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Human skeletal muscle fibroblasts stimulate in vitro myogenesis and in vivo muscle regeneration

The Journal of physiology, 2017-08, Vol.595 (15), p.5115-5127 [Peer Reviewed Journal]

2017 The Authors. The Journal of Physiology © 2017 The Physiological Society ;2017 The Authors. The Journal of Physiology © 2017 The Physiological Society. ;Journal compilation © 2017 The Physiological Society ;ISSN: 0022-3751 ;EISSN: 1469-7793 ;DOI: 10.1113/JP273997 ;PMID: 28369879

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Title:
Human skeletal muscle fibroblasts stimulate in vitro myogenesis and in vivo muscle regeneration
Author: Mackey, Abigail L. ; Magnan, Mélanie ; Chazaud, Bénédicte ; Kjaer, Michael
Subjects: Adult ; Antigens, CD - physiology ; Antigens, Differentiation, Myelomonocytic - physiology ; Biopsy ; Cell culture ; Cell fusion ; Cell number ; Cell proliferation ; Cells, Cultured ; Coculture Techniques ; co‐culture ; Cross sections ; Desmin ; Differentiation ; Diseases ; Electric Stimulation ; Embryos ; Extracellular matrix ; Fibers ; Fibroblasts ; Fibroblasts - physiology ; Human Umbilical Vein Endothelial Cells - physiology ; Humans ; In vitro methods and tests ; Leukocyte Common Antigens - physiology ; Macrophages - physiology ; Male ; Matrix protein ; Men ; Molecular and cellular ; Muscle Contraction ; Muscle Development - physiology ; Muscle, Skeletal - injuries ; Muscle, Skeletal - physiology ; Musculoskeletal system ; Myoblasts - physiology ; Myogenesis ; Myogenin ; Myosin ; Neonates ; Physiology ; Protein sources ; Regeneration - physiology ; Research Paper ; Rodents ; Sarcopenia ; Satellite cells ; Skeletal muscle ; skeletal muscle derived fibroblasts ; skeletal muscle regeneration ; Stimulation ; Transcription Factor 7-Like 2 Protein - physiology
Is Part Of: The Journal of physiology, 2017-08, Vol.595 (15), p.5115-5127
Description: Key points Accumulation of skeletal muscle extracellular matrix is an unfavourable characteristic of many muscle diseases, muscle injury and sarcopenia. The extent of cross‐talk between fibroblasts, as the source of matrix protein, and satellite cells in humans is unknown. We studied this in human muscle biopsies and cell‐culture studies. We observed a strong stimulation of myogenesis by human fibroblasts in cell culture. In biopsies collected 30 days after a muscle injury protocol, fibroblast number increased to four times control levels, where fibroblasts were found to be preferentially located immediately surrounding regenerating muscle fibres. These novel findings indicate an important role for fibroblasts in supporting the regeneration of muscle fibres, potentially through direct stimulation of satellite cell differentiation and fusion, and contribute to understanding of cell–cell cross‐talk during physiological and pathological muscle remodelling. Accumulation of skeletal muscle extracellular matrix is an unfavourable characteristic of many muscle diseases, muscle injury and sarcopenia. In addition to the indispensable role satellite cells play in muscle regeneration, there is emerging evidence in rodents for a regulatory influence on fibroblast activity. However, the influence of fibroblasts on satellite cells and muscle regeneration in humans is unknown. The purpose of this study was to investigate this in vitro and during in vivo regeneration in humans. Following a muscle injury protocol in young healthy men (n = 7), the number of fibroblasts (TCF7L2+), satellite cells (Pax7+), differentiating myogenic cells (myogenin+) and regenerating fibres (neonatal/embryonic myosin+) was determined from biopsy cross‐sections. Fibroblasts and myogenic precursor cells (MPCs) were also isolated from human skeletal muscle (n = 4) and co‐cultured using different cell ratios, with the two cell populations either in direct contact with each other or separated by a permeable membrane. MPC proliferation, differentiation and fusion were assessed from cells stained for BrdU, desmin and myogenin. On biopsy cross‐sections, fibroblast number was seen to increase, along with myogenic cell number, by d7 and increase further by d30, where fibroblasts were observed to be preferentially located immediately surrounding regenerating muscle fibres. In vitro, the presence of fibroblasts in direct contact with MPCs was found to moderately stimulate MPC proliferation and strongly stimulate both MPC differentiation and MPC fusion. It thus appears, in humans, that fibroblasts exert a strong positive regulatory influence on MPC activity, in line with observations during in vivo skeletal muscle regeneration. Key points Accumulation of skeletal muscle extracellular matrix is an unfavourable characteristic of many muscle diseases, muscle injury and sarcopenia. The extent of cross‐talk between fibroblasts, as the source of matrix protein, and satellite cells in humans is unknown. We studied this in human muscle biopsies and cell‐culture studies. We observed a strong stimulation of myogenesis by human fibroblasts in cell culture. In biopsies collected 30 days after a muscle injury protocol, fibroblast number increased to four times control levels, where fibroblasts were found to be preferentially located immediately surrounding regenerating muscle fibres. These novel findings indicate an important role for fibroblasts in supporting the regeneration of muscle fibres, potentially through direct stimulation of satellite cell differentiation and fusion, and contribute to understanding of cell–cell cross‐talk during physiological and pathological muscle remodelling.
Publisher: England: Wiley Subscription Services, Inc
Language: English
Identifier: ISSN: 0022-3751
EISSN: 1469-7793
DOI: 10.1113/JP273997
PMID: 28369879
Source: PubMed Central (Open access)
Geneva Foundation Free Medical Journals at publisher websites
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Human skeletal muscle fibroblasts stimulate in vitro myogenesis and in vivo muscle regeneration

2017 The Authors. The Journal of Physiology © 2017 The Physiological Society ;2017 The Authors. The Journal of Physiology © 2017 The Physiological Society. ;Journal compilation © 2017 The Physiological Society ;ISSN: 0022-3751 ;EISSN: 1469-7793 ;DOI: 10.1113/JP273997 ;PMID: 28369879

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