Neo-epitope Peptides as Biomarkers of Disease Progression for Muscular Dystrophies and Other Myopathies

A Arvanitidis, K Henriksen, M A Karsdal, A Nedergaard, A Arvanitidis, K Henriksen, M A Karsdal, A Nedergaard

Abstract

For several decades, serological biomarkers of neuromuscular diseases as dystrophies, myopathies and myositis have been limited to routine clinical biochemistry panels. Gauging the pathological progression is a prerequisite for proper treatment and therefore identifying accessible, easy to monitor biomarkers that can predict the disease progression would be an important advancement. Most muscle diseases involve accelerated muscle fiber degradation, inflammation, fatty tissue substitution and/or fibrosis. All these pathological traits have been shown to give rise to serological peptide biomarkers in other tissues, underlining the potential application of existing biomarkers of such traits in muscle disorders. A significant quantity of tissue is involved in these pathological mechanisms alongside with qualitative changes in protein turnover in myofibrillar, extra-cellular matrix and immunological cell protein fractions accompanied by alterations in body fluids. We propose that protein and peptides can leak out of the afflicted muscles and can be of use in diagnosis, prediction of pathology trajectory and treatment efficacy. Proteolytic cleavage systems are especially modulated during a range of muscle pathologies, thereby giving rise to peptides that are differentially released during disease manifestation. Therefore, we believe that pathology-specific post-translational modifications like cleavages can give rise to neoepitope peptides that may represent a promising class of peptides for discovery of biomarkers pertaining to neuromuscular diseases.

Keywords: Muscular dystrophies; biomarkers; myopathies; prognosis.

Figures

Fig.1
Fig.1
Ongoing clinical trials for DMD/BMD and LGMD diseases. The current stage at the time of writing for the most advanced in each category is illustrated. Indicatively “Exon skipping” drugs is a promising class, in which Drisapersen/PRO051 (Prosensa), Eteplirsen/AVI-4658 (Sarepta) are currently in phase III [65] Ataluren/PTC-124 has received marketing approval in Europe (but not in US) under the name Translarna mda.gov.
Fig.2
Fig.2
Anatomy of the muscle structure: The extracellular matrix, the sarcolemma and the intracellular domains are illustrated, depicting the relations between the different constituents. Proteins that are affected by mutations or deletions have the respective disease indicated in parentheses.

References

    1. Mercuri E, Muntoni F. Muscular dystrophies. Lancet. 2013;381:845–860.
    1. Reed P, Porter NC, Strong J, Pumplin DW, Corse AM, Luther PW, et al. Sarcolemmal reorganization in facioscapulohumeral muscular dystrophy. Ann Neurol. 2006;59:289–297.
    1. Shin J, Tajrishi MM, Ogura Y, Kumar A. Wasting mechanisms in muscular dystrophy. Int J Biochem Cell Biol. 2013;45:2266–2279.
    1. Klingler W, Jurkat-Rott K, Lehmann-Horn F, Schleip R. The role of fibrosis in Duchenne muscular dystrophy. Acta Myol. 2012;31:184–195.
    1. Rouillon J, Poupiot J, Zocevic A, Amor F, Léger T, Garcia C, et al. Serum proteomic profiling reveals fragments of MYOM3 as potential biomarkers for monitoring the outcome of therapeutic interventions in muscular dystrophies. Hum Mol Genet. 2015;24:4916–4932.
    1. Scharf G, Heineke J. Finding good biomarkers for sarcopenia. J Cachexia Sarcopenia Muscle. 2012;3:145–148.
    1. Nedergaard A, Karsdal MA, Sun S, Henriksen K. Serological muscle loss biomarkers: An overview of current concepts and future possibilities. J Cachexia Sarcopenia Muscle. 2013;4:1–17.
    1. Clark KA, McElhinny AS, Beckerle MC, Gregorio CC. Striated muscle cytoarchitecture: An intricate web of form and function. Annu Rev Cell Dev Biol. 2002;18:637–706.
    1. Brown KJ, Marathi R, Fiorillo AA, Ciccimaro EF, Sharma S, Rowlands DS, et al. Accurate quantitation of dystrophin protein in human skeletal muscle using mass spectrometry. J Bioanal Biomed. 2012;Suppl 7:1–16.
    1. Oak SA, Zhou YW, Harry W, Jarrett HW. Mechanisms of Signal Transduction: Skeletal Muscle Signaling Pathway through the Dystrophin Glycoprotein Complex and Skeletal Muscle Signaling Pathway through the Dystrophin Glycoprotein Complex and Rac1 *. J Biol chem. 2003;78:39287 doi:
    1. Zatz M, Rapaport D, Vainzof M, Passos-Bueno MR, Bortolini ER, Pavanello RDC, et al. Serum creatine-kinase (CK) and pyruvate-kinase (PK) activities in Duchenne (DMD) as compared with Becker (BMD) muscular dystrophy. J Neurol Sci. 1991;102:190–196.
    1. Hauerslev S, Sveen ML, Vissing J, Krag TO. Protein turnover and cellular stress in mildly and severely affected muscles from patients with limb girdle muscular dystrophy type 2I. PLoS One. 2013;8:e66929.
    1. Laval SH, Bushby KMD. Limb-girdle muscular dystro-phies–from genetics to molecular pathology. Neuropathol Appl Neurobiol. 2004;30:91–105.
    1. Kekou K, Fryssira H, Sophocleous C, Mavrou A, Manta P, Metaxotou C. Facioscapulohumeral muscular dystrophy molecular testing using a non radioactive protocol. Mol Cell Probes. 2005;9:422–424.
    1. Hengstman GJ, van Venrooij WJ, Vencovsky J, Moutsopoulos HM, van Engelen BG. The relative prevalence of dermatomyositis and polymyositis in Europe exhibits a latitudinal gradient. Ann Rheum Dis. 2000;59:141–142.
    1. Clapp J, Mitchell LM, Bolland DJ, Fantes J, Corcoran AE, Scotting PJ, et al. Evolutionary conservation of a coding function for D4Z4, the tandem DNA repeat mutated in facioscapulohumeral muscular dystrophy. Am J Hum Genet. 2007;81:264–279.
    1. Flanigan KM, Harper SQ. Facioscapulohumeral Dystrophy In: Muscle Disease: Pathology and Genetics, Second edition 2013, pp 288–297.
    1. Selva O’Callaghan A, Trallero Araguás E. Inflammatory myopathies. Dermatomyositis, polymyositis, and inclusion body myositis. Reumatol Clin. 2008;4:197–206.
    1. Hengstman GJD, De Bleecker JL, Feist E, Vissing J, Denton CP, Manoussakis MN, et al. Open-label trial of anti-TNF-alpha in dermato- and polymyositis treated concomitantly with methotrexate. Eur Neurol. 2008;59:159–163.
    1. Ayoglu B, Chaouch A, Lochmüller H, Politano L, Bertini E, Spitali P, et al. Affinity proteomics within rare diseases: A BIO-NMD study for blood biomarkers of muscular dystrophies. EMBO Mol Med. 2014;6:1–19.
    1. Scotton C, Passarelli C, Neri M, Ferlini A. Biomarkers in rare neuromuscular diseases. Exp Cell Res. 2013;1–6.
    1. Burch PM, Pogoryelova O, Goldstein R, Bennett D, Guglieri M, Straub V, et al. Muscle-derived proteins as serum biomarkers for monitoring disease progression in three forms of muscular dystrophy. J Neuromuscul Dis. 2015;2:241–255.
    1. Chen Y-W, Nagaraju K, Bakay M, McIntyre O, Rawat R, Shi R, et al. Early onset of inflammation and later involvement of TGFbeta in Duchenne muscular dystrophy. Neurology. 2005;65:826–834.
    1. Haslett JN, Sanoudou D, Kho AT, Bennett RR, Greenberg SA, Kohane IS, et al. Gene expression comparison of biopsies from Duchenne muscular dystrophy (DMD) and normal skeletal muscle. Proc Natl Acad Sci U S A. 2002;99:15000–15005.
    1. Bay-jensen AC, Byrjalsen I, Siebuhr AS. Serological biomarkers of joint tissue turnover predict tocilizumab response at baseline. J Clin Rheumatol. 2014;20:332–335.
    1. van Spil WE, DeGroot J, Lems WF, Oostveen JCM, Lafeber FPJG. Serum and urinary biochemical markers for knee and hip-osteoarthritis: A systematic review applying the consensus BIPED criteria. Osteoarthritis Cartilage. 2010;18:605–612.
    1. Fukushima K, Nakamura A, Ueda H, Yuasa K, Yoshida K, Takeda S, et al. Activation and localization of matrix metalloproteinase-2 and -9 in the skeletal muscle of the muscular dystrophy dog (CXMDJ). BMC Musculoskelet Disord. 2007;8:54.
    1. Li H, Mittal A, Makonchuk DY, Bhatnagar S, Kumar A. Matrix metalloproteinase-9 inhibition ameliorates pathogenesis and improves skeletal muscle regeneration in muscular dystrophy. Hum Mol Genet. 2009;18:2584–2598.
    1. Gosselin LE, Williams JE, Personius K, Farkas GA. A comparison of factors associated with collagen metabolism in different skeletal muscles from dystrophic (mdx) mice: Impact of pirfenidone. Muscle Nerve. 2007;35:208–216.
    1. Tandon A, Villa CR, Hor KN, Jefferies JL, Gao Z, Towbin JA, et al. Myocardial fibrosis burden predicts left ventricular ejection fraction and is associated with age and steroid treatment duration in duchenne muscular dystrophy. J Am Heart Assoc. 2015;4 doi:
    1. Desguerre I, Mayer M, Leturcq F, Barbet J-P, Gherardi RK, Christov C. Endomysial fibrosis in Duchenne muscular dystrophy: A marker of poor outcome associated with macrophage alternative activation. J Neuropathol Exp Neurol. 2009;68:762–773.
    1. Gillies AR, Lieber RL. Structure and function of the skeletal muscle extracellular matrix. Muscle Nerve. 2011;44:318–331.
    1. Haus JM, Carrithers JA, Trappe SW, Trappe TA. Collagen, cross-linking, and advanced glycation end products in aging human skeletal muscle. J Appl Physiol. 2007;47306:2068–2076.
    1. Chen X, Li Y. Role of matrix metalloproteinases in skeletal muscle. Cell Adhes Migr. 2009;3:337–341.
    1. Rennie M, Edwards R, Griggs R, Matthews S, Read M, Matthews D, et al. Total protein-turnover and muscle protein-synthesis by stable isotope techniques in duchenne muscular-dystrophy. Eur J Clin Invest. 1982;12:32–34.
    1. Sohar I, Laszlo A, Gaal K, Mechler F. Cysteine and metalloproteinase activities in serum of Duchenne muscular dystrophic genotypes. Biol Chem Hoppe Seyler. 1988;369(Suppl):277–279.
    1. von Moers A, Zwirner A, Reinhold A, Brückmann O, van Landeghem F, Stoltenburg-Didinger G, et al. Increased mRNA expression of tissue inhibitors of metalloproteinase-1 and -2 in Duchenne muscular dystrophy. Acta Neuropathol. 2005;109:285–293.
    1. Nadarajah VD, van Putten M, Chaouch A, Garrood P, Straub V, Lochmüller H, et al. Serum matrix metalloproteinase-9 (MMP-9) as a biomarker for monitoring disease progression in Duchenne muscular dystrophy (DMD). Neuromuscul Disord. 2011;21:569–578.
    1. Kumar A, Bhatnagar S, Kumar A. Matrix metalloproteinase inhibitor batimastat alleviates pathology and improves skeletal muscle function in dystrophin-deficient mdx mice. Am J Pathol. 2010;177:248–260.
    1. Stevenson EJ, Giresi PG, Koncarevic A, Kandarian SC. Global analysis of gene expression patterns during disuse atrophy in rat skeletal muscle. J Physiol. 2003;551:33–48.
    1. Taillandier D, Aurousseau E, Meynial-Denis D, Bechet D, Ferrara M, Cottin P, et al. Coordinate activation of lysosomal, Ca 2+-activated and ATP-ubiquitin-dependent proteinases in the unweighted rat soleus muscle. Biochem J. 1996;316(Pt 1):65–72.
    1. Goll DE, Thompson VF, Li H, Wei W, Cong J. The Calpain System. Physiol Rev. 2003;1990:731–801.
    1. Hauerslev S, Sveen M-L, Duno M, Angelini C, Vissing J, Krag TO. Calpain 3 is important for muscle regeneration: Evidence from patients with limb girdle muscular dystrophies. BMC Musculoskelet Disord. 2012;13:43.
    1. Ojima K, Kawabata Y, Nakao H, Nakao K, Doi N, Kitamura F, et al. Dynamic distribution of muscle-specific calpain in mice has a key role in physical-stress adaptation and is impaired in muscular dystrophy. J Clin Invest. 2010;120:2672–2683.
    1. Jackman RW, Kandarian SC. The molecular basis of skeletal muscle atrophy. Am J Physiol Cell Physiol.C. 2004;287:834–843.
    1. Aronson JK. Biomarkers and surrogate endpoints. Br J Clin Pharmacol. 2005;59:491–494.
    1. Bauer DC, Hunter DJ, Abramson SB, Attur M, Corr M, Felson D, et al. Classification of osteoarthritis biomarkers: A proposed approach. Osteoarthritis Cartilage. 2006;14:723–727.
    1. FDA report. Challenge and opportunity on the critical path to new medical products. US Dep Heal Hum Serv Food drug Adm. 2004.
    1. Trollet C, Athanasopoulos T, Popplewell L, Malerba A, Dickson G. Gene therapy for muscular dystrophy: Current progress and future prospects. Expert Opin Biol Ther. 2009;9(7):849–866.
    1. Schwartz M, Hertz JM, Sveen ML, Vissing J. LGMD2I presenting with a characteristic Duchenne or Becker muscular dystrophy phenotype. Neurology. 2005;64:1635–1637.
    1. Bonne G, Leturcq F, Ben YR. Emery-Dreifuss Muscular Dystrophy. Gene Rev. 2004. . (accessed 22 Apr. 2015).
    1. Gong QY, Phoenix J, Kemp GJ, García-Fiñana M, Frostick SP, Brodie DA, et al. Estimation of body composition in muscular dystrophy by MRI and stereology. J Magn Reson Imaging. 2000;12:467–475.
    1. Kampschulte M, Schneider CR, Litzlbauer H, Tscholl C, Schneider D, Zeiner C, et al. Quantitative 3D micro-CT imaging of human lung tissue quantitative 3-D-mikro-CT-bildgebung von humanem lungengewebe. Exp Radiol. 2013;869–876.
    1. Damilakis J, Adams JE, Guglielmi G, Link TM. Radiation exposure in X-ray-based imaging techniques used in osteoporosis. Eur Radiol. 2010;20:2707–2714.
    1. Levine JA, Abboud L, Barry M, Reed JE, Sheedy PF, Jensen MD. Measuring leg muscle and fat mass in humans: Comparison of CT and dual-energy X-ray absorptiometry elderly patients Measuring leg muscle and fat mass in humans: Comparison of CT and dual-energy X-ray absorptiometry. J Appl Physiol. 2014;88:452–456.
    1. Visser M, Fuerst T, Lang T, Salamone L, Tamara B. Validity of fan-beam dual-energy X-ray absorptiometry for measuring fat-free mass and leg muscle mass. J Appl Physiol. 2014;87:452–456.
    1. Clark BC, Cook SB, Ploutz-Snyder LL. Reliability of techniques to assess human neuromuscular function in vivo . J Electromyogr Kinesiol. 2007;17:90–101.
    1. Lee RC, Wang Z, Heymsfield SB. Skeletal muscle mass and aging: Regional and whole-bod measurment methods. Can J Appl Physiol. 2001;26:102–122.
    1. McDonald CM, Henricson EK, Abresch RT, Florence JM, Eagle M, Gappmaier E, et al. The 6-minute walk test and other endpoints in Duchenne muscular dystrophy: Longitudinal natural history observations over 48 weeks from a multicenter study. Muscle Nerve. 2013;48:343–356.
    1. Witting N, Duno M, Vissing J. Deletion of exon 26 of the dystrophin gene is associated with a mild Becker muscular dystrophy phenotype. Acta Myol. 2011;30:182–184.
    1. Cardamone M, Darras BT, Ryan MM. Inherited myopathies and muscular dystrophies. Semin Neurol. 2008;28:250–259.
    1. Witting N, Duno M, Petri H, Krag T, Bundgaard H, Kober L, et al. Anoctamin 5 muscular dystrophy in Denmark: Prevalence, genotypes, phenotypes, cardiac findings, and muscle protein expression. J Neurol. 2013;260:2084–2093.
    1. Jeanson-Leh L, Lameth J, Krimi S, Buisset J, Amor F, Le Guiner C, et al. Serum profiling identifies novel muscle miRNA and cardiomyopathy-related miRNA biomarkers in golden retriever muscular dystrophy dogs and duchenne muscular dystrophy patients. Am J Pathol. 2014;184:2885–2898.
    1. Li X, Li Y, Zhao L, Zhang D, Yao X, Zhang H, et al. Circulating muscle-specific miRNAs in duchenne muscular dystrophy patients. Mol Ther Nucleic Acids. 2014;3:e177.
    1. Zaharieva IT, Calissano M, Scoto M, Preston M, Cirak S, Feng L, et al. Dystromirs as serum biomarkers for monitoring the disease severity in Duchenne muscular dystrophy. PLoS One. 2013:8 doi: 10.1371/journal.pone.0080263
    1. Mizuno H, Nakamura A, Aoki Y, Ito N, Kishi S, Yamamoto K, et al. Identification of muscle-specific MicroRNAs in serum of muscular dystrophy animal models: Promising novel blood-based markers for muscular dystrophy. PLoS One. 2011;6:14–19.
    1. Coenen-Stass AML, McClorey G, Manzano R, Betts CA, Blain A, Saleh AF, et al. Identification of novel, therapy-responsive protein biomarkers in a mouse model of Duchenne muscular dystrophy by aptamer-based serum proteomics. Sci ReNature Publishing Group. 2015;5:17014.
    1. Ahtikoski AM, Tuominen H, Korpelainen JT, Takala TES, Oikarinen A. Collagen synthesis and degradation in polyneuropathy and myopathies. Muscle Nerve. 2004;30:602–608.
    1. Holmberg C, Ghesquière B, Impens F, Gevaert K, Kumar JD, Cash N, et al. Mapping proteolytic processing in the secretome of gastric cancer-associated myofibroblasts reveals activation of MMP-1, MMP-2, and MMP-3. J Proteome Res. 2013;12:3413–2422.
    1. Brundel BJJM, Ausma J, Van Gelder IC, Van Der Want JJL, Van Gilst WH, Crijns HJGM, et al. Activation of proteolysis by calpains and structural changes in human paroxysmal and persistent atrial fibrillation. Cardiovasc Res. 2002;54:380–389.
    1. Allen DG, Whitehead NP. Duchenne muscular dystrophy–what causes the increased membrane permeability in skeletal muscle? Int J Biochem Cell Biol. 2011;43:290–294.
    1. Rosen HN, Moses AC, Garber J, Iloputaife ID, Ross DS, Lee SL, et al. Serum CTX: A new marker of bone resorption that shows treatment effect more often than other markers because of low coefficient of variability and large changes with bisphosphonate therapy. Calcif Tissue Int. 2000;66:100–103.
    1. Rosenquist C, Fledelius C, Christgau S, Pedersen BJ, Bonde M, Qvist P, et al. Serum CrossLaps One Step ELISA. First application of monoclonal antibodies for measurement in serum of bone-related degradation products from C-terminal telopeptides of type I collagen. Clin Chem. 1998;44:2281–2289.
    1. Garnero P, Ferreras M, Karsdal MA, Nicamhlaoibh R, Risteli J, Borel O, et al. The type I collagen fragments ICTP and CTX reveal distinct enzymatic pathways of bone collagen degradation. J Bone Miner Res. 2003;18:859–867.
    1. Leeming, Leeming, Sand JM, Nielsen MJ, Genovese, Martinez, et al. Serological investigation of the collagen degradation profile of patients with chronic obstructive pulmonary disease or idiopathic pulmonary fibrosis. Biomark Insights. 2012;119.
    1. Bay-Jensen A-C, Wichuk S, Byrjalsen I, Karsdal MA, Maksymowych WP. Two novel diagnostic biomarkers of cartilage degradation and connective tissue inflammation are predictive of radiographic disease progression. Osteoarthr Cartil. 2012;20:S90.
    1. Bay-Jensen AC, Liu Q, Byrjalsen I, Li Y, Wang J, Pedersen C, et al. Enzyme-linked immunosorbent assay (ELISAs) for metalloproteinase derived type II collagen neoepitope, CIIM-Increased serum CIIM in subjects with severe radiographic osteoarthritis. Clin Biochem. 2011;44:423–429.
    1. Bay-Jensen AC, Karsdal MA, Vassiliadis E, Wichuk S, Marcher-Mikkelsen K, Lories R, et al. Circulating citrullinated vimentin fragments reflect disease burden in ankylosing spondylitis and have prognostic capacity for radiographic progression. Arthritis Rheum. 2013;65:972–980.
    1. Genovese F, Manresa AA, Leeming DJ, Karsdal MA, Boor P. The extracellular matrix in the kidney: A source of novel non-invasive biomarkers of kidney fibrosis? Fibrogenesis Tissue Repair. 2014;7:4.
    1. Vassiliadis E, Oliveira CP, Alvares-da-Silva MR, Zhang C, Carrilho FJ, Stefano JT, et al. Circulating levels of citrullinated and MMP-degraded vimentin (VICM) in liver fibrosis related pathology. Am J Transl Res. 2012;4:403–414.
    1. Siebuhr A, Bay-Jensen AC, Leeming DJ, Plat A, Byrjalsen I, Christiansen C, et al. Serological identification of fast progressors of structural damage with rheumatoid arthritis. Arthritis Res Ther. 2013;15:R86.
    1. Drey M, Sieber CC, Bauer JM, Uter W, Dahinden P, Fariello RG, et al. C-terminal Agrin Fragment as a potential marker for sarcopenia caused by degeneration of the neuromuscular junction. Exp Gerontol. 2013;48:76–80.
    1. Nedergaard A, Sun S, Karsdal MA, Henriksen K, Kjær M, Lou Y, et al. Type VI collagen turnover-related peptides-novel serological biomarkers of muscle mass and anabolic response to loading in young men. J Cachexia Sarcopenia Muscle. 2013;4:267–275.
    1. Leeming D, He Y, Veidal S, Nguyen Q, Larsen D, Koizumi M, et al. A novel marker for assessment of liver matrix remodeling: An enzyme-linked immunosorbent assay (ELISA) detecting a MMP generated type I collagen neo-epitope (C1M). Biomarkers. 2011;16:616–628.
    1. Barascuk N, Veidal SS, Larsen L, Larsen D V, Larsen MR, Wang J, et al. A novel assay for extracellular matrix remodeling associated with liver fibrosis: An enzyme-linked immunosorbent assay (ELISA) for a MMP-9proteolytically revealed neo-epitope of type III collagen. Clin Biochem. 2010;43:899–904.
    1. Nielsen MJ, Nedergaard AF, Sun S, Veidal SS, Larsen L, Zheng Q, et al. The neo-epitope specific PRO-C3 ELISA measures true formation of type III collagen associated with liver and muscle parameters. Am J Transl Res. 2013;5:303–315.
    1. Sun S, Henriksen K, Karsdal MA, Armbrecht G, Belavý DL, Felsenberg D, et al. Measurement of a MMP-2 degraded Titin fragment in serum reflects changes in muscle turnover induced by atrophy. Exp Gerontol. 2014;58:83–89.
    1. Hathout Y, Brody E, Clemens PR, Cripe L, DeLisle RK, Furlong P, et al. Large-scale serum protein biomarker discovery in Duchenne muscular dystrophy. Proc Natl Acad Sci. 2015;112:201507719.
    1. Manzur AY, Kuntzer T, Pike M, Swan A. Glucocorticoid corticosteroids for Duchenne muscular dystrophy. Cochrane Database Syst Rev. 2004;CD003725.
    1. Micks RH, Mullaney J. Dermatomyositis successfully treated by prednisone. Ir J Med Sci. 1958;333–334.
    1. van de Vlekkert J, Hoogendijk JE, de Haan RJ, Algra A, van der Tweel I, van der Pol WL, et al. Oral dexamethasone pulse therapy versus daily prednisolone in sub-acute onset myositis, a randomised clinical trial. Neuromuscul Disord. 2010;20:382–389.
    1. Ramanan AV, Campbell-Webster N, Ota S, Parker S, Tran D, Tyrrell PN, et al. The effectiveness of treating juvenile dermatomyositis with methotrexate and aggressively tapered corticosteroids. Arthritis Rheum. 2005;52:3570–3578.
    1. Aggarwal R, Oddis CV. Therapeutic advances in myositis. Curr Opin Rheumatol. 2012;24:635–641.
    1. 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.
    1. Efthimiou P. Tumor necrosis factor-alpha in inflammatory myopathies: Pathophysiology and therapeutic implications. Semin Arthritis Rheum. 2006;36:168–172.
    1. Hengstman GJD, van den Hoogen FHJ, Barrera P, Netea MG, Pieterse A, van de Putte LBA, et al. Successful treatment of dermatomyositis and polymyositis with anti-tumor-necrosis-factor-alpha: Preliminary observations. Eur Neurol. 2003;50:10–15.
    1. Mammen AL, Sartorelli V. IL-6 Blockade as a therapeutic approach for duchenne muscular dystrophy. Ebio Medicine. 2015;2–3.
    1. Evans WJ. Skeletal muscle loss: Cachexia, sarcopenia, and inactivity 1–3. 2010;91:1123–1127.
    1. Wei AS, Callaci JJ, Juknelis D, Marra G, Tonino P, Freedman KB, et al. The effect of corticosteroid on collagen expression in injuredrotator cuff tendon. J bone Jt surg Am. 2011;88:1331–1338.
    1. Ay M, Kuntzer T, Pike M, Av S. Glucocorticoid corticosteroids for Duchenne muscular dystrophy (Review). Cochrane Collab 2009;1
    1. Gressner AM, Weiskirchen R. Modern pathogenetic concepts of liver fibrosis suggest stellate cells and TGF-β as major players and therapeutic targets. J Cell Mol Med. 2006;10:76–99.
    1. Lieber RL, Ward SR. Cellular mechanisms of tissue fibrosis. 4. Structural and functional consequences of skeletal muscle fibrosis. Am J Physiol Cell Physiol. 2013;305:C241–C252.
    1. Veidal SS, Vassiliadis E, Bay-Jensen A-C, Tougas G, Vainer B, Karsdal MA. Procollagen type I N-terminal propeptide (PINP) is a marker for fibrogenesis in bile duct ligation-induced fibrosis in rats. Fibrogenesis Tissue Repair. 2010;3:5.
    1. Schierwagen R, Leeming DJ, Klein S, Granzow M, Nielsen MJ, Sauerbruch T, et al. Serum markers of the extracellular matrix remodeling reflect antifibrotic therapy in bile-duct ligated rats. Front Physiol. 2013. doi:
    1. Zhou L, Lu H. Targeting fibrosis in Duchenne muscular dystrophy. J Neuropathol Exp Neurol. 2010;69:771–776.
    1. Duance VC, Stephens HR, Dunn M, Bailey AJ, Dubowitz V. A role for collagen in the pathogenesis of muscular dystrophy? Nature. 1980;284:470.
    1. Foidart M, Foidart JM, Engel WK. Collagen localization in normal and fibrotic human skeletal muscle. Arch Neurol. 1981;38:152–157.
    1. Zhao BL, Kollias HD, Wagner KR. Myostatin directly regulates skeletal muscle fibrosis. J Biol Chem. 2008;283:19371–19378.
    1. Artaza JN, Singh R, Ferrini MG, Braga M, Tsao J, Gonzalez-Cadavid NF. Myostatin promotes a fibrotic phenotypic switch in multipotent C3H 10T1/2 cells without affecting their differentiation into myofibroblasts. J Endocrinol. 2008;196:235–249.
    1. Zion O, Genin O, Kawada N, Yoshizato K, Roffe S, Nagler A, et al. Inhibition of transforming growth factor beta signaling by halofuginone as a modality for pancreas fibrosis prevention. Pancreas. 2009;38:427–435.
    1. Karsdal MA, Henriksen K, Leeming DJ, Woodworth T, Vassiliadis E, Bay-Jensen A-C. Novel combinations of Post-Translational Modification (PTM) neo-epitopes provide tissue-specific biochemical markers–are they the cause or the consequence of the disease? Clin Biochem. 2010;43:793–804.
    1. Cynthia Martin F, Hiller M, Spitali P, Oonk S, Dalebout H, Palmblad M, et al. Fibronectin is a serum biomarker for Duchenne muscular dystrophy. Proteomics - Clin Appl. 2014;8:269–278.
    1. Norwood FLM, Harling C, Chinnery PF, Eagle M, Bushby K, Straub V. Prevalence of genetic muscle disease in Northern England: In-depth analysis of a muscle clinic population. Brain. 2009;132:3175–3186.
    1. Van der Kooi AJ, Barth PG, Busch HF, de Haan R, Ginjaar HB, van Essen AJ, et al. The clinical spectrum of limb girdle muscular dystrophy. A survey in The Netherlands. Brain. 1996;119(Pt 5):1471–1480.
    1. Cooper D, Upadhhyaya M. Facioscapulohumeral Muscular Dystrophy (FSHD): Clinical Medicine and Molecular Cell Biology. 2004.
    1. Tawil R, van der Maarel SM, Tapscott SJ. Facioscapulohumeral dystrophy: The path to consensus on pathophysiology. Skelet Muscle. 2014;4:12.
    1. Choy EHS, Isenberg DA. Treatment of dermatomyositis and polymyositis. Rheumatology (Oxford). 2002;41:7–13.
    1. Orphanet. Orphanet Report Series Prevalence of rare diseases: Bibliographic data. Rare Dis. 2014;1–29.
    1. Bernatsky S, Joseph L, Pineau CA, Bélisle P, Boivin JF, Banerjee D, et al. Estimating the prevalence of polymyositis and dermatomyositis from administrative data: Age, sex and regional differences. Ann Rheum Dis. 2009;68:1192–1196.
    1. Needham M, Corbett A, Day T, Christiansen F, Fabian V, Mastaglia FL. Prevalence of sporadic inclusion body myositis and factors contributing to delayed diagnosis. J Clin Neurosci. 2008;15:1350–1353.
    1. Böhm J, Vasli N, Malfatti E, Le Gras S, Feger C, Jost B, et al. An integrated diagnosis strategy for congenital myopathies. PLoS One. 2013;8:e67527.
    1. McNeil SM, Woulfe J, Ross C, Tarnopolsky MA. Congenital inflammatory myopathy: A demonstrative case and proposed diagnostic classification. Muscle Nerve. 2002;259–264.
    1. Vassiliadis E, Veidal SS, Barascuk N, Mullick JB, Clausen RE, Larsen L, et al. Measurement of matrix metalloproteinase 9-mediated collagen type III degradation fragment as a marker of skin fibrosis. BMC Dermatol. 2011;11:6.
    1. Rouillon J, Zocevic A, Leger T, Garcia C, Camadro J-M, Udd B, et al. Proteomics profiling of urine reveals specific titin fragments as biomarkers of Duchenne muscular dystrophy. Neuromuscul Disord. 2014;24:563–573.

Source: PubMed

Sponsors et collaborateurs

Les conditions médicales

Interventions en matière de drogue

3
S'abonner