{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T05:23:30Z","timestamp":1790832210832,"version":"4.1.0"},"reference-count":61,"publisher":"Springer Science and Business Media LLC","issue":"6","license":[{"start":{"date-parts":[[2019,10,15]],"date-time":"2019-10-15T00:00:00Z","timestamp":1571097600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2019,10,15]],"date-time":"2019-10-15T00:00:00Z","timestamp":1571097600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"University of Illinois Chancellor's Innovation Fund (CIF) Proof of Concept Award"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Stem Cell Rev and Rep"],"published-print":{"date-parts":[[2019,12]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Duchenne Muscular Dystrophy (DMD) is a progressive lethal disease caused by X-linked mutations of the dystrophin gene. Dystrophin deficiency clinically manifests as skeletal and cardiac muscle weakness, leading to muscle wasting and premature death due to cardiac and respiratory failure. Currently, no cure exists. Since heart disease is becoming a leading cause of death in DMD patients, there is an urgent need to develop new more effective therapeutic strategies for protection and improvement of cardiac function. We previously reported functional improvements correlating with dystrophin restoration following transplantation of Dystrophin Expressing Chimeric Cells (DEC) of myoblast origin in the<jats:italic>mdx<\/jats:italic>and<jats:italic>mdx\/scid<\/jats:italic>mouse models. Here, we confirm positive effect of DEC of myoblast (MB<jats:sup><jats:italic>wt<\/jats:italic><\/jats:sup>\/MB<jats:sup><jats:italic>mdx<\/jats:italic><\/jats:sup>) and mesenchymal stem cells (MB<jats:sup><jats:italic>wt<\/jats:italic><\/jats:sup>\/MSC<jats:sup><jats:italic>mdx<\/jats:italic><\/jats:sup>) origin on protection of cardiac function after systemic DEC transplant. Therapeutic effect of DEC transplant (0.5\u2009\u00d7\u200910<jats:sup>6<\/jats:sup>) was assessed by echocardiography at 30 and 90\u00a0days after systemic-intraosseous injection to the<jats:italic>mdx<\/jats:italic>mice. At 90\u00a0days post-transplant, dystrophin expression in cardiac muscles of DEC injected mice significantly increased (15.73%\u2009\u00b1\u20095.70 \u2013MB<jats:sup><jats:italic>wt<\/jats:italic><\/jats:sup>\/MB<jats:sup><jats:italic>mdx<\/jats:italic><\/jats:sup>and 5.22%\u2009\u00b1\u20091.10 \u2013 MB<jats:sup><jats:italic>wt<\/jats:italic><\/jats:sup>\/MSC<jats:sup><jats:italic>mdx<\/jats:italic><\/jats:sup>DEC) when compared to vehicle injected controls (2.01%\u2009\u00b1\u20091.36) and, correlated with improved ejection fraction and fractional shortening on echocardiography. DEC lines of MB and MSC origin introduce a new promising approach based on the combined effects of normal myoblasts with dystrophin delivery capacities and MSC with immunomodulatory properties. Our study confirms feasibility and efficacy of DEC therapy on cardiac function and represents a novel therapeutic strategy for cardiac protection and muscle regeneration in DMD.<\/jats:p>","DOI":"10.1007\/s12015-019-09916-0","type":"journal-article","created":{"date-parts":[[2019,10,15]],"date-time":"2019-10-15T06:49:53Z","timestamp":1571122193000},"page":"827-841","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":23,"title":["Cardiac Protection after Systemic Transplant of Dystrophin Expressing Chimeric (DEC) Cells to the mdx Mouse Model of Duchenne Muscular Dystrophy"],"prefix":"10.1007","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6372-6122","authenticated-orcid":false,"given":"Maria","family":"Siemionow","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M.","family":"Malik","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"P.","family":"Langa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J.","family":"Cwykiel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S.","family":"Brodowska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"A.","family":"Heydemann","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2019,10,15]]},"reference":[{"issue":"12","key":"9916_CR1","doi-asserted-by":"crossref","first-page":"1173","DOI":"10.1136\/archdischild-2014-307962","volume":"100","author":"EM Strehle","year":"2015","unstructured":"Strehle, E. M., & Straub, V. (2015). Recent advances in the management of Duchenne muscular dystrophy. Archives of Disease in Childhood, 100(12), 1173\u20131177.","journal-title":"Archives of Disease in Childhood"},{"issue":"10","key":"9916_CR2","doi-asserted-by":"crossref","first-page":"1451","DOI":"10.1016\/j.amjcard.2009.12.070","volume":"105","author":"SC Hagenbuch","year":"2010","unstructured":"Hagenbuch, S. C., Gottliebson, W. M., Wansapura, J., Mazur, W., Fleck, R., Benson, D. W., & Hor, K. N. (2010). Detection of progressive cardiac dysfunction by serial evaluation of circumferential strain in patients with Duchenne muscular dystrophy. The American Journal of Cardiology, 105(10), 1451\u20131455.","journal-title":"The American Journal of Cardiology"},{"key":"9916_CR3","doi-asserted-by":"crossref","DOI":"10.1155\/2018\/8979407","volume":"2018","author":"C Zito","year":"2018","unstructured":"Zito, C., Longobardo, L., Citro, R., et al. (2018). Ten years of 2D longitudinal strain for early myocardial dysfunction detection: A clinical overview. BioMed Research International, 2018, 8979407.","journal-title":"BioMed Research International"},{"issue":"4","key":"9916_CR4","first-page":"194","volume":"10","author":"M Toufan","year":"2015","unstructured":"Toufan, M., Mohammadzadeh Gharebaghi, S., Pourafkari, L., & Delir Abdolahinia, E. (2015). Systolic longitudinal function of the left ventricle assessed by speckle tracking in heart failure patients with preserved ejection fraction. The Journal of Tehran Heart Center, 10(4), 194\u2013200.","journal-title":"The Journal of Tehran Heart Center"},{"issue":"5","key":"9916_CR5","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1016\/j.nmd.2008.03.008","volume":"18","author":"CF Spurney","year":"2018","unstructured":"Spurney, C. F., Knoblach, S., Pistilli, E. E., Nagaraju, K., Martin, G. R., & Hoffman, E. P. (2018). Dystrophin-deficient cardiomyopathy in mouse: expression of Nox4 and Lox are associated with fibrosis and altered functional parameters in the heart. Neuromuscular Disorders, 18(5), 371\u2013381.","journal-title":"Neuromuscular Disorders"},{"issue":"5","key":"9916_CR6","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1016\/j.nmd.2011.10.025","volume":"22","author":"IE Verhaart","year":"2012","unstructured":"Verhaart, I. E., van Duijn, R. J., den Adel, B., et al. (2012). Assessment of cardiac function in three mouse dystrophinopathies by magnetic resonance imaging. Neuromuscular Disorders, 22(5), 418\u2013426.","journal-title":"Neuromuscular Disorders"},{"issue":"19","key":"9916_CR7","doi-asserted-by":"crossref","first-page":"3449","DOI":"10.1093\/hmg\/ddy258","volume":"27","author":"YS Gallot","year":"2018","unstructured":"Gallot, Y. S., Straughn, A. R., Bohnert, K. R., Xiong, G., Hindi, S. M., & Kumar, A. (2018). MyD88 is required for satellite cell-mediated myofiber regeneration in dystrophin-deficient mdx mice. Human Molecular Genetics, 27(19), 3449\u20133463.","journal-title":"Human Molecular Genetics"},{"issue":"1","key":"9916_CR8","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/0735-1097(95)00153-Q","volume":"26","author":"GP Aurigemma","year":"1995","unstructured":"Aurigemma, G. P., Silver, K. H., Priest, M. A., & Gaasch, W. H. (1995). Geometric changes allow normal ejection fraction despite depressed myocardial shortening in hypertensive left ventricular hypertrophy. Journal of the American College of Cardiology, 26(1), 195\u2013202.","journal-title":"Journal of the American College of Cardiology"},{"issue":"5","key":"9916_CR9","doi-asserted-by":"crossref","first-page":"757","DOI":"10.7863\/jum.2013.32.5.757","volume":"32","author":"A Fayssoil","year":"2013","unstructured":"Fayssoil, A., Renault, G., Guerchet, N., Marchiol-Fournigault, C., Fougerousse, F., & Richard, I. (2013). Cardiac characterization of mdx mice using high-resolution doppler echocardiography. Journal of Ultrasound in Medicine, 32(5), 757\u2013761.","journal-title":"Journal of Ultrasound in Medicine"},{"issue":"12","key":"9916_CR10","doi-asserted-by":"crossref","first-page":"2857","DOI":"10.1016\/j.ultrasmedbio.2014.07.015","volume":"40","author":"AB Bondoc","year":"2014","unstructured":"Bondoc, A. B., Detombe, S., Dunmore-Buyze, J., Gutpell, K. M., Liu, L., Kaszuba, A., Han, S., McGirr, R., Hadway, J., Drangova, M., & Hoffman, L. M. (2014). Application of 3-d echocardiography and gated micro-computed tomography to assess cardiomyopathy in a mouse model of duchenne muscular dystrophy. Ultrasound in Medicine & Biology, 40(12), 2857\u20132867.","journal-title":"Ultrasound in Medicine & Biology"},{"issue":"23","key":"9916_CR11","doi-asserted-by":"crossref","first-page":"4585","DOI":"10.1007\/s00018-013-1396-z","volume":"70","author":"A Govoni","year":"2013","unstructured":"Govoni, A., Magri, F., Brajkovic, S., Zanetta, C., Faravelli, I., Corti, S., Bresolin, N., & Comi, G. P. (2013). Ongoing therapeutic trials and outcome measures for Duchenne muscular dystrophy. Cellular and Molecular Life Sciences, 70(23), 4585\u20134602.","journal-title":"Cellular and Molecular Life Sciences"},{"issue":"4","key":"9916_CR12","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1177\/1756285615586123","volume":"8","author":"D Sienkiewicz","year":"2015","unstructured":"Sienkiewicz, D., Kulak, W., Okurowska-Zawada, B., Paszko-Patej, G., & Kawnik, K. (2015). Duchenne muscular dystrophy: Current cell therapies. Therapeutic Advances in Neurological Disorders, 8(4), 166\u2013177.","journal-title":"Therapeutic Advances in Neurological Disorders"},{"issue":"5","key":"9916_CR13","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1093\/eurjhf\/hfp028","volume":"11","author":"R Bauer","year":"2009","unstructured":"Bauer, R., Straub, V., Blain, A., Bushby, K., & MacGowan, G. A. (2009). Contrasting effects of steroids and angiotensin-converting-enzyme inhibitors in a mouse model of dystrophin-deficient cardiomyopathy. European Journal of Heart Failure, 11(5), 463\u2013471.","journal-title":"European Journal of Heart Failure"},{"issue":"5","key":"9916_CR14","doi-asserted-by":"crossref","first-page":"582","DOI":"10.1161\/CIRCULATIONAHA.111.031716","volume":"124","author":"JA Rafael-Fortney","year":"2011","unstructured":"Rafael-Fortney, J. A., Chimanji, N. S., Schill, K. E., Martin, C. D., Murray, J. D., Ganguly, R., Stangland, J. E., Tran, T., Xu, Y., Canan, B. D., Mays, T. A., Delf\u00edn, D. A., Janssen, P. M. L., & Raman, S. V. (2011). Early treatment with lisinopril and spironolactone preserves cardiac and skeletal muscle in Duchenne muscular dystrophy mice. Circulation, 124(5), 582\u2013588.","journal-title":"Circulation"},{"key":"9916_CR15","unstructured":"Shawi, F., Perras, C., & Severn, M. (2016). Emerging Drugs for Duchenne Muscular Dystrophy. CADTH Issues in Emerging Health Technologies (pp. 1\u201319). Ottawa (ON): Canadian Agency for Drugs and Technologies in Health."},{"issue":"6271","key":"9916_CR16","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1126\/science.aad5143","volume":"351","author":"CE Nelson","year":"2016","unstructured":"Nelson, C. E., Hakim, C. H., Ousterout, D. G., Thakore, P. I., Moreb, E. A., Rivera, R. M. C., Madhavan, S., Pan, X., Ran, F. A., Yan, W. X., Asokan, A., Zhang, F., Duan, D., & Gersbach, C. A. (2016). In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science, 351(6271), 403\u2013407.","journal-title":"Science"},{"issue":"6201","key":"9916_CR17","doi-asserted-by":"crossref","first-page":"1184","DOI":"10.1126\/science.1254445","volume":"345","author":"C Long","year":"2014","unstructured":"Long, C., McAnally, J. R., Shelton, J. M., Mireault, A. A., Bassel-Duby, R., & Olson, E. N. (2014). Prevention of muscular dystrophy in mice by CRISPR\/Cas9-mediated editing of germline DNA. Science, 345(6201), 1184\u20131188.","journal-title":"Science"},{"key":"9916_CR18","doi-asserted-by":"crossref","unstructured":"Gee, P., Xu, H., & Hotta, A. (2017). Cellular reprogramming, genome editing, and alternative CRISPR Cas9 Technologies for Precise Gene Therapy of Duchenne muscular dystrophy. Stem Cells International, 2017, 8765154, 1, 11.","DOI":"10.1155\/2017\/8765154"},{"issue":"5","key":"9916_CR19","doi-asserted-by":"crossref","first-page":"876","DOI":"10.1161\/CIRCRESAHA.116.309727","volume":"120","author":"T Doetschman","year":"2017","unstructured":"Doetschman, T., & Georgieva, T. (2017). Gene editing with CRISPR\/Cas9 RNA-directed nuclease. Circulation Research, 120(5), 876\u2013894.","journal-title":"Circulation Research"},{"issue":"6","key":"9916_CR20","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1002\/ana.22024","volume":"67","author":"V Malik","year":"2010","unstructured":"Malik, V., Rodino-Klapac, L. R., Viollet, L., Wall, C., King, W., al-Dahhak, R., Lewis, S., Shilling, C. J., Kota, J., Serrano-Munuera, C., Hayes, J., Mahan, J. D., Campbell, K. J., Banwell, B., Dasouki, M., Watts, V., Sivakumar, K., Bien-Willner, R., Flanigan, K. M., Sahenk, Z., Barohn, R. J., Walker, C. M., & Mendell, J. R. (2010). Gentamicin-induced readthrough of stop codons in Duchenne muscular dystrophy. Annals of Neurology, 67(6), 771\u2013780.","journal-title":"Annals of Neurology"},{"issue":"6","key":"9916_CR21","doi-asserted-by":"crossref","first-page":"807","DOI":"10.1172\/JCI0216098","volume":"110","author":"E Gussoni","year":"2002","unstructured":"Gussoni, E., Bennett, R. R., Muskiewicz, K. R., Meyerrose, T., Nolta, J. A., Gilgoff, I., Stein, J., Chan, Y. M., Lidov, H. G., B\u00f6nnemann, C. G., von Moers, A., Morris, G. E., den Dunnen, J. T., Chamberlain, J. S., Kunkel, L. M., & Weinberg, K. (2002). Long-term persistence of donor nuclei in a Duchenne muscular dystrophy patient receiving bone marrow transplantation. The Journal of Clinical Investigation, 110(6), 807\u2013814.","journal-title":"The Journal of Clinical Investigation"},{"issue":"10","key":"9916_CR22","doi-asserted-by":"crossref","first-page":"918","DOI":"10.1016\/S1474-4422(09)70211-X","volume":"8","author":"M Kinali","year":"2009","unstructured":"Kinali, M., Arechavala-Gomeza, V., Feng, L., Cirak, S., Hunt, D., Adkin, C., Guglieri, M., Ashton, E., Abbs, S., Nihoyannopoulos, P., Garralda, M. E., Rutherford, M., Mcculley, C., Popplewell, L., Graham, I. R., Dickson, G., Wood, M. J. A., Wells, D. J., Wilton, S. D., Kole, R., Straub, V., Bushby, K., Sewry, C., Morgan, J. E., & Muntoni, F. (2009). Local restoration of dystrophin expression with the morpholino oligomer AVI-4658 in Duchenne muscular dystrophy: A single-blind, placebo-controlled, dose-escalation, proof-of-concept study. The Lancet Neurology, 8(10), 918\u2013928.","journal-title":"The Lancet Neurology"},{"issue":"3","key":"9916_CR23","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1093\/cvr\/cvp335","volume":"85","author":"N Jearawiriyapaisarn","year":"2010","unstructured":"Jearawiriyapaisarn, N., Moulton, H. M., Sazani, P., Kole, R., & Willis, M. S. (2010). Long-term improvement in mdx cardiomyopathy after therapy with peptide-conjugated morpholino oligomers. Cardiovascular Research, 85(3), 444\u2013453.","journal-title":"Cardiovascular Research"},{"key":"9916_CR24","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.yjmcc.2014.01.009","volume":"69","author":"M van Putten","year":"2014","unstructured":"van Putten, M., van der Pijl, E. M., Hulsker, M., Verhaart, I. E. C., Nadarajah, V. D., van der Weerd, L., & Aartsma-Rus, A. (2014). Low dystrophin levels in heart can delay heart failure in mdx mice. Journal of Molecular and Cellular Cardiology, 69, 17\u201323.","journal-title":"Journal of Molecular and Cellular Cardiology"},{"issue":"9791","key":"9916_CR25","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1016\/S0140-6736(11)60756-3","volume":"378","author":"S Cirak","year":"2011","unstructured":"Cirak, S., Arechavala-Gomeza, V., Guglieri, M., Feng, L., Torelli, S., Anthony, K., Abbs, S., Garralda, M. E., Bourke, J., Wells, D. J., Dickson, G., Wood, M. J. A., Wilton, S. D., Straub, V., Kole, R., Shrewsbury, S. B., Sewry, C., Morgan, J. E., Bushby, K., & Muntoni, F. (2011). Exon skipping and dystrophin restoration in patients with Duchenne muscular dystrophy after systemic phosphorodiamidate morpholino oligomer treatment: An open-label, phase 2, dose-escalation study. Lancet, 378(9791), 595\u2013605.","journal-title":"Lancet"},{"issue":"11","key":"9916_CR26","doi-asserted-by":"crossref","first-page":"2153","DOI":"10.1038\/mt.2012.188","volume":"20","author":"S Goudenege","year":"2012","unstructured":"Goudenege, S., Lebel, C., Huot, N. B., Dufour, C., Fujii, I., Gekas, J., Rousseau, J., & Tremblay, J. P. (2012). Myoblasts derived from normal hESCs and dystrophic hiPSCs efficiently fuse with existing muscle fibers following transplantation. Molecular Therapy, 20(11), 2153\u20132167.","journal-title":"Molecular Therapy"},{"key":"9916_CR27","volume":"6","author":"J Meng","year":"2016","unstructured":"Meng, J., Counsell, J. R., Reza, M., Laval, S. H., Danos, O., Thrasher, A., Lochm\u00fcller, H., Muntoni, F., & Morgan, J. E. (2016). Autologous skeletal muscle derived cells expressing a novel functional dystrophin provide a potential therapy for Duchenne muscular dystrophy. Scientific Reports, 6, 19750.","journal-title":"Scientific Reports"},{"issue":"1","key":"9916_CR28","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1038\/mt.2011.181","volume":"20","author":"Y Nitahara-Kasahara","year":"2012","unstructured":"Nitahara-Kasahara, Y., Hayashita-Kinoh, H., Ohshima-Hosoyama, S., Okada, H., Wada-Maeda, M., Nakamura, A., Okada, T., & Takeda, S.'. (2012). Long-term engraftment of multipotent mesenchymal stromal cells that differentiate to form myogenic cells in dogs with Duchenne muscular dystrophy. Molecular Therapy, 20(1), 168\u2013177.","journal-title":"Molecular Therapy"},{"issue":"7","key":"9916_CR29","doi-asserted-by":"crossref","first-page":"1342","DOI":"10.1038\/mt.2014.62","volume":"22","author":"M Noviello","year":"2014","unstructured":"Noviello, M., Tedesco, F. S., Bondanza, A., Tonlorenzi, R., Rosaria Carbone, M., Gerli, M. F. M., Marktel, S., Napolitano, S., Cicalese, M. P., Ciceri, F., Peretti, G., Cossu, G., & Bonini, C. (2014). Inflammation converts human mesoangioblasts into targets of alloreactive immune responses: Implications for allogeneic cell therapy of DMD. Molecular Therapy, 22(7), 1342\u20131352.","journal-title":"Molecular Therapy"},{"issue":"7","key":"9916_CR30","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1111\/j.1399-3046.2010.01377.x","volume":"14","author":"B Palmieri","year":"2010","unstructured":"Palmieri, B., Tremblay, J. P., & Daniele, L. (2010). Past, present and future of myoblast transplantation in the treatment of Duchenne muscular dystrophy. Pediatric Transplantation, 14(7), 813\u2013819.","journal-title":"Pediatric Transplantation"},{"issue":"3","key":"9916_CR31","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1007\/s12015-018-9807-z","volume":"14","author":"M Siemionow","year":"2018","unstructured":"Siemionow, M., Cwykiel, J., Heydemann, A., Garcia, J., Marchese, E., Siemionow, K., & Szilagyi, E. (2018). Dystrophin expressing chimeric (DEC) human cells provide a potential therapy for Duchenne muscular dystrophy. Stem Cell Reviews and Reports, 14(3), 370\u2013384.","journal-title":"Stem Cell Reviews and Reports"},{"issue":"2","key":"9916_CR32","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1007\/s12015-017-9792-7","volume":"14","author":"M Siemionow","year":"2018","unstructured":"Siemionow, M., Cwykiel, J., Heydemann, A., Garcia-Martinez, J., Siemionow, K., & Szilagyi, E. (2018). Creation of dystrophin expressing chimeric cells of myoblast origin as a novel stem cell based therapy for Duchenne muscular dystrophy. Stem Cell Reviews and Reports, 14(2), 189\u2013199.","journal-title":"Stem Cell Reviews and Reports"},{"issue":"11","key":"9916_CR33","doi-asserted-by":"crossref","first-page":"1949","DOI":"10.1038\/mt.2016.163","volume":"24","author":"C Sitzia","year":"2016","unstructured":"Sitzia, C., Farini, A., Jardim, L., Razini, P., Belicchi, M., Cassinelli, L., Villa, C., Erratico, S., Parolini, D., Bella, P., da Silva Bizario, J. C., Garcia, L., Dias-Baruffi, M., Meregalli, M., & Torrente, Y. (2016). Adaptive immune response impairs the efficacy of autologous transplantation of engineered stem cells in dystrophic dogs. Molecular therapy : the journal of the American Society of Gene Therapy, 24(11), 1949\u20131964.","journal-title":"Molecular therapy : the journal of the American Society of Gene Therapy"},{"issue":"9","key":"9916_CR34","doi-asserted-by":"crossref","first-page":"1307","DOI":"10.1517\/14712598.2015.1057564","volume":"15","author":"D Skuk","year":"2015","unstructured":"Skuk, D., & Tremblay, J. P. (2015). Cell therapy in muscular dystrophies: Many promises in mice and dogs, few facts in patients. Expert Opinion on Biological Therapy, 15(9), 1307\u20131319.","journal-title":"Expert Opinion on Biological Therapy"},{"issue":"5","key":"9916_CR35","doi-asserted-by":"crossref","first-page":"979","DOI":"10.1002\/mus.25129","volume":"54","author":"D Skuk","year":"2016","unstructured":"Skuk, D., & Tremblay, J. P. (2016). Confirmation of donor-derived dystrophin in a duchenne muscular dystrophy patient allotransplanted with normal myoblasts. Muscle & Nerve, 54(5), 979\u2013981.","journal-title":"Muscle & Nerve"},{"issue":"21","key":"9916_CR36","doi-asserted-by":"crossref","first-page":"6029","DOI":"10.1093\/hmg\/ddv316","volume":"24","author":"Y Zhang","year":"2015","unstructured":"Zhang, Y., Zhu, Y., Li, Y., Cao, J., Zhang, H., Chen, M., Wang, L., & Zhang, C. (2015). Long-term engraftment of myogenic progenitors from adipose-derived stem cells and muscle regeneration in dystrophic mice. Human Molecular Genetics, 24(21), 6029\u20136040.","journal-title":"Human Molecular Genetics"},{"issue":"2","key":"9916_CR37","first-page":"141","volume":"10","author":"BS Rajput","year":"2015","unstructured":"Rajput, B. S., Chakrabarti, S. K., Dongare, V. S., Ramirez, C. M., & Deb, K. D. (2015). Human umbilical cord mesenchymal stem cells in the treatment of Duchenne muscular dystrophy: Safety and feasibility study in India. Journal of Stem Cells, 10(2), 141\u2013156.","journal-title":"Journal of Stem Cells"},{"issue":"1","key":"9916_CR38","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.nmd.2006.10.003","volume":"17","author":"D Skuk","year":"2007","unstructured":"Skuk, D., Goulet, M., Roy, B., Piette, V., C\u00f4t\u00e9, C. H., Chapdelaine, P., Hogrel, J. Y., Paradis, M., Bouchard, J. P., Sylvain, M., Lachance, J. G., & Tremblay, J. P. (2007). First test of a \"high-density injection\" protocol for myogenic cell transplantation throughout large volumes of muscles in a Duchenne muscular dystrophy patient: Eighteen months follow-up. Neuromuscular Disorders, 17(1), 38\u201346.","journal-title":"Neuromuscular Disorders"},{"issue":"6","key":"9916_CR39","doi-asserted-by":"crossref","first-page":"563","DOI":"10.3727\/000000007783465064","volume":"16","author":"Y Torrente","year":"2007","unstructured":"Torrente, Y., Belicchi, M., Marchesi, C., D'antona, G., Cogiamanian, F., Pisati, F., Gavina, M., Giordano, R., Tonlorenzi, R., Fagiolari, G., Lamperti, C., Porretti, L., Lopa, R., Sampaolesi, M., Vicentini, L., Grimoldi, N., Tiberio, F., Songa, V., Baratta, P., Prelle, A., Forzenigo, L., Guglieri, M., Pansarasa, O., Rinaldi, C., Mouly, V., Butler-Browne, G. S., Comi, G. P., Biondetti, P., Moggio, M., Gaini, S. M., Stocchetti, N., Priori, A., D'angelo, M. G., Turconi, A., Bottinelli, R., Cossu, G., Rebulla, P., & Bresolin, N. (2007). Autologous transplantation of muscle-derived CD133+ stem cells in Duchenne muscle patients. Cell Transplantation, 16(6), 563\u2013577.","journal-title":"Cell Transplantation"},{"issue":"9","key":"9916_CR40","doi-asserted-by":"crossref","first-page":"970","DOI":"10.1038\/nm0997-970","volume":"3","author":"E Gussoni","year":"1997","unstructured":"Gussoni, E., Blau, H. M., & Kunkel, L. M. (1997). The fate of individual myoblasts after transplantation into muscles of DMD patients. Nature Medicine, 3(9), 970\u2013977.","journal-title":"Nature Medicine"},{"issue":"4","key":"9916_CR41","doi-asserted-by":"crossref","first-page":"448","DOI":"10.1007\/s12015-016-9659-3","volume":"12","author":"MV Pelatti","year":"2016","unstructured":"Pelatti, M. V., Gomes, J. P., Vieira, N. M., et al. (2016). Transplantation of human adipose mesenchymal stem cells in non-immunosuppressed GRMD dogs is a safe procedure. Stem Cell Reviews and Reports, 12(4), 448\u2013453.","journal-title":"Stem Cell Reviews and Reports"},{"issue":"6","key":"9916_CR42","doi-asserted-by":"crossref","first-page":"830","DOI":"10.1007\/s12015-014-9537-9","volume":"10","author":"MC Valadares","year":"2014","unstructured":"Valadares, M. C., Gomes, J. P., Castello, G., Assoni, A., Pellati, M., Bueno, C., Corselli, M., Silva, H., Bartolini, P., Vainzof, M., Margarido, P. F., Baracat, E., P\u00e9ault, B., & Zatz, M. (2014). Human adipose tissue derived pericytes increase life span in Utrn (tm1Ked) Dmd (mdx) \/J mice. Stem Cell Reviews and Reports, 10(6), 830\u2013840.","journal-title":"Stem Cell Reviews and Reports"},{"issue":"4","key":"9916_CR43","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1007\/s00005-015-0380-8","volume":"64","author":"M Hivelin","year":"2016","unstructured":"Hivelin, M., Klimczak, A., Cwykiel, J., Sonmez, E., Nasir, S., Gatherwright, J., & Siemionow, M. (2016). Immunomodulatory effects of different cellular therapies of bone marrow origin on Chimerism induction and maintenance across MHC barriers in a face Allotransplantation model. Archivum Immunologiae et Therapiae Experimentalis, 64(4), 299\u2013310.","journal-title":"Archivum Immunologiae et Therapiae Experimentalis"},{"issue":"5","key":"9916_CR44","doi-asserted-by":"crossref","first-page":"1625","DOI":"10.1016\/j.transproceed.2006.02.154","volume":"38","author":"S Ozmen","year":"2006","unstructured":"Ozmen, S., Ulusal, B. G., Ulusal, A. E., Izycki, D., Yoder, B., & Siemionow, M. (2006). Trafficking of donor-derived bone marrow correlates with chimerism and extension of composite allograft survival across MHC barrier. Transplantation Proceedings, 38(5), 1625\u20131633.","journal-title":"Transplantation Proceedings"},{"issue":"5","key":"9916_CR45","doi-asserted-by":"crossref","first-page":"2303","DOI":"10.1016\/j.transproceed.2005.03.127","volume":"37","author":"M Siemionow","year":"2005","unstructured":"Siemionow, M., Zielinski, M., Ozmen, S., & Izycki, D. (2005). Intraosseus transplantation of donor-derived hematopoietic stem and progenitor cells induces donor-specific chimerism and extends composite tissue allograft survival. Transplantation Proceedings, 37(5), 2303\u20132308.","journal-title":"Transplantation Proceedings"},{"issue":"1","key":"9916_CR46","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/j.transproceed.2004.12.216","volume":"37","author":"M Siemionow","year":"2005","unstructured":"Siemionow, M., Klimczak, A., & Unal, S. (2005). Different routes of donor-derived hematopoietic stem cell transplantation for donor-specific chimerism induction across MHC barrier. Transplantation Proceedings, 37(1), 62\u201364.","journal-title":"Transplantation Proceedings"},{"issue":"2","key":"9916_CR47","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1089\/hum.2011.147","volume":"23","author":"JH Shin","year":"2012","unstructured":"Shin, J. H., Yue, Y., Srivastava, A., Smith, B., Lai, Y., & Duan, D. (2012). A simplified immune suppression scheme leads to persistent micro-dystrophin expression in Duchenne muscular dystrophy dogs. Human Gene Therapy, 23(2), 202\u2013209.","journal-title":"Human Gene Therapy"},{"issue":"6","key":"9916_CR48","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1007\/s12015-017-9759-8","volume":"13","author":"D Macrin","year":"2017","unstructured":"Macrin, D., Joseph, J. P., Pillai, A. A., & Devi, A. (2017). Eminent sources of adult mesenchymal stem cells and their therapeutic imminence. Stem Cell Reviews and Reports, 13(6), 741\u2013756.","journal-title":"Stem Cell Reviews and Reports"},{"issue":"6","key":"9916_CR49","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1007\/s12015-017-9760-2","volume":"13","author":"GS Oggu","year":"2017","unstructured":"Oggu, G. S., Sasikumar, S., Reddy, N., Ella, K. K. R., Rao, C. M., & Bokara, K. K. (2017). Gene delivery approaches for mesenchymal stem cell therapy: Strategies to increase efficiency and specificity. Stem Cell Reviews and Reports, 13(6), 725\u2013740.","journal-title":"Stem Cell Reviews and Reports"},{"issue":"1","key":"9916_CR50","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1258\/00236770460734416","volume":"38","author":"G Szczesny","year":"2004","unstructured":"Szczesny, G., Veihelmann, A., Massberg, S., Nolte, D., & Messmer, K. (2004). Long-term anaesthesia using inhalatory isoflurane in different strains of mice-the haemodynamic effects. Laboratory Animals, 38(1), 64\u201369.","journal-title":"Laboratory Animals"},{"issue":"1","key":"9916_CR51","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1155\/2012\/909656","volume":"19","author":"J Lemay","year":"2012","unstructured":"Lemay, J., Series, F., Senechal, M., Maranda, B., & Maltais, F. (2012). Unusual respiratory manifestations in two young adults with Duchenne muscular dystrophy. Canadian Respiratory Journal, 19(1), 37\u201340.","journal-title":"Canadian Respiratory Journal"},{"issue":"8","key":"9916_CR52","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1016\/j.echo.2017.03.009","volume":"30","author":"Z Li","year":"2017","unstructured":"Li, Z., Li, Y., Zhang, L., Zhang, X., Sullivan, R., Ai, X., Szeto, C., Cai, A., Liu, L., Xiao, W., Li, Q., Ge, S., & Chen, X. (2017). Reduced myocardial Reserve in Young X-linked muscular dystrophy mice diagnosed by two-dimensional strain analysis combined with stress echocardiography. Journal of the American Society of Echocardiography: official publication of the American Society of Echocardiography, 30(8), 815\u2013827.","journal-title":"Journal of the American Society of Echocardiography: official publication of the American Society of Echocardiography"},{"issue":"1","key":"9916_CR53","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1111\/jcmm.13294","volume":"22","author":"Y Liu","year":"2018","unstructured":"Liu, Y., Tal, R., Pluchino, N., Mamillapalli, R., & Taylor, H. S. (2018). Systemic administration of bone marrow-derived cells leads to better uterine engraftment than use of uterine-derived cells or local injection. Journal of Cellular and Molecular Medicine, 22(1), 67\u201376.","journal-title":"Journal of Cellular and Molecular Medicine"},{"issue":"6","key":"9916_CR54","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1016\/j.nmd.2016.03.008","volume":"26","author":"L. van den Engel-Hoek","year":"2016","unstructured":"van den Engel-Hoek, L., de Groot, I.J., Sie, L.T., et. al. (2016). Dystrophic changes in masticatory muscles related chewing problems and malocclusions in Duchenne muscular dystrophy. Neuromuscular Disorders, 26(6), 354\u2013360.","journal-title":"Neuromuscular Disorders"},{"issue":"3","key":"9916_CR55","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1016\/j.jacbts.2018.03.007","volume":"3","author":"HM Viola","year":"2018","unstructured":"Viola, H. M., Johnstone, V. P. A., Adams, A. M., Fletcher, S., & Hool, L. C. (2018). A Morpholino oligomer therapy regime that restores mitochondrial function and prevents mdx cardiomyopathy. JACC Basic to Translational Science, 3(3), 391\u2013402.","journal-title":"JACC Basic to Translational Science"},{"issue":"3","key":"9916_CR56","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1111\/echo.12351","volume":"31","author":"TG Andrews","year":"2014","unstructured":"Andrews, T. G., Lindsey, M. L., Lange, R. A., & Aune, G. J. (2014). Cardiac assessment in pediatric mice: Strain analysis as a diagnostic measurement. Echocardiography, 31(3), 375\u2013384.","journal-title":"Echocardiography"},{"issue":"3","key":"9916_CR57","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1002\/nbm.1164","volume":"20","author":"A Feintuch","year":"2007","unstructured":"Feintuch, A., Zhu, Y., Bishop, J., Davidson, L., Dazai, J., Bruneau, B. G., & Henkelman, R. M. (2007). 4D cardiac MRI in the mouse. NMR in Biomedicine, 20(3), 360\u2013365.","journal-title":"NMR in Biomedicine"},{"issue":"5","key":"9916_CR58","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1136\/hrt.2007.132803","volume":"96","author":"AM Johri","year":"2010","unstructured":"Johri, A. M., Passeri, J. J., & Picard, M. H. (2010). Three dimensional echocardiography: Approaches and clinical utility. Heart, 96(5), 390\u2013397.","journal-title":"Heart"},{"issue":"1","key":"9916_CR59","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1177\/1074248410381757","volume":"16","author":"CF Spurney","year":"2011","unstructured":"Spurney, C. F., Sali, A., Guerron, A. D., Iantorno, M., Yu, Q., Gordish-Dressman, H., Rayavarapu, S., van der Meulen, J., Hoffman, E. P., & Nagaraju, K. (2011). Losartan decreases cardiac muscle fibrosis and improves cardiac function in dystrophin-deficient mdx mice. Journal of Cardiovascular Pharmacology and Therapeutics, 16(1), 87\u201395.","journal-title":"Journal of Cardiovascular Pharmacology and Therapeutics"},{"issue":"4","key":"9916_CR60","doi-asserted-by":"crossref","first-page":"600","DOI":"10.1002\/mus.21763","volume":"42","author":"B Bostick","year":"2010","unstructured":"Bostick, B., Yue, Y., & Duan, D. (2010). Gender influences cardiac function in the mdx model of Duchenne cardiomyopathy. Muscle & Nerve, 42(4), 600\u2013603.","journal-title":"Muscle & Nerve"},{"issue":"6","key":"9916_CR61","doi-asserted-by":"crossref","first-page":"H2134","DOI":"10.1152\/ajpheart.00845.2001","volume":"282","author":"DM Roth","year":"2002","unstructured":"Roth, D. M., Swaney, J. S., Dalton, N. D., Gilpin, E. A., & Ross, J., Jr. (2002). Impact of anesthesia on cardiac function during echocardiography in mice. American Journal of Physiology. Heart and Circulatory Physiology, 282(6), H2134\u2013H2140.","journal-title":"American Journal of Physiology. Heart and Circulatory Physiology"}],"container-title":["Stem Cell Reviews and Reports"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s12015-019-09916-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s12015-019-09916-0\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s12015-019-09916-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,7,25]],"date-time":"2024-07-25T00:52:54Z","timestamp":1721868774000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s12015-019-09916-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,10,15]]},"references-count":61,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2019,12]]}},"alternative-id":["9916"],"URL":"https:\/\/doi.org\/10.1007\/s12015-019-09916-0","relation":{},"ISSN":["2629-3269","2629-3277"],"issn-type":[{"value":"2629-3269","type":"print"},{"value":"2629-3277","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,10,15]]},"assertion":[{"value":"15 October 2019","order":1,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Compliance with Ethical Standards"}},{"value":"MS is CMO and shareholder of Dystrogen Therapeutics SA, the company holds a license for DEC Therapy. The author declares a potential conflict of interest. MS is the inventor on the patent application filed by University of Illinois at Chicago related to chimeric cell therapy for Duchenne muscular dystrophy (WO\/2016\/201182). AH is the adviser to the Dystrogen Therapeutics.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of Financial Interests"}},{"value":"The authors MS, MM, PL, JC, SB and AH do not have any non-financial conflict of interest.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of Non-Financial Interest"}}]}}