Cited by 327Muscle Physiology and DisordersMuscle metabolism and nutritionNeurogenetic and Muscular Disorders Research

The DOI matches its Crossref record; 56 of the 57 references it cites were found in a registry or an index.

Myonuclei acquired by overload exercise precede hypertrophy and are not lost on detraining

Open access

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.0913935107PMC PMC2930527

Open this paper in CoChat — free account

Abstract

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.

Integrity signals

Registry

Crossref · 10.1073/pnas.0913935107

Cites

56 of 56 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Morphologic and biochemical hallmarks of apoptosis
Saraste, A. (2000) · Cardiovascular Research · doi:10.1016/s0008-6363(99)00384-3 · Cited by 1,454
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
Coincidence, coevolution, or causation? DNA content, cellsize, and the C‐value enigma
GREGORY, T. R. (2001) · Biological Reviews · doi:10.1111/j.1469-185x.2000.tb00059.x · Cited by 730
Nuclear volume control by nucleoskeletal DNA, selection for cell volume and cell growth rate, and the solution of the DNA C-value paradox
Cavalier‐Smith, T. (1978) · Journal of Cell Science · doi:10.1242/jcs.34.1.247 · Cited by 683
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
Testosterone-induced increase in muscle size in healthy young men is associated with muscle fiber hypertrophy
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
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
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
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
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

Show all 57 references

Research works printed but not linked: 10

E Strassburger, Ûber die Wirkungssphäre der kerne und die zellgrösse. Histologische Beiträge 5, 97–124 (1893).
10.1017/S1464793100005595 · DOI · Paper page
RS O’Connor, GK Pavlath, In response to Point:Counterpoint: Satellite cell addition is/is not obligatory for skeletal muscle hypertrophy. J Appl Physiol 103, 1102 (2007).
10.1152/japplphysiol.00101.2007a · DOI
10.1152/japplphysiol.00466.2007 · DOI
10.1152/japplphysiol.00466.2007 · DOI
FW Booth, In response to Point:Counterpoint: Satellite cell addition is/is not obligatory for skeletal muscle hypertrophy. J Appl Physiol 103, 1105, (lett). (2007).
F Kadi, In response to Point:Counterpoint: Satellite cell addition is/is not obligatory for skeletal muscle hypertrophy. J Appl Physiol 103, 1105, (lett). (2007).
SC Bodine, In response to Point:Counterpoint: Satellite cell addition is/is not obligatory for skeletal muscle hypertrophy. J Appl Physiol 103, 1105–1106, (lett). (2007).
DA Lowe, In response to Point:Counterpoint: Satellite cell addition is/is not obligatory for skeletal muscle hypertrophy. J Appl Physiol 103, 1106, (lett). (2007).

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
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
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 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
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 404
Myogenic progenitor cells control extracellular matrix production by fibroblasts during skeletal muscle hypertrophy
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
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
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
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
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
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
Proliferation of myogenic stem cells in human skeletal muscle in response to low‐load resistance training with blood flow restriction
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
Mechanisms Modulating Skeletal Muscle Phenotype
Blaauw, B., Schiaffino, S., & Reggiani, C. (2013) · Comprehensive physiology · doi:10.1002/cphy.c130009 · Cited by 298
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 281
Self-citation
The Biological Basis of Sex Differences in Athletic Performance: Consensus Statement for the American College of Sports Medicine
HUNTER, 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
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
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 216
Self-citation
Skeletal muscle wasting with disuse atrophy is multi-dimensional: the response and interaction of myonuclei, satellite cells and signaling pathways
Brooks, N. E., & Myburgh, K. H. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00099 · Cited by 206
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
Fourteen days of bed rest induces a decline in satellite cell content and robust atrophy of skeletal muscle fibers in middle-aged adults
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 193
Does skeletal muscle have an ‘epi’-memory? The role of epigenetics in nutritional programming, metabolic disease, aging and exercise
Sharples, A. P., Stewart, C. E., & Seaborne, R. A. (2016) · Aging Cell · doi:10.1111/acel.12486 · Cited by 180
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 189
Transgender Women in the Female Category of Sport: Perspectives on Testosterone Suppression and Performance Advantage
Hilton, E. N., & Lundberg, T. R. (2021) · Sports Medicine · doi:10.1007/s40279-020-01389-3 · Cited by 236
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
Self-citation
Molecular 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 192
How does hormone transition in transgender women change body composition, muscle strength and haemoglobin? Systematic review with a focus on the implications for sport participation
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 206
Interactions between muscle stem cells, mesenchymal-derived cells and immune cells in muscle homeostasis, regeneration and disease
Farup, J., Madaro, L., Puri, P., & Mikkelsen, U. R. (2015) · Cell Death and Disease · doi:10.1038/cddis.2015.198 · Cited by 162
A cellular memory mechanism aids overload hypertrophy in muscle long after an episodic exposure to anabolic steroids
Egner, I. M., Bruusgaard, J. C., Eftestøl, E., & Gundersen, K. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2013.264457 · Cited by 159
Self-citation
Requirement of myomaker-mediated stem cell fusion for skeletal muscle hypertrophy
Goh, Q., & Millay, D. P. (2017) · eLife · doi:10.7554/elife.20007 · Cited by 167
A systems-based investigation into vitamin D and skeletal muscle repair, regeneration, and hypertrophy
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
Srf-Dependent Paracrine Signals Produced by Myofibers Control Satellite Cell-Mediated Skeletal Muscle Hypertrophy
Guerci, A., Lahoute, C., Hébrard, S., Collard, L., Graindorge, D., Favier, M., Cagnard, N., Batonnet‐Pichon, S., Précigout, G., García, L., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2011.12.001 · Cited by 152
Villous trophoblast apoptosis is elevated and restricted to cytotrophoblasts in pregnancies complicated by preeclampsia, IUGR, or preeclampsia with IUGR
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
Comparative Transcriptome and Methylome Analysis in Human Skeletal Muscle Anabolism, Hypertrophy and Epigenetic Memory
Turner, D. C., Seaborne, R. A. E., & Sharples, A. P. (2019) · Scientific Reports · doi:10.1038/s41598-019-40787-0 · Cited by 135
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
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
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 128
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 126
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 122
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 123
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 111
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
Self-citation
Elevated myonuclear density during skeletal muscle hypertrophy in response to training is reversed during detraining
Dungan, 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
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
The effect of resistance training, detraining and retraining on muscle strength and power, myofibre size, satellite cells and myonuclei in older men
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 107
Androgen Misuse and Abuse
Handelsman, D. J. (2021) · Endocrine Reviews · doi:10.1210/endrev/bnab001 · Cited by 104
Low-Load Bench Press Training to Fatigue Results in Muscle Hypertrophy Similar to High-Load Bench Press Training
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
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
Myonuclear Domain Flexibility Challenges Rigid Assumptions on Satellite Cell Contribution to Skeletal Muscle Fiber Hypertrophy
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
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
Effects of training, detraining, and retraining on strength, hypertrophy, and myonuclear number in human skeletal muscle
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
Self-citation
Fusion-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
Muscle memory: myonuclear accretion, maintenance, morphology, and miRNA levels with training and detraining in adult mice
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 98
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 98
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 98
Mechanical loading stimulates hypertrophy in tissue‐engineered skeletal muscle: Molecular and phenotypic responses
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
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 89
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
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 85
Self-citation
The 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 87
Is the myonuclear domain size fixed?
van der Meer, S. F. T., Jaspers, R. T., & Degens, H. (2011) · PubMed · Cited by 78
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 90
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
Green tea extract attenuates muscle loss and improves muscle function during disuse, but fails to improve muscle recovery following unloading in aged rats
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
Distribution of Dietary Protein Intake in Daily Meals Influences Skeletal Muscle Hypertrophy Via the Circadian Clock
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 77
Lactate Promotes Myoblast Differentiation and Myotube Hypertrophy via a Pathway Involving MyoD In Vitro and Enhances Muscle Regeneration In Vivo
Tsukamoto, S., Shibasaki, A., Naka, A., Saito, H., & Iida, K. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19113649 · Cited by 71
Influence of exercise contraction mode and protein supplementation on human skeletal muscle satellite cell content and muscle fiber growth.
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
Caspase-mediated apoptosis of trophoblasts in term human placental villi is restricted to cytotrophoblasts and absent from the multinucleated syncytiotrophoblast
Longtine, M. S., Chen, B., Odibo, A. O., Zhong, Y., & Nelson, D. M. (2011) · Reproduction · doi:10.1530/rep-11-0340 · Cited by 67
Muscle mass and strength gains following 6 months of resistance type exercise training are only partly preserved within one year with autonomous exercise continuation in older adults
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 74
The Impact of Endurance Training on Human Skeletal Muscle Memory, Global Isoform Expression and Novel Transcripts
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
A cellular mechanism of muscle memory facilitates mitochondrial remodelling following resistance training
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 71
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 81
MicroRNA-29a in Adult Muscle Stem Cells Controls Skeletal Muscle Regeneration During Injury and Exercise Downstream of Fibroblast Growth Factor-2
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 71
Eccentric resistance training increases and retains maximal strength, muscle endurance, and hypertrophy in trained men
Coratella, G., & Schena, F. F. (2016) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2016-0321 · Cited by 66
Role of damage and management in muscle hypertrophy: Different behaviors of muscle stem cells in regeneration and hypertrophy
Fukada, S., Akimoto, T., & Sotiropoulos, A. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2020.118742 · Cited by 71
Skeletal Muscles Do Not Undergo Apoptosis During Either Atrophy or Programmed Cell Death-Revisiting the Myonuclear Domain Hypothesis
Schwartz, L. M. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2018.01887 · Cited by 65
Skeletal muscle cells possess a ‘memory’ of acute early life TNF-α exposure: role of epigenetic adaptation
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
Specific labelling of myonuclei by an antibody against pericentriolar material 1 on skeletal muscle tissue sections
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
Self-citation
MyD88 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
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
The α 7 β 1 -integrin accelerates fiber hypertrophy and myogenesis following a single bout of eccentric exercise
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
CSCCa and NSCA Joint Consensus Guidelines for Transition Periods: Safe Return to Training Following Inactivity
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 58
Adapting to ‘extreme’ weather: mobile practice memories of keeping warm and cool as a climate change adaptation strategy
Strengers, Y., & Maller, C. J. (2017) · Environment and Planning A Economy and Space · doi:10.1177/0308518x17694029 · Cited by 57
Global Challenges of Being a Strength Athlete during a Pandemic: Impacts and Sports-Specific Training Considerations and Recommendations
Latella, C., & Haff, G. G. (2020) · Sports · doi:10.3390/sports8070100 · Cited by 60
Effects of periodic and continued resistance training on muscle CSA and strength in previously untrained men
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 61
Satellite cell pool enhancement in rat plantaris muscle by endurance training depends on intensity rather than duration
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
Skeletal muscle memory
Sharples, A. P., & Turner, D. C. (2023) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00099.2023 · Cited by 57
Detraining Increases Body Fat and Weight and Decreases V[Combining Dot Above]O2peak and Metabolic Rate
Ormsbee, M. J., & Arciero, P. J. (2011) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0b013e31823b874c · Cited by 53
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 56
What determines myonuclear domain size?
Qaisar, R., & Larsson, L. (2014) · PubMed · Cited by 51
The effect of strength training volume on satellite cells, myogenic regulatory factors, and growth factors
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 53
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
Cytokine Response of Cultured Skeletal Muscle Cells Stimulated with Proinflammatory Factors Depends on Differentiation Stage
Podbregar, M., Lainščak, M., Prelovsek, O., & Mars, T. (2013) · TheScientificWorldJournal · doi:10.1155/2013/617170 · Cited by 49
Effects of strength training on muscle cellular outcomes in prostate cancer patients on androgen deprivation therapy
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
Gender, Steroids, and Fairness in Sport
Devine, J. (2018) · Sport Ethics and Philosophy · doi:10.1080/17511321.2017.1404627 · Cited by 45
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
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 47
The Biological Basis of Sex Differences in Athletic Performance: Consensus Statement for the American College of Sports Medicine
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
Coenzyme Q10 Supplementation and Its Impact on Exercise and Sport Performance in Humans: A Recovery or a Performance-Enhancing Molecule?
Drobnic, F., Lizarraga, M. A., Caballero-García, A., & Córdova, A. (2022) · Nutrients · doi:10.3390/nu14091811 · Cited by 46
A focused review of myokines as a potential contributor to muscle hypertrophy from resistance-based exercise
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
Ageing leads to selective type II myofibre deterioration and denervation independent of reinnervative capacity in human skeletal muscle
Horwath, O., Moberg, M., Edman, S., Philp, A., & Apró, W. (2024) · Experimental Physiology · doi:10.1113/ep092222 · Cited by 41

Authors: Bruusgaard, J. C., Johansen, I. B., Egner, I. M., Rana, Z. A., & Gundersen, K.
Affiliations: University of Oslo (NO)
ORCID: Bruusgaard, J. C.
Johansen, I. B.
Egner, I. M.
Gundersen, K.
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
DOI: 10.1073/pnas.0913935107
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
Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
Health Sciences › Medicine › Genetics (clinical) › 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

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Myonuclei acquired by overload exercise precede hypertrophy and are not lost on detraining

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks