{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T15:52:39Z","timestamp":1790092359056,"version":"4.0.1"},"reference-count":102,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2025,6,13]],"date-time":"2025-06-13T00:00:00Z","timestamp":1749772800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"European Research Council (ERC) under the European Union Horizon 2020 research and innovation program","award":["G.A. 852585"],"award-info":[{"award-number":["G.A. 852585"]}]},{"name":"European Research Council (ERC) under the European Union Horizon 2020 research and innovation program","award":["AZ 802-08"],"award-info":[{"award-number":["AZ 802-08"]}]},{"name":"European Research Council (ERC) under the European Union Horizon 2020 research and innovation program","award":["PDOC-90-15"],"award-info":[{"award-number":["PDOC-90-15"]}]},{"name":"European Research Council (ERC) under the European Union Horizon 2020 research and innovation program","award":["2015_180"],"award-info":[{"award-number":["2015_180"]}]},{"name":"European Research Council (ERC) under the European Union Horizon 2020 research and innovation program","award":["2018_T20"],"award-info":[{"award-number":["2018_T20"]}]},{"name":"European Research Council (ERC) under the European Union Horizon 2020 research and innovation program","award":["2022_EKSE.41"],"award-info":[{"award-number":["2022_EKSE.41"]}]},{"name":"European Research Council (ERC) under the European Union Horizon 2020 research and innovation program","award":["Network 23CVD01"],"award-info":[{"award-number":["Network 23CVD01"]}]},{"name":"Bayerische Forschungsstiftung","award":["G.A. 852585"],"award-info":[{"award-number":["G.A. 852585"]}]},{"name":"Bayerische Forschungsstiftung","award":["AZ 802-08"],"award-info":[{"award-number":["AZ 802-08"]}]},{"name":"Bayerische Forschungsstiftung","award":["PDOC-90-15"],"award-info":[{"award-number":["PDOC-90-15"]}]},{"name":"Bayerische Forschungsstiftung","award":["2015_180"],"award-info":[{"award-number":["2015_180"]}]},{"name":"Bayerische Forschungsstiftung","award":["2018_T20"],"award-info":[{"award-number":["2018_T20"]}]},{"name":"Bayerische Forschungsstiftung","award":["2022_EKSE.41"],"award-info":[{"award-number":["2022_EKSE.41"]}]},{"name":"Bayerische Forschungsstiftung","award":["Network 23CVD01"],"award-info":[{"award-number":["Network 23CVD01"]}]},{"name":"Else Kr\u00f6ner-Fresenius-Stiftung","award":["G.A. 852585"],"award-info":[{"award-number":["G.A. 852585"]}]},{"name":"Else Kr\u00f6ner-Fresenius-Stiftung","award":["AZ 802-08"],"award-info":[{"award-number":["AZ 802-08"]}]},{"name":"Else Kr\u00f6ner-Fresenius-Stiftung","award":["PDOC-90-15"],"award-info":[{"award-number":["PDOC-90-15"]}]},{"name":"Else Kr\u00f6ner-Fresenius-Stiftung","award":["2015_180"],"award-info":[{"award-number":["2015_180"]}]},{"name":"Else Kr\u00f6ner-Fresenius-Stiftung","award":["2018_T20"],"award-info":[{"award-number":["2018_T20"]}]},{"name":"Else Kr\u00f6ner-Fresenius-Stiftung","award":["2022_EKSE.41"],"award-info":[{"award-number":["2022_EKSE.41"]}]},{"name":"Else Kr\u00f6ner-Fresenius-Stiftung","award":["Network 23CVD01"],"award-info":[{"award-number":["Network 23CVD01"]}]},{"name":"ForTra gGmbH f\u00fcr Forschungstransfer der EKFS","award":["G.A. 852585"],"award-info":[{"award-number":["G.A. 852585"]}]},{"name":"ForTra gGmbH f\u00fcr Forschungstransfer der EKFS","award":["AZ 802-08"],"award-info":[{"award-number":["AZ 802-08"]}]},{"name":"ForTra gGmbH f\u00fcr Forschungstransfer der EKFS","award":["PDOC-90-15"],"award-info":[{"award-number":["PDOC-90-15"]}]},{"name":"ForTra gGmbH f\u00fcr Forschungstransfer der EKFS","award":["2015_180"],"award-info":[{"award-number":["2015_180"]}]},{"name":"ForTra gGmbH f\u00fcr Forschungstransfer der EKFS","award":["2018_T20"],"award-info":[{"award-number":["2018_T20"]}]},{"name":"ForTra gGmbH f\u00fcr Forschungstransfer der EKFS","award":["2022_EKSE.41"],"award-info":[{"award-number":["2022_EKSE.41"]}]},{"name":"ForTra gGmbH f\u00fcr Forschungstransfer der EKFS","award":["Network 23CVD01"],"award-info":[{"award-number":["Network 23CVD01"]}]},{"name":"Leducq Foundation","award":["G.A. 852585"],"award-info":[{"award-number":["G.A. 852585"]}]},{"name":"Leducq Foundation","award":["AZ 802-08"],"award-info":[{"award-number":["AZ 802-08"]}]},{"name":"Leducq Foundation","award":["PDOC-90-15"],"award-info":[{"award-number":["PDOC-90-15"]}]},{"name":"Leducq Foundation","award":["2015_180"],"award-info":[{"award-number":["2015_180"]}]},{"name":"Leducq Foundation","award":["2018_T20"],"award-info":[{"award-number":["2018_T20"]}]},{"name":"Leducq Foundation","award":["2022_EKSE.41"],"award-info":[{"award-number":["2022_EKSE.41"]}]},{"name":"Leducq Foundation","award":["Network 23CVD01"],"award-info":[{"award-number":["Network 23CVD01"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Recent studies on myogenic satellite cells (SCs) in Duchenne muscular dystrophy (DMD) documented altered division capacities and impaired regeneration potential of SCs in DMD patients and animal models. It remains unknown, however, if SC-intrinsic effects trigger these deficiencies at pre-contractile stages of myogenesis rather than resulting from the pathologic environment. In this study, we isolated SCs from a porcine DMD model and age-matched wild-type (WT) piglets for comprehensive analysis. Using immunofluorescence, differentiation assays, traction force microscopy (TFM), RNA-seq, and label-free proteomic measurements, SCs behavior was characterized, and molecular changes were investigated. TFM revealed significantly higher average traction forces in DMD than WT SCs (90.4 \u00b1 10.5 Pa vs. 66.9 \u00b1 8.9 Pa; p = 0.0018). We identified 1390 differentially expressed genes and 1261 proteins with altered abundance in DMD vs. WT SCs. Dysregulated pathways uncovered by gene ontology (GO) enrichment analysis included sarcomere organization, focal adhesion, and response to hypoxia. Multi-omics factor analysis (MOFA) integrating transcriptomic and proteomic data, identified five factors accounting for the observed variance with an overall higher contribution of the transcriptomic data. Our findings suggest that SC impairments result from their inherent genetic abnormality rather than from environmental influences. The observed biological changes are intrinsic and not reactive to the pathological surrounding of DMD muscle.<\/jats:p>","DOI":"10.3390\/cells14120892","type":"journal-article","created":{"date-parts":[[2025,6,13]],"date-time":"2025-06-13T03:53:12Z","timestamp":1749786792000},"page":"892","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Multi-Modal Analysis of Satellite Cells Reveals Early Impairments at Pre-Contractile Stages of Myogenesis in Duchenne Muscular Dystrophy"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1265-6790","authenticated-orcid":false,"given":"Sophie","family":"Franzmeier","sequence":"first","affiliation":[{"name":"Section of Clinical & Comparative Neuropathology, Institute of Veterinary Pathology, Center for Clinical Veterinary Medicine, Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen, 80539 Munich, Germany"},{"name":"Department of Neuropathology, Institute of Pathology, School of Medicine and Health, Technical University Munich, 81675 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shounak","family":"Chakraborty","sequence":"additional","affiliation":[{"name":"Institute of Pathology, School of Medicine and Health, Technical University Munich, 81675 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-2237-6159","authenticated-orcid":false,"given":"Armina","family":"Mortazavi","sequence":"additional","affiliation":[{"name":"Department of Veterinary Sciences, Institute for Infectious Diseases and Zoonoses, Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen, 80752 Munich, Germany"},{"name":"Faculty of Physics and Center for NanoScience, Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen, 80752 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6432-1271","authenticated-orcid":false,"given":"Jan B.","family":"St\u00f6ckl","sequence":"additional","affiliation":[{"name":"Laboratory of Functional Genome Analysis (LAFUGA), Gene Center, Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen, 81377 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9582-8705","authenticated-orcid":false,"given":"Jianfei","family":"Jiang","sequence":"additional","affiliation":[{"name":"Department of Veterinary Sciences, Institute for Infectious Diseases and Zoonoses, Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen, 80752 Munich, Germany"},{"name":"Faculty of Physics and Center for NanoScience, Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen, 80752 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5977-5375","authenticated-orcid":false,"given":"Nicole","family":"Pfarr","sequence":"additional","affiliation":[{"name":"Institute of Pathology, School of Medicine and Health, Technical University Munich, 81675 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Benedikt","family":"Sabass","sequence":"additional","affiliation":[{"name":"Department of Veterinary Sciences, Institute for Infectious Diseases and Zoonoses, Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen, 80752 Munich, Germany"},{"name":"Faculty of Physics and Center for NanoScience, Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen, 80752 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4709-3211","authenticated-orcid":false,"given":"Thomas","family":"Fr\u00f6hlich","sequence":"additional","affiliation":[{"name":"Laboratory of Functional Genome Analysis (LAFUGA), Gene Center, Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen, 81377 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-6104-5699","authenticated-orcid":false,"given":"Clara","family":"Kaufhold","sequence":"additional","affiliation":[{"name":"Section of Clinical & Comparative Neuropathology, Institute of Veterinary Pathology, Center for Clinical Veterinary Medicine, Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen, 80539 Munich, Germany"},{"name":"Metabolic Biochemistry, Faculty of Medicine, Biomedical Center (BMC), Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen, 81377 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Stirm","sequence":"additional","affiliation":[{"name":"Molecular Animal Breeding and Biotechnology, Gene Center and Department of Veterinary Science, Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen, 81377 Munich, Germany"},{"name":"Center for Innovative Medical Models (CiMM), Department of Veterinary Sciences, Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen, 85764 Oberschlei\u00dfheim, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0430-9510","authenticated-orcid":false,"given":"Eckhard","family":"Wolf","sequence":"additional","affiliation":[{"name":"Molecular Animal Breeding and Biotechnology, Gene Center and Department of Veterinary Science, Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen, 81377 Munich, Germany"},{"name":"Center for Innovative Medical Models (CiMM), Department of Veterinary Sciences, Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen, 85764 Oberschlei\u00dfheim, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5544-2717","authenticated-orcid":false,"given":"J\u00fcrgen","family":"Schlegel","sequence":"additional","affiliation":[{"name":"Department of Neuropathology, Institute of Pathology, School of Medicine and Health, Technical University Munich, 81675 Munich, Germany"},{"name":"Exercise Biology, Department of Sport and Health Sciences, TUM School of Medicine and Health, Technical University Munich, 80809 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kaspar","family":"Matiasek","sequence":"additional","affiliation":[{"name":"Section of Clinical & Comparative Neuropathology, Institute of Veterinary Pathology, Center for Clinical Veterinary Medicine, Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen, 80539 Munich, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,6,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1455","DOI":"10.1038\/nm.3990","article-title":"Dystrophin expression in muscle stem cells regulates their polarity and asymmetric division","volume":"21","author":"Dumont","year":"2015","journal-title":"Nat. Med."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1152\/physrev.00043.2011","article-title":"Satellite cells and the muscle stem cell niche","volume":"93","author":"Yin","year":"2013","journal-title":"Physiol. Rev."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Hildyard, J.C.W., Roskrow, L.E., Wells, D.J., and Piercy, R.J. (2024). Spatiotemporal analysis of dystrophin expression during muscle repair. bioRxiv.","DOI":"10.1101\/2024.12.06.627177"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Kodippili, K., and Rudnicki, M.A. (2023). Satellite cell contribution to disease pathology in Duchenne muscular dystrophy. Front. Physiol., 14.","DOI":"10.3389\/fphys.2023.1180980"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"e75521","DOI":"10.7554\/eLife.75521","article-title":"Loss of full-length dystrophin expression results in major cell-autonomous abnormalities in proliferating myoblasts","volume":"11","author":"Gosselin","year":"2022","journal-title":"eLife"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1007\/s00441-010-0976-6","article-title":"Elevated satellite cell number in Duchenne muscular dystrophy","volume":"340","author":"Kottlors","year":"2010","journal-title":"Cell Tissue Res."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"826","DOI":"10.1111\/his.12231","article-title":"Fibre type-specific satellite cell content in two models of muscle disease","volume":"63","author":"Bankole","year":"2013","journal-title":"Histopathology"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1016\/S0960-8966(99)00118-2","article-title":"Regenerative capacity and the number of satellite cells in soleus muscles of normal and mdx mice","volume":"10","author":"Reimann","year":"2000","journal-title":"Neuromuscul. Disord."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Ribeiro, A.F., Souza, L.S., Almeida, C.F., Ishiba, R., Fernandes, S.A., Guerrieri, D.A., Santos, A.L.F., Onofre-Oliveira, P.C.G., and Vainzof, M. (2019). Muscle satellite cells and impaired late stage regeneration in different murine models for muscular dystrophies. Sci. Rep., 9.","DOI":"10.1038\/s41598-019-48156-7"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2299","DOI":"10.1242\/jcs.113.12.2299","article-title":"Evidence for a myogenic stem cell that is exhausted in dystrophic muscle","volume":"113","author":"Heslop","year":"2000","journal-title":"J. Cell Sci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1590\/S0100-879X2002000600009","article-title":"Impaired regeneration of dystrophin-deficient muscle fibers is caused by exhaustion of myogenic cells","volume":"35","author":"Luz","year":"2002","journal-title":"Braz. J. Med. Biol. Res."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"16006","DOI":"10.1038\/npjregenmed.2016.6","article-title":"Targeting muscle stem cell intrinsic defects to treat Duchenne muscular dystrophy","volume":"1","author":"Dumont","year":"2016","journal-title":"npj Regen. Med."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"113086","DOI":"10.1016\/j.expneurol.2019.113086","article-title":"Stem cell-based therapies for Duchenne muscular dystrophy","volume":"323","author":"Sun","year":"2020","journal-title":"Exp. Neurol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1083\/jcb.9.2.493","article-title":"Satellite cell of skeletal muscle fibers","volume":"9","author":"Mauro","year":"1961","journal-title":"J. Biophys. Biochem. Cytol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"692","DOI":"10.1038\/s41467-020-20760-6","article-title":"Perspectives on skeletal muscle stem cells","volume":"12","author":"Relaix","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.semcdb.2015.09.017","article-title":"PAX3 and PAX7 as upstream regulators of myogenesis","volume":"44","author":"Buckingham","year":"2015","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.semcdb.2017.11.011","article-title":"Function of the myogenic regulatory factors Myf5, MyoD, Myogenin and MRF4 in skeletal muscle, satellite cells and regenerative myogenesis","volume":"72","author":"Zammit","year":"2017","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"112906","DOI":"10.1016\/j.yexcr.2021.112906","article-title":"Defining and identifying satellite cell-opathies within muscular dystrophies and myopathies","volume":"411","author":"Ganassi","year":"2022","journal-title":"Exp. Cell Res."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"10064","DOI":"10.4081\/ejtm.2022.10064","article-title":"Involvement of muscle satellite cell dysfunction in neuromuscular disorders: Expanding the portfolio of satellite cell-opathies","volume":"32","author":"Ganassi","year":"2022","journal-title":"Eur. J. Transl. Myol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/0960-8966(91)90039-U","article-title":"Population Frequencies of Inherited Neuromuscular Diseases\u2014A World Survey","volume":"1","author":"Emery","year":"1991","journal-title":"Neuromuscul. Disord."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1002\/ana.23528","article-title":"Evidence-based path to newborn screening for Duchenne muscular dystrophy","volume":"71","author":"Mendell","year":"2012","journal-title":"Ann. Neurol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1080\/14737175.2023.2249607","article-title":"Gene therapy for Duchenne muscular dystrophy: An update on the latest clinical developments","volume":"23","author":"Tremblay","year":"2023","journal-title":"Expert Rev. Neurother."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1223","DOI":"10.1002\/j.2040-4603.2015.tb00638.x","article-title":"The Dystrophin Complex: Structure, Function, and Implications for Therapy","volume":"5","author":"Gao","year":"2015","journal-title":"Compr. Physiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1038\/s41572-021-00248-3","article-title":"Duchenne muscular dystrophy","volume":"7","author":"Duan","year":"2021","journal-title":"Nat. Rev. Dis. Primers"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"2120","DOI":"10.1093\/hmg\/ddz044","article-title":"Sunitinib promotes myogenic regeneration and mitigates disease progression in the mdx mouse model of Duchenne muscular dystrophy","volume":"28","author":"Fontelonga","year":"2019","journal-title":"Hum. Mol. Genet."},{"key":"ref_26","first-page":"121","article-title":"Improvement of survival in Duchenne Muscular Dystrophy: Retrospective analysis of 835 patients","volume":"31","author":"Passamano","year":"2012","journal-title":"Acta Myol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1007\/s10654-021-00819-4","article-title":"One in five patients with Duchenne muscular dystrophy dies from other causes than cardiac or respiratory failure","volume":"37","author":"Wahlgren","year":"2022","journal-title":"Eur. J. Epidemiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1242\/dmm.018424","article-title":"Animal models of Duchenne muscular dystrophy: From basic mechanisms to gene therapy","volume":"8","author":"McGreevy","year":"2015","journal-title":"Dis. Models Mech."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1007\/s11248-021-00278-3","article-title":"Animal models for researching approaches to therapy of Duchenne muscular dystrophy","volume":"30","author":"Zaynitdinova","year":"2021","journal-title":"Transgenic Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1038\/s41591-019-0738-2","article-title":"Somatic gene editing ameliorates skeletal and cardiac muscle failure in pig and human models of Duchenne muscular dystrophy","volume":"26","author":"Moretti","year":"2020","journal-title":"Nat. Med."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"dmm049285","DOI":"10.1242\/dmm.049285","article-title":"A scalable, clinically severe pig model for Duchenne muscular dystrophy","volume":"14","author":"Stirm","year":"2021","journal-title":"Dis. Models Mech."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"950","DOI":"10.1016\/j.molmed.2024.04.013","article-title":"Pig models for translational Duchenne muscular dystrophy research","volume":"30","author":"Stirm","year":"2024","journal-title":"Trends Mol. Med."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"4368","DOI":"10.1093\/hmg\/ddt287","article-title":"Dystrophin-deficient pigs provide new insights into the hierarchy of physiological derangements of dystrophic muscle","volume":"22","author":"Klymiuk","year":"2013","journal-title":"Hum. Mol. Genet."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"17003","DOI":"10.1038\/cddiscovery.2017.3","article-title":"Characterization and isolation of highly purified porcine satellite cells","volume":"3","author":"Ding","year":"2017","journal-title":"Cell Death Discov."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Holenstein, C.N., Silvan, U., and Snedeker, J.G. (2017). High-resolution traction force microscopy on small focal adhesions\u2014Improved accuracy through optimal marker distribution and optical flow tracking. Sci. Rep., 7.","DOI":"10.1038\/srep41633"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Huang, Y., Schell, C., Huber, T.B., \u015eim\u015fek, A.N., Hersch, N., Merkel, R., Gompper, G., and Sabass, B. (2019). Traction force microscopy with optimized regularization and automated Bayesian parameter selection for comparing cells. Sci. Rep., 9.","DOI":"10.1038\/s41598-018-36896-x"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1096","DOI":"10.1038\/nmeth.2639","article-title":"Smart-seq2 for sensitive full-length transcriptome profiling in single cells","volume":"10","author":"Picelli","year":"2013","journal-title":"Nat. Methods"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1038\/nprot.2014.006","article-title":"Full-length RNA-seq from single cells using Smart-seq2","volume":"9","author":"Picelli","year":"2014","journal-title":"Nat. Protoc."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2937","DOI":"10.1038\/s41467-018-05347-6","article-title":"Sensitive and powerful single-cell RNA sequencing using mcSCRB-seq","volume":"9","author":"Bagnoli","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_40","unstructured":"Andrews, S. (2023, October 16). A Quality Control Tool for High Throughput Sequence Data. Available online: http:\/\/www.bioinformatics.babraham.ac.uk\/projects\/fastqc\/."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"3047","DOI":"10.1093\/bioinformatics\/btw354","article-title":"MultiQC: Summarize analysis results for multiple tools and samples in a single report","volume":"32","author":"Ewels","year":"2016","journal-title":"Bioinformatics"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1101\/gr.209601.116","article-title":"UMI-tools: Modeling sequencing errors in Unique Molecular Identifiers to improve quantification accuracy","volume":"27","author":"Smith","year":"2017","journal-title":"Genome Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1093\/bioinformatics\/bts635","article-title":"STAR: Ultrafast universal RNA-seq aligner","volume":"29","author":"Dobin","year":"2013","journal-title":"Bioinformatics"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1093\/bioinformatics\/btp616","article-title":"edgeR: A Bioconductor package for differential expression analysis of digital gene expression data","volume":"26","author":"Robinson","year":"2010","journal-title":"Bioinformatics"},{"key":"ref_45","unstructured":"Korotkevich, G., Sukhov, V., Budin, N., Shpak, B., Artyomov, M.N., and Sergushichev, A. (2021). Fast gene set enrichment analysis. bioRxiv."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1367","DOI":"10.1038\/nbt.1511","article-title":"MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification","volume":"26","author":"Cox","year":"2008","journal-title":"Nat. Biotechnol."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Signorelli, M., Tsonaka, R., Aartsma-Rus, A., and Spitali, P. (2023). Multiomic characterization of disease progression in mice lacking dystrophin. PLoS ONE, 18.","DOI":"10.1371\/journal.pone.0283869"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1038\/nmeth.3901","article-title":"The Perseus computational platform for comprehensive analysis of (prote)omics data","volume":"13","author":"Tyanova","year":"2016","journal-title":"Nat. Methods"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.gep.2010.09.005","article-title":"The expression pattern of myogenic regulatory factors MyoD, Myf6 and Pax7 in postnatal porcine skeletal muscles","volume":"11","author":"Eckert","year":"2011","journal-title":"Gene Expr. Patterns"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1824","DOI":"10.1242\/jcs.02908","article-title":"Pax7 and myogenic progression in skeletal muscle satellite cells","volume":"119","author":"Zammit","year":"2006","journal-title":"J. Cell Sci."},{"key":"ref_51","first-page":"997","article-title":"Notch signaling deficiency underlies age-dependent depletion of satellite cells in muscular dystrophy","volume":"7","author":"Jiang","year":"2014","journal-title":"Dis. Models Mech."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1007\/s10561-017-9614-9","article-title":"Isolation, culture and biological characteristics of multipotent porcine skeletal muscle satellite cells","volume":"18","author":"Yang","year":"2017","journal-title":"Cell Tissue Bank."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.yexcr.2004.08.004","article-title":"Desmin: A major intermediate filament protein essential for the structural integrity and function of muscle","volume":"301","author":"Paulin","year":"2004","journal-title":"Exp. Cell Res."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1177\/1535370217749494","article-title":"Myogenic regulatory factors: The orchestrators of myogenesis after 30 years of discovery","volume":"243","author":"Asfour","year":"2018","journal-title":"Exp. Biol. Med."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Shirakawa, T., Toyono, T., Inoue, A., Matsubara, T., Kawamoto, T., and Kokabu, S. (2022). Factors Regulating or Regulated by Myogenic Regulatory Factors in Skeletal Muscle Stem Cells. Cells, 11.","DOI":"10.3390\/cells11091493"},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Bruyere, C., Versaevel, M., Mohammed, D., Alaimo, L., Luciano, M., Vercruysse, E., and Gabriele, S. (2019). Actomyosin contractility scales with myoblast elongation and enhances differentiation through YAP nuclear export. Sci. Rep., 9.","DOI":"10.1038\/s41598-019-52129-1"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1016\/j.molmed.2016.04.002","article-title":"Satellite Cells in Muscular Dystrophy\u2014Lost in Polarity","volume":"22","author":"Chang","year":"2016","journal-title":"Trends Mol. Med."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"e20200064","DOI":"10.1590\/1984-3143-ar2020-0064","article-title":"A decade of experience with genetically tailored pig models for diabetes and metabolic research","volume":"17","author":"Zettler","year":"2020","journal-title":"Anim. Reprod."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1016\/j.nmd.2022.04.005","article-title":"Pig models for Duchenne muscular dystrophy\u2014From disease mechanisms to validation of new diagnostic and therapeutic concepts","volume":"32","author":"Stirm","year":"2022","journal-title":"Neuromuscul. Disord."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1183\/20734735.012716","article-title":"Physiology of respiratory disturbances in muscular dystrophies","volume":"12","author":"Aliverti","year":"2016","journal-title":"Breathe"},{"key":"ref_61","unstructured":"Baig, M.A., and Bordoni, B. (2024). Anatomy, Shoulder and Upper Limb, Pectoral Muscles. StatPearls, StatPearls Publishing LLC."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1032","DOI":"10.1093\/jbcr\/irac091","article-title":"Advantages and Disadvantages of Using Small and Large Animals in Burn Research: Proceedings of the 2021 Research Special Interest Group","volume":"43","author":"Burmeister","year":"2022","journal-title":"J. Burn Care Res."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1002\/ame2.12223","article-title":"Advances in pig models of human diseases","volume":"5","author":"Hou","year":"2022","journal-title":"Anim. Models Exp. Med."},{"key":"ref_64","first-page":"e52049","article-title":"Isolation and quantitative immunocytochemical characterization of primary myogenic cells and fibroblasts from human skeletal muscle","volume":"95","author":"Agley","year":"2015","journal-title":"J. Vis. Exp."},{"key":"ref_65","first-page":"117","article-title":"Isolation and Purification of Satellite Cells for Skeletal Muscle Tissue Engineering","volume":"3","author":"Syverud","year":"2014","journal-title":"J. Regen. Med."},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Dan-Jumbo, S.O., Riley, S.E., Cortes-Araya, Y., Ho, W., Lee, S., Thrower, T., Esteves, C.L., and Donadeu, F.X. (2024). Derivation and long-term maintenance of porcine skeletal muscle progenitor cells. Sci. Rep., 14.","DOI":"10.1038\/s41598-024-59767-0"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1002\/jcp.20376","article-title":"Phenotypic changes of adult porcine mesenchymal stem cells induced by prolonged passaging in culture","volume":"205","author":"Vacanti","year":"2005","journal-title":"J. Cell. Physiol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"105486","DOI":"10.1016\/j.archger.2024.105486","article-title":"Integrating transcriptomic and proteomic data for a comprehensive molecular perspective on the association between sarcopenia and osteoporosis","volume":"125","author":"Chen","year":"2024","journal-title":"Arch. Gerontol. Geriatr."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"6889","DOI":"10.1007\/s00216-023-04759-8","article-title":"A review of the current state of single-cell proteomics and future perspective","volume":"415","author":"Ahmad","year":"2023","journal-title":"Anal. Bioanal. Chem."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1798","DOI":"10.1038\/s12276-020-00528-0","article-title":"Single-cell network biology for resolving cellular heterogeneity in human diseases","volume":"52","author":"Cha","year":"2020","journal-title":"Exp. Mol. Med."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"4856","DOI":"10.1073\/pnas.80.15.4856","article-title":"Defective myoblasts identified in Duchenne muscular dystrophy","volume":"80","author":"Blau","year":"1983","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1212\/WNL.37.4.675","article-title":"Comparison of Duchenne and normal myoblasts from a heterozygote","volume":"37","author":"Hurko","year":"1987","journal-title":"Neurology"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1002\/jcsm.12665","article-title":"Myogenesis modelled by human pluripotent stem cells: A multi-omic study of Duchenne myopathy early onset","volume":"12","author":"Mournetas","year":"2021","journal-title":"J. Cachexia Sarcopenia Muscle"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"e1153777","DOI":"10.1080\/21675511.2016.1153777","article-title":"Dystrophin: The dead calm of a dogma","volume":"4","year":"2016","journal-title":"Rare Dis."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1016\/S0092-8674(00)00066-0","article-title":"Pax7 is required for the specification of myogenic satellite cells","volume":"102","author":"Seale","year":"2000","journal-title":"Cell"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1159\/000514305","article-title":"Empowering Muscle Stem Cells for the Treatment of Duchenne Muscular Dystrophy","volume":"211","author":"Filippelli","year":"2022","journal-title":"Cells Tissues Organs"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1016\/j.stem.2019.01.002","article-title":"EGFR-Aurka Signaling Rescues Polarity and Regeneration Defects in Dystrophin-Deficient Muscle Stem Cells by Increasing Asymmetric Divisions","volume":"24","author":"Wang","year":"2019","journal-title":"Cell Stem Cell"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.bbadis.2006.05.010","article-title":"Dystrophin, its interactions with other proteins, and implications for muscular dystrophy","volume":"1772","author":"Ervasti","year":"2007","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_79","doi-asserted-by":"crossref","unstructured":"Hofemeier, A.D., Muenker, T.M., Herkenrath, F., Ristau, M., Brandt, M., Shahriyari, M., Tiburcy, M., Zimmermann, W.H., Lenz, C., and Mamchaoui, K. (2022). Dystrophin is a mechanical tension modulator. bioRxiv.","DOI":"10.1101\/2022.12.23.521750"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1186\/s13287-023-03363-y","article-title":"Insight into muscle stem cell regeneration and mechanobiology","volume":"14","author":"Pang","year":"2023","journal-title":"Stem Cell Res. Ther."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1038\/s41536-022-00204-z","article-title":"The jam session between muscle stem cells and the extracellular matrix in the tissue microenvironment","volume":"7","author":"Loreti","year":"2022","journal-title":"npj Regen. Med."},{"key":"ref_82","doi-asserted-by":"crossref","unstructured":"Lu, P., Takai, K., Weaver, V.M., and Werb, Z. (2011). Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb. Perspect. Biol., 3.","DOI":"10.1101\/cshperspect.a005058"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1242\/jcs.006064","article-title":"Extracellular matrix dynamics in development and regenerative medicine","volume":"121","author":"Daley","year":"2008","journal-title":"J. Cell Sci."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"267ra176","DOI":"10.1126\/scitranslmed.3008411","article-title":"A Wnt-TGFbeta2 axis induces a fibrogenic program in muscle stem cells from dystrophic mice","volume":"6","author":"Biressi","year":"2014","journal-title":"Sci. Transl. Med."},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Giovarelli, M., Arnaboldi, F., Zecchini, S., Cornaghi, L.B., Nava, A., Sommariva, M., Clementi, E.G.I., and Gagliano, N. (2022). Characterisation of Progressive Skeletal Muscle Fibrosis in the Mdx Mouse Model of Duchenne Muscular Dystrophy: An In Vivo and In Vitro Study. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23158735"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"e2205536119","DOI":"10.1073\/pnas.2205536119","article-title":"Dystrophin missense mutations alter focal adhesion tension and mechanotransduction","volume":"119","author":"Ramirez","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"877","DOI":"10.1083\/jcb.200405004","article-title":"Myotubes differentiate optimally on substrates with tissue-like stiffness: Pathological implications for soft or stiff microenvironments","volume":"166","author":"Engler","year":"2004","journal-title":"J. Cell Biol."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"956","DOI":"10.1016\/j.stemcr.2018.01.027","article-title":"Loss of MyoD and Myf5 in Skeletal Muscle Stem Cells Results in Altered Myogenic Programming and Failed Regeneration","volume":"10","author":"Yamamoto","year":"2018","journal-title":"Stem Cell Rep."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1016\/j.ydbio.2004.05.038","article-title":"Myf5 expression in satellite cells and spindles in adult muscle is controlled by separate genetic elements","volume":"273","author":"Zammit","year":"2004","journal-title":"Dev. Biol."},{"key":"ref_90","doi-asserted-by":"crossref","unstructured":"Abdul-Hussein, S., van der Ven, P.F.M., and Tajsharghi, H. (2012). Expression profiles of muscle disease-associated genes and their isoforms during differentiation of cultured human skeletal muscle cells. BMC Musculoskelet. Disord., 13.","DOI":"10.1186\/1471-2474-13-262"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1186\/s13395-023-00330-2","article-title":"Hypoxia enhances human myoblast differentiation: Involvement of HIF1\u03b1 and impact of DUX4, the FSHD causal gene","volume":"13","author":"Nguyen","year":"2023","journal-title":"Skelet. Muscle"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"3615","DOI":"10.1007\/s00018-009-0146-8","article-title":"The response of human skeletal muscle tissue to hypoxia","volume":"66","author":"Lundby","year":"2009","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1083\/jcb.201609037","article-title":"Integrin-mediated mechanotransduction","volume":"215","author":"Sun","year":"2016","journal-title":"J. Cell Biol."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1159\/000074631","article-title":"Distribution and localization of vinculin-talin-integrin system and dystrophin-glycoprotein complex in human skeletal muscle. Immunohistochemical study using confocal laser scanning microscopy","volume":"175","author":"Anastasi","year":"2003","journal-title":"Cells Tissues Organs"},{"key":"ref_95","doi-asserted-by":"crossref","unstructured":"Wilson, D.G.S., Tinker, A., and Iskratsch, T. (2022). The role of the dystrophin glycoprotein complex in muscle cell mechanotransduction. Commun. Biol., 5.","DOI":"10.1038\/s42003-022-03980-y"},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1007\/s00441-023-03838-7","article-title":"ALDH1A1 and ALDH1A3 paralogues of aldehyde dehydrogenase 1 control myogenic differentiation of skeletal muscle satellite cells by retinoic acid-dependent and -independent mechanisms","volume":"394","author":"Steingruber","year":"2023","journal-title":"Cell Tissue Res."},{"key":"ref_97","doi-asserted-by":"crossref","unstructured":"Argelaguet, R., Velten, B., Arnol, D., Dietrich, S., Zenz, T., Marioni, J.C., Buettner, F., Huber, W., and Stegle, O. (2018). Multi-Omics Factor Analysis-a framework for unsupervised integration of multi-omics data sets. Mol. Syst. Biol., 14.","DOI":"10.15252\/msb.20178124"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"e200219","DOI":"10.1212\/NXI.0000000000200219","article-title":"Metabolomics of Multiple Sclerosis Lesions Demonstrates Lipid Changes Linked to Alterations in Transcriptomics-Based Cellular Profiles","volume":"11","author":"Ladakis","year":"2024","journal-title":"Neurol. Neuroimmunol. Neuroinflamm."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1038\/s41531-025-00899-z","article-title":"Longitudinal multi-omics in alpha-synuclein Drosophila model discriminates disease- from age-associated pathologies in Parkinson\u2019s disease","volume":"11","author":"Moore","year":"2025","journal-title":"npj Park. Dis."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1016\/j.matbio.2020.04.004","article-title":"Spatial-omics: Novel approaches to probe cell heterogeneity and extracellular matrix biology","volume":"91\u201392","author":"Bingham","year":"2020","journal-title":"Matrix Biol."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1093\/nar\/30.1.207","article-title":"Gene Expression Omnibus: NCBI gene expression and hybridization array data repository","volume":"30","author":"Edgar","year":"2002","journal-title":"Nucleic Acids Res."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"D543","DOI":"10.1093\/nar\/gkae1011","article-title":"The PRIDE database at 20 years: 2025 update","volume":"53","author":"Bandla","year":"2025","journal-title":"Nucleic Acids Res."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/14\/12\/892\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:51:11Z","timestamp":1760032271000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/14\/12\/892"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,6,13]]},"references-count":102,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2025,6]]}},"alternative-id":["cells14120892"],"URL":"https:\/\/doi.org\/10.3390\/cells14120892","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2025.01.24.634739","asserted-by":"object"}]},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,6,13]]}}}