Serum protein biomarker signature of Duchenne muscular dystrophy
DOI:
https://doi.org/10.4081/ejtm.2025.13956Keywords:
Dystrophinopathy, liquid biopsy, muscle proteomics, myofibrosis, myonecrosisAbstract
In contrast to invasive skeletal muscle biopsies and the associated complexity of tissue sampling techniques and potential detrimental side effects, the alternative application of liquid biopsy procedures has considerable advantages concerning minimal invasiveness, repeated sampling options, assay robustness and cost effectiveness. This article outlines the current status of serum biomarkers used for diagnosing and characterizing Duchenne muscular dystrophy (DMD), a primary muscle wasting disease of early childhood due to primary abnormalities in the extremely large DMD gene. Reviewed are important aspects of the discovery, characterization and diagnostic value of biofluid-based protein markers of dystrophinopathy. This includes an overview of traditional general skeletal muscle damage markers, such as creatine kinase, myoglobin and lactate dehydrogenase, which have been used for many decades in clinical applications to evaluate patients with muscular weakness. In addition, this article outlines the biochemical identification of novel biomarker candidates focusing on the usage of mass spectrometry-based proteomic surveys to establish comprehensive profiles of protein alterations in dystrophinopathy. Pathoproteomic serum markers of myonecrosis with great potential for improved patient screening, differential diagnosis, stage-specific prognosis and therapeutic monitoring include specific isoforms of muscle-derived cytosolic proteins, such as carbonic anhydrase isoform CA3 and fatty acid binding protein FABP3, as well as sarcomeric proteins, including specific isoforms of myosin light chain, myosin binding protein, troponin, and myomesin, in addition to peptide fragments derived from the giant protein titin. Biofluid-associated marker proteins of reactive myofibrosis include the extracellular matrix proteins fibronectin, osteopontin, collagen and matrix-metalloproteinases.
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Feng LT, Chen ZN, Bian H. Skeletal muscle: molecular structure, myogenesis, biological functions, and diseases. MedComm (2020) 2024;5:e649. DOI: https://doi.org/10.1002/mco2.649
Duan D, Goemans N, Takeda S, et al. Duchenne muscular dystrophy. Nat Rev Dis Primers 2021;7:13. DOI: https://doi.org/10.1038/s41572-021-00248-3
Gambetta KE, McCulloch MA, Lal AK, et al. Diversity of dystrophin gene mutations and disease progression in a contemporary cohort of Duchenne muscular dystrophy. Pediatr Cardiol 2022;43:855-67. DOI: https://doi.org/10.1007/s00246-021-02797-6
Ohlendieck K, Matsumura K, Ionasescu VV, et al. Duchenne muscular dystrophy: deficiency of dystrophin-associated proteins in the sarcolemma. Neurology 1993;43:795-800. DOI: https://doi.org/10.1212/WNL.43.4.795
Grounds MD, Terrill JR, Al-Mshhdani BA, et al. Biomarkers for Duchenne muscular dystrophy: myonecrosis, inflammation and oxidative stress. Dis Model Mech 2020;13:dmm043638. DOI: https://doi.org/10.1242/dmm.043638
Dowling P, Swandulla D, Ohlendieck K. Cellular pathogenesis of Duchenne muscular dystrophy: progressive myofibre degeneration, chronic inflammation, reactive myofibrosis and satellite cell dysfunction. Eur J Transl Myol 2023;33:11856. DOI: https://doi.org/10.4081/ejtm.2023.11856
Ohlendieck K, Swandulla D. Complexity of skeletal muscle degeneration: multi-systems pathophysiology and organ crosstalk in dystrophinopathy. Pflugers Arch 2021;473:1813-39. DOI: https://doi.org/10.1007/s00424-021-02623-1
Mercuri E, Pane M, Cicala G, et al. Detecting early signs in Duchenne muscular dystrophy: comprehensive review and diagnostic implications. Front Pediatr 2023;11:1276144. DOI: https://doi.org/10.3389/fped.2023.1276144
Song Y, Xu HY, Xu K, et al. Clinical utilisation of multimodal quantitative magnetic resonance imaging in investigating muscular damage in Duchenne muscular dystrophy: a study on the association between gluteal muscle groups and motor function. Pediatr Radiol 2023;53:1648-58. DOI: https://doi.org/10.1007/s00247-023-05632-7
Zweyer M, Sabir H, Dowling P, et al. Histopathology of Duchenne muscular dystrophy in correlation with changes in proteomic biomarkers. Histol Histopathol 2022;37:101-16.
van Dommelen P, van Dijk O, de Wilde JA, Verkerk PH. Short developmental milestone risk assessment tool to identify Duchenne muscular dystrophy in primary care. Orphanet J Rare Dis 2024;19:192. DOI: https://doi.org/10.1186/s13023-024-03208-8
Benemei S, Gatto F, Boni L, Pane M. "If you cannot measure it, you cannot improve it". Outcome measures in Duchenne Muscular Dystrophy: current and future perspectives. Acta Neurol Belg 2025;125:1-12. Erratum in: Acta Neurol Belg 2024;124:1763. DOI: https://doi.org/10.1007/s13760-024-02600-2
Ohlendieck K. Proteomic identification of biomarkers of skeletal muscle disorders. Biomark Med 2013;7:169-86. DOI: https://doi.org/10.2217/bmm.12.96
Carp SJ, Barr AE, Barbe MF. Serum biomarkers as signals for risk and severity of work-related musculoskeletal injury. Biomark Med 2008;2:67-79. DOI: https://doi.org/10.2217/17520363.2.1.67
Brancaccio P, Lippi G, Maffulli N. Biochemical markers of muscular damage. Clin Chem Lab Med 2010;48:757-67. DOI: https://doi.org/10.1515/CCLM.2010.179
Goldstein RA. Skeletal muscle injury biomarkers: assay qualification efforts and translation to the clinic. Toxicol Pathol 2017;45:943-51. DOI: https://doi.org/10.1177/0192623317738927
Murphy S, Zweyer M, Mundegar RR, et al. Proteomic serum biomarkers for neuromuscular diseases. Expert Rev Proteomics 2018;15:277-91. DOI: https://doi.org/10.1080/14789450.2018.1429923
Ostrowski P, Bonczar M, Avram AE, et al. Safety monitoring of drug-induced muscle injury and rhabdomyolysis: a biomarker-guided approach for clinical practice and drug trials. Clin Chem Lab Med 2023;61:1688-99. DOI: https://doi.org/10.1515/cclm-2023-0313
Chemello F, Olson EN, Bassel-Duby R. CRISPR-editing therapy for duchenne muscular dystrophy. Hum Gene Ther 2023;34:379-87. DOI: https://doi.org/10.1089/hum.2023.053
Roberts TC, Wood MJA, Davies KE. Therapeutic approaches for Duchenne muscular dystrophy. Nat Rev Drug Discov 2023;22:917-34. DOI: https://doi.org/10.1038/s41573-023-00775-6
Patterson G, Conner H, Groneman M, et al. Duchenne muscular dystrophy: Current treatment and emerging exon skipping and gene therapy approach. Eur J Pharmacol 2023;947:175675. DOI: https://doi.org/10.1016/j.ejphar.2023.175675
McDonald C, Camino E, Escandon R, et al. Draft guidance for industry: Duchenne muscular dystrophy, Becker muscular dystrophy, and related dystrophinopathies - developing potential treatments for the entire spectrum of disease. J Neuromuscul Dis 2024;11:499-523. DOI: https://doi.org/10.3233/JND-230219
Saad FA, Saad JF, Siciliano G, et al. Duchenne muscular dystrophy gene therapy. Curr Gene Ther 2024;24:17-28. DOI: https://doi.org/10.2174/1566523223666221118160932
Dowling P, Swandulla D, Ohlendieck K. Mass spectrometry-based proteomic technology and its application to study skeletal muscle cell biology. Cells 2023;12:2560. DOI: https://doi.org/10.3390/cells12212560
Hathout Y. Proteomic methods for biomarker discovery and validation. Are we there yet? Expert Rev Proteomics 2015;12:329-31. DOI: https://doi.org/10.1586/14789450.2015.1064771
Dowling P, Trollet C, Negroni E, et al. How can proteomics help to elucidate the pathophysiological crosstalk in muscular dystrophy and associated multi-system dysfunction? Proteomes 2024;12:4. DOI: https://doi.org/10.3390/proteomes12010004
Adhit KK, Wanjari A, Menon S, K S. Liquid biopsy: an evolving paradigm for non-invasive disease diagnosis and monitoring in medicine. Cureus 2023;15:e50176. DOI: https://doi.org/10.7759/cureus.50176
O'Sullivan EM, Dowling P, Swandulla D, Ohlendieck K. Proteomic Identification of Saliva Proteins as Noninvasive Diagnostic Biomarkers. Methods Mol Biol 2023;2596:147-67. DOI: https://doi.org/10.1007/978-1-0716-2831-7_12
Csősz É, Kalló G, Márkus B, et al. Quantitative body fluid proteomics in medicine - A focus on minimal invasiveness. J Proteomics 2017;153:30-43. DOI: https://doi.org/10.1016/j.jprot.2016.08.009
Dayon L, Cominetti O, Affolter M. Proteomics of human biological fluids for biomarker discoveries: technical advances and recent applications. Expert Rev Proteomics 2022;19:131-51. DOI: https://doi.org/10.1080/14789450.2022.2070477
Bader JM, Albrecht V, Mann M. MS-based proteomics of body fluids: the end of the beginning. Mol Cell Proteomics 2023;22:100577. DOI: https://doi.org/10.1016/j.mcpro.2023.100577
Komaki H, Takeshita E, Kunitake K, et al. Phase 1/2 trial of brogidirsen: Dual-targeting antisense oligonucleotides for exon 44 skipping in Duchenne muscular dystrophy. Cell Rep Med 2025;6:101901. DOI: https://doi.org/10.1016/j.xcrm.2024.101901
Cabral BMI, Edding SN, Portocarrero JP, Lerma EV. Rhabdomyolysis. Dis Mon 2020;66:101015. DOI: https://doi.org/10.1016/j.disamonth.2020.101015
Muraine L, Bensalah M, Butler-Browne G, et al. Update on anti-fibrotic pharmacotherapies in skeletal muscle disease. Curr Opin Pharmacol 2023;68:102332. DOI: https://doi.org/10.1016/j.coph.2022.102332
Proud CM. 50 years ago in the Journal of Pediatrics: the use of serum creatine phosphokinase and other serum enzymes in the diagnosis of progressive muscular dystrophy. J Pediatr 2013;163:1656. DOI: https://doi.org/10.1016/j.jpeds.2013.06.015
Dowling P, Holland A, Ohlendieck K. Mass spectrometry-based identification of muscle-associated and muscle-derived proteomic biomarkers of dystrophinopathies. J Neuromuscul Dis. 2014;1(1):15-40. PMID: 27858666. DOI: https://doi.org/10.3233/JND-140011
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;39:1357-70. DOI: https://doi.org/10.3892/ijmm.2017.2952
Murphy S, Zweyer M, Mundegar RR, et al. Dataset on the comparative proteomic profiling of mouse saliva and serum from wild type versus the dystrophic mdx-4cv mouse model of dystrophinopathy. Data Brief 2018;21:1236-45. DOI: https://doi.org/10.1016/j.dib.2018.10.082
Deng YT, You J, He Y, et al. Atlas of the plasma proteome in health and disease in 53,026 adults. Cell 2025;188:253-271.e7. DOI: https://doi.org/10.1016/j.cell.2024.10.045
de Freitas Nakata KC, da Silva Pereira PP, Salgado Riveros B. Creatine kinase test diagnostic accuracy in neonatal screening for Duchenne Muscular Dystrophy: A systematic review. Clin Biochem 2021;98:1-9. DOI: https://doi.org/10.1016/j.clinbiochem.2021.09.010
Tang L, Pan M, Wu F. Diagnostic Accuracy of Creatine Kinase Isoenzyme-MM Test in Newborn Screening for Duchenne Muscular Dystrophy: A Systematic Review and Meta-Analysis. Pediatr Neurol 2024;153:84-91. DOI: https://doi.org/10.1016/j.pediatrneurol.2024.01.010
Kucera KS, Boyea BL, Migliore B, et al. Two years of newborn screening for Duchenne muscular dystrophy as a part of the statewide Early Check research program in North Carolina. Genet Med 2024;26:101009. DOI: https://doi.org/10.1016/j.gim.2023.101009
Brancaccio P, Maffulli N, Limongelli FM. Creatine kinase monitoring in sport medicine. Br Med Bull 2007;81-82:209-30. DOI: https://doi.org/10.1093/bmb/ldm014
Burlo F, Grigoletto V, Pastore S, et al. Elevated creatine kinase is mainly harmless in children but persistent and severe hyperCKaemia should raise suspicions of serious muscle damage. Acta Paediatr 2023;112:1592-3. DOI: https://doi.org/10.1111/apa.16755
Fechner A, Willenberg A, Ziegelasch N, et al. Creatine kinase serum levels in children revisited: New reference intervals from a large cohort of healthy children and adolescents. Clin Chim Acta 2024;560:119726. DOI: https://doi.org/10.1016/j.cca.2024.119726
Hendgen-Cotta UB, Flögel U, Kelm M, Rassaf T. Unmasking the Janus face of myoglobin in health and disease. J Exp Biol 2010;213:2734-40. DOI: https://doi.org/10.1242/jeb.041178
Ordway GA, Garry DJ. Myoglobin: an essential hemoprotein in striated muscle. J Exp Biol 2004;207:3441-6. DOI: https://doi.org/10.1242/jeb.01172
Adepu KK, Anishkin A, Adams SH, Chintapalli SV. A versatile delivery vehicle for cellular oxygen and fuels or metabolic sensor? A review and perspective on the functions of myoglobin. Physiol Rev 2024;104:1611-42. DOI: https://doi.org/10.1152/physrev.00031.2023
Dowling P, Gargan S, Zweyer M, et al. Proteomic profiling of carbonic anhydrase CA3 in skeletal muscle. Expert Rev Proteomics 2021;18:1073-86. DOI: https://doi.org/10.1080/14789450.2021.2017776
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;23:6458-69. DOI: https://doi.org/10.1093/hmg/ddu366
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;6:918-36. DOI: https://doi.org/10.15252/emmm.201303724
Hathout Y, Brody E, Clemens PR, et al. Large-scale serum protein biomarker discovery in Duchenne muscular dystrophy. Proc Natl Acad Sci U S A 2015;112:7153-8. DOI: https://doi.org/10.1073/pnas.1507719112
Maughan DW, Henkin JA, Vigoreaux JO. Concentrations of glycolytic enzymes and other cytosolic proteins in the diffusible fraction of a vertebrate muscle proteome. Mol Cell Proteomics 2005;4:1541-9. DOI: https://doi.org/10.1074/mcp.M500053-MCP200
Ohlendieck K. Proteomics of skeletal muscle glycolysis. Biochim Biophys Acta 2010;1804:2089-101. DOI: https://doi.org/10.1016/j.bbapap.2010.08.001
Dowling P, Gargan S, Swandulla D, Ohlendieck K. Identification of Subproteomic Markers for Skeletal Muscle Profiling. Methods Mol Biol 2023;2596:291-302. DOI: https://doi.org/10.1007/978-1-0716-2831-7_20
Anderson NL, Anderson NG. The human plasma proteome: history, character, and diagnostic prospects. Mol Cell Proteomics 2002;1:845-67. Erratum in: Mol Cell Proteomics 2003;2:50. DOI: https://doi.org/10.1074/mcp.A300001-MCP200
Seay AR, Ziter FA, Wu LH, Wu JT. Serum creatine phosphokinase and pyruvate kinase in neuromuscular disorders and Duchenne dystrophy carriers. Neurology 1978;28:1047-50. DOI: https://doi.org/10.1212/WNL.28.10.1047
Yasmineh WG, Ibrahim GA, Abbasnezhad M, Awad EA. 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;24:1985-9. DOI: https://doi.org/10.1093/clinchem/24.11.1985
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;102:190-6. DOI: https://doi.org/10.1016/0022-510X(91)90068-I
Capitanio D, Moriggi M, Torretta E, et al. Comparative proteomic analyses of Duchenne muscular dystrophy and Becker muscular dystrophy muscles: changes contributing to preserve muscle function in Becker muscular dystrophy patients. J Cachexia Sarcopenia Muscle 2020;11:547-63. DOI: https://doi.org/10.1002/jcsm.12527
da Silva JCT, Nogueira MRA, da Silva YM, et al. Label-free proteomic analysis of Duchenne and Becker muscular dystrophy showed decreased sarcomere proteins and increased ubiquitination-related proteins. Sci Rep 2025;15:3293. DOI: https://doi.org/10.1038/s41598-025-87995-5
Holland A, Carberry S, Ohlendieck K. Proteomics of the dystrophin-glycoprotein complex and dystrophinopathy. Curr Protein Pept Sci 2013;14:680-97. DOI: https://doi.org/10.2174/13892037113146660083
Carberry S, Brinkmeier H, Zhang Y, et al. Comparative proteomic profiling of soleus, extensor digitorum longus, flexor digitorum brevis and interosseus muscles from the mdx mouse model of Duchenne muscular dystrophy. Int J Mol Med 2013;32:544-56. DOI: https://doi.org/10.3892/ijmm.2013.1429
Holland A, Henry M, Meleady P, et al. Comparative label-free mass spectrometric analysis of mildly versus severely affected mdx mouse skeletal muscles identifies annexin, lamin, and vimentin as universal dystrophic markers. Molecules 2015;20:11317-44. DOI: https://doi.org/10.3390/molecules200611317
Carr SJ, Zahedi RP, Lochmüller H, Roos A. Mass spectrometry-based protein analysis to unravel the tissue pathophysiology in Duchenne muscular dystrophy. Proteomics Clin Appl 2018;12:71. DOI: https://doi.org/10.1002/prca.201700071
Dowling P, Murphy S, Zweyer M, et al. Emerging proteomic biomarkers of X-linked muscular dystrophy. Expert Rev Mol Diagn 2019;19:739-55. DOI: https://doi.org/10.1080/14737159.2019.1648214
Gargan S, Dowling P, Zweyer M, et al. Proteomic identification of markers of membrane repair, regeneration and fibrosis in the aged and dystrophic diaphragm. Life (Basel) 2022;12:1679. DOI: https://doi.org/10.3390/life12111679
Murphy S, Ohlendieck K. The biochemical and mass spectrometric profiling of the dystrophin complexome from skeletal muscle. Comput Struct Biotechnol J 2015;14:20-7. DOI: https://doi.org/10.1016/j.csbj.2015.11.002
Dowling P, Gargan S, Murphy S, et al. The dystrophin node as integrator of cytoskeletal organization, lateral force transmission, fiber stability and cellular signaling in skeletal muscle. Proteomes 2021;9:9. DOI: https://doi.org/10.3390/proteomes9010009
Dowling P, Gargan S, Swandulla D, Ohlendieck K. Proteomic profiling of impaired excitation-contraction coupling and abnormal calcium handling in muscular dystrophy. Proteomics 2022;22:e2200003. DOI: https://doi.org/10.1002/pmic.202200003
Cynthia Martin F, Hiller M, Spitali P, et al. Fibronectin is a serum biomarker for Duchenne muscular dystrophy. Proteomics Clin Appl 2014;8:269-78. DOI: https://doi.org/10.1002/prca.201300072
Hathout Y, Seol H, Han MH, et al. Clinical utility of serum biomarkers in Duchenne muscular dystrophy. Clin Proteomics 2016;13:9. DOI: https://doi.org/10.1186/s12014-016-9109-x
Hathout Y, Conklin LS, Seol H, et al. Serum pharmacodynamic biomarkers for chronic corticosteroid treatment of children. Sci Rep 2016;6:31727. DOI: https://doi.org/10.1038/srep31727
Guiraud S, Edwards B, Squire SE, et al. Identification of serum protein biomarkers for utrophin based DMD therapy. Sci Rep 2017;7:43697. DOI: https://doi.org/10.1038/srep43697
Spitali P, Hettne K, Tsonaka R, et al. Tracking disease progression non-invasively in Duchenne and Becker muscular dystrophies. J Cachexia Sarcopenia Muscle 2018;9:715-26. DOI: https://doi.org/10.1002/jcsm.12304
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 2020;11:505-17. DOI: https://doi.org/10.1002/jcsm.12517
Hathout Y, Liang C, Ogundele M, et al. Disease-specific and glucocorticoid-responsive serum biomarkers for Duchenne Muscular Dystrophy. Sci Rep 2019;9:12167. DOI: https://doi.org/10.1038/s41598-019-48548-9
Alayi TD, Tawalbeh SM, Ogundele M, et al. Tandem mass tag-based serum proteome profiling for biomarker discovery in young duchenne muscular dystrophy boys. ACS Omega 2020;5:26504-17. DOI: https://doi.org/10.1021/acsomega.0c03206
Johansson C, Hunt H, Signorelli M, et al. Orthogonal proteomics methods warrant the development of Duchenne muscular dystrophy biomarkers. Clin Proteomics 2023;20:23. DOI: https://doi.org/10.1186/s12014-023-09412-1
Al-Khalili Szigyarto C. Duchenne Muscular Dystrophy: recent advances in protein biomarkers and the clinical application. Expert Rev Proteomics 2020;17:365-75. DOI: https://doi.org/10.1080/14789450.2020.1773806
Fortunato F, Ferlini A. Biomarkers in duchenne muscular dystrophy: current status and future directions. J Neuromuscul Dis 2023;10:987-1002. DOI: https://doi.org/10.3233/JND-221666
Willis AB, Zelikovich AS, Sufit R, et al. Serum protein and imaging biomarkers after intermittent steroid treatment in muscular dystrophy. Sci Rep 2024;14:28745. DOI: https://doi.org/10.1038/s41598-024-79024-8
Strandberg K, Ayoglu B, Roos A, et al. Blood-derived biomarkers correlate with clinical progression in Duchenne muscular dystrophy. J Neuromuscul Dis 2020;7:231-46. DOI: https://doi.org/10.3233/JND-190454
Dowling P, Gargan S, Zweyer M, et al. Proteomic profiling of fatty acid binding proteins in muscular dystrophy. Expert Rev Proteomics 2020;17:137-48. DOI: https://doi.org/10.1080/14789450.2020.1732214
Gargan S, Dowling P, Zweyer M, et al. Identification of marker proteins of muscular dystrophy in the urine proteome from the mdx-4cv model of dystrophinopathy. Mol Omics 2020;1:268-78. DOI: https://doi.org/10.1039/C9MO00182D
Ishii MN, Nakashima M, Kamiguchi H, et al. Urine titin as a novel biomarker for Duchenne muscular dystrophy. Neuromuscul Disord 2023;33:302-8. DOI: https://doi.org/10.1016/j.nmd.2023.02.003
Hiramuki Y, Hosokawa M, Osawa K, et al. Titin fragment is a sensitive biomarker in Duchenne muscular dystrophy model mice carrying full-length human dystrophin gene on human artificial chromosome. Sci Rep 2025;15:1778. DOI: https://doi.org/10.1038/s41598-025-85369-5
Riddell DO, Hildyard JCW, Harron RCM, et al. Serum inflammatory cytokines as disease biomarkers in the DE50-MD dog model of Duchenne muscular dystrophy. Dis Model Mech 2022;15:dmm049394. DOI: https://doi.org/10.1242/dmm.049394
Pérez-López DO, Burke MJ, Hakim CH, et al. Circulatory CCL2 distinguishes Duchenne muscular dystrophy dogs. Dis Model Mech 2025;18:dmm052137. DOI: https://doi.org/10.1242/dmm.052137
Crowe KE, Shao G, Flanigan KM, Martin PT. N-terminal α Dystroglycan (αDG-N): A Potential Serum Biomarker for Duchenne Muscular Dystrophy. J Neuromuscul Dis 2016;3:247-60. DOI: https://doi.org/10.3233/JND-150127
Ikelaar NA, Barnard AM, Eng SWM, et al. Large scale serum proteomics identifies proteins associated with performance decline and clinical milestones in Duchenne muscular dystrophy. medRxiv 2024. doi: 10.1101/2024.08.05.24311516. DOI: https://doi.org/10.1101/2024.08.05.24311516
Mokuno K, Riku S, Matsuoka Y, et al. Serum carbonic anhydrase III in progressive muscular dystrophy. J Neurol Sci 1985;67:223-8. DOI: https://doi.org/10.1016/0022-510X(85)90118-2
Väänänen HK, Takala TE, Tolonen U, et al. Muscle-specific carbonic anhydrase III is a more sensitive marker of muscle damage than creatine kinase in neuromuscular disorders. Arch Neurol 1988;45:1254-6. DOI: https://doi.org/10.1001/archneur.1988.00520350092022
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;37:36-9. DOI: https://doi.org/10.1093/clinchem/37.1.36
Schiaffino S, Reggiani C. Fiber types in mammalian skeletal muscles. Physiol Rev 2011;91:1447-531. DOI: https://doi.org/10.1152/physrev.00031.2010
Schiaffino S. Muscle fiber type diversity revealed by anti-myosin heavy chain antibodies. FEBS J 2018;285:3688-94. DOI: https://doi.org/10.1111/febs.14502
Ciciliot S, Rossi AC, Dyar KA, et al. Muscle type and fiber type specificity in muscle wasting. Int J Biochem Cell Biol 2013;45:2191-9. DOI: https://doi.org/10.1016/j.biocel.2013.05.016
Dowling P, Murphy S, Ohlendieck K. Proteomic profiling of muscle fibre type shifting in neuromuscular diseases. Expert Rev Proteomics 2016;13:783-99. DOI: https://doi.org/10.1080/14789450.2016.1209416
Murphy S, Zweyer M, Henry M, et al. Proteomic profiling of liver tissue from the mdx-4cv mouse model of Duchenne muscular dystrophy. Clin Proteomics 2018;15:34. DOI: https://doi.org/10.1186/s12014-018-9212-2
Dowling P, Zweyer M, Raucamp M, et al. Dataset on the mass spectrometry-based proteomic profiling of the kidney from wild type and the dystrophic mdx-4cv mouse model of X-linked muscular dystrophy. Data Brief 2020;28:105067. DOI: https://doi.org/10.1016/j.dib.2019.105067
Dowling P, Zweyer M, Raucamp M, et al. Proteomic and cell biological profiling of the renal phenotype of the mdx-4cv mouse model of Duchenne muscular dystrophy. Eur J Cell Biol 2020;99:151059. DOI: https://doi.org/10.1016/j.ejcb.2019.151059
Dowling P, Gargan S, Zweyer M, et al. Proteomic profiling of the interface between the stomach wall and the pancreas in dystrophinopathy. Eur J Transl Myol 2021;31:9627. DOI: https://doi.org/10.4081/ejtm.2020.9627
Dowling P, Gargan S, Zweyer M, et al. Proteome-wide changes in the mdx-4cv spleen due to pathophysiological cross talk with dystrophin-deficient skeletal muscle. iScience 2020;23:101500. DOI: https://doi.org/10.1016/j.isci.2020.101500
Dowling P, Gargan S, Zweyer M, et al. Protocol for the bottom-up proteomic analysis of mouse spleen. STAR Protoc 2020;1:100196. DOI: https://doi.org/10.1016/j.xpro.2020.100196
Holland A, Ohlendieck K. Proteomic profiling of the contractile apparatus from skeletal muscle. Expert Rev Proteomics 2013;10:239-57. DOI: https://doi.org/10.1586/epr.13.20
Dowling P, Gargan S, Swandulla D, Ohlendieck K. Fiber-type shifting in sarcopenia of old age: proteomic profiling of the contractile apparatus of skeletal muscles. Int J Mol Sci 2023;24:2415. DOI: https://doi.org/10.3390/ijms24032415
Murphy S, Dowling P, Zweyer M, et al. Proteomic profiling of giant skeletal muscle proteins. Expert Rev Proteomics 2019;16:241-56. DOI: https://doi.org/10.1080/14789450.2019.1575205
Linke WA. Stretching the story of titin and muscle function. J Biomech 2023;152:111553. DOI: https://doi.org/10.1016/j.jbiomech.2023.111553
Rouillon J, Zocevic A, Leger T, et al. Proteomics profiling of urine reveals specific titin fragments as biomarkers of Duchenne muscular dystrophy. Neuromuscul Disord 2014;24:563-73. DOI: https://doi.org/10.1016/j.nmd.2014.03.012
Yamaguchi H, Awano H, Yamamoto T, et al. Serum cardiac troponin I is a candidate biomarker for cardiomyopathy in Duchenne and Becker muscular dystrophies. Muscle Nerve 2022;65:521-30. DOI: https://doi.org/10.1002/mus.27522
Soslow JH, Xu M, Slaughter JC, et al. Cardiovascular measures of all-cause mortality in duchenne muscular dystrophy. Circ Heart Fail 2023;16:e010040. DOI: https://doi.org/10.1161/CIRCHEARTFAILURE.122.010040
Anderson J, Seol H, Gordish-Dressman H, et al. CINRG Investigators. Interleukin 1 Receptor-Like 1 Protein (ST2) is a Potential Biomarker for Cardiomyopathy in Duchenne Muscular Dystrophy. Pediatr Cardiol 2017;38:1606-12. DOI: https://doi.org/10.1007/s00246-017-1703-9
Brinkmeier H, Ohlendieck K. Chaperoning heat shock proteins: proteomic analysis and relevance for normal and dystrophin-deficient muscle. Proteomics Clin Appl 2014;8:875-95. DOI: https://doi.org/10.1002/prca.201400015
Doran P, Martin G, Dowling P, et al. Proteome analysis of the dystrophin-deficient MDX diaphragm reveals a drastic increase in the heat shock protein cvHSP. Proteomics 2006;6:4610-21. DOI: https://doi.org/10.1002/pmic.200600082
Doran P, Wilton SD, Fletcher S, Ohlendieck K. Proteomic profiling of antisense-induced exon skipping reveals reversal of pathobiochemical abnormalities in dystrophic mdx diaphragm. Proteomics 2009;9:671-85. DOI: https://doi.org/10.1002/pmic.200800441
Csapo R, Gumpenberger M, Wessner B. Skeletal muscle extracellular matrix - what do we know about its composition, regulation, and physiological roles? A narrative review. Front Physiol 2020;11:253. DOI: https://doi.org/10.3389/fphys.2020.00253
Halper J. Basic components of connective tissues and extracellular matrix: fibronectin, fibrinogen, laminin, elastin, fibrillins, fibulins, matrilins, tenascins and thrombospondins. Adv Exp Med Biol 2021;1348:105-26. DOI: https://doi.org/10.1007/978-3-030-80614-9_4
Zhang W, Liu Y, Zhang H. Extracellular matrix: an important regulator of cell functions and skeletal muscle development. Cell Biosci 2021;11:65. DOI: https://doi.org/10.1186/s13578-021-00579-4
Murphy S, Brinkmeier H, Krautwald M, et al. Proteomic profiling of the dystrophin complex and membrane fraction from dystrophic mdx muscle reveals decreases in the cytolinker desmoglein and increases in the extracellular matrix stabilizers biglycan and fibronectin. J Muscle Res Cell Motil 2017;38:251-68. DOI: https://doi.org/10.1007/s10974-017-9478-4
Holland A, Dowling P, Meleady P, et al. Label-free mass spectrometric analysis of the mdx-4cv diaphragm identifies the matricellular protein periostin as a potential factor involved in dystrophinopathy-related fibrosis. Proteomics 2015;15:2318-31. DOI: https://doi.org/10.1002/pmic.201400471
Holland A, Murphy S, Dowling P, Ohlendieck K. Pathoproteomic profiling of the skeletal muscle matrisome in dystrophinopathy associated myofibrosis. Proteomics 2016;16:345-66. DOI: https://doi.org/10.1002/pmic.201500158
Ohlendieck K, Swandulla D. Molekulare Pathogenese der Fibrose bei Muskeldystrophie vom Typ Duchenne [Molecular pathogenesis of Duchenne muscular dystrophy-related fibrosis]. Pathologe 2017;38:21-9. German. DOI: https://doi.org/10.1007/s00292-017-0265-1
Dowling P, Gargan S, Zweyer M, et al. Extracellular matrix proteomics: The mdx-4cv mouse diaphragm as a surrogate for studying myofibrosis in dystrophinopathy. Biomolecules 2023;13:1108. DOI: https://doi.org/10.3390/biom13071108
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;7:17888. DOI: https://doi.org/10.1038/s41598-017-17982-y
Kuraoka M, Kimura E, Nagata T, et al. Serum osteopontin as a novel biomarker for muscle regeneration in duchenne muscular dystrophy. Am J Pathol 2016;186:1302-12. DOI: https://doi.org/10.1016/j.ajpath.2016.01.002
Taglietti V, Kefi K, Bronisz-Budzyńska I, et al. Duchenne muscular dystrophy trajectory in R-DMDdel52 preclinical rat model identifies COMP as biomarker of fibrosis. Acta Neuropathol Commun 2022;10:60. DOI: https://doi.org/10.1186/s40478-022-01355-2
McDonald CM, Signorovitch J, Mercuri E, et al. Functional trajectories before and after loss of ambulation in Duchenne muscular dystrophy and implications for clinical trials. PLoS One 2024;19:e0304099. DOI: https://doi.org/10.1371/journal.pone.0304099
Schiava M, McDermott MP, Broomfield J, et al. Factors associated with early motor function trajectories in DMD after glucocorticoid initiation: post hoc analysis of the FOR-DMD Trial. Neurology 2024;102:e209206. DOI: https://doi.org/10.1212/WNL.0000000000209206
Stimpson G, Ridout D, Wolfe A, et al. Quantifying variability in motor function in duchenne muscular dystrophy: UK Centiles for the NorthStar Ambulatory Assessment, 10 m walk run velocity and rise from floor velocity in GC treated boys. J Neuromuscul Dis 2024;11:153-66. DOI: https://doi.org/10.3233/JND-230159
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