Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014 (2014), Article ID 560629, 9 pages
http://dx.doi.org/10.1155/2014/560629
Review Article

Macrophage Plasticity in Skeletal Muscle Repair

1Division of Regenerative Medicine, Stem Cells and Gene Therapy, San Raffaele Scientific Institute, Via Olgettina 58, 20132 Milano, Italy
2San Raffaele University, Via Olgettina 58, 20132 Milano, Italy
3Department of Health Sciences, University of Milano-Bicocca, via Cadore 48, 20900 Monza, Italy

Received 18 January 2014; Revised 13 March 2014; Accepted 31 March 2014; Published 17 April 2014

Academic Editor: Pura Muñoz-Cánoves

Copyright © 2014 Elena Rigamonti 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. Y. Bertrand, A. Jalil, M. Klaine, S. Jung, A. Cumano, and I. Godin, “Three pathways to mature macrophages in the early mouse yolk sac,” Blood, vol. 106, no. 9, pp. 3004–3011, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. D. A. Ovchinnikov, “Macrophages in the embryo and beyond: much more than just giant phagocytes,” Genesis, vol. 46, no. 9, pp. 447–462, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Sica, P. Invernizzi, and A. Mantovani, “Macrophage plasticity and polarization in liver homeostasis and pathology,” Hepatology, 2013. View at Publisher · View at Google Scholar
  4. A. Mantovani and M. Locati, “Tumor-associated macrophages as a paradigm of macrophage plasticity, diversity, and polarization: lessons and open questions,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 33, no. 7, pp. 1478–1483, 2013. View at Publisher · View at Google Scholar
  5. G. P. Fadini, R. Cappellari, M. Mazzucato, C. Agostini, S. V. de Kreutzenberg, and A. Avogaro, “Monocyte-macrophage polarization balance in pre-diabetic individuals,” Acta Diabetologica, vol. 50, no. 6, pp. 977–982, 2013. View at Publisher · View at Google Scholar
  6. A. Mantovani, A. Sica, and M. Locati, “Macrophage polarization comes of age,” Immunity, vol. 23, no. 4, pp. 344–346, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Sica and A. Mantovani, “Macrophage plasticity and polarization: in vivo veritas,” Journal of Clinical Investigation, vol. 122, no. 3, pp. 787–795, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. D. M. Mosser and J. P. Edwards, “Exploring the full spectrum of macrophage activation,” Nature Reviews Immunology, vol. 8, no. 12, pp. 958–969, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Mantovani, S. K. Biswas, M. R. Galdiero, A. Sica, and M. Locati, “Macrophage plasticity and polarization in tissue repair and remodelling,” The Journal of Pathology, vol. 229, no. 2, pp. 176–185, 2013. View at Publisher · View at Google Scholar
  10. J. M. Daley, S. K. Brancato, A. A. Thomay, J. S. Reichner, and J. E. Albina, “The phenotype of murine wound macrophages,” Journal of Leukocyte Biology, vol. 87, no. 1, pp. 59–67, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. S. K. Brancato and J. E. Albina, “Wound macrophages as key regulators of repair: origin, phenotype, and function,” American Journal of Pathology, vol. 178, no. 1, pp. 19–25, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Sindrilaru, T. Peters, S. Wieschalka et al., “An unrestrained proinflammatory M1 macrophage population induced by iron impairs wound healing in humans and mice,” Journal of Clinical Investigation, vol. 121, no. 3, pp. 985–997, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. P. F. Lesault, M. Théret, M. Magnan et al., “Macrophages improve survival, proliferation and migration of engrafted myogenic precursor cells into MDX skeletal muscle,” PLoS ONE, vol. 7, no. 10, Article ID e46698, 2012. View at Publisher · View at Google Scholar
  14. O. Gonzalez-Perez, F. Gutierrez-Fernandez, V. Lopez-Virgen, J. Collas-Aguilar, A. Quinones-Hinojosa, and J. M. Garcia-Verdugo, “Immunological regulation of neurogenic niches in the adult brain,” Neuroscience, vol. 226, pp. 270–281, 2012. View at Publisher · View at Google Scholar
  15. L. Bosurgi, G. Corna, M. Vezzoli et al., “Transplanted mesoangioblasts require macrophage IL-10 for survival in a mouse model of muscle injury,” Journal of Immunology, vol. 188, no. 12, pp. 6267–6277, 2012. View at Publisher · View at Google Scholar
  16. T. Lucas, A. Waisman, R. Ranjan et al., “Differential roles of macrophages in diverse phases of skin repair,” Journal of Immunology, vol. 184, no. 7, pp. 3964–3977, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. R. Mirza, L. A. DiPietro, and T. J. Koh, “Selective and specific macrophage ablation is detrimental to wound healing in mice,” American Journal of Pathology, vol. 175, no. 6, pp. 2454–2462, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. J. S. Duffield, S. J. Forbes, C. M. Constandinou et al., “Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair,” Journal of Clinical Investigation, vol. 115, no. 1, pp. 56–65, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. H. Suga, M. Sugaya, H. Fujita et al., “TLR4, rather than TLR2, regulates wound healing through TGF-beta and CCL5 expression,” Journal of Dermatological Science, vol. 73, no. 2, pp. 117–124, 2014. View at Publisher · View at Google Scholar
  20. M. J. van Amerongen, M. C. Harmsen, N. van Rooijen, A. H. Petersen, and M. J. A. van Luyn, “Macrophage depletion impairs wound healing and increases left ventricular remodeling after myocardial injury in mice,” American Journal of Pathology, vol. 170, no. 3, pp. 818–829, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Nahrendorf, F. K. Swirski, E. Aikawa et al., “The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions,” Journal of Experimental Medicine, vol. 204, no. 12, pp. 3037–3047, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. H. Tsujioka, T. Imanishi, H. Ikejima et al., “Impact of heterogeneity of human peripheral blood monocyte subsets on myocardial salvage in patients with primary acute myocardial infarction,” Journal of the American College of Cardiology, vol. 54, no. 2, pp. 130–138, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Troidl, H. Möllmann, H. Nef et al., “Classically and alternatively activated macrophages contribute to tissue remodelling after myocardial infarction,” Journal of Cellular and Molecular Medicine, vol. 13, no. 9, pp. 3485–3496, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. R. Safadi, M. Ohta, C. E. Alvarez et al., “Immune stimulation of hepatic fibrogenesis by CD8 cells and attenuation by transgenic interleukin-10 from hepatocytes,” Gastroenterology, vol. 127, no. 3, pp. 870–882, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. O. Park, W.-I. Jeong, L. Wang et al., “Diverse roles of invariant natural killer T cells in liver injury and fibrosis induced by carbon tetrachloride,” Hepatology, vol. 49, no. 5, pp. 1683–1694, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. C. A. Rivera, B. U. Bradford, K. J. Hunt et al., “Attenuation of CCl4-induced hepatic fibrosis by GdCl3 treatment or dietary glycine,” American Journal of Physiology: Gastrointestinal and Liver Physiology, vol. 281, no. 1, pp. G200–G207, 2001. View at Google Scholar · View at Scopus
  27. M. Imamura, T. Ogawa, Y. Sasaguri, K. Chayama, and H. Ueno, “Suppression of macrophage infiltration inhibits activation of hepatic stellate cells and liver fibrogenesis in rats,” Gastroenterology, vol. 128, no. 1, pp. 138–146, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. J. A. Fallowfield, M. Mizuno, T. J. Kendall et al., “Scar-associated macrophages are a major source of hepatic matrix metalloproteinase-13 and facilitate the resolution of murine hepatic fibrosis,” Journal of Immunology, vol. 178, no. 8, pp. 5288–5295, 2007. View at Google Scholar · View at Scopus
  29. E. Liaskou, H. W. Zimmermann, K. K. Li et al., “Monocyte subsets in human liver disease show distinct phenotypic and functional characteristics,” Hepatology, vol. 57, no. 1, pp. 385–398, 2013. View at Publisher · View at Google Scholar
  30. K. R. Karlmark, R. Weiskirchen, H. W. Zimmermann et al., “Hepatic recruitment of the inflammatory Gr1+ monocyte subset upon liver injury promotes hepatic fibrosis,” Hepatology, vol. 50, no. 1, pp. 261–274, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Mitchell, D. Couton, J.-P. Couty et al., “Dual role of CCR2 in the constitution and the resolution of liver fibrosis in mice,” American Journal of Pathology, vol. 174, no. 5, pp. 1766–1775, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. M. A. Gibbons, A. C. MacKinnon, P. Ramachandran et al., “Ly6Chi monocytes direct alternatively activated profibrotic macrophage regulation of lung fibrosis,” American Journal of Respiratory and Critical Care Medicine, vol. 184, no. 5, pp. 569–581, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. D. V. Pechkovsky, A. Prasse, F. Kollert et al., “Alternatively activated alveolar macrophages in pulmonary fibrosis-mediator production and intracellular signal transduction,” Clinical Immunology, vol. 137, no. 1, pp. 89–101, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. E. Bargagli, A. Prasse, C. Olivieri, J. Muller-Quernheim, and P. Rottoli, “Macrophage-derived biomarkers of idiopathic pulmonary fibrosis,” Pulmonary Medicine, vol. 2011, Article ID 717130, 7 pages, 2011. View at Publisher · View at Google Scholar
  35. S. Brunelli and P. Rovere-Querini, “The immune system and the repair of skeletal muscle,” Pharmacological Research, vol. 58, no. 2, pp. 117–121, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. 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
  37. 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
  38. 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
  39. 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
  40. F. S. Tedesco, A. Dellavalle, J. Diaz-Manera, G. Messina, and G. Cossu, “Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells,” Journal of Clinical Investigation, vol. 120, no. 1, pp. 11–19, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. G. Paulsen, R. Crameri, H. B. Benestad et al., “Time course of leukocyte accumulation in human muscle after eccentric exercise,” Medicine and Science in Sports and Exercise, vol. 42, no. 1, pp. 75–85, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. K. Zerria, E. Jerbi, S. Hammami et al., “Recombinant integrin CD11b A-domain blocks polymorphonuclear cells recruitment and protects against skeletal muscle inflammatory injury in the rat,” Immunology, vol. 119, no. 4, pp. 431–440, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. 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
  44. N. Dumont, P. Bouchard, and J. Frenette, “Neutrophil-induced skeletal muscle damage: a calculated and controlled response following hindlimb unloading and reloading,” American Journal of Physiology: Regulatory Integrative and Comparative Physiology, vol. 295, no. 6, pp. R1831–R1838, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. J. G. Tidball, E. Berchenko, and J. Frenette, “Macrophage invasion does not contribute to muscle membrane injury during inflammation,” Journal of Leukocyte Biology, vol. 65, no. 4, pp. 492–498, 1999. View at Google Scholar · View at Scopus
  46. B. Chazaud, “Macrophages: supportive cells for tissue repair and regeneration,” Immunobiology, vol. 219, no. 3, pp. 172–178, 2014. View at Publisher · View at Google Scholar
  47. C. Johnson-Léger, M. Aurrand-Lions, and B. A. Imhof, “The parting of the endothelium: miracle, or simply a junctional affair?” Journal of Cell Science, vol. 113, part 6, pp. 921–933, 2000. View at Google Scholar · View at Scopus
  48. M. R. Elliott and K. S. Ravichandran, “Clearance of apoptotic cells: implications in health and disease,” Journal of Cell Biology, vol. 189, no. 7, pp. 1059–1070, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. B.-Z. Qian and J. W. Pollard, “Macrophage diversity enhances tumor progression and metastasis,” Cell, vol. 141, no. 1, pp. 39–51, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. I. S. Mclennan, “Degenerating and regenerating skeletal muscles contain several subpopulations of macrophages with distinct spatial and temporal distributions,” Journal of Anatomy, vol. 188, part 1, pp. 17–28, 1996. View at Google Scholar · View at Scopus
  51. 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
  52. M. Summan, G. L. Warren, R. R. Mercer et al., “Macrophages and skeletal muscle regeneration: a clodronate-containing liposome depletion study,” 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
  53. N. Dumont and J. Frenette, “Macrophages protect against muscle atrophy and promote muscle recovery in vivo and in vitro: a mechanism partly dependent on the insulin-like growth factor-1 signaling molecule,” American Journal of Pathology, vol. 176, no. 5, pp. 2228–2235, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. 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
  55. J. G. Tidball, “Interactions between muscle and the immune system during modified musculoskeletal loading,” Clinical Orthopaedics and Related Research, no. 403, pp. S100–S109, 2002. View at Google Scholar · View at Scopus
  56. J. E. Heredia, L. Mukundan, F. M. Chen et al., “Type 2 innate signals stimulate fibro/adipogenic progenitors to facilitate muscle regeneration,” Cell, vol. 153, no. 2, pp. 376–388, 2013. View at Publisher · View at Google Scholar
  57. M. Brigitte, C. Schilte, A. Plonquet et al., “Muscle resident macrophages control the immune cell reaction in a mouse model of notexin-induced myoinjury,” Arthritis and Rheumatism, vol. 62, no. 1, pp. 268–279, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. G. L. Warren, T. Hulderman, D. Mishra et al., “Chemokine receptor CCR2 involvement in skeletal muscle regeneration,” FASEB Journal, vol. 19, no. 3, pp. 413–415, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. 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
  60. L. Zhang, L. Ran, G. E. Garcia et al., “Chemokine CXCL16 regulates neutrophil and macrophage infiltration into injured muscle, promoting muscle regeneration,” American Journal of Pathology, vol. 175, no. 6, pp. 2518–2527, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. 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
  62. E. Rigamonti, T. Touvier, E. Clementi, A. A. Manfredi, S. Brunelli, and P. Rovere-Querini, “Requirement of inducible nitric oxide synthase for skeletal muscle regeneration after acute damage,” Journal of Immunology, vol. 190, no. 4, pp. 1767–1777, 2013. View at Publisher · View at Google Scholar
  63. M. Saclier, H. Yacoub-Youssef, A. L. Mackey et al., “Differentially activated macrophages orchestrate myogenic precursor cell fate during human skeletal muscle regeneration,” Stem Cells, vol. 31, no. 2, pp. 384–396, 2013. View at Publisher · View at Google Scholar
  64. D. Ruffell, F. Mourkioti, A. Gambardella et al., “A CREB-C/EBPβ cascade induces M2 macrophage-specific gene expression and promotes muscle injury repair,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 41, pp. 17475–17480, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. E. Perdiguero, P. Sousa-Victor, V. Ruiz-Bonilla et al., “p38/MKP-1-regulated AKT coordinates macrophage transitions and resolution of inflammation during tissue repair,” Journal of Cell Biology, vol. 195, no. 2, pp. 307–322, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. 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 Google Scholar · View at Scopus
  67. 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
  68. D. Burzyn, W. Kuswanto, D. Kolodin et al., “A special population of regulatory T cells potentiates muscle repair,” Cell, vol. 155, no. 6, pp. 1282–1295, 2013. View at Publisher · View at Google Scholar
  69. A. E. H. Emery, “The muscular dystrophies,” The Lancet, vol. 359, no. 9307, pp. 687–695, 2002. View at Publisher · View at Google Scholar · View at Scopus
  70. S. Decary, C. B. Hamida, V. Mouly, J. P. Barbet, F. Hentati, and G. S. Butler-Browne, “Shorter telomeres in dystrophic muscle consistent with extensive regeneration in young children,” Neuromuscular Disorders, vol. 10, no. 2, pp. 113–120, 2000. View at Publisher · View at Google Scholar · View at Scopus
  71. M. Vezzoli, P. Castellani, G. Corna et al., “High-mobility group box 1 release and redox regulation accompany regeneration and remodeling of skeletal muscle,” Antioxidants and Redox Signaling, vol. 15, no. 8, pp. 2161–2174, 2011. View at Publisher · View at Google Scholar · View at Scopus
  72. 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
  73. S. Hodgetts, H. Radley, M. Davies, and M. D. Grounds, “Reduced necrosis of dystrophic muscle by depletion of host neutrophils, or blocking TNFα function with Etanercept in mdx mice,” Neuromuscular Disorders, vol. 16, no. 9-10, pp. 591–602, 2006. View at Publisher · View at Google Scholar · View at Scopus
  74. M. D. Grounds and J. Torrisi, “Anti-TNFα (Remicade) therapy protects dystrophic skeletal muscle from necrosis,” FASEB Journal, vol. 18, no. 6, pp. 676–682, 2004. View at Publisher · View at Google Scholar · View at Scopus
  75. S. A. Villalta, B. Deng, C. Rinaldi, M. Wehling-Henricks, and J. G. Tidball, “IFN-γ promotes muscle damage in the mdx mouse model of duchenne muscular dystrophy by suppressing M2 macrophage activation and inhibiting muscle cell proliferation,” Journal of Immunology, vol. 187, no. 10, pp. 5419–5428, 2011. View at Publisher · View at Google Scholar · View at Scopus
  76. K. Ohlendieck and K. P. Campbell, “Dystrophin-associated proteins are greatly reduced in skeletal muscle from mdx mice,” Journal of Cell Biology, vol. 115, no. 6, pp. 1685–1694, 1991. View at Google Scholar · View at Scopus
  77. B. Weller, G. Karpati, and S. Carpenter, “Dystrophin-deficient mdx muscle fibers are preferentially vulnerable to necrosis induced by experimental lengthening contractions,” Journal of the Neurological Sciences, vol. 100, no. 1-2, pp. 9–13, 1990. View at Publisher · View at Google Scholar · View at Scopus
  78. J. E. Brenman, D. S. Chao, H. Xia, K. Aldape, and D. S. Bredt, “Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy,” Cell, vol. 82, no. 5, pp. 743–752, 1995. View at Google Scholar · View at Scopus
  79. W.-J. Chang, S. T. Iannaccone, K. S. Lau et al., “Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 17, pp. 9142–9147, 1996. View at Publisher · View at Google Scholar · View at Scopus
  80. R. H. Crosbie, R. Barresi, and K. P. Campbell, “Loss of sarcolemma nNOS in sarcoglycan-deficient muscle,” FASEB Journal, vol. 16, no. 13, pp. 1786–1791, 2002. View at Publisher · View at Google Scholar · View at Scopus
  81. Y. Sunada, H. Ohi, A. Hase et al., “Transgenic mice expressing mutant caveolin-3 show severe myopathy associated with incrased nNOS activity,” Human Molecular Genetics, vol. 10, no. 3, pp. 173–178, 2001. View at Google Scholar · View at Scopus
  82. 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
  83. M. Wehling-Henricks and J. G. Tidball, “Neuronal nitric oxide synthase-rescue of dystrophin/utrophin double knockout mice does not require nNOS localization to the cell membrane,” PLoS ONE, vol. 6, no. 10, Article ID e25071, 2011. View at Publisher · View at Google Scholar · View at Scopus
  84. 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, Article ID ddq523, pp. 790–805, 2011. View at Publisher · View at Google Scholar · View at Scopus
  85. P. Zordan, C. Sciorati, L. Campana et al., “The nitric oxide-donor molsidomine modulates the innate inflammatory response in a mouse model of muscular dystrophy,” European Journal of Pharmacology, vol. 715, no. 1–3, pp. 296–303, 2013. View at Publisher · View at Google Scholar
  86. P. Rovere-Querini, E. Clementi, and S. Brunelli, “Nitric oxide and muscle repair: multiple actions converging on therapeutic efficacy,” European Journal of Pharmacology, 2013. View at Publisher · View at Google Scholar
  87. M. C. Dalakas and K. Sivakumar, “The immunopathologic and inflammatory differences between dermatomyositis, polymyositis and sporadic inclusion body myositis,” Current Opinion in Neurology, vol. 9, no. 3, pp. 235–239, 1996. View at Google Scholar · View at Scopus
  88. A. Ghirardello, S. Zampieri, E. Tarricone, L. Iaccarino, L. Gorza, and A. Doria, “Cutting edge issues in polymyositis,” Clinical Reviews in Allergy and Immunology, vol. 41, no. 2, pp. 179–189, 2011. View at Publisher · View at Google Scholar · View at Scopus
  89. P. Venalis and I. E. Lundberg, “Immune mechanisms in polymyositis and dermatomyositis and potential targets for therapy,” Rheumatology, vol. 53, no. 3, pp. 397–405, 2014. View at Publisher · View at Google Scholar
  90. R. Hohlfeld, A. G. Engel, N. Goebels, and L. Behrens, “Cellular immune mechanisms in inflammatory myopathies,” Current Opinion in Rheumatology, vol. 9, no. 6, pp. 520–526, 1997. View at Google Scholar · View at Scopus
  91. K. M. Rostasy, J. Schmidt, E. Bahn et al., “Distinct inflammatory properties of late-activated macrophages in inflammatory myopathies,” Acta Myologica, vol. 27, pp. 49–53, 2008. View at Google Scholar · View at Scopus
  92. J. Reimann, S. Schnell, S. Schwartz, K. Kappes-Horn, R. Dodel, and M. Bacher, “Macrophage migration inhibitory factor in normal human skeletal muscle and inflammatory myopathies,” Journal of Neuropathology and Experimental Neurology, vol. 69, no. 6, pp. 654–662, 2010. View at Publisher · View at Google Scholar · View at Scopus
  93. S. Khan and L. Christopher-Stine, “Polymyositis, dermatomyositis, and autoimmune necrotizing myopathy: clinical features,” Rheumatic Disease Clinics of North America, vol. 37, no. 2, pp. 143–158, 2011. View at Publisher · View at Google Scholar · View at Scopus
  94. C. Preuße, H. H. Goebel, J. Held et al., “Immune-mediated necrotizing myopathy is characterized by a specific Th1-M1 polarized immune profile,” The American Journal of Pathology, vol. 181, no. 6, pp. 2161–2171, 2012. View at Publisher · View at Google Scholar