Skip to main content
Top
Published in: Sports Medicine 9/2021

01-09-2021 | Fatigue | Review Article

Muscle Glycogen Metabolism and High-Intensity Exercise Performance: A Narrative Review

Authors: Jeppe F. Vigh-Larsen, Niels Ørtenblad, Lawrence L. Spriet, Kristian Overgaard, Magni Mohr

Published in: Sports Medicine | Issue 9/2021

Login to get access

Abstract

Muscle glycogen is the main substrate during high-intensity exercise and large reductions can occur after relatively short durations. Moreover, muscle glycogen is stored heterogeneously and similarly displays a heterogeneous and fiber-type specific depletion pattern with utilization in both fast- and slow-twitch fibers during high-intensity exercise, with a higher degradation rate in the former. Thus, depletion of individual fast- and slow-twitch fibers has been demonstrated despite muscle glycogen at the whole-muscle level only being moderately lowered. In addition, muscle glycogen is stored in specific subcellular compartments, which have been demonstrated to be important for muscle function and should be considered as well as global muscle glycogen availability. In the present review, we discuss the importance of glycogen metabolism for single and intermittent bouts of high-intensity exercise and outline possible underlying mechanisms for a relationship between muscle glycogen and fatigue during these types of exercise. Traditionally this relationship has been attributed to a decreased ATP resynthesis rate due to inadequate substrate availability at the whole-muscle level, but emerging evidence points to a direct coupling between muscle glycogen and steps in the excitation–contraction coupling including altered muscle excitability and calcium kinetics.
Literature
1.
go back to reference Christensen EH, Hansen O. Arbeitsfähigkeit und ernärung (Physical performance and nutrition). Skandinavishes Archiv für Physiolgie. 1939;81:160–71.CrossRef Christensen EH, Hansen O. Arbeitsfähigkeit und ernärung (Physical performance and nutrition). Skandinavishes Archiv für Physiolgie. 1939;81:160–71.CrossRef
2.
go back to reference Hargreaves M, Hawley JA, Jeukendrup A. Pre-exercise carbohydrate and fat ingestion: effects on metabolism and performance. J Sports Sci. 2004;22(1):31–8.PubMedCrossRef Hargreaves M, Hawley JA, Jeukendrup A. Pre-exercise carbohydrate and fat ingestion: effects on metabolism and performance. J Sports Sci. 2004;22(1):31–8.PubMedCrossRef
3.
go back to reference Bergstrom J, Hermansen L, Hultman E, Saltin B. Diet, muscle glycogen and physical performance. Acta Physiol Scand. 1967;71(2):140–50.PubMedCrossRef Bergstrom J, Hermansen L, Hultman E, Saltin B. Diet, muscle glycogen and physical performance. Acta Physiol Scand. 1967;71(2):140–50.PubMedCrossRef
4.
go back to reference Hermansen L, Hultman E, Saltin B. Muscle glycogen during prolonged severe exercise. Acta Physiol Scand. 1967;71(2):129–39.PubMedCrossRef Hermansen L, Hultman E, Saltin B. Muscle glycogen during prolonged severe exercise. Acta Physiol Scand. 1967;71(2):129–39.PubMedCrossRef
5.
go back to reference Karlsson J, Saltin B. Diet, muscle glycogen, and endurance performance. J Appl Physiol. 1971;31(2):203–6.PubMedCrossRef Karlsson J, Saltin B. Diet, muscle glycogen, and endurance performance. J Appl Physiol. 1971;31(2):203–6.PubMedCrossRef
6.
go back to reference Gollnick PD, Piehl K, Saubert CW, Armstrong RB, Saltin B. Diet, exercise, and glycogen changes in human muscle fibers. J Appl Physiol. 1972;33(4):421–5.PubMedCrossRef Gollnick PD, Piehl K, Saubert CW, Armstrong RB, Saltin B. Diet, exercise, and glycogen changes in human muscle fibers. J Appl Physiol. 1972;33(4):421–5.PubMedCrossRef
7.
go back to reference Costill DL, Gollnick PD, Jansson ED, Saltin B, Stein EM. Glycogen depletion pattern in human muscle fibres during distance running. Acta Physiol Scand. 1973;89(3):374–83.PubMedCrossRef Costill DL, Gollnick PD, Jansson ED, Saltin B, Stein EM. Glycogen depletion pattern in human muscle fibres during distance running. Acta Physiol Scand. 1973;89(3):374–83.PubMedCrossRef
8.
go back to reference Hargreaves M. Skeletal muscle metabolism during exercise in humans. Clin Exp Pharmacol Physiol. 2000;27(3):225–8.PubMedCrossRef Hargreaves M. Skeletal muscle metabolism during exercise in humans. Clin Exp Pharmacol Physiol. 2000;27(3):225–8.PubMedCrossRef
9.
go back to reference Gaitanos GC, Williams C, Boobis LH, Brooks S. Human muscle metabolism during intermittent maximal exercise. J Appl Physiol (1985). 1993;75(2):712–9.CrossRef Gaitanos GC, Williams C, Boobis LH, Brooks S. Human muscle metabolism during intermittent maximal exercise. J Appl Physiol (1985). 1993;75(2):712–9.CrossRef
10.
go back to reference Jensen TE, Richter EA. Regulation of glucose and glycogen metabolism during and after exercise. J Physiol. 2012;590(5):1069–76.PubMedCrossRef Jensen TE, Richter EA. Regulation of glucose and glycogen metabolism during and after exercise. J Physiol. 2012;590(5):1069–76.PubMedCrossRef
11.
go back to reference Parolin ML, Chesley A, Matsos MP, Spriet LL, Jones NL, Heigenhauser GJ. Regulation of skeletal muscle glycogen phosphorylase and PDH during maximal intermittent exercise. Am J Physiol. 1999;277(5):E890-900.PubMed Parolin ML, Chesley A, Matsos MP, Spriet LL, Jones NL, Heigenhauser GJ. Regulation of skeletal muscle glycogen phosphorylase and PDH during maximal intermittent exercise. Am J Physiol. 1999;277(5):E890-900.PubMed
12.
go back to reference Hultman E, Greenhaff PL. Skeletal muscle energy metabolism and fatigue during intense exercise in man. Sci Prog. 1991;75(298 Pt 3–4):361–70.PubMed Hultman E, Greenhaff PL. Skeletal muscle energy metabolism and fatigue during intense exercise in man. Sci Prog. 1991;75(298 Pt 3–4):361–70.PubMed
13.
go back to reference Clausen T, Nielsen OB. The Na+, K(+)-pump and muscle contractility. Acta Physiol Scand. 1994;152(4):365–73.PubMedCrossRef Clausen T, Nielsen OB. The Na+, K(+)-pump and muscle contractility. Acta Physiol Scand. 1994;152(4):365–73.PubMedCrossRef
14.
go back to reference Allen DG, Lamb GD, Westerblad H. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev. 2008;88(1):287–332.PubMedCrossRef Allen DG, Lamb GD, Westerblad H. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev. 2008;88(1):287–332.PubMedCrossRef
15.
go back to reference Fitts RH. The role of acidosis in fatigue: pro perspective. Med Sci Sports Exerc. 2016;48(11):2335–8.PubMedCrossRef Fitts RH. The role of acidosis in fatigue: pro perspective. Med Sci Sports Exerc. 2016;48(11):2335–8.PubMedCrossRef
16.
go back to reference Cheng AJ, Place N, Westerblad H. Molecular basis for exercise-induced fatigue: the importance of strictly controlled cellular Ca(2+) handling. Cold Spring Harb Perspect Med. 2018;8(2):a029710.PubMedPubMedCentralCrossRef Cheng AJ, Place N, Westerblad H. Molecular basis for exercise-induced fatigue: the importance of strictly controlled cellular Ca(2+) handling. Cold Spring Harb Perspect Med. 2018;8(2):a029710.PubMedPubMedCentralCrossRef
18.
go back to reference McKenna MJ, Bangsbo J, Renaud JM. Muscle K+, Na+, and Cl disturbances and Na+-K+ pump inactivation: implications for fatigue. J Appl Physiol (1985). 2008;104(1):288–95.CrossRef McKenna MJ, Bangsbo J, Renaud JM. Muscle K+, Na+, and Cl disturbances and Na+-K+ pump inactivation: implications for fatigue. J Appl Physiol (1985). 2008;104(1):288–95.CrossRef
19.
go back to reference Vigh-Larsen JF, Ermidis G, Rago V, Randers MB, Fransson D, Nielsen JL, et al. Muscle metabolism and fatigue during simulated ice hockey match-play in elite players. Med Sci Sports Exerc. 2020;52(10):2162–71.PubMedCrossRef Vigh-Larsen JF, Ermidis G, Rago V, Randers MB, Fransson D, Nielsen JL, et al. Muscle metabolism and fatigue during simulated ice hockey match-play in elite players. Med Sci Sports Exerc. 2020;52(10):2162–71.PubMedCrossRef
20.
go back to reference Gollnick PD, Armstrong RB, Sembrowich WL, Shepherd RE, Saltin B. Glycogen depletion pattern in human skeletal muscle fibers after heavy exercise. J Appl Physiol. 1973;34(5):615–8.PubMedCrossRef Gollnick PD, Armstrong RB, Sembrowich WL, Shepherd RE, Saltin B. Glycogen depletion pattern in human skeletal muscle fibers after heavy exercise. J Appl Physiol. 1973;34(5):615–8.PubMedCrossRef
21.
go back to reference Nielsen J, Ørtenblad N. Physiological aspects of the subcellular localization of glycogen in skeletal muscle. Appl Physiol Nutr Metab. 2013;38(2):91–9.PubMedCrossRef Nielsen J, Ørtenblad N. Physiological aspects of the subcellular localization of glycogen in skeletal muscle. Appl Physiol Nutr Metab. 2013;38(2):91–9.PubMedCrossRef
23.
go back to reference Marchand I, Chorneyko K, Tarnopolsky M, Hamilton S, Shearer J, Potvin J, et al. Quantification of subcellular glycogen in resting human muscle: granule size, number, and location. J Appl Physiol (1985). 2002;93(5):1598–607.CrossRef Marchand I, Chorneyko K, Tarnopolsky M, Hamilton S, Shearer J, Potvin J, et al. Quantification of subcellular glycogen in resting human muscle: granule size, number, and location. J Appl Physiol (1985). 2002;93(5):1598–607.CrossRef
24.
go back to reference Friden J, Seger J, Ekblom B. Topographical localization of muscle glycogen: an ultrahistochemical study in the human vastus lateralis. Acta Physiol Scand. 1989;135(3):381–91.PubMedCrossRef Friden J, Seger J, Ekblom B. Topographical localization of muscle glycogen: an ultrahistochemical study in the human vastus lateralis. Acta Physiol Scand. 1989;135(3):381–91.PubMedCrossRef
25.
go back to reference Friden J, Seger J, Ekblom B. Implementation of periodic acid-thiosemicarbazide-silver proteinate staining for ultrastructural assessment of muscle glycogen utilization during exercise. Cell Tissue Res. 1985;242(1):229–32.PubMedCrossRef Friden J, Seger J, Ekblom B. Implementation of periodic acid-thiosemicarbazide-silver proteinate staining for ultrastructural assessment of muscle glycogen utilization during exercise. Cell Tissue Res. 1985;242(1):229–32.PubMedCrossRef
26.
go back to reference Sjostrom M, Friden J, Ekblom B. Fine structural details of human muscle fibres after fibre type specific glycogen depletion. Histochemistry. 1982;76(4):425–38.PubMedCrossRef Sjostrom M, Friden J, Ekblom B. Fine structural details of human muscle fibres after fibre type specific glycogen depletion. Histochemistry. 1982;76(4):425–38.PubMedCrossRef
27.
go back to reference Chin ER, Allen DG. Effects of reduced muscle glycogen concentration on force, Ca2+ release and contractile protein function in intact mouse skeletal muscle. J Physiol. 1997;498(Pt 1):17–29.PubMedPubMedCentralCrossRef Chin ER, Allen DG. Effects of reduced muscle glycogen concentration on force, Ca2+ release and contractile protein function in intact mouse skeletal muscle. J Physiol. 1997;498(Pt 1):17–29.PubMedPubMedCentralCrossRef
28.
go back to reference Ørtenblad N, Nielsen J, Saltin B, Holmberg HC. Role of glycogen availability in sarcoplasmic reticulum Ca2+ kinetics in human skeletal muscle. J Physiol. 2011;589(Pt 3):711–25.PubMedCrossRef Ørtenblad N, Nielsen J, Saltin B, Holmberg HC. Role of glycogen availability in sarcoplasmic reticulum Ca2+ kinetics in human skeletal muscle. J Physiol. 2011;589(Pt 3):711–25.PubMedCrossRef
29.
go back to reference Bangsbo J, Graham TE, Kiens B, Saltin B. Elevated muscle glycogen and anaerobic energy production during exhaustive exercise in man. J Physiol. 1992;451:205–27.PubMedPubMedCentralCrossRef Bangsbo J, Graham TE, Kiens B, Saltin B. Elevated muscle glycogen and anaerobic energy production during exhaustive exercise in man. J Physiol. 1992;451:205–27.PubMedPubMedCentralCrossRef
30.
go back to reference Hargreaves M, Finn JP, Withers RT, Halbert JA, Scroop GC, Mackay M, et al. Effect of muscle glycogen availability on maximal exercise performance. Eur J Appl Physiol Occup Physiol. 1997;75(2):188–92.PubMedCrossRef Hargreaves M, Finn JP, Withers RT, Halbert JA, Scroop GC, Mackay M, et al. Effect of muscle glycogen availability on maximal exercise performance. Eur J Appl Physiol Occup Physiol. 1997;75(2):188–92.PubMedCrossRef
31.
go back to reference Balsom PD, Gaitanos GC, Soderlund K, Ekblom B. High-intensity exercise and muscle glycogen availability in humans. Acta Physiol Scand. 1999;165(4):337–45.PubMedCrossRef Balsom PD, Gaitanos GC, Soderlund K, Ekblom B. High-intensity exercise and muscle glycogen availability in humans. Acta Physiol Scand. 1999;165(4):337–45.PubMedCrossRef
32.
go back to reference Sahlin K, Tonkonogi M, Soderlund K. Energy supply and muscle fatigue in humans. Acta Physiol Scand. 1998;162(3):261–6.PubMedCrossRef Sahlin K, Tonkonogi M, Soderlund K. Energy supply and muscle fatigue in humans. Acta Physiol Scand. 1998;162(3):261–6.PubMedCrossRef
33.
go back to reference Green HJ. How important is endogenous muscle glycogen to fatigue in prolonged exercise? Can J Physiol Pharmacol. 1991;69(2):290–7.PubMedCrossRef Green HJ. How important is endogenous muscle glycogen to fatigue in prolonged exercise? Can J Physiol Pharmacol. 1991;69(2):290–7.PubMedCrossRef
34.
go back to reference Jensen R, Nielsen J, Ørtenblad N. Inhibition of glycogenolysis prolongs action potential repriming period and impairs muscle function in rat skeletal muscle. J Physiol. 2020;598(4):789–803.PubMedCrossRef Jensen R, Nielsen J, Ørtenblad N. Inhibition of glycogenolysis prolongs action potential repriming period and impairs muscle function in rat skeletal muscle. J Physiol. 2020;598(4):789–803.PubMedCrossRef
35.
go back to reference Watanabe D, Wada M. Effects of reduced muscle glycogen on excitation-contraction coupling in rat fast-twitch muscle: a glycogen removal study. J Muscle Res Cell Motil. 2019;40(3–4):353–64.PubMedCrossRef Watanabe D, Wada M. Effects of reduced muscle glycogen on excitation-contraction coupling in rat fast-twitch muscle: a glycogen removal study. J Muscle Res Cell Motil. 2019;40(3–4):353–64.PubMedCrossRef
36.
go back to reference Dutka TL, Lamb GD. Na+-K+ pumps in the transverse tubular system of skeletal muscle fibers preferentially use ATP from glycolysis. Am J Physiol Cell Physiol. 2007;293(3):C967–77.PubMedCrossRef Dutka TL, Lamb GD. Na+-K+ pumps in the transverse tubular system of skeletal muscle fibers preferentially use ATP from glycolysis. Am J Physiol Cell Physiol. 2007;293(3):C967–77.PubMedCrossRef
37.
go back to reference Helander I, Westerblad H, Katz A. Effects of glucose on contractile function, [Ca2+]i, and glycogen in isolated mouse skeletal muscle. Am J Physiol Cell Physiol. 2002;282(6):C1306–12.PubMedCrossRef Helander I, Westerblad H, Katz A. Effects of glucose on contractile function, [Ca2+]i, and glycogen in isolated mouse skeletal muscle. Am J Physiol Cell Physiol. 2002;282(6):C1306–12.PubMedCrossRef
38.
go back to reference Kabbara AA, Nguyen LT, Stephenson GM, Allen DG. Intracellular calcium during fatigue of cane toad skeletal muscle in the absence of glucose. J Muscle Res Cell Motil. 2000;21(5):481–9.PubMedCrossRef Kabbara AA, Nguyen LT, Stephenson GM, Allen DG. Intracellular calcium during fatigue of cane toad skeletal muscle in the absence of glucose. J Muscle Res Cell Motil. 2000;21(5):481–9.PubMedCrossRef
39.
go back to reference Nielsen J, Schroder HD, Rix CG, Ørtenblad N. Distinct effects of subcellular glycogen localization on tetanic relaxation time and endurance in mechanically skinned rat skeletal muscle fibres. J Physiol. 2009;587(Pt 14):3679–90.PubMedPubMedCentralCrossRef Nielsen J, Schroder HD, Rix CG, Ørtenblad N. Distinct effects of subcellular glycogen localization on tetanic relaxation time and endurance in mechanically skinned rat skeletal muscle fibres. J Physiol. 2009;587(Pt 14):3679–90.PubMedPubMedCentralCrossRef
40.
go back to reference Hearris MA, Hammond KM, Fell JM, Morton JP. Regulation of muscle glycogen metabolism during exercise: implications for endurance performance and training adaptations. Nutrients. 2018;10(3):298.PubMedCentralCrossRef Hearris MA, Hammond KM, Fell JM, Morton JP. Regulation of muscle glycogen metabolism during exercise: implications for endurance performance and training adaptations. Nutrients. 2018;10(3):298.PubMedCentralCrossRef
42.
go back to reference Areta JL, Hopkins WG. Skeletal muscle glycogen content at rest and during endurance exercise in humans: a meta-analysis. Sports Med. 2018;48(9):2091–102.PubMedCrossRef Areta JL, Hopkins WG. Skeletal muscle glycogen content at rest and during endurance exercise in humans: a meta-analysis. Sports Med. 2018;48(9):2091–102.PubMedCrossRef
43.
go back to reference Saltin B. Metabolic fundamentals in exercise. Med Sci Sports. 1973;5(3):137–46.PubMed Saltin B. Metabolic fundamentals in exercise. Med Sci Sports. 1973;5(3):137–46.PubMed
44.
go back to reference Saltin B, Karlsson J. Muscle glycogen utilization during work of different intensities. In: Pernow B, Saltin B, editors. Muscle metabolism during exercise. New York: Plenum pub; 1971. p. 289–99.CrossRef Saltin B, Karlsson J. Muscle glycogen utilization during work of different intensities. In: Pernow B, Saltin B, editors. Muscle metabolism during exercise. New York: Plenum pub; 1971. p. 289–99.CrossRef
45.
go back to reference Bogdanis GC, Nevill ME, Lakomy HK, Boobis LH. Power output and muscle metabolism during and following recovery from 10 and 20 s of maximal sprint exercise in humans. Acta Physiol Scand. 1998;163(3):261–72.PubMedCrossRef Bogdanis GC, Nevill ME, Lakomy HK, Boobis LH. Power output and muscle metabolism during and following recovery from 10 and 20 s of maximal sprint exercise in humans. Acta Physiol Scand. 1998;163(3):261–72.PubMedCrossRef
46.
go back to reference Bogdanis GC, Nevill ME, Boobis LH, Lakomy HK. Contribution of phosphocreatine and aerobic metabolism to energy supply during repeated sprint exercise. J Appl Physiol (1985). 1996;80(3):876–84.CrossRef Bogdanis GC, Nevill ME, Boobis LH, Lakomy HK. Contribution of phosphocreatine and aerobic metabolism to energy supply during repeated sprint exercise. J Appl Physiol (1985). 1996;80(3):876–84.CrossRef
47.
go back to reference Jones NL, McCartney N, Graham T, Spriet LL, Kowalchuk JM, Heigenhauser GJ, et al. Muscle performance and metabolism in maximal isokinetic cycling at slow and fast speeds. J Appl Physiol (1985). 1985;59(1):132–6.PubMedCrossRef Jones NL, McCartney N, Graham T, Spriet LL, Kowalchuk JM, Heigenhauser GJ, et al. Muscle performance and metabolism in maximal isokinetic cycling at slow and fast speeds. J Appl Physiol (1985). 1985;59(1):132–6.PubMedCrossRef
48.
go back to reference Greenhaff PL, Nevill ME, Soderlund K, Bodin K, Boobis LH, Williams C, et al. The metabolic responses of human type I and II muscle fibres during maximal treadmill sprinting. J Physiol. 1994;478(Pt 1):149–55.PubMedPubMedCentralCrossRef Greenhaff PL, Nevill ME, Soderlund K, Bodin K, Boobis LH, Williams C, et al. The metabolic responses of human type I and II muscle fibres during maximal treadmill sprinting. J Physiol. 1994;478(Pt 1):149–55.PubMedPubMedCentralCrossRef
49.
go back to reference Spriet LL. Anaerobic metabolism in human skeletal muscle during short-term, intense activity. Can J Physiol Pharmacol. 1992;70(1):157–65.PubMedCrossRef Spriet LL. Anaerobic metabolism in human skeletal muscle during short-term, intense activity. Can J Physiol Pharmacol. 1992;70(1):157–65.PubMedCrossRef
50.
go back to reference Spriet LL, Lindinger MI, McKelvie RS, Heigenhauser GJ, Jones NL. Muscle glycogenolysis and H+ concentration during maximal intermittent cycling. J Appl Physiol (1985). 1989;66(1):8–13.CrossRef Spriet LL, Lindinger MI, McKelvie RS, Heigenhauser GJ, Jones NL. Muscle glycogenolysis and H+ concentration during maximal intermittent cycling. J Appl Physiol (1985). 1989;66(1):8–13.CrossRef
51.
go back to reference Vollestad NK, Tabata I, Medbo JI. Glycogen breakdown in different human muscle fibre types during exhaustive exercise of short duration. Acta Physiol Scand. 1992;144(2):135–41.PubMedCrossRef Vollestad NK, Tabata I, Medbo JI. Glycogen breakdown in different human muscle fibre types during exhaustive exercise of short duration. Acta Physiol Scand. 1992;144(2):135–41.PubMedCrossRef
52.
go back to reference Vollestad NK, Blom PC. Effect of varying exercise intensity on glycogen depletion in human muscle fibres. Acta Physiol Scand. 1985;125(3):395–405.PubMedCrossRef Vollestad NK, Blom PC. Effect of varying exercise intensity on glycogen depletion in human muscle fibres. Acta Physiol Scand. 1985;125(3):395–405.PubMedCrossRef
53.
go back to reference Vollestad NK, Vaage O, Hermansen L. Muscle glycogen depletion patterns in type I and subgroups of type II fibres during prolonged severe exercise in man. Acta Physiol Scand. 1984;122(4):433–41.PubMedCrossRef Vollestad NK, Vaage O, Hermansen L. Muscle glycogen depletion patterns in type I and subgroups of type II fibres during prolonged severe exercise in man. Acta Physiol Scand. 1984;122(4):433–41.PubMedCrossRef
54.
go back to reference Gollnick PD, Armstrong RB, Saubert CW, Sembrowich WL, Shepherd RE, Saltin B. Glycogen depletion patterns in human skeletal muscle fibers during prolonged work. Pflugers Arch. 1973;344(1):1–12.PubMedCrossRef Gollnick PD, Armstrong RB, Saubert CW, Sembrowich WL, Shepherd RE, Saltin B. Glycogen depletion patterns in human skeletal muscle fibers during prolonged work. Pflugers Arch. 1973;344(1):1–12.PubMedCrossRef
55.
go back to reference Essen B. Intramuscular substrate utilization during prolonged exercise. Ann N Y Acad Sci. 1977;301:30–44.PubMedCrossRef Essen B. Intramuscular substrate utilization during prolonged exercise. Ann N Y Acad Sci. 1977;301:30–44.PubMedCrossRef
56.
go back to reference Krustrup P, Soderlund K, Mohr M, Gonzalez-Alonso J, Bangsbo J. Recruitment of fibre types and quadriceps muscle portions during repeated, intense knee-extensor exercise in humans. Pflugers Arch. 2004;449(1):56–65.PubMedCrossRef Krustrup P, Soderlund K, Mohr M, Gonzalez-Alonso J, Bangsbo J. Recruitment of fibre types and quadriceps muscle portions during repeated, intense knee-extensor exercise in humans. Pflugers Arch. 2004;449(1):56–65.PubMedCrossRef
57.
go back to reference Krustrup P, Mohr M, Steensberg A, Bencke J, Kjaer M, Bangsbo J. Muscle and blood metabolites during a soccer game: implications for sprint performance. Med Sci Sports Exerc. 2006;38(6):1165–74.PubMedCrossRef Krustrup P, Mohr M, Steensberg A, Bencke J, Kjaer M, Bangsbo J. Muscle and blood metabolites during a soccer game: implications for sprint performance. Med Sci Sports Exerc. 2006;38(6):1165–74.PubMedCrossRef
58.
go back to reference Ball-Burnett M, Green HJ, Houston ME. Energy metabolism in human slow and fast twitch fibres during prolonged cycle exercise. J Physiol. 1991;437:257–67.PubMedPubMedCentralCrossRef Ball-Burnett M, Green HJ, Houston ME. Energy metabolism in human slow and fast twitch fibres during prolonged cycle exercise. J Physiol. 1991;437:257–67.PubMedPubMedCentralCrossRef
59.
go back to reference Gollnick PD, Piehl K, Saltin B. Selective glycogen depletion pattern in human muscle fibres after exercise of varying intensity and at varying pedalling rates. J Physiol. 1974;241(1):45–57.PubMedPubMedCentralCrossRef Gollnick PD, Piehl K, Saltin B. Selective glycogen depletion pattern in human muscle fibres after exercise of varying intensity and at varying pedalling rates. J Physiol. 1974;241(1):45–57.PubMedPubMedCentralCrossRef
60.
go back to reference Kristensen DE, Albers PH, Prats C, Baba O, Birk JB, Wojtaszewski JF. Human muscle fibre type-specific regulation of AMPK and downstream targets by exercise. J Physiol. 2015;593(8):2053–69.PubMedPubMedCentralCrossRef Kristensen DE, Albers PH, Prats C, Baba O, Birk JB, Wojtaszewski JF. Human muscle fibre type-specific regulation of AMPK and downstream targets by exercise. J Physiol. 2015;593(8):2053–69.PubMedPubMedCentralCrossRef
61.
go back to reference Norman B, Sollevi A, Jansson E. Increased IMP content in glycogen-depleted muscle fibres during submaximal exercise in man. Acta Physiol Scand. 1988;133(1):97–100.PubMedCrossRef Norman B, Sollevi A, Jansson E. Increased IMP content in glycogen-depleted muscle fibres during submaximal exercise in man. Acta Physiol Scand. 1988;133(1):97–100.PubMedCrossRef
62.
go back to reference Sahlin K, Soderlund K, Tonkonogi M, Hirakoba K. Phosphocreatine content in single fibers of human muscle after sustained submaximal exercise. Am J Physiol. 1997;273(1 Pt 1):C172–8.PubMedCrossRef Sahlin K, Soderlund K, Tonkonogi M, Hirakoba K. Phosphocreatine content in single fibers of human muscle after sustained submaximal exercise. Am J Physiol. 1997;273(1 Pt 1):C172–8.PubMedCrossRef
63.
go back to reference Karatzaferi C, de Haan A, Ferguson RA, van Mechelen W, Sargeant AJ. Phosphocreatine and ATP content in human single muscle fibres before and after maximum dynamic exercise. Pflugers Arch. 2001;442(3):467–74.PubMedCrossRef Karatzaferi C, de Haan A, Ferguson RA, van Mechelen W, Sargeant AJ. Phosphocreatine and ATP content in human single muscle fibres before and after maximum dynamic exercise. Pflugers Arch. 2001;442(3):467–74.PubMedCrossRef
64.
go back to reference Ørtenblad N, Nielsen J. Muscle glycogen and cell function—location, location, location. Scand J Med Sci Sports. 2015;25(Suppl 4):34–40.PubMedCrossRef Ørtenblad N, Nielsen J. Muscle glycogen and cell function—location, location, location. Scand J Med Sci Sports. 2015;25(Suppl 4):34–40.PubMedCrossRef
65.
go back to reference Wanson JC, Drochmans P. Role of the sarcoplasmic reticulum in glycogen metabolism. Binding of phosphorylase, phosphorylase kinase, and primer complexes to the sarcovesicles of rabbit skeletal muscle. J Cell Biol. 1972;54(2):206–24.PubMedPubMedCentralCrossRef Wanson JC, Drochmans P. Role of the sarcoplasmic reticulum in glycogen metabolism. Binding of phosphorylase, phosphorylase kinase, and primer complexes to the sarcovesicles of rabbit skeletal muscle. J Cell Biol. 1972;54(2):206–24.PubMedPubMedCentralCrossRef
66.
go back to reference Wanson JC, Drochmans P. Rabbit skeletal muscle glycogen. A morphological and biochemical study of glycogen beta-particles isolated by the precipitation-centrifugation method. J Cell Biol. 1968;38(1):130–50.PubMedPubMedCentralCrossRef Wanson JC, Drochmans P. Rabbit skeletal muscle glycogen. A morphological and biochemical study of glycogen beta-particles isolated by the precipitation-centrifugation method. J Cell Biol. 1968;38(1):130–50.PubMedPubMedCentralCrossRef
67.
go back to reference Nielsen J, Cheng AJ, Ørtenblad N, Westerblad H. Subcellular distribution of glycogen and decreased tetanic Ca2+ in fatigued single intact mouse muscle fibres. J Physiol. 2014;592(9):2003–12.PubMedPubMedCentralCrossRef Nielsen J, Cheng AJ, Ørtenblad N, Westerblad H. Subcellular distribution of glycogen and decreased tetanic Ca2+ in fatigued single intact mouse muscle fibres. J Physiol. 2014;592(9):2003–12.PubMedPubMedCentralCrossRef
68.
go back to reference Jensen R, Ørtenblad N, Stausholm MH, Skjaerbaek MC, Larsen DN, Hansen M, et al. Heterogeneity in subcellular muscle glycogen utilisation during exercise impacts endurance capacity in men. J Physiol. 2020;598(19):4271–92.PubMedCrossRef Jensen R, Ørtenblad N, Stausholm MH, Skjaerbaek MC, Larsen DN, Hansen M, et al. Heterogeneity in subcellular muscle glycogen utilisation during exercise impacts endurance capacity in men. J Physiol. 2020;598(19):4271–92.PubMedCrossRef
69.
go back to reference Gejl KD, Ørtenblad N, Andersson E, Plomgaard P, Holmberg HC, Nielsen J. Local depletion of glycogen with supramaximal exercise in human skeletal muscle fibres. J Physiol. 2017;595(9):2809–21.PubMedCrossRef Gejl KD, Ørtenblad N, Andersson E, Plomgaard P, Holmberg HC, Nielsen J. Local depletion of glycogen with supramaximal exercise in human skeletal muscle fibres. J Physiol. 2017;595(9):2809–21.PubMedCrossRef
70.
go back to reference Nielsen J, Holmberg HC, Schroder HD, Saltin B, Ørtenblad N. Human skeletal muscle glycogen utilization in exhaustive exercise: role of subcellular localization and fibre type. J Physiol. 2011;589(Pt 11):2871–85.PubMedPubMedCentralCrossRef Nielsen J, Holmberg HC, Schroder HD, Saltin B, Ørtenblad N. Human skeletal muscle glycogen utilization in exhaustive exercise: role of subcellular localization and fibre type. J Physiol. 2011;589(Pt 11):2871–85.PubMedPubMedCentralCrossRef
71.
go back to reference Marchand I, Tarnopolsky M, Adamo KB, Bourgeois JM, Chorneyko K, Graham TE. Quantitative assessment of human muscle glycogen granules size and number in subcellular locations during recovery from prolonged exercise. J Physiol. 2007;580(Pt. 2):617–28.PubMedPubMedCentralCrossRef Marchand I, Tarnopolsky M, Adamo KB, Bourgeois JM, Chorneyko K, Graham TE. Quantitative assessment of human muscle glycogen granules size and number in subcellular locations during recovery from prolonged exercise. J Physiol. 2007;580(Pt. 2):617–28.PubMedPubMedCentralCrossRef
72.
go back to reference Hokken R, Laugesen S, Aagaard P, Suetta C, Frandsen U, Ørtenblad N, et al. Subcellular localization- and fibre type-dependent utilization of muscle glycogen during heavy resistance exercise in elite power and Olympic weightlifters. Acta Physiol (Oxf). 2021;231(2):e13561. Hokken R, Laugesen S, Aagaard P, Suetta C, Frandsen U, Ørtenblad N, et al. Subcellular localization- and fibre type-dependent utilization of muscle glycogen during heavy resistance exercise in elite power and Olympic weightlifters. Acta Physiol (Oxf). 2021;231(2):e13561.
73.
go back to reference Stephenson DG, Nguyen LT, Stephenson GM. Glycogen content and excitation-contraction coupling in mechanically skinned muscle fibres of the cane toad. J Physiol. 1999;519(Pt 1):177–87.PubMedPubMedCentralCrossRef Stephenson DG, Nguyen LT, Stephenson GM. Glycogen content and excitation-contraction coupling in mechanically skinned muscle fibres of the cane toad. J Physiol. 1999;519(Pt 1):177–87.PubMedPubMedCentralCrossRef
74.
go back to reference Barnes M, Gibson LM, Stephenson DG. Increased muscle glycogen content is associated with increased capacity to respond to T-system depolarisation in mechanically skinned skeletal muscle fibres from the rat. Pflugers Arch. 2001;442(1):101–6.PubMedCrossRef Barnes M, Gibson LM, Stephenson DG. Increased muscle glycogen content is associated with increased capacity to respond to T-system depolarisation in mechanically skinned skeletal muscle fibres from the rat. Pflugers Arch. 2001;442(1):101–6.PubMedCrossRef
75.
go back to reference Symons JD, Jacobs I. High-intensity exercise performance is not impaired by low intramuscular glycogen. Med Sci Sports Exerc. 1989;21(5):550–7.PubMedCrossRef Symons JD, Jacobs I. High-intensity exercise performance is not impaired by low intramuscular glycogen. Med Sci Sports Exerc. 1989;21(5):550–7.PubMedCrossRef
76.
go back to reference Greenhaff PL, Gleeson M, Maughan RJ. Diet-induced metabolic acidosis and the performance of high intensity exercise in man. Eur J Appl Physiol Occup Physiol. 1988;57(5):583–90.PubMedCrossRef Greenhaff PL, Gleeson M, Maughan RJ. Diet-induced metabolic acidosis and the performance of high intensity exercise in man. Eur J Appl Physiol Occup Physiol. 1988;57(5):583–90.PubMedCrossRef
77.
go back to reference Greenhaff PL, Gleeson M, Maughan RJ. The effects of dietary manipulation on blood acid-base status and the performance of high intensity exercise. Eur J Appl Physiol Occup Physiol. 1987;56(3):331–7.PubMedCrossRef Greenhaff PL, Gleeson M, Maughan RJ. The effects of dietary manipulation on blood acid-base status and the performance of high intensity exercise. Eur J Appl Physiol Occup Physiol. 1987;56(3):331–7.PubMedCrossRef
78.
go back to reference Greenhaff PL, Gleeson M, Whiting PH, Maughan RJ. Dietary composition and acid-base status: limiting factors in the performance of maximal exercise in man? Eur J Appl Physiol Occup Physiol. 1987;56(4):444–50.PubMedCrossRef Greenhaff PL, Gleeson M, Whiting PH, Maughan RJ. Dietary composition and acid-base status: limiting factors in the performance of maximal exercise in man? Eur J Appl Physiol Occup Physiol. 1987;56(4):444–50.PubMedCrossRef
79.
go back to reference Maughan RJ, Poole DC. The effects of a glycogen-loading regimen on the capacity to perform anaerobic exercise. Eur J Appl Physiol Occup Physiol. 1981;46(3):211–9.PubMedCrossRef Maughan RJ, Poole DC. The effects of a glycogen-loading regimen on the capacity to perform anaerobic exercise. Eur J Appl Physiol Occup Physiol. 1981;46(3):211–9.PubMedCrossRef
80.
go back to reference Jacobs I. Lactate concentrations after short, maximal exercise at various glycogen levels. Acta Physiol Scand. 1981;111(4):465–9.PubMedCrossRef Jacobs I. Lactate concentrations after short, maximal exercise at various glycogen levels. Acta Physiol Scand. 1981;111(4):465–9.PubMedCrossRef
81.
go back to reference Wootton SAWC. Influence of carbohydrate-status on performance during maximal exercise. Int J Sports Med. 1984;5:126–7.CrossRef Wootton SAWC. Influence of carbohydrate-status on performance during maximal exercise. Int J Sports Med. 1984;5:126–7.CrossRef
82.
go back to reference Young K, Davies CT. Effect of diet on human muscle weakness following prolonged exercise. Eur J Appl Physiol Occup Physiol. 1984;53(1):81–5.PubMedCrossRef Young K, Davies CT. Effect of diet on human muscle weakness following prolonged exercise. Eur J Appl Physiol Occup Physiol. 1984;53(1):81–5.PubMedCrossRef
85.
go back to reference Hargreaves M, McKenna MJ, Jenkins DG, Warmington SA, Li JL, Snow RJ, et al. Muscle metabolites and performance during high-intensity, intermittent exercise. J Appl Physiol (1985). 1998;84(5):1687–91.CrossRef Hargreaves M, McKenna MJ, Jenkins DG, Warmington SA, Li JL, Snow RJ, et al. Muscle metabolites and performance during high-intensity, intermittent exercise. J Appl Physiol (1985). 1998;84(5):1687–91.CrossRef
86.
go back to reference Vandenberghe K, Hespel P, Vanden Eynde B, Lysens R, Richter EA. No effect of glycogen level on glycogen metabolism during high intensity exercise. Med Sci Sports Exerc. 1995;27(9):1278–83.PubMedCrossRef Vandenberghe K, Hespel P, Vanden Eynde B, Lysens R, Richter EA. No effect of glycogen level on glycogen metabolism during high intensity exercise. Med Sci Sports Exerc. 1995;27(9):1278–83.PubMedCrossRef
87.
go back to reference Jenkins DG, Palmer J, Spillman D. The influence of dietary carbohydrate on performance of supramaximal intermittent exercise. Eur J Appl Physiol Occup Physiol. 1993;67(4):309–14.PubMedCrossRef Jenkins DG, Palmer J, Spillman D. The influence of dietary carbohydrate on performance of supramaximal intermittent exercise. Eur J Appl Physiol Occup Physiol. 1993;67(4):309–14.PubMedCrossRef
88.
go back to reference Casey A, Short AH, Curtis S, Greenhaff PL. The effect of glycogen availability on power output and the metabolic response to repeated bouts of maximal, isokinetic exercise in man. Eur J Appl Physiol Occup Physiol. 1996;72(3):249–55.PubMedCrossRef Casey A, Short AH, Curtis S, Greenhaff PL. The effect of glycogen availability on power output and the metabolic response to repeated bouts of maximal, isokinetic exercise in man. Eur J Appl Physiol Occup Physiol. 1996;72(3):249–55.PubMedCrossRef
89.
go back to reference Pizza FX, Flynn MG, Duscha BD, Holden J, Kubitz ER. A carbohydrate loading regimen improves high intensity, short duration exercise performance. Int J Sport Nutr. 1995;5(2):110–6.PubMedCrossRef Pizza FX, Flynn MG, Duscha BD, Holden J, Kubitz ER. A carbohydrate loading regimen improves high intensity, short duration exercise performance. Int J Sport Nutr. 1995;5(2):110–6.PubMedCrossRef
90.
go back to reference Mitchell JB, DiLauro PC, Pizza FX, Cavender DL. The effect of preexercise carbohydrate status on resistance exercise performance. Int J Sport Nutr. 1997;7(3):185–96.PubMedCrossRef Mitchell JB, DiLauro PC, Pizza FX, Cavender DL. The effect of preexercise carbohydrate status on resistance exercise performance. Int J Sport Nutr. 1997;7(3):185–96.PubMedCrossRef
91.
go back to reference Langfort J, Zarzeczny R, Pilis W, Nazar K, Kaciuba-Uscitko H. The effect of a low-carbohydrate diet on performance, hormonal and metabolic responses to a 30-s bout of supramaximal exercise. Eur J Appl Physiol Occup Physiol. 1997;76(2):128–33.PubMedCrossRef Langfort J, Zarzeczny R, Pilis W, Nazar K, Kaciuba-Uscitko H. The effect of a low-carbohydrate diet on performance, hormonal and metabolic responses to a 30-s bout of supramaximal exercise. Eur J Appl Physiol Occup Physiol. 1997;76(2):128–33.PubMedCrossRef
92.
go back to reference Leveritt M, Abernethy PJ. Effects of carbohydrate restriction on strength performance. J Strength Cond Res. 1999;13:52–7. Leveritt M, Abernethy PJ. Effects of carbohydrate restriction on strength performance. J Strength Cond Res. 1999;13:52–7.
93.
go back to reference Rockwell MS, Rankin JW, Dixon H. Effects of muscle glycogen on performance of repeated sprints and mechanisms of fatigue. Int J Sport Nutr Exerc Metab. 2003;13(1):1–14.PubMedCrossRef Rockwell MS, Rankin JW, Dixon H. Effects of muscle glycogen on performance of repeated sprints and mechanisms of fatigue. Int J Sport Nutr Exerc Metab. 2003;13(1):1–14.PubMedCrossRef
94.
go back to reference Hatfield DL, Kraemer WJ, Volek JS, Rubin MR, Grebien B, Gomez AL, et al. The effects of carbohydrate loading on repetitive jump squat power performance. J Strength Cond Res. 2006;20(1):167–71.PubMed Hatfield DL, Kraemer WJ, Volek JS, Rubin MR, Grebien B, Gomez AL, et al. The effects of carbohydrate loading on repetitive jump squat power performance. J Strength Cond Res. 2006;20(1):167–71.PubMed
95.
go back to reference Lima-Silva AE, Pires FO, Bertuzzi R, Silva-Cavalcante MD, Oliveira RS, Kiss MA, et al. Effects of a low- or a high-carbohydrate diet on performance, energy system contribution, and metabolic responses during supramaximal exercise. Appl Physiol Nutr Metab. 2013;38(9):928–34.PubMedCrossRef Lima-Silva AE, Pires FO, Bertuzzi R, Silva-Cavalcante MD, Oliveira RS, Kiss MA, et al. Effects of a low- or a high-carbohydrate diet on performance, energy system contribution, and metabolic responses during supramaximal exercise. Appl Physiol Nutr Metab. 2013;38(9):928–34.PubMedCrossRef
96.
go back to reference Skein M, Duffield R, Kelly BT, Marino FE. The effects of carbohydrate intake and muscle glycogen content on self-paced intermittent-sprint exercise despite no knowledge of carbohydrate manipulation. Eur J Appl Physiol. 2012;112(8):2859–70.PubMedCrossRef Skein M, Duffield R, Kelly BT, Marino FE. The effects of carbohydrate intake and muscle glycogen content on self-paced intermittent-sprint exercise despite no knowledge of carbohydrate manipulation. Eur J Appl Physiol. 2012;112(8):2859–70.PubMedCrossRef
97.
go back to reference Gejl KD, Hvid LG, Frandsen U, Jensen K, Sahlin K, Ørtenblad N. Muscle glycogen content modifies SR Ca2+ release rate in elite endurance athletes. Med Sci Sports Exerc. 2014;46(3):496–505.PubMedCrossRef Gejl KD, Hvid LG, Frandsen U, Jensen K, Sahlin K, Ørtenblad N. Muscle glycogen content modifies SR Ca2+ release rate in elite endurance athletes. Med Sci Sports Exerc. 2014;46(3):496–505.PubMedCrossRef
98.
go back to reference Oliver JM, Almada AL, Van Eck LE, Shah M, Mitchell JB, Jones MT, et al. Ingestion of high molecular weight carbohydrate enhances subsequent repeated maximal power: a randomized controlled trial. PLoS ONE. 2016;11(9):e0163009.PubMedPubMedCentralCrossRef Oliver JM, Almada AL, Van Eck LE, Shah M, Mitchell JB, Jones MT, et al. Ingestion of high molecular weight carbohydrate enhances subsequent repeated maximal power: a randomized controlled trial. PLoS ONE. 2016;11(9):e0163009.PubMedPubMedCentralCrossRef
99.
go back to reference Cheng AJ, Chaillou T, Kamandulis S, Subocius A, Westerblad H, Brazaitis M, et al. Carbohydrates do not accelerate force recovery after glycogen-depleting followed by high-intensity exercise in humans. Scand J Med Sci Sports. 2020;30(6):998–1007.PubMedCrossRef Cheng AJ, Chaillou T, Kamandulis S, Subocius A, Westerblad H, Brazaitis M, et al. Carbohydrates do not accelerate force recovery after glycogen-depleting followed by high-intensity exercise in humans. Scand J Med Sci Sports. 2020;30(6):998–1007.PubMedCrossRef
100.
go back to reference Akermark C, Jacobs I, Rasmusson M, Karlsson J. Diet and muscle glycogen concentration in relation to physical performance in Swedish elite ice hockey players. Int J Sport Nutr. 1996;6(3):272–84.PubMedCrossRef Akermark C, Jacobs I, Rasmusson M, Karlsson J. Diet and muscle glycogen concentration in relation to physical performance in Swedish elite ice hockey players. Int J Sport Nutr. 1996;6(3):272–84.PubMedCrossRef
101.
go back to reference Bangsbo J, Norregaard L, Thorsoe F. The effect of carbohydrate diet on intermittent exercise performance. Int J Sports Med. 1992;13(2):152–7.PubMedCrossRef Bangsbo J, Norregaard L, Thorsoe F. The effect of carbohydrate diet on intermittent exercise performance. Int J Sports Med. 1992;13(2):152–7.PubMedCrossRef
102.
go back to reference Bendiksen M, Bischoff R, Randers MB, Mohr M, Rollo I, Suetta C, et al. The Copenhagen Soccer Test: physiological response and fatigue development. Med Sci Sports Exerc. 2012;44(8):1595–603.PubMedCrossRef Bendiksen M, Bischoff R, Randers MB, Mohr M, Rollo I, Suetta C, et al. The Copenhagen Soccer Test: physiological response and fatigue development. Med Sci Sports Exerc. 2012;44(8):1595–603.PubMedCrossRef
103.
go back to reference Green HJ, Daub BD, Painter DC, Thomson JA. Glycogen depletion patterns during ice hockey performance. Med Sci Sports. 1978;10(4):289–93.PubMed Green HJ, Daub BD, Painter DC, Thomson JA. Glycogen depletion patterns during ice hockey performance. Med Sci Sports. 1978;10(4):289–93.PubMed
105.
go back to reference Krustrup P, Ørtenblad N, Nielsen J, Nybo L, Gunnarsson TP, Iaia FM, et al. Maximal voluntary contraction force, SR function and glycogen resynthesis during the first 72 h after a high-level competitive soccer game. Eur J Appl Physiol. 2011;111(12):2987–95.PubMedCrossRef Krustrup P, Ørtenblad N, Nielsen J, Nybo L, Gunnarsson TP, Iaia FM, et al. Maximal voluntary contraction force, SR function and glycogen resynthesis during the first 72 h after a high-level competitive soccer game. Eur J Appl Physiol. 2011;111(12):2987–95.PubMedCrossRef
106.
go back to reference Pascoe DD, Gladden LB. Muscle glycogen resynthesis after short term, high intensity exercise and resistance exercise. Sports Med. 1996;21(2):98–118.PubMedCrossRef Pascoe DD, Gladden LB. Muscle glycogen resynthesis after short term, high intensity exercise and resistance exercise. Sports Med. 1996;21(2):98–118.PubMedCrossRef
107.
go back to reference Jentjens R, Jeukendrup A. Determinants of post-exercise glycogen synthesis during short-term recovery. Sports Med. 2003;33(2):117–44.PubMedCrossRef Jentjens R, Jeukendrup A. Determinants of post-exercise glycogen synthesis during short-term recovery. Sports Med. 2003;33(2):117–44.PubMedCrossRef
108.
go back to reference Jacobs I, Kaiser P, Tesch P. Muscle strength and fatigue after selective glycogen depletion in human skeletal muscle fibers. Eur J Appl Physiol Occup Physiol. 1981;46(1):47–53.PubMedCrossRef Jacobs I, Kaiser P, Tesch P. Muscle strength and fatigue after selective glycogen depletion in human skeletal muscle fibers. Eur J Appl Physiol Occup Physiol. 1981;46(1):47–53.PubMedCrossRef
109.
go back to reference Karlsson J, Sjodin B, Jacobs I, Kaiser P. Relevance of muscle fibre type to fatigue in short intense and prolonged exercise in man. Ciba Found Symp. 1981;82:59–74.PubMed Karlsson J, Sjodin B, Jacobs I, Kaiser P. Relevance of muscle fibre type to fatigue in short intense and prolonged exercise in man. Ciba Found Symp. 1981;82:59–74.PubMed
110.
go back to reference Nybo L. CNS fatigue and prolonged exercise: effect of glucose supplementation. Med Sci Sports Exerc. 2003;35(4):589–94.PubMedCrossRef Nybo L. CNS fatigue and prolonged exercise: effect of glucose supplementation. Med Sci Sports Exerc. 2003;35(4):589–94.PubMedCrossRef
111.
go back to reference Sahlin K, Katz A, Broberg S. Tricarboxylic acid cycle intermediates in human muscle during prolonged exercise. Am J Physiol. 1990;259(5 Pt 1):C834–41.PubMedCrossRef Sahlin K, Katz A, Broberg S. Tricarboxylic acid cycle intermediates in human muscle during prolonged exercise. Am J Physiol. 1990;259(5 Pt 1):C834–41.PubMedCrossRef
112.
go back to reference Norman B, Sollevi A, Kaijser L, Jansson E. ATP breakdown products in human skeletal muscle during prolonged exercise to exhaustion. Clin Physiol. 1987;7(6):503–10.PubMedCrossRef Norman B, Sollevi A, Kaijser L, Jansson E. ATP breakdown products in human skeletal muscle during prolonged exercise to exhaustion. Clin Physiol. 1987;7(6):503–10.PubMedCrossRef
113.
go back to reference Broberg S, Sahlin K. Adenine nucleotide degradation in human skeletal muscle during prolonged exercise. J Appl Physiol (1985). 1989;67(1):116–22.CrossRef Broberg S, Sahlin K. Adenine nucleotide degradation in human skeletal muscle during prolonged exercise. J Appl Physiol (1985). 1989;67(1):116–22.CrossRef
114.
go back to reference Sahlin K, Broberg S, Ren JM. Formation of inosine monophosphate (IMP) in human skeletal muscle during incremental dynamic exercise. Acta Physiol Scand. 1989;136(2):193–8.PubMedCrossRef Sahlin K, Broberg S, Ren JM. Formation of inosine monophosphate (IMP) in human skeletal muscle during incremental dynamic exercise. Acta Physiol Scand. 1989;136(2):193–8.PubMedCrossRef
115.
go back to reference Gollnick PD, Karlsson J, Piehl K, Saltin B. Selective glycogen depletion in skeletal muscle fibres of man following sustained contractions. J Physiol. 1974;241(1):59–67.PubMedPubMedCentralCrossRef Gollnick PD, Karlsson J, Piehl K, Saltin B. Selective glycogen depletion in skeletal muscle fibres of man following sustained contractions. J Physiol. 1974;241(1):59–67.PubMedPubMedCentralCrossRef
116.
go back to reference Meyer RA, Terjung RL. AMP deamination and IMP reamination in working skeletal muscle. Am J Physiol. 1980;239(1):C32–8.PubMedCrossRef Meyer RA, Terjung RL. AMP deamination and IMP reamination in working skeletal muscle. Am J Physiol. 1980;239(1):C32–8.PubMedCrossRef
117.
go back to reference Nelson CR, Debold EP, Fitts RH. Phosphate and acidosis act synergistically to depress peak power in rat muscle fibers. Am J Physiol Cell Physiol. 2014;307(10):C939–50.PubMedPubMedCentralCrossRef Nelson CR, Debold EP, Fitts RH. Phosphate and acidosis act synergistically to depress peak power in rat muscle fibers. Am J Physiol Cell Physiol. 2014;307(10):C939–50.PubMedPubMedCentralCrossRef
118.
go back to reference Bangsbo J, Graham T, Johansen L, Strange S, Christensen C, Saltin B. Elevated muscle acidity and energy production during exhaustive exercise in humans. Am J Physiol. 1992;263(4 Pt 2):R891–9.PubMed Bangsbo J, Graham T, Johansen L, Strange S, Christensen C, Saltin B. Elevated muscle acidity and energy production during exhaustive exercise in humans. Am J Physiol. 1992;263(4 Pt 2):R891–9.PubMed
119.
go back to reference Sherman WM, Costill DL, Fink WJ, Miller JM. Effect of exercise-diet manipulation on muscle glycogen and its subsequent utilization during performance. Int J Sports Med. 1981;2(2):114–8.PubMedCrossRef Sherman WM, Costill DL, Fink WJ, Miller JM. Effect of exercise-diet manipulation on muscle glycogen and its subsequent utilization during performance. Int J Sports Med. 1981;2(2):114–8.PubMedCrossRef
120.
go back to reference Bosch AN, Dennis SC, Noakes TD. Influence of carbohydrate loading on fuel substrate turnover and oxidation during prolonged exercise. J Appl Physiol (1985). 1993;74(4):1921–7.CrossRef Bosch AN, Dennis SC, Noakes TD. Influence of carbohydrate loading on fuel substrate turnover and oxidation during prolonged exercise. J Appl Physiol (1985). 1993;74(4):1921–7.CrossRef
121.
go back to reference Putman CT, Spriet LL, Hultman E, Lindinger MI, Lands LC, McKelvie RS, et al. Pyruvate dehydrogenase activity and acetyl group accumulation during exercise after different diets. Am J Physiol. 1993;265(5 Pt 1):E752–60.PubMed Putman CT, Spriet LL, Hultman E, Lindinger MI, Lands LC, McKelvie RS, et al. Pyruvate dehydrogenase activity and acetyl group accumulation during exercise after different diets. Am J Physiol. 1993;265(5 Pt 1):E752–60.PubMed
122.
go back to reference Hargreaves M, McConell G, Proietto J. Influence of muscle glycogen on glycogenolysis and glucose uptake during exercise in humans. J Appl Physiol (1985). 1995;78(1):288–92.CrossRef Hargreaves M, McConell G, Proietto J. Influence of muscle glycogen on glycogenolysis and glucose uptake during exercise in humans. J Appl Physiol (1985). 1995;78(1):288–92.CrossRef
123.
go back to reference Madsen K, Pedersen PK, Rose P, Richter EA. Carbohydrate supercompensation and muscle glycogen utilization during exhaustive running in highly trained athletes. Eur J Appl Physiol Occup Physiol. 1990;61(5–6):467–72.PubMedCrossRef Madsen K, Pedersen PK, Rose P, Richter EA. Carbohydrate supercompensation and muscle glycogen utilization during exhaustive running in highly trained athletes. Eur J Appl Physiol Occup Physiol. 1990;61(5–6):467–72.PubMedCrossRef
124.
go back to reference Costill DL, Coyle E, Dalsky G, Evans W, Fink W, Hoopes D. Effects of elevated plasma FFA and insulin on muscle glycogen usage during exercise. J Appl Physiol Respir Environ Exerc Physiol. 1977;43(4):695–9.PubMed Costill DL, Coyle E, Dalsky G, Evans W, Fink W, Hoopes D. Effects of elevated plasma FFA and insulin on muscle glycogen usage during exercise. J Appl Physiol Respir Environ Exerc Physiol. 1977;43(4):695–9.PubMed
125.
126.
go back to reference Stellingwerff T, Spriet LL, Watt MJ, Kimber NE, Hargreaves M, Hawley JA, et al. Decreased PDH activation and glycogenolysis during exercise following fat adaptation with carbohydrate restoration. Am J Physiol Endocrinol Metab. 2006;290(2):E380–8.PubMedCrossRef Stellingwerff T, Spriet LL, Watt MJ, Kimber NE, Hargreaves M, Hawley JA, et al. Decreased PDH activation and glycogenolysis during exercise following fat adaptation with carbohydrate restoration. Am J Physiol Endocrinol Metab. 2006;290(2):E380–8.PubMedCrossRef
127.
go back to reference Hespel P, Richter EA. Glucose uptake and transport in contracting, perfused rat muscle with different pre-contraction glycogen concentrations. J Physiol. 1990;427:347–59.PubMedPubMedCentralCrossRef Hespel P, Richter EA. Glucose uptake and transport in contracting, perfused rat muscle with different pre-contraction glycogen concentrations. J Physiol. 1990;427:347–59.PubMedPubMedCentralCrossRef
128.
go back to reference Hespel P, Richter EA. Mechanism linking glycogen concentration and glycogenolytic rate in perfused contracting rat skeletal muscle. Biochem J. 1992;284(Pt 3):777–80.PubMedPubMedCentralCrossRef Hespel P, Richter EA. Mechanism linking glycogen concentration and glycogenolytic rate in perfused contracting rat skeletal muscle. Biochem J. 1992;284(Pt 3):777–80.PubMedPubMedCentralCrossRef
129.
go back to reference Richter EA, Galbo H. High glycogen levels enhance glycogen breakdown in isolated contracting skeletal muscle. J Appl Physiol (1985). 1986;61(3):827–31.CrossRef Richter EA, Galbo H. High glycogen levels enhance glycogen breakdown in isolated contracting skeletal muscle. J Appl Physiol (1985). 1986;61(3):827–31.CrossRef
130.
go back to reference Spriet LL, Berardinucci L, Marsh DR, Campbell CB, Graham TE. Glycogen content has no effect on skeletal muscle glycogenolysis during short-term tetanic stimulation. J Appl Physiol (1985). 1990;68(5):1883–8.CrossRef Spriet LL, Berardinucci L, Marsh DR, Campbell CB, Graham TE. Glycogen content has no effect on skeletal muscle glycogenolysis during short-term tetanic stimulation. J Appl Physiol (1985). 1990;68(5):1883–8.CrossRef
131.
go back to reference Vandenberghe K, Richter EA, Hespel P. Regulation of glycogen breakdown by glycogen level in contracting rat muscle. Acta Physiol Scand. 1999;165(3):307–14.PubMedCrossRef Vandenberghe K, Richter EA, Hespel P. Regulation of glycogen breakdown by glycogen level in contracting rat muscle. Acta Physiol Scand. 1999;165(3):307–14.PubMedCrossRef
132.
go back to reference Klausen K, Sjogaard G. Glycogen stores and lactate accumulation in skeletal muscle of man during intense bicycle exercise. Scand J Sports Sci. 1980;2(1):7–12. Klausen K, Sjogaard G. Glycogen stores and lactate accumulation in skeletal muscle of man during intense bicycle exercise. Scand J Sports Sci. 1980;2(1):7–12.
133.
go back to reference Boobis LH, Williams C, Wootton SA. Influence of sprint training on muscle metabolism during brief maximal exercise in man. J Physiol. 1983;342:36–7. Boobis LH, Williams C, Wootton SA. Influence of sprint training on muscle metabolism during brief maximal exercise in man. J Physiol. 1983;342:36–7.
134.
go back to reference Ren JM, Broberg S, Sahlin K, Hultman E. Influence of reduced glycogen level on glycogenolysis during short-term stimulation in man. Acta Physiol Scand. 1990;139(3):467–74.PubMedCrossRef Ren JM, Broberg S, Sahlin K, Hultman E. Influence of reduced glycogen level on glycogenolysis during short-term stimulation in man. Acta Physiol Scand. 1990;139(3):467–74.PubMedCrossRef
135.
go back to reference Spencer MK, Katz A. Role of glycogen in control of glycolysis and IMP formation in human muscle during exercise. Am J Physiol. 1991;260(6 Pt 1):E859–64.PubMed Spencer MK, Katz A. Role of glycogen in control of glycolysis and IMP formation in human muscle during exercise. Am J Physiol. 1991;260(6 Pt 1):E859–64.PubMed
136.
go back to reference Greenhaff PL, Gleeson M, Maughan RJ. The effects of a glycogen loading regimen on acid-base status and blood lactate concentration before and after a fixed period of high intensity exercise in man. Eur J Appl Physiol Occup Physiol. 1988;57(2):254–9.PubMedCrossRef Greenhaff PL, Gleeson M, Maughan RJ. The effects of a glycogen loading regimen on acid-base status and blood lactate concentration before and after a fixed period of high intensity exercise in man. Eur J Appl Physiol Occup Physiol. 1988;57(2):254–9.PubMedCrossRef
137.
go back to reference Greenhaff PL, Gleeson M, Maughan RJ. The effects of diet on muscle pH and metabolism during high intensity exercise. Eur J Appl Physiol Occup Physiol. 1988;57(5):531–9.PubMedCrossRef Greenhaff PL, Gleeson M, Maughan RJ. The effects of diet on muscle pH and metabolism during high intensity exercise. Eur J Appl Physiol Occup Physiol. 1988;57(5):531–9.PubMedCrossRef
138.
go back to reference Spriet LL. New insights into the interaction of carbohydrate and fat metabolism during exercise. Sports Med. 2014;44(Suppl 1):S87-96.PubMedCrossRef Spriet LL. New insights into the interaction of carbohydrate and fat metabolism during exercise. Sports Med. 2014;44(Suppl 1):S87-96.PubMedCrossRef
139.
go back to reference Sahlin K, Harris RC. Control of lipid oxidation during exercise: role of energy state and mitochondrial factors. Acta Physiol (Oxf). 2008;194(4):283–91.CrossRef Sahlin K, Harris RC. Control of lipid oxidation during exercise: role of energy state and mitochondrial factors. Acta Physiol (Oxf). 2008;194(4):283–91.CrossRef
140.
go back to reference Sahlin K, Sallstedt EK, Bishop D, Tonkonogi M. Turning down lipid oxidation during heavy exercise–what is the mechanism? J Physiol Pharmacol. 2008;59(Suppl 7):19–30.PubMed Sahlin K, Sallstedt EK, Bishop D, Tonkonogi M. Turning down lipid oxidation during heavy exercise–what is the mechanism? J Physiol Pharmacol. 2008;59(Suppl 7):19–30.PubMed
141.
go back to reference Hargreaves M. Exercise, muscle, and CHO metabolism. Scand J Med Sci Sports. 2015;25(Suppl 4):29–33.PubMedCrossRef Hargreaves M. Exercise, muscle, and CHO metabolism. Scand J Med Sci Sports. 2015;25(Suppl 4):29–33.PubMedCrossRef
142.
go back to reference Ørtenblad N, Macdonald WA, Sahlin K. Glycolysis in contracting rat skeletal muscle is controlled by factors related to energy state. Biochem J. 2009;420(2):161–8.PubMedCrossRef Ørtenblad N, Macdonald WA, Sahlin K. Glycolysis in contracting rat skeletal muscle is controlled by factors related to energy state. Biochem J. 2009;420(2):161–8.PubMedCrossRef
143.
go back to reference Newsholme EA, Start C. Regulation in metabolism. Toronto: Wiley; 1973. Newsholme EA, Start C. Regulation in metabolism. Toronto: Wiley; 1973.
144.
go back to reference Juel C, Pilegaard H, Nielsen JJ, Bangsbo J. Interstitial K(+) in human skeletal muscle during and after dynamic graded exercise determined by microdialysis. Am J Physiol Regul Integr Comp Physiol. 2000;278(2):R400–6.PubMedCrossRef Juel C, Pilegaard H, Nielsen JJ, Bangsbo J. Interstitial K(+) in human skeletal muscle during and after dynamic graded exercise determined by microdialysis. Am J Physiol Regul Integr Comp Physiol. 2000;278(2):R400–6.PubMedCrossRef
145.
146.
go back to reference Nordsborg N, Mohr M, Pedersen LD, Nielsen JJ, Langberg H, Bangsbo J. Muscle interstitial potassium kinetics during intense exhaustive exercise: effect of previous arm exercise. Am J Physiol Regul Integr Comp Physiol. 2003;285(1):R143–8.PubMedCrossRef Nordsborg N, Mohr M, Pedersen LD, Nielsen JJ, Langberg H, Bangsbo J. Muscle interstitial potassium kinetics during intense exhaustive exercise: effect of previous arm exercise. Am J Physiol Regul Integr Comp Physiol. 2003;285(1):R143–8.PubMedCrossRef
147.
go back to reference Mohr M, Nordsborg N, Nielsen JJ, Pedersen LD, Fischer C, Krustrup P, et al. Potassium kinetics in human muscle interstitium during repeated intense exercise in relation to fatigue. Pflugers Arch. 2004;448(4):452–6.PubMedCrossRef Mohr M, Nordsborg N, Nielsen JJ, Pedersen LD, Fischer C, Krustrup P, et al. Potassium kinetics in human muscle interstitium during repeated intense exercise in relation to fatigue. Pflugers Arch. 2004;448(4):452–6.PubMedCrossRef
148.
go back to reference Cairns SP, Flatman JA, Clausen T. Relation between extracellular [K+], membrane potential and contraction in rat soleus muscle: modulation by the Na+-K+ pump. Pflugers Arch. 1995;430(6):909–15.PubMedCrossRef Cairns SP, Flatman JA, Clausen T. Relation between extracellular [K+], membrane potential and contraction in rat soleus muscle: modulation by the Na+-K+ pump. Pflugers Arch. 1995;430(6):909–15.PubMedCrossRef
149.
go back to reference Sejersted OM, Sjogaard G. Dynamics and consequences of potassium shifts in skeletal muscle and heart during exercise. Physiol Rev. 2000;80(4):1411–81.PubMedCrossRef Sejersted OM, Sjogaard G. Dynamics and consequences of potassium shifts in skeletal muscle and heart during exercise. Physiol Rev. 2000;80(4):1411–81.PubMedCrossRef
150.
go back to reference Ruff RL. Sodium channel slow inactivation and the distribution of sodium channels on skeletal muscle fibres enable the performance properties of different skeletal muscle fibre types. Acta Physiol Scand. 1996;156(3):159–68.PubMedCrossRef Ruff RL. Sodium channel slow inactivation and the distribution of sodium channels on skeletal muscle fibres enable the performance properties of different skeletal muscle fibre types. Acta Physiol Scand. 1996;156(3):159–68.PubMedCrossRef
151.
go back to reference Pedersen TH, Clausen T, Nielsen OB. Loss of force induced by high extracellular [K+] in rat muscle: effect of temperature, lactic acid and beta2-agonist. J Physiol. 2003;551(Pt 1):277–86.PubMedPubMedCentralCrossRef Pedersen TH, Clausen T, Nielsen OB. Loss of force induced by high extracellular [K+] in rat muscle: effect of temperature, lactic acid and beta2-agonist. J Physiol. 2003;551(Pt 1):277–86.PubMedPubMedCentralCrossRef
152.
go back to reference de Paoli FV, Overgaard K, Pedersen TH, Nielsen OB. Additive protective effects of the addition of lactic acid and adrenaline on excitability and force in isolated rat skeletal muscle depressed by elevated extracellular K+. J Physiol. 2007;581(Pt 2):829–39.PubMedPubMedCentralCrossRef de Paoli FV, Overgaard K, Pedersen TH, Nielsen OB. Additive protective effects of the addition of lactic acid and adrenaline on excitability and force in isolated rat skeletal muscle depressed by elevated extracellular K+. J Physiol. 2007;581(Pt 2):829–39.PubMedPubMedCentralCrossRef
153.
go back to reference Overgaard K, Nielsen OB. Activity-induced recovery of excitability in K(+)-depressed rat soleus muscle. Am J Physiol Regul Integr Comp Physiol. 2001;280(1):R48-55.PubMedCrossRef Overgaard K, Nielsen OB. Activity-induced recovery of excitability in K(+)-depressed rat soleus muscle. Am J Physiol Regul Integr Comp Physiol. 2001;280(1):R48-55.PubMedCrossRef
154.
go back to reference Leppik JA, Aughey RJ, Medved I, Fairweather I, Carey MF, McKenna MJ. Prolonged exercise to fatigue in humans impairs skeletal muscle Na+-K+-ATPase activity, sarcoplasmic reticulum Ca2+ release, and Ca2+ uptake. J Appl Physiol (1985). 2004;97(4):1414–23.CrossRef Leppik JA, Aughey RJ, Medved I, Fairweather I, Carey MF, McKenna MJ. Prolonged exercise to fatigue in humans impairs skeletal muscle Na+-K+-ATPase activity, sarcoplasmic reticulum Ca2+ release, and Ca2+ uptake. J Appl Physiol (1985). 2004;97(4):1414–23.CrossRef
155.
go back to reference Fowles JR, Green HJ, Tupling R, O’Brien S, Roy BD. Human neuromuscular fatigue is associated with altered Na+-K+-ATPase activity following isometric exercise. J Appl Physiol (1985). 2002;92(4):1585–93.CrossRef Fowles JR, Green HJ, Tupling R, O’Brien S, Roy BD. Human neuromuscular fatigue is associated with altered Na+-K+-ATPase activity following isometric exercise. J Appl Physiol (1985). 2002;92(4):1585–93.CrossRef
156.
go back to reference Fraser SF, Li JL, Carey MF, Wang XN, Sangkabutra T, Sostaric S, et al. Fatigue depresses maximal in vitro skeletal muscle Na(+)-K(+)-ATPase activity in untrained and trained individuals. J Appl Physiol (1985). 2002;93(5):1650–9.CrossRef Fraser SF, Li JL, Carey MF, Wang XN, Sangkabutra T, Sostaric S, et al. Fatigue depresses maximal in vitro skeletal muscle Na(+)-K(+)-ATPase activity in untrained and trained individuals. J Appl Physiol (1985). 2002;93(5):1650–9.CrossRef
157.
go back to reference Aughey RJ, Clark SA, Gore CJ, Townsend NE, Hahn AG, Kinsman TA, et al. Interspersed normoxia during live high, train low interventions reverses an early reduction in muscle Na+, K +ATPase activity in well-trained athletes. Eur J Appl Physiol. 2006;98(3):299–309.PubMedCrossRef Aughey RJ, Clark SA, Gore CJ, Townsend NE, Hahn AG, Kinsman TA, et al. Interspersed normoxia during live high, train low interventions reverses an early reduction in muscle Na+, K +ATPase activity in well-trained athletes. Eur J Appl Physiol. 2006;98(3):299–309.PubMedCrossRef
158.
go back to reference Petersen AC, Murphy KT, Snow RJ, Leppik JA, Aughey RJ, Garnham AP, et al. Depressed Na+-K+-ATPase activity in skeletal muscle at fatigue is correlated with increased Na+-K+-ATPase mRNA expression following intense exercise. Am J Physiol Regul Integr Comp Physiol. 2005;289(1):R266–74.PubMedCrossRef Petersen AC, Murphy KT, Snow RJ, Leppik JA, Aughey RJ, Garnham AP, et al. Depressed Na+-K+-ATPase activity in skeletal muscle at fatigue is correlated with increased Na+-K+-ATPase mRNA expression following intense exercise. Am J Physiol Regul Integr Comp Physiol. 2005;289(1):R266–74.PubMedCrossRef
159.
go back to reference Sandiford SD, Green HJ, Duhamel TA, Perco JG, Schertzer JD, Ouyang J. Inactivation of human muscle Na+-K+-ATPase in vitro during prolonged exercise is increased with hypoxia. J Appl Physiol (1985). 2004;96(5):1767–75.CrossRef Sandiford SD, Green HJ, Duhamel TA, Perco JG, Schertzer JD, Ouyang J. Inactivation of human muscle Na+-K+-ATPase in vitro during prolonged exercise is increased with hypoxia. J Appl Physiol (1985). 2004;96(5):1767–75.CrossRef
160.
go back to reference Aughey RJ, Murphy KT, Clark SA, Garnham AP, Snow RJ, Cameron-Smith D, et al. Muscle Na+-K+-ATPase activity and isoform adaptations to intense interval exercise and training in well-trained athletes. J Appl Physiol (1985). 2007;103(1):39–47.CrossRef Aughey RJ, Murphy KT, Clark SA, Garnham AP, Snow RJ, Cameron-Smith D, et al. Muscle Na+-K+-ATPase activity and isoform adaptations to intense interval exercise and training in well-trained athletes. J Appl Physiol (1985). 2007;103(1):39–47.CrossRef
161.
go back to reference Jannas-Vela S, Brownell S, Petrick HL, Heigenhauser GJF, Spriet LL, Holloway GP. Assessment of Na+/K+ ATPase activity in small rodent and human skeletal muscle samples. Med Sci Sports Exerc. 2019;51(11):2403–9.PubMedCrossRef Jannas-Vela S, Brownell S, Petrick HL, Heigenhauser GJF, Spriet LL, Holloway GP. Assessment of Na+/K+ ATPase activity in small rodent and human skeletal muscle samples. Med Sci Sports Exerc. 2019;51(11):2403–9.PubMedCrossRef
162.
go back to reference Juel C, Hostrup M, Bangsbo J. The effect of exercise and beta2-adrenergic stimulation on glutathionylation and function of the Na, K-ATPase in human skeletal muscle. Physiol Rep. 2015;3(8):e12515.PubMedPubMedCentralCrossRef Juel C, Hostrup M, Bangsbo J. The effect of exercise and beta2-adrenergic stimulation on glutathionylation and function of the Na, K-ATPase in human skeletal muscle. Physiol Rep. 2015;3(8):e12515.PubMedPubMedCentralCrossRef
163.
164.
go back to reference Juel C, Nordsborg NB, Bangsbo J. Exercise-induced increase in maximal in vitro Na-K-ATPase activity in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol. 2013;304(12):R1161–5.PubMedCrossRef Juel C, Nordsborg NB, Bangsbo J. Exercise-induced increase in maximal in vitro Na-K-ATPase activity in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol. 2013;304(12):R1161–5.PubMedCrossRef
165.
go back to reference Juel C. Maximal Na(+)-K(+)-ATPase activity is upregulated in association with muscle activity. J Appl Physiol (1985). 2012;112(12):2121–3.CrossRef Juel C. Maximal Na(+)-K(+)-ATPase activity is upregulated in association with muscle activity. J Appl Physiol (1985). 2012;112(12):2121–3.CrossRef
166.
go back to reference Dhar-Chowdhury P, Malester B, Rajacic P, Coetzee WA. The regulation of ion channels and transporters by glycolytically derived ATP. Cell Mol Life Sci. 2007;64(23):3069–83.PubMedCrossRef Dhar-Chowdhury P, Malester B, Rajacic P, Coetzee WA. The regulation of ion channels and transporters by glycolytically derived ATP. Cell Mol Life Sci. 2007;64(23):3069–83.PubMedCrossRef
167.
go back to reference James JH, Wagner KR, King JK, Leffler RE, Upputuri RK, Balasubramaniam A, et al. Stimulation of both aerobic glycolysis and Na(+)-K(+)-ATPase activity in skeletal muscle by epinephrine or amylin. Am J Physiol. 1999;277(1):E176–86.PubMed James JH, Wagner KR, King JK, Leffler RE, Upputuri RK, Balasubramaniam A, et al. Stimulation of both aerobic glycolysis and Na(+)-K(+)-ATPase activity in skeletal muscle by epinephrine or amylin. Am J Physiol. 1999;277(1):E176–86.PubMed
168.
go back to reference Okamoto K, Wang W, Rounds J, Chambers EA, Jacobs DO. ATP from glycolysis is required for normal sodium homeostasis in resting fast-twitch rodent skeletal muscle. Am J Physiol Endocrinol Metab. 2001;281(3):E479–88.PubMedCrossRef Okamoto K, Wang W, Rounds J, Chambers EA, Jacobs DO. ATP from glycolysis is required for normal sodium homeostasis in resting fast-twitch rodent skeletal muscle. Am J Physiol Endocrinol Metab. 2001;281(3):E479–88.PubMedCrossRef
169.
go back to reference Baekgaard Nielsen O, de Paoli FV, Riisager A, Pedersen TH. Chloride channels take center stage in acute regulation of excitability in skeletal muscle: implications for fatigue. Physiology (Bethesda). 2017;32(6):425–34. Baekgaard Nielsen O, de Paoli FV, Riisager A, Pedersen TH. Chloride channels take center stage in acute regulation of excitability in skeletal muscle: implications for fatigue. Physiology (Bethesda). 2017;32(6):425–34.
170.
go back to reference Imbrici P, Altamura C, Pessia M, Mantegazza R, Desaphy JF, Camerino DC. ClC-1 chloride channels: state-of-the-art research and future challenges. Front Cell Neurosci. 2015;9:156.PubMedPubMedCentralCrossRef Imbrici P, Altamura C, Pessia M, Mantegazza R, Desaphy JF, Camerino DC. ClC-1 chloride channels: state-of-the-art research and future challenges. Front Cell Neurosci. 2015;9:156.PubMedPubMedCentralCrossRef
171.
go back to reference Entman ML, Keslensky SS, Chu A, Van Winkle WB. The sarcoplasmic reticulum-glycogenolytic complex in mammalian fast twitch skeletal muscle. Proposed in vitro counterpart of the contraction-activated glycogenolytic pool. J Biol Chem. 1980;255(13):6245–52.PubMedCrossRef Entman ML, Keslensky SS, Chu A, Van Winkle WB. The sarcoplasmic reticulum-glycogenolytic complex in mammalian fast twitch skeletal muscle. Proposed in vitro counterpart of the contraction-activated glycogenolytic pool. J Biol Chem. 1980;255(13):6245–52.PubMedCrossRef
172.
go back to reference Xu KY, Becker LC. Ultrastructural localization of glycolytic enzymes on sarcoplasmic reticulum vesticles. J Histochem Cytochem. 1998;46(4):419–27.PubMedCrossRef Xu KY, Becker LC. Ultrastructural localization of glycolytic enzymes on sarcoplasmic reticulum vesticles. J Histochem Cytochem. 1998;46(4):419–27.PubMedCrossRef
173.
go back to reference Lees SJ, Chen YT, Williams JH. Glycogen debranching enzyme is associated with rat skeletal muscle sarcoplasmic reticulum. Acta Physiol Scand. 2004;181(2):239–45.PubMedCrossRef Lees SJ, Chen YT, Williams JH. Glycogen debranching enzyme is associated with rat skeletal muscle sarcoplasmic reticulum. Acta Physiol Scand. 2004;181(2):239–45.PubMedCrossRef
174.
go back to reference Lees SJ, Franks PD, Spangenburg EE, Williams JH. Glycogen and glycogen phosphorylase associated with sarcoplasmic reticulum: effects of fatiguing activity. J Appl Physiol (1985). 2001;91(4):1638–44.CrossRef Lees SJ, Franks PD, Spangenburg EE, Williams JH. Glycogen and glycogen phosphorylase associated with sarcoplasmic reticulum: effects of fatiguing activity. J Appl Physiol (1985). 2001;91(4):1638–44.CrossRef
175.
go back to reference Laver DR. Regulation of ryanodine receptors from skeletal and cardiac muscle during rest and excitation. Clin Exp Pharmacol Physiol. 2006;33(11):1107–13.PubMedCrossRef Laver DR. Regulation of ryanodine receptors from skeletal and cardiac muscle during rest and excitation. Clin Exp Pharmacol Physiol. 2006;33(11):1107–13.PubMedCrossRef
176.
go back to reference Laver DR, Lenz GK, Lamb GD. Regulation of the calcium release channel from rabbit skeletal muscle by the nucleotides ATP, AMP, IMP and adenosine. J Physiol. 2001;537(Pt 3):763–78.PubMedPubMedCentralCrossRef Laver DR, Lenz GK, Lamb GD. Regulation of the calcium release channel from rabbit skeletal muscle by the nucleotides ATP, AMP, IMP and adenosine. J Physiol. 2001;537(Pt 3):763–78.PubMedPubMedCentralCrossRef
177.
go back to reference Popova OB, Baker MR, Tran TP, Le T, Serysheva II. Identification of ATP-binding regions in the RyR1 Ca(2)(+) release channel. PLoS ONE. 2012;7(11):e48725.PubMedPubMedCentralCrossRef Popova OB, Baker MR, Tran TP, Le T, Serysheva II. Identification of ATP-binding regions in the RyR1 Ca(2)(+) release channel. PLoS ONE. 2012;7(11):e48725.PubMedPubMedCentralCrossRef
178.
go back to reference Ogawa H, Kurebayashi N, Yamazawa T, Murayama T. Regulatory mechanisms of ryanodine receptor/Ca(2+) release channel revealed by recent advancements in structural studies. J Muscle Res Cell Motil. 2020 Feb 10. Epub ahead of print. Ogawa H, Kurebayashi N, Yamazawa T, Murayama T. Regulatory mechanisms of ryanodine receptor/Ca(2+) release channel revealed by recent advancements in structural studies. J Muscle Res Cell Motil. 2020 Feb 10. Epub ahead of print.
179.
go back to reference Duhamel TA, Perco JG, Green HJ. Manipulation of dietary carbohydrates after prolonged effort modifies muscle sarcoplasmic reticulum responses in exercising males. Am J Physiol Regul Integr Comp Physiol. 2006;291(4):R1100–10.PubMedCrossRef Duhamel TA, Perco JG, Green HJ. Manipulation of dietary carbohydrates after prolonged effort modifies muscle sarcoplasmic reticulum responses in exercising males. Am J Physiol Regul Integr Comp Physiol. 2006;291(4):R1100–10.PubMedCrossRef
180.
go back to reference Goodman C, Blazev R, Stephenson G. Glycogen content and contractile responsiveness to T-system depolarization in skinned muscle fibres of the rat. Clin Exp Pharmacol Physiol. 2005;32(9):749–56.PubMedCrossRef Goodman C, Blazev R, Stephenson G. Glycogen content and contractile responsiveness to T-system depolarization in skinned muscle fibres of the rat. Clin Exp Pharmacol Physiol. 2005;32(9):749–56.PubMedCrossRef
181.
go back to reference Impey SG, Hearris MA, Hammond KM, Bartlett JD, Louis J, Close GL, et al. Fuel for the work required: a theoretical framework for carbohydrate periodization and the glycogen threshold hypothesis. Sports Med. 2018;48(5):1031–48.PubMedPubMedCentralCrossRef Impey SG, Hearris MA, Hammond KM, Bartlett JD, Louis J, Close GL, et al. Fuel for the work required: a theoretical framework for carbohydrate periodization and the glycogen threshold hypothesis. Sports Med. 2018;48(5):1031–48.PubMedPubMedCentralCrossRef
182.
go back to reference Cuenda A, Nogues M, Henao F, Gutierrez-Merino C. Interaction between glycogen phosphorylase and sarcoplasmic reticulum membranes and its functional implications. J Biol Chem. 1995;270(20):11998–2004.PubMedCrossRef Cuenda A, Nogues M, Henao F, Gutierrez-Merino C. Interaction between glycogen phosphorylase and sarcoplasmic reticulum membranes and its functional implications. J Biol Chem. 1995;270(20):11998–2004.PubMedCrossRef
183.
go back to reference Favero TG. Sarcoplasmic reticulum Ca(2+) release and muscle fatigue. J Appl Physiol (1985). 1999;87(2):471–83.CrossRef Favero TG. Sarcoplasmic reticulum Ca(2+) release and muscle fatigue. J Appl Physiol (1985). 1999;87(2):471–83.CrossRef
184.
go back to reference Shearer J, Graham TE. New perspectives on the storage and organization of muscle glycogen. Can J Appl Physiol. 2002;27(2):179–203.PubMedCrossRef Shearer J, Graham TE. New perspectives on the storage and organization of muscle glycogen. Can J Appl Physiol. 2002;27(2):179–203.PubMedCrossRef
185.
go back to reference Sacchetto R, Bovo E, Donella-Deana A, Damiani E. Glycogen- and PP1c-targeting subunit GM is phosphorylated at Ser48 by sarcoplasmic reticulum-bound Ca2+-calmodulin protein kinase in rabbit fast twitch skeletal muscle. J Biol Chem. 2005;280(8):7147–55.PubMedCrossRef Sacchetto R, Bovo E, Donella-Deana A, Damiani E. Glycogen- and PP1c-targeting subunit GM is phosphorylated at Ser48 by sarcoplasmic reticulum-bound Ca2+-calmodulin protein kinase in rabbit fast twitch skeletal muscle. J Biol Chem. 2005;280(8):7147–55.PubMedCrossRef
186.
go back to reference Prats C, Gomez-Cabello A, Hansen AV. Intracellular compartmentalization of skeletal muscle glycogen metabolism and insulin signalling. Exp Physiol. 2011;96(4):385–90.PubMedCrossRef Prats C, Gomez-Cabello A, Hansen AV. Intracellular compartmentalization of skeletal muscle glycogen metabolism and insulin signalling. Exp Physiol. 2011;96(4):385–90.PubMedCrossRef
187.
go back to reference Graham TE. Glycogen: an overview of possible regulatory roles of the proteins associated with the granule. Appl Physiol Nutr Metab. 2009;34(3):488–92.PubMedCrossRef Graham TE. Glycogen: an overview of possible regulatory roles of the proteins associated with the granule. Appl Physiol Nutr Metab. 2009;34(3):488–92.PubMedCrossRef
188.
go back to reference Graham TE, Yuan Z, Hill AK, Wilson RJ. The regulation of muscle glycogen: the granule and its proteins. Acta Physiol (Oxf). 2010;199(4):489–98.CrossRef Graham TE, Yuan Z, Hill AK, Wilson RJ. The regulation of muscle glycogen: the granule and its proteins. Acta Physiol (Oxf). 2010;199(4):489–98.CrossRef
189.
go back to reference Hoffman NJ, Whitfield J, Janzen NR, Belhaj MR, Galic S, Murray-Segal L, et al. Genetic loss of AMPK-glycogen binding destabilises AMPK and disrupts metabolism. Mol Metab. 2020;41:101048.PubMedPubMedCentralCrossRef Hoffman NJ, Whitfield J, Janzen NR, Belhaj MR, Galic S, Murray-Segal L, et al. Genetic loss of AMPK-glycogen binding destabilises AMPK and disrupts metabolism. Mol Metab. 2020;41:101048.PubMedPubMedCentralCrossRef
190.
go back to reference Janzen NR, Whitfield J, Hoffman NJ. Interactive roles for AMPK and glycogen from cellular energy sensing to exercise metabolism. Int J Mol Sci. 2018;19(11):3344.PubMedCentralCrossRef Janzen NR, Whitfield J, Hoffman NJ. Interactive roles for AMPK and glycogen from cellular energy sensing to exercise metabolism. Int J Mol Sci. 2018;19(11):3344.PubMedCentralCrossRef
191.
go back to reference McBride A, Ghilagaber S, Nikolaev A, Hardie DG. The glycogen-binding domain on the AMPK beta subunit allows the kinase to act as a glycogen sensor. Cell Metab. 2009;9(1):23–34.PubMedPubMedCentralCrossRef McBride A, Ghilagaber S, Nikolaev A, Hardie DG. The glycogen-binding domain on the AMPK beta subunit allows the kinase to act as a glycogen sensor. Cell Metab. 2009;9(1):23–34.PubMedPubMedCentralCrossRef
192.
go back to reference McBride A, Hardie DG. AMP-activated protein kinase–a sensor of glycogen as well as AMP and ATP? Acta Physiol (Oxf). 2009;196(1):99–113.CrossRef McBride A, Hardie DG. AMP-activated protein kinase–a sensor of glycogen as well as AMP and ATP? Acta Physiol (Oxf). 2009;196(1):99–113.CrossRef
193.
go back to reference Rauch HG, St Clair Gibson A, Lambert EV, Noakes TD. A signalling role for muscle glycogen in the regulation of pace during prolonged exercise. Br J Sports Med. 2005;39(1):34–8.PubMedPubMedCentralCrossRef Rauch HG, St Clair Gibson A, Lambert EV, Noakes TD. A signalling role for muscle glycogen in the regulation of pace during prolonged exercise. Br J Sports Med. 2005;39(1):34–8.PubMedPubMedCentralCrossRef
194.
go back to reference Karelis AD, Smith JW, Passe DH, Peronnet F. Carbohydrate administration and exercise performance: what are the potential mechanisms involved? Sports Med. 2010;40(9):747–63.PubMedCrossRef Karelis AD, Smith JW, Passe DH, Peronnet F. Carbohydrate administration and exercise performance: what are the potential mechanisms involved? Sports Med. 2010;40(9):747–63.PubMedCrossRef
195.
go back to reference Williams JH, Batts TW, Lees S. Reduced muscle glycogen differentially affects exercise performance and muscle fatigue. Int Scholarly Res Notices. 2013;2013:371235 Williams JH, Batts TW, Lees S. Reduced muscle glycogen differentially affects exercise performance and muscle fatigue. Int Scholarly Res Notices. 2013;2013:371235
196.
go back to reference Matsui T, Soya M, Soya H. Endurance and brain glycogen: a clue toward understanding central fatigue. Adv Neurobiol. 2019;23:331–46.PubMedCrossRef Matsui T, Soya M, Soya H. Endurance and brain glycogen: a clue toward understanding central fatigue. Adv Neurobiol. 2019;23:331–46.PubMedCrossRef
197.
go back to reference Matsui T, Soya S, Okamoto M, Ichitani Y, Kawanaka K, Soya H. Brain glycogen decreases during prolonged exercise. J Physiol. 2011;589(Pt 13):3383–93.PubMedPubMedCentral Matsui T, Soya S, Okamoto M, Ichitani Y, Kawanaka K, Soya H. Brain glycogen decreases during prolonged exercise. J Physiol. 2011;589(Pt 13):3383–93.PubMedPubMedCentral
Metadata
Title
Muscle Glycogen Metabolism and High-Intensity Exercise Performance: A Narrative Review
Authors
Jeppe F. Vigh-Larsen
Niels Ørtenblad
Lawrence L. Spriet
Kristian Overgaard
Magni Mohr
Publication date
01-09-2021
Publisher
Springer International Publishing
Keyword
Fatigue
Published in
Sports Medicine / Issue 9/2021
Print ISSN: 0112-1642
Electronic ISSN: 1179-2035
DOI
https://doi.org/10.1007/s40279-021-01475-0

Other articles of this Issue 9/2021

Sports Medicine 9/2021 Go to the issue