Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014, Article ID 438675, 12 pages
http://dx.doi.org/10.1155/2014/438675
Review Article

From Innate to Adaptive Immune Response in Muscular Dystrophies and Skeletal Muscle Regeneration: The Role of Lymphocytes

1IRCCS Fondazione Santa Lucia, Via del Fosso di Fiorano 64, 00143 Rome, Italy
2DAHFMO, Unit of Histology and Medical Embryology, Sapienza University of Rome, Via Antonio Scarpa 14, 00161 Rome, Italy

Received 15 February 2014; Accepted 2 May 2014; Published 16 June 2014

Academic Editor: Pura Muñoz-Cánoves

Copyright © 2014 Luca Madaro and Marina Bouché. 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. M. Saclier, S. Cuvellier, M. Magnan, R. Mounier, and B. Chazaud, “Monocyte/macrophage interactions with myogenic precursor cells during skeletal muscle regeneration,” FEBS Journal, vol. 280, no. 17, pp. 4118–4130, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. 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
  3. P. Seale, J. Ishibashi, A. Scimè, and M. A. Rudnicki, “Pax7 is necessary and sufficient for the myogenic specification of CD45+:Sca1+ stem cells from injured muscle,” PLoS Biology, vol. 2, no. 5, p. E130, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. D. Palacios, C. Mozzetta, S. Consalvi et al., “TNF/p38α/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration,” Cell Stem Cell, vol. 7, no. 4, pp. 455–469, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. A. L. Serrano, B. Baeza-Raja, E. Perdiguero, M. Jardí, and P. Muñoz-Cánoves, “Interleukin-6 is an essential regulator of satellite cell-mediated skeletal muscle hypertrophy,” Cell Metabolism, vol. 7, no. 1, pp. 33–44, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Kuang, M. A. Gillespie, and M. A. Rudnicki, “Niche regulation of muscle satellite cell self-renewal and differentiation,” Cell Stem Cell, vol. 2, no. 1, pp. 22–31, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. 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
  8. C. Alexakis, T. Partridge, and G. Bou-Gharios, “Implication of the satellite cell in dystrophic muscle fibrosis: a self-perpetuating mechanism of collagen overproduction,” The American Journal of Physiology—Cell Physiology, vol. 293, no. 2, pp. C661–C669, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. 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
  10. K. A. Lapidos, R. Kakkar, and E. M. McNally, “The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma,” Circulation Research, vol. 94, no. 8, pp. 1023–1031, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Sacco, F. Mourkioti, R. Tran et al., “Short telomeres and stem cell exhaustion model duchenne muscular dystrophy in mdx/mTR mice,” Cell, vol. 143, no. 7, pp. 1059–1071, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. J. R. Bach and D. Martinez, “Duchenne muscular dystrophy: continuous noninvasive ventilatory support prolongs survival,” Respiratory Care, vol. 56, no. 6, pp. 744–750, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Crisp, H. Yin, A. Goyenvalle et al., “Diaphragm rescue alone prevents heart dysfunction in dystrophic mice in vitro,” Human Molecular Genetics, vol. 20, no. 3, pp. 413–421, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Mosqueira, S. M. Baby, S. Lahiri, and T. S. Khurana, “Ventilatory chemosensory drive is blunted in the mdx mouse model of Duchenne Muscular Dystrophy (DMD),” PLoS ONE, vol. 8, no. 7, Article ID e69567, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. F. Mourkioti, J. Kustan, P. Kraft et al., “Role of telomere dysfunction in cardiac failure in Duchenne muscular dystrophy,” Nature Cell Biology, vol. 15, no. 8, pp. 895–904, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. N. P. Evans, S. A. Misyak, J. L. Robertson, J. Bassaganya-Riera, and R. W. Grange, “Dysregulated intracellular signaling and inflammatory gene expression during initial disease onset in duchenne muscular dystrophy,” The American Journal of Physical Medicine and Rehabilitation, vol. 88, no. 6, pp. 502–522, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. 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 · View at Scopus
  18. 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
  19. 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
  20. C. Zhang, Y. Li, Y. Wu, L. Wang, X. Wang, and J. Du, “Interleukin-6/signal transducer and activator of transcription 3 (STAT3) pathway is essential for macrophage infiltration and myoblast proliferation during muscle regeneration,” Journal of Biological Chemistry, vol. 288, no. 3, pp. 1489–1499, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Kharraz, J. Guerra, C. J. Mann, A. L. Serrano, and P. Muñoz-Cánoves, “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 · View at Scopus
  22. 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
  23. 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
  24. 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, no. 2, pp. 403–413, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. 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
  26. H. X. Nguyen and J. G. Tidball, “Null mutation of gp91phox reduces muscle membrane lysis during muscle inflammation in mice,” Journal of Physiology, vol. 553, no. 3, pp. 833–841, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. J. M. Daley, A. A. Thomay, M. D. Connolly, J. S. Reichner, and J. E. Albina, “Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice,” Journal of Leukocyte Biology, vol. 83, no. 1, pp. 64–70, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. T. J. Fleming, M. L. Fleming, and T. R. Malek, “Selective expression of Ly-6G on myeloid lineage cells in mouse bone marrow: RB6-8C5 mAb to granulocyte-differentiation antigen (Gr-1) detects members of the Ly-6 family,” Journal of Immunology, vol. 151, no. 5, pp. 2399–2408, 1993. View at Google Scholar · View at Scopus
  29. N. J. Pillon, P. J. Bilan, L. N. Fink, and A. Klip, “Cross-talk between skeletal muscle and immune cells: muscle-derived mediators and metabolic implications,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 304, no. 5, pp. E453–E465, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. C. H. Côté, P. Bouchard, N. van Rooijen, D. Marsolais, and E. Duchesne, “Monocyte depletion increases local proliferation of macrophage subsets after skeletal muscle injury,” BMC Musculoskeletal Disorders, vol. 14, article 359, 2013. View at Publisher · View at Google Scholar
  31. 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
  32. T. A. Wynn, A. Chawla, and J. W. Pollard, “Macrophage biology in development, homeostasis and disease,” Nature, vol. 496, no. 7446, pp. 445–455, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Gordon and P. R. Taylor, “Monocyte and macrophage heterogeneity,” Nature Reviews Immunology, vol. 5, no. 12, pp. 953–964, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. 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
  35. 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
  36. B. Vidal, E. Ardite, M. Suelves et al., “Amelioration of Duchenne muscular dystrophy in mdx mice by elimination of matrix-associated fibrin-driven inflammation coupled to the αmβ2 leukocyte integrin receptor,” Human Molecular Genetics, vol. 21, no. 9, pp. 1989–2004, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. 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
  38. 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
  39. 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
  40. J. R. M. Gorospe, B. K. Nishikawa, and E. P. Hoffman, “Recruitment of mast cells to muscle after mild damage,” Journal of the Neurological Sciences, vol. 135, no. 1, pp. 10–17, 1996. View at Publisher · View at Google Scholar · View at Scopus
  41. J. P. Abonia, D. S. Friend, W. G. Austen Jr. et al., “Mast cell protease 5 mediates ischemia-reperfusion injury of mouse skeletal muscle,” Journal of Immunology, vol. 174, no. 11, pp. 7285–7291, 2005. View at Google Scholar · View at Scopus
  42. H. G. Radley and M. D. Grounds, “Cromolyn administration (to block mast cell degranulation) reduces necrosis of dystrophic muscle in mdx mice,” Neurobiology of Disease, vol. 23, no. 2, pp. 387–397, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. B. A. Binstadt, P. R. Patel, H. Alencar et al., “Particularities of the vasculature can promote the organ specificity of autoimmune attack,” Nature Immunology, vol. 7, no. 3, pp. 284–292, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Yokota, K. Suzuki, K. Tokoyoda et al., “Roles of mast cells in the pathogenesis of inflammatory myopathy,” Arthritis Research & Therapy, vol. 16, no. 2, p. R72, 2014. View at Publisher · View at Google Scholar
  45. M. M. Dimachkie, “Idiopathic inflammatory myopathies,” Journal of Neuroimmunology, vol. 231, no. 1-2, pp. 32–42, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. L. Casciola-Rosen, K. Nagaraju, P. Plotz et al., “Enhanced autoantigen expression in regenerating muscle cells in idiopathic inflammatory myopathy,” Journal of Experimental Medicine, vol. 201, no. 4, pp. 591–601, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. D. S. Silberstein and J. R. David, “Tumor necrosis factor enhances eosinophil toxicity to Schistosoma mansoni larvae,” Proceedings of the National Academy of Sciences of the United States of America, vol. 83, no. 4, pp. 1055–1059, 1986. View at Google Scholar · View at Scopus
  48. N. Ben Baruch-Morgenstern, D. Shik, I. Moshkovits et al., “Paired immunoglobulin-like receptor A is an intrinsic, self-limiting suppressor of IL-5-induced eosinophil development,” Nature Immunology, vol. 15, no. 1, pp. 36–44, 2014. View at Google Scholar
  49. Y. Yamaguchi, Y. Hayashi, Y. Sugama et al., “Highly purified murine interleukin 5 (IL-5) stimulates eosinophil function and prolongs in vitro survival. IL-5 as an eosinophil chemotactic factor,” Journal of Experimental Medicine, vol. 167, no. 5, pp. 1737–1742, 1988. View at Google Scholar · View at Scopus
  50. M. Wehling-henricks, S. Sokolow, J. J. Lee, K. H. Myung, S. A. Villalta, and J. G. Tidball, “Major basic protein-1 promotes fibrosis of dystrophic muscle and attenuates the cellular immune response in muscular dystrophy,” Human Molecular Genetics, vol. 17, no. 15, pp. 2280–2292, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. B. Cai, M. J. Spencer, G. Nakamura, L. Tseng-Ong, and J. G. Tidball, “Eosinophilia of dystrophin-deficient muscle is promoted by perforin-mediated cytotoxicity by T cell effectors,” The American Journal of Pathology, vol. 156, no. 5, pp. 1789–1796, 2000. View at Google Scholar · View at Scopus
  52. M. Wehling-Henricks, J. J. Lee, and J. G. Tidball, “Prednisolone decreases cellular adhesion molecules required for inflammatory cell infiltration in dystrophin-deficient skeletal muscle,” Neuromuscular Disorders, vol. 14, no. 8-9, pp. 483–490, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. V. Horsley, K. M. Jansen, S. T. Mills, and G. K. Pavlath, “IL-4 acts as a myoblast recruitment factor during mammalian muscle growth,” Cell, vol. 113, no. 4, pp. 483–494, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Uezumi, S.-I. 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
  55. 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
  56. C. Mozzetta, S. Consalvi, V. Saccone et al., “Fibroadipogenic progenitors mediate the ability of HDAC inhibitors to promote regeneration in dystrophic muscles of young, but not old Mdx mice,” EMBO Molecular Medicine, vol. 5, no. 4, pp. 626–639, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. N. Cordani, V. Pisa, L. Pozzi, C. Sciorati, and E. Clementi, “Nitric oxide controls fat deposition in dystrophic skeletal muscle by regulating fibro-adipogenic precursor differentiation,” Stem Cells, vol. 32, no. 4, pp. 874–885, 2014. View at Publisher · View at Google Scholar
  58. J.-H. Choi, Y.-E. Park, S.-I. Kim et al., “Differential Immunohistological features of inflammatory myopathies and dysferlinopathy,” Journal of Korean Medical Science, vol. 24, no. 6, pp. 1015–1023, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Marino, F. Scuderi, P. Mazzarelli, F. Mannella, C. Provenzano, and E. Bartoccioni, “Constitutive and cytokine-induced expression of MHC and intercellular adhesion molecule-1 (ICAM-1) on human myoblasts,” Journal of Neuroimmunology, vol. 116, no. 1, pp. 94–101, 2001. View at Publisher · View at Google Scholar · View at Scopus
  60. J. Schmidt, G. Rakocevic, R. Raju, and M. C. Dalakas, “Upregulated inducible co-stimulator (ICOS) and ICOS-ligand in inclusion body myositis muscle: significance for CD8+ T cell cytotoxicity,” Brain, vol. 127, no. 5, pp. 1182–1190, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. A. Lerario, F. Cogiamanian, C. Marchesi et al., “Effects of rituximab in two patients with dysferlin-deficient muscular dystrophy,” BMC Musculoskeletal Disorders, vol. 11, article 157, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Salajegheh, J. L. Pinkus, A. A. Amato et al., “Permissive environment for B-cell maturation in myositis muscle in the absence of B-cell follicles,” Muscle and Nerve, vol. 42, no. 4, pp. 576–583, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. M. J. Spencer, E. Montecino-Rodriguez, K. Dorshkind, and J. G. Tidball, “Helper (CD4+) and cytotoxic (CD8+) T cells promote the pathology of dystrophin-deficient muscle,” Clinical Immunology, vol. 98, no. 2, pp. 235–243, 2001. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Eghtesad, S. Jhunjhunwala, S. R. Little, and P. R. Clemens, “Rapamycin ameliorates dystrophic phenotype in mdx mouse skeletal muscle,” Molecular Medicine, vol. 17, no. 9-10, pp. 917–924, 2011. View at Google Scholar · View at Scopus
  65. C. D. Tsoukas, B. Landgraf, J. Bentin et al., “Activation of resting T lymphocytes by anti-CD3 (T3) antibodies in the absence of monocytes,” Journal of Immunology, vol. 135, no. 3, pp. 1719–1723, 1985. View at Google Scholar · View at Scopus
  66. N. Al-Shanti, P. Durcan, S. Al-Dabbagh, G. A. Dimchev, and C. E. Stewart, “Activated lymphocytes secretome inhibits differentiation and induces proliferation of C2C12 myoblasts,” Cellular Physiology and Biochemistry, vol. 33, no. 1, pp. 117–128, 2014. View at Publisher · View at Google Scholar
  67. J. T. Kissel, D. J. Lynn, K. W. Rammohan et al., “Mononuclear cell analysis of muscle biopsies in prednisone- and azathioprine-treated Duchenne muscular dystrophy,” Neurology, vol. 43, no. 3, pp. 532–536, 1993. View at Google Scholar · View at Scopus
  68. J. R. Mendell, R. T. Moxley, R. C. Griggs et al., “Randomized, double-blind six-month trial of prednisone in Duchenne's muscular dystrophy,” The New England Journal of Medicine, vol. 320, no. 24, pp. 1592–1597, 1989. View at Google Scholar · View at Scopus
  69. E. Gussoni, G. K. Pavlath, R. G. Miller et al., “Specific T cell receptor gene rearrangements at the site of muscle degeneration in Duchenne muscular dystrophy,” Journal of Immunology, vol. 153, no. 10, pp. 4798–4805, 1994. View at Google Scholar · View at Scopus
  70. R. Mantegazza, F. Andreetta, P. Bernasconi et al., “Analysis of T cell receptor repertoire of muscle-infiltrating T lymphocytes in polymyositis. Restricted Vα/β rearrangements may indicate antigen-driven selection,” Journal of Clinical Investigation, vol. 91, no. 6, pp. 2880–2886, 1993. View at Google Scholar · View at Scopus
  71. S. Gordon, “Alternative activation of macrophages,” Nature Reviews Immunology, vol. 3, no. 1, pp. 23–35, 2003. View at Publisher · View at Google Scholar
  72. 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
  73. P. Wang and S. G. Zheng, “Regulatory T cells and B cells: implication on autoimmune diseases,” International Journal of Clinical and Experimental Pathology, vol. 6, no. 12, pp. 2668–2674, 2013. View at Google Scholar
  74. A. Farini, M. Meregalli, M. Belicchi et al., “T and B lymphocyte depletion has a marked effect on the fibrosis of dystrophic skeletal muscles in the scid/mdx mouse,” Journal of Pathology, vol. 213, no. 2, pp. 229–238, 2007. View at Publisher · View at Google Scholar · View at Scopus
  75. J. Morrison, D. B. Palmer, S. Cobbold, T. Partridge, and G. Bou-Gharios, “Effects of T-lymphocyte depletion on muscle fibrosis in the mdx mouse,” The American Journal of Pathology, vol. 166, no. 6, pp. 1701–1710, 2005. View at Google Scholar · View at Scopus
  76. D. Vallese, E. Negroni, S. Duguez et al., “The Rag2-Il2rb-Dmd- mouse: a novel dystrophic and immunodeficient model to assess innovating therapeutic strategies for muscular dystrophies,” Molecular Therapy, vol. 21, no. 10, pp. 1950–1957, 2013. View at Publisher · View at Google Scholar
  77. 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-β,” Journal of Clinical Investigation, vol. 119, no. 6, pp. 1583–1594, 2009. View at Publisher · View at Google Scholar · View at Scopus
  78. L. Madaro, A. Pelle, C. Nicoletti et al., “PKC theta ablation improves healing in a mouse model of muscular dystrophy,” PLoS ONE, vol. 7, no. 2, Article ID e31515, 2012. View at Publisher · View at Google Scholar · View at Scopus
  79. Z. Gao, Z. Wang, X. Zhang et al., “Inactivation of PKCθ leads to increased susceptibility to obesity and dietary insulin resistance in mice,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 292, no. 1, pp. E84–E91, 2007. View at Publisher · View at Google Scholar · View at Scopus
  80. L. Madaro, V. Marrocco, P. Fiore et al., “PKCθ signaling is required for myoblast fusion by regulating the expression of caveolin-3 and β1D integrin upstream focal adhesion kinase,” Molecular Biology of the Cell, vol. 22, no. 8, pp. 1409–1419, 2011. View at Publisher · View at Google Scholar · View at Scopus
  81. G. Messina, S. Biressi, S. Monteverde et al., “Nfix regulates fetal-specific transcription in developing skeletal muscle,” Cell, vol. 140, no. 4, pp. 554–566, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. M. D'Andrea, A. Pisaniello, C. Serra et al., “Protein kinase C theta co-operates with calcineurin in the activation of slow muscle genes in cultured myogenic cells,” Journal of Cellular Physiology, vol. 207, no. 2, pp. 379–388, 2006. View at Publisher · View at Google Scholar · View at Scopus
  83. L. Madaro, V. Marrocco, S. Carnio, M. Sandri, and M. Bouché, “Intracellular signaling in ER stress-induced autophagy in skeletal muscle cells,” The FASEB Journal, vol. 27, no. 5, pp. 1990–2000, 2013. View at Publisher · View at Google Scholar · View at Scopus
  84. J. O. Valenzuela, C. Iclozan, M. S. Hossain et al., “PKCθ is required for alloreactivity and GVHD but not for immune responses toward leukemia and infection in mice,” Journal of Clinical Investigation, vol. 119, no. 12, pp. 3774–3786, 2009. View at Publisher · View at Google Scholar · View at Scopus
  85. T. Gruber, N. Hermann-Kleiter, C. Pfeifhofer-Obermair et al., “PKCθ cooperates with PKCα in alloimmune responses of T cells in vivo,” Molecular Immunology, vol. 46, no. 10, pp. 2071–2079, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. B. J. Marsland, T. J. Soos, G. Späth, D. R. Littman, and M. Kopf, “Protein kinase C θ is critical for the development of in vivo T helper (Th)2 cell but not Th-1 cell responses,” Journal of Experimental Medicine, vol. 200, no. 2, pp. 181–189, 2004. View at Publisher · View at Google Scholar · View at Scopus
  87. A. M. Healy, E. Izmailova, M. Fitzgerald et al., “PKC-θ-deficient mice are protected from th1-dependent antigen-induced arthritis,” Journal of Immunology, vol. 177, no. 3, pp. 1886–1893, 2006. View at Google Scholar · View at Scopus
  88. S.-L. Tan, J. Zhao, C. Bi et al., “Resistance to experimental autoimmune encephalomyelitis and impaired IL-17 production in protein kinase Cθ-deficient mice,” Journal of Immunology, vol. 176, no. 5, pp. 2872–2879, 2006. View at Google Scholar · View at Scopus
  89. K. Nagahama, A. Ogawa, K. Shirane, Y. Shimomura, K. Sugimoto, and A. Mizoguchi, “Protein kinase C theta plays a fundamental role in different types of chronic colitis,” Gastroenterology, vol. 134, no. 2, pp. 459–469, 2008. View at Publisher · View at Google Scholar · View at Scopus
  90. A. Zanin-Zhorov, Y. Ding, S. Kumari et al., “Protein kinase C-θ mediates negative feedback on regulatory T cell function,” Science, vol. 328, no. 5976, pp. 372–376, 2010. View at Publisher · View at Google Scholar · View at Scopus
  91. J. Ma, Y. Ding, X. Fang, R. Wang, and Z. Sun, “Protein kinase C-θ inhibits inducible regulatory T cell differentiation via an AKT-Foxo1/3a-dependent pathway,” Journal of Immunology, vol. 188, no. 11, pp. 5337–5347, 2012. View at Publisher · View at Google Scholar · View at Scopus
  92. A. Farini, C. Sitzia, C. Navarro et al., “Absence of T and B lymphocytes modulates dystrophic features in dysferlin deficient animal model,” Experimental Cell Research, vol. 318, no. 10, pp. 1160–1174, 2012. View at Publisher · View at Google Scholar · View at Scopus
  93. R. Han and K. P. Campbell, “Dysferlin and muscle membrane repair,” Current Opinion in Cell Biology, vol. 19, no. 4, pp. 409–416, 2007. View at Publisher · View at Google Scholar · View at Scopus
  94. H. Liao, E. Franck, M. Fréret et al., “Myoinjury transiently activates muscle antigen-specific CD8+ T cells in lymph nodes in a mouse model,” Arthritis and Rheumatism, vol. 64, no. 10, pp. 3441–3451, 2012. View at Publisher · View at Google Scholar · View at Scopus
  95. N. A. Young, R. Sharma, A. K. Friedman, B. H. Kaffenberger, B. Bolon, and W. N. Jarjour, “Aberrant muscle antigen exposure in mice is sufficient to cause myositis in a Treg cell-deficient milieu,” Arthritis & Rheumatism, vol. 65, no. 12, pp. 3259–3270, 2013. View at Publisher · View at Google Scholar
  96. S. Chakrabarti, K. S. Kobayashi, R. A. Flavell et al., “Impaired membrane resealing and autoimmune myositis in synaptotagmin VII-deficient mice,” Journal of Cell Biology, vol. 162, no. 4, pp. 543–549, 2003. View at Publisher · View at Google Scholar · View at Scopus
  97. S. Z. Josefowicz, “Regulators of chromatin state and transcription in CD4 T-cell polarization,” Immunology, vol. 139, no. 3, pp. 299–308, 2013. View at Publisher · View at Google Scholar · View at Scopus
  98. J. P. Golding, E. Calderbank, T. A. Partridge, and J. R. Beauchamp, “Skeletal muscle stem cells express anti-apoptotic ErbB receptors during activation from quiescence,” Experimental Cell Research, vol. 313, no. 2, pp. 341–356, 2007. View at Publisher · View at Google Scholar · View at Scopus
  99. E. R. Andrechek, W. R. Hardy, A. A. Girgis-Gabardo et al., “ErbB2 is required for muscle spindle and myoblast cell survival,” Molecular and Cellular Biology, vol. 22, no. 13, pp. 4714–4722, 2002. View at Publisher · View at Google Scholar · View at Scopus
  100. H. Wiendl, R. Hohlfeld, and B. C. Kieseier, “Immunobiology of muscle: advances in understanding an immunological microenvironment,” Trends in Immunology, vol. 26, no. 7, pp. 373–380, 2005. View at Publisher · View at Google Scholar · View at Scopus
  101. M. Srinivasan and K. A. Frauwirth, “Peripheral tolerance in CD8+ T cells,” Cytokine, vol. 46, no. 2, pp. 147–159, 2009. View at Publisher · View at Google Scholar · View at Scopus
  102. M. J. Spencer, C. M. Walsh, K. A. Dorshkind, E. M. Rodriguez, and J. G. Tidball, “Myonuclear apoptosis in dystrophic mdx muscle occurs by perforin-mediated cytotoxicity,” Journal of Clinical Investigation, vol. 99, no. 11, pp. 2745–2751, 1997. View at Google Scholar · View at Scopus