Cited by 159Muscle Physiology and DisordersMuscle metabolism and nutritionHormonal and reproductive studies

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A cellular memory mechanism aids overload hypertrophy in muscle long after an episodic exposure to anabolic steroids

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Egner, Ingrid M., Bruusgaard, Jo C., Eftestøl, Einar, Gundersen, Kristian·2013·The Journal of Physiology

DOI 10.1113/jphysiol.2013.264457PMC PMC3892473

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Abstract

Key points Training studio folklore suggests that previous strength training, with or without the use of anabolic steroids facilitates re‐acquisition of muscle mass even after long intervening periods of inactivity. This ‘muscle memory’ has previously been attributed to motor learning, but our data suggest the existence of a cellular memory residing in the muscle fibres themselves. Muscle fibres have multiple nuclei, and the number of nuclei increases when muscle mass increases. When mice were briefly treated with steroids the muscle mass and number of nuclei increased. The drug was subsequently withdrawn for 3 months and the muscle mass returned to normal, but the excess cell nuclei persisted. When such muscles were subjected to overload they grew by 30% over 6 days while controls grew insignificantly. Our data suggest that previous strength training might be beneficial later in life, and that a brief exposure to anabolic steroids might have long lasting performance‐enhancing effects. Abstract Previous strength training with or without the use of anabolic steroids facilitates subsequent re‐acquisition of muscle mass even after long intervening periods of inactivity. Based on in vivo and ex vivo microscopy we here propose a cellular memory mechanism residing in the muscle cells. Female mice were treated with testosterone propionate for 14 days, inducing a 66% increase in the number of myonuclei and a 77% increase in fibre cross‐sectional area. Three weeks after removing the drug, fibre size was decreased to the same level as in sham treated animals, but the number of nuclei remained elevated for at least 3 months (>10% of the mouse lifespan). At this time, when the myonuclei‐rich muscles were exposed to overload‐exercise for 6 days, the fibre cross‐sectional area increased by 31% while control muscles did not grow significantly. We suggest that the lasting, elevated number of myonuclei constitutes a cellular memory facilitating subsequent muscle overload hypertrophy. Our findings might have consequences for the exclusion time of doping offenders. Since the ability to generate new myonuclei is impaired in the elderly our data also invites speculation that it might be beneficial to perform strength training when young in order to benefit in senescence.

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The effects of supraphysiologic doses of testosterone on muscle size and strength in normal men
Bhasin, S., Storer, T. W., Berman, N., Callegari, C., Clevenger, B., Phillips, J., Bunnell, T. J., Tricker, R., Shirazi, A., & Casaburi, R. (1996) · New England Journal of Medicine · doi:10.1056/nejm199607043350101 · Cited by 1,659
Mechanisms regulating skeletal muscle growth and atrophy
Schiaffino, S., Dyar, K. A., Ciciliot, S., Blaauw, B., & Sandri, M. (2013) · The FEBS Journal · doi:10.1111/febs.12253 · Cited by 1,492
Notch-Mediated Restoration of Regenerative Potential to Aged Muscle
Conboy, I. M., Conboy, M. J., Smythe, G. M., & Rando, T. A. (2003) · Science · doi:10.1126/science.1087573 · Cited by 1,121
Effective fiber hypertrophy in satellite cell-depleted skeletal muscle
McCarthy, J. J., Mula, J., Miyazaki, M., Erfani, R., Garrison, K., Farooqui, A. B., Srikuea, R., Lawson, B. A., Grimes, B., Keller, C., et al. (2011) · Development · doi:10.1242/dev.068858 · Cited by 616
Satellite cells, the engines of muscle repair
Wang, Y. X., & Rudnicki, M. A. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3265 · Cited by 493
The role of learning and coordination in strength training
Rutherford, O. M., & Jones, D. A. (1986) · European Journal of Applied Physiology · doi:10.1007/bf00422902 · Cited by 484
Lack of myostatin results in excessive muscle growth but impaired force generation
Amthor, H., Macharia, R., Navarrete, R., Schuelke, M., Brown, S., Otto, A., Voït, T., Muntoni, F., Vrbovà, G., Partridge, T. A., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604893104 · Cited by 438
Strength and skeletal muscle adaptations in heavy-resistance-trained women after detraining and retraining
Staron, R. S., Leonardi, M. J., Karapondo, D. L., Malicky, E. S., Falkel, J. E., Hagerman, F. C., & Hikida, R. S. (1991) · Journal of Applied Physiology · doi:10.1152/jappl.1991.70.2.631 · Cited by 400
Skeletal muscle satellite cells: Changes in proliferation potential as a function of age
Schultz, E., & Lipton, B. H. (1982) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(82)90105-1 · Cited by 335
Myonuclei acquired by overload exercise precede hypertrophy and are not lost on detraining
Bruusgaard, J. C., Johansen, I. B., Egner, I. M., Rana, Z. A., & Gundersen, K. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0913935107 · Cited by 327
Self-citation

Show all 61 references

Research works printed but not linked: 2

10.1152/ajpcell.00207.2012 · DOI
Puckelwartz M, 2011, Emery‐Drefuss muscular dystrophy, Handb Clin Neurol, 101, 156

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Authors: Egner, I. M., Bruusgaard, J. C., Eftestøl, E., & Gundersen, K.
Affiliations: University of Oslo (NO)
ORCID: Egner, Ingrid M.
Bruusgaard, Jo C.
Eftestøl, Einar
Gundersen, Kristian
Venue: The Journal of Physiology
Publisher: Wiley
Published: 2013-11-22
Volume: 591
Issue: 24
Pages: 6221-6230
ISSN: 0022-3751 (ISSN-L)
1469-7793
DOI: 10.1113/jphysiol.2013.264457
PMC: PMC3892473
OpenAlex: W2107574257
Cited by: 159
References: 61
Citations by year: 2026: 10 · 2025: 13 · 2024: 10 · 2023: 13 · 2022: 13 · 2021: 28 · 2020: 12 · 2019: 15 · 2018: 13 · 2017: 5 · 2016: 9 · 2015: 9 · 2014: 7 · 2013: 1
FWCI: 3.88
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The Journal of Physiology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Norges Forskningsråd
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 › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
Keywords: muscle memory, myonuclei, anabolic steroids, testosterone propionate, muscle hypertrophy, muscle fiber cross-sectional area, resistance training, doping, aging, motor learning
MeSH terms: Animals, Cell Nucleus, Physical Exertion, Female, Hypertrophy, Testosterone, Muscle Fibers, Skeletal, Mice

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A cellular memory mechanism aids overload hypertrophy in muscle long after an episodic exposure to anabolic steroids

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