Animal models in idiopathic inflammatory myopathies: How to overcome a translational roadblock?

Autoimmunity Reviews

Volumn 16, Issue 5, 2017, Pages 478-494

  Afzali, Ali Maisam ^a   Ruck, Tobias ^b   Wiendl, Heinz ^b   Meuth, Sven G ^b  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Animal models; Antigens; Infections; Inflammatory myopathies; Myositis; Transgenic model

Indexed keywords

ANIMAL MODEL; HUMAN; IMMUNOPATHOLOGY; INFECTION; MOUSE MODEL; MYOSITIS; NONHUMAN; NUTRITIONAL DISORDER; REVIEW; TRANSGENIC ANIMAL; TRANSLATIONAL RESEARCH; ANIMAL; DISEASE MODEL; PATHOLOGY;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; MYOSITIS;

EID: 85015337737     PISSN: 15689972     EISSN: 18730183     Source Type: Journal    
DOI: 10.1016/j.autrev.2017.03.001     Document Type: Review

References (172)

1. [1] Dalakas, M.C., Inflammatory muscle diseases: a critical review on pathogenesis and therapies. Curr Opin Pharmacol 10 (2010), 346–352.
2. [2] Dalakas, M.C., Review: an update on inflammatory and autoimmune myopathies. Neuropathol Appl Neurobiol 37 (2011), 226–242.
3. [3] Dorph, C., Lundberg, I.E., Idiopathic inflammatory myopathies – myositis. Best Pract Res Clin Rheumatol 16 (2002), 817–832.
4. [4] Targoff, I.N., Miller, F.W., Medsger, T.A. Jr, Oddis, C.V., Classification criteria for the idiopathic inflammatory myopathies. Curr Opin Rheumatol 9 (1997), 527–535.
5. [5] Espitia-Thibault, A., Masseau, A., Néel, A., Espitia, O., Toquet, C., Mussini, J.-M., et al. Sjögren's syndrome-associated myositis with germinal centre-like structures. Autoimmun Rev 16 (2017), 154–158.
6. [6] Vincze, M., Danko, K., Idiopathic inflammatory myopathies. Best Pract Res Clin Rheumatol 26 (2012), 25–45.
7. [7] Mammen, A., Dermatomyositis and polymyositis. Ann N Y Acad Sci 1184 (2009), 134–153.
8. [8] Dimachkie, M.M., Idiopathic inflammatory myopathies. J Neuroimmunol 231 (2011), 32–42.
9. [9] Ernste, F.C., Reed, A.M., Idiopathic inflammatory myopathies: current trends in pathogenesis, clinical features, and up-to-date treatment recommendations. Mayo Clin Proc 88 (2013), 83–105.
10. [10] Dalakas, M.C., Hohlfeld, R., Polymyositis and dermatomyositis. Lancet 362 (2003), 971–982.
11. [11] Needham, M., Mastaglia, F.L., Inclusion body myositis: current pathogenetic concepts and diagnostic and therapeutic approaches. Lancet Neurol 6 (2007), 620–631.
12. [12] De-Paula, V.J., Radanovic, M., Diniz, B.S., Forlenza, O.V., Alzheimer's disease. Subcell Biochem 65 (2012), 329–352.
13. [13] Selkoe, D.J., Hardy, J., The amyloid hypothesis of Alzheimer's disease at 25 years. EMBO Mol Med 8 (2016), 595–608.
14. [14] Bohan, A., Peter, J.B., Polymyositis and dermatomyositis. N Engl J Med 292 (1975), 344–347.
15. [15] Catalán, M., Selva-O'Callaghan, A., Grau, J.M., Diagnosis and classification of sporadic inclusion body myositis (sIBM). Autoimmun Rev 13 (2014), 363–366.
16. [16] Iaccarino, L., Ghirardello, A., Bettio, S., Zen, M., Gatto, M., Punzi, L., et al. The clinical features, diagnosis and classification of dermatomyositis. J Autoimmun 48–49 (2014), 122–127.
17. [17] Milisenda, J.C., Selva-O'Callaghan, A., Grau, J.M., The diagnosis and classification of polymyositis. J Autoimmun 48–49 (2014), 118–121.
18. [18] Sultan, S.M., Isenberg, D.A., Re-classifying myositis. Rheumatology 49 (2009), 831–833.
19. [19] Airio, A., Kautiainen, H., Hakala, M., Prognosis and mortality of polymyositis and dermatomyositis patients. Clin Rheumatol 25 (2006), 234–239.
20. [20] Miller, F.W., New approaches to the assessment and treatment of the idiopathic inflammatory myopathies. Ann Rheum Dis 71:Suppl. 2 (2012), i82–i85.
21. [21] Cavagnaro, J., Silva Lima, B., Regulatory acceptance of animal models of disease to support clinical trials of medicines and advanced therapy medicinal products. Eur J Pharmacol 759 (2015), 51–62.
22. [22] McGonigle, P., Ruggeri, B., Animal models of human disease: challenges in enabling translation. Biochem Pharmacol 87 (2014), 162–171.
23. [23] Ascherman, D.P., Animal models of inflammatory myopathy. Curr Rheumatol Rep 14 (2012), 257–263.
24. [24] Katsumata, Y., Ascherman, D.P., Animal models in myositis. Curr Opin Rheumatol 20 (2008), 681–685.
25. [25] Wagner, E., Fall einer seltenen Muskelkrankheit. Arch Heilkd, 4, 1863, 282.
26. [26] Unverricht, H., Über eine eigenthümliche form von akuter Muskelentzündung mit einem der Trichinose ähnelnden Krankheitsbilde. Münch Med Wochenschr 34 (1887), 488–492.
27. [27] Hargis, A.M., Haupt, K.H., Prieur, D.J., Moore, M.P., Animal model of human disease. Dermatomyositis. Familial canine dermatomyositis. Am J Pathol 120 (1985), 323–325.
28. [28] Hargis, A.M., Prieur, D.J., Animal models of polymyositis/ dermatomyositis. Clin Dermatol 6 (1988), 120–129.
29. [29] Wu, X., Li, Z.f., Brooks, R., Komives, E.A., Torpey, J.W., Engvall, E., et al. Autoantibodies in canine masticatory muscle myositis recognize a novel myosin binding protein-C family member. The Journal of Immunology 179 (2007), 4939–4944.
30. [30] Dalakas, M.C., From canine to man: on antibodies, macrophages, and dendritic cells in inflammatory myopathies. Muscle Nerve 29 (2004), 753–755.
31. [31] Pumarola, M., Moore, P.F., Shelton, G.D., Canine inflammatory myopathy: analysis of cellular infiltrates. Muscle Nerve 29 (2004), 782–789.
32. [32] Shelton, G.D., Hoffman, E.P., Ghimbovschi, S., Peters, I.R., Day, M.J., Mullins, M., et al. Immunopathogenic pathways in canine inflammatory myopathies resemble human myositis. Vet Immunol Immunopathol 113 (2006), 200–214.
33. [33] Sparks, D.L., Scheff, S.W., Hunsaker, J.C. 3rd, Liu, H., Landers, T., Gross, D.R., Induction of Alzheimer-like beta-amyloid immunoreactivity in the brains of rabbits with dietary cholesterol. Exp Neurol 126 (1994), 88–94.
34. [34] Chen, X., Ghribi, O., Geiger, J.D., Rabbits fed cholesterol-enriched diets exhibit pathological features of inclusion body myositis. Am J Physiol Regul Integr Comp Physiol 294 (2008), R829–R835.
35. [35] Liu, Q.Y., Koukiekolo, R., Zhang, D.L., Smith, B., Ly, D., Lei, J.X., et al. Molecular events linking cholesterol to Alzheimer's disease and inclusion body myositis in a rabbit model. Am J Neurodegener Dis 5 (2016), 74–84.
36. [36] Ghribi, O., Larsen, B., Schrag, M., Herman, M.M., High cholesterol content in neurons increases BACE, beta-amyloid, and phosphorylated tau levels in rabbit hippocampus. Exp Neurol 200 (2006), 460–467.
37. [37] Wood, W.G., Li, L., Müller, W.E., Eckert, G.P., Cholesterol as a causative factor in Alzheimer's disease: a debatable hypothesis. J Neurochem 129 (2014), 559–572.
38. [38] Alvarado-Cardenas, M., Marin-Sánchez, A., Martínez, M.A., Martínez-Martínez, L., Pinal-Fernandez, I., Labrador-Horrillo, M., et al. Statin-associated autoimmune myopathy: a distinct new IFL pattern can increase the rate of HMGCR antibody detection by clinical laboratories. Autoimmun Rev 15 (2016), 1161–1166.
39. [39] Mammen, A.L., Chung, T., Christopher-Stine, L., Rosen, P., Rosen, A., Doering, K.R., et al. Autoantibodies against 3-hydroxy-3-methylglutaryl-coenzyme a reductase in patients with statin-associated autoimmune myopathy. Arthritis Rheum 63 (2011), 713–721.
40. [40] Mohassel, P., Mammen, A.L., Statin-associated autoimmune myopathy and anti-HMGCR autoantibodies. Muscle Nerve 48 (2013), 477–483.
41. [41] Musset, L., Allenbach, Y., Benveniste, O., Boyer, O., Bossuyt, X., Bentow, C., et al. Anti-HMGCR antibodies as a biomarker for immune-mediated necrotizing myopathies: a history of statins and experience from a large international multi-center study. Autoimmun Rev 15 (2016), 983–993.
42. [42] Shovman, O., Gilburd, B., Chayat, C., Lazar, A.D., Amital, H., Blank, M., et al. Anti-HMGCR antibodies demonstrate high diagnostic value in the diagnosis of immune-mediated necrotizing myopathy following statin exposure. Immunol Res, 2016, 1–6.
43. [43] Palterer, B., Cammelli, D., Vitiello, G., Giudizi, M.G., Anti-HMGCR and anti-DFS70 antibodies immunofluorescence patterns. Autoimmun Rev 16 (2017), 321–322.
44. [44] Strongwater, S.L., Dorovini-Zis, K., Ball, R.D., Schnitzer, T.J., A murine model of polymyositis induced by coxsackievirus B1 (Tucson strain). Arthritis Rheum 27 (1984), 433–442.
45. [45] Ray, C.G., Minnich, L.L., Johnson, P.C., Selective polymyositis induced by coxsackievirus Bi in mice. J Infect Dis 140 (1979), 239–243.
46. [46] Jongen, P.J., Heessen, F.W., Bergmann, I., de Waal, R.M., ter Laak, H.J., Galama, J.M., et al. Coxsackie B1 virus-induced murine myositis: a correlative study of muscular lesions and serological changes. J Autoimmun 7 (1994), 727–737.
47. [47] Zoll, J., Jongen, P., Galama, J., Kuppeveld, F.v., Melchers, W., Coxsackievirus B1-induced murine myositis: no evidence for viral persistence. J Gen Virol, 74, 1993.
48. [48] Tam, P.E., Schmidt, A.M., Ytterberg, S.R., Messner, R.P., Duration of virus persistence and its relationship to inflammation in the chronic phase of coxsackievirus B1-induced murine polymyositis. J Lab Clin Med 123 (1994), 346–356.
49. [49] Tam, P.E., Schmidt, A.M., Ytterberg, S.R., Messner, R.P., Viral persistence during the developmental phase of coxsackievirus B1-induced murine polymyositis. J Virol 65 (1991), 6654–6660.
50. [50] Ytterberg, S.R., Coxsackievirus B 1 induced murine polymyositis: acute infection with active virus is required for myositis. J Rheumatol 14 (1987), 12–18.
51. [51] Ytterberg, S.R., Mahowald, M.L., Messner, R.P., T cells are required for coxsackievirus B1 induced murine polymyositis. J Rheumatol 15 (1988), 475–478.
52. [52] Tam, P.E., Weber-Sanders, M.L., Messner, R.P., Multiple viral determinants mediate myopathogenicity in coxsackievirus B1-induced chronic inflammatory myopathy. J Virol 77 (2003), 11849–11854.
53. [53] Tam, P.E., Messner, R.P., Genetic determinants of susceptibility to coxsackievirus B1-induced chronic inflammatory myopathy: effects of host background and major histocompatibility complex genes. J Lab Clin Med 128 (1996), 279–289.
54. [54] Morrison, T.E., Oko, L., Montgomery, S.A., Whitmore, A.C., Lotstein, A.R., Gunn, B.M., et al. A mouse model of chikungunya virus-induced musculoskeletal inflammatory disease: evidence of arthritis, tenosynovitis, myositis, and persistence. Am J Pathol 178 (2011), 32–40.
55. [55] Morrison, T.E., Whitmore, A.C., Shabman, R.S., Lidbury, B.A., Mahalingam, S., Heise, M.T., Characterization of Ross River virus tropism and virus-induced inflammation in a mouse model of viral arthritis and myositis. J Virol 80 (2006), 737–749.
56. [56] Hawman, D.W., Stoermer, K.A., Montgomery, S.A., Pal, P., Oko, L., Diamond, M.S., et al. Chronic joint disease caused by persistent chikungunya virus infection is controlled by the adaptive immune response. J Virol 87 (2013), 13878–13888.
57. [57] Morrison, T.E., Fraser, R.J., Smith, P.N., Mahalingam, S., Heise, M.T., Complement contributes to inflammatory tissue destruction in a mouse model of Ross River virus-induced disease. J Virol 81 (2007), 5132–5143.
58. [58] Morrison, T.E., Simmons, J.D., Heise, M.T., Complement receptor 3 promotes severe ross river virus-induced disease. J Virol 82 (2008), 11263–11272.
59. [59] Gunn, B.M., Morrison, T.E., Whitmore, A.C., Blevins, L.K., Hueston, L., Fraser, R.J., et al. Mannose binding lectin is required for alphavirus-induced arthritis/myositis. PLoS Pathog, 8, 2012, e1002586.
60. [60] Rulli, N.E., Guglielmotti, A., Mangano, G., Rolph, M.S., Apicella, C., Zaid, A., et al. Amelioration of alphavirus-induced arthritis and myositis in a mouse model by treatment with bindarit, an inhibitor of monocyte chemotactic proteins. Arthritis Rheum 60 (2009), 2513–2523.
61. [61] Herrero, L.J., Nelson, M., Srikiatkhachorn, A., Gu, R., Anantapreecha, S., Fingerle-Rowson, G., et al. Critical role for macrophage migration inhibitory factor (MIF) in Ross River virus-induced arthritis and myositis. Proc Natl Acad Sci U S A 108 (2011), 12048–12053.
62. [62] Herrero, L.J., Sheng, K.C., Jian, P., Taylor, A., Her, Z., Herring, B.L., et al. Macrophage migration inhibitory factor receptor CD74 mediates alphavirus-induced arthritis and myositis in murine models of alphavirus infection. Arthritis Rheum 65 (2013), 2724–2736.
63. [63] Sun, J., Tarleton, R.L., Predominance of CD8 + T lymphocytes in the inflammatory lesions of mice with acute Trypanosoma cruzi infection. Am J Trop Med Hyg 48 (1993), 161–169.
64. [64] Andersson, J., Englund, P., Sunnemark, D., Dahlstedt, A., Westerblad, H., Nennesmo, I., et al. CBA/J mice infected with Trypanosoma cruzi: an experimental model for inflammatory myopathies. Muscle Nerve 27 (2003), 442–448.
65. [65] Solana, M.E., Ferrer, M.F., Novoa, M.M., Song, W.C., Gomez, R.M., Decay-accelerating factor 1 deficiency exacerbates Trypanosoma cruzi-induced murine chronic myositis. Muscle Nerve 46 (2012), 582–587.
66. [66] Paciello, O., Oliva, G., Gradoni, L., Manna, L., Foglia Manzillo, V., Wojcik, S., et al. Canine inflammatory myopathy associated with Leishmania infantum infection. Neuromuscul Disord 19 (2009), 124–130.
67. [67] Vamvakidis, C.D., Koutinas, A.F., Kanakoudis, G., Georgiadis, G., Saridomichelakis, M., Masticatory and skeletal muscle myositis in canine leishmaniasis (Leishmania infantum). Vet Rec 146 (2000), 698–703.
68. [68] Paciello, O., Wojcik, S., Gradoni, L., Oliva, G., Trapani, F., Iovane, V., et al. Syrian hamster infected with Leishmania infantum: a new experimental model for inflammatory myopathies. Muscle Nerve 41 (2010), 355–361.
69. [69] Billiau, A., Matthys, P., Modes of action of Freund's adjuvants in experimental models of autoimmune diseases. J Leukoc Biol 70 (2001), 849–860.
70. [70] Hofstetter, H.H., Shive, C.L., Forsthuber, T.G., Pertussis toxin modulates the immune response to neuroantigens injected in incomplete Freund's adjuvant: induction of Th1 cells and experimental autoimmune encephalomyelitis in the presence of high frequencies of Th2 cells. J Immunol 169 (2002), 117–125.
71. [71] Hart, M.N., Linthicum, D.S., Waldschmidt, M.M., Tassell, S.K., Schelper, R.L., Robinson, R.A., Experimental autoimmune inflammatory myopathy. J Neuropathol Exp Neurol 46 (1987), 511–521.
72. [72] Pearson, C.M., Development of arthritis, periarthritis and periostitis in rats given adjuvants. Exp Biol Med 91 (1956), 95–101.
73. [73] Dawkins, R.L., Experimental myositis associated with hypersensitivity to muscle. J Pathol Bacteriol 90 (1965), 619–625.
74. [74] Takayanagi, T., Immunohistological studies of experimental myositis in relation to human polymyositis with special reference to passive transfer and fluorescent antibody technique. Psychiatry Clin Neurosci 21 (1967), 117–127.
75. [75] Morgan, G., Peter, J.B., Newbould, B.B., Experimental allergic myositis in rats. Arthritis Rheum 14 (1971), 599–609.
76. [76] Matsubara, S., Takamori, M., Experimental allergic myositis: strain 13 guinea pig immunised with rabbit myosin B fraction. Acta Neuropathol 74 (1987), 158–162.
77. [77] Matsubara, S., Takamori, M., Experimental allergic myositis: ultrastructural, histochemical, immunological and immunohistochemical studies. Acta Neuropathol 74 (1987), 151–157.
78. [78] Matsubara, S., Kitaguchi, T., Kawata, A., Miyamoto, K., Yagi, H., Hirai, S., Experimental allergic myositis in SJL/J mouse. Reappraisal of immune reaction based on changes after single immunization. J Neuroimmunol 119 (2001), 223–230.
79. [79] Allenbach, Y., Solly, S., Gregoire, S., Dubourg, O., Salomon, B., Butler-Browne, G., et al. Role of regulatory T cells in a new mouse model of experimental autoimmune myositis. Am J Pathol 174 (2009), 989–998.
80. [80] Ito, T., Kumamoto, T., Horinouchi, H., Yukishige, K., Sugihara, R., Fujimoto, S., et al. Adhesion molecule expression in experimental myositis. Muscle Nerve 25 (2002), 409–418.
81. [81] Matsubara, S., Okumura, S., Experimental autoimmune myositis in SJL/J mice produced by immunization with syngeneic myosin B fraction. Transfer by both immunoglobulin G and T cells. J Neurol Sci 144 (1996), 171–175.
82. [82] Matsubara, S., Shima, T., Takamori, M., Experimental allergic myositis in SJL/J mice immunized with rabbit myosin B fraction: immunohistochemical analysis and transfer. Acta Neuropathol 85 (1993), 138–144.
83. [83] Nemoto, H., Nemoto, K., Sugimoto, H., Kinoshita, M., FK506 suppressed the inflammatory change of EAM in SJL/J mice. J Neurol Sci 193 (2001), 7–11.
84. [84] Rosenberg, N.L., Ringel, S.P., Kotzin, B.L., Experimental autoimmune myositis in SJL/J mice. Clin Exp Immunol 68 (1987), 117–129.
85. [85] Wen-Jing, L., Chuan-Qiang, P., Hong-Hua, L., Xiang-Hui, L., Jie-Xiao, L., A new modified animal model of myosin-induced experimental autoimmune myositis enhanced by defibrase. Arch Med Sci 11 (2015), 1272–1278.
86. [86] Rosenberg, N.L., Kotzin, B.L., Aberrant expression of class II MHC antigens by skeletal muscle endothelial cells in experimental autoimmune myositis. J Immunol 142 (1989), 4289–4294.
87. [87] Kojima, T., Tanuma, N., Aikawa, Y., Shin, T., Sasaki, A., Matsumoto, Y., Myosin-induced autoimmune polymyositis in the rat. J Neurol Sci 151 (1997), 141–148.
88. [88] Suzuki, F., Nanki, T., Imai, T., Kikuchi, H., Hirohata, S., Kohsaka, H., et al. Inhibition of CX3CL1 (fractalkine) improves experimental autoimmune myositis in SJL/J mice. J Immunol 175 (2005), 6987–6996.
89. [89] Suzuki, F., Kubota, T., Miyazaki, Y., Ishikawa, K., Ebisawa, M., Hirohata, S., et al. Serum level of soluble CX3CL1/fractalkine is elevated in patients with polymyositis and dermatomyositis, which is correlated with disease activity. Arthritis Res Ther, 14, 2012, R48.
90. [90] Scuderi, F., Mannella, F., Marino, M., Provenzano, C., Bartoccioni, E., IL-6-deficient mice show impaired inflammatory response in a model of myosin-induced experimental myositis. J Neuroimmunol 176 (2006), 9–15.
91. [91] Narazaki, M., Hagihara, K., Shima, Y., Ogata, A., Kishimoto, T., Tanaka, T., Therapeutic effect of tocilizumab on two patients with polymyositis. Rheumatology 50 (2011), 1344–1346.
92. [92] Kang, J., Zhang, H.Y., Feng, G.D., Feng, D.Y., Jia, H.G., Development of an improved animal model of experimental autoimmune myositis. Int J Clin Exp Pathol 8 (2015), 14457–14464.
93. [93] Dalakas, M.C., Immunotherapy of myositis: issues, concerns and future prospects. Nat Rev Rheumatol 6 (2010), 129–137.
94. [94] Schneider, C., Matsumoto, Y., Kohyama, K., Toyka, K.V., Hartung, H.P., Gold, R., Experimental autoimmune myositis in the Lewis rat: lack of spontaneous T-cell apoptosis and therapeutic response to glucocorticosteroid application. J Neuroimmunol 107 (2000), 83–87.
95. [95] Wada, J., Shintani, N., Kikutani, K., Nakae, T., Yamauchi, T., Takechi, K., Intravenous immunoglobulin prevents experimental autoimmune myositis in SJL mice by reducing anti-myosin antibody and by blocking complement deposition. Clin Exp Immunol 124 (2001), 282–289.
96. [96] Civatte, M., Bartoli, C., Schleinitz, N., Chetaille, B., Pellissier, J.F., Figarella-Branger, D., Expression of the beta chemokines CCL3, CCL4, CCL5 and their receptors in idiopathic inflammatory myopathies. Neuropathol Appl Neurobiol 31 (2005), 70–79.
97. [97] De Bleecker, J.L., De Paepe, B., Vanwalleghem, I.E., Schroder, J.M., Differential expression of chemokines in inflammatory myopathies. Neurology 58 (2002), 1779–1785.
98. [98] Liprandi, A., Bartoli, C., Figarella-Branger, D., Pellissier, J.F., Lepidi, H., Local expression of monocyte chemoattractant protein-1 (MCP-1) in idiopathic inflammatory myopathies. Acta Neuropathol 97 (1999), 642–648.
99. [99] Ohyanagi, N., Ishido, M., Suzuki, F., Kaneko, K., Kubota, T., Miyasaka, N., et al. Retinoid ameliorates experimental autoimmune myositis, with modulation of Th cell differentiation and antibody production in vivo. Arthritis Rheum 60 (2009), 3118–3127.
100. [100] Prevel, N., Allenbach, Y., Klatzmann, D., Salomon, B., Benveniste, O., Beneficial role of rapamycin in experimental autoimmune myositis. PLoS One, 8, 2013, e74450.
101. [101] Sugihara, T., Sekine, C., Nakae, T., Kohyama, K., Harigai, M., Iwakura, Y., et al. A new murine model to define the critical pathologic and therapeutic mediators of polymyositis. Arthritis Rheum 56 (2007), 1304–1314.
102. [102] Weller, A.H., Magliato, S.A., Bell, K.P., Rosenberg, N.L., Spontaneous myopathy in the SJL/J mouse: pathology and strength loss. Muscle Nerve 20 (1997), 72–82.
103. [103] Kohyama, K., Matsumoto, Y., C-protein in the skeletal muscle induces severe autoimmune polymyositis in Lewis rats. J Neuroimmunol 98 (1999), 130–135.
104. [104] Matsumoto, Y., Kohyama, K., Park, I.K., Nakajima, M., Hiraki, K., Characterization of pathogenic T cells and autoantibodies in C-protein-induced autoimmune polymyositis. J Neuroimmunol 190 (2007), 90–100.
105. [105] Sugihara, T., Okiyama, N., Suzuki, M., Kohyama, K., Matsumoto, Y., Miyasaka, N., et al. Definitive engagement of cytotoxic CD8 T cells in C protein-induced myositis, a murine model of polymyositis. Arthritis Rheum 62 (2010), 3088–3092.
106. [106] Nagaraju, K., Raben, N., Villalba, M.L., Danning, C., Loeffler, L.A., Lee, E., et al. Costimulatory markers in muscle of patients with idiopathic inflammatory myopathies and in cultured muscle cells. Clin Immunol 92 (1999), 161–169.
107. [107] Sugiura, T., Kawaguchi, Y., Harigai, M., Takagi, K., Ohta, S., Fukasawa, C., et al. Increased CD40 expression on muscle cells of polymyositis and dermatomyositis: role of CD40-CD40 ligand interaction in IL-6, IL-8, IL-15, and monocyte chemoattractant protein-1 production. The Journal of Immunology 164 (2000), 6593–6600.
108. [108] Tews, D.S., Goebel, H.H., Expression of cell adhesion molecules in inflammatory myopathies. J Neuroimmunol 59 (1995), 185–194.
109. [109] Wiendl, H., Hohlfeld, R., Kieseier, B.C., Immunobiology of muscle: advances in understanding an immunological microenvironment. Trends Immunol 26 (2005), 373–380.
110. [110] Sugihara, T., Okiyama, N., Watanabe, N., Miyasaka, N., Kohsaka, H., Interleukin-1 and tumor necrosis factor alpha blockade treatment of experimental polymyositis in mice. Arthritis Rheum 64 (2012), 2655–2662.
111. [111] Yoshihashi-Nakazato, Y., Kawahata, K., Kimura, N., Miyasaka, N., Kohsaka, H., Interferon-gamma, but not interleukin-4, suppresses experimental polymyositis. Arthritis Rheumatol 68 (2016), 1505–1510.
112. [112] Okiyama, N., Sugihara, T., Iwakura, Y., Yokozeki, H., Miyasaka, N., Kohsaka, H., Therapeutic effects of interleukin-6 blockade in a murine model of polymyositis that does not require interleukin-17A. Arthritis Rheum 60 (2009), 2505–2512.
113. [113] Kim, J., Choi, J.Y., Park, S.H., Yang, S.H., Park, J.A., Shin, K., et al. Therapeutic effect of anti-C-X-C motif chemokine 10 (CXCL10) antibody on C protein-induced myositis mouse. Arthritis Res Ther, 16, 2014, R126.
114. [114] Katsumata, Y., Ridgway, W.M., Oriss, T., Gu, X., Chin, D., Wu, Y., et al. Species-specific immune responses generated by histidyl-tRNA synthetase immunization are associated with muscle and lung inflammation. J Autoimmun 29 (2007), 174–186.
115. [115] Oishi, K., Hamaguchi, Y., Matsushita, T., Hasegawa, M., Okiyama, N., Dernedde, J., et al. A crucial role of L-selectin in C protein-induced experimental polymyositis in mice. Arthritis Rheumatol 66 (2014), 1864–1871.
116. [116] Okiyama, N., Sugihara, T., Oida, T., Ohata, J., Yokozeki, H., Miyasaka, N., et al. T lymphocytes and muscle condition act like seeds and soil in a murine polymyositis model. Arthritis Rheum 64 (2012), 3741–3749.
117. [117] Lundberg, I.E., Vencovsky, J., Alexanderson, H., Therapy of myositis. Curr Opin Rheumatol 26 (2014), 704–711.
118. [118] Sprott, H., Glatzel, M., Michel, B.A., Treatment of myositis with etanercept (Enbrel®), a recombinant human soluble fusion protein of TNF-α type II receptor and IgG1. Rheumatology 43 (2004), 524–526.
119. [119] Kawachi, I., Tanaka, K., Tanaka, M., Tsuji, S., Dendritic cells presenting pyruvate kinase M1/M2 isozyme peptide can induce experimental allergic myositis in BALB/c mice. J Neuroimmunol 117 (2001), 108–115.
120. [120] Okiyama, N., Hasegawa, H., Oida, T., Hirata, S., Yokozeki, H., Fujimoto, M., et al. Experimental myositis inducible with transfer of dendritic cells presenting a skeletal muscle C protein-derived CD8 epitope peptide. Int Immunol, 2015.
121. [121] Nakano, J., Yoshimura, T., Okita, M., Motomura, M., Kamei, S., Matsuo, H., et al. Laminin-induced autoimmune myositis in rats. J Neuropathol Exp Neurol 64 (2005), 790–796.
122. [122] Stone, K.B., Oddis, C.V., Fertig, N., Katsumata, Y., Lucas, M., Vogt, M., et al. Anti-Jo-1 antibody levels correlate with disease activity in idiopathic inflammatory myopathy. Arthritis Rheum 56 (2007), 3125–3131.
123. [123] Blechynden, L.M., Lawson, M.A., Tabarias, H., Garlepp, M.J., Sherman, J., Raben, N., et al. Myositis induced by naked DNA immunization with the gene for histidyl-tRNA synthetase. Hum Gene Ther 8 (1997), 1469–1480.
124. [124] Soejima, M., Kang, E.H., Gu, X., Katsumata, Y., Clemens, P.R., Ascherman, D.P., Role of innate immunity in a murine model of histidyl-transfer RNA synthetase (Jo-1)-mediated myositis. Arthritis Rheum 63 (2011), 479–487.
125. [125] Howard, O.M.Z., Dong, H.F., Yang, D., Raben, N., Nagaraju, K., Rosen, A., et al. Histidyl–tRNA synthetase and asparaginyl–tRNA synthetase, autoantigens in myositis, activate chemokine receptors on T lymphocytes and immature dendritic cells. J Exp Med 196 (2002), 781–791.
126. [126] Harlow, L., Fernandez, I., Soejima, M., Ridgway, W.M., Ascherman, D.P., Characterization of TLR4-mediated auto-antibody production in a mouse model of histidyl-tRNA synthetase-induced myositis. Innate Immun 18 (2012), 876–885.
127. [127] Fernandez, I., Harlow, L., Zang, Y., Liu-Bryan, R., Ridgway, W.M., Clemens, P.R., et al. Functional redundancy of MyD88-dependent signaling pathways in a murine model of histidyl-transfer RNA synthetase-induced myositis. J Immunol 191 (2013), 1865–1872.
128. [128] Fukuchi, K., Pham, D., Hart, M., Li, L., Lindsey, J.R., Amyloid-beta deposition in skeletal muscle of transgenic mice: possible model of inclusion body myopathy. Am J Pathol 153 (1998), 1687–1693.
129. [129] Jin, L.W., Hearn, M.G., Ogburn, C.E., Dang, N., Nochlin, D., Ladiges, W.C., et al. Transgenic mice over-expressing the C-99 fragment of betaPP with an alpha-secretase site mutation develop a myopathy similar to human inclusion body myositis. Am J Pathol 153 (1998), 1679–1686.
130. [130] Sugarman, M.C., Yamasaki, T.R., Oddo, S., Echegoyen, J.C., Murphy, M.P., Golde, T.E., et al. Inclusion body myositis-like phenotype induced by transgenic overexpression of beta APP in skeletal muscle. Proc Natl Acad Sci U S A 99 (2002), 6334–6339.
131. [131] Sugarman, M.C., Kitazawa, M., Baker, M., Caiozzo, V.J., Querfurth, H.W., LaFerla, F.M., Pathogenic accumulation of APP in fast twitch muscle of IBM patients and a transgenic model. Neurobiol Aging 27 (2006), 423–432.
132. [132] Kitazawa, M., Green, K.N., Caccamo, A., LaFerla, F.M., Genetically augmenting Aβ42 levels in skeletal muscle exacerbates inclusion body myositis-like pathology and motor deficits in transgenic mice. Am J Pathol 168 (2006), 1986–1997.
133. [133] Moussa, C.E., Fu, Q., Kumar, P., Shtifman, A., Lopez, J.R., Allen, P.D., et al. Transgenic expression of beta-APP in fast-twitch skeletal muscle leads to calcium dyshomeostasis and IBM-like pathology. FASEB J 20 (2006), 2165–2167.
134. 2 + dysregulation in skeletal muscle. Muscle Nerve 42 (2010), 731–738.
135. 2 + release and contractility in skeletal muscle. Neurobiol Aging 31 (2010), 2080–2090.
136. [136] Boncompagni, S., Moussa, C.E., Levy, E., Pezone, M.J., Lopez, J.R., Protasi, F., et al. Mitochondrial dysfunction in skeletal muscle of amyloid precursor protein-overexpressing mice. J Biol Chem 287 (2012), 20534–20544.
137. [137] Zissimopoulos, S., Lai, F.A., Redox regulation of the ryanodine receptor/calcium release channel. Biochem Soc Trans 34 (2006), 919–921.
138. [138] Luo, Y.B., Johnsen, R.D., Griffiths, L., Needham, M., Fabian, V.A., Fletcher, S., et al. Primary over-expression of AbetaPP in muscle does not lead to the development of inclusion body myositis in a new lineage of the MCK-AbetaPP transgenic mouse. Int J Exp Pathol 94 (2013), 418–425.
139. [139] Seleznik, G., Seeger, H., Bauer, J., Fu, K., Czerkowicz, J., Papandile, A., et al. The lymphotoxin β receptor is a potential therapeutic target in renal inflammation. Kidney Int 89 (2016), 113–126.
140. [140] Bauer, J., Wolf, M., Blank, T., Bremer, J., Reimann, R., Maire, R., et al. A novel mouse model of chronic myositis triggers protein aggregation reminiscent of inclusion body myositis (IBM). Abstracts of 1st Int. Conference of Myositis Stockholm Sweden, 15, 2015, 98.
141. [141] Rebolledo, D.L., Minniti, A.N., Grez, P.M., Fadic, R., Kohn, R., Inestrosa, N.C., Inclusion body myositis: a view from the Caenorhabditis elegans muscle. Mol Neurobiol 38 (2008), 178–198.
142. [142] Link, C.D., Expression of human beta-amyloid peptide in transgenic Caenorhabditis elegans. Proc Natl Acad Sci U S A 92 (1995), 9368–9372.
143. [143] Drake, J., Oxidative stress precedes fibrillar deposition of Alzheimer's disease amyloid β-peptide (1–42) in a transgenic Caenorhabditis elegans model. Neurobiology of aging 24 (2003), 415–420.
144. [144] Fonte, V., Kapulkin, W.J., Taft, A., Fluet, A., Friedman, D., Link, C.D., Interaction of intracellular beta amyloid peptide with chaperone proteins. Proc Natl Acad Sci U S A 99 (2002), 9439–9444.
145. [145] Link, C.D., Cypser, J.R., Johnson, C.J., Johnson, T.E., Direct observation of stress response in Caenorhabditis elegans using a reporter transgene. Cell Stress Chaperones 4 (1999), 235–242.
146. [146] Minniti, A.N., Rebolledo, D.L., Grez, P.M., Fadic, R., Aldunate, R., Volitakis, I., et al. Intracellular amyloid formation in muscle cells of Abeta-transgenic Caenorhabditis elegans: determinants and physiological role in copper detoxification. Mol Neurodegener, 4, 2009, 2.
147. [147] Aldunate, R., Minniti, A.N., Rebolledo, D., Inestrosa, N.C., Synaptic defects associated with s-inclusion body myositis are prevented by copper. Biometals 25 (2012), 815–824.
148. [148] Rebolledo, D.L., Aldunate, R., Kohn, R., Neira, I., Minniti, A.N., Inestrosa, N.C., Copper reduces Abeta oligomeric species and ameliorates neuromuscular synaptic defects in a C. elegans model of inclusion body myositis. J Neurosci 31 (2011), 10149–10158.
149. [149] Diomede, L., Rigacci, S., Romeo, M., Stefani, M., Salmona, M., Oleuropein aglycone protects transgenic C. elegans strains expressing Abeta42 by reducing plaque load and motor deficit. PLoS One, 8, 2013, e58893.
150. [150] Emslie-Smith, A.M., Arahata, K., Engel, A.G., Major histocompatibility complex class I antigen expression, immunolocalization of interferon subtypes, and T cell-mediated cytotoxicity in myopathies. Hum Pathol 20 (1989), 224–231.
151. [151] Englund, P., Nennesmo, I., Klareskog, L., Lundberg, I.E., Interleukin-1alpha expression in capillaries and major histocompatibility complex class I expression in type II muscle fibers from polymyositis and dermatomyositis patients: important pathogenic features independent of inflammatory cell clusters in muscle tissue. Arthritis Rheum 46 (2002), 1044–1055.
152. [152] Karpati, G., Pouliot, Y., Carpenter, S., Expression of immunoreactive major histocompatibility complex products in human skeletal muscles. Ann Neurol 23 (1988), 64–72.
153. [153] Nagaraju, K., Casciola-Rosen, L., Lundberg, I., Rawat, R., Cutting, S., Thapliyal, R., et al. Activation of the endoplasmic reticulum stress response in autoimmune myositis: potential role in muscle fiber damage and dysfunction. Arthritis Rheum 52 (2005), 1824–1835.
154. [154] Nagaraju, K., Raben, N., Loeffler, L., Parker, T., Rochon, P.J., Lee, E., et al. Conditional up-regulation of MHC class I in skeletal muscle leads to self-sustaining autoimmune myositis and myositis-specific autoantibodies. Proc Natl Acad Sci U S A 97 (2000), 9209–9214.
155. [155] Li, C.K.-c., Knopp, P., Moncrieffe, H., Singh, B., Shah, S., Nagaraju, K., et al. Overexpression of MHC class I heavy chain protein in young skeletal muscle leads to severe myositis: implications for juvenile myositis. Am J Pathol 175 (2009), 1030–1040.
156. [156] Rayavarapu, S., Coley, W., Van der Meulen, J.H., Cakir, E., Tappeta, K., Kinder, T.B., et al. Activation of the ubiquitin proteasome pathway in a mouse model of inflammatory myopathy: a potential therapeutic target. Arthritis Rheum 65 (2013), 3248–3258.
157. [157] Coley, W., Rayavarapu, S., Pandey, G.S., Sabina, R.L., Van der Meulen, J.H., Ampong, B., et al. The molecular basis of skeletal muscle weakness in a mouse model of inflammatory myopathy. Arthritis Rheum 64 (2012), 3750–3759.
158. [158] Coley, W., Rayavarapu, S., van der Meulen, J.H., Duba, A.S., Nagaraju, K., Daily supplementation of D-ribose shows no therapeutic benefits in the MHC-I transgenic mouse model of inflammatory myositis. PLoS One, 8, 2013, e65970.
159. [159] Freret, M., Drouot, L., Obry, A., Ahmed-Lacheheb, S., Dauly, C., Adriouch, S., et al. Overexpression of MHC class I in muscle of lymphocyte-deficient mice causes a severe myopathy with induction of the unfolded protein response. Am J Pathol 183 (2013), 893–904.
160. [160] Figarella-Branger, D., Civatte, M., Bartoli, C., Pellissier, J.-F., Cytokines, chemokines, and cell adhesion molecules in inflammatory myopathies. Muscle Nerve 28 (2003), 659–682.
161. [161] Chakrabarti, S., Kobayashi, K.S., Flavell, R.A., Marks, C.B., Miyake, K., Liston, D.R., et al. Impaired membrane resealing and autoimmune myositis in synaptotagmin VII-deficient mice. J Cell Biol 162 (2003), 543–549.
162. 2 +-regulated exocytic vesicles in fibroblasts and epithelial cells. J Cell Biol 137 (1997), 93–104.
163. [163] Young, N.A., Sharma, R., Friedman, A.K., Kaffenberger, B.H., Bolon, B., Jarjour, W.N., Aberrant muscle antigen exposure in mice is sufficient to cause myositis in a Treg cell-deficient milieu. Arthritis Rheum 65 (2013), 3259–3270.
164. [164] Ghirardello, A., Borella, E., Beggio, M., Franceschini, F., Fredi, M., Doria, A., Myositis autoantibodies and clinical phenotypes. Auto Immun Highlights 5 (2014), 69–75.
165. [165] Gunawardena, H., The clinical features of myositis-associated autoantibodies: a review. Clin Rev Allergy Immunol 52 (2017), 45–57.
166. [166] Satoh, M., Tanaka, S., Ceribelli, A., Calise, S.J., Chan, E.K.L., A comprehensive overview on myositis-specific antibodies: new and old biomarkers in idiopathic inflammatory myopathy. Clin Rev Allergy Immunol 52 (2017), 1–19.
167. [167] Simon, J.-P., Marie, I., Jouen, F., Boyer, O., Martinet, J., Autoimmune myopathies: where do We stand?. Front Immunol, 7, 2016.
168. [168] Labrador-Horrillo, M., Martínez, M.A., Selva-O'Callaghan, A., Trallero-Araguás, E., Grau-Junyent, J.M., Vilardell-Tarrés, M., et al. Identification of a novel myositis-associated antibody directed against cortactin. Autoimmun Rev 13 (2014), 1008–1012.
169. [169] Cherin, P., Belizna, C., Cartry, O., Lascu-Dubos, G., de Jaeger, C., Delain, J.-C., et al. Long-term subcutaneous immunoglobulin use in inflammatory myopathies: a retrospective review of 19 cases. Autoimmun Rev 15 (2016), 281–286.
170. [170] Rongvaux, A., Willinger, T., Martinek, J., Strowig, T., Gearty, S.V., Teichmann, L.L., et al. Development and function of human innate immune cells in a humanized mouse model. Nat Biotechnol 32 (2014), 364–372.
171. [171] Shultz, L.D., Ishikawa, F., Greiner, D.L., Humanized mice in translational biomedical research. Nat Rev Immunol 7 (2007), 118–130.
172. [172] Shultz, L.D., Brehm, M.A., Garcia-Martinez, J.V., Greiner, D.L., Humanized mice for immune system investigation: progress, promise and challenges. Nat Rev Immunol 12 (2012), 786–798.