The DOI matches its Crossref record; 42 of the 42 references it cites were found in a registry or an index.
Substrate availability and transcriptional regulation of metabolic genes in human skeletal muscle during recovery from exercise
Abstract
In skeletal muscle of humans, transcription of several metabolic genes is transiently induced during recovery from exercise when no food is consumed. To determine the potential influence of substrate availability on the transcriptional regulation of metabolic genes during recovery from exercise, 9 male subjects (aged 22-27) completed 75 minutes of cycling exercise at 75% Vo2 max on 2 occasions, consuming either a high-carbohydrate (HC) or low-carbohydrate (LC) diet during the subsequent 24 hours of recovery. Nuclei were isolated and tissue frozen from vastus lateralis muscle biopsies obtained before exercise and 2, 5, 8, and 24 hours after exercise. Muscle glycogen was restored to near resting levels within 5 hours in the HC trial, but remained depressed through 24 hours in the LC trial. During the 2- to 8-hour recovery period, leg glucose uptake was 5- to 15-fold higher with HC ingestion, whereas arterial plasma free fatty acid levels were approximately 3- to 7-fold higher with LC ingestion. Exercise increased (P < .05) transcription and/or mRNA content of the pyruvate dehydrogenase kinase 4, uncoupling protein 3, lipoprotein lipase, carnitine palmitoyltransferase I, hexokinase II, peroxisome proliferator activated receptor gamma coactivator-1 alpha, and peroxisome proliferator activated receptor alpha. Providing HC during recovery reversed the activation of pyruvate dehydrogenase kinase 4, uncoupling protein 3, lipoprotein lipase, and carnitine palmitoyltransferase I within 5 to 8 hours after exercise, whereas providing LC during recovery elicited a sustained/enhanced increase in activation of these genes through 8 to 24 hours of recovery. These findings provide evidence that factors associated with substrate availability and/or cellular metabolic recovery (eg, muscle glycogen restoration) influence the transcriptional regulation of metabolic genes in skeletal muscle of humans during recovery from exercise.
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“On the basis that reduced pre- [15] and post-exercise [16] muscle glycogen availability augments expression of genes regulating substrate utilization and mitochondrial biogenesis”
From Fuel for the Work Required: A Theoretical Framework for Carbohydrate Periodization and the Glycogen Threshold Hypothesis (2018) · cites this paper as [16]
In the citing paper
“However, restoring post-exercise glycogen levels to > 500 mmol/kg dw attenuates exercise-induced changes in gene expression [16]”
From Fuel for the Work Required: A Theoretical Framework for Carbohydrate Periodization and the Glycogen Threshold Hypothesis (2018) · cites this paper as [16]
In the citing paper
“When studying the effects on gene expression post-exercise with or without carbohydrates, interesting observations were made by Pilegaard et al. [57]: activation of metabolic genes was augmented following 75 min of cycling exercise when carbohydrate intake was restricted for over 5 h compared with controls [57].”
From Periodized Nutrition for Athletes (2017) · cites this paper as [57]
In the citing paper
“The recovery period, which plays a central role in the development of training adaptation [19], is non optimal for prolonging the period of optimized response to the training stimulus [20].”
From Periodization of carbohydrate intake: short-term effect on performance (2016) · cites this paper as [20]
Citations
Cites
A Flexible System of Enzymatic Analysis
Lowry, O. H., & Passonneau, J. V. (1972) · Elsevier eBooks · doi:10.1016/b978-0-12-457950-7.x5001-3 · Cited by 4,050
Regulation of Muscle Fiber Type and Running Endurance by PPARδ
Wang, Y.-X., Zhang, C.-L., Yu, R. T., Cho, H. K., Nelson, M. C., Bayuga-Ocampo, C. R., Ham, J., Kang, H., & Evans, R. M. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020294 · Cited by 1,089
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
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
Self-citationTranscriptional regulation of gene expression in human skeletal muscle during recovery from exercise
Pilegaard, H., Ordway, G. A., Saltin, B., & Neufer, P. D. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.279.4.e806 · Cited by 563
Self-citationEffect of physical exercise on sensitivity and responsiveness to insulin in humans
Mikines, K. J., Sonne, B., Farrell, P. A., Tronier, B., & Galbo, H. (1988) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1988.254.3.e248 · Cited by 538
Regulation of gene expression by insulin
O’Brien, R. M., & Granner, D. K. (1996) · Physiological Reviews · doi:10.1152/physrev.1996.76.4.1109 · Cited by 532
Keller, C., Steensberg, A., Pilegaard, H., Osada, T., Saltin, B., Pedersen, B. K., & Neufer, P. D. (2001) · The FASEB Journal · doi:10.1096/fj.01-0507fje · Cited by 514
Self-citationProlonged increase in insulin-stimulated glucose transport in muscle after exercise
Cartee, G. D., Young, D. A., Sleeper, M. D., Zierath, J., Wallberg-Henriksson, H., & Holloszy, J. O. (1989) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1989.256.4.e494 · Cited by 342
Rådegran, G. (1997) · Journal of Applied Physiology · doi:10.1152/jappl.1997.83.4.1383 · Cited by 296
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
Wojtaszewski, J. F. P., Jørgensen, S. B., Hellsten, Y., Hardie, D. G., & Richter, E. A. (2002) · Diabetes · doi:10.2337/diabetes.51.2.284 · Cited by 261
Glucose, exercise and insulin: emerging concepts
Richter, E. A., Derave, W., & Wojtaszewski, J. F. P. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.t01-2-00313.x · Cited by 258
Cameron-Smith, D., Burke, L. M., Angus, D. J., Tunstall, R. J., Cox, G. R., Bonen, A., Hawley, J. A., & Hargreaves, M. (2003) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/77.2.313 · Cited by 243
Pilegaard, H., Keller, C., Steensberg, A., Wulff Helge, J., Klarlund Pedersen, B., Saltin, B., & Neufer, P. D. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.016832 · Cited by 234
Self-citationEnhanced muscle glucose metabolism after exercise in the rat: the two phases
Garetto, L. P., Richter, E. A., Goodman, M. N., & Ruderman, N. B. (1984) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1984.246.6.e471 · Cited by 198
Enhanced muscle glucose metabolism after exercise: modulation by local factors
Richter, E. A., Garetto, L. P., Goodman, M. N., & Ruderman, N. B. (1984) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1984.246.6.e476 · Cited by 194
Seip, R. L., Mair, K., Cole, T. G., & Semenkovich, C. F. (1997) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1997.272.2.e255 · Cited by 173
Magnitude and duration of excess postexercise oxygen consumption in healthy young subjects
Mæhlum, S., Grandmontagne, M., Newsholme, E. A., & Sejersted, O. M. (1986) · Metabolism · doi:10.1016/0026-0495(86)90132-0 · Cited by 171
Human muscle glycogen resynthesis after exercise: insulin-dependent and -independent phases
Price, T. B., Rothman, D. L., Taylor, R., Avison, M. J., Shulman, G. I., & Shulman, R. G. (1994) · Journal of Applied Physiology · doi:10.1152/jappl.1994.76.1.104 · Cited by 168
Gill, J. M. R., & Hardman, A. E. (2003) · The Journal of Nutritional Biochemistry · doi:10.1016/s0955-2863(02)00275-9 · Cited by 159
Peters, S. J., Harris, R. A., Wu, P., Pehleman, T. L., Heigenhauser, G. J. F., & Spriet, L. L. (2001) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2001.281.6.e1151 · Cited by 154
Effects of exercise on GLUT-4 and glycogenin gene expression in human skeletal muscle
Kraniou, Y. N., Cameron‐Smith, D., Misso, M. L., Collier, G. R., & Hargreaves, M. (2000) · Journal of Applied Physiology · doi:10.1152/jappl.2000.88.2.794 · Cited by 153
Pilegaard, H., Saltin, B., & Neufer, P. D. (2003) · Diabetes · doi:10.2337/diabetes.52.3.657 · Cited by 153
Self-citationNielsen, J. N., Derave, W., Kristiansen, S., Ralston, E., Ploug, T., & Richter, E. A. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.0757h.x · Cited by 138
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 134
Self-citationPilegaard, H., & Neufer, P. D. (2004) · Proceedings of The Nutrition Society · doi:10.1079/pns2004345 · Cited by 133
Self-citationHuman Skeletal Muscle Fatty Acid and Glycerol Metabolism During Rest, Exercise and Recovery
van Hall, G., Sacchetti, M., Rådegran, G., & Saltin, B. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.023796 · Cited by 119
Self-citationPrior exercise and postprandial substrate extraction across the human leg
Malkova, D., Evans, R. D., Frayn, K. N., Humphreys, S. M., Jones, P. R. M., & Hardman, A. E. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.279.5.e1020 · Cited by 117
Exercise increases susceptibility of muscle glucose transport to activation by various stimuli
Cartee, G. D., & Holloszy, J. O. (1990) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1990.258.2.e390 · Cited by 113
Hildebrandt, A. L., Pilegaard, H., & Neufer, P. D. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00234.2003 · Cited by 107
Self-citationMuscle glycogen content affects insulin-stimulated glucose transport and protein kinase B activity
Derave, W., Hansen, B. F., Lund, S., Kristiansen, S., & Richter, E. A. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.279.5.e947 · Cited by 102
Rat skeletal muscle hexokinase II mRNA and activity are increased by a single bout of acute exercise
O'Doherty, R. M., Bracy, D. P., Osawa, H., Wasserman, D. H., & Granner, D. K. (1994) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1994.266.2.e171 · Cited by 98
Hildebrandt, A. L., & Neufer, P. D. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.278.6.e1078 · Cited by 93
Self-citationNielsen, J. N., Wojtaszewski, J. F. P., Haller, R. G., Hardie, D. G., Kemp, B. E., Richter, E. A., & Vissing, J. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.018044 · Cited by 86
Khalfallah, Y., Fages, S., Laville, M., Langin, D., & Vidal, H. (2000) · Diabetes · doi:10.2337/diabetes.49.1.25 · Cited by 78
Jones, T. E., Baar, K., Ojuka, E. O., Chen, M. W., & Holloszy, J. O. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00316.2002 · Cited by 73
Insulin suppresses PDK-4 expression in skeletal muscle independently of plasma FFA
Lee, F. N., Zhang, L., Zheng, D., Choi, W. S., & Youn, J. H. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00461.2003 · Cited by 57
Effect of carbohydrate supplementation on postexercise GLUT-4 protein expression in skeletal muscle
Kuo, C., Hunt, D. G., Ding, Z., & Ivy, J. L. (1999) · Journal of Applied Physiology · doi:10.1152/jappl.1999.87.6.2290 · Cited by 50
Carbohydrate feeding speeds reversal of enhanced glucose uptake in muscle after exercise
Young, J. C., Garthwaite, S. M., Bryan, J. E., Cartier, L.-J., & Holloszy, J. O. (1983) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1983.245.5.r684 · Cited by 50
Effects of high-intensity intermittent swimming on glucose transport in rat epitrochlearis muscle
Kawanaka, K., Tabata, I., Tanaka, A., & Higuchi, M. (1998) · Journal of Applied Physiology · doi:10.1152/jappl.1998.84.6.1852 · Cited by 34
Kuo, C., Hwang, H., Lee, M.-C., Castle, A. L., & Ivy, J. L. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00830.2003 · Cited by 25
Research works printed but not linked: 1
- Bergstrom, 1962, Muscle electrolytes in man, Scand J Clin Lab Invest Suppl, 68, 1
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Nakamura, M., Yudell, B. E., & Loor, J. J. (2013) · Progress in Lipid Research · doi:10.1016/j.plipres.2013.12.001 · Cited by 858
The Molecular Bases of Training Adaptation
Coffey, V. G., & Hawley, J. A. (2007) · Sports Medicine · doi:10.2165/00007256-200737090-00001 · Cited by 756
Impact of Oxidative Stress on Exercising Skeletal Muscle
Steinbacher, P., & Eckl, P. (2015) · Biomolecules · doi:10.3390/biom5020356 · Cited by 436
Wasserman, D. H. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90563.2008 · Cited by 384
Coordination of metabolic plasticity in skeletal muscle
Hood, D. A., Irrcher, I., Ljubicic, V., & Joseph, A.-M. (2006) · Journal of Experimental Biology · doi:10.1242/jeb.02182 · Cited by 370
Metadata
- Authors
- Pilegaard, H., Osada, T., Andersen, L. T., Helge, J. W., Saltin, B., & Neufer, P. D.
- Affiliations
- University of Copenhagen (DK)
- Yale University (US)
- Venue
- Metabolism
- Publisher
- Elsevier BV
- Published
- 2005-08
- Volume
- 54
- Issue
- 8
- Pages
- 1048-1055
- ISSN
- 0026-0495 (ISSN-L)
- OpenAlex
- W2130919437
- Cited by
- 154
- References
- 42
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 7 · 2023: 2 · 2022: 5 · 2021: 9 · 2020: 7 · 2019: 8 · 2018: 12 · 2017: 8 · 2016: 9 · 2015: 11 · 2014: 4 · 2013: 6 · 2012: 3
- FWCI
- 3.11
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Funders
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR-45372, R01AR045372)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Health Sciences › Medicine › Physiology (medical) › Exercise and Physiological Responses
- Keywords
- post-exercise recovery, skeletal muscle, substrate availability, carbohydrate intake, muscle glycogen, glucose uptake, free fatty acids, PDK4, UCP3, lipoprotein lipase, carnitine palmitoyltransferase 1, hexokinase 2, PPARγ coactivator-1α, PPARα, vastus lateralis
- MeSH terms
- Forkhead Box Protein O1, Uncoupling Protein 3, Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha, Adult, Carnitine O-Palmitoyltransferase, Carrier Proteins, DNA-Binding Proteins, Energy Metabolism, Physical Exertion, Glycogen, Glycogen Synthase, Heat-Shock Proteins, Hexokinase, Humans, Ion Channels, Lipoprotein Lipase, Male, Monosaccharide Transport Proteins, Muscle Proteins, Protein Kinases, RNA, Messenger, Transcription Factors, Transcriptional Activation, Gene Expression Regulation, Enzymologic, Muscle, Skeletal, CD36 Antigens, Recovery of Function, Mitochondrial Proteins, PPAR alpha, Glucose Transporter Type 4, Forkhead Transcription Factors
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