Isolation and characterization of myogenic precursor cells from human cremaster muscle

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.

Contributors

María Fernanda Lara: [e-mail]

Ander Izeta:

ORCID: http://orcid.org/0000-0003-1879-7401

[e-mail]

Journal

Journal ID (nlm-ta): Sci Rep

Journal ID (iso-abbrev): Sci Rep

Title: Scientific Reports

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2045-2322

Publication date (Electronic): 5 March 2019

Publication date PMC-release: 5 March 2019

Publication date Collection: 2019

Volume: 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

Publisher ID: 40042

DOI: 10.1038/s41598-019-40042-6

PMC ID: 6401155

Copyright statement: © The Author(s) 2019

License:

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 : Neia Naldaiz-Gastesi Adolfo López de Munain

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 : Adolfo López de Munain Ander Izeta

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 : Ander Izeta

Categories

Subject: Article

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issue-copyright-statement © The Author(s) 2019