Inhibition of glycogenolysis prolongs action potential repriming period and impairs muscle function in rat skeletal muscle
Open accessAbstract
Key points: Muscle glycogen content is associated with muscle function, but the physiological link between the two is poorly understood. This study investigated the effects of inhibiting glycogenolysis, while maintaining high overall energy status, on different aspects of muscle function. We demonstrate here that Na+,K+‐ATPase activity depends on glycogenolytically derived ATP regardless of high global ATP, with a decrease in activity leading to reduced force production and accelerated fatigue development. The results support the concept of compartmentalized energy transfer with glycogen metabolism playing a crucial role in intramuscular ATP resynthesis and ion regulation. This study gives specific insights into muscular function and may help towards a better understanding of glycogen storage diseases and muscle fatigue. Skeletal muscle glycogen content is associated with muscle function and fatigability. However, little is known about the physiological link between glycogen content and muscle function. Here we aimed to investigate the importance of glycogenolytically derived ATP per se on muscle force and action potential (AP) repriming period, i.e. the time before a second AP can be produced (indicative of Na+,K+‐ATPase activity). Single fibres from rat extensor digitorum longus muscles were isolated and mechanically skinned in order to investigate force production and the AP repriming period while global ATP and PCr concentrations were kept high. The importance of glycogenolytically derived ATP was studied by inhibition of glycogen phosphorylase (1,4‐dideoxy‐1,4‐imino‐d‐arabinitol (DAB; 2 m m) or CP‐316,819 (CP; 10 µ m)) or glycogen removal (amyloglucosidase, 20 U ml−1). Tetanic force decreased by (mean (SD)) 21 (15)% (P < 0.001) and 76 (28)% (DAB) or 94 (6)% (CP, P < 0.001) in well‐polarized and partially depolarized fibres, respectively. In depolarized fibres, twitch force decreased by 16 (10)% and 55 (26)% with DAB and CP, respectively, with no effect in well‐polarized fibres (84 (10)%, P = 0.14). There was no effect of glycogen phosphorylase inhibition on repriming period in well‐polarized fibres (median (25th, 75th percentile): 5 (4, 5) vs. 4 (4, 5) ms, P = 0.26), while the repriming period was prolonged from 6 (5, 7) to 8 (7, 10) ms (P = 0.01) in partially depolarized fibres. In line with this, glycogen removal increased repriming period from 5 (5, 6) to 6 (5, 7) ms (P = 0.003) in depolarized fibres. Together, these data strongly indicate that blocking glycogenolysis attenuates Na+,K+‐ATPase activity, which in turn increases the repriming period and reduces force, demonstrating a functional link between glycogenolytically derived ATP and force production.
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Low muscle glycogen levels influence both force and power production by modulating muscle activation through effects on muscle excitability and sarcoplasmic reticulum Ca2+ release rate.
“Thus, low muscle glycogen levels influence both force and power production by modulating muscle activation through effects on muscle excitability and sarcoplasmic reticulum Ca2+ release rate [3, 14, 15], which becomes evident when muscle glycogen concentration falls below an apparent level of 250–200 mmol kg−1 dw in most [15, 16, 17], but not all studies [18].”
From Carbohydrate Storage and Supplementation Strategies for Peak Performance in Cross-Country Skiing (2026) · cites this paper as [14]
The Introduction (page unavailable) links low glycogen with reduced force, impaired sarcoplasmic-reticulum Ca2+ release rate, and possible effects on muscle excitability. The paper also examines force and excitability after inhibiting glycogen breakdown, but the passages do not address power production; that part of the attributed claim is unsupported. (LLM, conf=0.86)
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“Glycogen depletion may impair Na + ,K + -ATPase pump activity, and therefore the ability to regulate K + homeostasis and maintain muscle contractile function (Jensen et al. 2020).”
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“This effect would only reduce action potential generation between 100 and 200 Hz (Jensen et al., 2020) and we used 140 Hz.”
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“It is currently unclear what the exact underlying reasons for this are, but some evidence points towards utilisation of different muscle glycogen pools when exercising at different intensities and carbohydrate availability (Clark et al. 1985; Jensen et al. 2020a; Schytz et al. 2024).”
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A single oral glucose load decreases arterial plasma [K + ] during exercise and recovery
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“…reductions, extending previous findings from skinned single-fibres, where enzymatical glycogen removal or glycogen phosphorylase inhibition induced exacerbated force deteriorations in depolarised fibres, even in the presence of high global ATP and phosphocreatine levels (Jensen et al., 2020).”
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Carbohydrate Storage and Supplementation Strategies for Peak Performance in Cross-Country Skiing
Ørtenblad, N., Holmberg, H. ‐., Nybo, L., & Gejl, K. D. (2026) · Scandinavian Journal of Medicine & Science in Sports · doi:10.1111/sms.70242 · Cited by 1 · see citing works
Self-citationTrivino, A. R., Romero, C. D., Martín-Olmedo, J. J., Jiménez‐Martínez, P., Alix‐Fages, C., Cwiklinska, M., Pérez, D., & Jurado‐Fasoli, L. (2024) · European Journal of Applied Physiology · doi:10.1007/s00421-024-05689-8 · Cited by 1 · see citing works
“Therefore, maintaining minimum concentrations of muscle glycogen is essential for appropriate muscle contraction and exercise performance (Jensen et al. 2020).”
Renaud, J. (2020) · The Journal of Physiology · doi:10.1113/jp280698 · Cited by 1 · see citing works
“In an another study, an inhibition of glycogenolysis in mechanically skinned fibres exposed to a high ATP concentration (in the bathing solution) reduced t-tubular membrane excitability by diminishing Na+,K+-ATPase pump activity (Jensen et al. 2020).”
BackgroundLitwack, G. (2021) · Elsevier eBooks · doi:10.1016/b978-0-323-85718-5.00022-4
Impact of Nutrition and Exercise on Carbohydrate Metabolism
Matsunaga, Y. (2024) · BENTHAM SCIENCE PUBLISHERS eBooks · doi:10.2174/9789815313925124010005
Atanasovska, T., Farr, T., Smith, R. L., Petersen, A. C., GARNHAM, A. P., Andersen, M. J., Krum, H., Wong, C. Y., & McKenna, M. J. (2024) · The Journal of Physiology · doi:10.1113/jp287274
“This is consistent with an 8% inhibition of muscle NKA reducing muscle Lac − production, since NKA is fuelled by ATP supplied from glycogenolytic and glycolytic origins (Bundgaard et al., 2003; James et al., 1999; Jensen et al., 2020; McKenna, Renaud et al., 2024).”
A sympathetic nervous system theory of migraine
Rappoport, A. (2025) · Elsevier eBooks · doi:10.1016/b978-0-44-345008-2.00013-8
Matsumoto, M. S., Hamada, T., & Watanabe, D. (2025) · Journal of Muscle Research and Cell Motility · doi:10.1007/s10974-025-09702-1
“Additionally, recent studies have shown that glycogen depression, often observed during and after high-intensity exercise, can decrease membrane excitability (Cairns and Renaud 2023; Jensen et al. 2020; Watanabe and Wada 2019).”
Main, E., Yoon, S., James, S. L., Mellor, K. M., Brick, M. J., Leigh, W. B., & Maunder, E. (2026) · European Journal of Applied Physiology · doi:10.1007/s00421-026-06260-3
“Lowered muscle glycogen is linked to impaired Na⁺/K⁺-ATPase activity, disrupted Ca²⁺ handling, and reduced muscle contractile function (Ørten - blad et al. 2013; Duhamel et al. 2006a; Jensen et al. 2020a).”
- Authors
- Jensen, R., Nielsen, J., & Ørtenblad, N.
- Affiliations
- University of Southern Denmark (DK)
- Corresponding author
- Nielsen, Joachim
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2020-02
- Volume
- 598
- Issue
- 4
- Pages
- 789-803
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- OpenAlex
- W2995096992
- Cited by
- 38
- References
- 54
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 9 · 2023: 4 · 2022: 4 · 2021: 9 · 2020: 6
- FWCI
- 1.57
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed (publishedVersion)
- University of Southern Denmark Research Portal (University of Southern Denmark) (publishedVersion, other-oa)
- Funders
- Det Frie Forskningsråd (12‐132324)
- Lundbeckfonden (R118‐A11785, R164‐2013‐16132)
- Kulturministeriet (FPK.2017‐0013)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Keywords
- skeletal muscle glycogen, glycogenolysis, glycogen phosphorylase inhibition, Na+/K+-ATPase, muscle fatigue, muscle force production, glycogen storage disease, extensor digitorum longus, twitch force, depolarization, phosphocreatine
- MeSH terms
- Action Potentials, Animals, Glycogen, Muscle Contraction, Muscle, Skeletal, Muscle Fatigue, Glycogenolysis, Rats, In Vitro Techniques
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