Myonuclei acquired by overload exercise precede hypertrophy and are not lost on detraining
Open accessAbstract
Effects of previous strength training can be long-lived, even after prolonged subsequent inactivity, and retraining is facilitated by a previous training episode. Traditionally, such "muscle memory" has been attributed to neural factors in the absence of any identified local memory mechanism in the muscle tissue. We have used in vivo imaging techniques to study live myonuclei belonging to distinct muscle fibers and observe that new myonuclei are added before any major increase in size during overload. The old and newly acquired nuclei are retained during severe atrophy caused by subsequent denervation lasting for a considerable period of the animal's lifespan. The myonuclei seem to be protected from the high apoptotic activity found in inactive muscle tissue. A hypertrophy episode leading to a lasting elevated number of myonuclei retarded disuse atrophy, and the nuclei could serve as a cell biological substrate for such memory. Because the ability to create myonuclei is impaired in the elderly, individuals may benefit from strength training at an early age, and because anabolic steroids facilitate more myonuclei, nuclear permanency may also have implications for exclusion periods after a doping offense.
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The pre-existing, expanded nucleolar templates are immediately available to rapidly transcribe massive amounts of 45S pre-rRNA.
“The pre-existing, expanded nucleolar templates are immediately available to rapidly transcribe massive amounts of 45S pre-rRNA”
From Ribosome Biogenesis as a Putative Bottleneck to Skeletal Muscle Hypertrophy: Mechanisms, Human Evidence, and Practical Modulators (2026) · cites this paper as [115]
When an individual resumes training, the muscle fiber bypasses the initial, slow, and energetically demanding process of satellite cell proliferation.
“Consequently, when an individual resumes training, the muscle fiber bypasses the initial, slow, and energetically demanding process of satellite cell proliferation [115].”
From Ribosome Biogenesis as a Putative Bottleneck to Skeletal Muscle Hypertrophy: Mechanisms, Human Evidence, and Practical Modulators (2026) · cites this paper as [115]
The availability of pre-existing expanded nucleolar templates explains the accelerated rate of "re-growth" universally observed in previously trained humans.
“explaining the accelerated rate of “re-growth” universally observed in previously trained humans [115,117]”
From Ribosome Biogenesis as a Putative Bottleneck to Skeletal Muscle Hypertrophy: Mechanisms, Human Evidence, and Practical Modulators (2026) · cites this paper as [115]
Prolonged unloading leads to a slow decay in total RNA, whereas newly acquired myonuclei (donated via satellite cell fusion) are not eliminated via apoptosis.
“Studies by Bruusgaard et al. [115] and Kadi et al. [116] utilizing advanced single-fiber techniques demonstrated that prolonged unloading leads to a slow decay in total RNA, whereas newly acquired myonuclei (donated via satellite cell fusion) are not eliminated via apoptosis.”
From Ribosome Biogenesis as a Putative Bottleneck to Skeletal Muscle Hypertrophy: Mechanisms, Human Evidence, and Practical Modulators (2026) · cites this paper as [115]
In addition to hormone concentrations, the number of myonuclei can affect skeletal muscle training.
“Research shows that in addition to hormone concentrations, the number of myonuclei can affect skeletal muscle training [79, 80].”
From Integrating Transwomen and Female Athletes with Differences of Sex Development (DSD) into Elite Competition: The FIMS 2021 Consensus Statement (2021) · cites this paper as [80]
Detraining does not diminish the myonuclei number.
“However, detraining does not diminish the myonuclei number,27”
It is possible that strength advantages gained when training in a high-testosterone environment may not be fully reversed by testosterone suppression.
“Hence, it is possible that strength advantages gained when training in a high-testosterone environment may not be fully reversed by testosterone suppression.”
Cites
Morphologic and biochemical hallmarks of apoptosis
Saraste, A. (2000) · Cardiovascular Research · doi:10.1016/s0008-6363(99)00384-3 · Cited by 1,454 · see citing works
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 · see citing works
Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma
Gregory, T. R. (2001) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1017/s1464793100005595 · Cited by 699 · see citing works
Cavalier‐Smith, T. (1978) · Journal of Cell Science · doi:10.1242/jcs.34.1.247 · Cited by 683 · see citing works
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 479 · see citing works
Sinha-Hikim, I., Artaza, J., Woodhouse, L., Gonzalez-Cadavid, N., Singh, A. B., Lee, M. I., Storer, T. W., Casaburi, R., Shen, R., & Bhasin, S. (2002) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00502.2001 · Cited by 464 · see citing works
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 · see citing works
Concentration of acetylcholine receptor mRNA in synaptic regions of adult muscle fibres
Merlie, J. P., & Sanes, J. R. (1985) · Nature · doi:10.1038/317066a0 · Cited by 350 · see citing works
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 · see citing works
Effects of strength training and immobilization on human muscle fibres
MacDOUGALL, J. D., Elder, G. C. B., SALE, D. G., Moroz, J. R., & Sutton, J. R. (1980) · European Journal of Applied Physiology · doi:10.1007/bf00421352 · Cited by 299 · see citing works
Aging, Stem Cells and Tissue Regeneration: Lessons from Muscle
Conboy, I. M., & Rando, T. A. (2005) · Cell Cycle · doi:10.4161/cc.4.3.1518 · Cited by 298 · see citing works
Nature of dividing nuclei in skeletal muscle of growing rats
Moss, F. P., & Leblond, C. P. (1970) · The Journal of Cell Biology · doi:10.1083/jcb.44.2.459 · Cited by 289 · see citing works
Visualization of neuromuscular junctions over periods of several months in living mice
Lichtman, J., Magrassi, L., & Purves, D. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-04-01215.1987 · Cited by 273 · see citing works
Number and spatial distribution of nuclei in the muscle fibres of normal mice studied in vivo
Bruusgaard, J. C., Liestøl, K., Ekmark, M., Kollstad, K., & Gundersen, K. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.045328 · Cited by 254 · see citing works
Self-citationRosenblatt, J. D., & Parry, D. J. (1992) · Journal of Applied Physiology · doi:10.1152/jappl.1992.73.6.2538 · Cited by 251 · see citing works
Nuclear domains in muscle cells
Hall, Z. W., & Ralston, E. (1989) · Cell · doi:10.1016/0092-8674(89)90597-7 · Cited by 249 · see citing works
The Time Course for Elevated Muscle Protein Synthesis Following Heavy Resistance Exercise
MacDougall, J. D., Gibala, M. J., Tarnopolsky, M. A., MacDonald, J. R., Interisano, S. A., & Yarasheski, K. E. (1995) · Canadian Journal of Applied Physiology · doi:10.1139/h95-038 · Cited by 248 · see citing works
Effects of Strength Training and Detraining on Muscle Quality: Age and Gender Comparisons
Ivey, F. M., Tracy, B. L., Lemmer, J. T., NessAiver, M., Metter, E. J., Fozard, J. L., & Hurley, B. F. (2000) · The Journals of Gerontology Series A · doi:10.1093/gerona/55.3.b152 · Cited by 247 · see citing works
The Significance of Sarcopenia in Old Age
Dutta, C., & Hadley, E. C. (1995) · The Journals of Gerontology Series A · doi:10.1093/gerona/50a.special_issue.1 · Cited by 228 · see citing works
Developmental Fate of Skeletal Muscle Satellite Cells
Lipton, B. H., & Schultz, E. (1979) · Science · doi:10.1126/science.472747 · Cited by 201 · see citing works
Effects of anabolic steroids on the muscle cells of strength-trained athletes
KADI, F., ERIKSSON, A., HOLMNER, S., & THORNELL, L.-E. (1999) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-199911000-00006 · Cited by 190 · see citing works
Muscle growth in response to mechanical stimuli
Goldspink, D. F., Cox, V. M., Smith, S., Eaves, L. A., Osbaldeston, N. J., Lee, D. M., & Mantle, D. (1995) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1995.268.2.e288 · Cited by 189 · see citing works
Sanes, J. R., Johnson, Y. R., Kotzbauer, P. T., Mudd, J. L., Hanley, T. A., Marttnou, J.-C., & Merlie, J. P. (1991) · Development · doi:10.1242/dev.113.4.1181 · Cited by 187 · see citing works
Houston, M. E., Froese, E. A., Valeriote, S. P., Green, H. J., & Ranney, D. (1983) · European Journal of Applied Physiology · doi:10.1007/bf00952534 · Cited by 185 · see citing works
Laurent, G. J., Sparrow, M. P., & Millward, D. J. (1978) · Biochemical Journal · doi:10.1042/bj1760407 · Cited by 166 · see citing works
Alway, S. E., Degens, H., Krishnamurthy, G., & Smith, C. A. S. (2002) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00598.2001 · Cited by 164 · see citing works
In vivo time-lapse microscopy reveals no loss of murine myonuclei during weeks of muscle atrophy
Bruusgaard, J. C., & Gundersen, K. (2008) · Journal of Clinical Investigation · doi:10.1172/jci34022 · Cited by 162 · see citing works
Self-citationChen, Y., Nader, G. A., Baar, K. R., Fedele, M. J., Hoffman, E. P., & Esser, K. A. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.021220 · Cited by 158 · see citing works
Goldspink, D. F., Garlick, P. J., & McNurlan, M. A. (1983) · Biochemical Journal · doi:10.1042/bj2100089 · Cited by 146 · see citing works
Nuclear apoptosis contributes to sarcopenia
Alway, S. E., & Siu, P. M. (2008) · Exercise and Sport Sciences Reviews · doi:10.1097/jes.0b013e318168e9dc · Cited by 144 · see citing works
Distribution of myonuclei and microtubules in live muscle fibers of young, middle-aged, and old mice
Bruusgaard, J. C., Liestøl, K., & Gundersen, K. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00913.2005 · Cited by 144 · see citing works
Self-citationAging influences cellular and molecular responses of apoptosis to skeletal muscle unloading
Siu, P. M., Pistilli, E. E., Butler, D. C., & Alway, S. E. (2004) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00239.2004 · Cited by 143 · see citing works
Nuclear domains during muscle atrophy: nuclei lost or paradigm lost?
Gundersen, K., & Bruusgaard, J. C. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.154369 · Cited by 140 · see citing works
Self-citationSnow, M. H. (1990) · The Anatomical Record · doi:10.1002/ar.1092270407 · Cited by 137 · see citing works
The fate of newly formed satellite cells during compensatory muscle hypertrophy
Schiaffino, S., Pierobon Bormioli, S., & Aloisi, M. (1976) · Virchows Archiv B Cell Pathology · doi:10.1007/bf02899148 · Cited by 132 · see citing works
Point:Counterpoint: Satellite cell addition is/is not obligatory for skeletal muscle hypertrophy
O’Connor, R. S., & Pavlath, G. K. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00101.2007 · Cited by 121 · see citing works
Dynamic muscle strength alterations to detraining and retraining in elderly men
Taaffe, D. R., & Marcus, R. (1997) · Clinical Physiology · doi:10.1111/j.1365-2281.1997.tb00010.x · Cited by 110 · see citing works
Cell proliferation in rat skeletal muscle during early stages of compensatory hypertrophy
Schiaffino, S., Bormioli, S. P., & Aloisi, M. (1972) · Virchows Archiv B Cell Pathology Including Molecular Pathology · doi:10.1007/bf02889406 · Cited by 108 · see citing works
Smith, R. H., Palmer, R. M., & Reeds, P. J. (1983) · Biochemical Journal · doi:10.1042/bj2140153 · Cited by 101 · see citing works
Counterpoint: Satellite cell addition is not obligatory for skeletal muscle hypertrophy
McCarthy, J. J., & Esser, K. A. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00101.2007a · Cited by 97 · see citing works
Restricted distribution of mRNA produced from a single nucleus in hybrid myotubes.
Ralston, E., & Hall, Z. W. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.119.5.1063 · Cited by 83 · see citing works
Gundersen, K., Sanes, J. R., & Merlie, J. P. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.123.6.1535 · Cited by 82 · see citing works
Self-citationWinchester, P., Davis, M. E., Alway, S. E., & Gonyea, W. J. (1991) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1991.260.2.c206 · Cited by 82 · see citing works
Cavalier‐Smith, T. (1980) · Nature · doi:10.1038/285617a0 · Cited by 79 · see citing works
Siu, P. M. (2009) · Frontiers in bioscience · doi:10.2741/3253 · Cited by 71 · see citing works
Seiden, D. L. (1976) · American Journal of Anatomy · doi:10.1002/aja.1001450405 · Cited by 58 · see citing works
No decrease in myonuclear number after long-term denervation in mature mice
Wada, K., Takahashi, H., Katsuta, S., & Soya, H. (2002) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00025.2002 · Cited by 57 · see citing works
O’Connor, R. S., Pavlath, G. K., McCarthy, J. J., & Esser, K. A. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00502.2007 · Cited by 53 · see citing works
Detraining in the Older Adult: Effects of Prior Training Intensity on Strength Retention
Harris, C., DeBeliso, M., Adams, K. J., Irmischer, B. S., & Gibson, T. A. S. (2007) · The Journal of Strength and Conditioning Research · doi:10.1519/r-15654.1 · Cited by 50 · see citing works
Control of muscle fibre size: a crucial factor in ageing.
Hughes, S. M., & Schiaffino, S. (1999) · PubMed · doi:10.1046/j.1365-201x.1999.00622.x · Cited by 50 · see citing works
Smith, K. M., Winegard, K. J., Hicks, A. L., & McCartney, N. (2003) · Canadian Journal of Applied Physiology · doi:10.1139/h03-034 · Cited by 50 · see citing works
Control of muscle fibre size: a crucial factor in ageing
Hughes, S. M., & Schiaffino, S. (1999) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.1999.00619.x · Cited by 50 · see citing works
DNA Injection into Single Cells of Intact Mice
Utvik, J. K., Njå, A., & Gundersen, K. (1999) · Human Gene Therapy · doi:10.1089/10430349950019075 · Cited by 49 · see citing works
Self-citationHypertrophy and proliferation of skeletal muscle fibers from aged quail
Carson, J. A., Yamaguchi, M., & Alway, S. E. (1995) · Journal of Applied Physiology · doi:10.1152/jappl.1995.78.1.293 · Cited by 42 · see citing works
Satellite cell addition is/is not obligatory for skeletal muscle hypertrophy
Rehfeldt, C. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00466.2007 · Cited by 29 · see citing works
Natural Occurrence of Myofiber Cytoplasmic Enlargement Accompanied by Decrease in Myonuclear Number
Wada, K., Katsuta, S., & Soya, H. (2003) · The Japanese Journal of Physiology · doi:10.2170/jjphysiol.53.145 · Cited by 29 · see citing works
Flagged first, then by citations
1 of the 57 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Sarcopenia: Aging-Related Loss of Muscle Mass and Function
Larsson, L., Degens, H., Li, M., Salviati, L., Lee, Y. I., Thompson, W., Kirkland, J. L., & Sandri, M. (2019) · Physiological Reviews · doi:10.1152/physrev.00061.2017 · Cited by 1,797 · see citing works
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 · see citing works
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 · see citing works
Satellite cells in human skeletal muscle; from birth to old age
Verdijk, L. B., Snijders, T., Drost, M., Delhaas, T., Kadi, F., & van Loon, L. J. C. (2014) · AGE · doi:10.1007/s11357-013-9583-2 · Cited by 399 · see citing works
On Having No Head: Cognition throughout Biological Systems
Baluška, F., & Levin, M. G. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.00902 · Cited by 383 · see citing works
Fry, C. S., Kirby, T. J., Kosmac, K., McCarthy, J. J., & Peterson, C. A. (2017) · Cell stem cell · doi:10.1016/j.stem.2016.09.010 · Cited by 372 · see citing works
Human skeletal muscle possesses an epigenetic memory of hypertrophy
Seaborne, R. A., Strauss, J., Cocks, M., Shepherd, S., O’Brien, T. D., van Someren, K. A., Bell, P. G., Murgatroyd, C., Morton, J. P., Stewart, C. E., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-20287-3 · Cited by 334 · see citing works
Mitochondrial pathways in sarcopenia of aging and disuse muscle atrophy
Calvani, R., Joseph, A.-M., Adhihetty, P. J., Miccheli, A., Bossola, M., Leeuwenburgh, C., Bernabei, R., & Marzetti, E. (2013) · bchm · doi:10.1515/hsz-2012-0247 · Cited by 328 · see citing works
Exercise‐induced muscle damage: What is it, what causes it and what are the nutritional solutions?
Owens, D. J., Twist, C., Cobley, J. N., Howatson, G., & Close, G. L. (2018) · European Journal of Sport Science · doi:10.1080/17461391.2018.1505957 · Cited by 309 · see citing works
Muscle fiber type diversification during exercise and regeneration
Qaisar, R., Bhaskaran, S., & Van Remmen, H. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.03.025 · Cited by 283 · see citing works
Regulation of the muscle fiber micro environment by activated satellite cells during hypertrophy
Fry, C. S., Lee, J. D., Jackson, J. R., Kirby, T. J., Stasko, S. A., Liu, H., Dupont‐Versteegden, E. E., McCarthy, J. J., & Peterson, C. A. (2014) · The FASEB Journal · doi:10.1096/fj.13-239426 · Cited by 273 · see citing works
Nielsen, J. L., Aagaard, P., Bech, R. D., Nygaard, T., Hvid, L. G., Wernbom, M., Suetta, C., & Frandsen, U. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.237008 · Cited by 268 · see citing works
Mechanisms Modulating Skeletal Muscle Phenotype
Blaauw, B., Schiaffino, S., & Reggiani, C. (2013) · Comprehensive physiology · doi:10.1002/cphy.c130009 · Cited by 278 · see citing works
Excitation‐transcription coupling in skeletal muscle: the molecular pathways of exercise
Gundersen, K. (2010) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2010.00161.x · Cited by 254 · see citing works
Self-citationHUNTER, S. K., S. ANGADI, S., BHARGAVA, A., HARPER, J., HIRSCHBERG, A. L., D. LEVINE, B., L. MOREAU, K., J. NOKOFF, N., STACHENFELD, N. S., & BERMON, S. (2023) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000003300 · Cited by 241 · see citing works
The effects of obesity on skeletal muscle regeneration
Akhmedov, D., & Berdeaux, R. (2013) · Frontiers in Physiology · doi:10.3389/fphys.2013.00371 · Cited by 241 · see citing works
Satellite cell depletion prevents fiber hypertrophy in skeletal muscle
Egner, I. M., Bruusgaard, J. C., & Gundersen, K. (2016) · Development · doi:10.1242/dev.134411 · Cited by 203 · see citing works
Self-citationBrooks, N. E., & Myburgh, K. H. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00099 · Cited by 194 · see citing works
Bone and skeletal muscle: neighbors with close ties
DiGirolamo, D. J., Kiel, D. P., & Esser, K. A. (2013) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.1969 · Cited by 193 · see citing works
Arentson‐Lantz, E. J., English, K. L., Paddon‐Jones, D., & Fry, C. S. (2016) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00799.2015 · Cited by 183 · see citing works
Sharples, A. P., Stewart, C. E., & Seaborne, R. A. (2016) · Aging Cell · doi:10.1111/acel.12486 · Cited by 180 · see citing works
Role of satellite cells in muscle growth and maintenance of muscle mass
Pallafacchina, G., Blaauw, B., & Schiaffino, S. (2012) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2012.02.002 · Cited by 173 · see citing works
Hilton, E. N., & Lundberg, T. R. (2021) · Sports Medicine · doi:10.1007/s40279-020-01389-3 · Cited by 170 · see citing works
Muscle memory and a new cellular model for muscle atrophy and hypertrophy
Gundersen, K. (2016) · Journal of Experimental Biology · doi:10.1242/jeb.124495 · Cited by 169 · see citing works
Self-citationMolecular Mechanisms of Skeletal Muscle Hypertrophy
Schiaffino, S., Reggiani, C., Akimoto, T., & Blaauw, B. (2020) · Journal of Neuromuscular Diseases · doi:10.3233/jnd-200568 · Cited by 169 · see citing works
Harper, J., O'Donnell, E., Sorouri Khorashad, B., McDermott, H., & Witcomb, G. L. (2021) · British Journal of Sports Medicine · doi:10.1136/bjsports-2020-103106 · Cited by 167 · see citing works
Farup, J., Madaro, L., Puri, P., & Mikkelsen, U. R. (2015) · Cell Death and Disease · doi:10.1038/cddis.2015.198 · Cited by 156 · see citing works
Egner, I. M., Bruusgaard, J. C., Eftestøl, E., & Gundersen, K. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2013.264457 · Cited by 159 · see citing works
Self-citationRequirement of myomaker-mediated stem cell fusion for skeletal muscle hypertrophy
Goh, Q., & Millay, D. P. (2017) · eLife · doi:10.7554/elife.20007 · Cited by 157 · see citing works
Owens, D. J., Sharples, A. P., Polydorou, I., Alwan, N., Donovan, T. F., TANG, J. C. Y., Fraser, W. D., Cooper, R. G., Morton, J. P., Stewart, C. E., et al. (2015) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00375.2015 · Cited by 156 · see citing works
Guerci, A., Lahoute, C., Hébrard, S., Collard, L., Graindorge, D., Favier, M., Cagnard, N., Batonnet‐Pichon, S., Précigout, G., Garcı́a, L., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2011.12.001 · Cited by 138 · see citing works
Longtine, M. S., Chen, B., Odibo, A. O., Zhong, Y., & Nelson, D. M. (2012) · Placenta · doi:10.1016/j.placenta.2012.01.017 · Cited by 134 · see citing works
Turner, D. C., Seaborne, R. A. E., & Sharples, A. P. (2019) · Scientific Reports · doi:10.1038/s41598-019-40787-0 · Cited by 132 · see citing works
The global migration of everyday life: Investigating the practice memories of Australian migrants
Maller, C. J., & Strengers, Y. (2012) · Geoforum · doi:10.1016/j.geoforum.2012.09.002 · Cited by 129 · see citing works
Satellite Cells Contribution to Exercise Mediated Muscle Hypertrophy and Repair.
Bazgir, B., Fathi, R., Valojerdi, M. R., Mozdziak, P. E., & Asgari, A. (2017) · PubMed Central · doi:10.22074/cellj.2016.4714 · Cited by 124 · see citing works
Myostatin inhibition induces muscle fibre hypertrophy prior to satellite cell activation
Wang, Q., & McPherron, A. C. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2011.226001 · Cited by 122 · see citing works
Deterioration of nuclear morphology and architecture: A hallmark of senescence and aging
Pathak, R. U., Soujanya, M., & Mishra, R. K. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101264 · Cited by 119 · see citing works
Satellite cells in ageing: use it or lose it
Chen, W., Datzkiw, D., & Rudnicki, M. A. (2020) · Open Biology · doi:10.1098/rsob.200048 · Cited by 116 · see citing works
Characterization and Regulation of Mechanical Loading‐Induced Compensatory Muscle Hypertrophy
Adams, G. R., & Bamman, M. M. (2012) · Comprehensive physiology · doi:10.1002/cphy.c110066 · Cited by 114 · see citing works
Myonuclear accretion is a determinant of exercise-induced remodeling in skeletal muscle
Goh, Q., Song, T., Petrany, M. J., Cramer, A., Sun, C., Sadayappan, S., Lee, S., & Millay, D. P. (2019) · eLife · doi:10.7554/elife.44876 · Cited by 110 · see citing works
No change in myonuclear number during muscle unloading and reloading
Bruusgaard, J. C., Egner, I. M., Larsen, T. K., Dupre-Aucouturier, S., Desplanches, D., & Gundersen, K. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00436.2012 · Cited by 107 · see citing works
Self-citationDungan, C. M., Murach, K. A., Frick, K. K., Jones, S. R., Crow, S. E., Englund, D. A., Vechetti, I. J., Figueiredo, V. C., Levitan, B. M., Satin, J., et al. (2019) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00050.2019 · Cited by 103 · see citing works
Classification and Determination Model of Resistance Training Status
Santos Junior, E. R. T., de Salles, B. F., Dias, I., Ribeiro, A. S., Simão, R., & Willardson, J. M. (2021) · Strength & Conditioning Journal · doi:10.1519/ssc.0000000000000627 · Cited by 100 · see citing works
Blocquiaux, S., Gorski, T., Roie, E. V., Ramaekers, M., Thienen, R. V., Nielens, H., Delecluse, C., Bock, K. D., & Thomis, M. A. (2020) · Experimental Gerontology · doi:10.1016/j.exger.2020.110860 · Cited by 100 · see citing works
Handelsman, D. (2021) · Endocrine reviews · doi:10.1210/endrev/bnab001 · Cited by 67 · see citing works
Ogasawara, R., Loenneke, J. P., Thiebaud, R. S., & Abe, T. (2013) · International Journal of Clinical Medicine · doi:10.4236/ijcm.2013.42022 · Cited by 139 · see citing works
Is There a Minimum Intensity Threshold for Resistance Training-Induced Hypertrophic Adaptations?
Schoenfeld, B. J. (2013) · Sports Medicine · doi:10.1007/s40279-013-0088-z · Cited by 97 · see citing works
Murach, K. A., Englund, D. A., Dupont‐Versteegden, E. E., McCarthy, J. J., & Peterson, C. A. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00635 · Cited by 96 · see citing works
The concept of skeletal muscle memory: Evidence from animal and human studies
Snijders, T., Aussieker, T., Holwerda, A. M., Parise, G., van Loon, L. J. C., & Verdijk, L. B. (2020) · Acta Physiologica · doi:10.1111/apha.13465 · Cited by 96 · see citing works
Psilander, N., Eftestøl, E., Cumming, K. T., Juvkam, I., Ekblom, M. M., Sunding, K., Wernbom, M., Holmberg, H.-C., Ekblom, B., Bruusgaard, J. C., et al. (2019) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00917.2018 · Cited by 95 · see citing works
Self-citationFusion-independent satellite cell communication to muscle fibers during load-induced hypertrophy
Murach, K. A., Vechetti, I. J., Van Pelt, D. W., Crow, S. E., Dungan, C. M., Figueiredo, V. C., Kosmac, K., Fu, X., Richards, C. I., Fry, C. S., et al. (2020) · Function · doi:10.1093/function/zqaa009 · Cited by 94 · see citing works
Murach, K. A., Mobley, C. B., Zdunek, C. J., Frick, K. K., Jones, S. R., McCarthy, J. J., Peterson, C. A., & Dungan, C. M. (2020) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12617 · Cited by 93 · see citing works
Modulating exercise-induced hormesis: Does less equal more?
Peake, J. M., Markworth, J. F., Nosaka, K., Raastad, T., Wadley, G. D., & Coffey, V. G. (2015) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01055.2014 · Cited by 96 · see citing works
Eccentric Exercise Facilitates Mesenchymal Stem Cell Appearance in Skeletal Muscle
Valero, M. C., Huntsman, H. D., Liu, J., Zou, K., & Boppart, M. D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029760 · Cited by 90 · see citing works
Aguilar‐Agon, K. W., Capel, A. J., Martin, N. R. W., Player, D. J., & Lewis, M. P. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.28923 · Cited by 84 · see citing works
Skeletal muscle adaptations to physical inactivity and subsequent retraining in young men
Campbell, E. L., Seynnes, O., Bottinelli, R., McPhee, J. S., Atherton, P. J., Jones, D. A., Butler-Browne, G. S., & Narici, M. V. (2013) · Biogerontology · doi:10.1007/s10522-013-9427-6 · Cited by 84 · see citing works
Mixing it up: the biological significance of hybrid skeletal muscle fibers
Medler, S. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.200832 · Cited by 80 · see citing works
Myonuclear content regulates cell size with similar scaling properties in mice and humans
Hansson, K., Eftestøl, E., Bruusgaard, J. C., Juvkam, I. S., Cramer, A., Malthe‐Sørenssen, A., Millay, D. P., & Gundersen, K. (2020) · Nature Communications · doi:10.1038/s41467-020-20057-8 · Cited by 79 · see citing works
Self-citationThe Role of Satellite Cells in Skeletal Muscle Regeneration—The Effect of Exercise and Age
Kaczmarek, A., Kaczmarek, M., Ciałowicz, M., Clemente, F. M., Wolański, P. M., Bădicu, G., & Murawska‐Ciałowicz, E. (2021) · Biology · doi:10.3390/biology10101056 · Cited by 80 · see citing works
Is the myonuclear domain size fixed?
van der Meer, S. F. T., Jaspers, R. T., & Degens, H. (2011) · PubMed · Cited by 78 · see citing works
The role of satellite cells in muscle hypertrophy
Blaauw, B., & Reggiani, C. (2014) · Journal of Muscle Research and Cell Motility · doi:10.1007/s10974-014-9376-y · Cited by 78 · see citing works
Sex differences in the response to resistance exercise training in older people
Da Boit, M., Sibson, R., Meakin, J. R., Aspden, R. M., Thies, F., Mangoni, A. A., & Gray, S. R. (2016) · Physiological Reports · doi:10.14814/phy2.12834 · Cited by 73 · see citing works
Alway, S. E., Bennett, B. T., Wilson, J. C., Sperringer, J., Mohamed, J. S., Edens, N. K., & Pereira, S. L. (2015) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00674.2014 · Cited by 73 · see citing works
Aoyama, S., Kim, H., Hirooka, R., Tanaka, M., Shimoda, T., Chijiki, H., Kojima, S., Sasaki, K., Takahashi, K., Makino, S., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2021.109336 · Cited by 73 · see citing works
Tsukamoto, S., Shibasaki, A., Naka, A., Saito, H., & Iida, K. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19113649 · Cited by 71 · see citing works
Farup, J., Rahbek, S. K., Riis, S., Vendelbo, M. H., Paoli, F. D., & Vissing, K. (2014) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00261.2014 · Cited by 70 · see citing works
Longtine, M. S., Chen, B., Odibo, A. O., Zhong, Y., & Nelson, D. M. (2011) · Reproduction · doi:10.1530/rep-11-0340 · Cited by 67 · see citing works
Snijders, T., Leenders, M., de Groot, C. P. G. M., van Loon, L. J. C., & Verdijk, L. B. (2019) · Experimental Gerontology · doi:10.1016/j.exger.2019.04.002 · Cited by 69 · see citing works
Lindholm, M. E., Giacomello, S., Solnestam, B. W., Fischer, H., Huss, M., Kjellqvist, S., & Sundberg, C. J. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006294 · Cited by 67 · see citing works
Lee, H., Kim, K., Kim, B., Shin, J., Rajan, S., Wu, J., Chen, X., Brown, M. D., Lee, S., & Park, J. (2018) · The Journal of Physiology · doi:10.1113/jp275308 · Cited by 67 · see citing works
An Integrated Approach to Skeletal Muscle Health in Aging
Agostini, D., Gervasi, M., Ferrini, F., Bartolacci, A., Stranieri, A., Piccoli, G., Barbieri, E., Sestili, P., Patti, A., Stocchi, V., et al. (2023) · Nutrients · doi:10.3390/nu15081802 · Cited by 76 · see citing works
Galimov, A., Merry, T. L., Luca, E., Rushing, E. J., Mizbani, A., Turcekova, K., Hartung, A., Croce, C. M., Ristow, M., & Krützfeldt, J. (2016) · Stem Cells · doi:10.1002/stem.2281 · Cited by 66 · see citing works
Coratella, G., & Schena, F. F. (2016) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2016-0321 · Cited by 66 · see citing works
Fukada, S., Akimoto, T., & Sotiropoulos, A. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2020.118742 · Cited by 65 · see citing works
Schwartz, L. M. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2018.01887 · Cited by 65 · see citing works
Sharples, A. P., Polydorou, I., Hughes, D. C., Owens, D. J., Hughes, T. M., & Stewart, C. E. (2015) · Biogerontology · doi:10.1007/s10522-015-9604-x · Cited by 64 · see citing works
Winje, I. M., Bengtsen, M., Eftestøl, E., Juvkam, I. S., Bruusgaard, J. C., & Gundersen, K. (2018) · Acta Physiologica · doi:10.1111/apha.13034 · Cited by 60 · see citing works
Self-citationMyD88 promotes myoblast fusion in a cell-autonomous manner
Hindi, S. M., Shin, J. S., Gallot, Y. S., Straughn, A. R., Simionescu-Bankston, A., Hindi, L., Xiong, G., Friedland, R. P., & Kumar, A. (2017) · Nature Communications · doi:10.1038/s41467-017-01866-w · Cited by 61 · see citing works
Lifetime analysis of mdx skeletal muscle reveals a progressive pathology that leads to myofiber loss
Massopust, R. T., Lee, Y. I., Pritchard, A. L., Nguyen, V.-K. M., McCreedy, D. A., & Thompson, W. J. (2020) · Scientific Reports · doi:10.1038/s41598-020-74192-9 · Cited by 58 · see citing works
Lueders, T. N., Zou, K., Huntsman, H. D., Meador, B. M., Mahmassani, Z. S., Abel, M., Valero, M. C., Huey, K. A., & Boppart, M. D. (2011) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00515.2010 · Cited by 60 · see citing works
Caterisano, A., Decker, D., Snyder, B., Feigenbaum, M. S., Glass, R. G., House, P., Sharp, C., Waller, M., & Witherspoon, Z. (2019) · Strength and conditioning journal · doi:10.1519/ssc.0000000000000477 · Cited by 59 · see citing works
Strengers, Y., & Maller, C. J. (2017) · Environment and Planning A Economy and Space · doi:10.1177/0308518x17694029 · Cited by 57 · see citing works
Latella, C., & Haff, G. G. (2020) · Sports · doi:10.3390/sports8070100 · Cited by 56 · see citing works
Ogasawara, R., Yasuda, T., Sakamaki, M., Ozaki, H., & Abe, T. (2011) · Clinical Physiology and Functional Imaging · doi:10.1111/j.1475-097x.2011.01031.x · Cited by 54 · see citing works
Kurosaka, M., Naıto, H., Ogura, Y., Machida, S., & Katamoto, S. (2011) · Acta Physiologica · doi:10.1111/j.1748-1716.2011.02381.x · Cited by 54 · see citing works
Sharples, A. P., & Turner, D. C. (2023) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00099.2023 · Cited by 53 · see citing works
Ormsbee, M. J., & Arciero, P. J. (2011) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0b013e31823b874c · Cited by 53 · see citing works
Skeletal muscle apoptotic response to physical activity: potential mechanisms for protection
Quadrilatero, J., Alway, S. E., & Dupont‐Versteegden, E. E. (2011) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h11-064 · Cited by 52 · see citing works
What determines myonuclear domain size?
Qaisar, R., & Larsson, L. (2014) · PubMed · Cited by 52 · see citing works
Hanssen, K. E., Kvamme, N. H., Nilsen, T. S., Rønnestad, B. R., Ambjørnsen, I. K., Norheim, F., Kadi, F., Hallén, J., Drevon, C. A., & Raastad, T. (2012) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2012.01452.x · Cited by 51 · see citing works
Transgender and Intersex Athletes and the Women’s Category in Sport
Sailors, P. R. (2020) · Sport Ethics and Philosophy · doi:10.1080/17511321.2020.1756904 · Cited by 75 · see citing works
Podbregar, M., Lainščak, M., Prelovsek, O., & Marš, T. (2013) · The Scientific World JOURNAL · doi:10.1155/2013/617170 · Cited by 49 · see citing works
Nilsen, T. S., Thorsen, L., Fosså, S. D., Wiig, M., Kirkegaard, C., Skovlund, E., Benestad, H. B., & Raastad, T. (2015) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.12543 · Cited by 46 · see citing works
Gender, Steroids, and Fairness in Sport
Devine, J. (2018) · Sport Ethics and Philosophy · doi:10.1080/17511321.2017.1404627 · Cited by 45 · see citing works
The Role of Fiber Types in Muscle Hypertrophy
Ogborn, D. I., & Schoenfeld, B. J. (2014) · Strength and conditioning journal · doi:10.1519/ssc.0000000000000030 · Cited by 45 · see citing works
Cellular and molecular pathways controlling muscle size in response to exercise
Attwaters, M., & Hughes, S. M. (2021) · FEBS Journal · doi:10.1111/febs.15820 · Cited by 45 · see citing works
Hunter, S. K., Angadi, S. S., Bhargava, A., Harper, J., Hirschberg, A. L., Levine, B. D., Moreau, K. L., Nokoff, N. J., Stachenfeld, N. S., & Bermon, S. (2023) · Translational Journal of the American College of Sports Medicine · doi:10.1249/tjx.0000000000000236 · Cited by 43 · see citing works
Drobnic, F., Lizarraga, M. A., Caballero-García, A., & Córdova, A. (2022) · Nutrients · doi:10.3390/nu14091811 · Cited by 43 · see citing works
Cornish, S. M., Bugera, E. M., Duhamel, T. A., Peeler, J. D., & Anderson, J. E. (2020) · European Journal of Applied Physiology · doi:10.1007/s00421-020-04337-1 · Cited by 43 · see citing works
Horwath, O., Moberg, M., Edman, S., Philp, A., & Apró, W. (2024) · Experimental Physiology · doi:10.1113/ep092222 · Cited by 41 · see citing works
- Authors
- Bruusgaard, J. C., Johansen, I. B., Egner, I. M., Rana, Z. A., & Gundersen, K.
- Affiliations
- University of Oslo (NO)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-08-16
- Volume
- 107
- Issue
- 34
- Pages
- 15111-15116
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2930527
- OpenAlex
- W2057868246
- Cited by
- 327
- References
- 57
- Citations by year
- 2026: 11 · 2025: 21 · 2024: 14 · 2023: 22 · 2022: 25 · 2021: 43 · 2020: 27 · 2019: 22 · 2018: 18 · 2017: 13 · 2016: 26 · 2015: 15 · 2014: 20 · 2013: 17 · 2012: 17
- FWCI
- 6.52
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Norges Forskningsråd (rcn-foriss-191730, rcn-foriss-182717)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
- Health Sciences › Medicine › Genetics › Neurogenetic and Muscular Disorders Research
- Keywords
- myonuclei, muscle hypertrophy, detraining, muscle memory, resistance training, denervation atrophy, disuse atrophy, apoptosis, myonuclear domain, aging, anabolic steroids
- MeSH terms
- Animals, Cell Nucleus, Female, Humans, Hypertrophy, Male, Models, Biological, Muscle Denervation, Muscular Atrophy, Physical Conditioning, Animal, Rats, Wistar, Apoptosis, Muscle Fibers, Skeletal, Models, Animal, Mice, Rats, Resistance Training
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