Duchenne Muscular Dystrophy: recent advances in protein biomarkers and the clinical application

References

• Anderson NL. The clinical plasma proteome: a survey of clinical assays for proteins in plasma and serum. Clin Chem. 2010;56(2):177–185.
   PubMed Web of Science ®Google Scholar
• Landegren U, Vänelid J, Hammond M, et al. Opportunities for sensitive plasma proteome analysis. Anal Chem. 2012;84(4): 1824–1830.
   PubMed Web of Science ®Google Scholar
• Borrebaeck CAK. Precision diagnostics: moving towards protein biomarker signatures of clinical utility in cancer. Nat Rev Cancer. 2017;17(3):199–204.
   PubMed Web of Science ®Google Scholar
• Patil H, Saxena SG, Barrow CJ, et al. Chasing the personalized medicine dream through biomarker validation in colorectal cancer. Drug Discov Today. 2017;22(1):111–119.
   PubMed Web of Science ®Google Scholar
• Pritzker K. Biomarker imprecision in precision medicine. Expert Rev Mol Diagn. 2018;18(8):685–687.
   PubMed Web of Science ®Google Scholar
• Califf RM. Biomarker definitions and their applications. Exp Biol Med (Maywood). 2018;243(3):213–221.
   PubMed Web of Science ®Google Scholar
• FDA-NIH Biomarker Working Group. BEST (Biomarkers, endpoints, and other tools) resource. 2016.
   Google Scholar
• Romitti PA, Zhu Y, Puzhankara S, et al. Prevalence of Duchenne and Becker muscular dystrophies in the United States. Pediatrics. 2015;135(3):513–521.
   PubMed Web of Science ®Google Scholar
• Giegerich E, Stuntz M. Duchenne Muscular Dystrophy prevalence in the US: a novel incidence-based modeling approach using system dynamics. Value Health. 2019;22:S244–S244.
   Web of Science ®Google Scholar
• Bladen CL, Salgado D, Monges S, et al. The TREAT-NMD DMD global database: analysis of more than 7,000 Duchenne Muscular Dystrophy mutations. Hum Mutat. 2015;36(4):395–402.
   PubMed Web of Science ®Google Scholar
• Falzarano MS, Scotton C, Passarelli C, et al. Duchenne Muscular Dystrophy: from diagnosis to therapy. Molecules. 2015;20(10):18168–18184.
   PubMed Web of Science ®Google Scholar
• Emery AEH. Muscular dystrophy into the new millennium. Neuromuscul Disord. 2002;12(4):343–349.
   PubMed Web of Science ®Google Scholar
• Bushby K, Finkel R, Birnkrant DJ, et al. Diagnosis and management of Duchenne Muscular Dystrophy, part 1: diagnosis, and pharmacological and psychosocial management. Lancet Neurol. 2010;9(1):77–93.
   PubMed Web of Science ®Google Scholar
• Van Ruiten HJA, Marini Bettolo C, Cheetham T, et al. Why are some patients with Duchenne Muscular Dystrophy dying young: an analysis of causes of death in North East England. Eur J Paediatr Neurol. 2016;20(6):904–909.
   PubMed Web of Science ®Google Scholar
• Landfeldt E, Thompson R, Sejersen T, et al. Life expectancy at birth in Duchenne Muscular Dystrophy: a systematic review and meta-analysis. Eur J Epidemiol. 2020;71(3):304.
   Google Scholar
• Koenig M, Monaco AP, Kunkel LM. The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell. 1988;53(2):219–228.
   PubMed Web of Science ®Google Scholar
• Campbell KP. Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell. 1995;80(5):675–679.
   PubMed Web of Science ®Google Scholar
• Le Rumeur E, Winder SJ, Hubert J-F. Dystrophin: more than just the sum of its parts. Biochim Biophys Acta. 2010;1804(9):1713–1722.
   PubMed Web of Science ®Google Scholar
• Gumerson JD, Research DMB. The dystrophin-glycoprotein complex in the prevention of muscle damage. J Biomed Biotechnol. 2011;83:ID210797.
   Google Scholar
• Feige P, Rudnicki MA. Muscle stem cells. Curr Biol. 2018;28(10):R589–R590.
   PubMed Web of Science ®Google Scholar
• Serrano AL, Mann CJ, Vidal B, et al. Cellular and molecular mechanisms regulating fibrosis in skeletal muscle repair and disease. Curr Top Dev Biol. 2011;96:167–201.
   PubMed Web of Science ®Google Scholar
• Chang NC, Chevalier FP, Rudnicki MA. Satellite cells in muscular dystrophy - lost in polarity. Trends Mol Med. 2016;22(6):479–496.
   PubMed Web of Science ®Google Scholar
• Feige P, Brun CE, Ritso M, et al. Orienting muscle stem cells for regeneration in homeostasis, aging, and disease. Cell Stem Cell. 2018;23(5):653–664.
   PubMed Web of Science ®Google Scholar
• Duguez S, Duddy W, Johnston H, et al. Dystrophin deficiency leads to disturbance of LAMP1-vesicle-associated protein secretion. Cell. Mol. Life Sci. 2013;70(12):2159–2174.
   PubMed Web of Science ®Google Scholar
• Straub V, Rafael JA, Chamberlain JS, et al. Animal models for muscular dystrophy show different patterns of sarcolemmal disruption. J Cell Biol. 1997;139(2):375–385.
   PubMed Web of Science ®Google Scholar
• McArdle A, Edwards R, Jackson MJ. Time-course of changes in plasma-membrane permeability in the dystrophin-deficient Mdx mouse. Muscle Nerve. 1994;17(12):1378–1384.
   PubMed Web of Science ®Google Scholar
• Hodgetts S, Radley H, Davies M, et al. Reduced necrosis of dystrophic muscle by depletion of host neutrophils, or blocking TNFalpha function with etanercept in mdx mice. Neuromuscul Disord. 2006;16(9–10):591–602.
   PubMed Web of Science ®Google Scholar
• Panovský R, Pešl M, Holeček T, et al. Cardiac profile of the Czech population of Duchenne Muscular Dystrophy patients: a cardiovascular magnetic resonance study with T1 mapping. Orphanet J Rare Dis. 2019;14(1):10.
   PubMedGoogle Scholar
• Barp A, Bello L, Caumo L, et al. Muscle MRI and functional outcome measures in Becker muscular dystrophy. Sci Rep. 2017;7(1):16060.
   PubMedGoogle Scholar
• Barnard AM, Willcocks RJ, Triplett WT, et al. MR biomarkers predict clinical function in Duchenne Muscular Dystrophy. Neurology. 2020;94(9):e897-e909.
   PubMed Web of Science ®Google Scholar
• Barnard AM, Willcocks RJ, Finanger EL, et al. Skeletal muscle magnetic resonance biomarkers correlate with function and sentinel events in Duchenne Muscular Dystrophy. PLoS ONE. 2018;13(3):e0194283.
   PubMed Web of Science ®Google Scholar
• Willcocks RJ, Rooney WD, Triplett WT, et al. Multicenter prospective longitudinal study of magnetic resonance biomarkers in a large Duchenne Muscular Dystrophy cohort. Ann Neurol. 2016;79(4):535–547.
   PubMed Web of Science ®Google Scholar
• Warman Chardon J, Diaz-Manera J, Tasca G, et al. MYO-MRI diagnostic protocols in genetic myopathies. Neuromuscul Disord. 2019;29(11):827–841.
   PubMed Web of Science ®Google Scholar
• Hathout Y, Marathi RL, Rayavarapu S, et al. Discovery of serum protein biomarkers in the mdx mouse model and cross-species comparison to Duchenne Muscular Dystrophy patients. Hum Mol Genet. 2014;23(24):6458–6469.
   PubMed Web of Science ®Google Scholar
• Nadarajah VD, Mertens B, Dalebout H. Serum peptide profiles of Duchenne Muscular Dystrophy (DMD) patients evaluated by data handling strategies for high resolution content. J Proteom Bioinform [ Internet]. 2012;5(4):096.
   Google Scholar
• Ayoglu B, Chaouch A, Lochmüller H, et al. Affinity proteomics within rare diseases: a BIO-NMD study for blood biomarkers of muscular dystrophies. EMBO Mol Med. 2014;6(7):918–936.
   PubMed Web of Science ®Google Scholar
• Cynthia Martin F, Hiller M, Spitali P, et al. Fibronectin is a serum biomarker for Duchenne Muscular Dystrophy. Proteomics Clin Appl. 2014;8(3–4):269–278.
   PubMed Web of Science ®Google Scholar
• Catapano F, Domingos J, Perry M, et al. Downregulation of miRNA-29, −23 and −21 in urine of Duchenne Muscular Dystrophy patients. Epigenomics. 2018;10(7):875–889.
   PubMed Web of Science ®Google Scholar
• Roberts TC, Coenen-Stass AML, Wood MJA. Assessment of RT-qPCR normalization strategies for accurate quantification of extracellular microRNAs in murine serum. PLoS ONE. 2014;9(2):e89237.
   PubMed Web of Science ®Google Scholar
• Roberts TC, Godfrey C, McClorey G, et al. Extracellular microRNAs are dynamic non-vesicular biomarkers of muscle turnover. Nucleic Acids Res. 2013;41(20):9500–9513.
   PubMed Web of Science ®Google Scholar
• Hrach HC, Mangone M. miRNA profiling for early detection and treatment of Duchenne Muscular Dystrophy. Int J Mol Sci. 2019;20(18):4638.
   PubMed Web of Science ®Google Scholar
• Coenen-Stass AML, Wood MJA, Roberts TC. Biomarker Potential of Extracellular miRNAs in Duchenne Muscular Dystrophy. Trends Mol Med. 2017;23(11):989–1001.
   PubMed Web of Science ®Google Scholar
• Tsonaka R, Signorelli M, Sabir E, et al. Longitudinal metabolomic analysis of plasma enables modeling disease progression in Duchenne Muscular Dystrophy mouse models. Hum Mol Genet. 2020;29(5):745–755.
   PubMed Web of Science ®Google Scholar
• Boca SM, Nishida M, Harris M, et al. Discovery of metabolic biomarkers for Duchenne Muscular Dystrophy within a natural history study. PLoS ONE. 2016;11(4):e0153461.
   PubMed Web of Science ®Google Scholar
• Spitali P, Hettne K, Tsonaka R, et al. Cross-sectional serum metabolomic study of multiple forms of muscular dystrophy. J Cell Mol Med. 2018;22(4):2442–2448.
   PubMed Web of Science ®Google Scholar
• Szigyarto CA-K, Spitali P. Biomarkers of Duchenne Muscular Dystrophy: current findings. DNND. 2018;8:1–13.
   Google Scholar
• Yasmineh WG, Ibrahim GA, Abbasnezhad M, et al. Isoenzyme distribution of creatine kinase and lactate dehydrogenase in serum and skeletal muscle in Duchenne Muscular Dystrophy, collagen disease, and other muscular disorders. Clin Chem. 1978;24(11):1985–1989.
   PubMed Web of Science ®Google Scholar
• Kiessling WR, Beckmann R. Serum levels of myoglobin and creatine kinase in Duchenne Muscular Dystrophy. Klin Wochenschr. 1981;59(7):347–348.
   PubMedGoogle Scholar
• Pernice W, Guggolz MA, Guggolz M, et al. A mathematical analysis of creatine kinase activity in the course of Duchenne Muscular Dystrophy. Muscle Nerve. 1986;9(4):333–340.
   PubMed Web of Science ®Google Scholar
• Percy ME, Chang LS, Murphy EG, et al. Serum creatine kinase and pyruvate kinase in Duchenne Muscular Dystrophy carrier detection. Muscle Nerve. 1979;2(5):329–339.
   PubMed Web of Science ®Google Scholar
• Cardon MW. 50 years ago in the journal of pediatrics: an assessment of the creatine kinase test in the detection of carriers of Duchenne Muscular Dystrophy. J Pediatr. 2017;186:63.
   PubMed Web of Science ®Google Scholar
• Nakamura A, Kobayashi M, Kuraoka M, et al. Initial pulmonary respiration causes massive diaphragm damage and hyper-CKemia in Duchenne Muscular Dystrophy dog. Sci Rep. 2013;3(1):359.
   Google Scholar
• Burch PM, Pogoryelova O, Palandra J, et al. Reduced serum myostatin concentrations associated with genetic muscle disease progression. J Neurol. 2017;264(3):541–553.
   PubMed Web of Science ®Google Scholar
• Oonk S, Spitali P, Hiller M, et al. Comparative mass spectrometric and immunoassay-based proteome analysis in serum of Duchenne Muscular Dystrophy patients. Proteomics Clin Appl. 2015;10(3):290–299.
   Web of Science ®Google Scholar
• Sun G, Haginoya K, Chiba Y, et al. Elevated plasma levels of tissue inhibitors of metalloproteinase-1 and their overexpression in muscle in human and mouse muscular dystrophy. J Neurol Sci. 2010;297(1–2):19–28.
   PubMed Web of Science ®Google Scholar
• Zelikovich AS, Quattrocelli M, Salamone IM, et al. Moderate exercise improves function and increases adiponectin in the mdx mouse model of muscular dystrophy. Sci Rep. 2019;9(1):281.
   PubMedGoogle Scholar
• Crowe KE, Shao G, Flanigan KM, et al. N-terminal α dystroglycan (αDG-N): a potential serum biomarker for Duchenne Muscular Dystrophy. J Neuromuscul Dis. 2016;3(2):247–260.
   PubMedGoogle Scholar
• Colussi CC, Banfi CC, Brioschi MM, et al. Proteomic profile of differentially expressed plasma proteins from dystrophic mice and following suberoylanilide hydroxamic acid treatment. Proteomics Clin Appl. 2009;4(1):71–83.
   PubMed Web of Science ®Google Scholar
• Guiraud S, Edwards B, Squire SE, et al. Identification of serum protein biomarkers for utrophin based DMD therapy. Sci Rep. 2017;7:43697.
   PubMed Web of Science ®Google Scholar
• Saito K, Koboyashi D, Komatsu M et al. A sensitive assay of tumor necrosis factor a in sera from Duchenne muscular dystrophy patients. Clin Chem 2000;46(10):1703e4
   Web of Science ®Google Scholar
• Füzéry AK, Levin J, Chan MM, et al. Translation of proteomic biomarkers into FDA approved cancer diagnostics: issues and challenges. Clin Proteomics. 2013;10(1):13.
   PubMed Web of Science ®Google Scholar
• Dochez V, Caillon H, Vaucel E, et al. Biomarkers and algorithms for diagnosis of ovarian cancer: CA125, HE4, RMI and ROMA, a review. J Ovarian Res. 2019;12(1):28–29.
   PubMedGoogle Scholar
• McDonagh TA, Cunningham AD, Morrison CE, et al. Left ventricular dysfunction, natriuretic peptides, and mortality in an urban population. Heart. 2001;86(1):21–26.
   PubMed Web of Science ®Google Scholar
• Dowling P, Murphy S, Zweyer M, et al. Emerging proteomic biomarkers of X-linked muscular dystrophy. Expert Rev Mol Diagn. 2019;19(8): 739–755.
   PubMed Web of Science ®Google Scholar
• Richterich R, Rosin S, Aebi U, et al. Progressive muscular dystrophy. V. The identification of the carrier state in the Duchenne type by serum creatine kinase determination. Am J Hum Genet. 1963;15(2):133–154.
   PubMed Web of Science ®Google Scholar
• Pearce MJ, Walton NJ, Pennington R. Serum enzyme studies in muscle disease. III. serum creatine kinase activity in relatives of patients with the Duchenne type of muscular dystrophy. J Neurol Neurosurg Psychiatry. 1964;27(3):181–185.
   PubMed Web of Science ®Google Scholar
• Mokuno K, Riku S, Matsuoka Y, et al. Serum muscle-specific enolase in progressive muscular dystrophy and other neuromuscular diseases. J Neurol Sci. 1984;63(3):345–352.
   PubMed Web of Science ®Google Scholar
• Kato K, Okagawa Y, Suzuki F, et al. Immunoassay of human-muscle enolase subunit in serum - a novel marker antigen for muscle diseases. Clin Chim Acta. 1983;131(1–2):75–85.
   PubMed Web of Science ®Google Scholar
• Carter ND, Heath R, Jeffery S, et al. Carbonic anhydrase III in Duchenne Muscular Dystrophy. Clin Chim Acta. 1983;133(2):201–208.
   PubMed Web of Science ®Google Scholar
• Mokuno K, Riku S, Matsuoka Y, et al. Serum carbonic anhydrase III in progressive muscular dystrophy. J Neurol Sci. 1985;67(2):223–228.
   PubMed Web of Science ®Google Scholar
• Ozawa E, Hagiwara Y, Yoshida M. Creatine kinase, cell membrane and Duchenne Muscular Dystrophy. Mol Cell Biochem. 1999;190(1–2):143–151.
   PubMed Web of Science ®Google Scholar
• Carberry S, Zweyer M, Swandulla D, et al. Profiling of age-related changes in the tibialis anterior muscle proteome of the mdx mouse model of dystrophinopathy. J Biomed Biotechnol. 2012;691641–691641:2011.
   Google Scholar
• Guevel L, Lavoie JR, Perez-Iratxeta C, et al. Quantitative proteomic analysis of dystrophic dog muscle. J Proteome Res. 2011;10(5):2465–2478.
   PubMed Web of Science ®Google Scholar
• Rayavarapu S, Coley W, Cakir E, et al. Identification of disease specific pathways using in vivo SILAC proteomics in dystrophin deficient mdx mouse. Mol Cell Proteomics. 2013;12(5):1061–1073.
   PubMed Web of Science ®Google Scholar
• Lewis C, Jockusch H, Ohlendieck K. Proteomic profiling of the dystrophin-deficient MDX heart reveals drastically altered levels of key metabolic and contractile proteins. J Biomed Biotechnol. 2010;2010(3):648501–648520.
   PubMedGoogle Scholar
• Alagaratnam S, Mertens BJA, Dalebout JC, et al. Serum protein profiling in mice: identification of Factor XIIIa as a potential biomarker for muscular dystrophy. Proteomics. 2008;8(8):1552–1563.
   PubMed Web of Science ®Google Scholar
• Rouillon J, Poupiot J, Zocevic A, et al. molecular FAH, 2015. 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(17):4916–4932.
   PubMed Web of Science ®Google Scholar
• Pietrowska M, Wlosowicz A, Gawin M, et al. MS-based proteomic analysis of serum and plasma: problem of high abundant components and lights and shadows of albumin removal. Adv Exp Med Biol. 2019;1073(5):57–76.
   PubMedGoogle Scholar
• Kuhn E, Addona T, Keshishian H, et al. Developing multiplexed assays for troponin I and interleukin-33 in plasma by peptide immunoaffinity enrichment and targeted mass spectrometry. Clinl Chem. 2009;55(6):1108–1117.
   PubMed Web of Science ®Google Scholar
• Murphy S, Dowling P, Zweyer M, et al. Proteomic profiling of mdx-4cv serum reveals highly elevated levels of the inflammation-induced plasma marker haptoglobin in muscular dystrophy. Int J Mol Med. 2017;39(6):1357–1370.
   PubMed Web of Science ®Google Scholar
• Granger J, Siddiqui J, Copeland S, et al. Albumin depletion of human plasma also removes low abundance proteins including the cytokines. Proteomics. 2005;5(18):4713–4718.
   PubMed Web of Science ®Google Scholar
• Seam N, Gonzales DA, Kern SJ, et al. Quality control of serum albumin depletion for proteomic analysis. Clin Chem. 2007;53(11):1915–1920.
   PubMed Web of Science ®Google Scholar
• Uhlén M, Fagerberg L, Hallström BM, et al. Proteomics. Tissue-based map of the human proteome. Science. 2015;347(6220):1260419.
   PubMed Web of Science ®Google Scholar
• Signorelli M, Ayoglu B, Johansson C, et al. Longitudinal serum biomarker screening identifies malate dehydrogenase 2 as candidate prognostic biomarker for Duchenne Muscular Dystrophy. J Cachexia, Sarcopenia Muscle. 2019;87:149.
   Google Scholar
• Schwenk JM, Nilsson P. Antibody suspension bead arrays. Methods Mol Biol. 2011;723:29–36.
   PubMedGoogle Scholar
• Breen EJ, Tan W, Khan A. The statistical value of raw fluorescence signal in luminex xMAP based multiplex immunoassays. Sci Rep. 2016;6(1):26996.
   PubMedGoogle Scholar
• Algenäs C, Agaton C, Fagerberg L, et al. Antibody performance in western blot applications is context-dependent. Biotechnol J. 2014;9(3):435–445.
   PubMed Web of Science ®Google Scholar
• Bourbeillon J, Orchard S, Benhar I, et al. Minimum information about a protein affinity reagent (MIAPAR). Nat Biotech. 2010;28(7):650–653.
   PubMed Web of Science ®Google Scholar
• Uhlén M, Bandrowski A, Carr S, et al. A proposal for validation of antibodies. Nat Methods. 2016;13(10): 823.
   PubMed Web of Science ®Google Scholar
• Edfors F, Hober A, Linderbäck K, et al. Enhanced validation of antibodies for research applications. Nat Commun. 2018;9(1):4130.
   PubMedGoogle Scholar
• Doerr A. Enhanced antibody validation. Nat Methods. 2018;15(12):1001.
   PubMed Web of Science ®Google Scholar
• Hathout Y, Brody E, Clemens PR, et al. Large-scale serum protein biomarker discovery in Duchenne Muscular Dystrophy. Proc Natl Acad Sci USA. 2015;112(23):7153–7158.
   PubMed Web of Science ®Google Scholar
• Voleti S, Olivieri L, Hamann K, et al. Troponin I Levels Correlate With Cardiac MR LGE and Native T1 Values in Duchenne Muscular Dystrophy Cardiomyopathy and Identify Early Disease Progression. Pediatr Cardiol. 2020;10.1007/s00246-020-02372-5.
   Google Scholar
• Hathout Y, Liang C, Ogundele M, et al. Disease-specific and glucocorticoid-responsive serum biomarkers for Duchenne Muscular Dystrophy. Sci Rep. 2019;9(1):12167.
   PubMedGoogle Scholar
• Anderson J, Seol H, Gordish-Dressman H, et al. Interleukin 1 receptor-like 1 protein (ST2) is a potential biomarker for cardiomyopathy in Duchenne Muscular Dystrophy. Pediatr Cardiol. 2017;38(8):1606–1612.
   PubMed Web of Science ®Google Scholar
• Parolo S, Marchetti L, Lauria M, et al. Combined use of protein biomarkers and network analysis unveils deregulated regulatory circuits in Duchenne Muscular Dystrophy. PLoS ONE. 2018;13(3):e0194225.
   PubMed Web of Science ®Google Scholar
• Zatz M, Rapaport D, Vainzof M, 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(2):190–196.
   PubMed Web of Science ®Google Scholar
• Mokuno K, Riku S, Sugimura K, et al. Serum creatine kinase isoenzymes in Duchenne Muscular Dystrophy determined by sensitive enzyme immunoassay methods. Muscle Nerve. 1987;10(5):459–463.
   PubMed Web of Science ®Google Scholar
• Baird MF, Graham SM, Baker JS, et al. Creatine-kinase- and exercise-related muscle damage implications for muscle performance and recovery. J Nutr Metab. 2012;960363:2012.
   Google Scholar
• Magal M, Dumke CL, Urbiztondo ZG, et al. Relationship between serum creatine kinase activity following exercise-induced muscle damage and muscle fibre composition. J Sports Sci. 2010;28(3):257–266.
   PubMed Web of Science ®Google Scholar
• Kobayashi YM, Rader EP, Crawford RW, et al. Endpoint measures in the mdx mouse relevant for muscular dystrophy pre-clinical studies. Neuromuscul Disord. 2012;22(1):34–42.
   PubMed Web of Science ®Google Scholar
• Aartsma-Rus A, Ferlini A, Vroom E. Biomarkers and surrogate endpoints in Duchenne: meeting report. Neuromuscul Disord. 2014;24(8):743–745.
   PubMed Web of Science ®Google Scholar
• Timonen A, Lloyd-Puryear M, Neonatal DHJO. Duchenne Muscular Dystrophy newborn screening: evaluation of a new GSP® neonatal creatine kinase-MM Kit in a US and Danish population. Int J Neonatal Screen. 2019;5(27). DOI:10.3390/ijns5030027
   Google Scholar
• Moat SJ, Bradley DM, Salmon R, et al. Newborn bloodspot screening for Duchenne Muscular Dystrophy: 21 years experience in Wales (UK). Eur J Hum Genet. 2013;21(10):1049–1053.
   PubMed Web of Science ®Google Scholar
• Mendell JR, Shilling C, Leslie ND, et al. Evidence-based path to newborn screening for Duchenne Muscular Dystrophy. Ann Neurol. 2012;71(3):304–313.
   PubMed Web of Science ®Google Scholar
• Murphy S, Zweyer M, Mundegar RR, et al. Proteomic serum biomarkers for neuromuscular diseases. Expert Rev Proteomic. 2018;15(3):277–291.
   PubMed Web of Science ®Google Scholar
• Spitali P, Hettne K, Tsonaka R, et al. Tracking disease progression non‐invasively in Duchenne and Becker muscular dystrophies. J Cachexia, Sarcopenia Muscle. 2018;80(4):706–726.
   Google Scholar
• Ohta M, Itagaki Y, Itoh N, et al. Carbonic anhydrase III in serum in muscular dystrophy and other neurological disorders: relationship with creatine kinase. Clin Chem. 1991;37(1):36–39.
   PubMed Web of Science ®Google Scholar
• Cheeran D, Khan S, Khera R, et al. Predictors of death in adults with Duchenne Muscular Dystrophy–associated cardiomyopathy. J Am Heart Assoc. 2017;6(10):121.
   Web of Science ®Google Scholar
• Matsumura T, Saito T, Fujimura H, et al. Cardiac troponin I for accurate evaluation of cardiac status in myopathic patients. Brain Dev. 2007;29(8):496–501.
   PubMed Web of Science ®Google Scholar
• Townsend DW, Turner I, Yasuda S, et al. Chronic administration of membrane sealant prevents severe cardiac injury and ventricular dilatation in dystrophic dogs. J Clin Invest. 2010;120(4):1140–1150.
   PubMed Web of Science ®Google Scholar
• Nadarajah VD, van Putten M, Chaouch A, et al. Serum matrix metalloproteinase-9 (MMP-9) as a biomarker for monitoring disease progression in Duchenne Muscular Dystrophy (DMD). Neuromuscul Disord. 2011;21(8):569–578.
   PubMed Web of Science ®Google Scholar
• Lourbakos A, Yau N, de Bruijn P, et al. Evaluation of serum MMP-9 as predictive biomarker for antisense therapy in Duchenne. Sci Rep. 2017;7(1):17888.
   PubMedGoogle Scholar
• Soslow JH, Xu M, Slaughter JC, et al. The role of matrix metalloproteinases and tissue inhibitors of metalloproteinases in Duchenne Muscular Dystrophy cardiomyopathy. J Card Fail. 2019;25(4):259–267.
   PubMed Web of Science ®Google Scholar
• Zocevic A, Rouillon J, Wong B, et al. Evaluation of the serum matrix metalloproteinase-9 as a biomarker for monitoring disease progression in Duchenne Muscular Dystrophy. Neuromuscul Disord. 2015;25(5):444–446.
   PubMed Web of Science ®Google Scholar
• Spitali P, Aartsma-Rus A, T’ Hoen PAC. Response to: evaluation of the serum matrix metalloproteinase-9 as a biomarker for monitoring disease progression in Duchenne Muscular Dystrophy. Neuromuscul Disord. 2015;25(5):5.
   PubMed Web of Science ®Google Scholar
• Rodríguez-Cruz M, Cruz-Guzmán OR, Escobar RE, et al. Leptin and metabolic syndrome in patients with Duchenne/Becker muscular dystrophy. Acta Neurol Scand. 2016;133(4):253–260.
   PubMed Web of Science ®Google Scholar
• Cruz-Guzmán ODR, Rodríguez-Cruz M, Escobar-Cedillo RE. Systemic inflammation in Duchenne Muscular Dystrophy: association with muscle function and nutritional status. Biomed Res Int. 2015;2015(3):891972–891977.
   PubMedGoogle Scholar
• John HA, Purdom IF. Elevated plasma levels of haptoglobin in Duchenne Muscular Dystrophy: electrophoretic variants in patients with a severe form of the disease. Electrophoresis. 1989;10(7):489–493.
   PubMed Web of Science ®Google Scholar
• Flanigan KM, Voit T, Rosales XQ, et al. Pharmacokinetics and safety of single doses of drisapersen in non-ambulant subjects with Duchenne Muscular Dystrophy: results of a double-blind randomized clinical trial. Neuromuscul Disord. 2014;24(1):16–24.
   PubMed Web of Science ®Google Scholar
• de Carvalho SC, Matsumura CY, Santo Neto H, et al. Identification of plasma interleukins as biomarkers for deflazacort and omega-3 based Duchenne Muscular Dystrophy therapy. Cytokine. 2018;102:55–61.
   PubMed Web of Science ®Google Scholar
• Dharnidharka VR, Kwon C, Stevens G. Serum cystatin C is superior to serum creatinine as a marker of kidney function: a meta-analysis. Am J Kidney Dis. 2002;40(2):221–226.
   PubMed Web of Science ®Google Scholar
• Viollet L, Gailey S, Thornton DJ, et al. Utility of cystatin C to monitor renal function in Duchenne Muscular Dystrophy. Muscle Nerve. 2009;40(3):438–442.
   PubMed Web of Science ®Google Scholar
• Strandberg K, Ayoglu B, Roos A, et al. Blood-derived biomarkers correlate with clinical progression in Duchenne Muscular Dystrophy. J Neuromuscul Dis. 2020;7(3).
   PubMedGoogle Scholar
• van der Burgt YEM. Protein biomarker discovery is still relevant and has entered a new phase. EBioMedicine. 2019;43:15.
   PubMed Web of Science ®Google Scholar
• Drucker E, Krapfenbauer K. Pitfalls and limitations in translation from biomarker discovery to clinical utility in predictive and personalised medicine. Epma J. 2013;4(1):7.
   PubMedGoogle Scholar
• Wilson JL, Altman RB. Biomarkers: delivering on the expectation of molecularly driven, quantitative health. Exp Biol Med (Maywood). 2018;243(3):313–322.
   PubMed Web of Science ®Google Scholar
• Rodrigues M, Yokota T. An overview of recent advances and clinical applications of exon skipping and splice modulation for muscular dystrophy and various genetic diseases. Methods Mol Biol. 1828;31–55:2018.
   Google Scholar
• Bushby K, Finkel R, Wong B, et al. Ataluren treatment of patients with nonsense mutation dystrophinopathy. Muscle Nerve. 2014;50(4):477–487.
   PubMed Web of Science ®Google Scholar
• Mora M, Angelini C, Bignami F, et al. The EuroBioBank network: 10 years of hands-on experience of collaborative, transnational biobanking for rare diseases. Eur J Hum Genet. 2015;23(9):1116–1123.
   PubMed Web of Science ®Google Scholar
• Graham C, Dawkins H, Terry S, et al. Current trends in biobanking for rare diseases: a review. BSAM. 2014;2:49–61.
   Google Scholar
• Gainotti S, Torreri P, Wang CM, et al. The RD-connect registry & biobank finder: a tool for sharing aggregated data and metadata among rare disease researchers. Eur J Hum Genet. 2018;26(5): 631–643.
   PubMed Web of Science ®Google Scholar
• Greco V, Piras C, Pieroni L, et al. Direct assessment of plasma/Serum sample quality for proteomics biomarker investigation. Methods Mol Biol. 2017;1619(3):3–21.
   PubMedGoogle Scholar
• Menezes MP, North KN. Inherited neuromuscular disorders: pathway to diagnosis. J Paediatr Child Health. 2012;48(6):458–465.
   PubMed Web of Science ®Google Scholar
• Deenen JCW, Arnts H, van der Maarel SM, et al. Population-based incidence and prevalence of facioscapulohumeral dystrophy. Neurology. 2014;83(12):1056–1059.
   PubMed Web of Science ®Google Scholar
• Gudde AEEG, González-Barriga A, van den Broek WJAA, et al. A low absolute number of expanded transcripts is involved in myotonic dystrophy type 1 manifestation in muscle. Hum Mol Genet. 2016;25(8):1648–1662.
   PubMed Web of Science ®Google Scholar
• Mahmood OA, Jiang XM. Limb-girdle muscular dystrophies: where next after six decades from the first proposal (Review). Mol Med Rep. 2014;9(5):1515–1532.
   PubMed Web of Science ®Google Scholar
• Bushby K. Report on the 12th ENMC sponsored international workshop–the “limb-girdle” muscular dystrophies. Neuromuscul Disord. 1992;2:3–5.
   PubMed Web of Science ®Google Scholar
• van der Kooi AJ, Barth PG, Busch HF, et al. The clinical spectrum of limb girdle muscular dystrophy. A survey in The Netherlands. Brain. 1996;119(Pt 5):1471–1480.
   PubMedGoogle Scholar
• Dunnen Den JT, Grootscholten PM, Bakker E, et al. Topography of the Duchenne Muscular Dystrophy (DMD) gene: FIGE and cDNA analysis of 194 cases reveals 115 deletions and 13 duplications. Am J Hum Genet. 1989;45(6):835–847.
   PubMed Web of Science ®Google Scholar
• Becker PE, Kiener F. A new x-chromosomal muscular dystrophy. Arch Psychiatr Nervenkr Z Gesamte Neurol Psychiatr. 1955;193(4):427–448.
   PubMedGoogle Scholar
• Burch PM, Pogoryelova O, Goldstein R, et al. Muscle-derived proteins as serum biomarkers for monitoring disease progression in three forms of muscular dystrophy. J Neuromuscul Dis. 2015;2(3):241–255.
   PubMedGoogle Scholar
• Ibrahim GA, Zweber BA, Awad EA. Muscle and serum enzymes and isoenzymes in muscular-dystrophies. Arch Phys Med Rehab. 1981;62(6):265–269.
   PubMed Web of Science ®Google Scholar
• Coenen-Stass AML, McClorey G, Manzano R, et al. Identification of novel, therapy-responsive protein biomarkers in a mouse model of Duchenne Muscular Dystrophy by aptamer-based serum proteomics. Sci Rep. 2015;5(1):e38–11.
   Google Scholar
• Aartsma-Rus A, Morgan J, Lonkar P, et al. Report of a TREAT-NMD/world duchenne organisation meeting on dystrophin quantification methodology. J Neuromuscul Dis. 2019;6(1):147–159.
   PubMedGoogle Scholar
• Gaasterland CMW, van der Weide MCJ, Du Prie-Olthof MJ, et al. The patient’s view on rare disease trial design - a qualitative study. Orphanet J Rare Dis. 2019;14(1):31–39.
   PubMedGoogle Scholar
• Verhaart IEC, T Hoen PAC, Roos M, et al. Meeting on data sharing for Duchenne 21–22 March 2019 Amsterdam, the Netherlands. Neuromuscul Disord. 2019;29(10):800–810.
   PubMed Web of Science ®Google Scholar
• Aartsma-Rus A, Ferlini A, McNally EM, et al. Workshop participants. 226th ENMC international workshop:: towards validated and qualified biomarkers for therapy development for Duchenne Muscular Dystrophy 20–22 January 2017, Heemskerk, The Netherlands. Neuromuscul Disord. 2018;28(1):77–86.
   PubMed Web of Science ®Google Scholar
• Zurriaga Ó, Martínez J, Corrochano V, et al. Rare disease registries and biobanks: A way forward. Arbor. 2018;194(789):469.
   Google Scholar