Targeting protein homeostasis in sporadic inclusion body myositis

Science Translational Medicine

Volumn 8, Issue 331, 2016, Pages

  Ahmed, Mhoriam ^a   MacHado, Pedro M ^a   Miller, Adrian ^a   Spicer, Charlotte ^a   Herbelin, Laura ^b   He, Jianghua ^b   Noel, Janelle ^b   Wang, Yunxia ^b   McVey, April L ^b   Pasnoor, Mamatha ^b   Gallagher, Philip ^c   Statland, Jeffrey ^b   Lu, Ching Hua ^a   Kalmar, Bernadett ^a   Brady, Stefen ^a   Sethi, Huma ^d   Samandouras, George ^d   Parton, Matt ^a   Holton, Janice L ^a   Weston, Anne ^e   Collinson, Lucy ^e   Taylor, J Paul ^f   Schiavo, Giampietro ^a   Hanna, Michael G ^a   Barohn, Richard J ^b   Dimachkie, Mazen M ^b   Greensmith, Linda ^a   more..

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF KANSAS   (United States)

^d NATIONAL HOSPITAL FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

^e THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^f ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARIMOCLOMOL; HEAT SHOCK PROTEIN 70; PLACEBO; ADENOSINE TRIPHOSPHATASE; AMYLOID BETA PROTEIN; AUTACOID; CDC48 PROTEIN; CELL CYCLE PROTEIN; HYDROXYLAMINE; PROTEIN;

ANIMAL CELL; ARTICLE; BODY WEIGHT; CELL SURVIVAL; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG EFFICACY; DRUG RESPONSE; DRUG SAFETY; DRUG TARGETING; DRUG TOLERABILITY; ENDOPLASMIC RETICULUM STRESS; GRIP STRENGTH; HUMAN; IN VITRO STUDY; INCLUSION BODY MYOSITIS; MALE; MOUSE; MUSCLE CONTRACTILITY; MUSCLE FUNCTION; MUSCLE STRENGTH; MYOBLAST; NONHUMAN; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN HOMEOSTASIS; RANDOMIZED CONTROLLED TRIAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); RAT; TREATMENT DURATION; UNSPECIFIED SIDE EFFECT; UPREGULATION; ANIMAL; CELL CULTURE; CLINICAL TRIAL (TOPIC); DRUG EFFECTS; GENETICS; HOMEOSTASIS; METABOLISM; MUSCLE CONTRACTION; MUTATION; PATHOLOGY; PATHOPHYSIOLOGY; TREATMENT OUTCOME;

ADENOSINE TRIPHOSPHATASES; AMYLOID BETA-PEPTIDES; ANIMALS; CELL CYCLE PROTEINS; CELL SURVIVAL; CELLS, CULTURED; CLINICAL TRIALS AS TOPIC; ENDOPLASMIC RETICULUM STRESS; HOMEOSTASIS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; HYDROXYLAMINES; INFLAMMATION MEDIATORS; MICE; MUSCLE CONTRACTION; MUSCLE STRENGTH; MUTATION; MYOBLASTS; MYOSITIS, INCLUSION BODY; PROTEINS; RATS; TREATMENT OUTCOME;

EID: 84961773841     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aad4583     Document Type: Article

References (60)

1. M.M. Dimachkie, R. J. Barohn, Inclusion bodymyositis. Curr. Neurol. Neurosci. Rep. 13, 321 (2013).
2. P. Machado, S. Brady, M. G. Hanna, Update in inclusion body myositis. Curr. Opin. Rheumatol. 25, 763-771 (2013).
3. A. A. Amato, G. S. Gronseth, C. E. Jackson, G. I. Wolfe, J. S. Katz, W. W. Bryan, R. J. Barohn, Inclusion body myositis: Clinical and pathological boundaries. Ann. Neurol. 40, 581-586 (1996).
4. A. A. Amato, R. J. Barohn, Evaluation and treatment of inflammatory myopathies. J. Neurol. Neurosurg. Psychiatry 80, 1060-1068 (2009).
5. F. M. Cox, M. J. Titulaer, J. K. Sont, A. R. Wintzen, J. J. G. M. Verschuuren, U. A. Badrising, A 12-year follow-up in sporadic inclusion body myositis: An end stage with major disabilities. Brain 134(Pt. 11), 3167-3175 (2011).
6. O. Benveniste, M. Guiguet, J. Freebody, O. Dubourg, W. Squier, T. Maisonobe, T. Stojkovic, M. I. Leite, Y. Allenbach, S. Herson, S. Brady, B. Eymard, D. Hilton-Jones, Long-term observational study of sporadic inclusion body myositis. Brain 134(Pt. 11), 3176-3184 (2011).
7. A. Cortese, P. Machado, J. Morrow, L. Dewar, A. Hiscock, A. Miller, S. Brady, D. Hilton-Jones, M. Parton, M. G. Hanna, Longitudinal observational study of sporadic inclusion body myositis: Implications for clinical trials. Neuromuscul. Disord. 23, 404-412 (2013).
8. U. A. Badrising, M. Maat-Schieman, S. G. van Duinen, F. Breedveld, P. van Doorn, B. van Engelen, F. vandenHoogen, J.Hoogendijk, C.Höweler, A. deJager, F. Jennekens, P.Koehler, H. vander Leeuw, M. de Visser, J. J. Verschuuren, A. R. Wintzen, Epidemiology of inclusion body myositis in the Netherlands: A nationwide study. Neurology 55, 1385-1388 (2000).
9. B. A. Phillips, P. J. Zilko, F. L. Mastaglia, Prevalence of sporadic inclusion body myositis in Western Australia. Muscle Nerve 23, 970-972 (2000).
10. K. J. Felice, W. A. North, Inclusion body myositis in Connecticut: Observations in 35 patients during an 8-year period. Medicine 80, 320-327 (2001).
11. F. C. Wilson, S. R. Ytterberg, J. L. St. Sauver, A. M. Reed, Epidemiology of sporadic inclusion body myositis and polymyositis in Olmsted County, Minnesota. J. Rheumatol. 35, 445-447 (2008).
12. M. Needham, A. Corbett, T. Day, F. Christiansen, V. Fabian, F. L. Mastaglia, Prevalence of sporadic inclusion body myositis and factors contributing to delayed diagnosis. J. Clin. Neurosci. 15, 1350-1353 (2008).
13. E. A. Shamim, L.G. Rider, J. P. Pandey, T. P.O'Hanlon, L. J. Jara, E. A. Samayoa, R. Burgos-Vargas, J. Vazquez-Mellado, J. Alcocer-Varela, M. Salazar-Paramo, A. G. Kutzbach, J. D. Malley, I. N. Targoff, I. Garcia-De La Torre, F. W. Miller, Differences in idiopathic inflammatory myopathy phenotypes and genotypes between Mesoamerican Mestizos and North American Caucasians: Ethnogeographic influences in the genetics and clinical expression of myositis. Arthritis Rheum. 46, 1885-1893 (2002).
14. S. A. Greenberg, Theories of the pathogenesis of inclusion body myositis. Curr. Rheumatol. Rep. 12, 221-228 (2010).
15. M. C. Dalakas, Pathogenesis and therapies of immune-mediated myopathies. Autoimmun. Rev. 11, 203-206 (2012).
16. S. A. Greenberg, Inclusion body myositis. Curr. Opin. Rheumatol. 23, 574-578 (2011).
17. V. Askanas, W. K. Engel, Inclusion-body myositis, a multifactorial muscle disease associated with aging: Current concepts of pathogenesis. Curr. Opin. Rheumatol. 19, 550-559 (2007).
18. M. Needham, F. L. Mastaglia, Inclusion body myositis: Current pathogenetic concepts and diagnostic and therapeutic approaches. Lancet Neurol. 6, 620-631 (2007).
19. M. Salajegheh, J. L. Pinkus, J. P. Taylor, A. A. Amato, R. Nazareno, R. H. Baloh, S. A. Greenberg, Sarcoplasmic redistribution of nuclear TDP-43 in inclusion body myositis. Muscle Nerve 40, 19-31 (2009).
20. C. C. Weihl, P. Temiz, S. E. Miller, G. Watts, C. Smith, M. Forman, P. I. Hanson, V. Kimonis, A. Pestronk, TDP-43 accumulation in inclusion body myopathy muscle suggests a common pathogenic mechanism with frontotemporal dementia. J. Neurol. Neurosurg. Psychiatry 79, 1186-1189 (2008).
21. V. Askanas, W. K. Engel, Inclusion-body myositis: A myodegenerative conformational disorder associated with Ab, protein misfolding, and proteasome inhibition. Neurology 66 (Suppl. 1), S39-S48 (2006).
22. A. Nogalska, C. Terracciano, C. D'Agostino, W. K. Engel, V. Askanas, p62/SQSTM1 is overexpressed and prominently accumulated in inclusions of sporadic inclusion-body myositis muscle fibers, and can help differentiating it from polymyositis and dermatomyositis. Acta Neuropathol. 118, 407-413 (2009).
23. J. McFerrin, W. K. Engel, V. Askanas, Impaired innervation of cultured human muscle overexpressing bAPP experimentally and genetically: Relevance to inclusion-body myopathies. Neuroreport 9, 3201-3205 (1998).
24. V. Askanas, J. McFerrin, S. Baqué, R. B. Alvarez, E. Sarkozi, W. K. Engel, Transfer of b-amyloid precursor protein gene using adenovirus vector causes mitochondrial abnormalities in cultured normal human muscle. Proc. Natl. Acad. Sci. U.S.A. 93, 1314-1319 (1996).
25. C. E.-H. Moussa, Q. Fu, P. Kumar, A. Shtifman, J. R. Lopez, P. D. Allen, F. LaFerla, D. Weinberg, J. Magrane, T. Aprahamian, K. Walsh, K. M. Rosen, H. W. Querfurth, Transgenic expression of b-APP in fast-twitch skeletal muscle leads to calcium dyshomeostasis and IBM-like pathology. FASEB J. 20, 2165-2167 (2006).
26. J. Schmidt, K. Barthel, J. Zschüntzsch, I. E. Muth, E. J. Swindle, A. Hombach, S. Sehmisch, A. Wrede, F. Lühder, R. Gold, M. C. Dalakas, Nitric oxide stress in sporadic inclusion body myositis muscle fibres: Inhibition of inducible nitric oxide synthase prevents interleukin- 1b-induced accumulation of b-amyloid and cell death. Brain 135 (Pt. 4), 1102-1114 (2012).
27. J. Schmidt, K. Barthel, A. Wrede, M. Salajegheh, M. Bähr, M. C. Dalakas, Interrelation of inflammation and APP in sIBM: IL-1b induces accumulation of b-amyloid in skeletal muscle. Brain 131, 1228-1240 (2008).
28. A. A. Amato, R. J. Barohn, C. E. Jackson, E. J. Pappert, Z. Sahenk, J. T. Kissel, Inclusion body myositis: Treatment with intravenous immunoglobulin. Neurology 44, 1516-1518 (1994).
29. M. C. Dalakas, B. Koffman, M. Fujii, S. Spector, K. Sivakumar, E. Cupler, A controlled study of intravenous immunoglobulin combined with prednisone in the treatment of IBM. Neurology 56, 323-327 (2001).
30. The Muscle Study Group, Randomized pilot trial of high-dose bINF-1a in patients with inclusion body myositis. Neurology 63, 718-720 (2004).
31. M. Breithaupt, J. Schmidt, Update on treatment of inclusion body myositis. Curr. Rheumatol. Rep. 15, 329 (2013).
32. P. M. Douglas, D. M. Cyr, Interplay between protein homeostasis networks in protein aggregation and proteotoxicity. Biopolymers 93, 229-236 (2010).
33. R. R. Kopito, Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 10, 524-530 (2000).
34. I. R. Brown, Heat shock proteins and protection of the nervous system. Ann. N. Y. Acad. Sci. 1113, 147-158 (2007).
35. B. Kalmar, L. Greensmith, Activation of the heat shock response in a primary cellular model of motoneuron neurodegeneration-evidence for neuroprotective and neurotoxic effects. Cell. Mol. Biol. Lett. 14, 319-335 (2009).
36. D. Kieran, B. Kalmar, J. R. T. Dick, J. Riddoch-Contreras, G. Burnstock, L. Greensmith, Treatment with arimoclomol, a coinducer of heat shock proteins, delays disease progression in ALS mice. Nat. Med. 10, 402-405 (2004).
37. B. Kalmar, G. Burnstock, G. Vrbová, R. Urbanics, P. Csermely, L. Greensmith, Upregulation of heat shock proteins rescues motoneurones from axotomy-induced cell death in neonatal rats. Exp. Neurol. 176, 87-97 (2002).
38. B. Kalmar, L. Greensmith, M. Malcangio, S. B. McMahon, P. Csermely, G. Burnstock, The effect of treatment with BRX-220, a co-inducer of heat shock proteins, on sensory fibers of the rat following peripheral nerve injury. Exp. Neurol. 184, 636-647 (2003).
39. J. Hargitai, H. Lewis, I. Boros, T. Rácz, A. Fiser, I. Kurucz, I. Benjamin, L. Vígh, Z. Pénzes, P. Csermely, D. S. Latchman, Bimoclomol, a heat shock protein co-inducer, acts by the prolonged activation of heat shock factor-1. Biochem. Biophys. Res. Commun. 307, 689-695 (2003).
40. L. Vígh, P. N. Literáti, I. Horváth, Z. Török, G. Balogh, A. Glatz, E. Kovács, I. Boros, P. Ferdinándy, B. Parkas, L. Jaszlits, A. Jednákovits, L. Korányi, B. Maresca, Bimoclomol: A nontoxic, hydroxylamine derivative with stress protein-inducing activity and cytoprotective effects. Nat. Med. 3, 1150-1154 (1997).
41. S. K. Custer, M. Neumann, H. Lu, A. C. Wright, J. P. Taylor, Transgenic mice expressing mutant forms VCP/p97 recapitulate the full spectrum of IBMPFD including degeneration in muscle, brain and bone. Hum. Mol. Genet. 19, 1741-1755 (2010).
42. T. T. Rohn, Caspase-cleaved TAR DNA-binding protein-43 is a major pathological finding in Alzheimer's disease. Brain Res. 1228, 189-198 (2008).
43. P. Kuner, R. Schubenel, C. Hertel, b-amyloid binds to p57NTR and activates NFkB in human neuroblastoma cells. J. Neurosci. Res. 54, 798-804 (1998).
44. D. L. Feinstein, E. Galea, D. A. Aquino, G. C. Li, H. Xu, D. J. Reis, Heat shock protein 70 suppresses astroglial-inducible nitric-oxide synthase expression by decreasing NFkB activation. J. Biol. Chem. 271, 17724-17732 (1996).
45. R. Njemini, I. Bautmans, O. O. Onyema, K. Van Puyvelde, C. Demanet, T. Mets, Circulating heat shock protein 70 in health, aging and disease. BMC Immunol. 12, 24 (2011).
46. D. C. Henstridge, J. M. Forbes, S. A. Penfold, M. F. Formosa, S. Dougherty, A. Gasser, M. P. de Courten, M. E. Cooper, B. A. Kingwell, B. de Courten, The relationship between heat shock protein 72 expression in skeletal muscle and insulin sensitivity is dependent on adiposity. Metabolism 59, 1556-1561 (2010).
47. J. P. Morton, A. C. Kayani, A. McArdle, B. Drust, The exercise-induced stress response of skeletal muscle, with specific emphasis on humans. Sports Med. 39, 643-662 (2009).
48. V. Lanka, S. Wieland, J. Barber, M. Cudkowicz, Arimoclomol: A potential therapy under development for ALS. Expert Opin. Investig. Drugs 18, 1907-1918 (2009).
49. M. Kürthy, T. Mogyorósi, K. Nagy, T. Kukorelli, A. Jednákovits, L. Tálosi, K. Bíró, Effect of BRX- 220 against peripheral neuropathy and insulin resistance in diabetic rat models. Ann. N. Y. Acad. Sci. 967, 482-489 (2002).
50. B. Kalmar, S. Novoselov, A. Gray, M. E. Cheetham, B. Margulis, L. Greensmith, Late stage treatment with arimoclomol delays disease progression and prevents protein aggregation in the SOD1G93A mouse model of ALS. J. Neurochem. 107, 339-350 (2008).
51. B.Malik, N. Nirmalananthan, A. L. Gray, A. R. La Spada, M. G. Hanna, L.Greensmith, Co-induction of the heat shock response ameliorates disease progression in a mouse model of human spinal and bulbar muscular atrophy: Implications for therapy. Brain 136 (Pt. 3), 926-943 (2013).
52. M. E. Cudkowicz, J. M. Shefner, E. Simpson, D. Grasso, H. Yu, H. Zhang, A. Shui, D. Schoenfeld, R. H. Brown, S. Wieland, J. R. Barber; Northeast ALS Consortium, Arimoclomol at dosages up to 300 mg/day is well tolerated and safe in amyotrophic lateral sclerosis. Muscle Nerve 38, 837-844 (2008).
53. R. Tawil, R. C. Griggs, Inclusion body myositis. Curr. Opin. Rheumatol. 14, 653-657 (2002).
54. R. C. Griggs, V. Askanas, S. DiMauro, A. Engel, G. Karpati, J. R. Mendell, L. P. Rowland, Inclusion body myositis and myopathies. Ann. Neurol. 38, 705-713 (1995).
55. C. E. Jackson, R. J. Barohn, G. Gronseth, S. Pandya, L. Herbelin, Inclusion body myositis functional rating scale: A reliable and valid measure of disease severity. Muscle Nerve 37, 473-476 (2008).
56. J. M. Morrow, G. M. Ramdharry, P. Machado, T. Burns, A. Amato, R. Barohn, L. Phillips, R. Seyedsadjadi, A. Joshi, M. Dimachkie, K. Gwathmey, L. Herbelin, G. Solorzano, M. Hanna, Rasch analysis of the IBMFRS. Muscle Nerve 48 (Suppl. 1), S2-S3 (2013).
57. The Muscle Study Group, Randomized pilot trial of bINF1a (Avonex) in patients with inclusion body myositis. Neurology 57, 1566-1570 (2001).
58. M. R. Rose, M. P. McDermott, C. A. Thornton, C. Palenski, W. B. Martens, R. C. Griggs, A prospective natural history study of inclusion body myositis: Implications for clinical trials. Neurology 57, 548-550 (2001).
59. T. J. Deerinck, E. A. Bushong, A. Thor, M. H. Ellisman, NCMIR methods for 3D EM: A new protocol for preparation of biological specimens for serial block face scanning electron microscopy. Available from http://ncmir.ucsd.edu/sbfsem-protocol.pdf (2010).
60. D. Kieran, L. Greensmith, Inhibition of calpains, by treatment with leupeptin, improves motoneuron survival and muscle function in models of motoneuron degeneration. Neuroscience 125, 427-439 (2004).