Pronounced Effects of Acute Endurance Exercise on Gene Expression in Resting and Exercising Human Skeletal Muscle
Open accessAbstract
Regular physical activity positively influences whole body energy metabolism and substrate handling in exercising muscle. While it is recognized that the effects of exercise extend beyond exercising muscle, it is unclear to what extent exercise impacts non-exercising muscles. Here we investigated the effects of an acute endurance exercise bouts on gene expression in exercising and non-exercising human muscle. To that end, 12 male subjects aged 44-56 performed one hour of one-legged cycling at 50% W(max). Muscle biopsies were taken from the exercising and non-exercising leg before and immediately after exercise and analyzed by microarray. One-legged cycling raised plasma lactate, free fatty acids, cortisol, noradrenalin, and adrenalin levels. Surprisingly, acute endurance exercise not only caused pronounced gene expression changes in exercising muscle but also in non-exercising muscle. In the exercising leg the three most highly induced genes were all part of the NR4A family. Remarkably, many genes induced in non-exercising muscle were PPAR targets or related to PPAR signalling, including PDK4, ANGPTL4 and SLC22A5. Pathway analysis confirmed this finding. In conclusion, our data indicate that acute endurance exercise elicits pronounced changes in gene expression in non-exercising muscle, which are likely mediated by changes in circulating factors such as free fatty acids. The study points to a major influence of exercise beyond the contracting muscle.
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?
ANGPTL4 is upregulated by SkM after aerobic or resistance exercise.
“Although it is upregulated by SkM after aerobic or resistance exercise [171,172,196], surprisingly, an even greater degree of ANGPTL4 mRNA expression was found in the portion of SkM that remained inactive during the bout of exercise compared with the active SkM [172,196], representing a mechanism to redistribute FFA delivery from unexercised to exercised SkM.”
From The Role of Exercise in the Interplay between Myokines, Hepatokines, Osteokines, Adipokines, and Modulation of Inflammation for Energy Substrate Redistribution and Fat Mass Loss: A Review (2020) · cites this paper as [196]
The Discussion (page not provided) reports that ANGPTL4 was induced in human skeletal muscle after one-legged endurance cycling, supporting the aerobic-exercise part of the claim. The paper does not report ANGPTL4 upregulation after resistance exercise. (LLM, conf=0.88)
Experimental — accuracy not yet measuredAn even greater degree of ANGPTL4 mRNA expression was found in the portion of SkM that remained inactive during the bout of exercise compared with the active SkM.
“Although it is upregulated by SkM after aerobic or resistance exercise [171,172,196], surprisingly, an even greater degree of ANGPTL4 mRNA expression was found in the portion of SkM that remained inactive during the bout of exercise compared with the active SkM [172,196], representing a mechanism to redistribute FFA delivery from unexercised to exercised SkM.”
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
Cytoscape: A software Environment for integrated models of biomolecular interaction networks
Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., & Ideker, T. (2003) · Genome Research · doi:10.1101/gr.1239303 · Cited by 51,888 · see citing works
Bolstad, B. M., Irizarry, R. A., Åstrand, M., & Speed, T. P. (2003) · Bioinformatics · doi:10.1093/bioinformatics/19.2.185 · Cited by 8,185 · see citing works
Bindea, G., Mlecnik, B., Hackl, H., Charoentong, P., Tosolini, M., Kirilovsky, A., Fridman, W.-H., Pagès, F., Trajanoski, Z., & Galon, J. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp101 · Cited by 6,280 · see citing works
Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data
Dai, M. (2005) · Nucleic Acids Research · doi:10.1093/nar/gni179 · Cited by 1,797 · see citing works
Peroxisome proliferator-activated receptor a target genes
Mandard, S., M�ller, M., & Kersten, S. (2004) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-003-3216-3 · Cited by 1,222 · see citing works
Self-citationKrey, G. D., Braissant, O., L’Horset, F., Kalkhoven, E., Perroud, M., Parker, M. G., & Wahli, W. (1997) · Molecular Endocrinology · doi:10.1210/mend.11.6.0007 · Cited by 1,221 · see citing works
Peroxisome Proliferator-Activated Receptor Alpha Target Genes
Rakhshandehroo, M., Knoch, B., Müller, M., & Kersten, S. (2010) · PPAR Research · doi:10.1155/2010/612089 · Cited by 1,020 · see citing works
Self-citationTranscriptional regulation of gene expression in human skeletal muscle during recovery from exercise
Pilegaard, H., Ordway, G. A., Saltin, B., & Neufer, P. D. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.279.4.e806 · Cited by 563 · see citing works
Contralateral effects of unilateral strength training: evidence and possible mechanisms
Carroll, T. J., Herbert, R., Munn, J., Lee, M., & Gandevia, S. C. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00531.2006 · Cited by 504 · see citing works
Changes in human muscle protein synthesis after resistance exercise
Chesley, A., MacDougall, J. D., Tarnopolsky, M. A., Atkinson, S. A., & Smith, K. (1992) · Journal of Applied Physiology · doi:10.1152/jappl.1992.73.4.1383 · Cited by 436 · see citing works
Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise
Mahoney, D. J., Parise, G., Melov, S., Safdar, A., & Tarnopolsky, M. A. (2005) · The FASEB Journal · doi:10.1096/fj.04-3149fje · Cited by 418 · see citing works
Physical Activity and Exercise in the Regulation of Human Adipose Tissue Physiology
Thompson, D., Karpe, F., Lafontan, M., & Frayn, K. N. (2012) · Physiological Reviews · doi:10.1152/physrev.00012.2011 · Cited by 403 · see citing works
Comparative Analysis of Gene Regulation by the Transcription Factor PPARα between Mouse and Human
Rakhshandehroo, M., Hooiveld, G. J. E. J., Müller, M. M., & Kersten, S. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006796 · Cited by 307 · see citing works
Self-citationSullivan, S. A., Kirk, E. P., Mittendorfer, B., Patterson, B. W., & Klein, S. (2011) · Hepatology · doi:10.1002/hep.25548 · Cited by 303 · see citing works
Yang, Y., Creer, A., Jemiolo, B., & Trappe, S. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01185.2004 · Cited by 290 · see citing works
Sartor, M. A., Tomlinson, C. R., Wesselkamper, S. C., Sivaganesan, S., Leikauf, G. D., & Medvedovic, M. (2006) · BMC Bioinformatics · doi:10.1186/1471-2105-7-538 · Cited by 263 · see citing works
Slentz, C. A., Bateman, L. A., Willis, L. H., Shields, A. T., Tanner, C. J., Piner, L. W., Hawk, V. H., Muehlbauer, M. J., Samsa, G. P., Nelson, R. C., et al. (2011) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00291.2011 · Cited by 235 · see citing works
Real-time RT-PCR analysis of housekeeping genes in human skeletal muscle following acute exercise
Mahoney, D. J., Carey, K. A., Fu, M., Snow, R. J., Cameron‐Smith, D., Parise, G., & Tarnopolsky, M. A. (2004) · Physiological Genomics · doi:10.1152/physiolgenomics.00067.2004 · Cited by 211 · see citing works
Human VEGF gene expression in skeletal muscle: effect of acute normoxic and hypoxic exercise
Richardson, R. S., Wagner, H. E., Mudaliar, S. R. D., Henry, R. R., Noyszewski, E. A., & Wagner, P. D. (1999) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1999.277.6.h2247 · Cited by 202 · see citing works
Bartlett, J. D., Joo, C.-H., Jeong, T.-S., Louhelainen, J., Cochran, A. J. R., Gibala, M. J., Gregson, W. A., Close, G. L., Drust, B., & Morton, J. P. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01040.2011 · Cited by 200 · see citing works
Keller, C., Steensberg, A., Hansen, A. K., Fischer, C. P., Plomgaard, P., & Pedersen, B. K. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00590.2005 · Cited by 179 · see citing works
Lundby, C., Nordsborg, N. B., Kusuhara, K., Kristensen, K. M., Neufer, P. D., & Pilegaard, H. (2005) · European Journal of Applied Physiology · doi:10.1007/s00421-005-0022-7 · Cited by 173 · see citing works
Nur77 Coordinately Regulates Expression of Genes Linked to Glucose Metabolism in Skeletal Muscle
Chao, L. C., Zhang, Z., Pei, L., Saito, T., Tontonoz, P., & Pilch, P. F. (2007) · Molecular Endocrinology · doi:10.1210/me.2007-0169 · Cited by 173 · see citing works
Fasted‐state skeletal muscle protein synthesis after resistance exercise is altered with training
Kim, P. L., Staron, R. S., & Phillips, S. M. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.093708 · Cited by 171 · see citing works
MADMAX – Management and analysis database for multiple ~omics experiments
Lin, K., Kools, H. J., de Groot, P. J., Gavai, A., Basnet, R. K., Cheng, F., Wu, J., Wang, X., Lommen, A., Hooiveld, G. J. E. J., et al. (2011) · Berichte aus der medizinischen Informatik und Bioinformatik/Journal of integrative bioinformatics · doi:10.1515/jib-2011-160 · Cited by 170 · see citing works
Self-citationNur77 Regulates Lipolysis in Skeletal Muscle Cells
Maxwell, M., Cleasby, M. E., Harding, A. S., Stark, A., Cooney, G. J., & Muscat, G. E. O. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m409580200 · Cited by 158 · see citing works
Pro‐ and anti‐angiogenic factors in human skeletal muscle in response to acute exercise and training
Høier, B., Nordsborg, N. B., Andersen, S., Jensen, L., Nybo, L., Bangsbo, J., & Hellsten, Y. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.216135 · Cited by 158 · see citing works
Pearen, M. A., Myers, S., Raichur, S., Ryall, J. G., Lynch, G. S., & Muscat, G. E. O. (2008) · Endocrinology · doi:10.1210/en.2007-1202 · Cited by 156 · see citing works
Sanderson, L. M., Degenhardt, T., Koppen, A., Kalkhoven, E., Desvergne, B., Müller, M. M., & Kersten, S. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.00370-09 · Cited by 145 · see citing works
Self-citationInterleukin-6 production by contracting human skeletal muscle: autocrine regulation by IL-6
Keller, P., Keller, C., Carey, A. L., Jauffred, S., Fischer, C. P., Steensberg, A., & Pedersen, B. K. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2003.09.048 · Cited by 135 · see citing works
Resistance exercise-induced changes of inflammatory gene expression within human skeletal muscle
Buford, T. W., Cooke, M. B., & Willoughby, D. S. (2009) · European Journal of Applied Physiology · doi:10.1007/s00421-009-1145-z · Cited by 111 · see citing works
Strength training the free limb attenuates strength loss during unilateral immobilization
Farthing, J. P., Krentz, J. R., & Magnus, C. R. A. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91331.2008 · Cited by 110 · see citing works
Endurance training modulates the muscular transcriptome response to acute exercise
Schmutz, S., Däpp, C., Wittwer, M., Vogt, M., Hoppeler, H. H., & Flück, M. (2005) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-005-1497-0 · Cited by 99 · see citing works
Magnus, C. R. A., Barss, T. S., Lanovaz, J. L., & Farthing, J. P. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00597.2010 · Cited by 90 · see citing works
Valkeinen, H., Aaltonen, S., & Kujala, U. M. (2010) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2010.01133.x · Cited by 87 · see citing works
Calcineurin Regulates Skeletal Muscle Metabolism via Coordinated Changes in Gene Expression
Long, Y. C., Glund, S., García-Rovés, P. M., & Zierath, J. R. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m609208200 · Cited by 86 · see citing works
Cohen, T. J., Barrientos, T., Hartman, Z. C., Garvey, S. M., Cox, G. A., & Yao, T. (2008) · The FASEB Journal · doi:10.1096/fj.08-115931 · Cited by 86 · see citing works
Myers, S., Eriksson, N. A., Burow, R., Wang, S.-C., & Muscat, G. E. O. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.05.006 · Cited by 82 · see citing works
MADMAX - Management and analysis database for multiple ~omics experiments
Lin, K., Kools, H. J., de Groot, P. J., et al. (2011) · PubMed · doi:10.2390/biecoll-jib-2011-160 · Cited by 77 · see citing works
Farid, R., Azad, F. J., Atri, A. E., Rahimi, M. B., Khaledan, A. A., Talaei‐Khoei, M., Javad, G., & Ghasemi, R. (2005) · PubMed · Cited by 74 · see citing works
Mitochondrial gene expression in elite cyclists: effects of high-intensity interval exercise
Psilander, N., Wang, L., Westergren, J., Tonkonogi, M., & Sahlin, K. (2010) · European Journal of Applied Physiology · doi:10.1007/s00421-010-1544-1 · Cited by 64 · see citing works
Intracellular Ca2+ Signaling in Skeletal Muscle
Chin, E. R. (2010) · Exercise and Sport Sciences Reviews · doi:10.1097/jes.0b013e3181d495d2 · Cited by 50 · see citing works
Kawasaki, E., Hokari, F., Sasaki, M., Sakai, A., Koshinaka, K., & Kawanaka, K. (2009) · Journal of applied physiology · doi:10.1152/japplphysiol.90923.2008 · Cited by 41 · see citing works
Psilander, N., Wang, L., Westergren, J., Tonkonogi, M., & Sahlin, K. (2010) · European Journal of Applied Physiology · doi:10.1007/s00421-010-1581-9 · Cited by 37 · see citing works
Kanzleiter, T., Wilks, D. L., Preston, E., Ye, J., Frangioudakis, G., & Cooney, G. J. (2009) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2009.05.002 · Cited by 33 · see citing works
Jensen, J. H., Conley, L. N., Hedegaard, J., Nielsen, M., Young, J. F., Oksbjerg, N., Hornshøj, H., Bendixen, C., & Thomsen, B. (2012) · Experimental Physiology · doi:10.1113/expphysiol.2011.063727 · Cited by 31 · see citing works
Friedmann‐Bette, B., Schwartz, F. R., Eckhardt, H., Billeter-Clark, R., Bonaterra, G. A., & Kinscherf, R. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00959.2011 · Cited by 31 · see citing works
The effect of an acute bout of exercise on selected pulmonary function measurements
Buono, M. J., Constable, S. H., Morton, A. R., ROTKIS, T. C., Stanforth, P. R., & Wilmore, J. H. (1981) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-198105000-00003 · Cited by 21 · see citing works
Wall Suction Applied to Needle Muscle Biopsy—A Novel Technique for Increasing Sample Size
Meléndez, M. M., Vosswinkel, J. A., Shapiro, M. J., Gelato, M. C., Mynarcik, D. C., Gavi, S., Xu, X., & McNurlan, M. A. (2007) · Journal of Surgical Research · doi:10.1016/j.jss.2007.03.043 · Cited by 20 · see citing works
Kawasaki, E., Hokari, F., Sasaki, M., Sakai, A., Koshinaka, K., & Kawanaka, K. (2010) · The Journal of Physiological Sciences · doi:10.1007/s12576-010-0114-y · Cited by 17 · see citing works
Zanchi, N. E., Lira, F. S., Seelaender, M. C. L., & Lancha, A. H. (2010) · Cell Biochemistry and Function · doi:10.1002/cbf.1665 · Cited by 16 · see citing works
Brass, E. P., Peters, M. A., Hinchcliff, K. W., He, Y. D., & Ulrich, R. G. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91347.2008 · Cited by 14 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Role of Skeletal Muscle in Insulin Resistance and Glucose Uptake
Merz, K. E., & Thurmond, D. C. (2020) · Comprehensive Physiology · doi:10.1002/cphy.c190029 · Cited by 494 · see citing works
AMPK in skeletal muscle function and metabolism
Kjøbsted, R., Hingst, J. R., Fentz, J., Foretz, M., Sanz, M.-N., Pehmøller, C. K., Shum, M., Marette, A., Mounier, R., Treebak, J. T., et al. (2017) · The FASEB Journal · doi:10.1096/fj.201700442r · Cited by 496 · see citing works
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
The pivotal role of pyruvate dehydrogenase kinases in metabolic flexibility
Zhang, S., Hulver, M. W., McMillan, R. P., Cline, M. A., & Gilbert, E. R. (2014) · Nutrition & Metabolism · doi:10.1186/1743-7075-11-10 · Cited by 450 · see citing works
Adipo-myokines: two sides of the same coin–mediators of inflammation and mediators of exercise
Raschke, S., & Eckel, J. (2013) · Mediators of Inflammation · doi:10.1155/2013/320724 · Cited by 296 · see citing works
Role of Skeletal Muscle in Insulin Resistance and Glucose Uptake
Merz, K. E., & Thurmond, D. C. (2020) · Comprehensive physiology · doi:10.1002/j.2040-4603.2020.tb00136.x · Cited by 283 · see citing works
Gonzalez-Gil, A. M., & Elizondo-Montemayor, L. (2020) · Nutrients · doi:10.3390/nu12061899 · Cited by 278 · see citing works
Egan, B., & Sharples, A. P. (2023) · Physiological Reviews · doi:10.1152/physrev.00054.2021 · Cited by 278 · see citing works
Raschke, S., Eckardt, K., Bjørklund Holven, K., Jensen, J., & Eckel, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062008 · Cited by 199 · see citing works
Identification of human exercise-induced myokines using secretome analysis
Catoire, M., Mensink, M., Kalkhoven, E., Schrauwen, P., & Kersten, S. (2014) · Physiological Genomics · doi:10.1152/physiolgenomics.00174.2013 · Cited by 179 · see citing works
Klymiuk, N., Blutke, A., Graf, A., Krause, S., Burkhardt, K., Wuensch, A., Krebs, S., Keßler, B., Zakhartchenko, V., Kurome, M., et al. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt287 · Cited by 177 · see citing works
Fatty acid-inducible ANGPTL4 governs lipid metabolic response to exercise
Catoire, M., Alex, S., Paraskevopulos, N., Mattijssen, F., Evers-van Gogh, I., Schaart, G., Jeppesen, J., Kneppers, A., Mensink, M., Voshol, P. J., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400889111 · Cited by 150 · see citing works
Self-citationTranscriptomic analyses reveal rhythmic and CLOCK-driven pathways in human skeletal muscle
Perrin, L., Loizides-Mangold, U., Chanon, S., Gobet, C., Hulo, N., Isenegger, L., Weger, B. D., Migliavacca, E., Charpagne, A., Betts, J. A., et al. (2018) · eLife · doi:10.7554/elife.34114 · Cited by 139 · see citing works
The search for exercise factors in humans
Catoire, M., & Kersten, S. (2015) · The FASEB Journal · doi:10.1096/fj.14-263699 · Cited by 137 · see citing works
Self-citationShafi, O. (2016) · BMC Neurology · doi:10.1186/s12883-016-0765-2 · Cited by 125 · see citing works
ROLE of exercise in maintaining the integrity of the neuromuscular junction
Nishimune, H., Stanford, J. A., & Mori, Y. (2013) · Muscle & Nerve · doi:10.1002/mus.24095 · Cited by 125 · see citing works
Ni, A., & Ernst, C. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.826193 · Cited by 115 · see citing works
Exercise-induced Nrf2-signaling is impaired in aging
Done, A. J., Gage, M. J., Nieto, N. C., & Traustadóttir, T. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.04.024 · Cited by 99 · see citing works
Exercise conditioning in old mice improves skeletal muscle regeneration
Joanisse, S., Nederveen, J. P., Baker, J. M., Snijders, T., Iacono, C., & Parise, G. (2016) · The FASEB Journal · doi:10.1096/fj.201600143rr · Cited by 83 · see citing works
Викторович, П. Д., Makhnovskii, P. A., Shagimardanova, E. I., Gazizova, G. R., Lysenko, E. A., Gusev, O., & Виноградова, О. Л. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00449.2018 · Cited by 80 · see citing works
Bouchard‐Mercier, A., Paradis, A.-M., Rudkowska, I., Lemieux, S., Couture, P., & Vohl, M. (2013) · Nutrition Journal · doi:10.1186/1475-2891-12-24 · Cited by 76 · see citing works
Shefer, G., Rauner, G., Stuelsatz, P., Benayahu, D., & Yablonka‐Reuveni, Z. (2013) · The FEBS Journal · doi:10.1111/febs.12228 · Cited by 72 · see citing works
Simplified data access on human skeletal muscle transcriptome responses to differentiated exercise
Vissing, K., & Schjerling, P. (2014) · Scientific Data · doi:10.1038/sdata.2014.41 · Cited by 70 · see citing works
Factors mediating exercise‐induced organ crosstalk
Sabaratnam, R., Wojtaszewski, J. F. P., & Højlund, K. (2022) · Acta Physiologica · doi:10.1111/apha.13766 · Cited by 70 · see citing works
Renzo, L. D., Marsella, L., Carraro, A., Valente, R., Gualtieri, P., Gratteri, S., Tomasi, D., Gaiotti, F., & LORENZO, A. D. (2015) · Mediators of Inflammation · doi:10.1155/2015/317348 · Cited by 64 · see citing works
Pearen, M. A., Goode, J. M., Fitzsimmons, R. L., Eriksson, N. A., Thomas, G. P., Cowin, G., Wang, S.-C., Tuong, Z. K., & Muscat, G. E. O. (2013) · Molecular Endocrinology · doi:10.1210/me.2013-1205 · Cited by 63 · see citing works
Gene and MicroRNA Expression Responses to Exercise; Relationship with Insulin Sensitivity
McLean, C. G., Mielke, C. J., Cordova, J. M., Langlais, P. R., Bowen, B. P., Miranda, D. N., Coletta, D. K., & Mandarino, L. J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0127089 · Cited by 60 · see citing works
Role of exercise-induced hepatokines in metabolic disorders
Ennequin, G., Sirvent, P., & Whitham, M. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00433.2018 · Cited by 54 · see citing works
Gogh, I. J. A. E., Alex, S., Stienstra, R., Brenkman, A. B., Kersten, S., & Kalkhoven, E. (2015) · Scientific Reports · doi:10.1038/srep10944 · Cited by 54 · see citing works
Self-citationExercise and the Skeletal Muscle EpigenomePreprint
McGee, S. L., & Walder, K. R. (2017) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a029876 · Cited by 54 · see citing works
NR4A orphan nuclear receptors in glucose homeostasis: A minireview
Close, A. F., Rouillard, C., & Buteau, J. (2013) · Diabetes & Metabolism · doi:10.1016/j.diabet.2013.07.005 · Cited by 52 · see citing works
NURR1 activation in skeletal muscle controls systemic energy homeostasis
Amoasii, L., Sanchez‐Ortiz, E., Fujikawa, T., Elmquist, J. K., Bassel‐Duby, R., & Olson, E. N. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1902490116 · Cited by 50 · see citing works
SF-1 expression in the hypothalamus is required for beneficial metabolic effects of exercise
Fujikawa, T., Castorena, C. M., Pearson, M. J., Kusminski, C. M., Ahmed, N. I., Battiprolu, P. K., Kim, K. W., Lee, S., Hill, J. A., Scherer, P. E., et al. (2016) · eLife · doi:10.7554/elife.18206 · Cited by 51 · see citing works
Maasar, M. F., Turner, D. C., Gorski, P. P., Seaborne, R. A. E., Strauss, J. A., Shepherd, S. O., Cocks, M. S., Pillon, N. J., Zierath, J. R., Hulton, A. T., et al. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.619447 · Cited by 49 · see citing works
Physical activity and its mechanistic effects on prostate cancer
Wekesa, A., Harrison, M., & Watson, R. W. G. (2015) · Prostate Cancer and Prostatic Diseases · doi:10.1038/pcan.2015.9 · Cited by 47 · see citing works
Intensity-dependent gene expression after aerobic exercise in endurance-trained skeletal muscle
Викторович, П. Д., Makhnovskii, P. A., Kurochkina, N. S., Lysenko, E. A., Vepkhvadze, T. F., & Виноградова, О. Л. (2018) · Biology of Sport · doi:10.5114/biolsport.2018.77828 · Cited by 45 · see citing works
Amoasii, L., Holland, W. L., Sanchez‐Ortiz, E., Baskin, K. K., Pearson, M. J., Burgess, S. C., Nelson, B. R., Bassel‐Duby, R., & Olson, E. N. (2016) · Genes & Development · doi:10.1101/gad.273128.115 · Cited by 45 · see citing works
Muscle Contraction Induces Acute Hydroxymethylation of the Exercise-Responsive Gene Nr4a3
Pattamaprapanont, P., Garde, C., Fabre, O., & Barrès, R. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00165 · Cited by 40 · see citing works
Innate immune receptors in skeletal muscle metabolism
Pillon, N. J., & Krook, A. (2017) · Experimental Cell Research · doi:10.1016/j.yexcr.2017.02.035 · Cited by 43 · see citing works
Aoi, W., Hirano, N., Lassiter, D. G., Björnholm, M., Chibalin, A., Sakuma, K., Tanimura, Y., Mizushima, K., Takagi, T., Naito, Y., et al. (2019) · The FASEB Journal · doi:10.1096/fj.201900453r · Cited by 43 · see citing works
Lagerwaard, B., Keijer, J., McCully, K. K., de Boer, V. C. J., & Nieuwenhuizen, A. G. (2019) · European Journal of Applied Physiology · doi:10.1007/s00421-019-04169-8 · Cited by 40 · see citing works
Hart, C. R., Ryan, Z. C., Pfaffenbach, K. T., Dasari, S., Parvizi, M., Lalia, A. Z., & Lanza, I. R. (2019) · Aging · doi:10.18632/aging.102273 · Cited by 39 · see citing works
Exercise-induced mitochondrial dysfunction: a myth or reality?
Ostojić, S. M. (2016) · Clinical Science · doi:10.1042/cs20160200 · Cited by 37 · see citing works
Vendelbo, M. H., Møller, A. B., Treebak, J. T., Gormsen, L. C., Goodyear, L. J., Wojtaszewski, J. F. P., Jørgensen, J. O. L., Møller, N., & Jessen, N. (2014) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00044.2014 · Cited by 34 · see citing works
Little, H. C., Tan, S. Y., Cali, F. M., Rodriguez, S., Lei, X., Wolfe, A., Hug, C., & Wong, G. W. (2018) · Molecular & Cellular Proteomics · doi:10.1074/mcp.ra118.000794 · Cited by 33 · see citing works
Norepinephrine Stimulates Mobilization of Endothelial Progenitor Cells after Limb Ischemia
Jiang, Q., Ding, S., Wu, J., Liu, X., & Wu, Z. (2014) · PLoS ONE · doi:10.1371/journal.pone.0101774 · Cited by 32 · see citing works
The orphan nuclear receptor Nor1/Nr4a3 is a negative regulator of β-cell mass
Close, A.-F., Dadheech, N., Villela, B. S., Rouillard, C., & Buteau, J. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.005135 · Cited by 33 · see citing works
Aerobic exercise training partially reverses the impairment of Nrf2 activation in older humans
Ostrom, E. L., & Traustadóttir, T. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.08.016 · Cited by 33 · see citing works
Popov, D. V., Lysenko, E. A., Bokov, R. O., Volodina, M. A., Kurochkina, N. S., Makhnovskii, P. A., Vyssokikh, M. Y., & Виноградова, О. Л. (2018) · Physiological Reports · doi:10.14814/phy2.13868 · Cited by 30 · see citing works
Fan, Z., Ardicoglu, R., Batavia, A. A., Rust, R., von Ziegler, L., Waag, R., Zhang, J., Desgeorges, T., Sturman, O., Dang, H., et al. (2023) · Angiogenesis · doi:10.1007/s10456-023-09870-z · Cited by 33 · see citing works
Hargreaves, M. (2015) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2015.07.006 · Cited by 32 · see citing works
Nur77 deletion impairs muscle growth during developmental myogenesis and muscle regeneration in mice
Cortez-Toledo, O., Schnair, C., Sangngern, P., METZGER, D., & Chao, L. C. (2017) · PLoS ONE · doi:10.1371/journal.pone.0171268 · Cited by 32 · see citing works
Macrophages on the run: Exercise balances macrophage polarization for improved health
Voskoboynik, Y., McCulloch, A. D., & Sahoo, D. (2024) · Molecular Metabolism · doi:10.1016/j.molmet.2024.102058 · Cited by 31 · see citing works
Gjyshi, A., Dash, S., Cen, L., Cheng, C., Zhang, C. H., Yoder, S., Teer, J. K., Armaiz-Peña, G. N., & Monteiro, Á. N. A. (2018) · Scientific Reports · doi:10.1038/s41598-018-26670-4 · Cited by 30 · see citing works
Makhnovskii, P., Bokov, R. O., Kolpakov, F., & Popov, D. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22031208 · Cited by 27 · see citing works
Transcriptional memory in skeletal muscle. Don't forget (to) exercise
Beiter, T., Niess, A. M., & Moser, D. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.29535 · Cited by 29 · see citing works
Pérez‐Schindler, J., & Philp, A. (2015) · Clinical Science · doi:10.1042/cs20150246 · Cited by 28 · see citing works
Role of Angptl4/Fiaf in exercise-induced skeletal muscle AMPK activation
Chang, H., Kwon, O., Shin, M.-S., Kang, G. M., Leem, Y. H., Lee, C. H., Kim, S. J., Roh, E., Kim, H.-K., Youn, B., et al. (2018) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00984.2016 · Cited by 27 · see citing works
Yang, H. J., Xiao, L., & Xu, D. (2020) · Cardiovascular Drugs and Therapy · doi:10.1007/s10557-020-07001-0 · Cited by 26 · see citing works
Stirm, M., Fonteyne, L. M., Shashikadze, B., Stöckl, J. B., Kurome, M., Keßler, B., Zakhartchenko, V., Kemter, E., Blum, H., Arnold, G. J., et al. (2022) · Neuromuscular Disorders · doi:10.1016/j.nmd.2022.04.005 · Cited by 25 · see citing works
Na, C.-S., Yoon, S. Y., Kim, J. B., Na, D. S., Dong, M., Lee, M., & Hong, C. Y. (2013) · The American Journal of Chinese Medicine · doi:10.1142/s0192415x13500638 · Cited by 25 · see citing works
Chen, L., Bai, J., & Li, Y. (2020) · Molecular Medicine Reports · doi:10.3892/mmr.2020.11164 · Cited by 24 · see citing works
Alves, R. D. A. M., Dane, A. D., Harms, A. C., Strassburg, K., Seifar, R. M., Verdijk, L. B., Kersten, S., Berger, R., Hankemeier, T., & Vreeken, R. J. (2014) · Metabolomics · doi:10.1007/s11306-014-0701-7 · Cited by 23 · see citing works
Self-citationGórecka, M., Krzeminski, K., Buraczewska, M., Kozacz, A., Dąbrowski, J., & Ziemba, A. W. (2019) · European Journal of Applied Physiology · doi:10.1007/s00421-019-04256-w · Cited by 21 · see citing works
Exercise-induced gene expression changes in skeletal muscle of old mice
Endo, Y., Zhang, Y., Olumi, S., Karvar, M., Argawal, S., Neppl, R. L., & Sinha, I. (2021) · Genomics · doi:10.1016/j.ygeno.2021.06.035 · Cited by 20 · see citing works
Regulation of PPARGC1A gene expression in trained and untrained human skeletal muscle
Викторович, П. Д., Lysenko, E. A., Makhnovskii, P. A., Kurochkina, N. S., & Виноградова, О. Л. (2017) · Physiological Reports · doi:10.14814/phy2.13543 · Cited by 20 · see citing works
Akberdin, I. R., Kiselev, I. N., Pintus, S. S., Sharipov, R., Vertyshev, A. Y., Виноградова, О. Л., Викторович, П. Д., & Kolpakov, F. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910353 · Cited by 19 · see citing works
Diverio, S., Guelfi, G., Barbato, O., Mari, W. D., Egidi, M. G., & Santoro, M. M. (2014) · animal · doi:10.1017/s1751731114002304 · Cited by 16 · see citing works
Preliminary evidence that age and sex affect exercise-induced hTERT expression
Cluckey, T. G., Nieto, N. C., Rodoni, B. M., & Traustadóttir, T. (2017) · Experimental Gerontology · doi:10.1016/j.exger.2017.06.003 · Cited by 16 · see citing works
Transcriptomic Responses of Skeletal Muscle to Acute Exercise in Diabetic Goto-Kakizaki Rats
Fu, S., Meng, Y., Zhang, W., Wang, J., He, Y., Huang, L., Chen, H., Kuang, J., & Du, H. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00872 · Cited by 15 · see citing works
Han, S., Wu, Q., Wang, M., Yang, M., Sun, C., Liang, J., Guo, X., Zhang, Z., Xu, J., Qiu, X., et al. (2023) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjad016 · Cited by 14 · see citing works
Effects of extracellular orotic acid on acute contraction-induced adaptation patterns in C2C12 cells
Beiter, T., Hudemann, J., Burgstahler, C., Niess, A. M., & Munz, B. (2018) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-018-3330-z · Cited by 14 · see citing works
Uninterrupted Sedentary Behavior Downregulates BRCA1 Gene Expression
Pettapiece-Phillips, R., Kotlyar, M., Chehade, R., Salmena, L., Narod, S. A., Akbari, M. R., Jurišica, I., & Kotsopoulos, J. (2015) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-15-0291 · Cited by 14 · see citing works
Sabaratnam, R., Pedersen, A. J. T., Eskildsen, T., Kristensen, J. M., Wojtaszewski, J., & Højlund, K. (2019) · Journal of Clinical Endocrinology and Metabolism · doi:10.1210/jc.2018-02679 · Cited by 13 · see citing works
Beiter, T., Zügel, M., Hudemann, J., Schild, M., Fragasso, A., Burgstahler, C., Krüger, K., Mooren, F. C., Steinacker, J. M., & Niess, A. M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25052881 · Cited by 14 · see citing works
Effects of Training Status and Exercise Mode on Global Gene Expression in Skeletal Muscle
Bizjak, D. A., Zügel, M., Treff, G., Winkert, K., Jerg, A., Hudemann, J., Mooren, F. C., Krüger, K., Niess, A. M., & Steinacker, J. M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222212578 · Cited by 14 · see citing works
Reibe, S., Hjorth, M., Febbraio, M., & Whitham, M. (2018) · Physiological Genomics · doi:10.1152/physiolgenomics.00127.2017 · Cited by 11 · see citing works
Modulation of PGC-1α activity as a treatment for metabolic and muscle-related diseases
Svensson, K., & Handschin, C. (2014) · Drug Discovery Today · doi:10.1016/j.drudis.2014.02.013 · Cited by 13 · see citing works
Nagase, H., Yao, S., & Ikeda, S. (2017) · PLoS ONE · doi:10.1371/journal.pone.0182456 · Cited by 10 · see citing works
Akberdin, I. R., Kiselev, I. N., Pintus, S. S., Sharipov, R. N., Vertyshev, A. Y., Vinogradova, O. L., Popov, D. V., & Kolpakov, F. A. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.31.446385 · Cited by 9 · see citing works
Plasma from exercised rats administered to sedentary rats induces systemic and tissue inflammation
Γουτιάνος, Γ., Veskoukis, A. S., Tzioura, A., Paschalis, V., Margaritelis, N. V., Δίπλα, Κ., Zafeiridis, A., Vrabas, I. S., Nikolaidis, M. G., & Kyparos, A. (2016) · Physiological Reports · doi:10.14814/phy2.13087 · Cited by 8 · see citing works
Control of Muscle Metabolism by the Mediator ComplexPreprint
Amoasii, L., Olson, E. N., & Bassel‐Duby, R. (2017) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a029843 · Cited by 8 · see citing works
Akberdin, I. R., Vertyshev, A. Y., Pintus, S. S., Викторович, П. Д., & Kolpakov, F. (2020) · Mathematical Biology and Bioinformatics · doi:10.17537/2020.15.20 · Cited by 7 · see citing works
Marston, K. J., de Frutos‐Lucas, J., Porter, T., Milicic, L., Vacher, M. A., Sewell, K. R., Peiffer, J. J., Laws, S. M., & Brown, B. M. (2024) · Journal of science and medicine in sport · doi:10.1016/j.jsams.2024.07.017 · Cited by 6 · see citing works
Gehrmann, T., Beekman, M., Deelen, J., Partridge, L., van de Rest, O., Mei, L., Raz, Y., de Groot, C. P. G. M., van der Breggen, R., Reinders, M. J. T., et al. (2024) · doi:10.59368/agingbio.20240036 · Cited by 5 · see citing works
Katayama, M., Nomura, K., Mudry, J. M., Chibalin, A., Krook, A., & Zierath, J. R. (2024) · Molecular Metabolism · doi:10.1016/j.molmet.2024.102081 · Cited by 5 · see citing works
Paez, H. G., Pitzer, C. R., Ferrandi, P. J., Mohamed, J. S., & Alway, S. E. (2025) · The FASEB Journal · doi:10.1096/fj.202500375r · Cited by 5 · see citing works
Γουτιάνος, Γ., Margaritelis, N. V., Sparopoulou, T., Veskoukis, A. S., Vrabas, I. S., Paschalis, V., Nikolaidis, M. G., & Kyparos, A. (2020) · The Journal of Physiological Sciences · doi:10.1186/s12576-020-00737-2 · Cited by 6 · see citing works
Lee, H., Kim, J., Kim, K. H., Jeong, S., Cho, Y., & Kim, N. (2020) · Genes · doi:10.3390/genes11111359 · Cited by 5 · see citing works
Bizjak, D. A., Nussbaumer, D., Winkert, K., Treff, G., Takabajashi, K., Mentz, L., Schober, F., Buhl, J. L., John, L., Dreyhaupt, J., et al. (2023) · Sports Medicine - Open · doi:10.1186/s40798-023-00630-3 · Cited by 4 · see citing works
Bokov, R. O., & Викторович, П. Д. (2022) · Human Physiology · doi:10.1134/s0362119722030033 · Cited by 4 · see citing works
Pacak, C. A., Suzuki‐Hatano, S., Khadir, F., Daugherty, A. L., Sriramvenugopal, M., Gosiker, B. J., Kang, P. B., & Cade, W. T. (2023) · Journal of Translational Medicine · doi:10.1186/s12967-023-04626-1 · Cited by 4 · see citing works
Sulforaphane improves exercise-induced NRF2 signaling in older adults: an in vivo-ex vivo approach
Rodriguez, D. J., Ostrom, E. L., Chassman, C., Robertson, J., Pan, V., Buscaglia, R., Eggler, A. L., & Traustadóttir, T. (2025) · GeroScience · doi:10.1007/s11357-025-01939-5 · Cited by 4 · see citing works
Proteomic and transcriptomic response of human skeletal muscle to 12-week resistance training
Lednev, E. M., Vepkhvadze, T. F., Smirnov, I. P., Илгизович, С. Р., Викторович, Ж. А., Kanygina, A. V., Викторович, П. Д., & Generozov, E. V. (2024) · Genes and Cells · doi:10.17816/gc624325 · Cited by 3 · see citing works
Bakhshi, M., Banaeifar, A., Arshadi, S., & Bazgir, B. (2025) · Archives of Medical Research · doi:10.1016/j.arcmed.2025.103223 · Cited by 3 · see citing works
Bácsi, A., Penyige, A., Becs, G., Benkő, S., Kovács, E. G., Jenei, C., Pócsi, I., Balla, J., Csernoch, L. J., & Balatoni, I. (2022) · Physiological Genomics · doi:10.1152/physiolgenomics.00090.2022 · Cited by 2 · see citing works
Impact of exercise and fasting on mitochondrial regulators in human muscle
Menezes, E. S., Islam, H., Arhen, B. B., Simpson, C. A., McGlory, C., & Gurd, B. J. (2024) · Translational Exercise Biomedicine · doi:10.1515/teb-2024-0014 · Cited by 2 · see citing works
Petrie, M. A., Suneja, M., & Shields, R. K. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms251810189 · Cited by 2 · see citing works
Maasar, M., Turner, D., Gorski, P., Seaborne, R. A., Strauss, J., Shepherd, S., Cocks, M., Pillon, N. J., Zierath, J., Hulton, A., et al. (2020) · bioRxiv · doi:10.1101/2020.09.11.292805 · Cited by 3 · see citing works
Androulakis, N. E. M., Koundourakis, N. E., Tsiakiris, C., & Notas, G. (2020) · The Journal of Sports Medicine and Physical Fitness · doi:10.23736/s0022-4707.20.11119-8 · Cited by 1 · see citing works
- Authors
- Catoire, M., Mensink, M., Boekschoten, M. V., Hangelbroek, R., Müller, M., Schrauwen, P., & Kersten, S.
- Affiliations
- Wageningen University & Research (NL)
- Maastricht University Medical Centre (NL)
- Corresponding author
- Kersten, Sander
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-11-30
- Volume
- 7
- Issue
- 11
- Pages
- e51066
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3511348
- OpenAlex
- W2098809392
- Cited by
- 116
- References
- 51
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 10 · 2023: 6 · 2022: 7 · 2021: 9 · 2020: 14 · 2019: 12 · 2018: 8 · 2017: 10 · 2016: 9 · 2015: 8 · 2014: 9 · 2013: 10
- FWCI
- 9.14
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion, cc-by)
- Socio-Environmental Systems Modeling (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- UEA Digital Repository (University of East Anglia) (submittedVersion)
- Research Publications (Maastricht University) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Topics
- Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Peroxisome Proliferator-Activated Receptors
- Keywords
- acute endurance exercise, skeletal muscle gene expression, PPAR signaling, PDK4, ANGPTL4, SLC22A5, free fatty acids, circulating factors, plasma lactate, cortisol, norepinephrine, energy metabolism
- MeSH terms
- Fatty Acids, Nonesterified, Gene Expression Regulation, Heart Rate, Humans, Hydrocortisone, Insulin, Leg, Male, Middle Aged, Norepinephrine, Physical Endurance, Rest, Transcription Factors, Exercise, Up-Regulation, Muscle, Skeletal, Gene Regulatory Networks
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
