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      Autologous transplantation of adipose-derived stem cells improves functional recovery of skeletal muscle without direct participation in new myofiber formation

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          Abstract

          Background

          Skeletal muscle has a remarkable regenerative capacity. However, extensive damage that exceeds the self-regenerative ability of the muscle can lead to irreversible fibrosis, scarring, and significant loss of function. Adipose-derived stem cells (ADSC) are a highly abundant source of progenitor cells that have been previously reported to support the regeneration of various muscle tissues, including striated muscles. The aim of this study was to evaluate the effect of ADSC transplantation on functional skeletal muscle regeneration in an acute injury model.

          Methods

          Mouse ADSC were isolated from subcutaneous fat tissue and transplanted with a collagen hydrogel into the crushed tibialis anterior muscle of mice. Recovering muscles were analyzed for gene and protein expression by real-time quantitative polymerase chain reaction and immunohistochemistry. The muscle contractility was assessed by myography in an organ bath system.

          Results

          Intramuscular transplantation of ADSC into crushed tibialis anterior muscle leads to an improved muscle regeneration with ADSC residing in the damaged area. We did not observe ADSC differentiation into new muscle fibers or endothelial cells. However, the ADSC-injected muscles had improved contractility in comparison with the collagen-injected controls 28 days post-transplantation. Additionally, an increase in fiber cross-sectional size and in the number of mature fibers with centralized nuclei was observed.

          Conclusions

          ADSC transplantation into acute damaged skeletal muscle significantly improves functional muscle tissue regeneration without direct participation in muscle fiber formation. Cellular therapy with ADSC represents a novel approach to promote skeletal muscle regeneration.

          Electronic supplementary material

          The online version of this article (10.1186/s13287-018-0922-1) contains supplementary material, which is available to authorized users.

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          Most cited references38

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          Myogenic satellite cells: physiology to molecular biology.

          T J Hawke, D Garry (2001)
          Adult skeletal muscle has a remarkable ability to regenerate following myotrauma. Because adult myofibers are terminally differentiated, the regeneration of skeletal muscle is largely dependent on a small population of resident cells termed satellite cells. Although this population of cells was identified 40 years ago, little is known regarding the molecular phenotype or regulation of the satellite cell. The use of cell culture techniques and transgenic animal models has improved our understanding of this unique cell population; however, the capacity and potential of these cells remain ill-defined. This review will highlight the origin and unique markers of the satellite cell population, the regulation by growth factors, and the response to physiological and pathological stimuli. We conclude by highlighting the potential therapeutic uses of satellite cells and identifying future research goals for the study of satellite cell biology.
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            Adipose tissue derived stem cells secretome: soluble factors and their roles in regenerative medicine.

            António J Braga Osório Gomes Salgado, RuI Reis, Nuno Jorge Carvalho Sousa … (2010)
            Stem cells have been long looked at as possible therapeutic vehicles for different health related problems. Among the different existing stem cell populations, Adipose- derived Stem Cells (ASCs) have been gathering attention in the last 10 years. When compared to other stem cells populations and sources, ASCs can be easily isolated while providing simultaneously higher yields upon the processing of adipose tissue. Similar to other stem cell populations, it was initially thought that the main potential of ASCs for regenerative medicine approaches was intimately related to their differentiation capability. Although this is true, there has been an increasing body of literature describing the trophic effects of ASCs on the protection, survival and differentiation of variety of endogenous cells/tissues. Moreover, they have also shown to possess an immunomodulatory character. This effect is closely related to the ASCs' secretome and the soluble factors found within it. Molecules such as hepatocyte growth factor (HGF), granulocyte and macrophage colony stimulating factors, interleukins (ILs) 6, 7, 8 and 11, tumor necrosis factor-alpha (TNF-alpha), vascular endothelial growth factor (VEGF), brain derived neurotrophic factor (BDNF), nerve growth factor (NGF), adipokines and others have been identified within the ASCs' secretome. Due to its importance regarding future applications for the field of regenerative medicine, we aim, in the present review, to make a comprehensive analysis of the literature relating to the ASCs' secretome and its relevance to the immune and central nervous system, vascularization and cardiac regeneration. The concluding section will highlight some of the major challenges that remain before ASCs can be used for future clinical applications.
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              Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells.

              Francesco Saverio Tedesco, Arianna Dellavalle, Jordi Díaz-Manera … (2010)
              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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                Author and article information

                Contributors
                Agata Gorecka: agata.gorecka@dbmr.unibe.ch
                Souzan Salemi: souzan.salemi@usz.ch
                Deana Haralampieva: deana.haralampieva@usz.ch
                Federica Moalli: federica.moalli@tki.unibe.ch , moalli.federica@hsr.it
                Deborah Stroka: deborah.stroka@dbmr.unibe.ch
                Daniel Candinas: daniel.candinas@insel.ch
                Daniel Eberli: daniel.eberli@usz.ch
                Lukas Brügger:
                ORCID: http://orcid.org/0000-0001-7578-2295
                +41 76 340 19 66 , lukas.bruegger@insel.ch
                Journal
                Journal ID (nlm-ta): Stem Cell Res Ther
                Journal ID (iso-abbrev): Stem Cell Res Ther
                Title: Stem Cell Research & Therapy
                Publisher: BioMed Central (London )
                ISSN (Electronic): 1757-6512
                Publication date (Electronic): 17 July 2018
                Publication date PMC-release: 17 July 2018
                Publication date Collection: 2018
                Volume: 9
                Electronic Location Identifier: 195
                Affiliations
                [1 ]ISNI 0000 0001 0726 5157, GRID grid.5734.5, Department of Clinical Research, Laboratory for Visceral Surgery and Medicine, , University of Bern, ; Murtenstrasse 35, 3008 Bern, Switzerland
                [2 ]ISNI 0000 0004 0478 9977, GRID grid.412004.3, Department of Urology, Laboratory for Tissue Engineering and Stem Cell Therapy, , University Hospital Zurich, ; Zurich, Switzerland
                [3 ]ISNI 0000 0004 0479 0855, GRID grid.411656.1, University Clinic for Visceral Surgery and Medicine, Bauchzentrum Bern, , Inselspital, ; CH-3010 Bern, Switzerland
                [4 ]ISNI 0000 0001 0726 5157, GRID grid.5734.5, Theodor Kocher Institute, University of Bern, ; Bern, Switzerland
                [5 ]ISNI 0000000417581884, GRID grid.18887.3e, Current address: Division of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific Institute, ; Milan, Italy
                Author information
                http://orcid.org/0000-0001-7578-2295
                Article
                Publisher ID: 922
                DOI: 10.1186/s13287-018-0922-1
                PMC ID: 6050693
                PubMed ID: 30016973
                SO-VID: 71e80ff5-eb90-4714-9aa7-7eaab2e6946b
                Copyright © © The Author(s). 2018
                License:

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                Date received : 17 November 2017
                Date revision received : 29 May 2018
                Date accepted : 8 June 2018
                Funding
                Funded by: Ruth & Arthur Scherbarth Stiftung, Switzerland
                Categories
                Subject: Research
                Custom metadata
                issue-copyright-statement © The Author(s) 2018

                ScienceOpen disciplines: Molecular medicine
                Keywords: adipose-derived stem cells,crush injury,skeletal muscle regeneration,stem cell therapy,tissue engineering
                Data availability:
                ScienceOpen disciplines: Molecular medicine
                Keywords: adipose-derived stem cells, crush injury, skeletal muscle regeneration, stem cell therapy, tissue engineering

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