{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T20:14:43Z","timestamp":1790799283815,"version":"4.1.0"},"reference-count":74,"publisher":"MDPI AG","issue":"15","license":[{"start":{"date-parts":[[2020,8,4]],"date-time":"2020-08-04T00:00:00Z","timestamp":1596499200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Strength, Science, and Stories of Inspiration-Muscular Dystrophy Association Postdoctoral Fellowship","award":["Postdoctoral Fellowship"],"award-info":[{"award-number":["Postdoctoral Fellowship"]}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["2T32AR056993"],"award-info":[{"award-number":["2T32AR056993"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01AR055686"],"award-info":[{"award-number":["R01AR055686"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["U54HD090257"],"award-info":[{"award-number":["U54HD090257"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009657","name":"FSHD Global Research Foundation","doi-asserted-by":"publisher","award":["Research Grant"],"award-info":[{"award-number":["Research Grant"]}],"id":[{"id":"10.13039\/100009657","id-type":"DOI","asserted-by":"publisher"}]},{"name":"FSHD Society","award":["Research Grant"],"award-info":[{"award-number":["Research Grant"]}]},{"DOI":"10.13039\/100012644","name":"Friends of FSH Research","doi-asserted-by":"publisher","award":["Research Grant"],"award-info":[{"award-number":["Research Grant"]}],"id":[{"id":"10.13039\/100012644","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Deficits in plasma membrane repair have been identified in dysferlinopathy and Duchenne Muscular Dystrophy, and contribute to progressive myopathy. Although Facioscapulohumeral Muscular Dystrophy (FSHD) shares clinicopathological features with these muscular dystrophies, it is unknown if FSHD is characterized by plasma membrane repair deficits. Therefore, we exposed immortalized human FSHD myoblasts, immortalized myoblasts from unaffected siblings, and myofibers from a murine model of FSHD (FLExDUX4) to focal, pulsed laser ablation of the sarcolemma. Repair kinetics and success were determined from the accumulation of intracellular FM1-43 dye post-injury. We subsequently treated FSHD myoblasts with a DUX4-targeting antisense oligonucleotide (AON) to reduce DUX4 expression, and with the antioxidant Trolox to determine the role of DUX4 expression and oxidative stress in membrane repair. Compared to unaffected myoblasts, FSHD myoblasts demonstrate poor repair and a greater percentage of cells that failed to repair, which was mitigated by AON and Trolox treatments. Similar repair deficits were identified in FLExDUX4 myofibers. This is the first study to identify plasma membrane repair deficits in myoblasts from individuals with FSHD, and in myofibers from a murine model of FSHD. Our results suggest that DUX4 expression and oxidative stress may be important targets for future membrane-repair therapies.<\/jats:p>","DOI":"10.3390\/ijms21155575","type":"journal-article","created":{"date-parts":[[2020,8,4]],"date-time":"2020-08-04T10:45:17Z","timestamp":1596537917000},"page":"5575","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":28,"title":["Membrane Repair Deficit in Facioscapulohumeral Muscular Dystrophy"],"prefix":"10.3390","volume":"21","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2134-418X","authenticated-orcid":false,"given":"Adam J.","family":"Bittel","sequence":"first","affiliation":[{"name":"Research Center for Genetic Medicine, Children\u2019s National Hospital, 111 Michigan Ave NW, Washington, DC 20010, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sen Chandra","family":"Sreetama","sequence":"additional","affiliation":[{"name":"Research Center for Genetic Medicine, Children\u2019s National Hospital, 111 Michigan Ave NW, Washington, DC 20010, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7951-1900","authenticated-orcid":false,"given":"Daniel C.","family":"Bittel","sequence":"additional","affiliation":[{"name":"Research Center for Genetic Medicine, Children\u2019s National Hospital, 111 Michigan Ave NW, Washington, DC 20010, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adam","family":"Horn","sequence":"additional","affiliation":[{"name":"Research Center for Genetic Medicine, Children\u2019s National Hospital, 111 Michigan Ave NW, Washington, DC 20010, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9989-8724","authenticated-orcid":false,"given":"James S.","family":"Novak","sequence":"additional","affiliation":[{"name":"Research Center for Genetic Medicine, Children\u2019s National Hospital, 111 Michigan Ave NW, Washington, DC 20010, USA"},{"name":"Department of Genomics and Precision Medicine, The George Washington University School of Medicine and Health Science, 111 Michigan Ave NW, Washington, DC 20010, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6672-6742","authenticated-orcid":false,"given":"Toshifumi","family":"Yokota","sequence":"additional","affiliation":[{"name":"Department of Medical Genetics, University of Alberta, 116 St. &amp; 85 Ave., Edmonton, AB T6G 2R3, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aiping","family":"Zhang","sequence":"additional","affiliation":[{"name":"Research Center for Genetic Medicine, Children\u2019s National Hospital, 111 Michigan Ave NW, Washington, DC 20010, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5656-6930","authenticated-orcid":false,"given":"Rika","family":"Maruyama","sequence":"additional","affiliation":[{"name":"Department of Medical Genetics, University of Alberta, 116 St. &amp; 85 Ave., Edmonton, AB T6G 2R3, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5484-4183","authenticated-orcid":false,"given":"Kenji","family":"Rowel Q. Lim","sequence":"additional","affiliation":[{"name":"Department of Medical Genetics, University of Alberta, 116 St. &amp; 85 Ave., Edmonton, AB T6G 2R3, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jyoti K.","family":"Jaiswal","sequence":"additional","affiliation":[{"name":"Research Center for Genetic Medicine, Children\u2019s National Hospital, 111 Michigan Ave NW, Washington, DC 20010, USA"},{"name":"Department of Integrative Systems Biology, Institute for Biomedical Sciences, The George Washington University, 2121 I St. NW, Washington, DC 20052, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yi-Wen","family":"Chen","sequence":"additional","affiliation":[{"name":"Research Center for Genetic Medicine, Children\u2019s National Hospital, 111 Michigan Ave NW, Washington, DC 20010, USA"},{"name":"Department of Integrative Systems Biology, Institute for Biomedical Sciences, The George Washington University, 2121 I St. NW, Washington, DC 20052, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,8,4]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/mus.20522","article-title":"Facioscapulohumeral muscular dystrophy","volume":"34","author":"Tawil","year":"2006","journal-title":"Muscle Nerve"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1038\/ng0992-26","article-title":"Chromosome 4q DNA rearrangements associated with facioscapulohumeral muscular dystrophy","volume":"2","author":"Wijmenga","year":"1992","journal-title":"Nat. Genet."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1016\/S0092-8674(02)00826-7","article-title":"Inappropriate Gene Activation in FSHD","volume":"110","author":"Gabellini","year":"2002","journal-title":"Cell"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1370","DOI":"10.1038\/ng.2454","article-title":"Digenic inheritance of an SMCHD1 mutation and an FSHD-permissive D4Z4 allele causes facioscapulohumeral muscular dystrophy type 2","volume":"44","author":"Lemmers","year":"2012","journal-title":"Nat. Genet."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"884","DOI":"10.1086\/521986","article-title":"Specific sequence variations within the 4q35 region are associated with facioscapulohumeral muscular dystrophy","volume":"81","author":"Lemmers","year":"2007","journal-title":"Am. J. Hum. Genet."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.devcel.2011.11.013","article-title":"DUX4 Activates germline genes, retroelements, and immune mediators: Implications for facioscapulohumeral dystrophy","volume":"22","author":"Geng","year":"2012","journal-title":"Dev. Cell"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"3816","DOI":"10.1242\/jcs.180372","article-title":"DUX4 induces a transcriptome more characteristic of a less-differentiated cell state and inhibits myogenesis","volume":"129","author":"Knopp","year":"2016","journal-title":"J. Cell Sci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"04996","DOI":"10.7554\/eLife.04996","article-title":"A feedback loop between nonsense-mediated decay and the retrogene DUX4 in facioscapulohumeral muscular dystrophy","volume":"4","author":"Feng","year":"2015","journal-title":"eLife"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1002\/ana.22275","article-title":"DUX4, a candidate gene for facioscapulohumeral muscular dystrophy, causes p53-dependent myopathy in vivo","volume":"69","author":"Wallace","year":"2010","journal-title":"Ann. Neurol."},{"key":"ref_10","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","year":"2015","journal-title":"Hum. Mol. Genet."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2186","DOI":"10.1172\/JCI136133","article-title":"It\u2019s not all about muscle: Fibroadipogenic progenitors contribute to facioscapulohumeral muscular dystrophy","volume":"130","author":"Serra","year":"2020","journal-title":"J. Clin. Investig."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2646","DOI":"10.1007\/s00415-018-9037-y","article-title":"Quantitative muscle MRI and ultrasound for facioscapulohumeral muscular dystrophy: Complementary imaging biomarkers","volume":"265","author":"Mul","year":"2018","journal-title":"J. Neurol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"E72","DOI":"10.1055\/s-0043-124361","article-title":"Differential diagnosis of HyperCKemia","volume":"2","author":"Kley","year":"2018","journal-title":"Neurol. Int. Open"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1136\/jmedgenet-2011-100101","article-title":"Patients with a phenotype consistent with facioscapulohumeral muscular dystrophy display genetic and epigenetic heterogeneity","volume":"49","author":"Sacconi","year":"2011","journal-title":"J. Med Genet."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1007\/s12199-014-0405-7","article-title":"Three novel serum biomarkers, miR-1, miR-133a, and miR-206 for Limb-girdle muscular dystrophy, Facioscapulohumeral muscular dystrophy, and Becker muscular dystrophy","volume":"19","author":"Matsuzaka","year":"2014","journal-title":"Environ. Heal. Prev. Med."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1002\/mus.880100105","article-title":"An examination of some factors influencing creatine kinase in the blood of patients with muscular dystrophy","volume":"10","author":"Jackson","year":"1987","journal-title":"Muscle Nerve"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"897","DOI":"10.1002\/mus.23846","article-title":"Creatine kinase response to high-intensity aerobic exercise in adult-onset muscular dystrophy","volume":"48","author":"Andersen","year":"2013","journal-title":"Muscle Nerve"},{"key":"ref_18","first-page":"1097","article-title":"Disruptions of muscle fiber plasma membranes. Role in exercise-induced damage","volume":"140","author":"McNeil","year":"1992","journal-title":"Am. J. Pathol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1038\/nature01573","article-title":"Defective membrane repair in dysferlin-deficient muscular dystrophy","volume":"423","author":"Bansal","year":"2003","journal-title":"Nature"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1038\/cdd.2016.127","article-title":"Mitochondria mediate cell membrane repair and contribute to Duchenne muscular dystrophy","volume":"24","author":"Vila","year":"2016","journal-title":"Cell Death Differ."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"828","DOI":"10.3389\/fphys.2019.00828","article-title":"Contribution of extracellular vesicles in rebuilding injured muscles","volume":"10","author":"Bittel","year":"2019","journal-title":"Front. Physiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3751","DOI":"10.1007\/s00018-018-2888-7","article-title":"Cellular mechanisms and signals that coordinate plasma membrane repair","volume":"75","author":"Horn","year":"2018","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"4024","DOI":"10.1093\/hmg\/ddy293","article-title":"A patient-derived iPSC model revealed oxidative stress increases facioscapulohumeral muscular dystrophy-causative DUX4","volume":"27","author":"Jonouchi","year":"2018","journal-title":"Hum. Mol. Genet."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1244","DOI":"10.1093\/hmg\/ddy405","article-title":"Dynamic transcriptomic analysis reveals suppression of PGC1\u03b1\/ERR\u03b1 drives perturbed myogenesis in facioscapulohumeral muscular dystrophy","volume":"28","author":"Banerji","year":"2018","journal-title":"Hum. Mol. Genet."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1068","DOI":"10.1016\/j.freeradbiomed.2012.06.041","article-title":"Functional muscle impairment in facioscapulohumeral muscular dystrophy is correlated with oxidative stress and mitochondrial dysfunction","volume":"53","author":"Turki","year":"2012","journal-title":"Free Radic. Boil. Med."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/j.2617-1619.2018.tb00002.x","article-title":"Impaired oxygen demand during exercise is related to oxidative stress and muscle function in Facioscapulohumeral Muscular Dystrophy","volume":"1","author":"Wilson","year":"2018","journal-title":"JCSM Rapid Commun."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Sharma, V., Harafuji, N., Belayew, A., and Chen, Y.-W. (2013). DUX4 differentially regulates transcriptomes of human rhabdomyosarcoma and mouse C2C12 cells. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0064691"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"eaaj1978","DOI":"10.1126\/scisignal.aaj1978","article-title":"Mitochondrial redox signaling enables repair of injured skeletal muscle cells","volume":"10","author":"Horn","year":"2017","journal-title":"Sci. Signal"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2735","DOI":"10.1007\/s10439-015-1341-4","article-title":"Oxidative stress and plasma membrane repair in single myoblasts after femtosecond laser photoporation","volume":"43","author":"Duan","year":"2015","journal-title":"Ann. Biomed. Eng."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"41740","DOI":"10.7554\/eLife.41740","article-title":"Quantitative proteomics reveals key roles for post-transcriptional gene regulation in the molecular pathology of facioscapulohumeral muscular dystrophy","volume":"8","author":"Jagannathan","year":"2019","journal-title":"eLife"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"883","DOI":"10.1101\/gr.233288.117","article-title":"4q-D4Z4 chromatin architecture regulates the transcription of muscle atrophic genes in facioscapulohumeral muscular dystrophy","volume":"29","author":"Cortesi","year":"2019","journal-title":"Genome Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"404","DOI":"10.1038\/ejhg.2011.213","article-title":"A unique library of myogenic cells from facioscapulohumeral muscular dystrophy subjects and unaffected relatives: Family, disease and cell function","volume":"20","author":"Homma","year":"2011","journal-title":"Eur. J. Hum. Genet."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1186\/2044-5040-1-12","article-title":"Establishment of clonal myogenic cell lines from severely affected dystrophic muscles\u2014CDK4 maintains the myogenic population","volume":"1","author":"Stadler","year":"2011","journal-title":"Skelet. Muscle"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"8304","DOI":"10.3390\/molecules20058304","article-title":"Culture conditions affect expression of DUX4 in FSHD myoblasts","volume":"20","author":"Pandey","year":"2015","journal-title":"Molecules"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"e1306","DOI":"10.1038\/cddis.2014.272","article-title":"Dysferlin regulates cell membrane repair by facilitating injury-triggered acid sphingomyelinase secretion","volume":"5","author":"Defour","year":"2014","journal-title":"Cell Death Dis."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1405","DOI":"10.1038\/mt.2016.111","article-title":"Morpholino-mediated knockdown of DUX4 toward facioscapulohumeral muscular dystrophy therapeutics","volume":"24","author":"Chen","year":"2016","journal-title":"Mol. Ther."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1417","DOI":"10.1038\/mt.2012.68","article-title":"RNA interference inhibits DUX4-induced muscle toxicity In Vivo: Implications for a targeted FSHD therapy","volume":"20","author":"Wallace","year":"2012","journal-title":"Mol. Ther."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"6147","DOI":"10.1242\/jcs.115220","article-title":"Glutathione peroxidase 3, a new retinoid target gene, is crucial for human skeletal muscle precursor cell survival","volume":"125","author":"Jean","year":"2012","journal-title":"J. Cell Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1186\/2044-5040-4-4","article-title":"High-throughput screening identifies inhibitors of DUX4-induced myoblast toxicity","volume":"4","author":"Bosnakovski","year":"2014","journal-title":"Skelet. Muscle"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1007\/s11483-009-9129-4","article-title":"Antioxidant activity of vitamin E and trolox: Understanding of the factors that govern lipid peroxidation studies In Vitro","volume":"4","author":"Nunes","year":"2009","journal-title":"Food Biophys."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1016\/j.freeradbiomed.2015.03.016","article-title":"The antioxidant requirement for plasma membrane repair in skeletal muscle","volume":"84","author":"Labazi","year":"2015","journal-title":"Free. Radic. Boil. Med."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"16","DOI":"10.4103\/0976-9668.71667","article-title":"Intracellular scavenging activity of Trolox (6-hydroxy-2,5,7,8-tetramethylchromane-2-carboxylic acid) in the fission yeast, Schizosaccharomyces pombe","volume":"1","author":"Hamad","year":"2010","journal-title":"J. Nat. Sci. Boil. Med."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"2410","DOI":"10.1016\/j.bpj.2013.04.039","article-title":"Small-molecule photostabilizing agents are modifiers of lipid bilayer properties","volume":"104","author":"Alejo","year":"2013","journal-title":"Biophys. J."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1016\/j.freeradbiomed.2016.08.007","article-title":"DUX4-induced constitutive DNA damage and oxidative stress contribute to aberrant differentiation of myoblasts from FSHD patients","volume":"99","author":"Dmitriev","year":"2016","journal-title":"Free Radic. Biol. Med."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1274","DOI":"10.1016\/j.celrep.2019.09.063","article-title":"Dysregulation of mitochondrial Ca2+ uptake and sarcolemma repair underlie muscle weakness and wasting in patients and mice lacking MICU1","volume":"29","author":"Debattisti","year":"2019","journal-title":"Cell Rep."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"2231","DOI":"10.1016\/j.ymthe.2018.07.021","article-title":"Membrane stabilization by modified steroid offers a potential therapy for muscular dystrophy due to dysferlin deficit","volume":"26","author":"Sreetama","year":"2018","journal-title":"Mol. Ther."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"30455","DOI":"10.1074\/jbc.M112.354415","article-title":"Use of quantitative membrane proteomics identifies a novel role of mitochondria in healing injured muscles","volume":"287","author":"Sharma","year":"2012","journal-title":"J. Boil. Chem."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Jones, T., and Jones, P.L. (2018). A cre-inducible DUX4 transgenic mouse model for investigating facioscapulohumeral muscular dystrophy. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0192657"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1087","DOI":"10.1016\/j.nmd.2014.05.012","article-title":"Skeletal muscle imaging in facioscapulohumeral muscular dystrophy, pattern and asymmetry of individual muscle involvement","volume":"24","author":"Rijken","year":"2014","journal-title":"Neuromuscul. Disord."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1038\/sc.1995.97","article-title":"Influence of electrical stimulation of the tibialis anterior muscle in paraplegic subjects. 1. Contractile properties","volume":"33","author":"Rochester","year":"1995","journal-title":"Spinal Cord"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"6554","DOI":"10.1096\/fj.202000240RR","article-title":"Blocking CTGF\/CCN2 reduces established skeletal muscle fibrosis in a rat model of overuse injury","volume":"34","author":"Barbe","year":"2020","journal-title":"FASEB J."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1002\/ana.20750","article-title":"Sarcolemmal reorganization in facioscapulohumeral muscular dystrophy","volume":"59","author":"Reed","year":"2006","journal-title":"Ann. Neurol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"173","DOI":"10.4103\/0028-3886.173646","article-title":"Atypical initial manifestation of facioscapulohumeral muscular dystrophy mimicking neuralgic amyotrophy","volume":"64","author":"Sung","year":"2016","journal-title":"Neurol. India"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1016\/S0960-8966(01)00245-0","article-title":"Myopathy with lobulated muscle fibers: Evidence for heterogeneous etiology and clinical presentation","volume":"12","author":"Saenz","year":"2002","journal-title":"Neuromuscul. Disord."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2015\/359740","article-title":"Oxidative stress-mediated skeletal muscle degeneration: molecules, mechanisms, and therapies","volume":"2016","author":"Choi","year":"2015","journal-title":"Oxidative Med. Cell. Longev."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"89","DOI":"10.3389\/fphys.2014.00089","article-title":"Dysferlin at transverse tubules regulates Ca2+ homeostasis in skeletal muscle","volume":"5","author":"Kerr","year":"2014","journal-title":"Front. Physiol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1017\/erm.2014.17","article-title":"Dysregulation of calcium homeostasis in muscular dystrophies","volume":"16","author":"Aldanondo","year":"2014","journal-title":"Expert Rev. Mol. Med."},{"key":"ref_58","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":"Tawil","year":"2011","journal-title":"Trends Mol. Med."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1476","DOI":"10.2353\/ajpath.2008.080098","article-title":"Dysferlin deficiency shows compensatory induction of Rab27A\/Slp2a that may contribute to inflammatory onset","volume":"173","author":"Kesari","year":"2008","journal-title":"Am. J. Pathol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1016\/S0960-8966(02)00284-5","article-title":"Facioscapulohumeral muscular dystrophy (FSHD) myoblasts demonstrate increased susceptibility to oxidative stress","volume":"13","author":"Winokur","year":"2003","journal-title":"Neuromuscul. Disord."},{"key":"ref_61","first-page":"216","article-title":"Increased levels of adenine nucleotide translocator 1 protein and response to oxidative stress are early events in facioscapulohumeral muscular dystrophy muscle","volume":"83","author":"Carnac","year":"2004","journal-title":"J. Mol. Med."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1016\/S0928-4680(00)00053-5","article-title":"Oxidative stress and apoptosis","volume":"7","author":"Kannan","year":"2000","journal-title":"Pathophysiology"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"101","DOI":"10.2174\/1874609811104020101","article-title":"Oxidative stress and skeletal muscle dysfunction with aging","volume":"4","author":"Aoi","year":"2011","journal-title":"Curr. Aging Sci."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"396","DOI":"10.1016\/j.clinph.2013.08.001","article-title":"Assessement of quadriceps strength, endurance and fatigue in FSHD and CMT: Benefits and limits of femoral nerve magnetic stimulation","volume":"125","author":"Bachasson","year":"2014","journal-title":"Clin. Neurophysiol."},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Janssen, B.H., Voet, N.B.M., Nabuurs, C.I., Kan, H., De Rooy, J.W.J., Geurts, A.C., Padberg, G.W., Van Engelen, B.G.M., and Heerschap, A. (2014). Distinct disease phases in muscles of facioscapulohumeral dystrophy patients identified by MR detected fat infiltration. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0085416"},{"key":"ref_66","first-page":"1","article-title":"Epigenetics and oxidative stress in aging","volume":"2017","author":"Calabria","year":"2017","journal-title":"Oxidative Med. Cell. Longev."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1038\/s41467-017-00730-1","article-title":"Muscle pathology from stochastic low level DUX4 expression in an FSHD mouse model","volume":"8","author":"Bosnakovski","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1212\/WNL.0b013e318282513b","article-title":"Sarcomeric dysfunction contributes to muscle weakness in facioscapulohumeral muscular dystrophy","volume":"80","author":"Lassche","year":"2013","journal-title":"Neurology"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"C613","DOI":"10.1152\/ajpcell.00232.2007","article-title":"Functional, structural, and chemical changes in myosin associated with hydrogen peroxide treatment of skeletal muscle fibers","volume":"294","author":"Prochniewicz","year":"2008","journal-title":"Am. J. Physiol. Physiol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1038\/ncomms1594","article-title":"Promotion of plasma membrane repair by vitamin E","volume":"2","author":"Howard","year":"2011","journal-title":"Nat. Commun."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1016\/j.freeradbiomed.2014.09.014","article-title":"Effects of vitamin C, vitamin E, zinc gluconate, and selenomethionine supplementation on muscle function and oxidative stress biomarkers in patients with facioscapulohumeral dystrophy: A double-blind randomized controlled clinical trial","volume":"81","author":"Passerieux","year":"2015","journal-title":"Free Radic. Boil. Med."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1186\/s13072-018-0215-z","article-title":"Sporadic DUX4 expression in FSHD myocytes is associated with incomplete repression by the PRC2 complex and gain of H3K9 acetylation on the contracted D4Z4 allele","volume":"11","author":"Haynes","year":"2018","journal-title":"Epigenet. Chromatin"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1064","DOI":"10.1093\/hmg\/ddy400","article-title":"Single-cell RNA sequencing in facioscapulohumeral muscular dystrophy disease etiology and development","volume":"28","author":"Heuvel","year":"2018","journal-title":"Hum. Mol. Genet."},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Jiang, S., Williams, K., Kong, X., Zeng, W., Nguyen, N.V., Ma, X., Tawil, R., Yokomori, K., and Mortazavi, A. (2020). Single-nucleus RNA-seq identifies divergent populations of FSHD2 myotube nuclei. PLoS Genet., 16.","DOI":"10.1371\/journal.pgen.1008754"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/15\/5575\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:54:11Z","timestamp":1760176451000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/15\/5575"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,8,4]]},"references-count":74,"journal-issue":{"issue":"15","published-online":{"date-parts":[[2020,8]]}},"alternative-id":["ijms21155575"],"URL":"https:\/\/doi.org\/10.3390\/ijms21155575","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,8,4]]}}}