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      Skeletal muscle satellite cells are located at a closer proximity to capillaries in healthy young compared with older men

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          Abstract

          Background

          Skeletal muscle satellite cells (SC) are instrumental in maintenance of muscle fibres, the adaptive responses to exercise, and there is an age‐related decline in SC. A spatial relationship exists between SC and muscle fibre capillaries. In the present study, we aimed to investigate whether chronologic age has an impact on the spatial relationship between SC and muscle fibre capillaries. Secondly, we determined whether this spatial relationship changes in response to a single session of resistance exercise.

          Methods

          Muscle biopsies were obtained from the vastus lateralis of previously untrained young men (YM, 24 ± 3 years; n = 23) and older men (OM, 67 ± 4 years; n = 22) at rest. A subset of YM ( n = 9) performed a single bout of resistance exercise, where additional muscle biopsies taken at 24 and 72 h post‐exercise recovery. Skeletal muscle fibre capillarization, SC content, and activation status were assessed using immunofluorescent microscopy of muscle cross sections.

          Results

          Type II muscle fibre SC and capillary content was significantly lower in the YM compared with OM ( P < 0.05). Furthermore, type II muscle fibre SC were located at a greater distance from the nearest capillary in OM compared with YM (21.6 ± 1.3 vs. 17.0 ± 0.8 µm, respectively; P < 0.05). In response to a single bout of exercise, we observed a significant increase in SC number and activation status ( P < 0.05). In addition, activated vs. quiescent SC were situated closer ( P < 0.05) to capillaries.

          Conclusions

          We demonstrate that there is a greater distance between capillaries and type II fibre‐associated SC in OM as compared with YM. Furthermore, quiescent SC are located significantly further away from capillaries than active SC after single bout of exercise. Our data have implications for how muscle adapts to exercise and how aging may affect such adaptations.

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          Most cited references20

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          MyoD is required for myogenic stem cell function in adult skeletal muscle.

          To investigate the function of MyoD in adult skeletal muscle, we interbred MyoD mutant mice with mdx mice, a model for Duchenne and Becker muscular dystrophy. Mice lacking both MyoD and dystrophin displayed a marked increase in severity of myopathy leading to premature death, suggesting a role for MyoD in muscle regeneration. Examination of MyoD mutant muscle revealed elevated numbers of myogenic cells; however, myoblasts derived from these cells displayed normal differentiation potential in vitro. Following injury, MyoD mutant muscle was severely deficient in regenerative ability, and we observed a striking reduction in the in vivo proliferation of myogenic cells during regeneration. Therefore, we propose that the failure of MyoD-deficient muscle to regenerate efficiently is not caused by a reduction in numbers of satellite cells, the stem cells of adult skeletal muscle, but results from an increased propensity for stem-cell self-renewal rather than progression through the myogenic program.
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            Human aging, muscle mass, and fiber type composition.

            J Lexell (1995)
            To assess the age-related loss of muscle mass and to determine the mechanisms behind this aging atrophy, the muscle structure and fiber type composition have been estimated, using invasive and noninvasive techniques. Limb muscles from older men and women are 25-35% smaller and have significantly more fat and connective tissue than limb muscles from younger individuals. Comparisons of muscle biopsies from younger and older individuals reveal that type 2 (fast-twitch) fibers are smaller in the old, while the size of type 1 (slow-twitch) fibers is much less affected. Studies of whole muscle cross sections also show a significantly smaller number of muscle fibers, a significantly lower relative type 2 fiber area, and a significant increase in fiber type grouping with increasing age. These results indicate a gradual decrease in size/volume with advancing age, accompanied by a replacement by fat and connective tissue. This aging atrophy seems to be due to a reduction in both number and size of muscle fibers, mainly of type 2, and is to some extent caused by a slowly progressive neurogenic process.
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              Satellite cells in human skeletal muscle plasticity

              Skeletal muscle satellite cells are considered to play a crucial role in muscle fiber maintenance, repair and remodeling. Our knowledge of the role of satellite cells in muscle fiber adaptation has traditionally relied on in vitro cell and in vivo animal models. Over the past decade, a genuine effort has been made to translate these results to humans under physiological conditions. Findings from in vivo human studies suggest that satellite cells play a key role in skeletal muscle fiber repair/remodeling in response to exercise. Mounting evidence indicates that aging has a profound impact on the regulation of satellite cells in human skeletal muscle. Yet, the precise role of satellite cells in the development of muscle fiber atrophy with age remains unresolved. This review seeks to integrate recent results from in vivo human studies on satellite cell function in muscle fiber repair/remodeling in the wider context of satellite cell biology whose literature is largely based on animal and cell models.
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                Author and article information

                Contributors
                pariseg@mcmaster.ca
                Journal
                J Cachexia Sarcopenia Muscle
                J Cachexia Sarcopenia Muscle
                10.1007/13539.2190-6009
                JCSM
                Journal of Cachexia, Sarcopenia and Muscle
                John Wiley and Sons Inc. (Hoboken )
                2190-5991
                2190-6009
                15 February 2016
                December 2016
                : 7
                : 5 ( doiID: 10.1002/jcsm.v7.5 )
                : 547-554
                Affiliations
                [ 1 ] Department of KinesiologyMcMaster University Hamilton OntarioCanada L8S 4L8
                [ 2 ] Department of Medical Physics and Applied Radiation SciencesMcMaster University Hamilton OntarioCanada L8S 4L8
                [ 3 ] Department of MedicineMcMaster University Hamilton OntarioCanada L8S 4L8
                Author notes
                [*] [* ]Correspondence to: Gianni Parise, Departments of Kinesiology and Medical Physics and Applied Radiation Sciences, McMaster University, Hamilton, Ontario, Canada L8S 4L8, Tel.: 905 525 9140 ext. 27353, Email: pariseg@ 123456mcmaster.ca
                Article
                JCSM12105 JCSM-D-15-00152
                10.1002/jcsm.12105
                4864218
                27239425
                e8a157c6-877b-40eb-87d4-c1e961d19203
                © 2016 The Authors. Journal of Cachexia, Sarcopenia and Muscle published by John Wiley & Sons Ltd on behalf of the Society of Sarcopenia, Cachexia and Wasting Disorders

                This is an open access article under the terms of the Creative Commons Attribution‐NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

                History
                : 10 September 2015
                : 06 January 2016
                : 25 January 2016
                Page count
                Figures: 2, Tables: 4, Pages: 8, Words: 3719
                Funding
                Funded by: Natural Sciences and Engineering Research Council of Canada (NSERC)
                Award ID: 1455843
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                jcsm12105
                jcsm12105-hdr-0001
                December 2016
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.7 mode:remove_FC converted:18.11.2016

                Orthopedics
                muscle stem cells,pax7,myod,capillaries,perfusion
                Orthopedics
                muscle stem cells, pax7, myod, capillaries, perfusion

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