Cited by 252Muscle metabolism and nutritionCardiovascular and exercise physiologyMetabolism, Diabetes, and Cancer

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Regulation of Muscle Glycogen Metabolism during Exercise: Implications for Endurance Performance and Training Adaptations

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Hearris, Mark, Hammond, Kelly, Fell, J., Morton, James·2018·Nutrients

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Abstract

Since the introduction of the muscle biopsy technique in the late 1960s, our understanding of the regulation of muscle glycogen storage and metabolism has advanced considerably. Muscle glycogenolysis and rates of carbohydrate (CHO) oxidation are affected by factors such as exercise intensity, duration, training status and substrate availability. Such changes to the global exercise stimulus exert regulatory effects on key enzymes and transport proteins via both hormonal control and local allosteric regulation. Given the well-documented effects of high CHO availability on promoting exercise performance, elite endurance athletes are typically advised to ensure high CHO availability before, during and after high-intensity training sessions or competition. Nonetheless, in recognition that the glycogen granule is more than a simple fuel store, it is now also accepted that glycogen is a potent regulator of the molecular cell signaling pathways that regulate the oxidative phenotype. Accordingly, the concept of deliberately training with low CHO availability has now gained increased popularity amongst athletic circles. In this review, we present an overview of the regulatory control of CHO metabolism during exercise (with a specific emphasis on muscle glycogen utilization) in order to discuss the effects of both high and low CHO availability on modulating exercise performance and training adaptations, respectively.

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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
Adaptations of skeletal muscle to endurance exercise and their metabolic consequences
Holloszy, J. O., & Coyle, E. F. (1984) · Journal of Applied Physiology · doi:10.1152/jappl.1984.56.4.831 · Cited by 1,985
Diet, muscle glycogen and physical performance.
Bergström, J., Hermansen, L., Hultman, E., & Saltin, B. (1967) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1967.tb03720.x · Cited by 1,740 · cited 1×
“The basic principles of CHO loading were developed in the late 1960s where it was identified that a period of exhaustive exercise followed by several days of high dietary CHO intake induces a super-compensation effect so that glycogen storage is augmented [3,4].”
Background
Position of the Academy of Nutrition and Dietetics, Dietitians of Canada, and the American College of Sports Medicine: Nutrition and Athletic Performance
Thomas, D. T., Erdman, K. A., & Burke, L. M. (2016) · Journal of the Academy of Nutrition and Dietetics · doi:10.1016/j.jand.2015.12.006 · Cited by 1,359
Muscle glycogen utilization during prolonged strenuous exercise when fed carbohydrate
Coyle, E. F., Coggan, A. R., Hemmert, M. K., & Ivy, J. L. (1986) · Journal of Applied Physiology · doi:10.1152/jappl.1986.61.1.165 · Cited by 1,022
The effects of increasing exercise intensity on muscle fuel utilisation in humans
van Loon, L. J. C., Greenhaff, P. L., Constantin‐Teodosiu, D., Saris, W. H. M., & Wagenmakers, A. J. M. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.00295.x · Cited by 897
Muscle Glycogen during Prolonged Severe Exercise
Hermansen, L., Hultman, E., & Saltin, B. (1967) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1967.tb03719.x · Cited by 752
Muscle and Blood Metabolites during a Soccer Game: Implications for Sprint Performance
KRUSTRUP, P., MOHR, M., STEENSBERG, A., BENCKE, J., KJÆR, M., & BANGSBO, J. (2006) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000222845.89262.cd · Cited by 742
Selective glycogen depletion pattern in human muscle fibres after exercise of varying intensity and at varying pedalling rates
Gollnick, P. D., Piehl, K., & Saltin, B. (1974) · The Journal of Physiology · doi:10.1113/jphysiol.1974.sp010639 · Cited by 643
Carbohydrate sensing in the human mouth: effects on exercise performance and brain activity
Chambers, E. S., Bridge, M., & Jones, D. A. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.164285 · Cited by 625
Metabolic Characteristics of Fibre Types in Human Skeletal Muscle
Essén, B., Jansson, E., Henriksson, J., Taylor, A. W., & Saltin, B. (1975) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1975.tb10038.x · Cited by 582
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
Muscle Glycogen Synthesis after Exercise : an Enhancing Factor localized to the Muscle Cells in Man
BERGSTRÖM, J., & HULTMAN, E. (1966) · Nature · doi:10.1038/210309a0 · Cited by 473
The effect of carbohydrate mouth rinse on 1-h cycle time trial performance
CARTER, J. M., JEUKENDRUP, A. E., & JONES, D. A. (2004) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000147585.65709.6f · Cited by 437
The Glycogen-Binding Domain on the AMPK β Subunit Allows the Kinase to Act as a Glycogen Sensor
McBride, A., Ghilagaber, S., Nikolaev, A., & Hardie, D. G. (2009) · Cell Metabolism · doi:10.1016/j.cmet.2008.11.008 · Cited by 432
The Nature of the Training Response; Peripheral and Central Adaptations to One‐Legged Exercise
Saltin, B., Nazar, K., COSTILL, D. L., Stein, E., Jansson, E., Essén, B., & Gollnick, P. D. (1976) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1976.tb10200.x · Cited by 412
A Step Towards Personalized Sports Nutrition: Carbohydrate Intake During Exercise
Jeukendrup, A. (2014) · Sports Medicine · doi:10.1007/s40279-014-0148-z · Cited by 412
The Relative Value of Fat and Carbohydrate as Sources of Muscular Energy
Krogh, A., & Lindhard, J. (1920) · Biochemical Journal · doi:10.1042/bj0140290 · Cited by 411
Low carbohydrate, high fat diet impairs exercise economy and negates the performance benefit from intensified training in elite race walkers
Burke, L. M., Ross, M. L., Garvican‐Lewis, L. A., Welvaert, M., Heikura, I. A., Forbes, S. G., Mirtschin, J. G., Cato, L. E., Strobel, N., Sharma, A. P., et al. (2017) · The Journal of Physiology · doi:10.1113/jp273230 · Cited by 407
Skeletal Muscle Glucose Uptake During Exercise: How is it Regulated?
Rose, A. J., & Richter, E. A. (2005) · Physiology · doi:10.1152/physiol.00012.2005 · Cited by 386
Exercise, nutrition and immune function
Gleeson, M., Nieman, D. C., & Pedersen, B. K. (2004) · Journal of Sports Sciences · doi:10.1080/0264041031000140590 · Cited by 362
Optimizing fat oxidation through exercise and diet
Achten, J., & Jeukendrup, A. E. (2004) · Nutrition · doi:10.1016/j.nut.2004.04.005 · Cited by 361
Muscle glycogen stores and fatigue
Ørtenblad, N., Westerblad, H., & Nielsen, J. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2013.251629 · Cited by 353
Regulation of 5′AMP-activated protein kinase activity and substrate utilization in exercising human skeletal muscle
Wojtaszewski, J. F. P., MacDonald, C., Nielsen, J. N., Hellsten, Y., Hardie, D. G., Kemp, B. E., Kiens, B., & Richter, E. A. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00436.2002 · Cited by 348
Regulation of skeletal muscle glycogen phosphorylase and PDH during maximal intermittent exercise
Parolin, M. L., Chesley, A., Matsos, M. P., Spriet, L. L., Jones, N. L., & Heigenhauser, G. J. F. (1999) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1999.277.5.e890 · Cited by 334
Effect of Exercise-Diet Manipulation on Muscle Glycogen and Its Subsequent Utilization During Performance*
Sherman, W., Costill, D., Fink, W., & Miller, J. (1981) · International Journal of Sports Medicine · doi:10.1055/s-2008-1034594 · Cited by 325
Fatty acid oxidation is directly regulated by carbohydrate metabolism during exercise
Coyle, E. F., Jeukendrup, A. E., Wagenmakers, A. J. M., & Saris, W. H. M. (1997) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1997.273.2.e268 · Cited by 296
Training induced adaptation of skeletal muscle and metabolism during submaximal exercise
Henriksson, J. (1977) · The Journal of Physiology · doi:10.1113/jphysiol.1977.sp011974 · Cited by 293
Nutritional Intake and Gastrointestinal Problems during Competitive Endurance Events
PFEIFFER, B., STELLINGWERFF, T., HODGSON, A. B., RANDELL, R., PÖTTGEN, K., RES, P., & JEUKENDRUP, A. E. (2012) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31822dc809 · Cited by 287
Skeletal muscle adaptation: training twice every second day vs. training once daily
Hansen, A. K., Fischer, C. P., Plomgaard, P., Andersen, J. L., Saltin, B., & Pedersen, B. K. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00163.2004 · Cited by 286
Skeletal muscle adaptation and performance responses to once a day versus twice every second day endurance training regimens
Yeo, W. K., Paton, C. D., Garnham, A. P., Burke, L. M., Carey, A. L., & Hawley, J. A. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.90882.2008 · Cited by 283
Effects of training duration on substrate turnover and oxidation during exercise
Phillips, S. M., Green, H. J., Tarnopolsky, M. A., Heigenhauser, G. J. F., Hill, R. E., & Grant, S. (1996) · Journal of Applied Physiology · doi:10.1152/jappl.1996.81.5.2182 · Cited by 279
Oxidation of Carbohydrate Feedings During Prolonged Exercise: Current Thoughts, Guidelines and Directions for Future Research
Jeukendrup, A. E., & Jentjens, R. (2000) · Sports Medicine · doi:10.2165/00007256-200029060-00004 · Cited by 279
Lipolytic suppression following carbohydrate ingestion limits fat oxidation during exercise.
Horowitz, J. F., Mora-Rodríguez, R., Byerley, L., & Coyle, E. (1997) · American Journal of Physiology. Endocrinology and Metabolism · doi:10.1152/ajpendo.1997.273.4.e768 · Cited by 277
Carbohydrate-Electrolyte Feedings Improve 1 h Time Trial Cycling Performance
Jeukendrup, A., Brouns, F., Wagenmakers, A., & Saris, W. (1997) · International Journal of Sports Medicine · doi:10.1055/s-2007-972607 · Cited by 271
Carbohydrate-Loading and Exercise Performance: An Update
Hawley, J. A., Schabort, E. J., Noakes, T. D., & Dennis, S. C. (1997) · Sports Medicine · doi:10.2165/00007256-199724020-00001 · Cited by 263 · cited 2×
“[69] cited that CHO loading can improve exercise capacity by approximately 20%, and time trial performance can increase by 2–3%.”
Background
Carbohydrate feedings before, during, or in combination improve cycling endurance performance
Wright, D. A., Sherman, W. M., & Dernbach, A. R. (1991) · Journal of Applied Physiology · doi:10.1152/jappl.1991.71.3.1082 · Cited by 259
Muscle glycogen storage after prolonged exercise: effect of the glycemic index of carbohydrate feedings
Burke, L. M., Collier, G. R., & Hargreaves, M. (1993) · Journal of Applied Physiology · doi:10.1152/jappl.1993.75.2.1019 · Cited by 247
Systematic review: Carbohydrate supplementation on exercise performance or capacity of varying durations
Stellingwerff, T., & Cox, G. R. (2014) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2014-0027 · Cited by 246
Influence of pre‐exercise muscle glycogen content on exercise‐induced transcriptional regulation of metabolic genes
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
Fuel for the Work Required: A Theoretical Framework for Carbohydrate Periodization and the Glycogen Threshold Hypothesis
Impey, S. G., Hearris, M. A., Hammond, K. M., Bartlett, J. D., Louis, J., Close, G. L., & Morton, J. P. (2018) · Sports Medicine · doi:10.1007/s40279-018-0867-7 · Cited by 232 · cited 2×
“[111] for an extensive review of this topic).”
BackgroundSelf-citation
Carbohydrate availability and exercise training adaptation: Too much of a good thing?
Bartlett, J. D., Hawley, J. A., & Morton, J. P. (2015) · European Journal of Sport Science · doi:10.1080/17461391.2014.920926 · Cited by 230
Self-citation
Role of glycogen availability in sarcoplasmic reticulum Ca2+ kinetics in human skeletal muscle
Ørtenblad, N., Nielsen, J., Saltin, B., & Holmberg, H. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2010.195982 · Cited by 225
Liver glycogen metabolism during and after prolonged endurance-type exercise
Gonzalez, J. T., Fuchs, C. J., Betts, J. A., & van Loon, L. J. C. (2016) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00232.2016 · Cited by 206
Intramuscular triacylglycerol, glycogen and acetyl group metabolism during 4 h of moderate exercise in man
Watt, M. J., Heigenhauser, G. J. F., Dyck, D. J., & Spriet, L. L. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.018820 · Cited by 201
Leg glucose uptake during maximal dynamic exercise in humans
Katz, A., Broberg, S., Sahlin, K., & Wahren, J. (1986) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1986.251.1.e65 · Cited by 198
Training with Low Muscle Glycogen Enhances Fat Metabolism in Well-Trained Cyclists
HULSTON, C. J., VENABLES, M. C., MANN, C. H., MARTIN, C., PHILP, A., BAAR, K., & JEUKENDRUP, A. E. (2010) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181dd5070 · Cited by 196
Influence of carbohydrate loading on fuel substrate turnover and oxidation during prolonged exercise
Bosch, A. N., Dennis, S. C., & Noakes, T. D. (1993) · Journal of Applied Physiology · doi:10.1152/jappl.1993.74.4.1921 · Cited by 196
Beneficial metabolic adaptations due to endurance exercise training in the fasted state
Van Proeyen, K., Szlufcik, K., Nielens, H., Ramaekers, M., & Hespel, P. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00907.2010 · Cited by 196
Reduced carbohydrate availability does not modulate training-induced heat shock protein adaptations but does upregulate oxidative enzyme activity in human skeletal muscle
Morton, J. P., Croft, L., Bartlett, J. D., MacLaren, D. P. M., Reilly, T., Evans, L., McArdle, A., & Drust, B. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00003.2009 · Cited by 179
Self-citation
Chronic oral ingestion of l ‐carnitine and carbohydrate increases muscle carnitine content and alters muscle fuel metabolism during exercise in humans
Wall, B. T., Stephens, F. B., Constantin‐Teodosiu, D., Marimuthu, K., Macdonald, I. A., & Greenhaff, P. L. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2010.201343 · Cited by 175
Malonyl-coa and carnitine in regulation of fat oxidation in human skeletal muscle during exercise
Roepstorff, C., Halberg, N., Hillig, T., Saha, A. K., Ruderman, N. B., Wojtaszewski, J. F. P., Richter, E. A., & Kiens, B. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00379.2004 · Cited by 173
Influence of muscle glycogen on glycogenolysis and glucose uptake during exercise in humans
Hargreaves, M., McConell, G., & Proietto, J. (1995) · Journal of Applied Physiology · doi:10.1152/jappl.1995.78.1.288 · Cited by 172 · cited 2×
“Increasing muscle glycogen concentration enhances glycogenolysis during exercise [46] by enhancing phosphorylase activity given that glycogen is a substrate for phosphorylase.”
Background
Regulation of skeletal muscle glycogen phosphorylase and PDH at varying exercise power outputs
Howlett, R. A., Parolin, M. L., Dyck, D. J., Hultman, E., Jones, N. L., Heigenhauser, G. J. F., & Spriet, L. L. (1998) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1998.275.2.r418 · Cited by 170
SOME CHANGES IN THE CHEMICAL CONSTITUENTS OF THE BLOOD FOLLOWING A MARATHON RACE
Levine, S. A., Gordon, B., & DERICK, C. L. (1924) · JAMA · doi:10.1001/jama.1924.02650480034015 · Cited by 167
Carbohydrate ingestion and single muscle fiber glycogen metabolism during prolonged running in men
Tsintzas, O. K., Williams, C., Boobis, L., & Greenhaff, P. (1996) · Journal of Applied Physiology · doi:10.1152/jappl.1996.81.2.801 · Cited by 166
Daily training with high carbohydrate availability increases exogenous carbohydrate oxidation during endurance cycling
Cox, G. R., Clark, S. A., Cox, A. J., Halson, S. L., Hargreaves, M., Hawley, J. A., Jeacocke, N., Snow, R. J., Yeo, W. K., & Burke, L. M. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00950.2009 · Cited by 165
More than a store: regulatory roles for glycogen in skeletal muscle adaptation to exercise
Philp, A., Hargreaves, M., & Baar, K. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00004.2012 · Cited by 156
Substrate availability and transcriptional regulation of metabolic genes in human skeletal muscle during recovery from exercise
Pilegaard, H., Osada, T., Andersen, L. T., Helge, J. W., Saltin, B., & Neufer, P. D. (2005) · Metabolism · doi:10.1016/j.metabol.2005.03.008 · Cited by 154
Carbohydrate loading in human muscle: an improved 1 day protocol
Bussau, V., Fairchild, T., Rao, A., Steele, P., & Fournier, P. (2002) · European Journal of Applied Physiology · doi:10.1007/s00421-002-0621-5 · Cited by 153
Endurance training increases gluconeogenesis during rest and exercise in men
Bergman, B. C., Horning, M. A., Casazza, G. A., Wolfel, E. E., Butterfield, G. E., & Brooks, G. A. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.278.2.e244 · Cited by 153
Effect of a carbohydrate mouth rinse on simulated cycling time-trial performance commenced in a fed or fasted state
Lane, S. C., Bird, S. R., Burke, L. M., & Hawley, J. A. (2012) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2012-0300 · Cited by 151
Splanchnic and muscle metabolism during exercise in NIDDM patients
Martin, I. K., Katz, A., & Wahren, J. (1995) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1995.269.3.e583 · Cited by 149
Ingestion of a high-glycemic index meal increases muscle glycogen storage at rest but augments its utilization during subsequent exercise
Wee, S.-L., Williams, C., Tsintzas, K., & Boobis, L. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01261.2004 · Cited by 147
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
Self-citation
Effect of carbohydrate ingestion on glycogen resynthesis in human liver and skeletal muscle, measured by 13C MRS
Casey, A., Mann, R., Banister, K., Fox, J., Morris, P. G., Macdonald, I. A., & Greenhaff, P. L. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.278.1.e65 · Cited by 140
Carbohydrate feedings 1 h before exercise improves cycling performance
Sherman, W. M., Peden, M., & Wright, D. (1991) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/54.5.866 · Cited by 139
The effect of glucose infusion on glucose kinetics during a 1-h time trial
CARTER, J. M., JEUKENDRUP, A. E., MANN, C. H., & JONES, D. A. (2004) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000139892.69410.d8 · Cited by 137
Enhanced Endurance Performance by Periodization of Carbohydrate Intake: “Sleep Low” Strategy
MARQUET, L.-A., BRISSWALTER, J., LOUIS, J., TIOLLIER, E., BURKE, L. M., HAWLEY, J. A., & HAUSSWIRTH, C. (2016) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000823 · Cited by 134
Effect of glycogen availability on human skeletal muscle protein turnover during exercise and recovery
Howarth, K. R., Phillips, S. M., MacDonald, M. J., Richards, D. L., Moreau, N. A., & Gibala, M. J. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00108.2009 · Cited by 131
Altering dietary nutrient intake that reduces glycogen content leads to phosphorylation of nuclear p38 MAP kinase in human skeletal muscle: association with IL‐6 gene transcription during contraction
Chan, M. H. S., McGee, S. L., Watt, M. J., Hargreaves, M., & Febbraio, M. A. (2004) · The FASEB Journal · doi:10.1096/fj.03-1039fje · Cited by 127
Human skeletal muscle glycogen utilization in exhaustive exercise: role of subcellular localization and fibre type
Nielsen, J., Holmberg, H., Schrøder, H. D., Saltin, B., & Ørtenblad, N. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2010.204487 · Cited by 122
Carbohydrate dependence during marathon running
BRIEN, M. J. O., Viguie, C. A., Mazzeo, R. S., & Brooks, G. A. (1993) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-199309000-00007 · Cited by 121
The Effect of Exercise on Muscle Glycogen and Electrolytes in Normals
Bergström, J. P., & Hultman, E. (1966) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.3109/00365516609065602 · Cited by 119
Carbohydrate ingestion and glycogen utilization in different muscle fibre types in man
Tsintzas, O. K., Williams, C., Boobis, L., & Greenhaff, P. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp021046 · Cited by 117
Acute exercise and GLUT4 expression in human skeletal muscle: influence of exercise intensity
Kraniou, G. N., Cameron‐Smith, D., & Hargreaves, M. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01489.2005 · Cited by 117
Quantification of subcellular glycogen in resting human muscle: granule size, number, and location
Marchand, I., Chorneyko, K., Tarnopolsky, M. A., Hamilton, S., Shearer, J., Potvin, J. R., & Graham, T. E. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00585.2001 · Cited by 114
Carbohydrate supplementation during prolonged cycling exercise spares muscle glycogen but does not affect intramyocellular lipid use
Stellingwerff, T., Boon, H., Gijsen, A. P., Stegen, J. H. C. H., Kuipers, H., & van Loon, L. J. C. (2007) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-007-0236-0 · Cited by 110
Fuel for the work required: A practical approach to amalgamating train-low paradigms for endurance athletes
Impey, S. G., Hammond, K. M., Shepherd, S. O., Sharples, A. P., Stewart, C., Limb, M., Smith, K., Philp, A., Jeromson, S., Hamilton, D. L., et al. (2016) · Physiological Reports · doi:10.14814/phy2.12803 · Cited by 109
Self-citation
Influence of carbohydrate ingestion on fuel substrate turnover and oxidation during prolonged exercise
Bosch, A. N., Dennis, S. C., & Noakes, T. D. (1994) · Journal of Applied Physiology · doi:10.1152/jappl.1994.76.6.2364 · Cited by 107
Muscle net glucose uptake and glucose kinetics after endurance training in men
Bergman, B. C., Butterfield, G. E., Wolfel, E. E., Lopaschuk, G. D., Casazza, G. A., Horning, M. A., & Brooks, G. A. (1999) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1999.277.1.e81 · Cited by 104
Effects of sleeping with reduced carbohydrate availability on acute training responses
Lane, S. C., Camera, D. M., Lassiter, D. G., Areta, J. L., Bird, S. R., Yeo, W. K., Jeacocke, N. A., Krook, A., Zierath, J. R., Burke, L. M., et al. (2015) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00857.2014 · Cited by 102
Regulation of muscle glycogen phosphorylase activity following short-term endurance training
Chesley, A., Heigenhauser, G. J. F., & Spriet, L. L. (1996) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1996.270.2.e328 · Cited by 100
Effect of carbohydrate ingestion on exercise-induced alterations in metabolic gene expression
Cluberton, L. J., McGee, S. L., Murphy, R. M., & Hargreaves, M. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00197.2005 · Cited by 100
Glucose ingestion during exercise blunts exercise-induced gene expression of skeletal muscle fat oxidative genes
Civitarese, A. E., Hesselink, M. K. C., Russell, A. P., Ravussin, E., & Schrauwen, P. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00193.2005 · Cited by 99
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GEJL, K. D., HVID, L. G., FRANDSEN, U., JENSEN, K., SAHLIN, K., & ØRTENBLAD, N. (2014) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000132 · Cited by 94
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Rose, A. J., Frøsig, C., Kiens, B., Wojtaszewski, J. F. P., & Richter, E. A. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.138529 · Cited by 92
Regulation of fuel metabolism by preexercise muscle glycogen content and exercise intensity
Arkinstall, M. J., Bruce, C. R., Clark, S. A., Rickards, C. A., Burke, L. M., & Hawley, J. A. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00421.2004 · Cited by 91
Carbohydrate feeding during recovery alters the skeletal muscle metabolic response to repeated sessions of high-intensity interval exercise in humans
Cochran, A. J. R., Little, J. P., Tarnopolsky, M. A., & Gibala, M. J. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00659.2009 · Cited by 90
Muscle Glycogen Utilization during Exercise after Physical Training
Karlsson, J., Nordesjö, L., & Saltin, B. (1974) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1974.tb05579.x · Cited by 84
β‐adrenergic stimulation of skeletal muscle HSL can be overridden by AMPK signaling
Watt, M. J., Steinberg, G. R., Chan, S. M. H., GARNHAM, A. P., Kemp, B. E., & Febbraio, M. A. (2004) · The FASEB Journal · doi:10.1096/fj.03-1067fje · Cited by 83
The Governor has a sweet tooth – Mouth sensing of nutrients to enhance sports performance
Burke, L. M., & Maughan, R. J. (2014) · European Journal of Sport Science · doi:10.1080/17461391.2014.971880 · Cited by 81
Oral glucose ingestion attenuates exercise-induced activation of 5′-AMP-activated protein kinase in human skeletal muscle
Akerstrom, T. C. A., Birk, J. B., Klein, D. K., Erikstrup, C., Plomgaard, P., Pedersen, B. K., & Wojtaszewski, J. F. P. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.02.057 · Cited by 75
Oxidation of Solid versus Liquid CHO Sources during Exercise
Pfeiffer, B., Stellingwerff, T., Zaltas, E., & Jeukendrup, A. E. (2010) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181e0efc9 · Cited by 75
Human skeletal muscle pyruvate dehydrogenase kinase activity increases after a low-carbohydrate diet
Peters, S. J., Amand, T. A. S., Howlett, R. A., Heigenhauser, G. J. F., & Spriet, L. L. (1998) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1998.275.6.e980 · Cited by 74
Quantitative assessment of human muscle glycogen granules size and number in subcellular locations during recovery from prolonged exercise
Marchand, I., Tarnopolsky, M., Adamo, K. B., Bourgeois, J. M., Chorneyko, K., & Graham, T. E. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2006.122457 · Cited by 71
Sarcolemmal glucose transport and GLUT-4 translocation during exercise are diminished by endurance training
Richter, E. A., Jensen, P. B., Kiens, B., & Kristiansen, S. (1998) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1998.274.1.e89 · Cited by 71
The regulation of muscle glycogen: the granule and its proteins
Graham, T. E., Yuan, Z., Hill, A. K., & Wilson, R. J. (2010) · Acta Physiologica · doi:10.1111/j.1748-1716.2010.02131.x · Cited by 69
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Arkinstall, M. J., Bruce, C. R., Nikolopoulos, V., Garnham, A. P., & Hawley, J. A. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.91.5.2125 · Cited by 63
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Kasper, A. M., Cocking, S., Cockayne, M., Barnard, M., Tench, J., Parker, L., McAndrew, J., Langan‐Evans, C., Close, G. L., & Morton, J. P. (2016) · European Journal of Sport Science · doi:10.1080/17461391.2015.1041063 · Cited by 61
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Trimmer, J. K., Schwarz, J., Casazza, G. A., Horning, M. A., Rodriguez, N., & Brooks, G. A. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01050.2001 · Cited by 58
Impact of carbohydrate supplementation during endurance training on glycogen storage and performance
Nybo, L., Pedersen, K., Christensen, B., Aagaard, P., Brandt, N., & Kiens, B. (2009) · Acta Physiologica · doi:10.1111/j.1748-1716.2009.01996.x · Cited by 58
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GEJL, K. D., THAMS, L. B., HANSEN, M., ROKKEDAL-LAUSCH, T., PLOMGAARD, P., NYBO, L., LARSEN, F. J., CARDINALE, D. A., JENSEN, K., HOLMBERG, H.-C., et al. (2017) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001377 · Cited by 57
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LeBlanc, P. J., Howarth, K. R., Gibala, M. J., & Heigenhauser, G. J. F. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00517.2004 · Cited by 56
Glycogen Content of Individual Muscle Fibres in Man
Essén, B., & Henriksson, J. (1974) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1974.tb05629.x · Cited by 54
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Smith, B. K., Perry, C. G. R., Koves, T. R., Wright, D. C., Smith, J. C., Neufer, P. D., Muoio, D. M., & Holloway, G. P. (2012) · Biochemical Journal · doi:10.1042/bj20121110 · Cited by 44
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Watt, M. J., Heigenhauser, G. J. F., LeBlanc, P. J., Inglis, J., Spriet, L. L., & Peters, S. J. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00132.2004 · Cited by 42
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Hills, S. P., & Russell, M. A. (2017) · Nutrients · doi:10.3390/nu10010022 · Cited by 41
The regulation of muscle phosphorylase kinase by calcium ions, calmodulin and troponin-C
Picton, C., Klee, C. B., & Cohen, P. (1981) · Cell Calcium · doi:10.1016/0143-4160(81)90021-x · Cited by 39
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Newell, M. L., Wallis, G. A., Hunter, A. M., Tipton, K. D., & Galloway, S. D. R. (2018) · Nutrients · doi:10.3390/nu10010037 · Cited by 39
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Louis, J., Marquet, L.-A., Tiollier, E., Bermon, S., Hausswirth, C., & Brisswalter, J. (2016) · European Journal of Applied Physiology · doi:10.1007/s00421-016-3446-3 · Cited by 26
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Ali, A., Yoo, M. J. Y., Moss, C., & Breier, B. H. (2016) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-016-0131-1 · Cited by 23
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Molecular Responses to Acute Exercise and Their Relevance for Adaptations in Skeletal Muscle to Exercise Training
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Gut-Muscle Axis Exists and May Affect Skeletal Muscle Adaptation to Training
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Exercise-induced oxidative stress and melatonin supplementation: current evidence
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Toward a Common Understanding of Diet–Exercise Strategies to Manipulate Fuel Availability for Training and Competition Preparation in Endurance Sport
Burke, L. M., Hawley, J. A., Jeukendrup, A., Morton, J. P., Stellingwerff, T., & Maughan, R. J. (2018) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2018-0289 · Cited by 132
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Authors: Hearris, M., Hammond, K., Fell, J., & Morton, J.
Affiliations: Liverpool John Moores University (GB)
Corresponding author: Morton, James
ORCID: Hearris, Mark
Morton, James
Venue: Nutrients
Publisher: MDPI AG
Published: 2018-03-02
Volume: 10
Issue: 3
Pages: 298
ISSN: 2072-6643 (ISSN-L)
DOI: 10.3390/nu10030298
PMC: PMC5872716
OpenAlex: W2792934062
Cited by: 252
References: 120
Citations by year: 2026: 30 · 2025: 31 · 2024: 34 · 2023: 26 · 2022: 38 · 2021: 40 · 2020: 27 · 2019: 17 · 2018: 9
FWCI: 2.61
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: Nutrients (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Liverpool John Moores University (acceptedVersion)
e-space (Manchester Metropolitan University) (acceptedVersion)
Figshare (submittedVersion, cc-by)
Funders: GlaxoSmithKline
Topics: Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
Health Sciences › Medicine › Physiology (medical) › Cardiovascular and exercise physiology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Keywords: muscle glycogen metabolism, glycogenolysis, carbohydrate oxidation, endurance performance, training effects, carbohydrate availability, glycogen storage, allosteric regulation, hormonal regulation, exercise intensity
MeSH terms: Adaptation, Physiological, Animals, Dietary Carbohydrates, Energy Metabolism, Glycogen, Humans, Muscle Contraction, Oxidation-Reduction, Phenotype, Physical Endurance, Signal Transduction, Muscle, Skeletal, Diet, Carbohydrate-Restricted

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Regulation of Muscle Glycogen Metabolism during Exercise: Implications for Endurance Performance and Training Adaptations

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