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

Hearris, Mark; Hammond, Kelly; Fell, J.; Morton, James

doi:10.3390/nu10030298

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

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

DOI 10.3390/nu10030298PMC PMC5872716

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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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Low initial muscle glycogen reduces substrate availability by limiting glycogen phosphorylase activity and indirectly downregulates carbohydrate oxidation via reduced activation of pyruvate dehydrogenase.
“Mechanistically, low initial muscle glycogen reduces substrate availability by limiting glycogen phosphorylase activity and indirectly downregulates carbohydrate oxidation via reduced activation of pyruvate dehydrogenase (78).”
From Carbohydrate ingestion during prolonged exercise and net skeletal muscle glycogen utilization: A meta-analysis. (2026) · cites this paper as [78]
Glycogen is not only an energy substrate but also a regulator of the signaling pathways that regulate exercise-induced adaptations.
“Glycogen is currently not only considered an energy substrate but also a regulator of the signaling pathways that regulate exercise-induced adaptations.”
From Carbohydrate Availability and Physical Performance: Physiological Overview and Practical Recommendations (2019) · cites this paper as [13]

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Influence of carbohydrate ingestion on fuel substrate turnover and oxidation during prolonged exercise
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Muscle net glucose uptake and glucose kinetics after endurance training in men
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Effects of sleeping with reduced carbohydrate availability on acute training responses
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Regulation of muscle glycogen phosphorylase activity following short-term endurance training
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Effect of carbohydrate ingestion on exercise-induced alterations in metabolic gene expression
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Glucose ingestion during exercise blunts exercise-induced gene expression of skeletal muscle fat oxidative genes
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Ingestion of glucose or sucrose prevents liver but not muscle glycogen depletion during prolonged endurance-type exercise in trained cyclists
Gonzalez, J. T., Fuchs, C. J., Smith, F. E., Thelwall, P. E., Taylor, R., Stevenson, E. J., Trenell, M. I., Cermak, N. M., & van Loon, L. J. C. (2015) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00376.2015 · Cited by 95 · see citing works
Muscle Glycogen Content Modifies SR Ca2+ Release Rate in Elite Endurance Athletes
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Effect of endurance exercise training on Ca 2+ –calmodulin‐dependent protein kinase II expression and signalling in skeletal muscle of humans
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Carbohydrate feeding during recovery alters the skeletal muscle metabolic response to repeated sessions of high-intensity interval exercise in humans
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Muscle Glycogen Utilization during Exercise after Physical Training
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β‐adrenergic stimulation of skeletal muscle HSL can be overridden by AMPK signaling
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Oral glucose ingestion attenuates exercise-induced activation of 5′-AMP-activated protein kinase in human skeletal muscle
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Human skeletal muscle pyruvate dehydrogenase kinase activity increases after a low-carbohydrate diet
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CHO Oxidation from a CHO Gel Compared with a Drink during Exercise
Pfeiffer, B., Stellingwerff, T., Zaltas, E., & Jeukendrup, A. E. (2010) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181e0efe6 · Cited by 69 · see citing works
Effect of carbohydrate ingestion on metabolism during running and cycling
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Carbohydrate mouth rinse and caffeine improves high‐intensity interval running capacity when carbohydrate restricted
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Measurement of gluconeogenesis in exercising men by mass isotopomer distribution analysis
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 · see citing works
Impact of carbohydrate supplementation during endurance training on glycogen storage and performance
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No superior adaptations to carbohydrate periodization in elite endurance athletes
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Effects of 7 wk of endurance training on human skeletal muscle metabolism during submaximal exercise
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Glycogen Content of Individual Muscle Fibres in Man
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Protein ingestion does not impair exercise-induced AMPK signalling when in a glycogen-depleted state: implications for train-low compete-high
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Rapid upregulation of pyruvate dehydrogenase kinase activity in human skeletal muscle during prolonged exercise
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Low Muscle Glycogen and Elevated Plasma Free Fatty Acid Modify but Do Not Prevent Exercise-Induced PDH Activation in Human Skeletal Muscle
Kiilerich, K., Gudmundsson, M., Birk, J. B., Lundby, C., Taudorf, S., Plomgaard, P., Saltin, B., Pedersen, P. A., Wojtaszewski, J. F. P., & Pilegaard, H. (2009) · Diabetes · doi:10.2337/db09-1032 · Cited by 42 · see citing works
Identification of a novel malonyl-CoA IC50 for CPT-I: implications for predicting in vivo fatty acid oxidation rates
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The regulation of muscle phosphorylase kinase by calcium ions, calmodulin and troponin-C
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Metabolic Responses to Carbohydrate Ingestion during Exercise: Associations between Carbohydrate Dose and Endurance Performance
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Carbohydrates for Soccer: A Focus on Skilled Actions and Half-Time Practices
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Altering fatty acid availability does not impair prolonged, continuous running to fatigue: evidence for carbohydrate dependence
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Self-citation
Self-selecting Fluid Intake while Maintaining High Carbohydrate Availability Does not Impair Half-marathon Performance
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The impact of sleeping with reduced glycogen stores on immunity and sleep in triathletes
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Carbohydrate mouth rinsing has no effect on power output during cycling in a glycogen-reduced state
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Extreme Variation of Nutritional Composition and Osmolality of Commercially Available Carbohydrate Energy Gels
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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
Muscle Glycogen Metabolism and High-Intensity Exercise Performance: A Narrative Review
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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
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Self-citation
A Framework for Periodized Nutrition for Athletics
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Carbohydrate Availability and Physical Performance: Physiological Overview and Practical Recommendations
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Regulation of Energy Substrate Metabolism in Endurance Exercise
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Lactobacillus salivarius Subspecies salicinius SA-03 is a New Probiotic Capable of Enhancing Exercise Performance and Decreasing Fatigue
Lee, M., Hsu, Y.-J., Ho, H.-H., Hsieh, S., Kuo, Y., Sung, H., & Huang, C. (2020) · Microorganisms · doi:10.3390/microorganisms8040545 · Cited by 98 · see citing works
Applications of Medium-Chain Triglycerides in Foods
Watanabe, S., & Tsujino, S. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.802805 · Cited by 102 · see citing works
Effects of 120 g/h of Carbohydrates Intake during a Mountain Marathon on Exercise-Induced Muscle Damage in Elite Runners
Viribay, A., Arribalzaga, S., Mielgo‐Ayuso, J., Castañeda-Babarro, A., Seco‐Calvo, J., & Urdampilleta, A. (2020) · Nutrients · doi:10.3390/nu12051367 · Cited by 85 · see citing works
Direct and indirect impact of low energy availability on sports performance
Melin, A., Areta, J. L., Heikura, I. A., Stellingwerff, T., Torstveit, M. K., & Hackney, A. C. (2023) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.14327 · Cited by 94 · see citing works
Exogenous Ketone Supplements in Athletic Contexts: Past, Present, and Future
Evans, M., McClure, T. S., Koutnik, A. P., & Egan, B. (2022) · Sports Medicine · doi:10.1007/s40279-022-01756-2 · Cited by 76 · see citing works
Progress of linking gut microbiota and musculoskeletal health: casualty, mechanisms, and translational values
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A map of metabolic phenotypes in patients with myalgic encephalomyelitis/chronic fatigue syndrome
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Blood flow-restricted training enhances thigh glucose uptake during exercise and muscle antioxidant function in humans
Christiansen, D., Eibye, K., Hostrup, M., & Bangsbo, J. (2019) · Metabolism · doi:10.1016/j.metabol.2019.06.003 · Cited by 58 · see citing works
Glycogen metabolism and structure: A review
Neoh, G. K. S., Tan, X., Chen, S., Roura, E., Dong, X., & Gilbert, R. G. (2024) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2024.122631 · Cited by 56 · see citing works
Is a vegan diet detrimental to endurance and muscle strength?
Boutros, G. H., Landry-Duval, M.-A., Garzón, M., & Karelis, A. D. (2020) · European Journal of Clinical Nutrition · doi:10.1038/s41430-020-0639-y · Cited by 58 · see citing works
Exercise-Induced Illness and Inflammation: Can Immunonutrition and Iron Help?
Castell, L. M., Nieman, D. C., Bermon, S., & Peeling, P. (2018) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2018-0288 · Cited by 53 · see citing works
Transcriptomic, proteomic and phosphoproteomic underpinnings of daily exercise performance and zeitgeber activity of training in mouse muscle
Maier, G., Delezie, J., Westermark, P. O., Santos, G., Ritz, D., & Handschin, C. (2021) · The Journal of Physiology · doi:10.1113/jp281535 · Cited by 51 · see citing works
In Vivo Ergogenic Properties of the Bifidobacterium longum OLP-01 Isolated from a Weightlifting Gold Medalist
Lee, M., Hsu, Y.-J., Chuang, H.-L., Hsieh, P.-S., Ho, H.-H., Chen, W.-L., Chiu, Y., & Huang, C. (2019) · Nutrients · doi:10.3390/nu11092003 · Cited by 50 · see citing works
Effects of 120 vs. 60 and 90 g/h Carbohydrate Intake during a Trail Marathon on Neuromuscular Function and High Intensity Run Capacity Recovery
Urdampilleta, A., Arribalzaga, S., Viribay, A., Castañeda-Babarro, A., Seco‐Calvo, J., & Mielgo‐Ayuso, J. (2020) · Nutrients · doi:10.3390/nu12072094 · Cited by 50 · see citing works
Exercise Training Combined with Bifidobacterium longum OLP-01 Supplementation Improves Exercise Physiological Adaption and Performance
Huang, W.-C., Hsu, Y.-J., Huang, C., Liu, H., & Lee, M. (2020) · Nutrients · doi:10.3390/nu12041145 · Cited by 47 · see citing works
Exercising with low muscle glycogen content increases fat oxidation and decreases endogenous, but not exogenous carbohydrate oxidation
Margolis, L. M., Wilson, M. A., Whitney, C. C., Carrigan, C. T., Murphy, N. E., Hatch‐McChesney, A., Montain, S. J., & Pasiakos, S. M. (2019) · Metabolism · doi:10.1016/j.metabol.2019.05.003 · Cited by 43 · see citing works
Is a Four-Week Ketogenic Diet an Effective Nutritional Strategy in CrossFit-Trained Female and Male Athletes?
Durkalec‐Michalski, K., Nowaczyk, P. M., Główka, N., Ziobrowska, A., & Podgórski, T. (2021) · Nutrients · doi:10.3390/nu13030864 · Cited by 45 · see citing works
Carbohydrates and Endurance Exercise: A Narrative Review of a Food First Approach
Naderi, A., Gobbi, N., Ali, A., Berjisian, E., Hamidvand, A., Forbes, S. C., Koozehchian, M. S., Karayigit, R., & Saunders, B. (2023) · Nutrients · doi:10.3390/nu15061367 · Cited by 42 · see citing works
Gut Microbial Stability is Associated with Greater Endurance Performance in Athletes Undertaking Dietary Periodization
Furber, M., Young, G. R., Holt, G. S., Pyle, S., Davison, G., Roberts, M. G., Roberts, J., Howatson, G., & Smith, D. (2022) · mSystems · doi:10.1128/msystems.00129-22 · Cited by 43 · see citing works
Self-reported periodization of nutrition in elite female and male runners and race walkers
Heikura, I. A., Stellingwerff, T., & Burke, L. M. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01732 · Cited by 40 · see citing works
Complex I is bypassed during high intensity exercise
Nilsson, A., Björnson, E., Flockhart, M., Larsen, F. J., & Nielsen, J. (2019) · Nature Communications · doi:10.1038/s41467-019-12934-8 · Cited by 37 · see citing works
Low-carbohydrate diets: Effects on metabolism and exercise – A comprehensive literature review
Macedo, R. C. O., Santos, H. O., Tinsley, G. M., & Reischak-Oliveira, Á. (2020) · Clinical Nutrition ESPEN · doi:10.1016/j.clnesp.2020.07.022 · Cited by 38 · see citing works
Caffeine Increases Maximal Fat Oxidation during a Graded Exercise Test: Is There a Diurnal Variation?
Ramírez-Maldonado, M., Jurado-Fasoli, L., del Coso, J., R. Ruiz, J., & Amaro-Gahete, F. J. (2021) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-020-00400-6 · Cited by 36 · see citing works
Transcriptomic and Metabolomic Profile Analysis of Muscles Reveals Pathways and Biomarkers Involved in Flavor Differences between Caged and Cage-Free Chickens
Yang, L., Yuan, F., Rong, L., Cai, J., Yang, S., Jia, Z., & Li, S. (2022) · Foods · doi:10.3390/foods11182890 · Cited by 36 · see citing works
Carbohydrate Intake in the Context of Exercise in People with Type 1 Diabetes
Scott, S. N., Kempf, P., Bally, L., & Stettler, C. (2019) · Nutrients · doi:10.3390/nu11123017 · Cited by 39 · see citing works
Acute Ketone Supplementation and Exercise Performance: A Systematic Review and Meta-Analysis of Randomized Controlled Trials
Valenzuela, P. L., Morales, J. S., Castillo‐García, A., & Lucía, A. (2020) · International Journal of Sports Physiology and Performance · doi:10.1123/ijspp.2019-0918 · Cited by 36 · see citing works
Carbohydrate Consumption and Periodization Strategies Applied to Elite Soccer Players
Fernandes, H. S. (2020) · Current Nutrition Reports · doi:10.1007/s13668-020-00338-w · Cited by 35 · see citing works
Muscle Glycogen Assessment and Relationship with Body Hydration Status: A Narrative Review
Shiose, K., Takahashi, H., & Yamada, Y. (2022) · Nutrients · doi:10.3390/nu15010155 · Cited by 35 · see citing works
Metabolic Adaptations to Weight Loss: A Brief Review
Martínez-Gómez, M. G., & Roberts, B. M. (2022) · Journal of Strength & Conditioning Research · doi:10.1519/jsc.0000000000003991 · Cited by 32 · see citing works
Creatine: A valuable supplement in aquafeeds?
Wuertz, S., & Reiser, S. (2022) · Reviews in Aquaculture · doi:10.1111/raq.12717 · Cited by 31 · see citing works
Biomarkers and genetic polymorphisms associated with maximal fat oxidation during physical exercise: implications for metabolic health and sports performance
Chávez-Guevara, I. A., Hernández‐Torres, R. P., González-Rodríguez, E., Ramos‐Jiménez, A., & Amaro‐Gahete, F. J. (2022) · European Journal of Applied Physiology · doi:10.1007/s00421-022-04936-0 · Cited by 31 · see citing works
No Modification in Blood Lipoprotein Concentration but Changes in Body Composition After 4 Weeks of Low Carbohydrate Diet (LCD) Followed by 7 Days of Carbohydrate Loading in Basketball Players
Michalczyk, M. M., Zając, A., Mikołajec, K., Zydek, G., & Langfort, J. (2018) · Journal of Human Kinetics · doi:10.2478/hukin-2018-0102 · Cited by 31 · see citing works
Impact of Physical Activity on Cellular Metabolism Across Both Neurodegenerative and General Neurological Conditions: A Narrative Review
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Carbohydrate Metabolism During Exercise
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Exercise and Muscle Glycogen Metabolism
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Sending the Signal: Muscle Glycogen Availability as a Regulator of Training Adaptation
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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: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
Health Sciences › Medicine › Complementary and alternative medicine › 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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