The DOI matches its Crossref record; 208 of the 210 references it cites were found in a registry or an index.
Exercise Metabolism and the Molecular Regulation of Skeletal Muscle Adaptation
Open accessAbstract
Preservation of aerobic fitness and skeletal muscle strength through exercise training can ameliorate metabolic dysfunction and prevent chronic disease. These benefits are mediated in part by extensive metabolic and molecular remodeling of skeletal muscle by exercise. Aerobic and resistance exercise represent extremes on the exercise continuum and elicit markedly different training responses that are mediated by a complex interplay between a myriad of signaling pathways coupled to downstream regulators of transcription and translation. Here, we review the metabolic responses and molecular mechanisms that underpin the adaptatation of skeletal muscle to acute exercise and exercise training.
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In the citing paper
“This is principally achieved by an augmentation in mitochondrial volume, FA transport and enzymatic adaptations (e.g., increase hydroacyl-CoA-dehydrogenase) to use fat, and a reduction of cell signals such as ADP and AMP during exercise at submaximal work rates thus reducing the activation of key enzymes (e.g., glycogen phosphorylase and pyruvate dehydrogenase) of carbohydrate metabolism [92,160].”
From Regulation of Energy Substrate Metabolism in Endurance Exercise (2021) · cites this paper as [160]
In the citing paper
“Exercise promotes glucose uptake and glycogen synthesis and increases insulin sensitivity, and this persists long after the cessation of exercise (1, 2).”
From Skeletal muscle NOX4 is required for adaptive responses that prevent insulin resistance (2021) · cites this paper as [2]
In the citing paper
“The induction of PGC1α (peroxisome proliferator–activated receptor gamma coactivator 1α) after exercise can promote mitochondrial biogenesis by driving the expression of nuclear- and mitochondrial-encoded genes.”
From Skeletal muscle NOX4 is required for adaptive responses that prevent insulin resistance (2021) · cites this paper as [2]
In the citing paper
“The enhanced skeletal muscle insulin sensitivity after exercise affords metabolic flexibility and a means for replenishing glycogen to deal with subsequent bouts of intense physical activity (1, 2).”
From Skeletal muscle NOX4 is required for adaptive responses that prevent insulin resistance (2021) · cites this paper as [2]
In the citing paper
“Exercise results in skeletal muscle exposure to acute stresses that stimulate compensatory and adaptive physiological responses (1, 2).”
From Skeletal muscle NOX4 is required for adaptive responses that prevent insulin resistance (2021) · cites this paper as [2]
In the citing paper
“These adaptive responses increase tolerance and protect against subsequent stressors and are considered important for the health-promoting effects of exercise (1, 2).”
From Skeletal muscle NOX4 is required for adaptive responses that prevent insulin resistance (2021) · cites this paper as [2]
In the citing paper
“In particular, PGC1α promotes the expression of NRF (nuclear respiratory factor)–1 and NRF-2, which induce the expression of nuclear-encoded genes, as well as TFAM (mitochondrial transcription factor A), which facilitates mitochondrial DNA transcription and replication (2, 3).”
From Skeletal muscle NOX4 is required for adaptive responses that prevent insulin resistance (2021) · cites this paper as [2]
In the citing paper
“A fundamental hormetic response to exercise is the induction of mitochondrial biogenesis, which serves to enhance respiratory capacity and endurance (2, 3).”
From Skeletal muscle NOX4 is required for adaptive responses that prevent insulin resistance (2021) · cites this paper as [2]
In the citing paper
“It is well established that contracting muscle generates ROS and that this is accompanied by increased antioxidant defense orchestrated by NFE2L2 (2, 7, 36).”
From Skeletal muscle NOX4 is required for adaptive responses that prevent insulin resistance (2021) · cites this paper as [2]
In the citing paper
“These observations confirm the hypothesis that endurance exercise training may affect a specific set of functions (e.g., oxidative metabolism and mitochondrial biogenesis) and overall muscle metabolism [93].”
From Role of Age-Related Mitochondrial Dysfunction in Sarcopenia (2020) · cites this paper as [93]
In the citing paper
“Multiple molecular pathways are activated by exercise and these pathways have been shown to contribute to the adaptive remodelling of skeletal muscle [1,2].”
From New strategies in sport nutrition to increase exercise performance (2016) · cites this paper as [2]
In the citing paper
“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 [2]
In the citing paper
“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 [2]
In the citing paper
“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 [2]
In the citing paper
“It is a key factor in metabolism of all major biomolecules (lipids, carbohydrates, amino acids) as well as ATP synthesis by the electron transport chain [164, 165]”
From Targeting Intramyocellular Lipids to Improve Aging Muscle Function (2025) · cites this paper as [165]
In the citing paper
“A higher mitochondrial volume density and improved mitochondrial quality can be seen as consequences of chronic activation of AMPK and expression induction of PGC1α, myocyte-specific enhancer factor 2 (MEF2), NRF-1 and NRF-2, and nuclear expulsion of histone deacetylase 4 and 5 (41, 222, 224).”
From Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease (2018) · cites this paper as [222]
In the citing paper
“Additionally, PGC1α is expressed upon muscle contraction-induced activation of p38 MAPK (222).”
From Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease (2018) · cites this paper as [222]
In the citing paper
“Both promote considerable health benefits such as increased mitochondrial content and improvements in glycemic control (222).”
From Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease (2018) · cites this paper as [222]
In the citing paper
“Acute AMPK activation reduces glycogen and protein synthesis while promoting glucose transport and FAO (222).”
From Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease (2018) · cites this paper as [222]
In the citing paper
“Because exercise and ApN share similar signaling pathways [75,76] and the potential of counteracting several facets of this metabolic syndrome, numerous studies attempted to establish relationships between exercise and ApN parameters.”
From Adiponectin and Its Mimics on Skeletal Muscle: Insulin Sensitizers, Fat Burners, Exercise Mimickers, Muscling Pills … or Everything Together? (2020) · cites this paper as [76]
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Raney, M. A., & Turcotte, L. P. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01282.2007 · Cited by 135
Mechano-transduction to muscle protein synthesis is modulated by FAK
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Myostatin inhibition induces muscle fibre hypertrophy prior to satellite cell activation
Wang, Q., & McPherron, A. C. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2011.226001 · Cited by 128
Gavin, T. P., Ruster, R. S., Carrithers, J. A., Zwetsloot, K. A., Kraus, R. M., Evans, C. A., Knapp, D. J., Drew, J. L., McCartney, J. S., Garry, J. P., et al. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.143198 · Cited by 126
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Bouzakri, K., Plomgaard, P., Berney, T., Donath, M. Y., Pedersen, B. K., & Halban, P. A. (2011) · Diabetes · doi:10.2337/db10-1178 · Cited by 122
Yu, M., Blomstrand, E., Chibalin, A., Krook, A., & Zierath, J. R. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.00273.x · Cited by 121
Self-citationDivergent cell signaling after short-term intensified endurance training in human skeletal muscle
Benziane, B., Burton, T. J., Scanlan, B., Galuska, D., Canny, B. J., Chibalin, A. V., Zierath, J. R., & Stepto, N. K. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90428.2008 · Cited by 119
Self-citationRegulatory mechanisms in the interaction between carbohydrate and lipid oxidation during exercise
Spriet, L. L., & Watt, M. J. (2003) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.2003.01152.x · Cited by 117
Koopman, R., MANDERS, R. J. F., Zorenc, A. H. G., Hul, G. B. J., Kuipers, H., KEIZER, H. A., & van Loon, L. J. C. (2005) · European Journal of Applied Physiology · doi:10.1007/s00421-004-1307-y · Cited by 110
Whitham, M., Chan, M. H. S., Pal, M., Matthews, V. B., Prelovsek, O., Lunke, S., El-Osta, A., Broenneke, H., Alber, J., Brüning, J. C., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.310581 · Cited by 107
Protein metabolism in rat gastrocnemius muscle after stimulated chronic concentric exercise
Wong, T., & Booth, F. W. (1990) · Journal of Applied Physiology · doi:10.1152/jappl.1990.69.5.1709 · Cited by 104
Banerjee, P., Caulfield, B., Crowe, L., & Clark, A. L. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00891.2004 · Cited by 103
Endurance training modulates the muscular transcriptome response to acute exercise
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Booth, F. W., & Laye, M. J. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.179507 · Cited by 99
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Self-citationStellingwerff, T., Boon, H., Jonkers, R. A. M., Senden, J. M., Spriet, L. L., Koopman, R., & van Loon, L. J. C. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00678.2006 · Cited by 81
Exercise-induced mitogen-activated protein kinase signalling in skeletal muscle
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Self-citationHumoral nature of hypoglycemia in muscular exercise
Goldstein, M. S. (1961) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1961.200.1.67 · Cited by 73 · cited 1×
“New Vistas in Molecular Exercise Physiology Skeletal Muscle as a Secretory Organ Over half a century ago, a humoral factor associated with exercise but whose source was unknown was speculated to act in an endocrine manner to regulate glycemia independent of insulin (Goldstein, 1961).”
BackgroundTriacylglycerol lipases and metabolic control: implications for health and disease
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Effects of 7 wk of endurance training on human skeletal muscle metabolism during submaximal exercise
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O’Connor, R. S., Pavlath, G. K., McCarthy, J. J., & Esser, K. A. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00502.2007 · Cited by 53
Gold standards for scientists who are conducting animal-based exercise studies
Booth, F. W., Laye, M. J., & Spangenburg, E. E. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00125.2009 · Cited by 53
Intracellular Ca2+ Signaling in Skeletal Muscle
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Flagged first, then by citations
2 of the 210 references couldn’t be matched to a known paper.
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Nrf2-Keap1 signaling in oxidative and reductive stress
Bellezza, I., Giambanco, I., Minelli, A., & Donato, R. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2018.02.010 · Cited by 2,134
The mitochondrial basis of aging
Sun, N., Youle, R. J., & Finkel, T. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.01.028 · Cited by 1,441
Skeletal muscle energy metabolism during exercise
Hargreaves, M., & Spriet, L. L. (2020) · Nature Metabolism · doi:10.1038/s42255-020-0251-4 · Cited by 1,408
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
Self-citationPhysiological adaptations to interval training and the role of exercise intensity
MacInnis, M. J., & Gibala, M. J. (2017) · The Journal of Physiology · doi:10.1113/jp273196 · Cited by 1,124
Metadata
- Authors
- Egan, B., & Zierath, J. R.
- Affiliations
- University College Dublin (IE)
- University of Copenhagen (DK)
- Corresponding author
- Zierath, Juleen R.
- Venue
- Cell Metabolism
- Publisher
- Elsevier BV
- Published
- 2013-02
- Volume
- 17
- Issue
- 2
- Pages
- 162-184
- ISSN
- 1550-4131 (ISSN-L)
- OpenAlex
- W1995381409
- Semantic Scholar
- 735dcdabdb4efc5dec9569db8f5a316859b70bd6
- Cited by
- 2,084
- References
- 210
- Citations by year
- 2026: 157 · 2025: 168 · 2024: 162 · 2023: 190 · 2022: 209 · 2021: 204 · 2020: 198 · 2019: 189 · 2018: 151 · 2017: 145 · 2016: 122 · 2015: 103 · 2014: 63 · 2013: 21
- FWCI
- 9.69
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 369 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Vetenskapsrådet
- University College Dublin
- Novo Nordisk Fonden
- Karolinska Institutet
- European Research Council
- Knut och Alice Wallenbergs Stiftelse
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Physiology (medical) › Cardiovascular and exercise physiology
- Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
- Keywords
- exercise metabolism, skeletal muscle adaptation, exercise training, aerobic exercise, resistance training, acute exercise, metabolic remodeling, signaling pathways, transcriptional regulation, translational regulation, muscle strength, cardiorespiratory fitness, chronic disease prevention
- MeSH terms
- Adaptation, Physiological, Humans, Hypertrophy, Muscle Contraction, Signal Transduction, Exercise, Muscle, Skeletal
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