Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle: Molecular responses during mitochondrial biogenesis

Perry, Christopher G. R.; Lally, James; Holloway, Graham P.; Heigenhauser, George J. F.; Bonen, Arend; Spriet, Lawrence L.

doi:10.1113/jphysiol.2010.199448

Cited by 559Adipose Tissue and MetabolismCardiovascular and exercise physiologyMuscle Physiology and Disorders

Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle: Molecular responses during mitochondrial biogenesis

Open access

Perry, Christopher G. R., Lally, James, Holloway, Graham P., Heigenhauser, George J. F., Bonen, Arend, Spriet, Lawrence L.·2010·The Journal of Physiology

DOI 10.1113/jphysiol.2010.199448PMC PMC3010147

Open this paper in CoChat — free account

Abstract

Exercise training induces mitochondrial biogenesis, but the time course of molecular sequelae that accompany repetitive training stimuli remains to be determined in human skeletal muscle. Therefore, throughout a seven-session, high-intensity interval training period that increased (12%), we examined the time course of responses of (a) mitochondrial biogenesis and fusion and fission proteins, and (b) selected transcriptional and mitochondrial mRNAs and proteins in human muscle. Muscle biopsies were obtained 4 and 24 h after the 1st, 3rd, 5th and 7th training session. PGC-1α mRNA was increased >10-fold 4 h after the 1st session and returned to control within 24 h. This 'saw-tooth' pattern continued until the 7th bout, with smaller increases after each bout. In contrast, PGC-1α protein was increased 24 h after the 1st bout (23%) and plateaued at +30-40% between the 3rd and 7th bout. Increases in PGC-1β mRNA and protein were more delayed and smaller, and did not persist. Distinct patterns of increases were observed in peroxisome proliferator-activated receptor (PPAR) α and γ protein (1 session), PPAR β/δ mRNA and protein (5 sessions) and nuclear respiratory factor-2 protein (3 sessions) while no changes occurred in mitochondrial transcription factor A protein. Citrate synthase (CS) and β-HAD mRNA were rapidly increased (1 session), followed 2 sessions later (session 3) by increases in CS and β-HAD activities, and mitochondrial DNA. Changes in COX-IV mRNA (session 3) and protein (session 5) were more delayed. Training also increased mitochondrial fission proteins (fission protein-1, >2-fold; dynamin-related protein-1, 47%) and the fusion protein mitofusin-1 (35%) but not mitofusin-2. This study has provided the following novel information: (a) the training-induced increases in transcriptional and mitochondrial proteins appear to result from the cumulative effects of transient bursts in their mRNAs, (b) training-induced mitochondrial biogenesis appears to involve re-modelling in addition to increased mitochondrial content, and (c) the 'transcriptional capacity' of human muscle is extremely sensitive, being activated by one training bout.

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

Crossref · 10.1113/jphysiol.2010.199448

Cites

82 of 82 references verified0 citation errors · 0 not checkable

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?

Compared to trained athletes, untrained individuals have a greater capacity to activate the molecular machinery in muscle in response to contractile activity because any overload stimulus induces large perturbations to cellular homeostasis regardless of the mode of exercise.
“Compared to trained athletes, untrained individuals have a greater capacity to activate the molecular machinery in muscle in response to contractile activity because any overload stimulus induces large perturbations to cellular homeostasis regardless of the mode of exercise (Benziane et al., 2008b;Perry et al., 2010;Nader et al., 2014).”
From Concurrent exercise training: do opposites distract? (2017) · cites this paper as Perry et al., 2010
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
Repeated, transient increases in mRNA induced after each exercise session are necessary to elicit the sustained increases observed in the content of transcription and metabolic proteins.
“They demonstrated that the repeated, transient increases in mRNA induced after each exercise session were necessary to elicit the sustained increases observed in the content of transcription and metabolic proteins.”
From Concurrent exercise training: do opposites distract? (2017) · cites this paper as Perry et al., 2010
The Discussion reports repeated transient mRNA increases followed by sustained increases in transcription and metabolic proteins. It says the findings support a hypothesis that mRNA bursts are required for adaptation, but does not demonstrate that they are necessary; the citing sentence overstates that conclusion. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Even during a short-term intervention, mRNA responses to exercise are attenuated as the muscle adapts to the exercise challenge, even in the face of an increasing training intensity.
“Of note was that even during such a short-term intervention, the mRNA responses to exercise were attenuated as the muscle adapted to the exercise challenge, even in the face of an increasing training intensity.”
From Concurrent exercise training: do opposites distract? (2017) · cites this paper as Perry et al., 2010
Transcriptional changes accumulate over time such that the protein expression profile of muscle is changed, resulting in an altered phenotype.
“The transcriptional changes accumulate over time such that the protein expression profile of muscle is changed resulting in an altered phenotype [2,8].”
From New strategies in sport nutrition to increase exercise performance (2016) · cites this paper as [8]
The adaptive processes of endurance training are driven by transcriptional changes in response to each bout of exercise.
“These adaptive processes are driven by transcriptional changes in response to each bout of exercise [2,8].”
From New strategies in sport nutrition to increase exercise performance (2016) · cites this paper as [8]

Endurance exercise adaptations are believed to be driven primarily by transcriptional responses, whereas the muscle growth adaptation to resistance exercise is driven primarily by changes in translation, in particular by increases in mRNA activity.
“Whilst endurance exercise adaptations are believed to be driven primarily by transcriptional responses [2,8], the muscle growth adaptation to resistance exercise is driven primarily by changes in translation, in particular by increases in mRNA activity (protein produced per unit of mRNA) [85][86][87].”
From New strategies in sport nutrition to increase exercise performance (2016) · cites this paper as [8]
Endurance exercise increases the activity of muscle oxidative enzymes and FAO, in part from increased volume of the mitochondrial reticulum and elevated levels of cardiolipin, a lipid necessary for the assembly of OXPHOS complexes.
“Endurance exercise increases the activity of muscle oxidative enzymes and FAO, in part from increased volume of the mitochondrial reticulum and elevated levels of cardiolipin, a lipid that is necessary for the assembly of OXPHOS complexes (41, 51, 225).”
From Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease (2018) · cites this paper as [51]
A high-intensity exercise training program showed elevated citrate synthase and β-hydroxyacyl CoA dehydrogenase activity after 5 days and increased levels of mitochondrial complexes after 10 days.
“A high-intensity exercise training program, however, showed elevated citrate synthase and β-hydroxyacyl CoA dehydrogenase activity after 5 days and increased levels of mitochondrial complexes after 10 days (51).”
From Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease (2018) · cites this paper as [51]
Increases in mitochondrial proteins occurred within five days and following three sessions of high-intensity interval training, while at the end of 2 weeks, VO2max had also increased by 12%.
“Increases in mitochondrial proteins occurred within five days and following three sessions of high-intensity interval training, while at the end of the 2 weeks, VO2max had also increased by 12% (Perry et al., 2010).”
From Concurrent exercise training: do opposites distract? (2017) · cites this paper as Perry et al., 2010

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1
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 · see citing works
A Cold-Inducible Coactivator of Nuclear Receptors Linked to Adaptive Thermogenesis
Puigserver, P., Wu, Z., Park, C. W., Graves, R., Wright, M., & Spiegelman, B. M. (1998) · Cell · doi:10.1016/s0092-8674(00)81410-5 · Cited by 3,864 · see citing works
Adaptations 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 · see citing works
Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans
Burgomaster, K. A., Howarth, K. R., Phillips, S. M., Rakobowchuk, M., MacDonald, M. J., McGee, S. L., & Gibala, M. J. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2007.142109 · Cited by 1,257 · see citing works
Transcriptional regulatory circuits controlling mitochondrial biogenesis and function
Kelly, D. P., & Scarpulla, R. C. (2004) · Genes & Development · doi:10.1101/gad.1177604 · Cited by 1,243 · see citing works
Defects in Adaptive Energy Metabolism with CNS-Linked Hyperactivity in PGC-1α Null Mice
Lin, J., Wu, P.-H., Tarr, P. T., Lindenberg, K. S., St-Pierre, J., Zhang, C.-Y., Mootha, V. K., Jäger, S., Vianna, C. R., Reznick, R. M., et al. (2004) · Cell · doi:10.1016/j.cell.2004.09.013 · Cited by 1,162 · see citing works
Short‐term sprint interval versus traditional endurance training: similar initial adaptations in human skeletal muscle and exercise performance
Gibala, M. J., Little, J. P., Van Essen, M., Wilkin, G. P., Burgomaster, K. A., Safdar, A., Raha, S., & Tarnopolsky, M. A. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.112094 · Cited by 1,082 · see citing works
Exercise, Glucose Transport, and Insulin Sensitivity
Goodyear, L. J., & Kahn, B. B. (1998) · Annual Review of Medicine · doi:10.1146/annurev.med.49.1.235 · Cited by 1,056 · see citing works
Biochemical Adaptations to Endurance Exercise in Muscle
Holloszy, J. O., & Booth, F. W. (1976) · Annual Review of Physiology · doi:10.1146/annurev.ph.38.030176.001421 · Cited by 1,053 · see citing works
Handbook of Physiology. Section 12. Exercise: Regulation and Integration of Multiple Systems
Coast, J. R. (1997) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-199703000-00021 · Cited by 915 · see citing works
Exercise 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 · see citing works
Six sessions of sprint interval training increases muscle oxidative potential and cycle endurance capacity in humans
Burgomaster, K. A., Hughes, S. C., Heigenhauser, G. J. F., Bradwel, S. N., & Gibala, M. J. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01095.2004 · Cited by 856 · see citing works
Self-citation
Mitofusin-2 Determines Mitochondrial Network Architecture and Mitochondrial Metabolism
Bach, D., Pich, S., Soriano, F. X., Vega, N., Baumgartner, B., Oriola, J., Daugaard, J. R., Lloberas, J., Camps, M., Zierath, J. R., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m212754200 · Cited by 832 · cited 2× · see citing works
“Importantly, fragmented mitochondria appear to possess lower maximal capacities to oxidize carbohydrates and fatty acids (Bach et al. 2003; Pich et al. 2005).”
Background
Control of mitochondrial transcription specificity factors (TFB1M and TFB2M) by nuclear respiratory factors (NRF-1 and NRF-2) and PGC-1 family coactivators
Gleyzer, N., Vercauteren, K., & Scarpulla, R. C. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.4.1354-1366.2005 · Cited by 711 · see citing works
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 · see citing works
Nuclear activators and coactivators in mammalian mitochondrial biogenesis
Scarpulla, R. C. (2002) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/s0167-4781(02)00343-3 · Cited by 631 · see citing works
Impact of Aerobic Exercise Training on Age-Related Changes in Insulin Sensitivity and Muscle Oxidative Capacity
Short, K. R., Vittone, J. L., Bigelow, M. L., Proctor, D. N., Rizza, R. A., Coenen-Schimke, J. M., & Nair, K. S. (2003) · Diabetes · doi:10.2337/diabetes.52.8.1888 · Cited by 631 · see citing works
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 · see citing works
Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1α muscle-specific knock-out animals.
Handschin, C., Chin, S., Li, P., Liu, F., Maratos-Flier, E., LeBrasseur, N. K., Yan, Z., & Spiegelman, B. M. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m704817200 · Cited by 611 · see citing works
Transcriptional 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
Muscle-specific Pparg deletion causes insulin resistance
Hevener, A. L., He, W., Barak, Y., Le, J., Bandyopadhyay, G. K., Olson, P., Wilkes, J. J., Evans, R. M., & Olefsky, J. M. (2003) · Nature Medicine · doi:10.1038/nm956 · Cited by 492 · see citing works
Nuclear control of respiratory gene expression in mammalian cells
Scarpulla, R. C. (2006) · Journal of Cellular Biochemistry · doi:10.1002/jcb.20743 · Cited by 489 · see citing works
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 · see citing works
Mitochondrial filaments and clusters as intracellular power-transmitting cables
Skulachev, V. P. (2001) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(00)01735-7 · Cited by 477 · see citing works
Molecular basis of skeletal muscle plasticity-from gene to form and function
Flück, M., & Hoppeler, H. H. (2003) · Reviews of physiology, biochemistry and pharmacology · doi:10.1007/s10254-002-0004-7 · Cited by 476 · see citing works
Nuclear Receptor Signaling and Cardiac Energetics
Huss, J. M., & Kelly, D. P. (2004) · Circulation Research · doi:10.1161/01.res.0000141774.29937.e3 · Cited by 472 · see citing works
Peroxisome Proliferator-activated Receptor-γ Co-activator 1α-mediated Metabolic Remodeling of Skeletal Myocytes Mimics Exercise Training and Reverses Lipid-induced Mitochondrial Inefficiency
Koves, T. R., Li, P., An, J., Akimoto, T., Slentz, D., Ilkayeva, O., Dohm, G. L., Yan, Z., Newgard, C. B., & Muoio, D. M. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m507621200 · Cited by 464 · see citing works
The Charcot-Marie-Tooth type 2A gene product, Mfn2, up-regulates fuel oxidation through expression of OXPHOS system
Pich, S., Bach, D., Briones, P., Liesa, M., Camps, M., Testar, X., Palacín, M., & Zorzano, A. (2005) · Human Molecular Genetics · doi:10.1093/hmg/ddi149 · Cited by 455 · see citing works
Endurance Training in Humans Leads to Fiber Type-Specific Increases in Levels of Peroxisome Proliferator-Activated Receptor-γ Coactivator-1 and Peroxisome Proliferator-Activated Receptor-α in Skeletal Muscle
Russell, A. P., Feilchenfeldt, J. W., Schreiber, S., Praz, M., Crettenand, A., Gobelet, C., Meier, C. A., Bell, D., Kralli, A., Giacobino, J., et al. (2003) · Diabetes · doi:10.2337/diabetes.52.12.2874 · Cited by 451 · see citing works
The ultrastructure of the normal human skeletal muscle
Hoppeler, H. H., L�thi, P., Claassen, H., Weibel, E. R., & HOWALD, H. (1973) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00588462 · Cited by 444 · see citing works
Two weeks of high-intensity aerobic interval training increases the capacity for fat oxidation during exercise in women
Talanian, J. L., Galloway, S. D. R., Heigenhauser, G. J. F., Bonen, A., & Spriet, L. L. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01098.2006 · Cited by 443 · see citing works
Self-citation
Muscle-specific PPARγ-deficient mice develop increased adiposity and insulin resistance but respond to thiazolidinediones
Norris, A. W., Chen, L., Fisher, S. J., Szanto, I., Ristow, M., Jozsi, A. C., Hirshman, M. F., Rosen, E. D., Goodyear, L. J., Gonzalez, F. J., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17305 · Cited by 417 · see citing works
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 · see citing works
The transcriptional coactivator PGC-1β drives the formation of oxidative type IIX fibers in skeletal muscle.
Arany, Z., Lebrasseur, N., Morris, C., Smith, E., Yang, W., Ma, Y., Chin, S., & Spiegelman, B. M. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2006.12.003 · Cited by 370 · see citing works
Peroxisome Proliferator-activated Receptor γ Co-activator 1α (PGC-1α) and Sirtuin 1 (SIRT1) Reside in Mitochondria
Aquilano, K., Vigilanza, P., Baldelli, S., Pagliei, B., Rotilio, G., & Ciriolo, M. R. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.070169 · Cited by 347 · see citing works
Abnormal glucose homeostasis in skeletal muscle–specific PGC-1α knockout mice reveals skeletal muscle–pancreatic β cell crosstalk
Handschin, C., Choi, C. S., Chin, S., Kim, S., Kawamori, D., Kurpad, A. J., Neubauer, N., Hu, J., Mootha, V. K., Kim, Y.-B., et al. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31785 · Cited by 335 · see citing works
Exercise-Induced Ultrastructural Changes in Skeletal Muscle*
Hoppeler, H. (1986) · International Journal of Sports Medicine · doi:10.1055/s-2008-1025758 · Cited by 333 · see citing works
High-intensity aerobic interval training increases fat and carbohydrate metabolic capacities in human skeletal muscle
Perry, C. G. R., Heigenhauser, G. J. F., Bonen, A., & Spriet, L. L. (2008) · Applied Physiology Nutrition and Metabolism · doi:10.1139/h08-097 · Cited by 309 · see citing works
Self-citation
PGC-1α mRNA expression is influenced by metabolic perturbation in exercising human skeletal muscle
Norrbom, J., Sundberg, C. J., Rundqvist, H., Kraus, W. E., Jansson, E., & Gustafsson, T. P. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00765.2003 · Cited by 263 · see citing works
Regulation of mitochondrial fusion and division
Cerveny, K. L., Tamura, Y., Zhang, Z., Jensen, R. E., & Sesaki, H. (2007) · Trends in Cell Biology · doi:10.1016/j.tcb.2007.08.006 · Cited by 261 · see citing works
Molecular Machinery of Mitochondrial Fusion and Fission
Westermann, B. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.r800011200 · Cited by 251 · see citing works
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 · see citing works
PGC-1α is not mandatory for exercise- and training-induced adaptive gene responses in mouse skeletal muscle
Leick, L., Wojtaszewski, J. F. P., Johansen, S. T., Kiilerich, K., Comes, G., Hellsten, Y., Hidalgo, J., & Pilegaard, H. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00666.2007 · Cited by 236 · see citing works
Identification of a peroxisome proliferator-responsive element upstream of the gene encoding rat peroxisomal enoyl-CoA hydratase/3-hydroxyacyl-CoA dehydrogenase.
Zhang, B., Marcus, S. L., Sajjadi, F. G., Alvares, K., Reddy, J. K., Subramani, S. E., Rachubinski, R. A., & Capone, J. P. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.16.7541 · Cited by 232 · see citing works
Modest PGC-1α Overexpression in Muscle in Vivo Is Sufficient to Increase Insulin Sensitivity and Palmitate Oxidation in Subsarcolemmal, Not Intermyofibrillar, Mitochondria
Benton, C. R., Nickerson, J. G., Lally, J., Han, X.-X., Holloway, G. P., Glatz, J. F. C., Luiken, J. J. F. P., Graham, T. E., Heikkila, J. J., & Bonen, A. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m704332200 · Cited by 214 · see citing works
Self-citation
Characterization of the human, mouse and rat PGC1beta (peroxisome-proliferator-activated receptor-gamma co-activator 1beta) gene in vitro and in vivo
Meirhaeghe, A., Crowley, V., Lenaghan, C., Lelliott, C. J., GREEN, K., Stewart, A., Kevin, H. A. R. T., Schinner, S., Sethi, J. K., Yeo, G. S. H., et al. (2003) · Biochemical Journal · doi:10.1042/bj20030200 · Cited by 210 · see citing works
Exercise and Myocyte Enhancer Factor 2 Regulation in Human Skeletal Muscle
McGee, S. L., & Hargreaves, M. (2004) · Diabetes · doi:10.2337/diabetes.53.5.1208 · Cited by 205 · see citing works
Exercise induces a transient increase in transcription of the GLUT-4 gene in skeletal muscle
Neufer, P. D., & Dohm, G. L. (1993) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1993.265.6.c1597 · Cited by 192 · see citing works
Effect of endurance training on lipid metabolism in women: a potential role for PPARα in the metabolic response to training
Horowitz, J. F., Leone, T. C., Feng, W., Kelly, D. P., & Klein, S. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.279.2.e348 · Cited by 181 · see citing works
Mitochondrial reticulum in limb skeletal muscle
Kirkwood, S. P., Munn, E. A., & Brooks, G. A. (1986) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1986.251.3.c395 · Cited by 179 · see citing works
Peroxisome proliferator-activated receptors (PPARS): regulators of gene expression in heart and skeletal muscle
Gilde, A. J., & Van Bilsen, M. (2003) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.2003.01161.x · Cited by 178 · see citing works
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 · see citing works
Regulation of metabolic transcriptional co‐activators and transcription factors with acute exercise
Russell, A. P., Hesselink, M. K. C., Lo, S. K., & Schrauwen, P. (2005) · The FASEB Journal · doi:10.1096/fj.04-3168fje · Cited by 173 · see citing works
Acute endurance exercise increases the nuclear abundance of PGC-1α in trained human skeletal muscle
Little, J. P., Safdar, A., Cermak, N. M., Tarnopolsky, M. A., & Gibala, M. J. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00409.2009 · Cited by 163 · see citing works
Selected Contribution: Effects of contractile activity on mitochondrial transcription factor A expression in skeletal muscle
Gordon, J. W., Rungi, A. A., Inagaki, H., & Hood, D. A. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.1.389 · Cited by 160 · see citing works
Rapid exercise-induced changes in PGC-1α mRNA and protein in human skeletal muscle
Mathai, A. S., Bonen, A., Benton, C. R., Robinson, D. L., & Graham, T. E. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00847.2007 · Cited by 158 · see citing works
Self-citation
Response of mitochondrial fusion and fission protein gene expression to exercise in rat skeletal muscle
Ding, H., Jiang, N., Liu, H., Liu, X., Liu, D., Zhao, F., Wen, L., Liu, S., Ji, L. L., & Zhang, Y. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2009.08.007 · Cited by 149 · see citing works
Sensitivity of Lipid Metabolism and Insulin Signaling to Genetic Alterations in Hepatic Peroxisome Proliferator–Activated Receptor-γ Coactivator-1α Expression
Estall, J. L., Kahn, M., Cooper, M. P., Fisher, F. M., Wu, M. K., Laznik, D., Qu, L., Cohen, D. E., Shulman, G. I., & Spiegelman, B. M. (2009) · Diabetes · doi:10.2337/db08-1571 · Cited by 148 · see citing works
Suppression of plasma free fatty acids upregulates peroxisome proliferator-activated receptor (PPAR) α and δ and PPAR coactivator 1α in human skeletal muscle, but not lipid regulatory genes
Watt, M. J., Southgate, R. J., Holmes, A. G., & Febbraio, M. A. (2004) · Journal of Molecular Endocrinology · doi:10.1677/jme.1.01499 · Cited by 144 · see citing works
Increased levels of peroxisome proliferator-activated receptor gamma, coactivator 1 alpha (PGC-1α) improve lipid utilisation, insulin signalling and glucose transport in skeletal muscle of lean and insulin-resistant obese Zucker rats
Benton, C. R., Holloway, G. P., Han, X.-X., Yoshida, Y., Snook, L. A., Lally, J., Glatz, J. F. C., Luiken, J. J. F. P., Chabowski, A., & Bonen, A. (2010) · Diabetologia · doi:10.1007/s00125-010-1773-1 · Cited by 143 · see citing works
Self-citation
Regulation of Gene Expression in Skeletal Muscle by Contractile Activity
Williams, R. S., & Neufer, P. D. (1996) · Comprehensive physiology · doi:10.1002/cphy.cp120125 · Cited by 132 · see citing works
Control of gene expression and mitochondrial biogenesis in the muscular adaptation to endurance exercise
Joseph, A.-M., Pilegaard, H., Litvintsev, A., Leick, L., & Hood, D. A. (2006) · Essays in Biochemistry · doi:10.1042/bse0420013 · Cited by 111 · see citing works
Regulation of muscle glycogen phosphorylase activity following short-term endurance training
Chesley, A., Heigenhauser, G. J. F., & Spriet, L. L. (1996) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1996.270.2.e328 · Cited by 100 · see citing works
Self-citation
PGC-1α increases skeletal muscle lactate uptake by increasing the expression of MCT1 but not MCT2 or MCT4
Benton, C. R., Yoshida, Y., Lally, J., Han, X.-X., Hatta, H., & Bonen, A. (2008) · Physiological Genomics · doi:10.1152/physiolgenomics.90217.2008 · Cited by 97 · see citing works
Self-citation
The deacetylase enzyme SIRT1 is not associated with oxidative capacity in rat heart and skeletal muscle and its overexpression reduces mitochondrial biogenesis
Gurd, B. J., Yoshida, Y., Lally, J., Holloway, G. P., & Bonen, A. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.168096 · Cited by 91 · see citing works
Self-citation
Role of calcineurin in exercise-induced mitochondrial biogenesis
García-Rovés, P. M., Huss, J. M., & Holloszy, J. O. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00633.2005 · Cited by 89 · see citing works
PGC-1α Serine 570 Phosphorylation and GCN5-mediated Acetylation by Angiotensin II Drive Catalase Down-regulation and Vascular Hypertrophy
Xiong, S., Salazar, G., Martín, A. S., Ahmad, M., Patrushev, N. A., Hilenski, L. L., Nazarewicz, R. R., Ma, M., Ushio‐Fukai, M., & Alexander, R. W. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.065235 · Cited by 85 · see citing works
Mitochondrial transcription factor A and respiratory complex IV increase in response to exercise training in humans
Bengtsson, J., Gustafsson, T. P., Widegren, U., Jansson, E., & Sundberg, C. J. (2001) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s004240100628 · Cited by 80 · see citing works
Effects of endurance training on a mitochondrial reticulum in limb skeletal muscle
Kirkwood, S. P., Packer, L., & Brooks, G. A. (1987) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(87)90296-7 · Cited by 77 · see citing works
Effect of 7-10 days of cycle ergometer exercise on skeletal muscle GLUT-4 protein content
Gulve, E. A., & Spina, R. J. (1995) · Journal of Applied Physiology · doi:10.1152/jappl.1995.79.5.1562 · Cited by 77 · see citing works
Antioxidant supplementation enhances the exercise-induced increase in mitochondrial uncoupling protein 3 and endothelial nitric oxide synthase mRNA content in human skeletal muscle
Hellsten, Y., Nielsen, J., Lykkesfeldt, J., Bruhn, M., Silveira, L. R., Pilegaard, H., & Bangsbo, J. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.02.029 · Cited by 65 · see citing works
Endurance exercise induces mRNA expression of oxidative enzymes in human skeletal muscle late in recovery
Leick, L., Plomgaard, P., Grønlykke, L., Al‐Abaiji, F., Wojtaszewski, J. F. P., & Pilegaard, H. (2009) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2009.00988.x · Cited by 61 · see citing works
Peroxisome Proliferator–Activated Receptor-γ Coactivator-1α Overexpression Increases Lipid Oxidation in Myocytes From Extremely Obese Individuals
Consitt, L. A., Bell, J. A., Koves, T. R., Muoio, D. M., Hulver, M. W., Haynie, K. R., Dohm, G. L., & Houmard, J. A. (2010) · Diabetes · doi:10.2337/db09-1704 · Cited by 61 · see citing works
PGC-1β is downregulated by training in human skeletal muscle: no effect of training twice every second day vs. once daily on expression of the PGC-1 family
Mortensen, O. H., Plomgaard, P., Fischer, C. P., Hansen, A. K., Pilegaard, H., & Pedersen, B. K. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00575.2007 · Cited by 56 · see citing works
Compensatory increases in nuclear PGC1α protein are primarily associated with subsarcolemmal mitochondrial adaptations in ZDF rats.
Holloway, G. P., Gurd, B. J., Snook, L. A., Lally, J., & Bonen, A. (2010) · Diabetes · doi:10.2337/db09-1519 · Cited by 55 · see citing works
Self-citation
Exercise training decreases the concentration of malonyl-CoA and increases the expression and activity of malonyl-CoA decarboxylase in human muscle
Kuhl, J., Ruderman, N. B., Musi, N., Goodyear, L. J., Patti, M., Crunkhorn, S., Dronamraju, D., Thorell, A., Nygren, J., Ljungkvist, O., et al. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00341.2005 · Cited by 54 · see citing works
Transcription of the rat skeletal muscle hexokinase II gene is increased by acute exercise
O'Doherty, R. M., Bracy, D. P., Granner, D. K., & Wasserman, D. H. (1996) · Journal of Applied Physiology · doi:10.1152/jappl.1996.81.2.789 · Cited by 50 · see citing works
PGC-1α's relationship with skeletal muscle palmitate oxidation is not present with obesity despite maintained PGC-1α and PGC-1β protein
Holloway, G. P., Perry, C. G. R., Thrush, A. B., Heigenhauser, G. J. F., Dyck, D. J., Bonen, A., & Spriet, L. L. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00726.2007 · Cited by 48 · see citing works
Self-citation
Relationship between insulin sensitivity and in vivo mitochondrial function in skeletal muscle
Sirikul, B., Gower, B. A., Hunter, G. R., Larson‐Meyer, D. E., & Newcomer, B. R. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00364.2005 · Cited by 43 · see citing works
Emerging roles of PPARδ in metabolism
Seedorf, U., & Aberle, J. (2007) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2007.04.017 · Cited by 42 · see citing works
Training response of mitochondrial transcription factors in human skeletal muscle
Norrbom, J., Wallman, S. E., Gustafsson, T. P., Rundqvist, H., Jansson, E., & Sundberg, C. J. (2009) · Acta Physiologica · doi:10.1111/j.1748-1716.2009.02030.x · Cited by 40 · see citing works
Untitled work
Ogata (1997) · doi:10.1002/(sici)1097-0185(199706)248:2

Flagged first, then by citations

Research works printed but not linked: 2

Bergmeyer HU. Methods in Enzymatic Analyses. New York: Academic; 1974. [Google Scholar]
Srere P. Citrate synthase. In: Lowenstein J, editor. Methods in Enzymology. New York: Academic Press; 1969. pp. 3–11. [Google Scholar]

Sorted by citations

Exercise 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 · see citing works
Integrative Biology of Exercise
Hawley, J. A., Hargreaves, M., Joyner, M. J., & Zierath, J. R. (2014) · Cell · doi:10.1016/j.cell.2014.10.029 · Cited by 1,152 · see citing works
Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease
Smith, R. L., Soeters, M. R., Wüst, R. C. I., & Houtkooper, R. H. (2018) · Endocrine Reviews · doi:10.1210/er.2017-00211 · Cited by 787 · see citing works
Exercise Attenuates the Major Hallmarks of Aging
Garatachea, N., Pareja-Galeano, H., Sanchis-Gomar, F., Santos-Lozano, A., Fiuza-Luces, C., Morán, M., Emanuele, E., Joyner, M. J., & Lucia, A. (2015) · Rejuvenation Research · doi:10.1089/rej.2014.1623 · Cited by 413 · see citing works
Concurrent exercise training: do opposites distract?
Coffey, V. G., & Hawley, J. A. (2017) · The Journal of Physiology · doi:10.1113/jp272270 · Cited by 351 · see citing works
Interference between concurrent resistance and endurance exercise: Molecular bases and the role of individual training variables
Fyfe, J. J., Bishop, D. J., & Stepto, N. K. (2014) · Sports Medicine · doi:10.1007/s40279-014-0162-1 · Cited by 347 · see citing works
Nrf2 mediates redox adaptations to exercise
Done, A. J., & Traustadóttir, T. (2016) · Redox Biology · doi:10.1016/j.redox.2016.10.003 · Cited by 308 · see citing works
Molecular mechanisms for mitochondrial adaptation to exercise training in skeletal muscle
Drake, J. C., Wilson, R. J., & Yan, Z. (2016) · The FASEB Journal · doi:10.1096/fj.15-276337 · Cited by 263 · see citing works
Mitochondrial Dynamics and Mitophagy in Skeletal Muscle Health and Aging
Leduc-Gaudet, J.-P., Hussain, S. N. A., Barreiro, E., & Gouspillou, G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22158179 · Cited by 268 · see citing works
Molecular Responses to Acute Exercise and Their Relevance for Adaptations in Skeletal Muscle to Exercise Training
Egan, B., & Sharples, A. P. (2023) · Physiological Reviews · doi:10.1152/physrev.00054.2021 · Cited by 278 · see citing works
Regulation of Muscle Glycogen Metabolism during Exercise: Implications for Endurance Performance and Training Adaptations
Hearris, M., Hammond, K., Fell, J., & Morton, J. (2018) · Nutrients · doi:10.3390/nu10030298 · Cited by 252 · see citing works
Aging Hallmarks: The Benefits of Physical Exercise
Rebelo-Marques, A., De Sousa Lages, A., Andrade, R., Ribeiro, C. F., Mota-Pinto, A., Carrilho, F., & Espregueira-Mendes, J. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00258 · Cited by 246 · see citing works
Training-Induced Changes in Mitochondrial Content and Respiratory Function in Human Skeletal Muscle
Granata, C., Jamnick, N. A., & Bishop, D. J. (2018) · Sports Medicine · doi:10.1007/s40279-018-0936-y · Cited by 247 · see citing works
Skeletal muscle aging and the mitochondrion
Johnson, M. L., Robinson, M. M., & Nair, K. S. (2013) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2012.12.003 · Cited by 233 · see citing works
Carbohydrate availability and exercise training adaptation: Too much of a good thing?
Bartlett, J. D., Hawley, J. A., & Morton, J. P. (2015) · European Journal of Sport Science · doi:10.1080/17461391.2014.920926 · Cited by 230 · see citing works
New strategies in sport nutrition to increase exercise performance
Close, G. L., Hamilton, D. L., Philp, A., Burke, L. M., & Morton, J. P. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.01.016 · Cited by 221 · see citing works
Superior mitochondrial adaptations in human skeletal muscle after interval compared to continuous single-leg cycling matched for total work
MacInnis, M. J., Zacharewicz, E., Martin, B. J., Haikalis, M. E., Skelly, L. E., Tarnopolsky, M. A., Murphy, R. M., & Gibala, M. J. (2017) · The Journal of Physiology · doi:10.1113/jp272570 · Cited by 224 · see citing works
Training intensity modulates changes in PGC‐1α and p53 protein content and mitochondrial respiration, but not markers of mitochondrial content in human skeletal muscle
Granata, C., Oliveira, R. S. F., Little, J. P., Renner, K., & Bishop, D. J. (2016) · The FASEB Journal · doi:10.1096/fj.15-276907 · Cited by 215 · see citing works
Beneficial effects of exercise on age‐related mitochondrial dysfunction and oxidative stress in skeletal muscle
Joseph, A., Adhihetty, P. J., & Leeuwenburgh, C. (2016) · The Journal of Physiology · doi:10.1113/jp270659 · Cited by 186 · see citing works
Markers of Human Skeletal Muscle Mitochondrial Biogenesis and Quality Control: Effects of Age and Aerobic Exercise Training
Konopka, A. R., Suer, M. K., Wolff, C. A., & Harber, M. P. (2014) · The Journals of Gerontology: Series A · doi:10.1093/gerona/glt107 · Cited by 187 · see citing works
High-intensity exercise and mitochondrial biogenesis: current controversies and future research directions
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
Three minutes of all-out intermittent exercise per week increases skeletal muscle oxidative capacity and improves cardiometabolic health
Gillen, J. B., Percival, M. E., Skelly, L. E., Martin, B. J., Tan, R. B., Tarnopolsky, M. A., & Gibala, M. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0111489 · Cited by 181 · see citing works
Vitamin C and E supplementation prevents some of the cellular adaptations to endurance-training in humans
Morrison, D., Hughes, J., Della Gatta, P. A., Mason, S., Lamon, S., Russell, A. P., & Wadley, G. D. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.10.412 · Cited by 171 · see citing works
Unravelling the mechanisms regulating muscle mitochondrial biogenesis
Hood, D. A., Tryon, L. D., Carter, H. N., Kim, Y., & Chen, C. C. W. (2016) · Biochemical Journal · doi:10.1042/bcj20160009 · Cited by 159 · see citing works
Reduced carbohydrate availability enhances exercise-induced p53 signaling in human skeletal muscle: implications for mitochondrial biogenesis
Bartlett, J. D., Louhelainen, J., Iqbal, Z., Cochran, A. J., Gibala, M. J., Gregson, W., Close, G. L., Drust, B., & Morton, J. P. (2013) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00498.2012 · Cited by 147 · see citing works
Exercise training decreases activation of the mitochondrial fission protein dynamin-related protein-1 in insulin-resistant human skeletal muscle
Fealy, C. E., Mulya, A., Lai, N., & Kirwan, J. P. (2014) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01064.2013 · Cited by 140 · see citing works
Skeletal muscle and resistance exercise training; the role of protein synthesis in recovery and remodeling
McGlory, C., Devries, M. C., & Phillips, S. M. (2017) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00613.2016 · Cited by 135 · see citing works
Exercise and mitochondrial dynamics: keeping in shape with ROS and AMPK
Trewin, A., Berry, B., & Wojtovich, A. (2018) · Antioxidants · doi:10.3390/antiox7010007 · Cited by 129 · see citing works
Lifelong physical activity is associated with promoter hypomethylation of genes involved in metabolism, myogenesis, contractile properties and oxidative stress resistance in aged human skeletal muscle
Sailani, M. R., Halling, J. F., Møller, H. D., Lee, H., Plomgaard, P., Pilegaard, H., Snyder, M. P., & Regenberg, B. (2019) · Scientific Reports · doi:10.1038/s41598-018-37895-8 · Cited by 129 · see citing works
Exercise-induced skeletal muscle signaling pathways and human athletic performance
Camera, D. M., Smiles, W. J., & Hawley, J. A. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.02.007 · Cited by 128 · see citing works
Autophagy plays a role in skeletal muscle mitochondrial biogenesis in an endurance exercise-trained condition
Ju, J.-S., Jeon, S.-I., Park, J.-Y., Lee, J.-Y., Lee, S.-C., Cho, K.-J., & Jeong, J.-M. (2016) · The Journal of Physiological Sciences · doi:10.1007/s12576-016-0440-9 · Cited by 125 · see citing works
Time Course Analysis Reveals Gene-Specific Transcript and Protein Kinetics of Adaptation to Short-Term Aerobic Exercise Training in Human Skeletal Muscle
Egan, B., O’Connor, P. L., Zierath, J. R., & O’Gorman, D. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074098 · Cited by 120 · see citing works
Influence of vitamin C and vitamin E on redox signaling: implications for exercise adaptations
Cobley, J. N., McHardy, H., Morton, J. P., Nikolaidis, M. G., & Close, G. L. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.03.018 · Cited by 118 · 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
IL-15 Overexpression Promotes Endurance, Oxidative Energy Metabolism, and Muscle PPARδ, SIRT1, PGC-1α, and PGC-1β Expression in Male Mice
Quinn, L. S., Anderson, B. G., Conner, J. D., & Wolden-Hanson, T. (2013) · Endocrinology · doi:10.1210/en.2012-1773 · Cited by 102 · see citing works
Coordination of mitochondrial biogenesis by PGC-1α in human skeletal muscle: A re-evaluation
Islam, H., Edgett, B. A., & Gurd, B. J. (2018) · Metabolism · doi:10.1016/j.metabol.2017.11.001 · Cited by 99 · see citing works
Mitochondrial quality control, promoted by PGC-1α, is dysregulated by Western diet-induced obesity and partially restored by moderate physical activity in mice
Greene, N. P., Lee, D. E., Brown, J. L., Rosa, M. E., Brown, L. A., Perry, R. A., Henry, J. N., & Washington, T. A. (2015) · Physiological Reports · doi:10.14814/phy2.12470 · Cited by 89 · see citing works
The truncated splice variants, NT -PGC -1α and PGC -1α4 , increase with both endurance and resistance exercise in human skeletal muscle
Ydfors, M., Fischer, H., Mascher, H., Blomstrand, E., Norrbom, J., & Gustafsson, T. (2013) · Physiological Reports · doi:10.1002/phy2.140 · Cited by 77 · see citing works
Ramping up the signal: promoting endurance training adaptation in skeletal muscle by nutritional manipulation
Hawley, J. A., & Morton, J. P. (2014) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/1440-1681.12246 · Cited by 70 · see citing works
A Time to Eat and a Time to Exercise
Parr, E. B., Heilbronn, L. K., & Hawley, J. A. (2020) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000207 · Cited by 65 · see citing works
The effects of sleep disruption on metabolism, hunger, and satiety, and the influence of psychosocial stress and exercise: A narrative review
Rogers, E. M., Banks, N. F., & Jenkins, N. D. M. (2024) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.3667 · Cited by 62 · see citing works
PGC-1α Transcriptional Response and Mitochondrial Adaptation to Acute Exercise Is Maintained in Skeletal Muscle of Sedentary Elderly Males
Cobley, J. N., Bartlett, J. D., Kayani, A., Murray, S. W., Louhelainen, J., Donovan, T., Waldron, S., Gregson, W., Burniston, J. G., Morton, J. P., et al. (2012) · Biogerontology · doi:10.1007/s10522-012-9408-1 · Cited by 58 · see citing works
Effect of electrical stimulation-induced resistance exercise on mitochondrial fission and fusion proteins in rat skeletal muscle
Kitaoka, Y., Ogasawara, R., Tamura, Y., Fujita, S., & Hatta, H. (2015) · Applied Physiology Nutrition and Metabolism · doi:10.1139/apnm-2015-0184 · Cited by 54 · see citing works
Effects of physical activity on the link between PGC-1a and FNDC5 in muscle, circulating Ιrisin and UCP1 of white adipocytes in humans: A systematic review
Dinas, P. C., Lahart, I. M., Timmons, J. A., Svensson, P.-A., Koutedakis, Y., Flouris, A. D., & Metsios, G. S. (2017) · F1000Research · doi:10.12688/f1000research.11107.2 · Cited by 51 · see citing works
Exercise reduces appetite and traffics excess nutrients away from energetically efficient pathways of lipid deposition during the early stages of weight regain
Steig, A. J., Jackman, M. R., Giles, E. D., Higgins, J. A., Johnson, G. C., Mahan, C., Melanson, E. L., Wyatt, H. R., Eckel, R. H., Hill, J. O., et al. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00212.2011 · Cited by 52 · see citing works
Short-term muscle disuse atrophy is not associated with increased intramuscular lipid deposition or a decline in the maximal activity of key mitochondrial enzymes in young and older males
Wall, B. T., Dirks, M. L., Snijders, T., Stephens, F. B., Senden, J. M. G., Verscheijden, M.-L., & van Loon, L. J. C. (2015) · Experimental Gerontology · doi:10.1016/j.exger.2014.11.019 · Cited by 52 · see citing works
Sodium bicarbonate ingestion augments the increase in PGC-1α mRNA expression during recovery from intense interval exercise in human skeletal muscle
Percival, M. E., Martin, B. J., Gillen, J. B., Skelly, L. E., MacInnis, M. J., Green, A. E., Tarnopolsky, M. A., & Gibala, M. J. (2015) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00048.2015 · Cited by 50 · see citing works
Interpretation of exercise-induced changes in human skeletal muscle mRNA expression depends on the timing of the post-exercise biopsies
Kuang, J., McGinley, C., Lee, M. J.-C., Saner, N. J., Garnham, A., & Bishop, D. J. (2022) · PeerJ · doi:10.7717/peerj.12856 · Cited by 45 · see citing works
Hormones, Metabolism and the Benefits of Exercise
(2017) · Research and Perspectives in Endocrine Interactions · doi:10.1007/978-3-319-72790-5 · Cited by 44 · see citing works
Protein ingestion does not impair exercise-induced AMPK signalling when in a glycogen-depleted state: implications for train-low compete-high
Taylor, C., Bartlett, J. D., van de Graaf, C. S., Louhelainen, J., Coyne, V., Iqbal, Z., MacLaren, D. P. M., Gregson, W., Close, G. L., & Morton, J. P. (2013) · European Journal of Applied Physiology · doi:10.1007/s00421-012-2574-7 · Cited by 43 · see citing works
Is exercise a viable therapeutic intervention to mitigate mitochondrial dysfunction and insulin resistance induced by sleep loss?
Saner, N. J., Bishop, D. J., & Bartlett, J. D. (2018) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2017.01.001 · Cited by 41 · see citing works
IL-15 is required for postexercise induction of the pro-oxidative mediators PPARδ and SIRT1 in male mice
Quinn, L. S., Anderson, B. G., Conner, J. D., Wolden-Hanson, T., & Marcell, T. J. (2014) · Endocrinology · doi:10.1210/en.2013-1645 · Cited by 40 · see citing works
Feeding influences adipose tissue responses to exercise in overweight men
Chen, Y.-C., Travers, R. L., Walhin, J.-P., Gonzalez, J. T., Koumanov, F., Betts, J. A., & Thompson, D. (2017) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00006.2017 · Cited by 39 · see citing works
Insights into the development of insulin resistance: Unraveling the interaction of physical inactivity, lipid metabolism and mitochondrial biology
Handy, R. M., & Holloway, G. P. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1151389 · Cited by 38 · see citing works
Self-citation
Performance effects of periodized carbohydrate restriction in endurance trained athletes – a systematic review and meta-analysis
Gejl, K. D., & Nybo, L. (2021) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-021-00435-3 · Cited by 33 · see citing works
Research progress on sarcopenia in the musculoskeletal system
Mao, X., Lv, K., Qi, W., Cheng, W., Li, T., Sun, Y., Jin, H., Pan, H., & Wang, D. (2025) · Bone Research · doi:10.1038/s41413-025-00455-8 · Cited by 37 · see citing works
Exercise-induced reductions in mitochondrial ADP sensitivity contribute to the induction of gene expression and mitochondrial biogenesis through enhanced mitochondrial H2O2 emission
Miotto, P. M., & Holloway, G. P. (2019) · Mitochondrion · doi:10.1016/j.mito.2018.03.003 · Cited by 30 · see citing works
Targeting skeletal muscle mitochondrial health in obesity
Pileggi, C. A., Hooks, B. G., McPherson, R., Dent, R. R. M., & Harper, M.-E. (2022) · Clinical Science · doi:10.1042/cs20210506 · Cited by 21 · see citing works
Over-Expressing Mitofusin-2 in Healthy Mature Mammalian Skeletal Muscle Does Not Alter Mitochondrial Bioenergetics
Lally, J. S. V., Herbst, E. A. F., Matravadia, S., Maher, A. C., Perry, C. G. R., Ventura-Clapier, R., & Holloway, G. P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055660 · Cited by 19 · see citing works
Self-citation
Modelling inter-individual variability in acute and adaptive responses to interval training: insights into exercise intensity normalisation
Bossi, A. H., Naumann, U., Passfield, L., & Hopker, J. (2024) · European Journal of Applied Physiology · doi:10.1007/s00421-023-05340-y · Cited by 13 · see citing works
Delaying post‐exercise carbohydrate intake impairs next‐day exercise capacity but not muscle glycogen or molecular responses
Díaz‐Lara, J., Reisman, E., Botella, J., Probert, B., Burke, L. M., Bishop, D. J., & Lee, M. J. (2024) · Acta Physiologica · doi:10.1111/apha.14215 · Cited by 10 · see citing works
Minimal alteration in muscle lipid genes following stabilized weight loss
Coker, R. H., Robinette, L., & Kern, P. A. (2017) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2017-0098 · Cited by 3 · see citing works

Aging and Calorie Restriction Oppositely Affect Mitochondrial Biogenesis through TFAM Binding at Both Origins of Mitochondrial DNA Replication in Rat Liver
Picca, A., Pesce, V., Fracasso, F., Joseph, A.-M., Leeuwenburgh, C., & Lezza, A. M. S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074644 · Cited by 80 · see citing works
Exercise induces mitochondrial biogenesis after brain ischemia in rats
Zhang, Q., Wu, Y., Zhang, P., Sha, H., Jia, J., Hu, Y., & Zhu, J. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.12.053 · Cited by 121 · see citing works
Old Player, New Tale: An Acute Bout of Endurance Exercise Increases Mitochondrial PGC-1· content
Safdar, A., Stokl, A., Little, J. P., Hettinga, B. P., & Tarnopolsky, M. A. (2010) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000389394.25923.0b
Mitochondrial biogenesis contributes to ischemic neuroprotection afforded by LPS pre‐conditioning
Stetler, R. A., Leak, R. K., Yin, W., Zhang, L., Wang, S., Gao, Y., & Chen, J. (2012) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2012.07951.x · Cited by 52 · see citing works
Impairment of PGC-1α-mediated mitochondrial biogenesis precedes mitochondrial dysfunction and Alzheimer's pathology in the 3xTg mouse model of Alzheimer's disease
Singulani, M. P., Pereira, C. P. M., Ferreira, A. F. F., Garcia, P. C., Ferrari, G. D., Alberici, L. C., & Britto, L. R. (2020) · Experimental Gerontology · doi:10.1016/j.exger.2020.110882 · Cited by 80 · see citing works

Authors: Perry, C. G. R., Lally, J., Holloway, G. P., Heigenhauser, G. J. F., Bonen, A., & Spriet, L. L.
Affiliations: East Carolina University (US)
University of Guelph (CA)
McMaster University (CA)
ORCID: Perry, Christopher G. R.
Lally, James
Holloway, Graham P.
Spriet, Lawrence L.
Venue: The Journal of Physiology
Publisher: Wiley
Published: 2010-11-30
Volume: 588
Issue: 23
Pages: 4795-4810
ISSN: 0022-3751 (ISSN-L)
DOI: 10.1113/jphysiol.2010.199448
PMC: PMC3010147
OpenAlex: W2124056915
Cited by: 559
References: 82
Citations by year: 2026: 21 · 2025: 31 · 2024: 35 · 2023: 33 · 2022: 38 · 2021: 44 · 2020: 41 · 2019: 49 · 2018: 42 · 2017: 44 · 2016: 44 · 2015: 41 · 2014: 26 · 2013: 38 · 2012: 23
FWCI: 15.17
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: doi.wiley.com/10.1002/tdm_license_1.1 (tdm, 1736 d)
Locations: The Journal of Physiology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: McMaster University
Canada Research Chairs
Natural Sciences and Engineering Research Council of Canada
Topics: Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Keywords: exercise training, skeletal muscle, mitochondrial biogenesis, high-intensity interval training, PGC-1α, PGC-1β, peroxisome proliferator-activated receptors, TFAM, mitochondrial fission, mitochondrial fusion, mitofusin 1, Drp1, citrate synthase, beta-hydroxyacyl-CoA dehydrogenase, cytochrome c oxidase subunit IV, mitochondrial DNA
MeSH terms: Gene Expression Regulation, Humans, Male, Muscle Proteins, RNA, Messenger, Transcription Factors, Exercise, Muscle, Skeletal, Protein Isoforms, Mitochondrial Proteins, Young Adult

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

Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle: Molecular responses during mitochondrial biogenesis

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks