Does skeletal muscle have an ‘epi’-memory? The role of epigenetics in nutritional programming, metabolic disease, aging and exercise
Open accessAbstract
Skeletal muscle mass, quality and adaptability are fundamental in promoting muscle performance, maintaining metabolic function and supporting longevity and healthspan. Skeletal muscle is programmable and can 'remember' early-life metabolic stimuli affecting its function in adult life. In this review, the authors pose the question as to whether skeletal muscle has an 'epi'-memory? Following an initial encounter with an environmental stimulus, we discuss the underlying molecular and epigenetic mechanisms enabling skeletal muscle to adapt, should it re-encounter the stimulus in later life. We also define skeletal muscle memory and outline the scientific literature contributing to this field. Furthermore, we review the evidence for early-life nutrient stress and low birth weight in animals and human cohort studies, respectively, and discuss the underlying molecular mechanisms culminating in skeletal muscle dysfunction, metabolic disease and loss of skeletal muscle mass across the lifespan. We also summarize and discuss studies that isolate muscle stem cells from different environmental niches in vivo (physically active, diabetic, cachectic, aged) and how they reportedly remember this environment once isolated in vitro. Finally, we will outline the molecular and epigenetic mechanisms underlying skeletal muscle memory and review the epigenetic regulation of exercise-induced skeletal muscle adaptation, highlighting exercise interventions as suitable models to investigate skeletal muscle memory in humans. We believe that understanding the 'epi'-memory of skeletal muscle will enable the next generation of targeted therapies to promote muscle growth and reduce muscle loss to enable healthy aging.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
This hypomethylated signature was preserved even after weeks of total detraining and macroscopic atrophy.
“Crucially, this hypomethylated signature was preserved even after weeks of total detraining and macroscopic atrophy [119,120].”
From Ribosome Biogenesis as a Putative Bottleneck to Skeletal Muscle Hypertrophy: Mechanisms, Human Evidence, and Practical Modulators (2026) · cites this paper as [119]
In the section on exercise adaptation and skeletal muscle memory (page unavailable), the review says it remains unknown whether exercise-induced methylation changes are retained and proposes a detraining–retraining study to investigate that question. It therefore does not report a hypomethylated signature preserved through weeks of detraining and atrophy. (LLM, conf=0.90)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Regulation of chromatin by histone modifications
Bannister, A. J., & Kouzarides, T. (2011) · Cell Research · doi:10.1038/cr.2011.22 · Cited by 6,012 · see citing works
Conversion of 5-Methylcytosine to 5-Hydroxymethylcytosine in Mammalian DNA by MLL Partner TET1
Tahiliani, M., Koh, K. P., Shen, Y., Pastor, W. A., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L. M., Liu, D. R., Aravind, L., et al. (2009) · Science · doi:10.1126/science.1170116 · Cited by 5,836 · see citing works
Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase
Brunet, A., Sweeney, L. B., Sturgill, J. F., Chua, K. F., Greer, P. L., Lin, Y., Tran, H., Ross, S. E., Mostoslavsky, R., Cohen, H. Y., et al. (2004) · Science · doi:10.1126/science.1094637 · Cited by 3,239 · see citing works
Cloning of adiponectin receptors that mediate antidiabetic metabolic effects
Yamauchi, T., Kamon, J., Ito, Y., Tsuchida, A., Yokomizo, T., Kita, S., Sugiyama, T., Miyagishi, M., Hara, K., Tsunoda, M., et al. (2003) · Nature · doi:10.1038/nature01705 · Cited by 3,176 · see citing works
Sandri, M., Sandri, C., Gilbert, A., Skurk, C., Calabria, E., Picard, A., Walsh, K., Schiaffino, S., Lecker, S. H., & Goldberg, A. L. (2004) · Cell · doi:10.1016/s0092-8674(04)00400-3 · Cited by 3,012 · see citing works
Epigenetic Transgenerational Actions of Endocrine Disruptors and Male Fertility
Anway, M. D., Cupp, A. S., Uzumcu, M., & Skinner, M. K. (2005) · Science · doi:10.1126/science.1108190 · Cited by 2,563 · see citing works
Ito, S., D’Alessio, A. C., Taranova, O., Hong, K., Sowers, L. C., & Zhang, Y. (2010) · Nature · doi:10.1038/nature09303 · Cited by 2,542 · see citing works
Weber, M., Hellmann, I., Stadler, M. B., Ramos, L., Pääbo, S., Rebhan, M., & Schübeler, D. (2007) · Nature Genetics · doi:10.1038/ng1990 · Cited by 2,267 · see citing works
Double muscling in cattle due to mutations in the myostatin gene
McPherron, A. C., & Lee, S.-J. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.23.12457 · Cited by 2,039 · see citing works
Glucose tolerance in adults after prenatal exposure to famine
Ravelli, A., van der Meulen, J., Michels, R., Osmond, C., Barker, D., Hales, C., & Bleker, O. (1998) · The Lancet · doi:10.1016/s0140-6736(97)07244-9 · Cited by 1,606 · see citing works
Midlife Hand Grip Strength as a Predictor of Old Age Disability
Rantanen, T. (1999) · JAMA · doi:10.1001/jama.281.6.558 · Cited by 1,481 · see citing works
Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder
Chen, Q., Yan, M., Cao, Z., Li, X., Zhang, Y., Shi, J., Feng, G.-H., Peng, H., Zhang, X., Zhang, Y., et al. (2016) · Science · doi:10.1126/science.aad7977 · Cited by 1,470 · see citing works
Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes
Wang, Z., Zang, C., Cui, K., Schones, D. E., Barski, A., Peng, W., & Zhao, K. (2009) · Cell · doi:10.1016/j.cell.2009.06.049 · Cited by 1,344 · see citing works
Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice
Gapp, K., Jawaid, A., Sarkies, P., Bohacek, J., Pelczar, P., Prados, J., Farinelli, L., Miska, E., & Mansuy, I. M. (2014) · Nature Neuroscience · doi:10.1038/nn.3695 · Cited by 1,306 · see citing works
FOXO transcription factors at the interface between longevity and tumor suppression
Greer, E. L., & Brunet, A. (2005) · Oncogene · doi:10.1038/sj.onc.1209086 · Cited by 1,306 · see citing works
Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals
Sharma, U., Conine, C. C., Shea, J. M., Boskovic, A., Derr, A. G., Bing, X. Y., Belleannee, C., Kucukural, A., Serra, R. W., Sun, F., et al. (2016) · Science · doi:10.1126/science.aad6780 · Cited by 1,275 · see citing works
Krssak, M., Falk Petersen, K., Dresner, A., DiPietro, L., Vogel, S. M., Rothman, D. L., Shulman, G. I., & Roden, M. (1999) · Diabetologia · doi:10.1007/s001250051123 · Cited by 1,264 · see citing works
Obesity at the age of 50 y in men and women exposed to famine prenatally
Ravelli, A. C. J., van der Meulen, J., Osmond, C., Barker, D. J. P., & Bleker, O. P. (1999) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/70.5.811 · Cited by 1,165 · see citing works
Geriatric muscle stem cells switch reversible quiescence into senescence
Sousa-Victor, P., Gutarra, S., García-Prat, L., Rodriguez-Ubreva, J., Ortet, L., Ruiz-Bonilla, V., Jardí, M., Ballestar, E., González, S., Serrano, A. L., et al. (2014) · Nature · doi:10.1038/nature13013 · Cited by 1,010 · see citing works
The Molecular Basis of Skeletal Muscle Atrophy
Jackman, R. W., & Kandarian, S. C. (2004) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00579.2003 · Cited by 1,008 · see citing works
CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing
Shukla, S., Kavak, E., Gregory, M., Imashimizu, M., Shutinoski, B., Kashlev, M., Oberdoerffer, P., Sandberg, R., & Oberdoerffer, S. (2011) · Nature · doi:10.1038/nature10442 · Cited by 973 · see citing works
Acute Exercise Remodels Promoter Methylation in Human Skeletal Muscle
Barrès, R., Yan, J., Egan, B., Treebak, J. T., Rasmussen, M., Fritz, T., Caidahl, K., Krook, A., O'Gorman, D. J., & Zierath, J. R. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.01.001 · Cited by 965 · cited 6× · see citing works
“…acute aerobic exercise at 80% of maximal aerobic capacity (until 1674 KJ was expended) and a reduction in PPARd methylation 3 h post exercise, corresponding with reductions in their own gene expression (3 h post exercise for PGC-1a, PDK4 and PPAR-d, immediately post for TFAM) (Barres et al., 2012).”
BackgroundInfluentialSamuelsson, A.-M., Matthews, P. A., Argenton, M., Christie, M. R., McConnell, J. M., Jansen, E. H. J. M., Piersma, A. H., Ozanne, S. E., Twinn, D. F., Remacle, C., et al. (2008) · Hypertension · doi:10.1161/hypertensionaha.107.101477 · Cited by 923 · see citing works
Aberrant repair and fibrosis development in skeletal muscle
Mann, C. J., Perdiguero, E., Kharraz, Y., Aguilar, S., Pessina, P., Serrano, A. L., & Muñoz-Cánoves, P. (2011) · Skeletal Muscle · doi:10.1186/2044-5040-1-21 · Cited by 853 · cited 2× · see citing works
“…vs. skeletal muscle tissue accretion in the foetal skeletal muscle (Tong et al., 2009), a hall mark of sarcopenia, and one of the fundamental causes of reduced muscle force and quality (force per cross-sectional area of muscle) (reviewed in Serrano & Munoz-Canoves, 2010; Mann et al., 2011).”
BackgroundStressing the role of FoxO proteins in lifespan and disease
van der Horst, A., & Burgering, B. M. T. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2190 · Cited by 759 · see citing works
Grip strength, body composition, and mortality
Galé, C. R., Martyn, C., Cooper, C. C., & Sayer, A. A. (2006) · International Journal of Epidemiology · doi:10.1093/ije/dyl224 · Cited by 740 · see citing works
The molecular regulation of myogenesis
Sabourin, L. A., & Rudnicki, M. A. (2000) · Clinical Genetics · doi:10.1034/j.1399-0004.2000.570103.x · Cited by 720 · see citing works
A model for transmission of the H3K27me3 epigenetic mark
Hansen, K. H., Bracken, A. P., Pasini, D., Dietrich, N., Gehani, S. S., Monrad, A., Rappsilber, J., Lerdrup, M., & Helin, K. (2008) · Nature Cell Biology · doi:10.1038/ncb1787 · Cited by 720 · see citing works
Bhutani, N., Burns, D. M., & Blau, H. M. (2011) · Cell · doi:10.1016/j.cell.2011.08.042 · Cited by 688 · see citing works
Coronary heart disease after prenatal exposure to the Dutch famine, 1944-45
Roseboom, T. J. (2000) · Heart · doi:10.1136/heart.84.6.595 · Cited by 682 · see citing works
SIRT2 deacetylates FOXO3a in response to oxidative stress and caloric restriction
Wang, F., Nguyen, M., Qin, F. X.-F., & Tong, Q. (2007) · Aging Cell · doi:10.1111/j.1474-9726.2007.00304.x · Cited by 652 · see citing works
Age-related inflammatory cytokines and disease
Brüünsgaard, H., & Pedersen, B. K. (2003) · Immunology and Allergy Clinics of North America · doi:10.1016/s0889-8561(02)00056-5 · Cited by 608 · see citing works
Non-CpG methylation of the PGC-1α promoter through DNMT3B controls mitochondrial density.
Barrès, R., Osler, M. E., Yan, J., Rune, A., Fritz, T., Caidahl, K., Krook, A., & Zierath, J. R. (2009) · Cell Metabolism · doi:10.1016/j.cmet.2009.07.011 · Cited by 602 · see citing works
Lau, M. M., Stewart, C. E., Liu, Z., Bhatt, H., Rotwein, P. S., & Stewart, C. L. (1994) · Genes & Development · doi:10.1101/gad.8.24.2953 · Cited by 602 · see citing works
Self-citationLong-Lived Drosophila with Overexpressed dFOXO in Adult Fat Body
Giannakou, M. E., Goss, M. W., Jünger, M. A., Hafen, E., Leevers, S. J., & Partridge, L. (2004) · Science · doi:10.1126/science.1098219 · Cited by 577 · see citing works
Maunakea, A. K., Chepelev, I., Cui, K., & Zhao, K. (2013) · Cell Research · doi:10.1038/cr.2013.110 · Cited by 552 · see citing works
Almeida, M., Li, H., Martín-Millán, M., O’Brien, C. A., & Manolagas, S. C. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m702811200 · Cited by 546 · see citing works
Obesity and Bariatric Surgery Drive Epigenetic Variation of Spermatozoa in Humans
Donkin, I., Versteyhe, S., Ingerslev, L. R., Qian, K., Mechta, M., Nordkap, L., Mortensen, B., Appel, E. V. R., Jørgensen, N., Kristiansen, V. B., et al. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.11.004 · Cited by 533 · see citing works
Satellite-cell pool size does matter: Defining the myogenic potency of aging skeletal muscle
Shefer, G., de Mark, D. P. V., Richardson, J. B., & Yablonka‐Reuveni, Z. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.02.022 · Cited by 506 · see citing works
Muscle fiber type is associated with obesity and weight loss
Tanner, C. J., Barakat, H. A., Dohm, G. L., Pories, W. J., MacDonald, K. G., Cunningham, P. R. G., Swanson, M. S., & Houmard, J. A. (2002) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00416.2001 · Cited by 493 · see citing works
DNA methylation and methyl-CpG binding proteins: developmental requirements and function
Bogdanović, O., & Veenstra, G. J. C. (2009) · Chromosoma · doi:10.1007/s00412-009-0221-9 · Cited by 474 · see citing works
Resistance exercise decreases skeletal muscle tumor necrosis factor α in frail elderly humans
GREIWE, J. S., CHENG, B., RUBIN, D. C., YARASHESKI, K. E., & SEMENKOVICH, C. F. (2001) · The FASEB Journal · doi:10.1096/fj.00-0274com · Cited by 454 · cited 2× · see citing works
“As chronic TNF-a is increased in the circulation (Greiwe et al., 2001; Bruunsgaard & Pedersen, 2003; Bruunsgaard et al., 2003a,b) and in that produced by skeletal muscle tissue in aged individuals (Greiwe et al., 2001; Leger et al., 2008) as well as being associated with sarcopenia and muscle loss…”
BackgroundTrithorax group proteins: switching genes on and keeping them active
Schuettengruber, B., Martinez, A., Iovino, N., & Cavalli, G. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3230 · Cited by 454 · see citing works
The nuclear factor kappa B signaling pathway: integrating metabolism with inflammation
Tornatore, L., Thotakura, A. K., Bennett, J., Moretti, M., & Franzoso, G. (2012) · Trends in Cell Biology · doi:10.1016/j.tcb.2012.08.001 · Cited by 448 · see citing works
Nuclear factor-kappa B signaling in skeletal muscle atrophy
Li, H., Malhotra, S., & Kumar, A. (2008) · Journal of Molecular Medicine · doi:10.1007/s00109-008-0373-8 · Cited by 442 · see citing works
RNA-mediated paternal heredity of diet-induced obesity and metabolic disorders
Grandjean, V., Fourré, S., de Abreu, D. A. F., Derieppe, M., Rémy, J., & Rassoulzadegan, M. (2015) · Scientific Reports · doi:10.1038/srep18193 · Cited by 417 · see citing works
Nitert, M. D., Dayeh, T., Volkov, P., Elgzyri, T., Hall, E., Nilsson, E., Yang, B. T., Lang, S., Parikh, H. M., Wessman, Y., et al. (2012) · Diabetes · doi:10.2337/db11-1653 · Cited by 405 · 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
Phillips, D. I. W., Caddy, S., Ilic, V., Fielding, B. A., Frayn, K. N., Borthwick, A. C., & Taylor, R. (1996) · Metabolism · doi:10.1016/s0026-0495(96)90260-7 · Cited by 390 · see citing works
Maternal nutrient restriction affects properties of skeletal muscle in offspring
Zhu, M. J., Ford, S. P., Means, W. J., Hess, B. W., Nathanielsz, P. W., & Du, . (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.112110 · Cited by 360 · see citing works
Khan, I. Y., Dekou, V., Douglas, G., Jensen, R., Hanson, M. A., Poston, L., & Taylor, P. D. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00354.2004 · Cited by 357 · see citing works
Plasma lipid profiles in adults after prenatal exposure to the Dutch famine
Roseboom, T. J., van der Meulen, J. H., Osmond, C., Barker, D. J., Ravelli, A. C., & Bleker, O. P. (2000) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/72.5.1101 · Cited by 357 · see citing works
Muscle Fiber Composition and Capillary Density in Women and Men With NIDDM
Mårin, P., Andersson, B., Krotkiewski, M., & Björntorp, P. A. (1994) · Diabetes Care · doi:10.2337/diacare.17.5.382 · Cited by 342 · see citing works
Ford, S. P., Hess, B. W., Schwope, M. M., Nijland, M. J., Gilbert, J. S., Vonnahme, K. A., Means, W. J., Han, H., & Nathanielsz, P. W. (2007) · Journal of Animal Science · doi:10.2527/jas.2005-624 · Cited by 331 · see citing works
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 · see citing works
Elevated levels of tumor necrosis factor alpha and mortality in centenarians
Bruunsgaard, H., Andersen-Ranberg, K., Hjelmborg, J. V. B., Pedersen, B. K., & Jeune, B. (2003) · The American Journal of Medicine · doi:10.1016/s0002-9343(03)00329-2 · Cited by 325 · see citing works
Muscle strength, disability and mortality
Rantanen, T. (2003) · Scandinavian Journal of Medicine & Science in Sports · doi:10.1034/j.1600-0838.2003.00298.x · Cited by 317 · cited 1× · see citing works
“These impairments in muscle function are associated with earlier onset of disability, morbidity and mortality (Laukkanen et al., 1995; Rantanen et al., 1999, 2002; Rantanen, 2003; Gale et al., 2007).”
BackgroundWnt signaling and the activation of myogenesis in mammals
Cossu, G., & Borello, U. (1999) · The EMBO Journal · doi:10.1093/emboj/18.24.6867 · Cited by 312 · see citing works
Gluckman, P. D., Lillycrop, K. A., Vickers, M. H., Pleasants, A. B., Phillips, E. S., Beedle, A. S., Burdge, G. C., & Hanson, M. A. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705667104 · Cited by 309 · see citing works
Predicting death from tumour necrosis factor-alpha and interleukin-6 in 80-year-old people
BRUUNSGAARD, H., LADELUND, S., PEDERSEN, A. N., SCHROLL, M., JØRGENSEN, T., & PEDERSEN, B. K. (2003) · Clinical and Experimental Immunology · doi:10.1046/j.1365-2249.2003.02137.x · Cited by 300 · see citing works
Exercise-induced histone modifications in human skeletal muscle
McGee, S. L., Fairlie, E., Garnham, A. P., & Hargreaves, M. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.181065 · Cited by 296 · see citing works
Regulation and dysregulation of fibrosis in skeletal muscle
Serrano, A. L., & Muñoz‐Cánoves, P. (2010) · Experimental Cell Research · doi:10.1016/j.yexcr.2010.05.035 · Cited by 291 · see citing works
Low birthweight is associated with specific changes in muscle insulin-signalling protein expression
Ozanne, S. E., Jensen, C. B., Tingey, K., Storgaard, H., Madsbad, S., & Vaag, A. A. (2005) · Diabetologia · doi:10.1007/s00125-005-1669-7 · Cited by 286 · see citing works
Léger, B., Derave, W., Bock, K. D., Hespel, P., & Russell, A. P. (2008) · Rejuvenation Research · doi:10.1089/rej.2007.0588 · Cited by 274 · see citing works
Taaffe, D. R., Henwood, T. R., Nalls, M. A., Walker, D. G., Lang, T. F., & Harris, T. B. (2009) · Gerontology · doi:10.1159/000182084 · Cited by 269 · see citing works
Troy, A., Cadwallader, A. B., Fedorov, Y., Tyner, K., Tanaka, K. K., & Olwin, B. B. (2012) · Cell Stem Cell · doi:10.1016/j.stem.2012.05.025 · Cited by 268 · cited 1× · see citing works
“Populations of the mitotic cells also self-renew to allow the replenishment of the stem cell pool for future regenerative bouts (Troy et al., 2012).”
BackgroundMuscle strength as a predictor of onset of ADL dependence in people aged 75 years.
Rantanen, T., Avlund, K., Suominen, H., Schroll, M., Frändin, K., & Era, P. A. (2002) · PubMed · Cited by 263 · see citing works
Muscle Strength and Mobility as Predictors of Survival in 75–84 - Year - old People
Laukkanen, P., Heikkinen, E. M., & Kauppinen, M. (1995) · Age and Ageing · doi:10.1093/ageing/24.6.468 · Cited by 259 · see citing works
Effect of Maternal Nutrient Restriction in Sheep on the Development of Fetal Skeletal Muscle1
Zhu, M.-J., Ford, S. P., Nathanielsz, P. W., & Du, . (2004) · Biology of Reproduction · doi:10.1095/biolreprod.104.034561 · Cited by 256 · see citing works
Srinivasan, M., Katewa, S. D., Palaniyappan, A., Pandya, J. D., & Patel, M. S. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00078.2006 · Cited by 254 · see citing works
Elahi, M. M., Cagampang, F. R. A., Mukhtar, D., Anthony, F. W., Ohri, S. K., & Hanson, M. A. (2009) · British Journal Of Nutrition · doi:10.1017/s000711450820749x · Cited by 254 · see citing works
TrxG and PcG Proteins but Not Methylated Histones Remain Associated with DNA through Replication
Petruk, S., Sedkov, Y., Johnston, D. M., Hodgson, J. W., Black, K. L., Kovermann, S. K., Beck, S., Canaani, E., Brock, H. W., & Mazo, A. (2012) · Cell · doi:10.1016/j.cell.2012.06.046 · Cited by 246 · see citing works
Programming of glucose-insulin metabolism in adult sheep after maternal undernutrition
Gardner, D. S., Tingey, K., van Bon, B. W. M., Ozanne, S. E., Wilson, V., Dandrea, J., Keisler, D. H., Stephenson, T. J., & Symonds, M. E. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00120.2005 · Cited by 242 · see citing works
Schmidl, C., Klug, M., Boeld, T. J., Andreesen, R., Hoffmann, P., Edinger, M., & Rehli, M. (2009) · Genome Research · doi:10.1101/gr.091470.109 · Cited by 239 · see citing works
Loss of stem cell regenerative capacity within aged niches
Carlson, M. E., & Conboy, I. M. (2007) · Aging Cell · doi:10.1111/j.1474-9726.2007.00286.x · Cited by 233 · see citing works
Does Sarcopenia Originate in Early Life? Findings From the Hertfordshire Cohort Study
Sayer, A. A., Syddall, H. E., Gilbody, H., Dennison, E. M., & Cooper, C. C. (2004) · The Journals of Gerontology Series A · doi:10.1093/gerona/59.9.m930 · Cited by 214 · see citing works
Bakkar, N., Wang, J., Ladner, K. J., Wang, H., Dahlman, J. M., Carathers, M., Acharyya, S., Rudnicki, M. A., Hollenbach, A. D., & D, D. C. G. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200707179 · Cited by 208 · see citing works
Laker, R., Lillard, T. S., Okutsu, M., Zhang, M., Hoehn, K. L., Connelly, J., & Yan, Z. (2014) · Diabetes · doi:10.2337/db13-1614 · Cited by 205 · see citing works
Sharples, A. P., Hughes, D. C., Deane, C. S., Saini, A. S., Selman, C., & Stewart, C. E. (2015) · Aging Cell · doi:10.1111/acel.12342 · Cited by 200 · see citing works
Self-citationJacobsen, S., Brøns, C., Bork-Jensen, J., Ribel-Madsen, R., Yang, B., Lara, E., Hall, E., Calvanese, V., Nilsson, E., Jørgensen, S. W., et al. (2012) · Diabetologia · doi:10.1007/s00125-012-2717-8 · Cited by 197 · see citing works
Sayer, A. A., Syddall, H. E., Dennison, E. M., Gilbody, H., Duggleby, S., Cooper, C. C., Barker, D. J., & Phillips, D. I. (2004) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/80.1.199 · Cited by 182 · see citing works
Maternal obesity downregulates myogenesis and β-catenin signaling in fetal skeletal muscle
Tong, J. F., Yan, X., Zhu, M. J., Ford, S. P., Nathanielsz, P. W., & Du, . (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90924.2008 · Cited by 182 · see citing works
Genome‐wide DNA methylation changes with age in disease‐free human skeletal muscle
Zykovich, A., Hubbard, A., Flynn, J. M., Tarnopolsky, M. A., Fraga, M. F., Kerksick, C. M., Ogborn, D. I., MacNeil, L., Mooney, S. D., & Melov, S. (2013) · Aging Cell · doi:10.1111/acel.12180 · Cited by 179 · see citing works
Jackson, M. J., & McArdle, A. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.206623 · Cited by 177 · see citing works
Bakkar, N., Wang, J., Ladner, K. J., Wang, H., Dahlman, J. M., Carathers, M., Acharyya, S., Rudnicki, M. A., Hollenbach, A. D., & D, D. C. G. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.20070717908082013c · Cited by 174 · 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
Fahey, A. J., Brameld, J. M., Parr, T., & BUTTERY, P. J. (2005) · Journal of Animal Science · doi:10.2527/2005.83112564x · Cited by 168 · see citing works
Epigenetic inheritance of cell differentiation status
Ng, R. K., & Gurdon, J. B. (2008) · Cell Cycle · doi:10.4161/cc.7.9.5791 · Cited by 166 · see citing works
Waste management—Cytokines, growth factors and cachexia
Saini, A., Al‐Shanti, N., & Stewart, C. E. (2006) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2006.09.006 · Cited by 165 · see citing works
Self-citationEgner, 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
Zhu, M. J., Han, B., Tong, J., Ma, C., Kimzey, J. M., Underwood, K. R., Xiao, Y., Hess, B. W., Ford, S. P., Nathanielsz, P. W., et al. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2007.149633 · Cited by 153 · see citing works
Epigenetic inheritance: histone bookmarks across generations
Campos, E. I., Stafford, J. M., & Reinberg, D. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2014.08.004 · Cited by 145 · see citing works
Replicative aging down‐regulates the myogenic regulatory factors in human myoblasts
Bigot, A., Jacquemin, V., Debacq‐Chainiaux, F., Butler-Browne, G. S., Toussaint, O., Furling, D., & Mouly, V. (2008) · Biology of the Cell · doi:10.1042/bc20070085 · Cited by 141 · see citing works
Draeger, A., Weeds, A. G., & Fitzsimons, R. B. (1987) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(87)90181-x · Cited by 141 · see citing works
Epigenetic regulation on gene expression induced by physical exercise.
Ntanasis‐Stathopoulos, I., Tzanninis, J. G., Philippou, Α., & Koutsilieris, M. (2013) · PubMed · Cited by 132 · see citing works
Heightened muscle inflammation susceptibility may impair regenerative capacity in aging humans
Merritt, E. K., Stec, M. J., Thalacker-Mercer, A., Windham, S. T., Cross, J. M., Shelley, D. P., Craig Tuggle, S., Kosek, D. J., Kim, J.-S., & Bamman, M. M. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00019.2013 · Cited by 127 · see citing works
Bigot, A., Duddy, W. J., Ouandaogo, Z. G., Négroni, E., Mariot, V., Ghimbovschi, S. D., Harmon, B. T., Wielgosik, A., Loiseau, C., Devaney, J., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.09.067 · Cited by 125 · see citing works
Impact of manipulations of myogenesis in utero on the performance of adult skeletal muscle
Maltin, C. A., Delday, M., Sinclair, K., Steven, J., & Sneddon, A. A. (2001) · Reproduction · doi:10.1530/rep.0.1220359 · Cited by 124 · see citing works
Brameld, J. M., Mostyn, A., Dandrea, J., Stephenson, T. J., Dawson, J. M., BUTTERY, P. J., & Symonds, M. E. (2000) · Journal of Endocrinology · doi:10.1677/joe.0.1670429 · Cited by 121 · see citing works
Fetal programming of body composition and musculoskeletal development
Sayer, A. A., & Cooper, C. C. (2005) · Early Human Development · doi:10.1016/j.earlhumdev.2005.07.003 · Cited by 120 · see citing works
Smith, J. A. H., Kohn, T. A., Chetty, A. K., & Ojuka, E. O. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00747.2007 · Cited by 115 · cited 1× · see citing works
“These included increases in DNA methylation of runt-related transcription factor 1 (RUNX1) and myocyte-specific enhancer factor 2A (MEF2A), transcription factors involved in exercise-induced changes in Glut4 expression influencing glucose uptake in skeletal muscle (Smith et al., 2007, 2008).”
BackgroundHenwood, T. R., & Taaffe, D. R. (2008) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/63.7.751 · Cited by 113 · see citing works
Aguer, C., Mercier, J. G., Man, C. Y. W., Metz, L., Bordenave, S., Lambert, K., Jean, E., Lantier, L., Bounoua, L., Brun, J. ‐., et al. (2010) · Diabetologia · doi:10.1007/s00125-010-1708-x · Cited by 110 · 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
Shelley, P., Martin‐Gronert, M. S., Rowlerson, A. M., Poston, L., Heales, S., Hargreaves, I. P., McConnell, J. M. L., Ozanne, S. E., & Fernandez‐Twinn, D. S. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00146.2009 · Cited by 107 · see citing works
Wilson, S. J., McEwan, J. C., Sheard, P. W., et al. (1992) · Journal of Muscle Research and Cell Motility · doi:10.1007/bf01737996 · Cited by 105 · see citing works
Effects of sleeping with reduced carbohydrate availability on acute training responses
Lane, S. C., Camera, D. M., Lassiter, D. G., Areta, J. L., Bird, S. R., Yeo, W. K., Jeacocke, N. A., Krook, A., Zierath, J. R., Burke, L. M., et al. (2015) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00857.2014 · Cited by 102 · see citing works
Multifaceted roles of TNF‐α in myoblast destruction: A multitude of signal transduction pathways
Stewart, C. E., Newcomb, P. V., & Holly, J. M. P. (2003) · Journal of Cellular Physiology · doi:10.1002/jcp.10387 · Cited by 99 · see citing works
Self-citationPietrangelo, T., Puglielli, C., Mancinelli, R., Beccafico, S., Fanò, G., & Fulle, S. (2009) · Experimental Gerontology · doi:10.1016/j.exger.2009.05.002 · Cited by 98 · see citing works
Early Life Nutrition Modulates Muscle Stem Cell Number: Implications for Muscle Mass and Repair
Woo, M., ISGANAITIS, E. M., Cerletti, M., Fitzpatrick, C., Wagers, A. J., Jimenez-Chillaron, J., & Patti, M. (2011) · Stem Cells and Development · doi:10.1089/scd.2010.0349 · Cited by 97 · see citing works
A Second Look at Fiber Type Differentiation in Porcine Skeletal Muscle
Beermann, D. H., CASSENS, R. G., & Hausman, G. (1978) · Journal of Animal Science · doi:10.2527/jas1978.461125x · Cited by 93 · see citing works
A critical period for formation of secondary myotubes defined by prenatal undernourishment in rats
Wilson, S. J., Ross, J. J., & Harris, A. (1988) · Development · doi:10.1242/dev.102.4.815 · Cited by 91 · see citing works
Kandalla, P. K., Goldspink, G., Butler-Browne, G. S., & Mouly, V. (2011) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2011.02.007 · Cited by 89 · see citing works
Fujimaki, S., Hidaka, R., Asashima, M., Takemasa, T., & Kuwabara, T. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.539247 · Cited by 89 · see citing works
Sati, S., Tanwar, V. S., Kumar, K. A., Patowary, A., Jain, V. K., Ghosh, S., Ahmad, S., Singh, M., Reddy, S., Chandak, G. R., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031621 · Cited by 88 · see citing works
Epigenetic Regulation by Heritable RNA
Liebers, R., Rassoulzadegan, M., & Lyko, F. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004296 · Cited by 86 · see citing works
Alsharidah, M. S., Lazarus, N. R., George, T., Agley, C. C., Velloso, C. P., & Harridge, S. D. R. (2013) · Aging Cell · doi:10.1111/acel.12051 · Cited by 85 · see citing works
Modelling in vivo skeletal muscle ageing in vitro using three‐dimensional bioengineered constructs
Sharples, A. P., Player, D. J., Martin, N. R. W., Mudera, V., Stewart, C. E., & Lewis, M. P. (2012) · Aging Cell · doi:10.1111/j.1474-9726.2012.00869.x · Cited by 84 · see citing works
Self-citationCHARGÉ, S. B. P., Brack, A. S., & Hughes, S. M. (2002) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00206.2002 · Cited by 84 · see citing works
Yates, D. T., Clarke, D. S., Macko, A. R., Anderson, M. J., Shelton, L. A., Nearing, M., Allen, R. E., Rhoads, R. P., & Limesand, S. W. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.272591 · Cited by 80 · see citing works
Costello, P. M., Rowlerson, A. M., Astaman, N. A., Anthony, F. E. W., Sayer, A. A., Cooper, C. C., Hanson, M. A., & Green, L. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.150987 · Cited by 79 · see citing works
Patel, H. P., Al‐Shanti, N., Davies, L., Barton, S. J., Grounds, M. D., Tellam, R. L., Stewart, C. E., Cooper, C. C., & Sayer, A. A. (2014) · Calcified Tissue International · doi:10.1007/s00223-014-9894-z · Cited by 77 · see citing works
Self-citationDNA Methylation in Skeletal Muscle Stem Cell Specification, Proliferation, and Differentiation
Laker, R. C., & Ryall, J. G. (2016) · Stem Cells International · doi:10.1155/2016/5725927 · Cited by 77 · see citing works
Myogenesis in sheep is altered by maternal feed intake during the peri-conception period
Quigley, S. P., Kleemann, D. O., Kakar, M. A., Owens, J. A., Nattrass, G. S., Maddocks, S., & Walker, S. K. (2004) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2004.11.005 · Cited by 76 · see citing works
Sayer, A., Dennison, E., Syddall, H., Jameson, K., Martin, H., & Cooper, C. (2008) · The journals of gerontology. Series A, Biological sciences and medical sciences · doi:10.1093/gerona/63.8.835 · Cited by 74 · see citing works
Epigenetic regulation of satellite cell activation during muscle regeneration
Dilworth, F. J., & Blais, A. (2011) · Stem Cell Research & Therapy · doi:10.1186/scrt59 · Cited by 73 · see citing works
Trasler, J., Deng, L.-Y., Melnyk, S., Pogribny, I., Hiou-Tim, F., Sibani, S., Oakes, C., Li, E., James, S., & Rozen, R. (2003) · Carcinogenesis · doi:10.1093/carcin/24.1.39 · Cited by 72 · see citing works
Latouche, C., Heywood, S. E., Henry, S. L., Ziemann, M., Lazarus, R. M., El‐Osta, A., Armitage, J. A., & Kingwell, B. A. (2013) · Journal of Nutrition · doi:10.3945/jn.113.186775 · Cited by 71 · see citing works
Dwyer, C. M., Madgwick, A. J. A., Ward, S., & Stickland, N. C. (1995) · Reproduction Fertility and Development · doi:10.1071/rd9951285 · Cited by 70 · see citing works
IGF-II Promotes Mesoderm Formation
Morali, O. G., Jouneau, A., McLaughlin, K. J., Thiery, J. P., & Larue, L. (2000) · Developmental Biology · doi:10.1006/dbio.2000.9875 · Cited by 70 · see citing works
Epigenetic control of adult skeletal muscle stem cell functions
Segalés, J., Perdiguero, E., & Muñoz‐Cánoves, P. (2014) · FEBS Journal · doi:10.1111/febs.13065 · Cited by 68 · see citing works
Developmental Influences, Muscle Morphology, and Sarcopenia in Community-Dwelling Older Men
Patel, H. P., Jameson, K. A., Syddall, H. E., Martin, H., Stewart, C. E., Cooper, C. C., & Sayer, A. A. (2011) · The Journals of Gerontology Series A · doi:10.1093/gerona/glr020 · Cited by 67 · see citing works
Self-citationSharples, 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
Self-citationSharples, A. P., Al‐Shanti, N., Lewis, M. P., & Stewart, C. E. (2011) · Journal of Cellular Biochemistry · doi:10.1002/jcb.23308 · Cited by 64 · see citing works
Self-citationHuman muscle satellite cells show age-related differential expression of S100B protein and RAGE
Beccafico, S., Riuzzi, F., Puglielli, C., Mancinelli, R., Fulle, S., Sorci, G., & Donato, R. (2010) · AGE · doi:10.1007/s11357-010-9197-x · Cited by 64 · see citing works
Sharples, A. P., Al‐Shanti, N., & Stewart, C. E. (2010) · Journal of Cellular Physiology · doi:10.1002/jcp.22252 · Cited by 63 · see citing works
Self-citationAgeing affects the differentiation potential of human myoblasts
Lorenzon, P., Bandi, E., de Guarrini, F., Pietrangelo, T., Schäfer, R. B., Zweyer, M., Wernig, A., & Ruzzier, F. (2004) · Experimental Gerontology · doi:10.1016/j.exger.2004.07.008 · Cited by 62 · see citing works
Smith, J. A. H., Collins, M., Grobler, L., Magee, C. J., & Ojuka, E. O. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00142.2006 · Cited by 60 · see citing works
Taguchi, T., Kishikawa, H., Motoshima, H., Sakai, K., Nishiyama, T., Yoshizato, K., Shirakami, A., Toyonaga, T., Shirotani, T., Araki, E., et al. (2000) · Metabolism · doi:10.1053/meta.2000.6755 · Cited by 59 · see citing works
Age-associated decrease in muscle precursor cell differentiation
Lees, S. J., Rathbone, C. R., & Booth, F. W. (2005) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00408.2005 · Cited by 58 · see citing works
Mallinson, J. E., Sculley, D., Craigon, J., Plant, R., Langley‐Evans, S. C., & Brameld, J. M. (2007) · British Journal Of Nutrition · doi:10.1017/s0007114507701678 · Cited by 58 · see citing works
Cell-Nonautonomous Effects of dFOXO/DAF-16 in Aging
Alic, N., Tullet, J. M. A., Niccoli, T., Broughton, S. J., Hoddinott, M. P., Slack, C., Gems, D., & Partridge, L. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.01.015 · Cited by 57 · see citing works
Satellite cell characterization from aging human muscle
Corbu, A., Scaramozza, A., Badiali-DeGiorgi, L., Tarantino, L., Papa, V., Rinaldi, R., D’Alessandro, R., Zavatta, M., Laus, M., Lattanzi, G., et al. (2010) · Neurological Research · doi:10.1179/174313209x385725 · Cited by 56 · see citing works
Epigenetic Modifications of the PGC-1α Promoter during Exercise Induced Expression in Mice
Lochmann, T. L., Thomas, R. R., Bennett, J. P., & Taylor, S. M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129647 · Cited by 54 · see citing works
Why are slow and fast muscles differentially affected during prenatal undernutrition?
Ward, S. S., & Stickland, N. C. (1991) · Muscle & Nerve · doi:10.1002/mus.880140310 · Cited by 50 · see citing works
Zeng, Y., Gu, P., Liu, K., & Huang, P. (2012) · Molecular Medicine Reports · doi:10.3892/mmr.2012.1134 · Cited by 50 · see citing works
Hertfordshire sarcopenia study: design and methods
Patel, H. P., Syddall, H. E., Martin, H. J., Stewart, C. E., Cooper, C., & Sayer, A. A. (2010) · BMC Geriatrics · doi:10.1186/1471-2318-10-43 · Cited by 48 · cited 2× · see citing works
“Aging Cell published by the Anatomical Society and John Wiley & Sons Ltd. the skeletal muscle mass, low strength and slower gait speed in men and women into old age (Sayer et al., 2004b, 2008; Sayer & Cooper, 2005; Patel et al., 2010, 2011, 2012, 2014).”
BackgroundSelf-citationOxidative Stress and Cancer: A β-Catenin Convergence
Bowerman, B. A. (2005) · Science · doi:10.1126/science.1113356 · Cited by 47 · see citing works
Dwyer, C. M., & Stickland, N. C. (1994) · British Journal Of Nutrition · doi:10.1079/bjn19940022 · Cited by 46 · see citing works
Saini, A. S., Al‐Shanti, N., Sharples, A. P., & Stewart, C. E. (2011) · Experimental Physiology · doi:10.1113/expphysiol.2011.061028 · Cited by 44 · see citing works
Self-citationBudge, H., Dandrea, J., Mostyn, A., Evens, Y., Watkins, R., SULLIVAN, C., INGLETON, P. M., Stephenson, T. J., & Symonds, M. E. (2003) · Pediatric Research · doi:10.1203/01.pdr.0000047653.73271.c4 · Cited by 42 · see citing works
Myoblast models of skeletal muscle hypertrophy and atrophy
Sharples, A. P., & Stewart, C. E. (2011) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e3283457ade · Cited by 41 · see citing works
Self-citationSca-1-Expressing Nonmyogenic Cells Contribute to Fibrosis in Aged Skeletal Muscle
Hidestrand, M., Richards-Malcolm, S. A., Gurley, C. M., Nolen, G. T., Grimes, B. A., Waterstrat, A., Zant, G. E. V., & Peterson, C. A. (2008) · The Journals of Gerontology Series A · doi:10.1093/gerona/63.6.566 · Cited by 41 · see citing works
Olsson, A. H., Rönn, T., Ladenvall, C., Parikh, H. M., Isomaa, B., Groop, L., & Ling, C. (2011) · European Journal of Endocrinology · doi:10.1530/eje-10-0995 · Cited by 38 · see citing works
Zwetsloot, K. A., Childs, T. E., Gilpin, L. T., & Booth, F. W. (2013) · Cell Proliferation · doi:10.1111/cpr.12007 · Cited by 35 · see citing works
da Silva Aragão, R., Guzmán-Quevedo, O., Pérez-García, G., Manhães-de-Castro, R., & Bolaños-Jiménez, F. (2014) · British Journal Of Nutrition · doi:10.1017/s0007114514000865 · Cited by 35 · see citing works
THE EFFECT OF MATERNAL MALNUTRITION ON THE PROGENY IN THE RAT
McLeod, K. I., Goldrick, R. B., & Hm, W. (1972) · Immunology and Cell Biology · doi:10.1038/icb.1972.37 · Cited by 35 · see citing works
Claycombe, K., Roemmich, J. N., Johnson, L. K., Vomhof‐DeKrey, E. E., & Johnson, W. T. (2014) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2014.10.003 · Cited by 33 · see citing works
Maples, J. M., Brault, J. J., Shewchuk, B. M., Witczak, C. A., Zou, K., Rowland, N. S., Hubal, M. J., Weber, T. M., & Houmard, J. A. (2015) · Physiological Genomics · doi:10.1152/physiolgenomics.00065.2014 · Cited by 33 · see citing works
In epidemiological studies: Findings from the hertfordshire sarcopenia study (HSS)
Patel, H. P., Syddall, H. E., Martin, H., Cooper, C. C., Stewart, C. E., & Sayer, A. A. (2011) · The journal of nutrition health & aging · doi:10.1007/s12603-011-0006-8 · Cited by 30 · see citing works
Self-citationBlesson, C. S., Sathishkumar, K., Chinnathambi, V., & Yallampalli, C. (2014) · Endocrinology · doi:10.1210/en.2014-1094 · Cited by 30 · see citing works
Patel, H. P., Syddall, H. E., Martin, H., Cooper, C. C., Stewart, C. E., & Sayer, A. A. (2010) · The journal of nutrition health & aging · doi:10.1007/s12603-010-0117-7 · Cited by 29 · see citing works
Self-citationEpigenetic Change as the Major Mediator of Fetal Programming in Humans: Are We There Yet?
Saffery, R. (2014) · Annals of Nutrition and Metabolism · doi:10.1159/000365020 · Cited by 28 · see citing works
Liu, X., Pan, S., Li, X., et al. (2014) · European Journal of Nutrition · doi:10.1007/s00394-014-0773-1 · Cited by 26 · see citing works
de Maredsous, C. D., Oozeer, R., Barbillon, P., Mary‐Huard, T., Delteil, C., Blachier, F., Tomé, D., van der Beek, E. M., & Davila, A. (2015) · Journal of Nutrition · doi:10.3945/jn.115.216465 · Cited by 26 · see citing works
Green, C., Bunprajun, T., Pedersen, B. K., & Scheele, C. C. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2013.251421 · Cited by 24 · see citing works
de Rooij, S. R., & Roseboom, T. J. (2013) · BMJ Open · doi:10.1136/bmjopen-2013-003167 · Cited by 24 · see citing works
Raychaudhuri, N., Thamotharan, S., Srinivasan, M., Mahmood, S., Patel, M. S., & Devaskar, S. U. (2014) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2014.05.011 · Cited by 22 · see citing works
Wang, H., Wilson, G. J., Zhou, D., Lezmi, S., Chen, X., Layman, D. K., & Pan, Y. (2015) · British Journal Of Nutrition · doi:10.1017/s0007114515002172 · Cited by 21 · see citing works
Confortim, H. D., Jerônimo, L. C., Centenaro, L. A., Pinheiro, P. F. F., Brancalhão, R. M. C., Matheus, S. M. M., & Torrejais, M. M. (2015) · Micron · doi:10.1016/j.micron.2014.12.006 · Cited by 20 · see citing works
Fainberg, H. P., Almond, K., Li, D., Rauch, C., Bikker, P., Symonds, M. E., & Mostyn, A. (2014) · BMC Physiology · doi:10.1186/s12899-014-0006-0 · Cited by 16 · see citing works
Kruse, M., Keyhani-Nejad, F., Isken, F., Nitz, B., Kretschmer, A., Reischl, E., Gala, T. D. L. H., Osterhoff, M., Grallert, H., & Pfeiffer, A. (2015) · Diabetes · doi:10.2337/db15-0478 · Cited by 16 · see citing works
Foulstone, E. J., Savage, P. B., Crown, A., et al. (2003) · Hormone and Metabolic Research · doi:10.1055/s-2004-814159 · Cited by 13 · see citing works
Guzmán‐Quevedo, O., Aragão, R. D. S., García, G. P., de Matos, R. J. B., Oliveira, A. D. S. B., Manhães‐de‐Castro, R., & Bolaños, F. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074990 · Cited by 12 · see citing works
Costello, P. M., Hollis, L. J., Cripps, R. L., Bearpark, N., Patel, H. P., Sayer, A. A., Cooper, C. C., Hanson, M. A., Ozanne, S. E., & Green, L. (2013) · Reproductive Sciences · doi:10.1177/1933719113477494 · Cited by 11 · see citing works
Lancioni, H., Lucentini, L., Palomba, A., et al. (2006) · Cell Biology International · doi:10.1016/j.cellbi.2006.10.002 · Cited by 10 · see citing works
Yakubu, D. P., Mostyn, A., Wilson, V. G., Pearce, S., Alves‐Guerra, M., Pecqueur, C., Miroux, B., Budge, H., Stephenson, T. J., & Symonds, M. E. (2007) · Reproduction · doi:10.1530/rep-06-0211 · Cited by 10 · see citing works
Influence of age on accumulation of α-actin in satellite-cell-derived myotubes in vitro
Allen, R. E., McAllister, P. K., Masak, K. C., et al. (1982) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(82)90033-1 · Cited by 10 · see citing works
Brown, L. D., Wesolowski, S. R., O'Meara, M. C., Lavezzi, J. R., & Rozance, P. J. (2014) · Physiological Reports · doi:10.14814/phy2.12045 · Cited by 10 · see citing works
c-Myc inactivation by mutant max alters growth and morphology of NCI-H-630 colon cancer cells
Borrè, A., Cultraro, C. M., & Segal, S. (1996) · Journal of Cellular Physiology · doi:10.1002/(sici)1097-4652(199610)169:1 · Cited by 10 · see citing works
Ontogeny and nutritional programming of mitochondrial proteins in the ovine kidney, liver and lung
Yakubu, D. P., Mostyn, A., Hyatt, M. A., Kurlak, L. O., Budge, H., Stephenson, T. J., & Symonds, M. E. (2007) · Reproduction · doi:10.1530/rep-07-0155 · Cited by 8 · see citing works
Deng, H., Deng, H.-Z., Hong, D., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0100459 · Cited by 7 · see citing works
Remembering those ‘lazy’ days – imprinting memory in our satellite cells
Valencia, A. P., & Spangenburg, E. E. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2013.261578 · Cited by 6 · see citing works
Epigenetic Modulation of Gene Expression by Exercise
Goto, S., Kawakami, K., Naito, H., Katamoto, S., & Radák, Z. (2015) · Healthy ageing and longevity · doi:10.1007/978-3-319-14830-4_5 · Cited by 4 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- NICE (2010) Weight management before, during and after pregnancy In PH27 (TNIfHaCE (NICE), eds). London, UK: The National Institute for Health and Care Excellence (NICE), pp. 1– 57.
- Oxford Dictionary (2015) http://www.oxforddictionaries.com/definition/english/epigenetics
Cited by
Sorted by citations
Transcriptomic profiling of skeletal muscle adaptations to exercise and inactivity
Pillon, N. J., Gabriel, B. M., Dollet, L., Smith, J. A. B., Sardón Puig, L., Botella, J., Bishop, D. J., Krook, A., & Zierath, J. R. (2020) · Nature Communications · doi:10.1038/s41467-019-13869-w · Cited by 457 · 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
Self-citationEgan, B., & Sharples, A. P. (2023) · Physiological Reviews · doi:10.1152/physrev.00054.2021 · Cited by 278 · see citing works
Self-citationRoberts, M. D., McCarthy, J. J., Hornberger, T. A., Phillips, S. M., Mackey, A. L., Nader, G. A., Boppart, M. D., Kavazis, A. N., Reidy, P. T., Ogasawara, R., et al. (2023) · Physiological Reviews · doi:10.1152/physrev.00039.2022 · Cited by 214 · see citing works
Bishop, D. J., Botella, J., Genders, A. J., Lee, M. J.-C., Saner, N. J., Kuang, J., Yan, X., & Granata, C. (2019) · Physiology · doi:10.1152/physiol.00038.2018 · Cited by 180 · see citing works
Physical exercise and epigenetic modifications in skeletal muscle
Widmann, M., Nieß, A. M., & Munz, B. (2019) · Sports Medicine · doi:10.1007/s40279-019-01070-4 · Cited by 165 · see citing works
Turner, D. C., Gorski, P. P., Maasar, M. F., Seaborne, R. A., Baumert, P., Brown, A. D., Kitchen, M. O., Erskine, R. M., Dos-Remedios, I., Voisin, S., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-72730-z · Cited by 139 · see citing works
Self-citationGenetic and epigenetic regulation of skeletal muscle ribosome biogenesis with exercise
Figueiredo, V. C., Wen, Y., Alkner, B., Fernandez‐Gonzalo, R., Norrbom, J., Vechetti, I. J., Valentino, T., Mobley, C. B., Zentner, G. E., Peterson, C. A., et al. (2021) · The Journal of Physiology · doi:10.1113/jp281244 · Cited by 64 · see citing works
Saini, A., Sharples, A. P., Al-Shanti, N., & Stewart, C. E. (2017) · Biogerontology · doi:10.1007/s10522-016-9667-3 · Cited by 53 · see citing works
Muñoz López, M., López-Gil, J. F., Ramírez de la piscina Viúdez, X., Baz-Valle, E., & Tornero Aguilera, J. F. (2026) · Cells · doi:10.3390/cells15111041 · Cited by 1 · see citing works
“Crucially, this hypomethylated signature was preserved even after weeks of total detraining and macroscopic atrophy [119,120].”
- Authors
- Sharples, A. P., Stewart, C. E., & Seaborne, R. A.
- Affiliations
- Liverpool John Moores University (GB)
- Corresponding author
- Sharples, Adam P.
- Venue
- Aging Cell
- Publisher
- Wiley
- Published
- 2016-04-22
- Volume
- 15
- Issue
- 4
- Pages
- 603-616
- ISSN
- 1474-9718 (ISSN-L)
- 1474-9726
- PMC
- PMC4933662
- OpenAlex
- W2342297429
- Cited by
- 180
- References
- 184
- Citations by year
- 2026: 11 · 2025: 12 · 2024: 10 · 2023: 19 · 2022: 16 · 2021: 27 · 2020: 20 · 2019: 30 · 2018: 17 · 2017: 16 · 2016: 2
- FWCI
- 1.96
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Aging Cell (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Liverpool John Moores University (acceptedVersion)
- Keele Research Repository (Keele University) (submittedVersion, cc-by)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
- Keywords
- epigenetics, nutritional programming, low birth weight, metabolic disorders, muscle aging, muscle stem cells, muscle atrophy, healthy aging, epigenetic regulation
- MeSH terms
- Aging, Animals, Humans, Metabolic Diseases, Exercise, Muscle, Skeletal, Epigenesis, Genetic, Stem Cell Niche
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