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      Isolation and characterization of myogenic precursor cells from human cremaster muscle

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          Abstract

          Human myogenic precursor cells have been isolated and expanded from a number of skeletal muscles, but alternative donor biopsy sites must be sought after in diseases where muscle damage is widespread. Biopsy sites must be relatively accessible, and the biopsied muscle dispensable. Here, we aimed to histologically characterize the cremaster muscle with regard number of satellite cells and regenerative fibres, and to isolate and characterize human cremaster muscle-derived stem/precursor cells in adult male donors with the objective of characterizing this muscle as a novel source of myogenic precursor cells. Cremaster muscle biopsies (or adjacent non-muscle tissue for negative controls; N = 19) were taken from male patients undergoing routine surgery for urogenital pathology. Myosphere cultures were derived and tested for their in vitro and in vivo myogenic differentiation and muscle regeneration capacities. Cremaster-derived myogenic precursor cells were maintained by myosphere culture and efficiently differentiated to myotubes in adhesion culture. Upon transplantation to an immunocompromised mouse model of cardiotoxin-induced acute muscle damage, human cremaster-derived myogenic precursor cells survived to the transplants and contributed to muscle regeneration. These precursors are a good candidate for cell therapy approaches of skeletal muscle. Due to their location and developmental origin, we propose that they might be best suited for regeneration of the rhabdosphincter in patients undergoing stress urinary incontinence after radical prostatectomy.

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          Most cited references 66

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          Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells.

          Skeletal muscle damaged by injury or by degenerative diseases such as muscular dystrophy is able to regenerate new muscle fibers. Regeneration mainly depends upon satellite cells, myogenic progenitors localized between the basal lamina and the muscle fiber membrane. However, other cell types outside the basal lamina, such as pericytes, also have myogenic potency. Here, we discuss the main properties of satellite cells and other myogenic progenitors as well as recent efforts to obtain myogenic cells from pluripotent stem cells for patient-tailored cell therapy. Clinical trials utilizing these cells to treat muscular dystrophies, heart failure, and stress urinary incontinence are also briefly outlined.
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            Human ES- and iPS-derived myogenic progenitors restore DYSTROPHIN and improve contractility upon transplantation in dystrophic mice.

            A major obstacle in the application of cell-based therapies for the treatment of neuromuscular disorders is obtaining the appropriate number of stem/progenitor cells to produce effective engraftment. The use of embryonic stem (ES) or induced pluripotent stem (iPS) cells could overcome this hurdle. However, to date, derivation of engraftable skeletal muscle precursors that can restore muscle function from human pluripotent cells has not been achieved. Here we applied conditional expression of PAX7 in human ES/iPS cells to successfully derive large quantities of myogenic precursors, which, upon transplantation into dystrophic muscle, are able to engraft efficiently, producing abundant human-derived DYSTROPHIN-positive myofibers that exhibit superior strength. Importantly, transplanted cells also seed the muscle satellite cell compartment, and engraftment is present over 11 months posttransplant. This study provides the proof of principle for the derivation of functional skeletal myogenic progenitors from human ES/iPS cells and highlights their potential for future therapeutic application in muscular dystrophies. Copyright © 2012 Elsevier Inc. All rights reserved.
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              Making muscle: skeletal myogenesis in vivo and in vitro

              Skeletal muscle is the largest tissue in the body and loss of its function or its regenerative properties results in debilitating musculoskeletal disorders. Understanding the mechanisms that drive skeletal muscle formation will not only help to unravel the molecular basis of skeletal muscle diseases, but also provide a roadmap for recapitulating skeletal myogenesis in vitro from pluripotent stem cells (PSCs). PSCs have become an important tool for probing developmental questions, while differentiated cell types allow the development of novel therapeutic strategies. In this Review, we provide a comprehensive overview of skeletal myogenesis from the earliest premyogenic progenitor stage to terminally differentiated myofibers, and discuss how this knowledge has been applied to differentiate PSCs into muscle fibers and their progenitors in vitro.
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                Author and article information

                Contributors
                mf.lara@fimabis.org
                ander.izeta@biodonostia.org
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                5 March 2019
                5 March 2019
                2019
                : 9
                Affiliations
                [1 ]GRID grid.432380.e, Tissue Engineering group, , Instituto Biodonostia, ; San Sebastian, Spain
                [2 ]GRID grid.432380.e, Neuromuscular diseases group, , Instituto Biodonostia, ; San Sebastian, Spain
                [3 ]ISNI 0000 0000 9314 1427, GRID grid.413448.e, Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas (CIBERNED), Instituto de Salud Carlos III, ; Madrid, Spain
                [4 ]CNIO-IBIMA Genitourinary Cancer Research Unit, Institute of Biomedical Research in Málaga (IBIMA), Málaga, Spain
                [5 ]ISNI 0000 0000 9788 2492, GRID grid.411062.0, Urology Department, , Hospital Universitario Virgen de la Victoria, ; Málaga, Spain
                [6 ]ISNI 0000000121671098, GRID grid.11480.3c, Department of Neurosciences, , Faculty of Medicine and Dentistry, UPV-EHU, ; San Sebastian, Spain
                [7 ]GRID grid.414651.3, Department of Neurology, , Hospital Universitario Donostia, ; San Sebastian, Spain
                [8 ]ISNI 0000 0000 9788 2492, GRID grid.411062.0, Department of Surgery, , Hospital Universitario Virgen de la Victoria, ; Málaga, Spain
                [9 ]ISNI 0000000463436020, GRID grid.488737.7, Health Research Institute of Aragón (IIS Aragón), ; Zaragoza, Spain
                [10 ]ISNI 0000 0000 9314 1427, GRID grid.413448.e, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), Instituto de Salud Carlos III, ; Madrid, Spain
                [11 ]GRID grid.419651.e, Health Research Institute of Jiménez Díaz Foundation (IIS FJD), ; Madrid, Spain
                [12 ]ISNI 0000 0001 2168 9183, GRID grid.7840.b, Biomedical and Aerospace Engineering Department, , University Carlos III of Madrid, ; Madrid, Spain
                [13 ]Digital industry, Product design, IDONIAL Technology Center, Gijón, Spain
                [14 ]ISNI 0000000419370271, GRID grid.5924.a, Department of Biomedical Engineering and Science, , School of Engineering, Tecnun-University of Navarra, ; San Sebastian, Spain
                [15 ]Present Address: Viralgen Vector Core, San Sebastian, Spain
                Article
                40042
                10.1038/s41598-019-40042-6
                6401155
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                Funding
                Funded by: FundRef https://doi.org/10.13039/501100003086, Eusko Jaurlaritza (Basque Government);
                Award ID: PRE2013-1-1168
                Award ID: RIS3 2017222021
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100004587, Ministry of Economy and Competitiveness | Instituto de Salud Carlos III (Institute of Health Carlos III);
                Award ID: PI17/01841
                Award ID: PI14/00436
                Award ID: PI13/02172
                Award ID: PI16/01430
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100003329, Ministerio de Economía y Competitividad (Ministry of Economy and Competitiveness);
                Award ID: RTC-2015-3750-1
                Award Recipient :
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