Molecular Networks of Human Muscle Adaptation to Exercise and Age
Open accessAbstract
Physical activity and molecular ageing presumably interact to precipitate musculoskeletal decline in humans with age. Herein, we have delineated molecular networks for these two major components of sarcopenic risk using multiple independent clinical cohorts. We generated genome-wide transcript profiles from individuals (n = 44) who then undertook 20 weeks of supervised resistance-exercise training (RET). Expectedly, our subjects exhibited a marked range of hypertrophic responses (3% to +28%), and when applying Ingenuity Pathway Analysis (IPA) up-stream analysis to ~580 genes that co-varied with gain in lean mass, we identified rapamycin (mTOR) signaling associating with growth (P = 1.4 × 10(-30)). Paradoxically, those displaying most hypertrophy exhibited an inhibited mTOR activation signature, including the striking down-regulation of 70 rRNAs. Differential analysis found networks mimicking developmental processes (activated all-trans-retinoic acid (ATRA, Z-score = 4.5; P = 6 × 10(-13)) and inhibited aryl-hydrocarbon receptor signaling (AhR, Z-score = -2.3; P = 3 × 10(-7))) with RET. Intriguingly, as ATRA and AhR gene-sets were also a feature of endurance exercise training (EET), they appear to represent "generic" physical activity responsive gene-networks. For age, we found that differential gene-expression methods do not produce consistent molecular differences between young versus old individuals. Instead, utilizing two independent cohorts (n = 45 and n = 52), with a continuum of subject ages (18-78 y), the first reproducible set of age-related transcripts in human muscle was identified. This analysis identified ~500 genes highly enriched in post-transcriptional processes (P = 1 × 10(-6)) and with negligible links to the aforementioned generic exercise regulated gene-sets and some overlap with ribosomal genes. The RNA signatures from multiple compounds all targeting serotonin, DNA topoisomerase antagonism, and RXR activation were significantly related to the muscle age-related genes. Finally, a number of specific chromosomal loci, including 1q12 and 13q21, contributed by more than chance to the age-related gene list (P = 0.01-0.005), implying possible epigenetic events. We conclude that human muscle age-related molecular processes appear distinct from the processes regulated by those of physical activity.
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Low responders to each exercise stimulus may be as high as 25% in studies of individuals undertaking resistance and endurance training in isolation.
“The characterisation of individual responses is not a new phenomenon, but the results of studies of individuals undertaking resistance and endurance training in isolation suggest that 'low responders' to each exercise stimulus may be as high as 25% (Timmons et al., 2005;Phillips et al., 2013;Gurd et al., 2016).”
From Concurrent exercise training: do opposites distract? (2017) · cites this paper as Phillips et al., 2013
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Limb proportions show developmental plasticity in response to embryo movement
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Self-citationAdaptations to Endurance and Strength TrainingPreprint
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There Are No Nonresponders to Resistance-Type Exercise Training in Older Men and Women
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Muscular and Systemic Correlates of Resistance Training-Induced Muscle Hypertrophy
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Biochemical Pathways of Sarcopenia and Their Modulation by Physical Exercise: A Narrative Review
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The Acute Satellite Cell Response and Skeletal Muscle Hypertrophy following Resistance Training
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The Importance of Resistance Exercise Training to Combat Neuromuscular Aging
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Exercise and the Regulation of Endocrine Hormones
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Exercise-induced skeletal muscle signaling pathways and human athletic performance
Camera, D. M., Smiles, W. J., & Hawley, J. A. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.02.007 · Cited by 128 · see citing works
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Skeletal muscle transcriptome in healthy aging
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Overexpression of the vitamin D receptor (VDR) induces skeletal muscle hypertrophy
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Self-citationTime trajectories in the transcriptomic response to exercise - a meta-analysis
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The Molecular Basis for Load-Induced Skeletal Muscle Hypertrophy
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Kynurenine signaling through the aryl hydrocarbon receptor: Implications for aging and healthspan
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Satellite Cell Depletion Disrupts Transcriptional Coordination and Muscle Adaptation to Exercise
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Transcriptome response of human skeletal muscle to divergent exercise stimuli
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A coding and non-coding transcriptomic perspective on the genomics of human metabolic disease
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Self-citationExercise and the regulation of skeletal muscle hypertrophy
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Sarcopenia: What Is the Origin of This Aging-Induced Disorder?
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Protein Ingestion Increases Myofibrillar Protein Synthesis after Concurrent Exercise
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Nutritional strategies to support concurrent training
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Mammalian Target of Rapamycin (mTOR) Signaling at the Crossroad of Muscle Fiber Fate in Sarcopenia
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Resistance Exercise, Aging, Disuse, and Muscle Protein Metabolism
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Molecular Transducers of Human Skeletal Muscle Remodeling under Different Loading States
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Longevity‐related molecular pathways are subject to midlife “switch” in humans
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Self-citationAge-Associated Differences in Recovery from Exercise-Induced Muscle Damage
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Identification of a KLF5-dependent program and drug development for skeletal muscle atrophy
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Self-citationChanges in Gene Expression in Responders and Nonresponders to a Low-Intensity Walking Intervention
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Self-citationMuscle Proteomic and Transcriptomic Profiling of Healthy Aging and Metabolic Syndrome in Men
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The link between Mitochondria and Sarcopenia
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Aerobic exercise augments muscle transcriptome profile of resistance exercise
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Self-citationThe 24-hour molecular landscape after exercise in humans reveals MYC is sufficient for muscle growth
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Exercise and Regulation of Protein Metabolism
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Self-citationChronic aryl hydrocarbon receptor activity phenocopies smoking‐induced skeletal muscle impairment
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Parathyroid hormone-related peptide.
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Transcriptomics for Clinical and Experimental Biology Research: Hang on a Seq
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Resistance Exercise, Aging, Disuse, and Muscle Protein Metabolism
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Higher resistance training volume offsets muscle hypertrophy nonresponsiveness in older individuals
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From molecular to physical function: The aging trajectory
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- Authors
- Phillips, B. E., Williams, J. P., Gustafsson, T., Bouchard, C., Rankinen, T., Knudsen, S., Smith, K., Timmons, J. A., & Atherton, P. J.
- Affiliations
- Royal Derby Hospital (GB)
- Karolinska Institutet (SE)
- Pennington Biomedical Research Center (US)
- Medical Prognosis Institute (Denmark) (DK)
- Loughborough University (GB)
- Corresponding author
- Timmons, James A.
- ORCID
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-03-21
- Volume
- 9
- Issue
- 3
- Pages
- e1003389
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC3605101
- OpenAlex
- W2094388228
- Cited by
- 199
- References
- 90
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 14 · 2023: 13 · 2022: 18 · 2021: 22 · 2020: 13 · 2019: 17 · 2018: 17 · 2017: 9 · 2016: 16 · 2015: 23 · 2014: 18 · 2013: 6
- FWCI
- 9.41
- Type
- journal article
- Language
- en
- Update notices
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Repository@Nottingham (University of Nottingham) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Nottingham ePrints (University of Nottingham) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Funders
- University of Stirling
- National Institutes of Health (HL- 47317, HL- 47327, HL- 47323)
- Directorate for Biological Sciences
- Medical Research Council (MR/K00414X/1)
- Biotechnology and Biological Sciences Research Council (BB/X5106971, BB/C516779/1)
- National Heart, Lung, and Blood Institute (R01HL047327, HL 47321, HL 45670, HL47323, R01HL047317, HL 47327, R01HL047323, HL47317, R01HL045670, R01HL047321)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Physical Performance
- Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
- Keywords
- muscle aging, resistance training, endurance training, sarcopenia, mTOR signaling, rapamycin, muscle hypertrophy, lean body mass, all-trans retinoic acid, aryl hydrocarbon receptor signaling, age-related gene expression, post-transcriptional regulation, ribosomal genes, gene regulatory networks
- MeSH terms
- Adaptation, Physiological, Adolescent, Adult, Aged, Aging, Female, Humans, Male, Middle Aged, Signal Transduction, Exercise, Down-Regulation, Muscle, Skeletal, Gene Expression Profiling, Gene Regulatory Networks, Ribosome Subunits, TOR Serine-Threonine Kinases
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