{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,10]],"date-time":"2026-10-10T04:27:19Z","timestamp":1791606439522,"version":"4.3.4"},"reference-count":100,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2021,5,10]],"date-time":"2021-05-10T00:00:00Z","timestamp":1620604800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100007393","name":"Association Fran\u00e7aise contre les Myopathies","doi-asserted-by":"publisher","award":["20225"],"award-info":[{"award-number":["20225"]}],"id":[{"id":"10.13039\/100007393","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Duchenne muscular dystrophy (DMD) is a devastating condition shortening the lifespan of young men. DMD patients suffer from age-related dilated cardiomyopathy (DCM) that leads to heart failure. Several molecular mechanisms leading to cardiomyocyte death in DMD have been described. However, the pathological progression of DMD-associated DCM remains unclear. In skeletal muscle, a dramatic decrease in stem cells, so-called satellite cells, has been shown in DMD patients. Whether similar dysfunction occurs with cardiac muscle cardiovascular progenitor cells (CVPCs) in DMD remains to be explored. We hypothesized that the number of CVPCs decreases in the dystrophin-deficient heart with age and disease state, contributing to DCM progression. We used the dystrophin-deficient mouse model (mdx) to investigate age-dependent CVPC properties. Using quantitative PCR, flow cytometry, speckle tracking echocardiography, and immunofluorescence, we revealed that young mdx mice exhibit elevated CVPCs. We observed a rapid age-related CVPC depletion, coinciding with the progressive onset of cardiac dysfunction. Moreover, mdx CVPCs displayed increased DNA damage, suggesting impaired cardiac muscle homeostasis. Overall, our results identify the early recruitment of CVPCs in dystrophic hearts and their fast depletion with ageing. This latter depletion may participate in the fibrosis development and the acceleration onset of the cardiomyopathy.<\/jats:p>","DOI":"10.3390\/ijms22095025","type":"journal-article","created":{"date-parts":[[2021,5,10]],"date-time":"2021-05-10T05:30:08Z","timestamp":1620624608000},"page":"5025","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Dystrophin Deficiency Causes Progressive Depletion of Cardiovascular Progenitor Cells in the Heart"],"prefix":"10.3390","volume":"22","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9385-4571","authenticated-orcid":false,"given":"Sarka","family":"Jelinkova","sequence":"first","affiliation":[{"name":"Department of Biology, Faculty of Medicine, Masaryk University, Kamenice 5\/A3, 62500 Brno, Czech Republic"},{"name":"ICRC, St Anne\u2019s University Hospital, Peka\u0159sk\u00e1 53, 65691 Brno, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1550-8945","authenticated-orcid":false,"given":"Yvonne","family":"Sleiman","sequence":"additional","affiliation":[{"name":"PhyMedExp, University of Montpellier, INSERM, CNRS, 34295 Montpellier, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0188-0022","authenticated-orcid":false,"given":"Petr","family":"Fojt\u00edk","sequence":"additional","affiliation":[{"name":"Department of Biology, Faculty of Medicine, Masaryk University, Kamenice 5\/A3, 62500 Brno, Czech Republic"},{"name":"ICRC, St Anne\u2019s University Hospital, Peka\u0159sk\u00e1 53, 65691 Brno, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Franck","family":"Aimond","sequence":"additional","affiliation":[{"name":"PhyMedExp, University of Montpellier, INSERM, CNRS, 34295 Montpellier, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amanda","family":"Finan","sequence":"additional","affiliation":[{"name":"PhyMedExp, University of Montpellier, INSERM, CNRS, 34295 Montpellier, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gerald","family":"Hugon","sequence":"additional","affiliation":[{"name":"PhyMedExp, University of Montpellier, INSERM, CNRS, 34295 Montpellier, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Valerie","family":"Scheuermann","sequence":"additional","affiliation":[{"name":"PhyMedExp, University of Montpellier, INSERM, CNRS, 34295 Montpellier, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6238-7365","authenticated-orcid":false,"given":"Deborah","family":"Beckerov\u00e1","sequence":"additional","affiliation":[{"name":"Department of Biology, Faculty of Medicine, Masaryk University, Kamenice 5\/A3, 62500 Brno, Czech Republic"},{"name":"ICRC, St Anne\u2019s University Hospital, Peka\u0159sk\u00e1 53, 65691 Brno, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olivier","family":"Cazorla","sequence":"additional","affiliation":[{"name":"PhyMedExp, University of Montpellier, INSERM, CNRS, 34295 Montpellier, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marie","family":"Vincenti","sequence":"additional","affiliation":[{"name":"PhyMedExp, University of Montpellier, INSERM, CNRS, 34295 Montpellier, France"},{"name":"Pediatric and Adult Congenital Cardiology Department, M3C Regional Reference CHD Center, CHU Montpellier, 371 Avenue du Doyen Giraud, 34295 Montpellier, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pascal","family":"Amedro","sequence":"additional","affiliation":[{"name":"PhyMedExp, University of Montpellier, INSERM, CNRS, 34295 Montpellier, France"},{"name":"Pediatric and Adult Congenital Cardiology Department, M3C Regional Reference CHD Center, CHU Montpellier, 371 Avenue du Doyen Giraud, 34295 Montpellier, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9460-6705","authenticated-orcid":false,"given":"Sylvain","family":"Richard","sequence":"additional","affiliation":[{"name":"PhyMedExp, University of Montpellier, INSERM, CNRS, 34295 Montpellier, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Josef","family":"Jaros","sequence":"additional","affiliation":[{"name":"ICRC, St Anne\u2019s University Hospital, Peka\u0159sk\u00e1 53, 65691 Brno, Czech Republic"},{"name":"Department of Histology and Embryology, Faculty of Medicine, Masaryk University, Kamenice 5\/A1, 62500 Brno, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Petr","family":"Dvorak","sequence":"additional","affiliation":[{"name":"Department of Biology, Faculty of Medicine, Masaryk University, Kamenice 5\/A3, 62500 Brno, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alain","family":"Lacampagne","sequence":"additional","affiliation":[{"name":"PhyMedExp, University of Montpellier, INSERM, CNRS, 34295 Montpellier, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gilles","family":"Carnac","sequence":"additional","affiliation":[{"name":"PhyMedExp, University of Montpellier, INSERM, CNRS, 34295 Montpellier, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1298-0849","authenticated-orcid":false,"given":"Vladimir","family":"Rotrekl","sequence":"additional","affiliation":[{"name":"Department of Biology, Faculty of Medicine, Masaryk University, Kamenice 5\/A3, 62500 Brno, Czech Republic"},{"name":"ICRC, St Anne\u2019s University Hospital, Peka\u0159sk\u00e1 53, 65691 Brno, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1727-3027","authenticated-orcid":false,"given":"Albano C.","family":"Meli","sequence":"additional","affiliation":[{"name":"PhyMedExp, University of Montpellier, INSERM, CNRS, 34295 Montpellier, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,5,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"482","DOI":"10.1016\/j.nmd.2014.03.008","article-title":"A Systematic Review and Meta-Analysis on the Epidemiology of Duchenne and Becker Muscular Dystrophy","volume":"24","author":"Mah","year":"2014","journal-title":"Neuromuscul. Disord."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1016\/0167-5273(90)90082-G","article-title":"The Incidence and Evolution of Cardiomyopathy in Duchenne Muscular Dystrophy","volume":"26","author":"Nigro","year":"1990","journal-title":"Int. J. Cardiol."},{"key":"ref_3","first-page":"361","article-title":"Duchenne, Charcot and Babinski, Three Neurologists of La Salpetri\u00e8re Hospital, and Their Contribution to Concepts of the Central Organization of Motor Synergy","volume":"103","author":"Clarac","year":"2009","journal-title":"J. Physiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1016\/j.echo.2018.10.017","article-title":"Speckle-Tracking Echocardiography in Children with Duchenne Muscular Dystrophy: A Prospective Multicenter Controlled Cross-Sectional Study","volume":"32","author":"Amedro","year":"2019","journal-title":"J. Am. Soc. Echocardiogr."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"986","DOI":"10.1136\/adc.2007.118141","article-title":"Update on the Management of Duchenne Muscular Dystrophy","volume":"93","author":"Manzur","year":"2008","journal-title":"Arch. Dis. Child."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1007\/s10741-009-9156-8","article-title":"Cardiomyopathy in Duchenne Muscular Dystrophy: Pathogenesis and Therapeutics","volume":"15","author":"Fayssoil","year":"2010","journal-title":"Heart Fail. Rev."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1083\/jcb.139.2.375","article-title":"Animal Models for Muscular Dystrophy Show Different Patterns of Sarcolemmal Disruption","volume":"139","author":"Straub","year":"1997","journal-title":"J. Cell Biol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1016\/j.ceca.2007.02.010","article-title":"A Guide to Sparkology: The Taxonomy of Elementary Cellular Ca2+ Signaling Events","volume":"42","author":"Niggli","year":"2007","journal-title":"Cell Calcium"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"H846","DOI":"10.1152\/ajpheart.00688.2006","article-title":"Intracellular Calcium Handling in Ventricular Myocytes from Mdx Mice","volume":"292","author":"Williams","year":"2007","journal-title":"Am. J. Physiol. Heart Circ. Physiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"766","DOI":"10.1093\/cvr\/cvm089","article-title":"Dystrophic Cardiomyopathy: Amplification of Cellular Damage by Ca2+ Signalling and Reactive Oxygen Species-Generating Pathways","volume":"77","author":"Jung","year":"2008","journal-title":"Cardiovasc. Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"81a","DOI":"10.1016\/j.bpj.2010.12.650","article-title":"Abnormal Sodium Handling and Mitochondrial Metabolism in Cardiac Dystrophy","volume":"100","author":"Shirokova","year":"2011","journal-title":"Biophys. J."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1038\/nm.1916","article-title":"Hypernitrosylated Ryanodine Receptor Calcium Release Channels Are Leaky in Dystrophic Muscle","volume":"15","author":"Bellinger","year":"2009","journal-title":"Nat. Med."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1559","DOI":"10.1073\/pnas.0908540107","article-title":"Leaky RyR2 Trigger Ventricular Arrhythmias in Duchenne Muscular Dystrophy","volume":"107","author":"Fauconnier","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Koenig, X., Dysek, S., Kimbacher, S., Mike, A.K., Cervenka, R., Lukacs, P., Nagl, K., Dang, X.B., Todt, H., and Bittner, R.E. (2011). Voltage-Gated Ion Channel Dysfunction Precedes Cardiomyopathy Development in the Dystrophic Heart. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0020300"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1945","DOI":"10.3727\/096368912X638919","article-title":"Alteration of Cardiac Progenitor Cell Potency in GRMD Dogs","volume":"21","author":"Cassano","year":"2012","journal-title":"Cell Transplant."},{"key":"ref_16","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_17","first-page":"3814","article-title":"Activation of Non-Myogenic Mesenchymal Stem Cells during the Disease Progression in Dystrophic Dystrophin\/Utrophin Knockout Mice","volume":"24","author":"Sohn","year":"2015","journal-title":"Hum. Mol. Genet."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2131","DOI":"10.1096\/fj.08-115618","article-title":"Nitric Oxide Deficiency Determines Global Chromatin Changes in Duchenne Muscular Dystrophy","volume":"23","author":"Colussi","year":"2009","journal-title":"FASEB J."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1101\/gad.234468.113","article-title":"HDAC-Regulated MyomiRs Control BAF60 Variant Exchange and Direct the Functional Phenotype of Fibro-Adipogenic Progenitors in Dystrophic Muscles","volume":"28","author":"Saccone","year":"2014","journal-title":"Genes Dev."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"4786","DOI":"10.1093\/hmg\/ddu194","article-title":"Rapid Depletion of Muscle Progenitor Cells in Dystrophic Mdx\/Utrophin-\/- Mice","volume":"23","author":"Lu","year":"2014","journal-title":"Hum. Mol. Genet."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1002\/mus.21716","article-title":"Timeline of Cardiac Dystrophy in 3-18-Month-Old MDX Mice","volume":"42","author":"Loch","year":"2010","journal-title":"Muscle Nerve"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3990","DOI":"10.1093\/hmg\/ddu113","article-title":"Dystrophic Mdx Mice Develop Severe Cardiac and Respiratory Dysfunction Following Genetic Ablation of the Anti-Inflammatory Cytokine IL-10","volume":"23","author":"Chiyo","year":"2014","journal-title":"Hum. Mol. Genet."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1242\/dev.120576","article-title":"View from the Heart: Cardiac Fibroblasts in Development, Scarring and Regeneration","volume":"143","author":"Furtado","year":"2016","journal-title":"Development"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1422","DOI":"10.1161\/CIRCRESAHA.114.302530","article-title":"Cardiogenic Genes Expressed in Cardiac Fibroblasts Contribute to Heart Development and Repair","volume":"114","author":"Salimova","year":"2014","journal-title":"Circ. Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1007\/s12265-012-9394-3","article-title":"The Dynamic Role of Cardiac Fibroblasts in Development and Disease","volume":"5","author":"Lajiness","year":"2012","journal-title":"J. Cardiovasc. Transl. Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"101","DOI":"10.3389\/fcvm.2018.00101","article-title":"Cardiomyocyte\u2014Endothelial Cell Interactions in Cardiac Remodeling and Regeneration","volume":"5","author":"Talman","year":"2018","journal-title":"Front. Cardiovasc. Med."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1128","DOI":"10.1016\/j.jtcvs.2017.09.106","article-title":"Heart Regeneration: The Endothelial Cell Comes First","volume":"155","author":"Mathison","year":"2018","journal-title":"J. Thorac. Cardiovasc. Surg."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1161\/CIRCRESAHA.117.312136","article-title":"Endocardial Cell Plasticity in Cardiac Development, Diseases and Regeneration","volume":"122","author":"Zhang","year":"2018","journal-title":"Circ. Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.cophys.2017.08.001","article-title":"Resident Cells of the Myocardium: More than Spectators in Cardiac Injury, Repair and Regeneration","volume":"1","author":"Gray","year":"2018","journal-title":"Curr. Opin. Physiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"47","DOI":"10.3389\/fcvm.2017.00047","article-title":"Cardiac Stem Cells for Myocardial Regeneration: They Are Not Alone","volume":"4","author":"Leong","year":"2017","journal-title":"Front. Cardiovasc. Med."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1161\/CIRCRESAHA.115.305373","article-title":"Emerging Concepts in Paracrine Mechanisms in Regenerative Cardiovascular Medicine and Biology","volume":"118","author":"Hodgkinson","year":"2016","journal-title":"Circ. Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1528","DOI":"10.1002\/stem.3088","article-title":"Electrical Stimulation of Pediatric Cardiac-Derived c-Kit+ Progenitor Cells Improves Retention and Cardiac Function in Right Ventricular Heart Failure","volume":"37","author":"Maxwell","year":"2019","journal-title":"Stem Cells"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1161\/CIRCRESAHA.118.313215","article-title":"Reassessment of C-Kit in Cardiac Cells: A Complex Interplay Between Expression, Fate, and Function","volume":"123","author":"Zhou","year":"2018","journal-title":"Circ. Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"18283","DOI":"10.1002\/jcp.28461","article-title":"Prolonged Elevated Levels of C-Kit+ Progenitor Cells after a Myocardial Infarction by Beta 2 Adrenergic Receptor Priming","volume":"234","author":"Finan","year":"2019","journal-title":"J. Cell. Physiol."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Hong, K.U., Guo, Y., Li, Q.-H., Cao, P., Al-Maqtari, T., Vajravelu, B.N., Du, J., Book, M.J., Zhu, X., and Nong, Y. (2014). C-Kit+ Cardiac Stem Cells Alleviate Post-Myocardial Infarction Left Ventricular Dysfunction Despite Poor Engraftment and Negligible Retention in the Recipient Heart. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0096725"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1093\/eurheartj\/ehz098","article-title":"Cardiac Stem Cells in the Post-Anversa Era","volume":"40","author":"Davis","year":"2019","journal-title":"Eur. Heart J."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1186\/s13023-019-1257-4","article-title":"Cardiovascular Progenitor Cells and Tissue Plasticity Are Reduced in a Myocardium Affected by Becker Muscular Dystrophy","volume":"15","author":"Pesl","year":"2020","journal-title":"Orphanet J. Rare Dis."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"H303","DOI":"10.1152\/ajpheart.00485.2014","article-title":"Early Right Ventricular Fibrosis and Reduction in Biventricular Cardiac Reserve in the Dystrophin-Deficient Mdx Heart","volume":"308","author":"Meyers","year":"2015","journal-title":"Am. J. Physiol. Heart Circ. Physiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1309\/AJCPZ3J4GEEYIRRA","article-title":"Mast Cells in Systemic Mastocytosis Have Distinctly Brighter CD45 Expression by Flow Cytometry","volume":"143","author":"Chisholm","year":"2015","journal-title":"Am. J. Clin. Pathol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"2170","DOI":"10.1016\/j.bbadis.2015.07.008","article-title":"Differential Roles of MMP-9 in Early and Late Stages of Dystrophic Muscles in a Mouse Model of Duchenne Muscular Dystrophy","volume":"1852","author":"Shiba","year":"2015","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"685","DOI":"10.1007\/s00418-012-1056-7","article-title":"Cyclooxygenase-2 Expression in Skeletal Muscle of Knockout Mice Suffering Duchenne Muscular Dystrophy","volume":"139","author":"Flavia","year":"2013","journal-title":"Histochem. Cell Biol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Jelinkova, S., Fojtik, P., Kohutova, A., Vilotic, A., Markov\u00e1, L., Pesl, M., Jurakova, T., Kruta, M., Vrbsky, J., and Gaillyova, R. (2019). Dystrophin Deficiency Leads to Genomic Instability in Human Pluripotent Stem Cells via NO Synthase-Induced Oxidative Stress. Cells, 8.","DOI":"10.3390\/cells8010053"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1038\/nature13309","article-title":"C-Kit+ Cells Minimally Contribute Cardiomyocytes to the Heart","volume":"509","author":"Kanisicak","year":"2014","journal-title":"Nature"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"8701","DOI":"10.1038\/ncomms9701","article-title":"Resident C-Kit(+) Cells in the Heart Are Not Cardiac Stem Cells","volume":"6","author":"Sultana","year":"2015","journal-title":"Nat. Commun."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"971","DOI":"10.1161\/CIRCRESAHA.109.210682","article-title":"Relative Roles of Direct Regeneration versus Paracrine Effects of Human Cardiosphere-Derived Cells Transplanted into Infarcted Mice","volume":"106","author":"Chimenti","year":"2010","journal-title":"Circ. Res."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"2088","DOI":"10.1002\/stem.532","article-title":"Cardiospheres Recapitulate a Niche-Like Microenvironment Rich in Stemness and Cell-Matrix Interactions, Rationalizing Their Enhanced Functional Potency for Myocardial Repair","volume":"28","author":"Li","year":"2010","journal-title":"Stem Cells"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1108","DOI":"10.1016\/j.jacc.2012.10.052","article-title":"Allogeneic Cardiospheres Safely Boost Cardiac Function and Attenuate Adverse Remodeling After Myocardial Infarction in Immunologically Mismatched Rat Strains","volume":"61","author":"Tseliou","year":"2013","journal-title":"J. Am. Coll. Cardiol."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Rogers, R.G., Fournier, M., Sanchez, L., Ibrahim, A.G., Aminzadeh, M.A., Lewis, M.I., and Marb\u00e1n, E. (2019). Disease-Modifying Bioactivity of Intravenous Cardiosphere-Derived Cells and Exosomes in Mdx Mice. JCI Insight, 4.","DOI":"10.1172\/jci.insight.130202"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"942","DOI":"10.1016\/j.stemcr.2018.01.023","article-title":"Exosome-Mediated Benefits of Cell Therapy in Mouse and Human Models of Duchenne Muscular Dystrophy","volume":"10","author":"Aminzadeh","year":"2018","journal-title":"Stem Cell Rep."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1161\/CIRCULATIONAHA.107.761031","article-title":"Increased Cardiac Myocyte Progenitors in Failing Human Hearts","volume":"118","author":"Kubo","year":"2008","journal-title":"Circulation"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1007\/s00392-014-0705-3","article-title":"Characteristic of C-Kit+ Progenitor Cells in Explanted Human Hearts","volume":"103","author":"Matuszczak","year":"2014","journal-title":"Clin. Res. Cardiol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/j.scr.2015.05.011","article-title":"Endogenous Resident C-Kit Cardiac Stem Cells Increase in Mice with an Exercise-Induced, Physiologically Hypertrophied Heart","volume":"15","author":"Leite","year":"2015","journal-title":"Stem Cell Res."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2197","DOI":"10.1242\/jcs.108.6.2197","article-title":"Apoptosis Precedes Necrosis of Dystrophin-Deficient Muscle","volume":"108","author":"Tidball","year":"1995","journal-title":"J. Cell. Sci."},{"key":"ref_54","first-page":"729","article-title":"Ultrastructural and morphometrical analysis of apoptosis stages in cardiomyocytes of MDX mice","volume":"43","author":"Komarov","year":"2001","journal-title":"Tsitologiia"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/0022-510X(86)90003-1","article-title":"The Association of Cardiac Muscle Necrosis and Inflammation with the Degenerative and Persistent Myopathy of MDX Mice","volume":"72","author":"Bridges","year":"1986","journal-title":"J. Neurol. Sci."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1073\/pnas.96.1.220","article-title":"Severe Cardiomyopathy in Mice Lacking Dystrophin and MyoD","volume":"96","author":"Megeney","year":"1999","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"e13567","DOI":"10.14814\/phy2.13567","article-title":"Calcium Current Properties in Dystrophin-deficient Ventricular Cardiomyocytes from Aged Mdx Mice","volume":"6","author":"Rubi","year":"2018","journal-title":"Physiol. Rep."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"535","DOI":"10.3389\/fbioe.2020.00535","article-title":"DMD Pluripotent Stem Cell Derived Cardiac Cells Recapitulate in Vitro Human Cardiac Pathophysiology","volume":"8","author":"Jelinkova","year":"2020","journal-title":"Front. Bioeng. Biotechnol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"918","DOI":"10.2353\/ajpath.2006.050673","article-title":"Lipid Peroxidation Inhibition Blunts Nuclear Factor-KappaB Activation, Reduces Skeletal Muscle Degeneration, and Enhances Muscle Function in Mdx Mice","volume":"168","author":"Messina","year":"2006","journal-title":"Am. J. Pathol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1016\/j.nmd.2007.11.002","article-title":"Reduced Muscle Necrosis and Long-Term Benefits in Dystrophic Mdx Mice after CV1q (Blockade of TNF) Treatment","volume":"18","author":"Radley","year":"2008","journal-title":"Neuromuscul. Disord."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1006","DOI":"10.1016\/j.nmd.2012.05.002","article-title":"Cardiomyopathy in the Dystrophin\/Utrophin-Deficient Mouse Model of Severe Muscular Dystrophy Is Characterized by Dysregulation of Matrix Metalloproteinases","volume":"22","author":"Zang","year":"2012","journal-title":"Neuromuscul. Disord."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"2723","DOI":"10.4049\/jimmunol.1101342","article-title":"Osteopontin-Stimulated Expression of Matrix Metalloproteinase-9 Causes Cardiomyopathy in the Mdx Model of Duchenne Muscular Dystrophy","volume":"187","author":"Dahiya","year":"2011","journal-title":"J. Immunol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1093\/cvr\/cvz109","article-title":"Absence of Full-Length Dystrophin Impairs Normal Maturation and Contraction of Cardiomyocytes Derived from Human-Induced Pluripotent Stem Cells","volume":"116","author":"Pioner","year":"2020","journal-title":"Cardiovasc. Res."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1356","DOI":"10.2353\/ajpath.2010.090479","article-title":"Delayed Cardiomyopathy in Dystrophin Deficient Mdx Mice Relies on Intrinsic Glutathione Resource","volume":"177","author":"Khouzami","year":"2010","journal-title":"Am. J. Pathol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1007\/s12015-019-09916-0","article-title":"Cardiac Protection after Systemic Transplant of Dystrophin Expressing Chimeric (DEC) Cells to the Mdx Mouse Model of Duchenne Muscular Dystrophy","volume":"15","author":"Siemionow","year":"2019","journal-title":"Stem Cell Rev. Rep."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1111\/j.1365-2613.2010.00750.x","article-title":"Increased Connective Tissue Growth Factor Associated with Cardiac Fibrosis in the Mdx Mouse Model of Dystrophic Cardiomyopathy","volume":"92","author":"Au","year":"2011","journal-title":"Int. J. Exp. Pathol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"757","DOI":"10.7863\/jum.2013.32.5.757","article-title":"Cardiac Characterization of Mdx Mice Using High-Resolution Doppler Echocardiography","volume":"32","author":"Fayssoil","year":"2013","journal-title":"J. Ultrasound Med."},{"key":"ref_68","doi-asserted-by":"crossref","unstructured":"Stuckey, D.J., Carr, C.A., Camelliti, P., Tyler, D.J., Davies, K.E., and Clarke, K. (2012). In Vivo MRI Characterization of Progressive Cardiac Dysfunction in the Mdx Mouse Model of Muscular Dystrophy. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0028569"},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Spurney, C., Yu, Q., and Nagaraju, K. (2011). Speckle Tracking Analysis of the Left Ventricular Anterior Wall Shows Significantly Decreased Relative Radial Strain Patterns in Dystrophin Deficient Mice after 9 Months of Age. PLoS Curr., 3.","DOI":"10.1371\/currents.RRN1273"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1422","DOI":"10.1007\/s00246-016-1451-2","article-title":"The Use of Speckle Tracking Echocardiography for Early Detection of Myocardial Dysfunction in Patients with Duchenne Muscular Dystrophy","volume":"37","author":"Taqatqa","year":"2016","journal-title":"Pediatr. Cardiol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"983","DOI":"10.1016\/j.echo.2016.07.001","article-title":"Evaluation of Echocardiographic Measures of Left Ventricular Function in Patients with Duchenne Muscular Dystrophy: Assessment of Reproducibility and Comparison to Cardiac Magnetic Resonance Imaging","volume":"29","author":"Soslow","year":"2016","journal-title":"J. Am. Soc. Echocardiogr."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1049","DOI":"10.1016\/j.echo.2008.03.001","article-title":"Early Regional Myocardial Dysfunction in Young Patients with Duchenne Muscular Dystrophy","volume":"21","author":"Mertens","year":"2008","journal-title":"J. Am. Soc. Echocardiogr."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1161\/CIRCRESAHA.114.300639","article-title":"Exosomes and Cardiac Repair after Myocardial Infarction","volume":"114","author":"Sahoo","year":"2014","journal-title":"Circ. Res."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1161\/CIRCRESAHA.115.307654","article-title":"More Than Tiny Sacks: Stem Cell Exosomes as Cell-Free Modality for Cardiac Repair","volume":"118","author":"Kishore","year":"2016","journal-title":"Circ. Res."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.coph.2016.01.003","article-title":"Stem Cells and Exosomes in Cardiac Repair","volume":"27","author":"Singla","year":"2016","journal-title":"Curr. Opin. Pharmacol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"297","DOI":"10.4252\/wjsc.v8.i9.297","article-title":"Stem Cell-Derived Exosomes as a Therapeutic Tool for Cardiovascular Disease","volume":"8","author":"Suzuki","year":"2016","journal-title":"World J. Stem Cells"},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Saha, P., Sharma, S., Korutla, L., Datla, S.R., Shoja-Taheri, F., Mishra, R., Bigham, G.E., Sarkar, M., Morales, D., and Bittle, G. (2019). Circulating Exosomes Derived from Transplanted Progenitor Cells Aid the Functional Recovery of Ischemic Myocardium. Sci. Transl. Med., 11.","DOI":"10.1126\/scitranslmed.aau1168"},{"key":"ref_78","doi-asserted-by":"crossref","unstructured":"Fang, S., Wei, J., Pentinmikko, N., Leinonen, H., and Salven, P. (2012). Generation of Functional Blood Vessels from a Single C-Kit+ Adult Vascular Endothelial Stem Cell. PLoS Biol., 10.","DOI":"10.1371\/journal.pbio.1001407"},{"key":"ref_79","first-page":"58","article-title":"C-Kit-Positive Cardiac Stem Cells and Myocardial Regeneration","volume":"2","author":"Hosoda","year":"2012","journal-title":"Am. J. Cardiovasc. Dis."},{"key":"ref_80","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_81","doi-asserted-by":"crossref","first-page":"9616","DOI":"10.1073\/pnas.83.24.9616","article-title":"Evidence for Reactive Oxygen Species Inducing Mutations in Mammalian Cells","volume":"83","author":"Hsie","year":"1986","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1021\/tx0155909","article-title":"DNA Tandem Lesions Containing 8-Oxo-7,8-Dihydroguanine and Formamido Residues Arise from Intramolecular Addition of Thymine Peroxyl Radical to Guanine","volume":"15","author":"Douki","year":"2002","journal-title":"Chem. Res. Toxicol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.yjmcc.2007.05.015","article-title":"Metabolic and Signaling Alterations in Dystrophin-Deficient Hearts Precede Overt Cardiomyopathy","volume":"43","author":"Khairallah","year":"2007","journal-title":"J. Mol. Cell. Cardiol."},{"key":"ref_84","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_85","doi-asserted-by":"crossref","first-page":"1027","DOI":"10.1089\/scd.2013.0388","article-title":"Murine Cardiosphere-Derived Cells Are Impaired by Age but Not by Cardiac Dystrophic Dysfunction","volume":"23","author":"Hsiao","year":"2014","journal-title":"Stem Cells Dev."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1248\/jhs.46.409","article-title":"Selenoprotein P: Its Structure and Functions","volume":"46","author":"Saito","year":"2000","journal-title":"J. Health Sci."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1016\/0003-9861(87)90624-2","article-title":"Purification and Characterization of Human Plasma Glutathione Peroxidase: A Selenoglycoprotein Distinct from the Known Cellular Enzyme","volume":"256","author":"Takahashi","year":"1987","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1089\/ars.2000.2.4-643","article-title":"Efficiency of Selenocysteine Incorporation in Human Thioredoxin Reductase","volume":"2","author":"Yarimizu","year":"2000","journal-title":"Antioxid. Redox Signal."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"H1969","DOI":"10.1152\/ajpheart.00489.2007","article-title":"The Role of Reactive Oxygen Species in the Hearts of Dystrophin-Deficient Mdx Mice","volume":"293","author":"Williams","year":"2007","journal-title":"Am. J. Physiol. Heart Circ. Physiol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"2714","DOI":"10.1089\/scd.2013.0135","article-title":"Exon Skipping and Gene Transfer Restore Dystrophin Expression in Human Induced Pluripotent Stem Cells-Cardiomyocytes Harboring DMD Mutations","volume":"22","author":"Dick","year":"2013","journal-title":"Stem Cells Dev."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"1088","DOI":"10.1016\/j.cell.2009.03.037","article-title":"Genotoxic Stress Abrogates Renewal of Melanocyte Stem Cells by Triggering Their Differentiation","volume":"137","author":"Inomata","year":"2009","journal-title":"Cell"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1038\/nature05862","article-title":"Deficiencies in DNA Damage Repair Limit the Function of Haematopoietic Stem Cells with Age","volume":"447","author":"Rossi","year":"2007","journal-title":"Nature"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"E6875","DOI":"10.1073\/pnas.1706508114","article-title":"DNA Damage Tolerance in Hematopoietic Stem and Progenitor Cells in Mice","volume":"114","author":"Pilzecker","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1016\/j.cell.2012.02.011","article-title":"DNA-Damage-Induced Differentiation in Hematopoietic Stem Cells","volume":"148","author":"Mandal","year":"2012","journal-title":"Cell"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.arr.2015.01.004","article-title":"Genome Instability of Ageing Stem Cells--Induction and Defence Mechanisms","volume":"23","author":"Burkhalter","year":"2015","journal-title":"Ageing Res. Rev."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1016\/j.resp.2017.06.001","article-title":"Effect of Pyridostigmine on in Vivo and in Vitro Respiratory Muscle of Mdx Mice","volume":"243","author":"Amancio","year":"2017","journal-title":"Respir. Physiol. Neurobiol."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-017-17204-5","article-title":"QuPath: Open Source Software for Digital Pathology Image Analysis","volume":"7","author":"Bankhead","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/0160-5402(79)90038-X","article-title":"The Langendorff Heart Preparation\u2014Reappraisal of Its Role as a Research and Teaching Model for Coronary Vasoactive Drugs","volume":"2","author":"Broadley","year":"1979","journal-title":"J. Pharmacol. Methods"},{"key":"ref_99","doi-asserted-by":"crossref","unstructured":"He, J.-Q., Vu, D.M., Hunt, G., Chugh, A., Bhatnagar, A., and Bolli, R. (2011). Human Cardiac Stem Cells Isolated from Atrial Appendages Stably Express C-Kit. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0027719"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"1079","DOI":"10.1016\/j.febslet.2004.12.081","article-title":"Alpha7B Integrin Changes in Mdx Mouse Muscles after L-Arginine Administration","volume":"579","author":"Chazalette","year":"2005","journal-title":"FEBS Lett."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/9\/5025\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:58:35Z","timestamp":1760162315000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/9\/5025"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,5,10]]},"references-count":100,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2021,5]]}},"alternative-id":["ijms22095025"],"URL":"https:\/\/doi.org\/10.3390\/ijms22095025","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,5,10]]}}}