Coordination of mitochondrial biogenesis by PGC-1α in human skeletal muscle: A re-evaluation

Islam, Hashim; Edgett, Brittany A.; Gurd, Brendon J.

doi:10.1016/j.metabol.2017.11.001

Cited by 99Adipose Tissue and MetabolismMetabolism, Diabetes, and CancerMitochondrial Function and Pathology

Coordination of mitochondrial biogenesis by PGC-1α in human skeletal muscle: A re-evaluation

Islam, Hashim, Edgett, Brittany A., Gurd, Brendon J.·2018·Metabolism

DOI 10.1016/j.metabol.2017.11.001

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Abstract

The transcriptional co-activator peroxisome proliferator-activated receptor gamma co-activator-1 alpha (PGC-1α) is proposed to coordinate skeletal muscle mitochondrial biogenesis through the integrated induction of nuclear- and mitochondrial-encoded gene transcription. This paradigm is based largely on experiments demonstrating PGC-1α's ability to co-activate various nuclear transcription factors that increase the expression of mitochondrial genes, as well as PGC-1α's direct interaction with mitochondrial transcription factor A within mitochondria to increase the transcription of mitochondrial DNA. While this paradigm is supported by evidence from cellular and transgenic animal models, as well as acute exercise studies involving animals, the up-regulation of nuclear- and mitochondrial-encoded genes in response to exercise does not appear to occur in a coordinated fashion in human skeletal muscle. This review re-evaluates our current understanding of this phenomenon by highlighting evidence from recent studies examining the exercise-induced expression of nuclear- and mitochondrial-encoded genes targeted by PGC-1α. We also highlight several possible theories that may explain the apparent inability of PGC-1α to coordinately up-regulate the expression of genes required for mitochondrial biogenesis in human skeletal muscle, and provide directions for future work exploring mitochondrial biogenic gene expression following exercise.

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PGC-1α, as a downstream effector of AMPK signaling, has the function of delaying sarcopenia.
“Moreover, PGC-1α, as a downstream effector of AMPK signaling, and has been confirmed to have the function of delaying sarcopenia [10].”
From Lifelong Aerobic Exercise Alleviates Sarcopenia by Activating Autophagy and Inhibiting Protein Degradation via the AMPK/PGC-1α Signaling Pathway (2021) · cites this paper as [10]

1 retracted

Exercise Increases Mitochondrial PGC-1α Content and Promotes Nuclear-Mitochondrial Cross-talk to Coordinate Mitochondrial Biogenesis
Safdar, A., Little, J. P., Stokl, A., Hettinga, B. P., Akhtar, M., & Tarnopolsky, M. A. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.211466 · Cited by 309 · see citing works
Retracted
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
Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibres
Lin, J., Wu, H., Tarr, P. T., Zhang, C.-Y., Wu, Z., Boss, O., Michael, L. F., Puigserver, P., Isotani, E., Olson, E. N., et al. (2002) · Nature · doi:10.1038/nature00904 · Cited by 2,546 · see citing works
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
Transcriptional paradigms in mammalian mitochondrial biogenesis and function
Scarpulla, R. C. (2008) · Physiological Reviews · doi:10.1152/physrev.00025.2007 · Cited by 1,666 · see citing works
Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network
Scarpulla, R. C. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2010.09.019 · Cited by 1,281 · 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
Regulation of pgc-1α, a nodal regulator of mitochondrial biogenesis
Fernandez-Marcos, P. J., & Auwerx, J. (2011) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.110.001917 · Cited by 1,237 · see citing works
Acute Exercise Remodels Promoter Methylation in Human Skeletal Muscle
Barrès, R., Yan, J., Egan, B., Treebak, J. T., Rasmussen, M., Fritz, T., Caidahl, K., Krook, A., O'Gorman, D. J., & Zierath, J. R. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.01.001 · Cited by 965 · cited 1× · see citing works
“NRF-1/2 via by PGC-1α might not be required for the up-regulation of TFAM [55].”
PGC-1α Deficiency Causes Multi-System Energy Metabolic Derangements: Muscle Dysfunction, Abnormal Weight Control and Hepatic Steatosis
Leone, T. C., Lehman, J. J., Finck, B. N., Schaeffer, P. J., Wende, A. R., Boudina, S., Courtois, M., Wozniak, D. F., Sambandam, N., Bernal-Mizrachi, C., et al. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030101 · Cited by 951 · see citing works
Mitochondrial transcription factor A regulates mtDNA copy number in mammals
Ekstrand, M. I. (2004) · Human Molecular Genetics · doi:10.1093/hmg/ddh109 · Cited by 919 · 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
Activation of the human mitochondrial transcriptionfactor A gene by nuclear respiratory factors: a potential regulatory linkbetween nuclear and mitochondrial gene expression in organellebiogenesis.
Virbasius, J. V., & Scarpulla, R. C. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.4.1309 · Cited by 819 · see citing works
The Molecular Bases of Training Adaptation
Coffey, V. G., & Hawley, J. A. (2007) · Sports Medicine · doi:10.2165/00007256-200737090-00001 · Cited by 756 · see citing works
An autoregulatory loop controls peroxisome proliferator-activated receptor γ coactivator 1α expression in muscle
Handschin, C., Rhee, J., Lin, J., Tarr, P. T., & Spiegelman, B. M. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1232352100 · Cited by 729 · see citing works
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
Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1
Michael, L. F., Wu, Z., Cheatham, R. B., Puigserver, P., Adelmant, G., Lehman, J. J., Kelly, D. P., & Spiegelman, B. M. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.061035098 · Cited by 663 · see citing works
Metabolic adaptations through the PGC‐1α and SIRT1 pathways
Rodgers, J. T., Lerín, C., Gerhart‐Hines, Z., & Puigserver, P. (2007) · FEBS Letters · doi:10.1016/j.febslet.2007.11.034 · Cited by 599 · see citing works
Mitochondrial transcription factors B1 and B2 activate transcription of human mtDNA
Falkenberg, M., Gaspari, M., Rantanen, A., Trifunovic, A., Larsson, N.-G., & Gustafsson, C. M. (2002) · Nature Genetics · doi:10.1038/ng909 · Cited by 598 · cited 1× · see citing works
“pathway also up-regulates the mitochondrial transcription factors B1 (TFB1M) and B2 (TFB2M), essential components of the mtDNA transcriptional machinery [25,26].”
Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle: Molecular responses during mitochondrial biogenesis
Perry, 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 · 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
Extracellular Cysteine in Connexins: Role as Redox Sensors
Retamal, M. A., García, I. E., Pinto, B. I., Pupo, A., Báez-Nieto, D., Stehberg, J., Río, R. D., & Gonzalez, C. L. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00001 · Cited by 482 · see citing works
Brief intense interval exercise activates AMPK and p38 MAPK signaling and increases the expression of PGC-1α in human skeletal muscle
Gibala, M. J., McGee, S. L., Garnham, A. P., Howlett, K. F., Snow, R. J., & Hargreaves, M. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.90880.2008 · Cited by 427 · 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
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
Muscle-specific expression of PPARγ coactivator-1α improves exercise performance and increases peak oxygen uptake
Calvo, J. A., Daniels, T. G., Wang, X., Paul, A., Lin, J., Spiegelman, B. M., Stevenson, S. C., & Rangwala, S. M. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01231.2007 · Cited by 377 · see citing works
NRF-1, an activator involved in nuclear-mitochondrial interactions, utilizes a new DNA-binding domain conserved in a family of developmental regulators.Preprint
Virbasius, C.-M. A., Virbasius, J. V., & Scarpulla, R. C. (1993) · Genes & Development · doi:10.1101/gad.7.12a.2431 · Cited by 356 · 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
Systematic identification of human mitochondrial disease genes through integrative genomics
Calvo, S. E., Jain, M., Xie, X. S., Sheth, S. A., Chang, B., Goldberger, O., Spinazzola, A., Zeviani, M., Carr, S. A., & Mootha, V. K. (2006) · Nature Genetics · doi:10.1038/ng1776 · Cited by 344 · see citing works
An acute bout of high-intensity interval training increases the nuclear abundance of PGC-1α and activates mitochondrial biogenesis in human skeletal muscle
Little, J. P., Safdar, A., Bishop, D., Tarnopolsky, M. A., & Gibala, M. J. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00538.2010 · Cited by 342 · see citing works
Regulation of exercise-induced fiber type transformation, mitochondrial biogenesis, and angiogenesis in skeletal muscle
Yan, Z., Okutsu, M., Akhtar, Y., & Lira, V. A. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00993.2010 · Cited by 338 · see citing works
Response of Skeletal Muscle Mitochondria to Hypoxia
Hoppeler, H. H., Vogt, M., Weibel, E. R., & Flück, M. (2003) · Experimental Physiology · doi:10.1113/eph8802513 · Cited by 329 · see citing works
Transcription and replication of mitochondrial DNA
Clayton, D. A. (2000) · Human Reproduction · doi:10.1093/humrep/15.suppl_2.11 · Cited by 318 · see citing works
Identity of GABP with NRF-2, a multisubunit activator of cytochrome oxidase expression, reveals a cellular role for an ETS domain activator of viral promoters.Preprint
Virbasius, J. V., Virbasius, C.-M. A., & Scarpulla, R. C. (1993) · Genes & Development · doi:10.1101/gad.7.3.380 · Cited by 291 · see citing works
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
A role for the transcriptional coactivator PGC-1α in muscle refueling.
Wende, A. R., Schaeffer, P. J., Parker, G. J., Zechner, C., Han, D.-H., Chen, M. M., Hancock, C. R., Lehman, J. J., Huss, J. M., McClain, D. A., et al. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m707006200 · Cited by 257 · 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
Regulation of Mitochondrial Biogenesis by Thyroid Hormone
Weitzel, J. M., Iwen, K. A., & Seitz, H. J. (2003) · Experimental Physiology · doi:10.1113/eph8802506 · Cited by 218 · see citing works
Regulation by exercise of skeletal muscle content of mitochondria and GLUT4.
Holloszy, J. O. (2008) · PubMed · Cited by 202 · see citing works
Matched work high-intensity interval and continuous running induce similar increases in PGC-1α mRNA, AMPK, p38, and p53 phosphorylation in human skeletal muscle
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
Effects of systemic hypoxia on human muscular adaptations to resistance exercise training
Kon, M., Ohiwa, N., Honda, A., Matsubayashi, T., Ikeda, T., Akimoto, T., Suzuki, Y., Hirano, Y., & Russell, A. P. (2014) · Physiological Reports · doi:10.14814/phy2.12033 · Cited by 161 · 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 · cited 5× · see citing works
“Collectively, these results support the involvement of the PGC-1α–NRF1/2 pathway in the coordinated induction of nuclear- and mitochondrial-encoded gene transcription.”
Influential
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
Overexpression of peroxisome proliferator-activated receptor γ coactivator-1α down-regulates GLUT4 mRNA in skeletal muscles.
Miura, S., Kai, Y., Ono, M., & Ezaki, O. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m304312200 · Cited by 146 · see citing works
Acute exercise induces tumour suppressor protein p53 translocation to the mitochondria and promotes a p53–Tfam–mitochondrial DNA complex in skeletal muscle
Saleem, A., & Hood, D. A. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2013.252791 · Cited by 141 · see citing works
Influence of aerobic exercise intensity on myofibrillar and mitochondrial protein synthesis in young men during early and late postexercise recovery
Donato, D. M. D., West, D. W. D., Churchward‐Venne, T. A., Breen, L., Baker, S. K., & Phillips, S. M. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00487.2013 · Cited by 141 · see citing works
The Relationship between Muscle Fiber Type-Specific PGC-1α Content and Mitochondrial Content Varies between Rodent Models and Humans
Gouspillou, G., Sgarioto, N., Norris, B. A., Barbat‐Artigas, S., Aubertin‐Leheudre, M., Morais, J. A., Burelle, Y., Taivassalo, T., & Hepple, R. T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103044 · Cited by 133 · 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
Are exercise‐induced genes induced by exercise?
Vissing, K., Andersen, J. L., & Schjerling, P. (2004) · The FASEB Journal · doi:10.1096/fj.04-2084fje · Cited by 118 · see citing works
Nuclear transcription factors in mammalian mitochondria
Leigh-Brown, S., Enrı́quez, J. A., & Odom, D. T. (2010) · Genome biology · doi:10.1186/gb-2010-11-7-215 · Cited by 116 · see citing works
Dissociation of Increases in PGC-1α and Its Regulators from Exercise Intensity and Muscle Activation Following Acute Exercise
Edgett, B. A., Foster, W. S., Hankinson, P. B., Simpson, C. A., Little, J. P., Graham, R. B., & Gurd, B. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071623 · Cited by 107 · see citing works
Mechanisms of Exercise‐Induced Mitochondrial Biogenesis in Skeletal Muscle: Implications for Health and Disease
Hood, D. A., Uguccioni, G., Vainshtein, A., & D’Souza, D. M. (2011) · Comprehensive physiology · doi:10.1002/cphy.c100074 · Cited by 101 · see citing works
Defects in energy homeostasis in Leigh syndrome French Canadian variant through PGC-1α/LRP130 complexPreprint
Cooper, M. P., Qu, L., Rohas, L. M., Lin, J. D., Yang, W., Erdjument‐Bromage, H., Tempst, P., & Spiegelman, B. M. (2006) · Genes & Development · doi:10.1101/gad.1483906 · Cited by 100 · 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
PPARβ Is Essential for Maintaining Normal Levels of PGC-1α and Mitochondria and for the Increase in Muscle Mitochondria Induced by Exercise
Koh, J., Hancock, C. R., Terada, S., Higashida, K., Holloszy, J. O., & Han, D.-H. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.04.029 · Cited by 95 · see citing works
Mitochondrial and Nuclear Genomic Responses to Loss of LRPPRC Expression
Gohil, V. M., Nilsson, R., Belcher-Timme, C. A., Luo, B., Root, D. E., & Mootha, V. K. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.098400 · Cited by 91 · see citing works
Sprint-interval but not continuous exercise increases PGC-1α protein content and p53 phosphorylation in nuclear fractions of human skeletal muscle
Granata, C., Oliveira, R. S. F., Little, J. P., Renner, K., & Bishop, D. J. (2017) · Scientific Reports · doi:10.1038/srep44227 · Cited by 78 · see citing works
Successive bouts of cycling stimulates genes associated with mitochondrial biogenesis
Dumke, C. L., Davis, J. M., Murphy, E. A., Nieman, D. C., Carmichael, M. D., Quindry, J. C., Triplett, N. T., Utter, A. C., Gross, S. J., Henson, D. A., et al. (2009) · European Journal of Applied Physiology · doi:10.1007/s00421-009-1143-1 · Cited by 72 · see citing works
Short-Term Intensified Cycle Training Alters Acute and Chronic Responses of PGC1α and Cytochrome C Oxidase IV to Exercise in Human Skeletal Muscle
Stepto, N., Benziane, B., Wadley, G., Chibalin, A., Canny, B., Eynon, N., & McConell, G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0053080 · Cited by 68 · see citing works
Multiple signaling pathways regulate contractile activity-mediated PGC-1 α gene expression and activity in skeletal muscle cells
Zhang, Y., Uguccioni, G., Ljubicic, V., Irrcher, I., Iqbal, S., Singh, K., Ding, S., & Hood, D. A. (2014) · Physiological Reports · doi:10.14814/phy2.12008 · Cited by 68 · 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
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
PGC-1 isoforms and their target genes are expressed differently in human skeletal muscle following resistance and endurance exercise
Silvennoinen, M., Ahtiainen, J. P., Hulmi, J. J., Pekkala, S., Taipale, R. S., Nindl, B. C., Laine, T., Häkkinen, K., Selänne, H., Kyröläinen, H., et al. (2015) · Physiological Reports · doi:10.14814/phy2.12563 · Cited by 64 · 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
Modulation of PGC-1 Coactivator Pathways in Brown Fat Differentiation through LRP130
Cooper, M. P., Uldry, M., Kajimura, S., Arany, Z. P., & Spiegelman, B. M. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m805431200 · Cited by 57 · see citing works
LRP130 Protein Remodels Mitochondria and Stimulates Fatty Acid Oxidation
Liu, L., Sanosaka, M., Shi, L., Bestwick, M. L., Frey, J. H., Surovtseva, Y. V., Shadel, G. S., & Cooper, M. P. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.276121 · Cited by 54 · see citing works
Modular Evolution of PGC-1α in Vertebrates
LeMoine, C. M. R., Lougheed, S. C., & Moyes, C. D. (2010) · Journal of Molecular Evolution · doi:10.1007/s00239-010-9347-x · Cited by 51 · 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
Effects of age and unaccustomed resistance exercise on mitochondrial transcript and protein abundance in skeletal muscle of men
Ogborn, D. I., McKay, B. R., Crane, J. D., Safdar, A., Akhtar, M., Parise, G., & Tarnopolsky, M. A. (2015) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00005.2014 · Cited by 49 · see citing works
Effect of chronic contractile activity on mRNA stability in skeletal muscle
Lai, R. Y. J., Ljubicic, V., D’Souza, D. M., & Hood, D. A. (2010) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00523.2009 · Cited by 49 · see citing works
Repeated Sprints Alter Signaling Related to Mitochondrial Biogenesis in Humans
Serpiello, F. R., McKenna, M. J., Bishop, D. J., Aughey, R. J., Caldow, M. K., Cameron‐Smith, D., & Stepto, N. K. (2011) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318240067e · Cited by 48 · see citing works
Similar Expression of Oxidative Genes after Interval and Continuous Exercise
Wang, L., Psilander, N., Tonkonogi, M., Ding, S., & Sahlin, K. (2009) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181abc1ec · Cited by 45 · see citing works
Rapidly elevated levels of PGC-1α-b protein in human skeletal muscle after exercise: exploring regulatory factors in a randomized controlled trial
Gidlund, E., Ydfors, M., Appel, S., Rundqvist, H., Sundberg, C. J., & Norrbom, J. (2015) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01000.2014 · Cited by 44 · see citing works
Acute Endurance Exercise Induces Nuclear p53 Abundance in Human Skeletal Muscle
Tachtsis, B., Smiles, W. J., Lane, S. C., Hawley, J. A., & CAMERA, D. M. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00144 · Cited by 44 · see citing works
AMP‐activated protein kinase is required for exercise‐induced peroxisome proliferator‐activated receptor γ co‐activator 1α translocation to subsarcolemmal mitochondria in skeletal muscle
Smith, B. K., Mukai, K., Lally, J., Maher, A. C., Gurd, B. J., Heigenhauser, G. J. F., Spriet, L. L., & Holloway, G. P. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2012.245944 · Cited by 43 · see citing works
An Assessment of Antimicrobial Resistant Disease Threats in Canada
Garner, M. J., Carson, C. A., Lingohr, E. J., Fazil, A., Edge, V. L., & Waddell, J. T. (2015) · PLoS ONE · doi:10.1371/journal.pone.0125155 · Cited by 42 · see citing works
The effect of acute and chronic sprint-interval training on LRP130, SIRT3, and PGC-1α expression in human skeletal muscle
Edgett, B. A., Bonafiglia, J. T., Baechler, B. L., Quadrilatero, J., & Gurd, B. J. (2016) · Physiological Reports · doi:10.14814/phy2.12879 · Cited by 41 · see citing works
Effect of sex on the acute skeletal muscle response to sprint interval exercise
Skelly, L. E., Gillen, J. B., MacInnis, M. J., Martin, B. J., Safdar, A., Akhtar, M., MacDonald, M. J., Tarnopolsky, M. A., & Gibala, M. J. (2017) · Experimental Physiology · doi:10.1113/ep086118 · Cited by 39 · see citing works
The effect of continuous and interval exercise on PGC‐1α and PDK4 mRNA in type I and type II fibres of human skeletal muscle
Wang, L., & Sahlin, K. (2011) · Acta Physiologica · doi:10.1111/j.1748-1716.2011.02354.x · Cited by 38 · see citing works
Carbohydrate restricted recovery from long term endurance exercise does not affect gene responses involved in mitochondrial biogenesis in highly trained athletes
Jensen, L., Gejl, K. D., Ørtenblad, N., Nielsen, J. L., Bech, R. D., Nygaard, T., Sahlin, K., & Frandsen, U. (2015) · Physiological Reports · doi:10.14814/phy2.12184 · Cited by 38 · see citing works
Erratum to: 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/s00421-010-1581-9 · Cited by 37 · see citing works
Adult expression of PGC-1α and -1β in skeletal muscle is not required for endurance exercise-induced enhancement of exercise capacity
Ballmann, C. G., Tang, Y., Bush, Z. D., & Rowe, G. C. (2016) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00209.2016 · Cited by 35 · see citing works
Impact of adrenaline and metabolic stress on exercise‐induced intracellular signaling and PGC‐1α mRNA response in human skeletal muscle
Brandt, N., Gunnarsson, T. P., Hostrup, M., Tybirk, J., Nybo, L., Pilegaard, H., & Bangsbo, J. (2016) · Physiological Reports · doi:10.14814/phy2.12844 · Cited by 31 · see citing works
Transcriptional control, but not subcellular location, of PGC-1α is altered following exercise in a hot environment
Heesch, M., Shute, R. J., Kreiling, J. L., & Slivka, D. R. (2016) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01065.2015 · Cited by 27 · see citing works
Acute exercise induces biphasic increase in respiratory mRNA in skeletal muscle
Ikeda, S., Kizaki, T., Haga, S., Ohno, H., & Takemasa, T. (2008) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2008.01.095 · Cited by 26 · see citing works
Acute upregulation of PGC-1α mRNA correlates with training-induced increases in SDH activity in human skeletal muscle
Bonafiglia, J. T., Edgett, B. A., Baechler, B. L., Nelms, M. W., Simpson, C. A., Quadrilatero, J., & Gurd, B. J. (2017) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2016-0463 · Cited by 25 · see citing works
Role of Nuclear Receptors in Exercise-Induced Muscle AdaptationsPreprint
Kupr, B., Schnyder, S., & Handschin, C. (2017) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a029835 · Cited by 22 · see citing works
Ammonium Chloride Ingestion Attenuates Exercise-Induced mRNA Levels in Human Muscle
Edge, J., Mündel, T., Pilegaard, H., Hawke, E. J., Leikis, M. J., Lopez-Villalobos, N., Oliveira, R. S. F., & Bishop, D. J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0141317 · Cited by 20 · see citing works
A systematic upregulation of nuclear and mitochondrial genes is not present in the initial postexercise recovery period in human skeletal muscle
Scribbans, T. D., Edgett, B. A., Bonafiglia, J. T., Baechler, B. L., Quadrilatero, J., & Gurd, B. J. (2017) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2016-0455 · Cited by 20 · see citing works
Effects of continuous and intermittent aerobic exercise upon mRNA expression of metabolic genes in human skeletal muscle.
Викторович, П. Д., Zinovkin, R. A., Karger, E. M., Tarasova, O. S., & Виноградова, О. Л. (2014) · PubMed · Cited by 18 · see citing works
Effect of Maternal Steroid on Developing Diaphragm Integrity
Song, Y., Demmer, D. L., Pinniger, G. J., Lavin, T., MacMillan, M. V., Pillow, J. J., & Bakker, A. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093224 · Cited by 12 · see citing works
The effect of single aerobic exercise on the regulation of mitochondrial biogenesis in skeletal muscles of trained men: A time-course study
Викторович, П. Д., Lysenko, E. A., Miller, T. F., Bachinin, A. V., Perfilov, D. V., & Виноградова, О. Л. (2015) · Human Physiology · doi:10.1134/s0362119715030123 · Cited by 9 · see citing works
Ingesting a Combined Carbohydrate and Essential Amino Acid Supplement Compared to a Non-Nutritive Placebo Blunts Mitochondrial Biogenesis-Related Gene Expression after Aerobic Exercise
Margolis, L. M., Murphy, N. E., Carrigan, C. T., McClung, H. L., & Pasiakos, S. M. (2017) · Current Developments in Nutrition · doi:10.3945/cdn.117.000893 · Cited by 6 · see citing works

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Mitochondrial dysfunction in metabolic syndrome
Prasun, P. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2020.165838 · Cited by 375 · 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
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
Mitochondrial Dysfunction Plays Central Role in Nonalcoholic Fatty Liver Disease
Ramanathan, R., Ali, A. H., & Ibdah, J. A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23137280 · Cited by 179 · see citing works
Mitochondrial dysfunction in nonalcoholic fatty liver disease and alcohol related liver disease
Prasun, P., Ginevic, I., & Oishi, K. (2020) · Translational Gastroenterology and Hepatology · doi:10.21037/tgh-20-125 · Cited by 137 · see citing works
High intensity interval training and molecular adaptive response of skeletal muscle
Torma, F., Gombos, Z., Jokai, M., Takeda, M., Mimura, T., & Radak, Z. (2019) · Sports Medicine and Health Science · doi:10.1016/j.smhs.2019.08.003 · Cited by 95 · see citing works
Transcriptional co-activators: emerging roles in signaling pathways and potential therapeutic targets for diseases
Talukdar, P. D., & Chatterji, U. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01651-w · Cited by 96 · see citing works
Human Skeletal Muscle Mitochondrial Adaptations Following Resistance Exercise Training
Parry, H. A., Roberts, M. D., & Kavazis, A. N. (2020) · International Journal of Sports Medicine · doi:10.1055/a-1121-7851 · Cited by 92 · see citing works
Circadian clock gene NPAS2 promotes reprogramming of glucose metabolism in hepatocellular carcinoma cells
Yuan, P., Yang, T., Mu, J., Zhao, J., Yang, Y., Yan, Z., Hou, Y., Chen, C., Xing, J., Zhang, H., et al. (2019) · Cancer Letters · doi:10.1016/j.canlet.2019.11.024 · Cited by 88 · see citing works
Lifelong Aerobic Exercise Alleviates Sarcopenia by Activating Autophagy and Inhibiting Protein Degradation via the AMPK/PGC-1α Signaling Pathway
Liang, J., Zhang, H., Zeng, Z., Wu, L., Zhang, Y., Guo, Y., Lv, J., Wang, C., Fan, J., & Chen, N. (2021) · Metabolites · doi:10.3390/metabo11050323 · Cited by 84 · see citing works
Baicalein resensitizes tamoxifen‐resistant breast cancer cells by reducing aerobic glycolysis and reversing mitochondrial dysfunction via inhibition of hypoxia‐inducible factor‐1α
Chen, Y., Zhang, J., Zhang, M., Song, Y., Zhang, Y., Fan, S., Ren, S., Fu, L., Zhang, N., Hui, H., et al. (2021) · Clinical and Translational Medicine · doi:10.1002/ctm2.577 · Cited by 82 · see citing works
Effect of Interval Training on the Factors Influencing Maximal Oxygen Consumption: A Systematic Review and Meta-Analysis
Rosenblat, M. A., Granata, C., & Thomas, S. G. (2022) · Sports Medicine · doi:10.1007/s40279-021-01624-5 · Cited by 73 · see citing works
Research progress on the pharmacological effects of berberine targeting mitochondria
Fang, X., Wu, H., Wei, J., Miao, R., Zhang, Y., & Tian, J. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.982145 · Cited by 72 · see citing works
Fibroblast growth factor 19 alleviates palmitic acid-induced mitochondrial dysfunction and oxidative stress via the AMPK/PGC-1α pathway in skeletal muscle
Guo, A., Li, K., & Xiao, Q. (2020) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2020.04.002 · Cited by 66 · see citing works
The Potential of the Mediterranean Diet to Improve Mitochondrial Function in Experimental Models of Obesity and Metabolic Syndrome
Khalil, M., Shanmugam, H., Abdallah, H., JohnBritto, J. S., Galerati, I., Gómez‐Ambrosi, J., Frühbeck, G., & Portincasa, P. (2022) · Nutrients · doi:10.3390/nu14153112 · Cited by 66 · see citing works
Dietary Anthocyanins: A Review of the Exercise Performance Effects and Related Physiological Responses
Cook, M. D., & Willems, M. E. T. (2018) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2018-0088 · Cited by 64 · see citing works
Looking beyond PGC-1α: emerging regulators of exercise-induced skeletal muscle mitochondrial biogenesis and their activation by dietary compounds
Islam, H., Hood, D. A., & Gurd, B. J. (2019) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2019-0069 · Cited by 62 · see citing works
Preventive and Therapeutic Potential of Physical Exercise in Neurodegenerative Diseases
Marques‐Aleixo, I., Beleza, J., Sampaio, A., Stevanović, J., Coxito, P. M., Gonçalves, I. O., Ascensão, A. A. M. R., & Magalhães, J. (2020) · Antioxidants and Redox Signaling · doi:10.1089/ars.2020.8075 · Cited by 62 · see citing works
Metformin and Vascular Diseases: A Focused Review on Smooth Muscle Cell Function
Deng, M., Su, D., Xu, S., Little, P. J., Feng, X., Tang, L., & Shen, A. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.00635 · Cited by 58 · see citing works
Mechanism of PGC-1α-mediated mitochondrial biogenesis in cerebral ischemia–reperfusion injury
Yuan, Y., Tian, Y., Jiang, H., Cai, L.-Y., Song, J., Peng, R., & Zhang, X.-M. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1224964 · Cited by 57 · see citing works
Exercise twice‐a‐day potentiates markers of mitochondrial biogenesis in men
Andrade‐Souza, V. A., Ghiarone, T., Sansonio, A., Silva, K. A. S., Tomazini, F., Arcoverde, L., Fyfe, J. J., Perri, E., Saner, N. J., Kuang, J., et al. (2019) · The FASEB Journal · doi:10.1096/fj.201901207rr · Cited by 52 · see citing works
The role of chronic low-grade inflammation in the development of sarcopenia: Advances in molecular mechanisms
Cheng, Y., Lin, S., Cao, Z., Yu, R., Fan, Y., & Chen, J. (2025) · International Immunopharmacology · doi:10.1016/j.intimp.2025.114056 · Cited by 49 · see citing works
Resistin destroys mitochondrial biogenesis by inhibiting the PGC-1α/ NRF1/TFAM signaling pathway
Chen, Z., Tao, S., Li, X., & Yao, Q. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.08.027 · Cited by 45 · 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
Oxidative stress and metabolism meet epigenetic modulation in physical exercise
García‐Giménez, J. L., Cánovas‐Cervera, I., & Pallardó, F. V. (2024) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2024.01.008 · Cited by 49 · see citing works
BPDE and B[a]P induce mitochondrial compromise by ROS-mediated suppression of the SIRT1/TERT/PGC-1α pathway in spermatogenic cells both in vitro and in vivo
Wang, Y., Zhang, G., Jiang, F., Zeng, Y., Zou, P., An, H., Chen, Q., Ling, X., Han, F., Liu, W., et al. (2019) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2019.05.004 · Cited by 44 · see citing works
Investigation of mitochondrial biogenesis defects in single substantia nigra neurons using post-mortem human tissues
Chen, C., Vincent, A. E., Blain, A. P., Smith, A. L., Turnbull, D. M., & Reeve, A. K. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104631 · Cited by 43 · see citing works
The impact of acute and chronic exercise on Nrf2 expression in relation to markers of mitochondrial biogenesis in human skeletal muscle
Islam, H., Bonafiglia, J. T., Turnbull, P. C., Simpson, C. A., Perry, C. G. R., & Gurd, B. J. (2019) · European Journal of Applied Physiology · doi:10.1007/s00421-019-04259-7 · Cited by 39 · see citing works
Effects of Pyrroloquinoline Quinone (PQQ) Supplementation on Aerobic Exercise Performance and Indices of Mitochondrial Biogenesis in Untrained Men
Hwang, P. S., Machek, S. B., Cardaci, T. D., Wilburn, D. T., Kim, C. S., Suezaki, E. S., & Willoughby, D. S. (2019) · Journal of the American College of Nutrition · doi:10.1080/07315724.2019.1705203 · Cited by 37 · see citing works
Repeatability of exercise‐induced changes in mRNA expression and technical considerations for qPCR analysis in human skeletal muscle
Islam, H., Edgett, B. A., Bonafiglia, J. T., Shulman, T., Ma, A., Quadrilatero, J., Simpson, C. A., & Gurd, B. J. (2019) · Experimental Physiology · doi:10.1113/ep087401 · Cited by 38 · see citing works
Red ginseng extract improves skeletal muscle energy metabolism and mitochondrial function in chronic fatigue mice
Zhang, H., Zhao, C., Hou, J., Su, P., Yang, Y., Xia, B., Zhao, X., He, R., Wang, L., Cao, C., et al. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.1077249 · Cited by 37 · see citing works
Role of the gut–muscle axis in mitochondrial function of ageing muscle under different exercise modes
Xie, X., & Huang, C. X. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102316 · Cited by 37 · see citing works
Cast immobilization of hindlimb upregulates sarcolipin expression in atrophied skeletal muscles and increases thermogenesis in C57BL/6J mice
Tomiya, S., Tamura, Y., Kouzaki, K., Kotani, T., Wakabayashi, Y., Noda, M., & Nakazato, K. (2019) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00118.2019 · Cited by 35 · see citing works
Molecular regulation of skeletal muscle mass and the contribution of nitric oxide: A review
Kobayashi, J., Uchida, H., Kofuji, A., Ito, J., Shimizu, M., Kim, H., Sekiguchi, Y., & Kushibe, S. (2019) · FASEB BioAdvances · doi:10.1096/fba.2018-00080 · Cited by 36 · see citing works
Dihydromyricetin Protects Against Gentamicin-Induced Ototoxicity via PGC-1α/SIRT3 Signaling in vitro
Han, H., Dong, Y., & Ma, X. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00702 · Cited by 34 · see citing works
Mitochondrial Quality Control: the Role in Cardiac Injury
Sygitowicz, G., & Sitkiewicz, D. (2022) · Frontiers in Bioscience-Landmark · doi:10.31083/j.fbl2703096 · Cited by 34 · see citing works
Impact of Different Training Modalities on Molecular Alterations in Skeletal Muscle of Patients With Heart Failure With Preserved Ejection Fraction: A Substudy of the OptimEx Trial
Winzer, E. B., Augstein, A., Schauer, A., Mueller, S., Fischer-Schaepmann, T., Goto, K., Hommel, J., Craenenbroeck, E. M. V., Wisløff, U., Pieske, B. M., et al. (2022) · Circulation Heart Failure · doi:10.1161/circheartfailure.121.009124 · Cited by 34 · see citing works
Effect of aerobic training on baseline expression of signaling and respiratory proteins in human skeletal muscle
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
Roles of NPAS2 in circadian rhythm and disease
Peng, L., Bai, G., & Pang, Y. (2021) · Acta Biochimica et Biophysica Sinica · doi:10.1093/abbs/gmab105 · Cited by 31 · see citing works
Impacts of altered exercise volume, intensity, and duration on the activation of AMPK and CaMKII and increases in PGC-1α mRNA
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Change in Central Cardiovascular Function in Response to Intense Interval Training: A Systematic Review and Meta-analysis
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Energy, Entropy and Quantum Tunneling of Protons and Electrons in Brain Mitochondria: Relation to Mitochondrial Impairment in Aging-Related Human Brain Diseases and Therapeutic Measures
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Muscular Changes in Animal Models of Heart Failure with Preserved Ejection Fraction: What Comes Closest to the Patient?
Goto, K., Schauer, A., Augstein, A., Methawasin, M., Granzier, H. L. M., Halle, M., Craenenbroeck, E. M. V., Rolim, N. P. L., Gielen, S., Pieske, B. M., et al. (2020) · ESC Heart Failure · doi:10.1002/ehf2.13142 · Cited by 25 · see citing works
Muscle strength after resistance training correlates to mediators of muscle mass and mitochondrial respiration in middle-aged adults
McKenna, C. F., Salvador, A. F., Keeble, A. R., Khan, N. A., Lisio, M. D., Konopka, A. R., Paluska, S. A., & Burd, N. A. (2022) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00186.2022 · Cited by 26 · see citing works
Activation of TGR5 promotes mitochondrial biogenesis in human aortic endothelial cells
Zhao, L., & Zhang, S.-F. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.04.210 · Cited by 24 · see citing works
Bufei Jianpi Formula Improves Mitochondrial Function and Suppresses Mitophagy in Skeletal Muscle via the Adenosine Monophosphate-Activated Protein Kinase Pathway in Chronic Obstructive Pulmonary Disease
Mao, J., Li, Y., Feng, S., Liu, X., Tian, Y., Bian, Q., Li, J., Hu, Y., Zhang, L., Ji, H., et al. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.587176 · Cited by 24 · see citing works
Baicalin Promotes Skeletal Muscle Fiber Remodeling by Activating the p38MAPK/PGC-1α Signaling Pathway
Wang, T., Sun, X., Zhang, Y., Wang, Q., Cheng, W., Gao, Y., Shi, X., & Jin, J. (2025) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.5c00300 · Cited by 21 · see citing works
Melatonin Potentiates Exercise-Induced Increases in Skeletal Muscle PGC-1α and Optimizes Glycogen Replenishment
Faria, V. S., Manchado-Gobatto, F. D. B., Scariot, P. P. M., Zagatto, A. M., & Beck, W. R. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.803126 · Cited by 20 · see citing works
Primary defects in lipid handling and resistance to exercise in myotubes from obese donors with and without type 2 diabetes
Løvsletten, N. G., Rustan, A. C., Laurens, C., Thoresen, G. H., Moro, C., & Nikolić, N. (2019) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2019-0265 · Cited by 19 · see citing works
Interleukin 15: A new intermediary in the effects of exercise and training on skeletal muscle and bone function
Duan, Z., Yang, Y., Qin, M., & Yi, X. (2024) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.70136 · Cited by 19 · see citing works
High phosphate impairs arterial endothelial function through AMPK‐related pathways in mouse resistance arteries
Hu, W., Jiang, S., Liao, Y., Li, J., Dong, F., Guo, J. Z., Wang, X., Fei, L., Cui, Y., Ren, X., et al. (2020) · Acta Physiologica · doi:10.1111/apha.13595 · Cited by 17 · see citing works
Molecular regulation of skeletal muscle mitochondrial biogenesis following blood flow-restricted aerobic exercise: a call to action
Preobrazenski, N., Islam, H., & Gurd, B. J. (2021) · European Journal of Applied Physiology · doi:10.1007/s00421-021-04669-6 · Cited by 17 · see citing works
Metformin induces M2 polarization via AMPK/PGC-1α/PPAR-γ pathway to improve peripheral nerve regeneration.
Zhou, Z., Luo, G., Li, C., Zhang, P., Chen, W., Li, X., Tang, J., & Qing, L. (2023) · PubMed Central · Cited by 17 · see citing works
Activation of CB1R-Dependent PGC-1α Is Involved in the Improved Mitochondrial Biogenesis Induced by Electroacupuncture Pretreatment
Sun, S., Jiang, T., Duan, N., Wu, M., Yan, C., Li, Y., Cai, M., & Wang, Q. (2020) · Rejuvenation Research · doi:10.1089/rej.2020.2315 · Cited by 16 · see citing works
Regulation of PGC-1α of the Mitochondrial Energy Metabolism Pathway in the Gills of Indian Medaka (Oryzias dancena) under Hypothermal Stress
Ranasinghe, N., Chen, W., Hu, Y.-C., Gamage, L., Lee, T., & Ho, C. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242216187 · Cited by 16 · see citing works
NAD+ Therapeutics and Skeletal Muscle Adaptation to Exercise in Humans
Campelj, D. G., & Philp, A. (2022) · Sports Medicine · doi:10.1007/s40279-022-01772-2 · Cited by 15 · see citing works
4-Octyl itaconate attenuates renal tubular injury in db/db mice by activating Nrf2 and promoting PGC-1α-mediated mitochondrial biogenesis
Shao, M., Chen, J., Zhang, F., Su, Q., Lin, X., Wang, W., Chen, C., Ren, H., Zheng, S., Hui, S., et al. (2024) · Renal Failure · doi:10.1080/0886022x.2024.2403653 · Cited by 14 · see citing works
KAP1-associated transcriptional inhibitory complex regulates C2C12 myoblasts differentiation and mitochondrial biogenesis via miR-133a repression
Zhang, J., Hua, C., Zhang, Y., Wei, P., Tu, Y., & Wei, T. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-02937-5 · Cited by 14 · see citing works
Repeatability of training-induced skeletal muscle adaptations in active young males
Islam, H., Bonafiglia, J. T., Giudice, M. D., Pathmarajan, R., Simpson, C. A., Quadrilatero, J., & Gurd, B. J. (2020) · Journal of science and medicine in sport · doi:10.1016/j.jsams.2020.10.016 · Cited by 14 · see citing works
Role of TRPV1 in High Temperature-Induced Mitochondrial Biogenesis in Skeletal Muscle: A Mini Review
Xu, Y., Zhao, Y., & Gao, B. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.882578 · Cited by 14 · see citing works
The Role of Mitochondria in Metabolic Syndrome–Associated Cardiomyopathy
Li, J., Li, J., Chen, Y., Hu, W., Gong, X., Qiu, H., Chen, H., Xin, Y., & Li, H. (2022) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2022/9196232 · Cited by 16 · see citing works
Ginsenoside Rf Enhances Exercise Endurance by Stimulating Myoblast Differentiation and Mitochondrial Biogenesis in C2C12 Myotubes and ICR Mice
Lim, W., Shin, E. J., Lim, T., Choi, J. W., Song, N., Hong, H., Cho, C., & Rhee, Y. K. (2022) · Foods · doi:10.3390/foods11121709 · Cited by 13 · see citing works
Impaired function of aorta and perivascular adipose tissue in IL-18-deficient mice
Li, W., Jin, D., Takai, S., Hayakawa, T., Ogata, J., Yamanishi, K., Yamanishi, H., & Okamura, H. (2019) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00813.2018 · Cited by 12 · see citing works
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Blagov, A. V., Kozlov, S. G., Blokhina, T., Sukhorukov, V. N., & Orekhov, A. N. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232314741 · Cited by 11 · see citing works
Effects of Diet and Exercise on Mitochondrial Health in Metabolic Dysfunction-Associated Steatotic Liver Disease (MASLD): Role of Ceramides
McCaffrey, J. M., & Ibdah, J. A. (2025) · Nutrients · doi:10.3390/nu17182972 · Cited by 12 · see citing works
Sex Differences in the Skeletal Muscle Response to a High Fat, High Sucrose Diet in Rats
Hulett, N. A., Knaub, L. A., Hull, S., Pott, G. B., Peelor, R., Miller, B. F., Shankar, K., Rudolph, M. C., Reusch, J. E. B., & Scalzo, R. L. (2023) · Nutrients · doi:10.3390/nu15204438 · Cited by 10 · see citing works
Mitochondrial Dysfunction in Glycogen Storage Disorders (GSDs)
Mishra, K., & Kakhlon, O. (2024) · Biomolecules · doi:10.3390/biom14091096 · Cited by 10 · see citing works
Applying exercise-mimetic engineered skeletal muscle model to interrogate the adaptive response of irisin to mechanical force
Zhang, Y., Wang, L., Kang, H., Lin, C.-Y. J., & Fan, Y. (2022) · iScience · doi:10.1016/j.isci.2022.104135 · Cited by 10 · see citing works
Effects of exercise-induced metabolic and mechanical loading on skeletal muscle mitochondrial function in male rats
Touron, J., Perrault, H., Maisonnave, L., Patrac, V., Walrand, S., Malpuech‐Brugère, C., Pereira, B., Burelle, Y., Costes, F., & Richard, R. (2022) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00719.2021 · Cited by 10 · see citing works
Therapeutic modulation of mitochondrial dynamics by agmatine in neurodegenerative disorders
Nibrad, D., Shiwal, A., Tadas, M., Katariya, R., Kale, M. B., Kotagale, N. R., Umekar, M. J., & Taksande, B. G. (2025) · Neuroscience · doi:10.1016/j.neuroscience.2025.01.061 · Cited by 7 · see citing works
Global Trends in Research of Mitochondrial Biogenesis over past 20 Years: A Bibliometric Analysis
Song, L., Liang, J., Wang, W., Gao, J., Chai, H., Tan, Y. T., Zheng, L., Xue, M., & Shi, D. (2023) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2023/7291284 · Cited by 7 · see citing works
Taming fatty liver: can taurine combat metabolic dysfunction in MASLD?
Meng, L., Lu, F., Zhang, B., Ma, Y., & Gao, J. (2025) · Cell Communication and Signaling · doi:10.1186/s12964-025-02439-x · Cited by 6 · see citing works
Fiber-specific and whole-muscle LRP130 expression in rested, exercised, and fasted human skeletal muscle
Islam, H., Ma, A., Amato, A., Cuillerier, A., Burelle, Y., Simpson, C. A., Quadrilatero, J., & Gurd, B. J. (2020) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-020-02359-4 · Cited by 6 · see citing works
The Effect of Training on Skeletal Muscle and Exercise Metabolism
MacInnis, M. J., Egan, B., & Gibala, M. J. (2022) · Physiology in health and disease · doi:10.1007/978-3-030-94305-9_10 · Cited by 6 · see citing works
Guilu Erxian Jiao enhances protein synthesis, glucose homeostasis, mitochondrial biogenesis and slow-twitch fibers in the skeletal muscle
Fang, W.-Y., Chang, W., Tsai, Y., Hsu, H., Chang, F., Lin, C., & Lo, Y. (2023) · Journal of Food and Drug Analysis · doi:10.38212/2224-6614.3435 · Cited by 4 · see citing works
Enhanced Mitochondrial Dynamics and Reactive Oxygen Species Levels with Reduced Antioxidant Defenses in Human Epicardial Adipose Tissue
Burgeiro, A., Santos, D., Fonseca, A. C. R. G., Baldeiras, I., Leal, E. C., Moura, J., Costa-Nunes, J., Seraphim, P. M., Pinho, A. C. O., Canotilho, A., et al. (2025) · Metabolites · doi:10.3390/metabo15070481 · Cited by 3 · see citing works
Some aspects of the influence of extreme climatic factors on the physical performance of athletes
Kobelkova, I. V., Korosteleva, M. M., & Nikityuk, D. B. (2022) · Sports medicine research and practice · doi:10.47529/2223-2524.2022.1.5 · Cited by 3 · see citing works
Mitochondrial biogenesis microcarriers break membrane barriers for endogenous nucleus pulposus repair
Li, X., Chang, H., Pang, L., Li, A., Wang, J., Yu, Y., Xiao, H., Cai, Z., Cui, W., & Liu, X. (2025) · Chemical Engineering Journal · doi:10.1016/j.cej.2025.160668 · Cited by 2 · see citing works
Celastrol induces cardiotoxicity by directly targeting AMOTL2 and inhibiting YAP1/PGC-1α/TFAM-dependent mitochondrial biogenesis
Shang, H., Cheng, H., Wei, Z., Tang, X., Han, W., Zhang, X., Xiao, C., Gao, Y., Liu, X., & Gao, Y. (2025) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2025.111885 · Cited by 2 · see citing works
The effect of 12-week aerobic trainings on mitochondrial biogenesis indicators in skeletal muscle among male rats
hashemkandi, R., Arshadi, S., Banaeifar, A., & Hajirasouli, M. (2020) · Medical Journal of Tabriz University of Medical Sciences and Health Services · doi:10.34172/mj.2020.055 · Cited by 2 · see citing works
Metabolism
Saghiv, M. S., & Sagiv, M. S. (2020) · Springer eBooks · doi:10.1007/978-3-030-48806-2_2 · Cited by 2 · see citing works
Adaptations métaboliques en réponse à l'exercice excentrique dynamique : application au réentrainement.
Touron, J. (2020) · doi:10.70675/2eb176cbzcab7z45ffzad4dz1b023ed7405d · Cited by 2 · see citing works
Downregulation of HSPA12A underlies myotoxicity of local anesthetic agent bupivacaine through inhibiting PGC1α-mediated mitochondrial integrity
Mao, Q., Yu, W., Liu, S., Cao, X., Dai, Y., Zhang, X., Min, X., Liu, L., & Ding, Z. (2021) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2021.115798 · Cited by 1 · see citing works
Inhibition of TWEAK/Fn14 Ameliorates Sarcopenic Obesity by Restoring Mitochondrial Biogenesis via the AMPK/SIRT1/PGC-1α Axis
Xuekelati, S., Maimaitiwusiman, Z., Guo, Y., Guo, S., Xu, Q., Ke, J., Xu, L., Yang, Y., & Wang, H. B. (2026) · Diabetes Metabolic Syndrome and Obesity · doi:10.2147/dmso.s596507 · Cited by 1 · see citing works
Renoprotective actions of puerarin and the prospects of kidney-targeted nanodelivery
Huang, Y., Zheng, J., Jin, F., Li, J., Lian, M., Chen, T., Jiang, M., Chen, H., Cao, Y., Atanasov, A. G., et al. (2026) · Frontiers in Pharmacology · doi:10.3389/fphar.2026.1896730 · Cited by 1 · see citing works
Mitochondrial DNA in systemic lupus erythematosus: pathogenic mechanisms, clinical biomarkers, and precision therapeutic strategies
Huang, F., Sun, K., Diao, L., Lu, K., Fan, Y., & Xie, G. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1928003 · Cited by 1 · see citing works
Oral administration of glutathione modulates exercise-related metabolic and oxidative factors in skeletal muscles of mice
Aoi, W., & Sato, K. (2024) · Advances in Redox Research · doi:10.1016/j.arres.2024.100104 · Cited by 1 · see citing works
The Effect of a Detraining After Resistance Training on the Histochemical Expression of Potassium Channels and Mitochondrial Biogenesis of Heart Tissue in Male Rats
Ahmadi, F., Siahkouhian, M., Mirdar, S., & Tapak, L. (2021) · Quarterly of Horizon of Medical Sciences · doi:10.32598/hms.27.2.3361.1
Prospective Advances in Exercise-Induced Autophagy on Health
Liang, J., Kirberger, M., & Chen, N. (2021) · Springer eBooks · doi:10.1007/978-981-16-4525-9_11
Peer Review #2 of "Interpretation of exercise-induced changes in human skeletal muscle mRNA expression depends on the timing of the post-exercise biopsies (v0.2)"
(2022) · PeerJ · doi:10.7287/peerj.12856v0.2/reviews/2
Peer Review #1 of "Interpretation of exercise-induced changes in human skeletal muscle mRNA expression depends on the timing of the post-exercise biopsies (v0.1)"
(2022) · PeerJ · doi:10.7287/peerj.12856v0.1/reviews/1
Management and Modification of Flavonoids Against Nonalcoholic Fatty Liver Disease
Bai, W., Huang, B., Zhao, W., Liu, G., Yu, L., Lü, Z., & Wang, H. (2025) · Food Bioengineering · doi:10.1002/fbe2.70026
Novel variants in ryanodine receptor type 3 predispose to acute rhabdomyolysis due to impaired autophagyPreprint
de Calbiac, H., Caccavelli, L., Renault, S., Madrange, M., Raas, Q., Straube, M., Brochier, G., Lacène, E., Chanut, A., Madelaine, A., et al. (2026) · medRxiv · doi:10.64898/2026.02.27.26345848
Yeast β-glucan selenium nanoparticles enhance meat quality in heat-stressed broilers via SelO-mediated mitochondrial biogenesis and oxidative myofiber remodeling
Yang, W., Fang, C., Yang, J., Lv, J., Shang, G., Song, X., Tang, Y., Wu, S., & Fang, R. (2026) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-026-01437-4
Sleep-Gated Adaptation: A Conceptual Framework Linking Exercise-Induced Adaptive Consolidation to Interindividual Variability in Training Response
Dominteanu, T., Stan, A. E., & Voinea, A. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27198811
Exercise Regulates Mitochondrial Quality Control: Maintenance and Remodeling of Skeletal Muscle Homeostasis
Zhao, H., & Chen, M. (2026) · Biology · doi:10.3390/biology15151240
Decoding the bile acid–mitochondria axis: Implications for disease management and therapeutic opportunities
Jia, X., Zhang, Z., Lin, X., Dong, X., Chen, R., Liang, N., Ding, H., & Li, F. (2026) · Pharmacological Research · doi:10.1016/j.phrs.2026.108415
Mitochondrial Biogenesis in Human Skeletal Muscle: High-Intensity Interval Training Versus Moderate-Intensity Continuous Training
Bischof, K. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27219537

Exercise increases mitochondrial PGC-1 α content and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis.
Safdar, A., Little, J. P., Stokl, A., Hettinga, B. P., Akhtar, M., & Tarnopolsky, M. A. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ec118.002682 · Cited by 22 · see citing works
doi:10.1155/2010/937123 Review Article Regulation of PPARγ Coactivator-1α Function and Expression in Muscle: Effect of Exercise
Uguccioni, G., & Hood, D. A. (2010)
The molecular dissection of the regulation of PGC-1α and the genome-wide activity of its transcriptional network in skeletal muscle cells
Barešić, M. (2013) · edoc (University of Basel) · doi:10.5451/unibas-006214634
PGC-1α is Dispensable for Exercise-Induced Mitochondrial Biogenesis in Skeletal Muscle
Rowe, G. C., El‐Khoury, R., Patten, I. S., Rustin, P., & Arany, Z. P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041817 · Cited by 127 · 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

Authors: Islam, H., Edgett, B. A., & Gurd, B. J.
Affiliations: Queen's University (CA)
Corresponding author: Islam, Hashim
Edgett, Brittany A.
Gurd, Brendon J.
ORCID: Islam, Hashim
Edgett, Brittany A.
Gurd, Brendon J.
Venue: Metabolism
Publisher: Elsevier BV
Published: 2018-02
Volume: 79
Pages: 42-51
ISSN: 0026-0495 (ISSN-L)
DOI: 10.1016/j.metabol.2017.11.001
OpenAlex: W2767352135
Cited by: 99
References: 96
Citations by year: 2026: 9 · 2025: 9 · 2024: 6 · 2023: 8 · 2022: 24 · 2021: 8 · 2020: 17 · 2019: 13 · 2018: 5
FWCI: 1.17
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Metabolism (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Keywords: PGC-1α, mitochondrial biogenesis, skeletal muscle, physical activity, mitochondrial transcription, TFAM, nuclear genes, gene expression regulation, human skeletal muscle
MeSH terms: Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha, Humans, Mitochondria, Muscle, Exercise, Muscle, Skeletal

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Coordination of mitochondrial biogenesis by PGC-1α in human skeletal muscle: A re-evaluation

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