Role of non-immune mechanisms of muscle damage in idiopathic inflammatory myopathies

Arthritis Research and Therapy

Volumn 14, Issue 2, 2012, Pages

  Coley, William ^a   Rayavarapu, Sree ^a   Nagaraju, Kanneboyina ^a  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; ADENOSINE TRIPHOSPHATE; AMYLOID BETA PROTEIN; BETA SECRETASE 1; CALCIUM ION; CALRETICULIN; CASPASE 4; GAMMA INTERFERON; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HIGH MOBILITY GROUP B1 PROTEIN; HISTIDINE TRANSFER RNA LIGASE; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7;

APOPTOSIS; CALCIUM TRANSPORT; CELLULAR STRESS RESPONSE; CYTOKINE RELEASE; DISEASE ASSOCIATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; FEEDBACK SYSTEM; HUMAN; HYPOXIA; IMMUNOSTIMULATION; INFLAMMATION; LYMPHOCYTIC INFILTRATION; METABOLIC REGULATION; MUSCLE ATROPHY; MUSCLE CONTRACTION; MUSCLE METABOLISM; MYOSITIS; NONHUMAN; PATHOGENESIS; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; UPREGULATION; ANIMAL; IMMUNOLOGY; PATHOLOGY;

ANIMALS; ENDOPLASMIC RETICULUM STRESS; HUMANS; MUSCLE, SKELETAL; MYOSITIS;

EID: 84860351862     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3791     Document Type: Review

References (75)

1. Mastaglia FL, Garlepp MJ, Phillips BA, Zilko PJ. Inflammatory myopathies: clinical, diagnostic and therapeutic aspects. Muscle Nerve 2003, 27:407-425. 10.1002/mus.10313, 12661042.
2. Tanimoto K, Nakano K, Kano S, Mori S, Ueki H, Nishitani H, Sato T, Kiuchi T, Ohashi Y. Classification criteria for polymyositis and dermatomyositis. J Rheumatol 1995, 22:668-674.
3. Miller F, Rider L, Plotz P, Oddis C, Isenberg D. Diagnostic criteria for polymyositis and dermatomyositis. Lancet 2003, 362:1762-1763. 10.1016/S0140-6736(03)14862-3, 14643132.
4. Santmyire-Rosenberger B, Dugan EM. Skin involvement in dermatomyositis. Curr Opin Rheumatol 2003, 15:714-722. 10.1097/00002281-200311000-00006, 14569200.
5. Ramanan AV, Feldman BM. Clinical features and outcomes of juvenile dermatomyositis and other childhood onset myositis syndromes. Rheum Dis Clin North Am 2002, 28:833-857. 10.1016/S0889-857X(02)00024-8, 12506775.
6. Mastaglia FL, Zilko PJ. Inflammatory myopathies: how to treat the difficult cases. J Clin Neurosci 2003, 10:99-101. 10.1016/S0967-5868(02)00271-0, 12464534.
7. Dalakas MC. Immunotherapy of myositis: issues, concerns and future prospects. Nat Rev Rheumatol 2010, 6:129-137. 10.1038/nrrheum.2010.2, 20125096.
8. Miller FW, Rider LG, Chung YL, Cooper R, Danko K, Farewell V, Lundberg I, Morrison C, Oakley L, Oakley I, Pilkington C, Vencovsky J, Vincent K, Scott DL, Isenberg DA. International Myositis Outcome Assessment Collaborative Study Group: Proposed preliminary core set measures for disease outcome assessment in adult and juvenile idiopathic inflammatory myopathies. Rheumatology (Oxford) 2001, 40:1262-1273.
9. Nagaraju K. Update on immunopathogenesis in inflammatory myopathies. Curr Opin Rheumatol 2001, 13:461-468. 10.1097/00002281-200111000-00002, 11698721.
10. Bunch TW. Prednisone and azathioprine for polymyositis: long-term followup. Arthritis Rheum 1981, 24:45-48. 10.1002/art.1780240107, 7008799.
11. Kissel JT, Halterman RK, Rammohan KW, Mendell JR. The relationship of complement-mediated microvasculopathy to the histologic features and clinical duration of disease in dermatomyositis. Arch Neurol 1991, 48:26-30. 10.1001/archneur.1991.00530130034016, 1986724.
12. Imai T, Hirayama K, Osumi E. [Muscle histopathology and responsiveness to steroid therapy in polymyositis and dermatomyositis]. Rinsho Shinkeigaku 1995, 35:243-246.
13. Lundberg I, Kratz AK, Alexanderson H, Patarroyo M. Decreased expression of interleukin-1alpha, interleukin-1beta, and cell adhesion molecules in muscle tissue following corticosteroid treatment in patients with polymyositis and dermatomyositis. Arthritis Rheum 2000, 43:336-348. 10.1002/1529-0131(200002)43:2<336::AID-ANR13>3.0.CO;2-V, 10693873.
14. Seong SY, Matzinger P. Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat Rev Immunol 2004, 4:469-478. 10.1038/nri1372, 15173835.
15. Takeda K, Kaisho T, Akira S. Toll-like receptors. Annu Rev Immunol 2003, 21:335-376. 10.1146/annurev.immunol.21.120601.141126, 12524386.
16. Barton GM, Medzhitov R. Toll-like receptor signaling pathways. Science 2003, 300:1524-1525. 10.1126/science.1085536, 12791976.
17. Grundtman C, Bruton J, Yamada T, Ostberg T, Pisetsky DS, Harris HE, Andersson U, Lundberg IE, Westerblad H. Effects of HMGB1 on in vitro responses of isolated muscle fibers and functional aspects in skeletal muscles of idiopathic inflammatory myopathies. FASEB J 2010, 24:570-578. 10.1096/fj.09-144782, 19837864.
18. Howard OM, Dong HF, Yang D, Raben N, Nagaraju K, Rosen A, Casciola-Rosen L, Härtlein M, Kron M, Yang D, Yiadom K, Dwivedi S, Plotz PH, Oppenheim JJ. Histidyl-tRNA synthetase and asparaginyl-tRNA synthetase, autoantigens in myositis, activate chemokine receptors on T lymphocytes and immature dendritic cells. J Exp Med 2002, 196:781-791. 10.1084/jem.20020186, 2194054, 12235211.
19. Tournadre A, Lenief V, Miossec P. Expression of Toll-like receptor 3 and Toll-like receptor 7 in muscle is characteristic of inflammatory myopathy and is differentially regulated by Th1 and Th17 cytokines. Arthritis Rheum 2010, 62:2144-2151.
20. Cappelletti C, Baggi F, Zolezzi F, Biancolini D, Beretta O, Severa M, Coccia EM, Confalonieri P, Morandi L, Mora M, Mantegazza R, Bernasconi P. Type I interferon and Toll-like receptor expression characterizes inflammatory myopathies. Neurology 2011, 76:2079-2088. 10.1212/WNL.0b013e31821f440a, 21670437.
21. Rawat R, Cohen TV, Ampong B, Francia D, Henriques-Pons A, Hoffman EP, Nagaraju K. Inflammasome up-regulation and activation in dysferlin-deficient skeletal muscle. Am J Pathol 2010, 176:2891-2900. 10.2353/ajpath.2010.090058, 2877850, 20413686.
22. Brouwer R, Hengstman GJ, Vree Egberts W, Ehrfeld H, Bozic B, Ghirardello A, Grøndal G, Hietarinta M, Isenberg D, Kalden JR, Lundberg I, Moutsopoulos H, Roux-Lombard P, Vencovsky J, Wikman A, Seelig HP, van Engelen BG, van Venrooij WJ. Autoantibody profiles in the sera of European patients with myositis. Ann Rheum Dis 2001, 60:116-123. 10.1136/ard.60.2.116, 1753477, 11156543.
23. Kattah NH, Kattah MG, Utz PJ. The U1-snRNP complex: structural properties relating to autoimmune pathogenesis in rheumatic diseases. Immunol Rev 2010, 233:126-145. 10.1111/j.0105-2896.2009.00863.x, 3074261, 20192997.
24. Bartoccioni E, Michaelis D, Hohlfeld R. Constitutive and cytokine-induced production of interleukin-6 by human myoblasts. Immunol Lett 1994, 42:135-138. 10.1016/0165-2478(94)90076-0, 7890313.
25. Nagaraju K, Raben N, Merritt G, Loeffler L, Kirk K, Plotz P. A variety of cytokines and immunologically relevant surface molecules are expressed by normal human skeletal muscle cells under proinflammatory stimuli. Clin Exp Immunol 1998, 113:407-414. 10.1046/j.1365-2249.1998.00664.x, 1905062, 9737670.
26. Bettelli E, Oukka M, Kuchroo VK. T(H)-17 cells in the circle of immunity and autoimmunity. Nat Immunol 2007, 8:345-350.
27. Nishimoto N, Yoshizaki K, Miyasaka N, Yamamoto K, Kawai S, Takeuchi T, Hashimoto J, Azuma J, Kishimoto T. Treatment of rheumatoid arthritis with humanized anti-interleukin-6 receptor antibody: a multicenter, double-blind, placebo-controlled trial. Arthritis Rheum 2004, 50:1761-1769. 10.1002/art.20303, 15188351.
28. 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 2009, 60:2505-2512. 10.1002/art.24689, 19644888.
29. Goebels N, Michaelis D, Engelhardt M, Huber S, Bender A, Pongratz D, Johnson MA, Wekerle H, Tschopp J, Jenne D, Hohlfeld R. Differential expression of perforin in muscle-infiltrating T cells in polymyositis and dermatomyositis. J Clin Invest 1996, 97:2905-2910. 10.1172/JCI118749, 507387, 8675705.
30. De Bleecker JL, Meire VI, Declercq W, Van Aken EH. Immunolocalization of tumor necrosis factor-alpha and its receptors in inflammatory myopathies. Neuromuscul Disord 1999, 9:239-246. 10.1016/S0960-8966(98)00126-6, 10399751.
31. Dastmalchi M, Grundtman C, Alexanderson H, Mavragani CP, Einarsdottir H, Helmers SB, Elvin K, Crow MK, Nennesmo I, Lundberg IE. A high incidence of disease flares in an open pilot study of infliximab in patients with refractory inflammatory myopathies. Ann Rheum Dis 2008, 67:1670-1677. 10.1136/ard.2007.077974, 18272672.
32. Eloranta ML, Barbasso Helmers S, Ulfgren AK, Ronnblom L, Alm GV, Lundberg IE. A possible mechanism for endogenous activation of the type I interferon system in myositis patients with anti-Jo-1 or anti-Ro 52/anti-Ro 60 autoantibodies. Arthritis Rheum 2007, 56:3112-3124. 10.1002/art.22860, 17763410.
33. Walsh RJ, Kong SW, Yao Y, Jallal B, Kiener PA, Pinkus JL, Beggs AH, Amato AA, Greenberg SA. Type I interferon-inducible gene expression in blood is present and reflects disease activity in dermatomyositis and polymyositis. Arthritis Rheum 2007, 56:3784-3792. 10.1002/art.22928, 2443782, 17968926.
34. Greenberg SA, Pinkus JL, Pinkus GS, Burleson T, Sanoudou D, Tawil R, Barohn RJ, Saperstein DS, Briemberg HR, Ericsson M, Park P, Amato AA. Interferon-alpha/beta-mediated innate immune mechanisms in dermatomyositis. Ann Neurol 2005, 57:664-678. 10.1002/ana.20464, 15852401.
35. Salajegheh M, Kong SW, Pinkus JL, Walsh RJ, Liao A, Nazareno R, Amato AA, Krastins B, Morehouse C, Higgs BW, Jallal B, Yao Y, Sarracino DA, Parker KC, Greenberg SA. Interferon-stimulated gene 15 (ISG15) conjugates proteins in dermatomyositis muscle with perifascicular atrophy. Ann Neurol 2010, 67:53-63.
36. Greenberg SA, Pinkus GS, Amato AA, Pinkus JL. Myeloid dendritic cells in inclusion-body myositis and polymyositis. Muscle Nerve 2007, 35:17-23. 10.1002/mus.20649, 16969836.
37. Rider LG, Miller FW. Mast cells and type I interferon responses in the skin of patients with juvenile dermatomyositis: are current therapies just scratching the surface?. Arthritis Rheum 2010, 62:2619-2622. 10.1002/art.27525, 2946445, 20506242.
38. Soejima M, Kang EH, Gu X, Katsumata Y, Clemens PR, Ascherman DP. Role of innate immunity in a murine model of histidyl-transfer RNA synthetase (Jo-1)-mediated myositis. Arthritis Rheum 2011, 63:479-487. 10.1002/art.30113, 3035731, 21280002.
39. Howard OM, Dong HF, Su SB, Caspi RR, Chen X, Plotz P, Oppenheim JJ. Autoantigens signal through chemokine receptors: uveitis antigens induce CXCR3- and CXCR5-expressing lymphocytes and immature dendritic cells to migrate. Blood 2005, 105:4207-4214. 10.1182/blood-2004-07-2697, 1895027, 15713799.
40. Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, Frazier A, Yang H, Ivanova S, Borovikova L, Manogue KR, Faist E, Abraham E, Andersson J, Andersson U, Molina PE, Abumrad NN, Sama A, Tracey KJ. HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999, 285:248-251. 10.1126/science.285.5425.248, 10398600.
41. Yang H, Ochani M, Li J, Qiang X, Tanovic M, Harris HE, Susarla SM, Ulloa L, Wang H, DiRaimo R, Czura CJ, Wang H, Roth J, Warren HS, Fink MP, Fenton MJ, Andersson U, Tracey KJ. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc Natl Acad Sci USA 2004, 101:296-301. 10.1073/pnas.2434651100, 314179, 14695889.
42. Li J, Xie H, Wen T, Liu H, Zhu W, Chen X. Expression of high mobility group box chromosomal protein 1 and its modulating effects on downstream cytokines in systemic lupus erythematosus. J Rheumatol 2010, 37:766-775. 10.3899/jrheum.090663, 20110525.
43. Park JS, Gamboni-Robertson F, He Q, Svetkauskaite D, Kim JY, Strassheim D, Sohn JW, Yamada S, Maruyama I, Banerjee A, Ishizaka A, Abraham E. High mobility group box 1 protein interacts with multiple Toll-like receptors. Am J Physiol Cell Physiol 2006, 290:C917-924.
44. Choi JH, Park YE, Kim SI, Kim JI, Lee CH, Park KH, Kim DS. Differential immunohistological features of inflammatory myopathies and dysferlinopathy. J Korean Med Sci 2009, 24:1015-1023. 10.3346/jkms.2009.24.6.1015, 2775846, 19949654.
45. Nagaraju K, Raben N, Loeffler L, Parker T, Rochon PJ, Lee E, Danning C, Wada R, Thompson C, Bahtiyar G, Craft J, Hooft Van Huijsduijnen R, Plotz P. Conditional up-regulation of MHC class I in skeletal muscle leads to self-sustaining autoimmune myositis and myositis-specific autoantibodies. Proc Natl Acad Sci USA 2000, 97:9209-9214. 10.1073/pnas.97.16.9209, 16847, 10922072.
46. Nagaraju K, Casciola-Rosen L, Lundberg I, Rawat R, Cutting S, Thapliyal R, Chang J, Dwivedi S, Mitsak M, Chen YW, Plotz P, Rosen A, Hoffman E, Raben N. Activation of the endoplasmic reticulum stress response in autoimmune myositis: potential role in muscle fiber damage and dysfunction. Arthritis Rheum 2005, 52:1824-1835. 10.1002/art.21103, 15934115.
47. Vitadello M, Doria A, Tarricone E, Ghirardello A, Gorza L. Myofiber stress-response in myositis: parallel investigations on patients and experimental animal models of muscle regeneration and systemic inflammation. Arthritis Res Ther 2010, 12:R52. 10.1186/ar2963, 2888201, 20334640.
48. Allison J, Campbell IL, Morahan G, Mandel TE, Harrison LC, Miller JF. Diabetes in transgenic mice resulting from over-expression of class I histocompatibility molecules in pancreatic beta cells. Nature 1988, 333:529-533. 10.1038/333529a0, 3287175.
49. Turnley AM, Morahan G, Okano H, Bernard O, Mikoshiba K, Allison J, Bartlett PF, Miller JF. Dysmyelination in transgenic mice resulting from expression of class I histocompatibility molecules in oligodendrocytes. Nature 1991, 353:566-569. 10.1038/353566a0, 1717849.
50. Oliveira AL, Thams S, Lidman O, Piehl F, Hokfelt T, Karre K, Linda H, Cullheim S. A role for MHC class I molecules in synaptic plasticity and regeneration of neurons after axotomy. Proc Natl Acad Sci USA 2004, 101:17843-17848. 10.1073/pnas.0408154101, 539738, 15591351.
51. Shatz CJ. MHC class I: an unexpected role in neuronal plasticity. Neuron 2009, 64:40-45. 10.1016/j.neuron.2009.09.044, 2773547, 19840547.
52. Thams S, Brodin P, Plantman S, Saxelin R, Karre K, Cullheim S. Classical major histocompatibility complex class I molecules in motoneurons: new actors at the neuromuscular junction. J Neurosci 2009, 29:13503-13515. 10.1523/JNEUROSCI.0981-09.2009, 19864563.
53. Yoshida H. ER stress and diseases. FEBS J 2007, 274:630-658. 10.1111/j.1742-4658.2007.05639.x, 17288551.
54. Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL, Ron D. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 1998, 12:982-995. 10.1101/gad.12.7.982, 316680, 9531536.
55. Kalai M, Lamkanfi M, Denecker G, Boogmans M, Lippens S, Meeus A, Declercq W, Vandenabeele P. Regulation of the expression and processing of caspase-12. J Cell Biol 2003, 162:457-467. 10.1083/jcb.200303157, 2172698, 12885762.
56. Rao RV, Hermel E, Castro-Obregon S, del Rio G, Ellerby LM, Ellerby HM, Bredesen DE. Coupling endoplasmic reticulum stress to the cell death program. Mechanism of caspase activation. J Biol Chem 2001, 276:33869-33874. 10.1074/jbc.M102225200, 11448953.
57. Iwawaki T, Akai R, Kohno K, Miura M. A transgenic mouse model for monitoring endoplasmic reticulum stress. Nat Med 2004, 10:98-102. 10.1038/nm970, 14702639.
58. Alger HM, Rayavarapu S, Nagaraju K. Measurement of activation of the endoplasmic reticulum stress response in autoimmune myositis. Methods Enzymol 2011, 489:207-225.
59. Vattemi G, Engel WK, McFerrin J, Askanas V. Endoplasmic reticulum stress and unfolded protein response in inclusion body myositis muscle. Am J Pathol 2004, 164:1-7. 10.1016/S0002-9440(10)63089-1, 1602240, 14695312.
60. Nogalska A, Engel WK, McFerrin J, Kokame K, Komano H, Askanas V. Homocysteine-induced endoplasmic reticulum protein (Herp) is up-regulated in sporadic inclusion-body myositis and in endoplasmic reticulum stress-induced cultured human muscle fibers. J Neurochem 2006, 96:1491-1499. 10.1111/j.1471-4159.2006.03668.x, 16441512.
61. Li CK, Knopp P, Moncrieffe H, Singh B, Shah S, Nagaraju K, Varsani H, Gao B, Wedderburn LR. Overexpression of MHC class I heavy chain protein in young skeletal muscle leads to severe myositis. Implications for juvenile myositis. Am J Pathol 2009, 175:1030-1040. 10.2353/ajpath.2009.090196, 2731122, 19700752.
62. Salomonsson S, Grundtman C, Zhang SJ, Lanner JT, Li C, Katz A, Wedderburn LR, Nagaraju K, Lundberg IE, Westerblad H. Upregulation of MHC class I in transgenic mice results in reduced force-generating capacity in slow-twitch muscle. Muscle Nerve 2009, 39:674-682. 10.1002/mus.21129, 2667561, 19229963.
63. Nogalska A, Wojcik S, Engel WK, McFerrin J, Askanas V. Endoplasmic reticulum stress induces myostatin precursor protein and NF-kappaB in cultured human muscle fibers: relevance to inclusion body myositis. Exp Neurol 2007, 204:610-618. 10.1016/j.expneurol.2006.12.014, 1909753, 17261282.
64. Parker KC, Walsh RJ, Salajegheh M, Amato AA, Krastins B, Sarracino DA, Greenberg SA. Characterization of human skeletal muscle biopsy samples using shotgun proteomics. J Proteome Res 2009, 8:3265-3277. 10.1021/pr800873q, 19382779.
65. Fratta P, Engel WK, McFerrin J, Davies KJ, Lin SW, Askanas V. Proteasome inhibition and aggresome formation in sporadic inclusion-body myositis and in amyloid-beta precursor protein-overexpressing cultured human muscle fibers. Am J Pathol 2005, 167:517-526. 10.1016/S0002-9440(10)62994-X, 1603556, 16049336.
66. Nogalska A, D'Agostino C, Terracciano C, Engel WK, Askanas V. Impaired autophagy in sporadic inclusion-body myositis and in endoplasmic reticulum stress-provoked cultured human muscle fibers. Am J Pathol 2010, 177:1377-1387. 10.2353/ajpath.2010.100050, 2928970, 20616343.
67. Norman B, Nygren AT, Nowak J, Sabina RL. The effect of AMPD1 genotype on blood flow response to sprint exercise. Eur J Appl Physiol 2008, 103:173-180. 10.1007/s00421-008-0683-0, 18224333.
68. Fischer H, Esbjornsson M, Sabina RL, Stromberg A, Peyrard-Janvid M, Norman B. AMP deaminase deficiency is associated with lower sprint cycling performance in healthy subjects. J Appl Physiol 2007, 103:315-322. 10.1152/japplphysiol.00185.2007, 17463303.
69. Park JH, Olsen NJ, King L, Vital T, Buse R, Kari S, Hernanz-Schulman M, Price RR. Use of magnetic resonance imaging and P-31 magnetic resonance spectroscopy to detect and quantify muscle dysfunction in the amyopathic and myopathic variants of dermatomyositis. Arthritis Rheum 1995, 38:68-77. 10.1002/art.1780380111, 7818575.
70. Wu J, Ruas JL, Estall JL, Rasbach KA, Choi JH, Ye L, Boström P, Tyra HM, Crawford RW, Campbell KP, Rutkowski DT, Kaufman RJ, Spiegelman BM. The unfolded protein response mediates adaptation to exercise in skeletal muscle through a PGC-1alpha/ATF6alpha complex. Cell Metab 2011, 13:160-169. 10.1016/j.cmet.2011.01.003, 3057411, 21284983.
71. Konttinen YT, Mackiewicz Z, Povilenaite D, Sukura A, Hukkanen M, Virtanen I. Disease-associated increased HIF-1, alphavbeta3 integrin, and Flt-1 do not suffice to compensate the damage-inducing loss of blood vessels in inflammatory myopathies. Rheumatol Int 2004, 24:333-339. 10.1007/s00296-003-0379-z, 13680145.
72. Grundtman C, Tham E, Ulfgren AK, Lundberg IE. Vascular endothelial growth factor is highly expressed in muscle tissue of patients with polymyositis and patients with dermatomyositis. Arthritis Rheum 2008, 58:3224-3238. 10.1002/art.23884, 18821695.
73. Nagaraju K, Rider LG, Fan C, Chen YW, Mitsak M, Rawat R, Patterson K, Grundtman C, Miller FW, Plotz PH, Hoffman E, Lundberg IE. Endothelial cell activation and neovascularization are prominent in dermatomyositis. J Autoimmune Dis 2006, 3:2. 10.1186/1740-2557-3-2, 1397829, 16504012.
74. Probst-Cousin S, Neundorfer B, Heuss D. Microvasculopathic neuromuscular diseases: lessons from hypoxia-inducible factors. Neuromuscul Disord 2010, 20:192-197. 10.1016/j.nmd.2010.01.005, 20122829.
75. Dastmalchi M, Alexanderson H, Loell I, Stahlberg M, Borg K, Lundberg IE, Esbjornsson M. Effect of physical training on the proportion of slow-twitch type I muscle fibers, a novel nonimmune-mediated mechanism for muscle impairment in polymyositis or dermatomyositis. Arthritis Rheum 2007, 57:1303-1310. 10.1002/art.22996, 17907213.