{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,21]],"date-time":"2026-05-21T05:07:39Z","timestamp":1779340059367,"version":"3.51.4"},"reference-count":63,"publisher":"Wiley","license":[{"start":{"date-parts":[[2026,5,20]],"date-time":"2026-05-20T00:00:00Z","timestamp":1779235200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,5,20]],"date-time":"2026-05-20T00:00:00Z","timestamp":1779235200000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/100012644","name":"Friends of FSH Research","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100012644","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Ann Clin Transl Neurol"],"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Objective<\/jats:title>\n                    <jats:p>Facioscapulohumeral muscular dystrophy (FSHD) is one of the most debilitating and common muscular dystrophies. Despite its severity, no approved therapy exists for FSHD patients. However, several therapeutic candidates are currently under development, and some have recently entered clinical trials, marking the need for reliable biomarkers and outcome measures to monitor disease progression and treatment response in FSHD. To date, clinicians have relied primarily on validated functional and patient\u2010reported outcome measures, while circulating molecular biomarkers remain unvalidated.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>Here, we investigated the plasma extracellular vesicle (EV) proteome to identify protein biomarkers that could be more reliably and conveniently used for FSHD prognosis, patient stratification for clinical trials and treatment response. In this study, we searched for EV protein biomarkers using plasma from 45 FSHD1 patients and 28 healthy controls distributed across two independent cohorts.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      Using integrated, batch\u2010corrected mass spectrometry analyses, we identified Lumican (LUM), along with several complement and extracellular matrix\u2013associated proteins, as consistently upregulated EV proteins in FSHD. Additionally, LUM levels correlated with disease severity (FSHD\u2010COM score; sex\u2010adjusted Partial Pearson\n                      <jats:italic>R<\/jats:italic>\n                      : 0.454,\n                      <jats:italic>p<\/jats:italic>\n                      : 0.039) and other continuous clinical outcome measures (self\u2010selected gait speed time; Pearson\n                      <jats:italic>R<\/jats:italic>\n                      : \u22120.485,\n                      <jats:italic>p<\/jats:italic>\n                      : 0.022 and timed up and go; Pearson\n                      <jats:italic>R<\/jats:italic>\n                      : 0.463,\n                      <jats:italic>p<\/jats:italic>\n                      : 0.034).\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Interpretation<\/jats:title>\n                    <jats:p>Our findings demonstrate that profiling circulating EV content in FSHD plasma can reveal EV protein biomarkers that warrant further validation in larger cohorts to assess their potential clinical relevance as minimally invasive surrogate molecular biomarkers for FSHD.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1002\/acn3.70435","type":"journal-article","created":{"date-parts":[[2026,5,21]],"date-time":"2026-05-21T04:16:05Z","timestamp":1779336965000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Plasma\n                    <scp>EV<\/scp>\n                    Proteomics Identifies\n                    <scp>ECM<\/scp>\n                    Remodeling and Inflammatory Proteins\n                    <scp>LUM<\/scp>\n                    and\n                    <scp>C7<\/scp>\n                    as Candidate Biomarkers in\n                    <scp>FSHD<\/scp>"],"prefix":"10.1002","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3935-0302","authenticated-orcid":false,"given":"Mustafa Bilal","family":"Bayazit","sequence":"first","affiliation":[{"name":"Jerry R. Mendell Center for Gene Therapy Abigail Wexner Research Institute at Nationwide Children's Hospital  Columbus Ohio USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chiranth K.","family":"Nagaraj","sequence":"additional","affiliation":[{"name":"William G. Lowrie Department of Chemical and Biomolecular Engineering The Ohio State University  Columbus Ohio USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jackson S.","family":"Newell","sequence":"additional","affiliation":[{"name":"Jerry R. Mendell Center for Gene Therapy Abigail Wexner Research Institute at Nationwide Children's Hospital  Columbus Ohio USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kim Truc","family":"Nguyen","sequence":"additional","affiliation":[{"name":"William G. Lowrie Department of Chemical and Biomolecular Engineering The Ohio State University  Columbus Ohio USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xilal Y.","family":"Rima","sequence":"additional","affiliation":[{"name":"William G. Lowrie Department of Chemical and Biomolecular Engineering The Ohio State University  Columbus Ohio USA"},{"name":"Diabetes and Metabolism Research Center The Ohio State University Wexner Medical Center  Columbus Ohio USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jacob","family":"Doon\u2010Ralls","sequence":"additional","affiliation":[{"name":"William G. Lowrie Department of Chemical and Biomolecular Engineering The Ohio State University  Columbus Ohio USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Eduardo","family":"Re\u00e1tegui","sequence":"additional","affiliation":[{"name":"William G. Lowrie Department of Chemical and Biomolecular Engineering The Ohio State University  Columbus Ohio USA"},{"name":"Comprehensive Cancer Center The Ohio State University  Columbus Ohio USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jeffrey M.","family":"Statland","sequence":"additional","affiliation":[{"name":"Department of Neurology University of Kansas Medical Center  Kansas City KA USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1394-1494","authenticated-orcid":false,"given":"Rabi","family":"Tawil","sequence":"additional","affiliation":[{"name":"Department of Neurology University of Rochester Medical Center  Rochester New York USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6440-3376","authenticated-orcid":false,"given":"Kevin M.","family":"Flanigan","sequence":"additional","affiliation":[{"name":"Jerry R. Mendell Center for Gene Therapy Abigail Wexner Research Institute at Nationwide Children's Hospital  Columbus Ohio USA"},{"name":"Department of Pediatrics The Ohio State University College of Medicine  Columbus Ohio USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5135-4317","authenticated-orcid":false,"given":"Scott Q.","family":"Harper","sequence":"additional","affiliation":[{"name":"Jerry R. Mendell Center for Gene Therapy Abigail Wexner Research Institute at Nationwide Children's Hospital  Columbus Ohio USA"},{"name":"Department of Pediatrics The Ohio State University College of Medicine  Columbus Ohio USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5453-1152","authenticated-orcid":false,"given":"Nizar Y.","family":"Saad","sequence":"additional","affiliation":[{"name":"Jerry R. Mendell Center for Gene Therapy Abigail Wexner Research Institute at Nationwide Children's Hospital  Columbus Ohio USA"},{"name":"Department of Pediatrics The Ohio State University College of Medicine  Columbus Ohio USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"311","published-online":{"date-parts":[[2026,5,20]]},"reference":[{"key":"e_1_2_10_2_1","doi-asserted-by":"crossref","first-page":"1662","DOI":"10.1212\/CON.0000000000000801","article-title":"Facioscapulohumeral Muscular Dystrophies","volume":"25","author":"Wagner K. R.","year":"2019","journal-title":"Continuum (Minneapolis, Minn)"},{"key":"e_1_2_10_3_1","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1016\/j.molmed.2011.01.001","article-title":"Facioscapulohumeral Muscular Dystrophy and DUX4: Breaking the Silence","volume":"17","author":"Maarel S. M.","year":"2011","journal-title":"Trends in Molecular Medicine"},{"key":"e_1_2_10_4_1","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1186\/s13395-025-00388-0","article-title":"DUX4 at 25: How It Emerged From \u2018Junk DNA\u2019 to Become the Cause of Facioscapulohumeral Muscular Dystrophy","volume":"15","author":"Belayew A.","year":"2025","journal-title":"Skeletal Muscle"},{"key":"e_1_2_10_5_1","doi-asserted-by":"crossref","first-page":"16957","DOI":"10.1038\/s41598-018-35150-8","article-title":"Low Level DUX4 Expression Disrupts Myogenesis Through Deregulation of Myogenic Gene Expression","volume":"8","author":"Bosnakovski D.","year":"2018","journal-title":"Scientific Reports"},{"key":"e_1_2_10_6_1","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1016\/j.freeradbiomed.2016.08.007","article-title":"DUX4\u2010Induced Constitutive DNA Damage and Oxidative Stress Contribute to Aberrant Differentiation of Myoblasts From FSHD Patients","volume":"99","author":"Dmitriev P.","year":"2016","journal-title":"Free Radical Biology & Medicine"},{"key":"e_1_2_10_7_1","doi-asserted-by":"crossref","first-page":"4","DOI":"10.7554\/eLife.04996","article-title":"A Feedback Loop Between Nonsense\u2010Mediated Decay and the Retrogene DUX4 in Facioscapulohumeral Muscular Dystrophy","volume":"4","author":"Feng Q.","year":"2015","journal-title":"eLife"},{"key":"e_1_2_10_8_1","doi-asserted-by":"crossref","first-page":"5901","DOI":"10.1093\/hmg\/ddv315","article-title":"Endogenous DUX4 Expression in FSHD Myotubes Is Sufficient to Cause Cell Death and Disrupts RNA Splicing and Cell Migration Pathways","volume":"24","author":"Rickard A. M.","year":"2015","journal-title":"Human Molecular Genetics"},{"key":"e_1_2_10_9_1","doi-asserted-by":"crossref","first-page":"2644","DOI":"10.1002\/1873-3468.14416","article-title":"The DUX4 Protein Is a Co\u2010Repressor of the Progesterone and Glucocorticoid Nuclear Receptors","volume":"596","author":"Quintero J.","year":"2022","journal-title":"FEBS Letters"},{"key":"e_1_2_10_10_1","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1002\/ana.26668","article-title":"Post\u2010Translational Modifications of the DUX4 Protein Impact Toxic Function in FSHD Cell Models","volume":"94","author":"Knox R. N.","year":"2023","journal-title":"Annals of Neurology"},{"key":"e_1_2_10_11_1","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0026820","article-title":"The FSHD Atrophic Myotube Phenotype Is Caused by DUX4 Expression","volume":"6","author":"Vanderplanck C.","year":"2011","journal-title":"PLoS One"},{"key":"e_1_2_10_12_1","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1002\/ana.22275","article-title":"DUX4, a Candidate Gene for Facioscapulohumeral Muscular Dystrophy, Causes p53\u2010Dependent Myopathy in Vivo","volume":"69","author":"Wallace L. M.","year":"2011","journal-title":"Annals of Neurology"},{"key":"e_1_2_10_13_1","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1038\/s41582-022-00762-2","article-title":"Facioscapulohumeral Muscular Dystrophy: The Road to Targeted Therapies","volume":"19","author":"Tihaya M. S.","year":"2023","journal-title":"Nature Reviews. Neurology"},{"key":"e_1_2_10_14_1","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.omtm.2017.12.005","article-title":"Pre\u2010Clinical Safety and Off\u2010Target Studies to Support Translation of AAV\u2010Mediated RNAi Therapy for FSHD","volume":"8","author":"Wallace L. M.","year":"2018","journal-title":"Mol Ther Methods Clin Dev"},{"key":"e_1_2_10_15_1","doi-asserted-by":"crossref","DOI":"10.1038\/s41467-021-27430-1","article-title":"Human miRNA miR\u2010675 Inhibits DUX4 Expression and May Be Exploited as a Potential Treatment for Facioscapulohumeral Muscular Dystrophy","volume":"12","author":"Saad N. Y.","year":"2021","journal-title":"Nature Communications"},{"key":"e_1_2_10_16_1","article-title":"Oligonucleotide Therapies for Facioscapulohumeral Muscular Dystrophy: Current Preclinical Landscape","volume":"25","author":"Beck S. L.","year":"2024","journal-title":"International Journal of Molecular Sciences"},{"key":"e_1_2_10_17_1","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1038\/s41419-025-07827-2","article-title":"Estrogen Rescues Muscle Regeneration Impaired by DUX4 in a Humanized Xenograft Mouse Model","volume":"16","author":"Maiullari S.","year":"2025","journal-title":"Cell Death & Disease"},{"key":"e_1_2_10_18_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.omtm.2025.101513","article-title":"A Systemically Deliverable Lipid\u2010Conjugated siRNA Targeting DUX4 as an Facioscapulohumeral Muscular Dystrophy Therapeutic","volume":"33","author":"Daman K.","year":"2025","journal-title":"Mol Ther Methods Clin Dev"},{"key":"e_1_2_10_19_1","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1111\/j.1582-4934.2012.01647.x","article-title":"DUX4 Expression in FSHD Muscle Cells: How Could Such a Rare Protein Cause a Myopathy?","volume":"17","author":"Tassin A.","year":"2013","journal-title":"Journal of Cellular and Molecular Medicine"},{"key":"e_1_2_10_20_1","doi-asserted-by":"crossref","first-page":"476","DOI":"10.1093\/hmg\/ddy364","article-title":"MRI\u2010Informed Muscle Biopsies Correlate MRI With Pathology and DUX4 Target Gene Expression in FSHD","volume":"28","author":"Wang L. H.","year":"2019","journal-title":"Human Molecular Genetics"},{"key":"e_1_2_10_21_1","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1016\/j.nmd.2016.04.012","article-title":"A Cross Sectional Study of Two Independent Cohorts Identifies Serum Biomarkers for Facioscapulohumeral Muscular Dystrophy (FSHD)","volume":"26","author":"Petek L. M.","year":"2016","journal-title":"Neuromuscular Disorders"},{"key":"e_1_2_10_22_1","doi-asserted-by":"crossref","first-page":"1821","DOI":"10.1093\/hmg\/ddab364","article-title":"Elevated Plasma Complement Components in Facioscapulohumeral Dystrophy","volume":"31","author":"Wong C. J.","year":"2022","journal-title":"Human Molecular Genetics"},{"key":"e_1_2_10_23_1","doi-asserted-by":"crossref","first-page":"83","DOI":"10.3233\/JND-210711","article-title":"Identification of Serum Interleukin 6 Levels as a Disease Severity Biomarker in Facioscapulohumeral Muscular Dystrophy","volume":"9","author":"Gros M.","year":"2022","journal-title":"Journal of Neuromuscular Diseases"},{"key":"e_1_2_10_24_1","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1186\/s12891-021-04134-7","article-title":"Longitudinal Study of MRI and Functional Outcome Measures in Facioscapulohumeral Muscular Dystrophy","volume":"22","author":"Wang L. H.","year":"2021","journal-title":"BMC Musculoskeletal Disorders"},{"key":"e_1_2_10_25_1","doi-asserted-by":"crossref","first-page":"2057","DOI":"10.1212\/WNL.0000000000004647","article-title":"Adding Quantitative Muscle MRI to the FSHD Clinical Trial Toolbox","volume":"89","author":"Mul K.","year":"2017","journal-title":"Neurology"},{"key":"e_1_2_10_26_1","doi-asserted-by":"crossref","first-page":"11","DOI":"10.3390\/cells11040687","article-title":"Outcome Measures in Facioscapulohumeral Muscular Dystrophy Clinical Trials","volume":"11","author":"Ghasemi M.","year":"2022","journal-title":"Cells"},{"key":"e_1_2_10_27_1","doi-asserted-by":"crossref","DOI":"10.1186\/s12883-019-1452-x","article-title":"Clinical Trial Readiness to Solve Barriers to Drug Development in FSHD (ReSolve): Protocol of a Large, International, Multi\u2010Center Prospective Study","volume":"19","author":"LoRusso S.","year":"2019","journal-title":"BMC Neurology"},{"key":"e_1_2_10_28_1","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1016\/j.tcb.2023.01.002","article-title":"Extracellular Vesicles and Nanoparticles: Emerging Complexities","volume":"33","author":"Jeppesen D. K.","year":"2023","journal-title":"Trends in Cell Biology"},{"key":"e_1_2_10_29_1","doi-asserted-by":"crossref","first-page":"8","DOI":"10.3390\/cells8070727","article-title":"Overview of Extracellular Vesicles, Their Origin, Composition, Purpose, and Methods for Exosome Isolation and Analysis","volume":"8","author":"Doyle L. M.","year":"2019","journal-title":"Cells"},{"key":"e_1_2_10_30_1","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1093\/biosci\/biv084","article-title":"Extracellular Vesicles: Composition, Biological Relevance, and Methods of Study","volume":"65","author":"Zaborowski M. P.","year":"2015","journal-title":"Bioscience"},{"key":"e_1_2_10_31_1","doi-asserted-by":"crossref","first-page":"21346","DOI":"10.1038\/s41598-020-78422-y","article-title":"Enrichment of Plasma Extracellular Vesicles for Reliable Quantification of Their Size and Concentration for Biomarker Discovery","volume":"10","author":"Holcar M.","year":"2020","journal-title":"Scientific Reports"},{"key":"e_1_2_10_32_1","doi-asserted-by":"crossref","DOI":"10.3390\/cells9061527","article-title":"Extracellular Vesicles From Skeletal Muscle Cells Efficiently Promote Myogenesis in Induced Pluripotent Stem Cells","volume":"9","author":"Baci D.","year":"2020","journal-title":"Cells"},{"key":"e_1_2_10_33_1","doi-asserted-by":"crossref","first-page":"2028","DOI":"10.1016\/j.cmet.2023.10.013","article-title":"Skeletal Muscle\u2010Derived Extracellular Vesicles Transport Glycolytic Enzymes to Mediate Muscle\u2010To\u2010Bone Crosstalk","volume":"35","author":"Ma S.","year":"2023","journal-title":"Cell Metabolism"},{"key":"e_1_2_10_34_1","doi-asserted-by":"crossref","first-page":"1644","DOI":"10.1158\/1078-0432.CCR-17-2046","article-title":"Extracellular Vesicles Released by Cardiomyocytes in a Doxorubicin\u2010Induced Cardiac Injury Mouse Model Contain Protein Biomarkers of Early Cardiac Injury","volume":"24","author":"Yarana C.","year":"2018","journal-title":"Clinical Cancer Research"},{"key":"e_1_2_10_35_1","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/j.canlet.2012.01.023","article-title":"Secreted 70kDa Lumican Stimulates Growth and Inhibits Invasion of Human Pancreatic Cancer","volume":"320","author":"Yamamoto T.","year":"2012","journal-title":"Cancer Letters"},{"key":"e_1_2_10_36_1","doi-asserted-by":"crossref","DOI":"10.1002\/jev2.12404","article-title":"Minimal Information for Studies of Extracellular Vesicles (MISEV2023): From Basic to Advanced Approaches","volume":"13","author":"Welsh J. A.","year":"2024","journal-title":"Journal of Extracellular Vesicles"},{"key":"e_1_2_10_37_1","doi-asserted-by":"crossref","first-page":"3526","DOI":"10.1039\/C8AN00599K","article-title":"Partial Least Squares\u2010Discriminant Analysis (PLS\u2010DA) for Classification of High\u2010Dimensional (HD) Data: A Review of Contemporary Practice Strategies and Knowledge Gaps","volume":"143","author":"Lee L. C.","year":"2018","journal-title":"Analyst"},{"key":"e_1_2_10_38_1","doi-asserted-by":"crossref","DOI":"10.1093\/nargab\/lqaa078","article-title":"ComBat\u2010Seq: Batch Effect Adjustment for RNA\u2010Seq Count Data","volume":"2","author":"Zhang Y.","year":"2020","journal-title":"NAR Genomics and Bioinformatics"},{"key":"e_1_2_10_39_1","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","article-title":"Moderated Estimation of Fold Change and Dispersion for RNA\u2010Seq Data With DESeq2","volume":"15","author":"Love M. 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T.","year":"2022","journal-title":"Nucleic Acids Research"},{"key":"e_1_2_10_43_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.jprot.2025.105468","article-title":"Proteomic Analysis of Plasma\u2010Derived Extracellular Vesicles: Insights Into Acute Stroke Pathophysiology","volume":"319","author":"Reymond S.","year":"2025","journal-title":"Journal of Proteomics"},{"key":"e_1_2_10_44_1","doi-asserted-by":"crossref","DOI":"10.1101\/cshperspect.a023234","article-title":"Actin\u2010Based Adhesion Modules Mediate Cell Interactions With the Extracellular Matrix and Neighboring Cells","volume":"9","author":"Bachir A. 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