp. 2947–2965, 2013. View at Google Scholar
  150. J. Menetrey, C. Kasemkijwattana, C. S. Day et al., “Growth factors improve muscle healing in vivo,” Journal of Bone and Joint Surgery B, vol. 82, no. 1, pp. 131–137, 2000. View at Google Scholar · View at Scopus
  151. R. Heumann, S. Korsching, C. Bandtlow, and H. Thoenen, “Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection,” Journal of Cell Biology, vol. 104, no. 6, pp. 1623–1631, 1987. View at Google Scholar · View at Scopus
  152. M. Lavasani, A. Lu, H. Peng, J. Cummins, and J. Huard, “Nerve growth factor improves the muscle regeneration capacity of muscle stem cells in dystrophic muscle,” Human Gene Therapy, vol. 17, no. 2, pp. 180–192, 2006. View at Publisher · View at Google Scholar · View at Scopus
  153. Y. Li and W. J. Thompson, “Nerve terminal growth remodels neuromuscular synapses in mice following regeneration of the postsynaptic muscle fiber,” The Journal of Neuroscience, vol. 31, no. 37, pp. 13191–13203, 2011. View at Publisher · View at Google Scholar · View at Scopus