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Time Course Analysis Reveals Gene-Specific Transcript and Protein Kinetics of Adaptation to Short-Term Aerobic Exercise Training in Human Skeletal Muscle
Open accessAbstract
Repeated bouts of episodic myofibrillar contraction associated with exercise training are potent stimuli for physiological adaptation. However, the time course of adaptation and the continuity between alterations in mRNA expression and protein content are not well described in human skeletal muscle. Eight healthy, sedentary males cycled for 60 min at 80% of peak oxygen consumption (VO2peak) each day for fourteen consecutive days, resulting in an increase in VO2peak of 17.5±3.8%. Skeletal muscle biopsies were taken at baseline, and on the morning following (+16 h after exercise) the first, third, seventh, tenth and fourteenth training sessions. Markers of mitochondrial adaptation (Cyt c and COXIV expression, and citrate synthase activity) were increased within the first week of training, but the mtDNA/nDNA ratio was unchanged by two weeks of training. Accumulation of PGC-1α and ERRα protein during training suggests a regulatory role for these factors in adaptations of mitochondrial and metabolic gene expression. A subset of genes were transiently increased after one training session, but returned to baseline levels thereafter, which is supportive of the concept of transcriptional capacity being particularly sensitive to the onset of a new level of contractile activity. Thus, gene-specific temporal patterns of induction of mRNA expression and protein content are described. Our results illustrate the phenomenology of skeletal muscle plasticity and support the notion that transcript level adjustments, coupled to accumulation of encoded protein, underlie the modulation of skeletal muscle metabolism and phenotype by regular exercise.
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“If said exercise stimulus is repeated over time, chronic structural and functional changes occur [2,200].”
From Regulation of Energy Substrate Metabolism in Endurance Exercise (2021) · cites this paper as [200]
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Cites
New methods for calculating metabolic rate with special reference to protein metabolism
Weir, J. B. D. V. (1949) · The Journal of Physiology · doi:10.1113/jphysiol.1949.sp004363 · Cited by 5,688
Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R. C., et al. (1999) · Cell · doi:10.1016/s0092-8674(00)80611-x · Cited by 4,139
Metabolic control through the PGC-1 family of transcription coactivators
Lin, J., Handschin, C., & Spiegelman, B. M. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.05.004 · Cited by 2,130 · cited 1×
“Altering the transcriptional activity of PGC-1a affects physiological responses that equip the cell to meet the energy demands of a changing environment, including augmentation of mitochondrial biogenesis, cellular respiration rates and substrate utilization [20].”
BackgroundExercise Metabolism and the Molecular Regulation of Skeletal Muscle Adaptation
Egan, B., & Zierath, J. R. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2012.12.012 · Cited by 2,084
Self-citationAdaptations of skeletal muscle to endurance exercise and their metabolic consequences
Holloszy, J. O., & Coyle, E. F. (1984) · Journal of Applied Physiology · doi:10.1152/jappl.1984.56.4.831 · Cited by 1,985
Biochemical Adaptations in Muscle
Holloszy, J. O. (1967) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)96046-1 · Cited by 1,517
Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects
Larsen, S., Nielsen, J., Hansen, C. N., Nielsen, L. B., Wibrand, F., Stride, N., Schroder, H. D., Boushel, R., Helge, J. W., Dela, F., et al. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.230185 · Cited by 1,180 · cited 2×
“Instead CS activity and markers of OXPHOS activity such as complex V protein content are considered more informative [35].”
BackgroundExercise induces transient transcriptional activation of the PGC‐1α gene in human skeletal muscle
Pilegaard, H., Saltin, B., & Neufer, P. D. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.034850 · Cited by 885
Reversible Ponceau staining as a loading control alternative to actin in Western blots
Romero-Calvo, I., Ocón, B., Martínez-Moya, P., Suárez, M. D., Zarzuelo, A., Martínez-Augustin, O., & de Medina, F. S. (2010) · Analytical Biochemistry · doi:10.1016/j.ab.2010.02.036 · Cited by 771
Molecular and cellular adaptation of muscle in response to exercise: perspectives of various models
Booth, F. W., & Thomason, D. B. (1991) · Physiological Reviews · doi:10.1152/physrev.1991.71.2.541 · Cited by 703
Invited Review: Contractile activity-induced mitochondrial biogenesis in skeletal muscle
Hood, D. A. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.3.1137 · Cited by 692
Gibala, M. J., & McGee, S. L. (2008) · Exercise and Sport Sciences Reviews · doi:10.1097/jes.0b013e318168ec1f · Cited by 682
Schreiber, S., Emter, R., Hock, M. B., Knutti, D., Cardenas, J., Podvinec, M., Oakeley, E. J., & Kralli, A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308686101 · Cited by 678
Endurance training in humans: aerobic capacity and structure of skeletal muscle.
Hoppeler, H., Howald, H., Conley, K., Lindstedt, S. L., Claassen, H., Vock, P., & Weibel, E. R. (1985) · Journal of Applied Physiology · doi:10.1152/jappl.1985.59.2.320 · Cited by 623
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
Self-citationPerry, C. G. R., Lally, J., Holloway, G. P., Heigenhauser, G. J. F., Bonen, A., & Spriet, L. L. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2010.199448 · Cited by 559
Suction applied to a muscle biopsy maximizes sample size
Evans, W. J., Phinney, S. D., & Young, V. R. (1982) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-198201000-00018 · Cited by 525
Huss, J. M., Pineda‐Torra, I., Staels, B., Giguère, V., & Kelly, D. P. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.20.9079-9091.2004 · Cited by 498
Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1α expression.
Wright, D. C., Han, D.-H., Garcia-Roves, P. M., Geiger, P. C., Jones, T. E., & Holloszy, J. O. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m606116200 · Cited by 488
Schreiber, S., Knutti, D., Brogli, K., Uhlmann, T., & Kralli, A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m212923200 · Cited by 458
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 429
Influence of exercise intensity and duration on biochemical adaptations in skeletal muscle
Dudley, G. A., Abraham, W. M., & Terjung, R. L. (1982) · Journal of Applied Physiology · doi:10.1152/jappl.1982.53.4.844 · Cited by 413
Mitofusins 1/2 and ERRα expression are increased in human skeletal muscle after physical exercise
Cartoni, R., Léger, B., Hock, M. B., Praz, M., Crettenand, A., Pich, S., Ziltener, J., Luthi, F., Dériaz, O., Zorzano, A., et al. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.092031 · Cited by 406
Biological control through regulated transcriptional coactivators
Spiegelman, B. M., & Heinrich, R. (2004) · Cell · doi:10.1016/j.cell.2004.09.037 · Cited by 377
Egan, B., Carson, B. P., Garcia-Roves, P. M., Chibalin, A. V., Sarsfield, F. M., Barron, N., McCaffrey, N., Moyna, N. M., Zierath, J. R., & O’Gorman, D. J. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2010.188011 · Cited by 373
Self-citationCoordination of metabolic plasticity in skeletal muscle
Hood, D. A., Irrcher, I., Ljubicic, V., & Joseph, A.-M. (2006) · Journal of Experimental Biology · doi:10.1242/jeb.02182 · Cited by 370
Timmons, J. A., Knudsen, S., Rankinen, T., Koch, L. G., Sarzynski, M., Jensen, T., Keller, P., Scheele, C., Vollaard, N. B. J., Nielsen, S., et al. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01295.2009 · Cited by 358
Yan, Z., Okutsu, M., Akhtar, Y., & Lira, V. A. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00993.2010 · Cited by 354
Wende, A. R., Huss, J. M., Schaeffer, P. J., Giguère, V., & Kelly, D. P. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.24.10684-10694.2005 · Cited by 354
Skeletal muscle NAMPT is induced by exercise in humans
Costford, S. R., Bajpeyi, S., Pasarica, M., Albarado, D. C., Thomas, S. C., Xie, H., Church, T. S., Jubrias, S. A., Conley, K. E., & Smith, S. R. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00318.2009 · Cited by 299
Yang, Y., Creer, A., Jemiolo, B., & Trappe, S. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01185.2004 · Cited by 290
Mitochondrial enzymes increase in muscle in response to 7-10 days of cycle exercise
Spina, R. J., Chi, M. M., Hopkins, M., Nemeth, P. M., Lowry, O. H., & Holloszy, J. O. (1996) · Journal of Applied Physiology · doi:10.1152/jappl.1996.80.6.2250 · Cited by 247
O’Gorman, D. J., Karlsson, H. K. R., McQuaid, S., Yousif, O., Rahman, Y., Gasparro, D., Glund, S., Chibalin, A. V., Zierath, J. R., & Nolan, J. J. (2006) · Diabetologia · doi:10.1007/s00125-006-0457-3 · Cited by 226
Self-citationReichmann, H., Hoppeler, H. H., Mathieu-Costello, O. A., Bergen, F., & Pette, D. (1985) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00581484 · Cited by 226
Time course of the adaptive responses of aerobic power and heart rate to training
HICKSON, R. C., HAGBERG, J. M., EHSANI, A. A., & HOLLOSZY, J. O. (1981) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-198101000-00012 · Cited by 187
ACSM's advanced exercise physiology
Tipton, C. M., Sawka, M. N., Tate, C. A., & Terjung, R. L. (2006) · Medical Entomology and Zoology · Cited by 175
Timmons, J. A., Larsson, O. S., Jansson, E., Fischer, H., Gustafsson, T. P., Greenhaff, P. L., Ridden, J., Rachman, J., Peyrard‐Janvid, M., Wahlestedt, C., et al. (2005) · The FASEB Journal · doi:10.1096/fj.04-1980com · Cited by 159
Coffey, V. G., SHIELD, A. J., Canny, B. J., Carey, K. A., Cameron‐Smith, D., & Hawley, J. A. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00299.2005 · Cited by 144
Metabolic adaptations to training precede changes in muscle mitochondrial capacity
Green, H. J., Helyar, R., Ball-Burnett, M. E., Kowalchuk, N., Symon, S., & Farrance, B. (1992) · Journal of Applied Physiology · doi:10.1152/jappl.1992.72.2.484 · Cited by 142
Physical activity levels and determinants of change in young adults: a longitudinal panel study
Zimmermann-Sloutskis, D., Wanner, M., Zimmermann, E., & Martin, B. W. (2010) · International Journal of Behavioral Nutrition and Physical Activity · doi:10.1186/1479-5868-7-2 · Cited by 133
Exercise induces expression of leukaemia inhibitory factor in human skeletal muscle
Broholm, C., Mortensen, O. H., Nielsen, S., Akerstrom, T., Zankari, A., Dahl, B., & Pedersen, B. K. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2007.149781 · Cited by 132
Divergent cell signaling after short-term intensified endurance training in human skeletal muscle
Benziane, B., Burton, T. J., Scanlan, B., Galuska, D., Canny, B. J., Chibalin, A. V., Zierath, J. R., & Stepto, N. K. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90428.2008 · Cited by 119
Self-citationmRNAs of enzymes involved in energy metabolism and mtDNA are increased in endurance-trained athletes
Puntschart, A., Claassen, H., Jostarndt, K., Hoppeler, H. H., & Billeter, R. (1995) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1995.269.3.c619 · Cited by 108
Relative Workload Determines Exercise-Induced Increases in PGC-1α mRNA
Nordsborg, N. B., Lundby, C., Leick, L., & Pilegaard, H. (2010) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181d2d21c · Cited by 86
Adaptations in muscle metabolism to prolonged voluntary exercise and training
Green, H. J., Jones, S. R., Ball-Burnett, M. E., Farrance, B., & Ranney, D. (1995) · Journal of Applied Physiology · doi:10.1152/jappl.1995.78.1.138 · Cited by 86
Suction applied to a muscle biopsy maximizes sample size
EVANS, W. J., PHINNEY, S. D., & Young, V. R. (1982) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-198214010-00018 · Cited by 85
Vercauteren, K., Gleyzer, N., & Scarpulla, R. C. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m710150200 · Cited by 84
Regulation of metabolic genes in human skeletal muscle by short-term exercise and diet manipulation
Arkinstall, M. J., Tunstall, R. J., Cameron‐Smith, D., & Hawley, J. A. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00557.2003 · Cited by 84
Egan, B., Dowling, P., O’Connor, P. L., Henry, M. A., Meleady, P., Zierath, J. R., & O’Gorman, D. J. (2011) · PROTEOMICS · doi:10.1002/pmic.201000597 · Cited by 84
Self-citationEffect of short‐term training on GLUT‐4 mRNA and protein expression in human skeletal muscle
Kraniou, G. N., Cameron‐Smith, D., & Hargreaves, M. (2004) · Experimental Physiology · doi:10.1113/expphysiol.2004.027409 · Cited by 78
Effects of exercise on mitochondrial DNA content in skeletal muscle of patients with COPD
Puente‐Maestu, L., Lázaro, A., Tejedor, A., Camaño, S., Fuentes, M., Cuervo, M., Navarro, B., & Agustí, A. G. N. (2010) · Thorax · doi:10.1136/thx.2010.153031 · Cited by 71
Mirebeau‐Prunier, D., Pennec, S. L., Jacques, C., Guéguen, N., Poirier, J., Malthièry, Y., & Savagner, F. (2010) · FEBS Journal · doi:10.1111/j.1742-4658.2009.07516.x · Cited by 67
Jb, M., Ordway, G. A., Richardson, J. A., & Williams, R. S. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117318 · Cited by 61
Wallace, M. A., Hock, M. B., Hazen, B. C., Kralli, A., Snow, R. J., & Russell, A. P. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.205468 · Cited by 55
Skeletal muscle mitochondrial DNA content in exercising humans
Marcuello, A., González‐Alonso, J., Calbet, J. A. L., Damsgaard, R., López-Pérez, M. J., & Díez‐Sánchez, C. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00289.2005 · Cited by 49
Contractile Activity-Induced Mitochondrial Biogenesis in Skeletal Muscle
Essig, D. A. (1996) · Exercise and Sport Sciences Reviews · doi:10.1249/00003677-199600240-00012 · Cited by 47
EFFECTS OF ENDURANCE EXERCISE ON CYTOCHROME C TURNOVER IN SKELETAL MUSCLE*
Booth, F. W. (1977) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1977.tb38219.x · Cited by 34
Research in the Exercise Sciences
Baldwin, K. M., & Haddad, F. (2010) · Exercise and Sport Sciences Reviews · doi:10.1097/jes.0b013e3181d49644 · Cited by 32
Mahoney, D. J., & Tarnopolsky, M. A. (2005) · Physical Medicine and Rehabilitation Clinics of North America · doi:10.1016/j.pmr.2005.08.018 · Cited by 30
Cardiorespiratory adaptation with short term training in older men
Govindasamy, D., Paterson, D. H., Poulin, M. J., & Cunningham, D. A. (1992) · European Journal of Applied Physiology · doi:10.1007/bf00705082 · Cited by 26
Dudley, G. A., Abraham, W. M., & Terjung, R. L. (1981) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-198101320-00349 · Cited by 5
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Metadata
- Authors
- Egan, B., O’Connor, P. L., Zierath, J. R., & O’Gorman, D. J.
- Affiliations
- University College Dublin (IE)
- Dublin City University (IE)
- Karolinska Institutet (SE)
- Corresponding author
- O’Gorman, Donal J.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-09-12
- Volume
- 8
- Issue
- 9
- Pages
- e74098
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3771935
- OpenAlex
- W2020255277
- Cited by
- 120
- References
- 61
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 7 · 2023: 11 · 2022: 10 · 2021: 14 · 2020: 7 · 2019: 12 · 2018: 10 · 2017: 8 · 2016: 20 · 2015: 8 · 2014: 5 · 2013: 1
- FWCI
- 26.79
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Irish Research Council for Science, Engineering and Technology
- Dublin City University
- European Foundation for the Study of Diabetes
- Irish Research Council
- Karolinska Institutet
- Novo Nordisk
- Vetenskapsrådet
- Topics
- Health Sciences › Medicine › Physiology (medical) › Cardiovascular and exercise physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Keywords
- aerobic exercise training, skeletal muscle adaptation, temporal gene expression, mRNA expression, protein content, mitochondrial biogenesis, PGC-1α, estrogen-related receptor alpha, citrate synthase, cytochrome c, cytochrome c oxidase subunit IV, mtDNA/nDNA ratio, skeletal muscle plasticity, human skeletal muscle
- MeSH terms
- Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha, Adaptation, Physiological, Adult, Carrier Proteins, Gene Expression Regulation, Humans, Kinetics, Male, Mitochondria, Oxygen Consumption, Time Factors, Transcription Factors, Transcription, Genetic, Biomarkers, Exercise, RNA-Binding Proteins, Muscle, Skeletal, Proteome, Young Adult, Transcriptome
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