{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,17]],"date-time":"2026-01-17T06:47:21Z","timestamp":1768632441530,"version":"3.49.0"},"reference-count":79,"publisher":"MDPI AG","issue":"13","license":[{"start":{"date-parts":[[2025,7,7]],"date-time":"2025-07-07T00:00:00Z","timestamp":1751846400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Medical Faculty, Ruhr University Bochum","award":["DFP2018"],"award-info":[{"award-number":["DFP2018"]}]},{"name":"Medical Faculty, Ruhr University Bochum","award":["005-2310-0032"],"award-info":[{"award-number":["005-2310-0032"]}]},{"name":"Ministry for Culture and Science (MKW NRW) of the German State of North-Rhine Westphalia","award":["DFP2018"],"award-info":[{"award-number":["DFP2018"]}]},{"name":"Ministry for Culture and Science (MKW NRW) of the German State of North-Rhine Westphalia","award":["005-2310-0032"],"award-info":[{"award-number":["005-2310-0032"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Background: Duchenne muscular dystrophy (DMD), which affects 1 in 3500 to 5000 newborn boys worldwide, is characterized by progressive skeletal muscle weakness and degeneration. The reduced muscle regeneration capacity presented by patients is associated with increased fibrosis. Satellite cells (SCs) are skeletal muscle stem cells that play an important role in adult muscle maintenance and regeneration. The absence or mutation of dystrophin in DMD is hypothesized to impair SC asymmetric division, leading to cell cycle arrest. Methods: To overcome the limited availability of biopsies from DMD patients, we used our 3D skeletal muscle organoid (SMO) system, which delivers a stable population of myogenic progenitors (MPs) in dormant, activated, and committed stages, to perform SMO cultures using three DMD patient-derived iPSC lines. Results: The results of scRNA-seq analysis of three DMD SMO cultures versus two healthy, non-isogenic, SMO cultures indicate reduced MP populations with constant activation and differentiation, trending toward embryonic and immature myotubes. Mapping our data onto the human myogenic reference atlas, together with primary SC scRNA-seq data, indicated a more immature developmental stage of DMD organoid-derived MPs. DMD fibro-adipogenic progenitors (FAPs) appear to be activated in SMOs. Conclusions: Our organoid system provides a promising model for studying muscular dystrophies in vitro, especially in the case of early developmental onset, and a methodology for overcoming the bottleneck of limited patient material for skeletal muscle disease modeling.<\/jats:p>","DOI":"10.3390\/cells14131033","type":"journal-article","created":{"date-parts":[[2025,7,7]],"date-time":"2025-07-07T08:58:23Z","timestamp":1751878703000},"page":"1033","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Duchenne Muscular Dystrophy Patient iPSCs\u2014Derived Skeletal Muscle Organoids Exhibit a Developmental Delay in Myogenic Progenitor Maturation"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9676-6323","authenticated-orcid":false,"given":"Urs","family":"Kindler","sequence":"first","affiliation":[{"name":"Department of Anatomy and Molecular Embryology, Institute of Anatomy, Faculty of Medicine, Ruhr University Bochum, 44801 Bochum, NRW, Germany"},{"name":"Department of Molecular Biochemistry, Faculty of Chemistry and Biochemistry, Ruhr University Bochum, 44801 Bochum, NRW, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lampros","family":"Mavrommatis","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Molecular Embryology, Institute of Anatomy, Faculty of Medicine, Ruhr University Bochum, 44801 Bochum, NRW, Germany"},{"name":"Department of Neurology with Heimer Institute for Muscle Research, Faculty of Medicine, University Hospital Bergmannsheil, Ruhr University Bochum, 44789 Bochum, NRW, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Franziska","family":"K\u00e4ppler","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Molecular Embryology, Institute of Anatomy, Faculty of Medicine, Ruhr University Bochum, 44801 Bochum, NRW, Germany"},{"name":"Department of Neurology with Heimer Institute for Muscle Research, Faculty of Medicine, University Hospital Bergmannsheil, Ruhr University Bochum, 44789 Bochum, NRW, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dalya Gebrehiwet","family":"Hiluf","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Molecular Embryology, Institute of Anatomy, Faculty of Medicine, Ruhr University Bochum, 44801 Bochum, NRW, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Stefanie","family":"Heilmann-Heimbach","sequence":"additional","affiliation":[{"name":"Institute of Human Genetics, NGS Core Facility, Faculty of Medicine, University of Bonn, 53127 Bonn, NRW, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3313-8845","authenticated-orcid":false,"given":"Katrin","family":"Marcus","sequence":"additional","affiliation":[{"name":"Medical Proteom Center, Faculty of Medicine, Ruhr University Bochum, 44801 Bochum, NRW, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4889-0829","authenticated-orcid":false,"given":"Thomas","family":"G\u00fcnther Pomorski","sequence":"additional","affiliation":[{"name":"Department of Molecular Biochemistry, Faculty of Chemistry and Biochemistry, Ruhr University Bochum, 44801 Bochum, NRW, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1782-4642","authenticated-orcid":false,"given":"Matthias","family":"Vorgerd","sequence":"additional","affiliation":[{"name":"Department of Neurology with Heimer Institute for Muscle Research, Faculty of Medicine, University Hospital Bergmannsheil, Ruhr University Bochum, 44789 Bochum, NRW, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3309-9724","authenticated-orcid":false,"given":"Beate","family":"Brand-Saberi","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Molecular Embryology, Institute of Anatomy, Faculty of Medicine, Ruhr University Bochum, 44801 Bochum, NRW, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8062-8428","authenticated-orcid":false,"given":"Holm","family":"Zaehres","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Molecular Embryology, Institute of Anatomy, Faculty of Medicine, Ruhr University Bochum, 44801 Bochum, NRW, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2025,7,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1152","DOI":"10.1016\/j.nmd.2017.10.005","article-title":"The 2018 Version of the Gene Table of Monogenic Neuromuscular Disorders (Nuclear Genome)","volume":"27","author":"Bonne","year":"2017","journal-title":"Neuromuscul. Disord."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2025","DOI":"10.1016\/S0140-6736(19)32910-1","article-title":"Muscular Dystrophies","volume":"394","author":"Mercuri","year":"2019","journal-title":"Lancet"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1313","DOI":"10.1016\/j.nmd.2021.11.004","article-title":"The 2022 Version of the Gene Table of Neuromuscular Disorders (Nuclear Genome)","volume":"31","author":"Cohen","year":"2021","journal-title":"Neuromuscul. Disord."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1007\/978-3-319-17362-7_2","article-title":"Muscular Dystrophy: Historical Background and Types","volume":"Volume 31","author":"Huml","year":"2015","journal-title":"Muscular Dystrophy"},{"key":"ref_5","unstructured":"Med, D.D.-A.G. (1868). Undefined Recherches Sur La Paralysie Musculaire Pseudo Hypertrophique Ou Paralysie Myo-Sclerosique, P. Asselin."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"236","DOI":"10.4103\/0028-3886.43441","article-title":"Duchenne Muscular Dystrophy","volume":"56","author":"Yiu","year":"2008","journal-title":"Neurol. India"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1186\/s13023-020-01430-8","article-title":"Global Epidemiology of Duchenne Muscular Dystrophy: An Updated Systematic Review and Meta-Analysis","volume":"15","author":"Crisafulli","year":"2020","journal-title":"Orphanet J. Rare Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1813","DOI":"10.1007\/s00424-021-02623-1","article-title":"Complexity of Skeletal Muscle Degeneration: Multi-Systems Pathophysiology and Organ Crosstalk in Dystrophinopathy","volume":"473","author":"Ohlendieck","year":"2021","journal-title":"Pfl\u00fcgers Arch.-Eur. J. Physiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/B978-0-12-385940-2.00007-3","article-title":"Cellular and Molecular Mechanisms Regulating Fibrosis in Skeletal Muscle Repair and Disease","volume":"96","author":"Serrano","year":"2011","journal-title":"Curr. Top. Dev. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1172\/JCI40373","article-title":"Repairing Skeletal Muscle: Regenerative Potential of Skeletal Muscle Stem Cells","volume":"120","author":"Tedesco","year":"2010","journal-title":"J Clin. Investig."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2559","DOI":"10.1007\/s00018-019-03093-6","article-title":"Adult Stem Cells at Work: Regenerating Skeletal Muscle","volume":"76","author":"Schmidt","year":"2019","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1572","DOI":"10.1242\/dev.114223","article-title":"Intrinsic and Extrinsic Mechanisms Regulating Satellite Cell Function","volume":"142","author":"Dumont","year":"2015","journal-title":"Development"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"590","DOI":"10.1016\/j.stem.2013.07.016","article-title":"Myf5-Positive Satellite Cells Contribute to Pax7-Dependent Long-Term Maintenance of Adult Muscle Stem Cells","volume":"13","author":"Kim","year":"2013","journal-title":"Cell Stem Cell"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1016\/j.devcel.2008.08.018","article-title":"Codependent Activators Direct Myoblast-Specific MyoD Transcription","volume":"15","author":"Hu","year":"2008","journal-title":"Dev. Cell"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.stem.2017.12.010","article-title":"Inhibition of Methyltransferase Setd7 Allows the In Vitro Expansion of Myogenic Stem Cells with Improved Therapeutic Potential","volume":"22","author":"Judson","year":"2018","journal-title":"Cell Stem Cell"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"75","DOI":"10.3390\/muscles1010008","article-title":"Does the Pathogenic Sequence of Skeletal Muscle Degeneration in Duchenne Muscular Dystrophy Begin and End with Unrestrained Satellite Cell Activation?","volume":"1","author":"Carlson","year":"2022","journal-title":"Muscles"},{"key":"ref_17","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_18","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_19","doi-asserted-by":"crossref","first-page":"812","DOI":"10.1016\/j.bbrc.2009.11.144","article-title":"The 8th and 9th Tandem Spectrin-like Repeats of Utrophin Cooperatively Form a Functional Unit to Interact with Polarity-Regulating Kinase PAR-1b","volume":"391","author":"Yamashita","year":"2010","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1174","DOI":"10.1038\/nm.3655","article-title":"Inhibition of JAK-STAT Signaling Stimulates Adult Satellite Cell Function","volume":"20","author":"Price","year":"2014","journal-title":"Nat. Med."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1016\/j.molmed.2016.04.002","article-title":"Satellite Cells in Muscular Dystrophy-Lost in Polarity","volume":"22","author":"Chang","year":"2016","journal-title":"Trends Mol. Med."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1016\/j.stemcr.2013.10.007","article-title":"Derivation and FACS-Mediated Purification of PAX3+\/PAX7+ Skeletal Muscle Precursors from Human Pluripotent Stem Cells","volume":"1","author":"Borchin","year":"2013","journal-title":"Stem Cell Rep."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"962","DOI":"10.1038\/nbt.3297","article-title":"Differentiation of Pluripotent Stem Cells to Muscle Fiber to Model Duchenne Muscular Dystrophy","volume":"33","author":"Chal","year":"2015","journal-title":"Nat. Biotechnol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1833","DOI":"10.1038\/nprot.2016.110","article-title":"Generation of Human Muscle Fibers and Satellite-like Cells from Human Pluripotent Stem Cells in Vitro","volume":"11","author":"Chal","year":"2016","journal-title":"Nat. Protoc."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1038\/s41556-017-0010-2","article-title":"ERBB3 and NGFR Mark a Distinct Skeletal Muscle Progenitor Cell in Human Development and HPSCs","volume":"20","author":"Hicks","year":"2018","journal-title":"Nat. Cell Biol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"516","DOI":"10.1016\/j.stemcr.2014.07.001","article-title":"Derivation and Expansion of PAX7-Positive Muscle Progenitors from Human and Mouse Embryonic Stem Cells","volume":"3","author":"Shelton","year":"2014","journal-title":"Stem Cell Rep."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"100158","DOI":"10.1016\/j.xpro.2020.100158","article-title":"Generation of PAX7 Reporter Cells to Investigate Skeletal Myogenesis from Human Pluripotent Stem Cells","volume":"1","author":"Xi","year":"2020","journal-title":"STAR Protoc."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"4388","DOI":"10.1016\/j.bmcl.2008.06.052","article-title":"Structure\u2013Activity Relationship Study of Bone Morphogenetic Protein (BMP) Signaling Inhibitors","volume":"18","author":"Cuny","year":"2008","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Gouti, M., Tsakiridis, A., Wymeersch, F.J., Huang, Y., Kleinjung, J., Wilson, V., and Briscoe, J. (2014). In Vitro Generation of Neuromesodermal Progenitors Reveals Distinct Roles for Wnt Signalling in the Specification of Spinal Cord and Paraxial Mesoderm Identity. PLoS Biol., 12.","DOI":"10.1371\/journal.pbio.1001937"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"dev187344","DOI":"10.1242\/dev.187344","article-title":"Differentiation of the Human PAX7-Positive Myogenic Precursors\/Satellite Cell Lineage in Vitro","volume":"147","author":"Tanoury","year":"2020","journal-title":"Development"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/bs.ctdb.2017.08.003","article-title":"The Muscle Stem Cell Niche in Health and Disease","volume":"126","author":"Mashinchian","year":"2018","journal-title":"Curr. Top Dev. Biol."},{"key":"ref_32","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_33","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1038\/ncb3312","article-title":"Organoids as an in Vitro Model of Human Development and Disease","volume":"18","author":"Fatehullah","year":"2016","journal-title":"Nat. Cell Biol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"6194","DOI":"10.1126\/science.1247125","article-title":"Organogenesis in a Dish: Modeling Development and Disease Using Organoid Technologies","volume":"345","author":"Lancaster","year":"2014","journal-title":"Science"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1016\/j.stem.2019.12.007","article-title":"Self-Organizing 3D Human Trunk Neuromuscular Organoids","volume":"26","author":"Fischer","year":"2020","journal-title":"Cell Stem Cell"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"899","DOI":"10.1016\/j.celrep.2018.03.091","article-title":"Three-Dimensional Human IPSC-Derived Artificial Skeletal Muscles Model Muscular Dystrophies and Enable Multilineage Tissue Engineering","volume":"23","author":"Maffioletti","year":"2018","journal-title":"Cell Rep."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Mavrommatis, L., Jeong, H.-W., Gomez-Giro, G., Stehling, M., Kienitz, M.-C., Psathaki, O.E., Bixel, M.G., Morosan-Puopolo, G., Gerovska, D., and Ara\u00fazo-Bravo, M.J. (2020). Human Skeletal Muscle Organoids Model Fetal Myogenesis and Sustain Uncommitted PAX7 Myogenic Progenitors. bioRxiv.","DOI":"10.1101\/2020.09.14.295832"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"RP87081","DOI":"10.7554\/eLife.87081","article-title":"Human Skeletal Muscle Organoids Model Fetal Myogenesis and Sustain Uncommitted PAX7 Myogenic Progenitors","volume":"12","author":"Mavrommatis","year":"2023","journal-title":"eLife"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1337","DOI":"10.1038\/s41596-022-00790-8","article-title":"3D Human Induced Pluripotent Stem Cell\u2013Derived Bioengineered Skeletal Muscles for Tissue, Disease and Therapy Modeling","volume":"18","author":"Pinton","year":"2023","journal-title":"Nat. Protoc."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Shin, M.K., Bang, J.S., Lee, J.E., Tran, H.D., Park, G., Lee, D.R., and Jo, J. (2022). Generation of Skeletal Muscle Organoids from Human Pluripotent Stem Cells to Model Myogenesis and Muscle Regeneration. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23095108"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"3106","DOI":"10.1002\/jcsm.13094","article-title":"Engineered Skeletal Muscle Recapitulates Human Muscle Development, Regeneration and Dystrophy","volume":"13","author":"Shahriyari","year":"2022","journal-title":"J. Cachexia Sarcopenia Muscle"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1016\/j.ydbio.2008.08.024","article-title":"A Gradient of Shh Establishes Mutually Repressing Somitic Cell Fates Induced by Nkx3.2 and Pax3","volume":"323","author":"Cairns","year":"2008","journal-title":"Dev. Biol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"877","DOI":"10.1016\/j.cell.2008.07.041","article-title":"Disease-Specific Induced Pluripotent Stem Cells","volume":"134","author":"Park","year":"2008","journal-title":"Cell"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1086","DOI":"10.1016\/j.stemcr.2017.03.012","article-title":"IPSCORE: A Resource of 222 IPSC Lines Enabling Functional Characterization of Genetic Variation across a Variety of Cell Types","volume":"8","author":"Panopoulos","year":"2017","journal-title":"Stem Cell Rep."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"32","DOI":"10.3324\/haematol.2014.108068","article-title":"Erythroid Differentiation of Human Induced Pluripotent Stem Cells Is Independent of Donor Cell Type of Origin","volume":"100","author":"Dorn","year":"2015","journal-title":"Haematologica"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Kindler, U., Zaehres, H., and Mavrommatis, L. (2024). Generation of Skeletal Muscle Organoids from Human Pluripotent Stem Cells. Bio Protoc., 14.","DOI":"10.21769\/BioProtoc.4984"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"3573","DOI":"10.1016\/j.cell.2021.04.048","article-title":"Integrated Analysis of Multimodal Single-Cell Data","volume":"184","author":"Hao","year":"2021","journal-title":"Cell"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1038\/nbt.3192","article-title":"Spatial Reconstruction of Single-Cell Gene Expression Data","volume":"33","author":"Satija","year":"2015","journal-title":"Nat. Biotechnol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1126\/science.aad0501","article-title":"Dissecting the Multicellular Ecosystem of Metastatic Melanoma by Single-Cell RNA-Seq","volume":"352","author":"Tirosh","year":"2016","journal-title":"Science"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1038\/nmeth.4437","article-title":"Single-Cell Sequencing Reveals Dissociation-Induced Gene Expression in Tissue Subpopulations","volume":"14","author":"Sage","year":"2017","journal-title":"Nat. Methods"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Rubenstein, A.B., Smith, G.R., Raue, U., Begue, G., Minchev, K., Ruf-Zamojski, F., Nair, V.D., Wang, X., Zhou, L., and Zaslavsky, E. (2020). Single-Cell Transcriptional Profiles in Human Skeletal Muscle. Sci. Rep., 10.","DOI":"10.1038\/s41598-019-57110-6"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1016\/j.stem.2020.04.017","article-title":"A Human Skeletal Muscle Atlas Identifies the Trajectories of Stem and Progenitor Cells across Development and from Human Pluripotent Stem Cells","volume":"27","author":"Xi","year":"2020","journal-title":"Cell Stem Cell"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"e51576","DOI":"10.7554\/eLife.51576","article-title":"Functionally Heterogeneous Human Satellite Cells Identified by Single Cell RNA Sequencing","volume":"9","author":"Barruet","year":"2020","journal-title":"eLife"},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Germain, P.L., Sonrel, A., and Robinson, M.D. (2020). PipeComp, a General Framework for the Evaluation of Computational Pipelines, Reveals Performant Single Cell RNA-Seq Preprocessing Tools. Genome Biol., 21.","DOI":"10.1186\/s13059-020-02136-7"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1186\/s13073-017-0467-4","article-title":"A Practical Guide to Single-Cell RNA-Sequencing for Biomedical Research and Clinical Applications","volume":"9","author":"Haque","year":"2017","journal-title":"Genome Med."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1038\/s41592-019-0654-x","article-title":"Orchestrating Single-Cell Analysis with Bioconductor","volume":"17","author":"Amezquita","year":"2019","journal-title":"Nat. Methods"},{"key":"ref_57","first-page":"2122","article-title":"A Step-by-Step Workflow for Low-Level Analysis of Single-Cell RNA-Seq Data with Bioconductor","volume":"5","author":"Lun","year":"2016","journal-title":"F1000Research"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1888","DOI":"10.1016\/j.cell.2019.05.031","article-title":"Comprehensive Integration of Single-Cell Data","volume":"177","author":"Stuart","year":"2019","journal-title":"Cell"},{"key":"ref_59","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_60","doi-asserted-by":"crossref","first-page":"105415","DOI":"10.1016\/j.isci.2022.105415","article-title":"Single Cell Sequencing Maps Skeletal Muscle Cellular Diversity as Disease Severity Increases in Dystrophic Mouse Models","volume":"25","author":"Saleh","year":"2022","journal-title":"iScience"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"105775","DOI":"10.1016\/j.isci.2022.105775","article-title":"Diverse Effector and Regulatory Functions of Fibro\/Adipogenic Progenitors during Skeletal Muscle Fibrosis in Muscular Dystrophy","volume":"26","author":"Wang","year":"2023","journal-title":"iScience"},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Pr\u00fcller, J., Mannhardt, I., Eschenhagen, T., Zammit, P.S., and Figeac, N. (2018). Satellite Cells Delivered in Their Niche Efficiently Generate Functional Myotubes in Three-Dimensional Cell Culture. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0202574"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"948","DOI":"10.1038\/nature03594","article-title":"A Pax3\/Pax7-Dependent Population of Skeletal Muscle Progenitor Cells","volume":"435","author":"Relaix","year":"2005","journal-title":"Nature"},{"key":"ref_64","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_65","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1083\/jcb.201603111","article-title":"A Human in Vitro Model of Duchenne Muscular Dystrophy Muscle Formation and Contractility","volume":"215","author":"Nesmith","year":"2016","journal-title":"J. Cell Biol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1016\/j.stem.2018.10.006","article-title":"Orienting Muscle Stem Cells for Regeneration in Homeostasis, Aging, and Disease","volume":"23","author":"Feige","year":"2018","journal-title":"Cell Stem Cell"},{"key":"ref_67","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_68","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1083\/jcb.200312007","article-title":"Muscle Satellite Cells Adopt Divergent Fates a Mechanism for Self-Renewal?","volume":"166","author":"Zammit","year":"2004","journal-title":"J. Cell Biol."},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Theret, M., Rossi, F.M.V., and Contreras, O. (2021). Evolving Roles of Muscle-Resident Fibro-Adipogenic Progenitors in Health, Regeneration, Neuromuscular Disorders, and Aging. Front. Physiol., 12.","DOI":"10.3389\/fphys.2021.673404"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"e135703","DOI":"10.1172\/jci.insight.135703","article-title":"TGF-\u03b2\u2013Driven Muscle Degeneration and Failed Regeneration Underlie Disease Onset in a DMD Mouse Model","volume":"5","author":"Novak","year":"2020","journal-title":"JCI Insight"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.33594\/000000196","article-title":"Control of Muscle Fibro-Adipogenic Progenitors by Myogenic Lineage Is Altered in Aging and Duchenne Muscular Dystrophy","volume":"53","author":"Moratal","year":"2019","journal-title":"Cell. Physiol. Biochem."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1075","DOI":"10.1038\/s41467-018-03425-3","article-title":"Basal Lamina Remodeling at the Skeletal Muscle Stem Cell Niche Mediates Stem Cell Self-Renewal","volume":"9","author":"Rayagiri","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"5776","DOI":"10.1038\/s41467-019-13650-z","article-title":"Human Muscle-Derived CLEC14A-Positive Cells Regenerate Muscle Independent of PAX7","volume":"10","author":"Marg","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"9246825","DOI":"10.1155\/2023\/9246825","article-title":"CRISPR\/Cas9 Genome Editing in LGMD2A\/R1 Patient-Derived Induced Pluripotent Stem and Skeletal Muscle Progenitor Cells","volume":"2023","author":"Mavrommatis","year":"2023","journal-title":"Stem Cells Int."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1016\/0092-8674(87)90579-4","article-title":"Dystrophin: The Protein Product of the Duchenne Muscular Dystrophy Locus","volume":"51","author":"Hoffman","year":"1987","journal-title":"Cell"},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Johnson, E.K., Li, B., Yoon, J.H., Flanigan, K.M., Martin, P.T., Ervasti, J., and Montanaro, F. (2013). Identification of new dystroglycan complexes in skeletal muscle. PLoS ONE., 8.","DOI":"10.1371\/journal.pone.0073224"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"4501","DOI":"10.1126\/sciadv.abe4501","article-title":"Injury-Mediated Stiffening Persistently Activates Muscle Stem Cells through YAP and TAZ Mechanotransduction","volume":"7","author":"Silver","year":"2021","journal-title":"Sci. Adv."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"2665","DOI":"10.1016\/j.bpj.2021.05.021","article-title":"Myofiber Stretch Induces Tensile and Shear Deformation of Muscle Stem Cells in Their Native Niche","volume":"120","author":"Haroon","year":"2021","journal-title":"Biophys. J."},{"key":"ref_79","doi-asserted-by":"crossref","unstructured":"Tao, J., Choudhury, M.I., Maity, D., Kim, T., Sun, S.X., and Fan, C.M. (2023). Mechanical Compression Creates a Quiescent Muscle Stem Cell Niche. Commun. Biol., 6.","DOI":"10.1038\/s42003-023-04411-2"}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/14\/13\/1033\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T18:05:57Z","timestamp":1760033157000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/14\/13\/1033"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,7,7]]},"references-count":79,"journal-issue":{"issue":"13","published-online":{"date-parts":[[2025,7]]}},"alternative-id":["cells14131033"],"URL":"https:\/\/doi.org\/10.3390\/cells14131033","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,7,7]]}}}