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Cited by 149Muscle Physiology and DisordersMuscle metabolism and nutritionExercise and Physiological Responses

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The Acute Satellite Cell Response and Skeletal Muscle Hypertrophy following Resistance Training

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Bellamy, Leeann M., Joanisse, Sophie, Grubb, Amanda, Mitchell, Cameron J., McKay, Bryon R., Phillips, Stuart M., Baker, Steven, Parise, Gianni·2014·PLoS ONE
DOI 10.1371/journal.pone.0109739PMC PMC4196938
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Abstract

The extent of skeletal muscle hypertrophy in response to resistance training is highly variable in humans. The main objective of this study was to explain the nature of this variability. More specifically, we focused on the myogenic stem cell population, the satellite cell (SC) as a potential mediator of hypertrophy. Twenty-three males (aged 18-35 yrs) participated in 16 wk of progressive, whole body resistance training, resulting in changes of 7.9±1.6% (range of -1.9-24.7%) and 21.0±4.0% (range of -7.0 to 51.7%) in quadriceps volume and myofibre cross-sectional area (CSA), respectively. The SC response to a single bout of resistance exercise (80% 1RM), analyzed via immunofluorescent staining resulted in an expansion of type II fibre associated SC 72 h following exercise (pre: 11.3±0.9; 72 h: 14.8±1.4 SC/type II fibre; p<0.05). Training resulted in an expansion of the SC pool associated with type I (pre: 10.7±1.1; post: 12.1±1.2 SC/type I fibre; p<0.05) and type II fibres (pre: 11.3±0.9; post: 13.0±1.2 SC/type II fibre; p<0.05). Analysis of individual SC responses revealed a correlation between the relative change in type I associated SC 24 to 72 hours following an acute bout of resistance exercise and the percentage increase in quadriceps lean tissue mass assessed by MRI (r2 = 0.566, p = 0.012) and the relative change in type II associated SC following 16 weeks of resistance training and the percentage increase in quadriceps lean tissue mass assessed by MRI (r2 = 0.493, p = 0.027). Our results suggest that the SC response to resistance exercise is related to the extent of muscular hypertrophy induced by training.

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Figure 1 Skeletal muscle hypertrophy following training. Skeletal muscle hypertrophy was assessed by taking measures pre- and post-training using (A) DEXA, (B) MRI, and (C and D) cross-sectional area specific to both type 1 and type 2 fibers respectively. Significant increases were seen in all measures. * denotes a significant difference from pre-training (p<0.001).
Figure 1 Skeletal muscle hypertrophy following training. Skeletal muscle hypertrophy was assessed by taking measures pre- and post-training using (A) DEXA, (B) MRI, and (C and D) cross-sectional area specific to both type 1 and type 2 fibers respectively. Significant increases were seen in all measures. * denotes a significant difference from pre-training (p<0.001).CC BY · PubMed Central
Figure 2 Myonuclear contribution to muscle hypertrophy. Myonuclear content and fibre size were quantified by visualization of nuclei (Pax7/DAPI) and myofibre borders (laminin) on muscle cross sections. Calculations of (A) myonuclear domain (fibre area (µm2) per nucleus) and (B) nuclei per muscle fibre cross section are reported. * denotes a significant difference from pre-training (p<0.05).
Figure 2 Myonuclear contribution to muscle hypertrophy. Myonuclear content and fibre size were quantified by visualization of nuclei (Pax7/DAPI) and myofibre borders (laminin) on muscle cross sections. Calculations of (A) myonuclear domain (fibre area (µm2) per nucleus) and (B) nuclei per muscle fibre cross section are reported. * denotes a significant difference from pre-training (p<0.05).CC BY · PubMed Central
Figure 3 The SC response to an acute bout of resistance exercise and to 16 wks of resistance training. (A), representative image (merge) of a Pax7/Laminin/MHCI/MCHII immunofluorescent stain. Arrow denotes a Pax7+ cell associated with a type 2 fibre. Single channel views of (a) Pax7 (pink), (b) DAPI (blue), (c) MHCII (red), (d) MHCI and laminin (green)are provided. Scale bar measures 10 µm. SC response to (B) an acute bout of resistance exercise and (C) 16 weeks of training are expressed as satellite cell number per 100 myofibres and are specific to fiber type. Changes in SC number correspond to increases in whole muscle Pax7 mRNA in both (C) the acute time course and (D) the training response of Pax7 mRNA. * denotes significant differences from pre- time point (p≤0.05).
Figure 3 The SC response to an acute bout of resistance exercise and to 16 wks of resistance training. (A), representative image (merge) of a Pax7/Laminin/MHCI/MCHII immunofluorescent stain. Arrow denotes a Pax7+ cell associated with a type 2 fibre. Single channel views of (a) Pax7 (pink), (b) DAPI (blue), (c) MHCII (red), (d) MHCI and laminin (green)are provided. Scale bar measures 10 µm. SC response to (B) an acute bout of resistance exercise and (C) 16 weeks of training are expressed as satellite cell number per 100 myofibres and are specific to fiber type. Changes in SC number correspond to increases in whole muscle Pax7 mRNA in both (C) the acute time course and (D) the training response of Pax7 mRNA. * denotes significant differences from pre- time point (p≤0.05).CC BY · PubMed Central
Figure 4 Cell cycle kinetics following an acute bout of resistance exercise. SC cell cycle kinetics in response to a bout of resistance exercise was analyzed through flow cytometry analysis of Pax7/PI staining in the acute time-course pre-training. Percentage of SC (Pax7+) in (A) all cell cycle phases (Go/GI, S, G2/M), and (B) S-phase are demonstrated. Representative FACS plots of cell cycle of Pax7+ cells pre (C), 24 h (D) and 72 h (E) following an acute bout of exercise. S phase is highlighted in each representative plot. Pax7+ cells in S phase represent 8.2% (C), 9.2% (D), and 12.3% (E) of total cells pre, 24 h and 72 h respectively. * denotes a significant difference from respective Pre timepoint (p<0.01).
Figure 4 Cell cycle kinetics following an acute bout of resistance exercise. SC cell cycle kinetics in response to a bout of resistance exercise was analyzed through flow cytometry analysis of Pax7/PI staining in the acute time-course pre-training. Percentage of SC (Pax7+) in (A) all cell cycle phases (Go/GI, S, G2/M), and (B) S-phase are demonstrated. Representative FACS plots of cell cycle of Pax7+ cells pre (C), 24 h (D) and 72 h (E) following an acute bout of exercise. S phase is highlighted in each representative plot. Pax7+ cells in S phase represent 8.2% (C), 9.2% (D), and 12.3% (E) of total cells pre, 24 h and 72 h respectively. * denotes a significant difference from respective Pre timepoint (p<0.01).CC BY · PubMed Central
Figure 5 The relationship between the acute SC and teh expansion of the SC pool to skeletal muscle hypertrophy. (A) displays a significant correlation between the increases in quadricep volume as measured by MRI as a result of training and type 1 fibre associated SC pool expansion from 24 to 72 hours after exercise. No such correlation is seen in (B) the type 2 fibre associated SC at that time point. However, a significant correlation (C) was seen between the MRI measured increase in quadricep volume and type 2 fibre associated SC pool expansion as a result of training. No correlation (D) associated with the increase in type 1 fibre associated SC as a result of training was seen with hypertrophy.
Figure 5 The relationship between the acute SC and teh expansion of the SC pool to skeletal muscle hypertrophy. (A) displays a significant correlation between the increases in quadricep volume as measured by MRI as a result of training and type 1 fibre associated SC pool expansion from 24 to 72 hours after exercise. No such correlation is seen in (B) the type 2 fibre associated SC at that time point. However, a significant correlation (C) was seen between the MRI measured increase in quadricep volume and type 2 fibre associated SC pool expansion as a result of training. No correlation (D) associated with the increase in type 1 fibre associated SC as a result of training was seen with hypertrophy.CC BY · PubMed Central
Figure 6 The association of MSTN with SC following an acute bout of resistance exercise and 16 wks of resistance training. (A), representative image (merge) of a MSTN/Pax7/Laminin/MHCI immunofluorescent stain. The arrow denotes a MSTN+/Pax7+ cell associated to a type 2 fibre. Single channel views of (a) Pax7 (red), (b) MSTN (yellow), (c) DAPI (blue), and (d) MHCI and Laminin (green) are provided, scale bar measures 10 µm. Quantification of MSTN colocalization to SCs was done in a fiber type specific manner. The changes in colocalization as a result of (B) an acute bout of resistance exercise and (C) 16 weeks of training is displayed. * and ** denote significant differences from the pre timepoint (p<0.05 and p<0.001 respectively). # and ## denote significant differences from the 24 hour timepoint (p<0.05 and p<0.001 respectively).
Figure 6 The association of MSTN with SC following an acute bout of resistance exercise and 16 wks of resistance training. (A), representative image (merge) of a MSTN/Pax7/Laminin/MHCI immunofluorescent stain. The arrow denotes a MSTN+/Pax7+ cell associated to a type 2 fibre. Single channel views of (a) Pax7 (red), (b) MSTN (yellow), (c) DAPI (blue), and (d) MHCI and Laminin (green) are provided, scale bar measures 10 µm. Quantification of MSTN colocalization to SCs was done in a fiber type specific manner. The changes in colocalization as a result of (B) an acute bout of resistance exercise and (C) 16 weeks of training is displayed. * and ** denote significant differences from the pre timepoint (p<0.05 and p<0.001 respectively). # and ## denote significant differences from the 24 hour timepoint (p<0.05 and p<0.001 respectively).CC BY · PubMed Central

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Metadata

Authors
Bellamy, L. M., Joanisse, S., Grubb, A., Mitchell, C. J., McKay, B. R., Phillips, S. M., Baker, S., & Parise, G.
Affiliations
McMaster University (CA)
Corresponding author
Parise, Gianni
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2014-10-14
Volume
9
Issue
10
Pages
e109739
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0109739
PMC
PMC4196938
OpenAlex
W1984074879
Cited by
149
References
42
Citations by year
2026: 2 · 2025: 7 · 2024: 6 · 2023: 5 · 2022: 14 · 2021: 10 · 2020: 16 · 2019: 19 · 2018: 20 · 2017: 15 · 2016: 16 · 2015: 16 · 2014: 3
FWCI
6.84
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • e-space (Manchester Metropolitan University) (acceptedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • ResearchSpace (University of Auckland) (submittedVersion, cc-by)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
  • Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
  • Health Sciences › Medicine › Physiology (medical) › Exercise and Physiological Responses
Keywords
satellite cells, skeletal muscle hypertrophy, resistance training, myogenic stem cells, muscle fiber cross-sectional area, type I muscle fibers, fast-twitch muscle, quadriceps, lean body mass
MeSH terms
Adolescent, Adult, Cell Cycle, Humans, Hypertrophy, Male, Muscle, Skeletal, Muscle Fibers, Slow-Twitch, Satellite Cells, Skeletal Muscle, Cell Proliferation, PAX7 Transcription Factor, Resistance Training, Myostatin, Young Adult

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