Advertisement

European Journal of Applied Physiology

, Volume 112, Issue 10, pp 3559–3567 | Cite as

Skeletal muscle glycogen content and particle size of distinct subcellular localizations in the recovery period after a high-level soccer match

  • Joachim NielsenEmail author
  • Peter Krustrup
  • Lars Nybo
  • Thomas P. Gunnarsson
  • Klavs Madsen
  • Henrik Daa Schrøder
  • Jens Bangsbo
  • Niels Ørtenblad
Original Article

Abstract

Whole muscle glycogen levels remain low for a prolonged period following a soccer match. The present study was conducted to investigate how this relates to glycogen content and particle size in distinct subcellular localizations. Seven high-level male soccer players had a vastus lateralis muscle biopsy collected immediately after and 24, 48, 72 and 120 h after a competitive soccer match. Transmission electron microscopy was used to estimate the subcellular distribution of glycogen and individual particle size. During the first day of recovery, glycogen content increased by ~60% in all subcellular localizations, but during the subsequent second day of recovery glycogen content located within the myofibrils (Intramyofibrillar glycogen, a minor deposition constituting 10–15% of total glycogen) did not increase further compared with an increase in subsarcolemmal glycogen (−7 vs. +25%, respectively, P = 0.047). Conversely, from the second to the fifth day of recovery, glycogen content increased (53%) within the myofibrils compared to no change in subsarcolemmal or intermyofibrillar glycogen (P < 0.005). Independent of location, increment in particle size preceded increment in number of particles. Intriguingly, average particle size decreased; however, in the period from 3 to 5 days after the match. These findings suggest that glycogen storage in skeletal muscle is influenced by subcellular localization-specific mechanisms, which account for an increase in number of glycogen particles located within the myofibrils in the period from 2 to 5 days after the soccer match.

Keywords

Carbohydrate metabolism Muscle contraction Muscle fatigue Physical exertion Skeletal muscle fibres Glycogen storage disease 

Notes

Acknowledgments

The authors would like to acknowledge the players and their elite soccer clubs for the participation. We would also like to thank Kirsten Hansen, Karin Trampedach, Benthe Jørgensen, Christian Hasson, Fedon Marcello Iaia, Ian Rollo and Sarah R Jackman for excellent technical assistance. This study was supported by grants from The Lundbeck Foundation, Team Denmark (Team Danmark) elite association and the Ministry of Culture Committee on Sports Research (Kulturministeriets Udvalg for Idrætsforskning).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

421_2012_2341_MOESM1_ESM.pdf (270 kb)
Supplementary material 1 (PDF 269 kb)

References

  1. Bangsbo J, Mohr M, Krustrup P (2006) Physical and metabolic demands of training and match-play in the elite football player. J Sports Sci 24:665–674PubMedCrossRefGoogle Scholar
  2. Bergström J, Hermansen L, Hultman E, Saltin B (1967) Diet, muscle glycogen and physical performance. Acta Physiol Scand 71:140–150PubMedCrossRefGoogle Scholar
  3. Doyle JA, Sherman WM, Strauss RL (1993) Effects of eccentric and concentric exercise on muscle glycogen replenishment. J Appl Physiol 74:1848–1855PubMedGoogle Scholar
  4. Fernandez-Novell JM, Lopez-Iglesias C, Ferrer JC, Guinovart JJ (2002) Zonal distribution of glycogen synthesis in isolated rat hepatocytes. FEBS Lett 531:222–228PubMedCrossRefGoogle Scholar
  5. Fridén J, Seger J, Ekblom B (1985) Implementation of periodic acid-thiosemicarbazide-silver proteinate staining for ultrastructural assessment of muscle glycogen utilization during exercise. Cell Tissue Res 242:229–232PubMedCrossRefGoogle Scholar
  6. Fridén J, Seger J, Ekblom B (1989) Topographical localization of muscle glycogen: an ultrahistochemical study in the human vastus lateralis. Acta Physiol Scand 135:381–391PubMedCrossRefGoogle Scholar
  7. Graham TE, Yuan Z, Hill AK, Wilson RJ (2010) The regulation of muscle glycogen: the granule and its proteins. Acta Physiol (Oxf) 199:489–498CrossRefGoogle Scholar
  8. Hermansen L, Hultman E, Saltin B (1967) Muscle glycogen during prolonged severe exercise. Acta Physiol Scand 71:129–139PubMedCrossRefGoogle Scholar
  9. Howard CV, Reed MG (2005) Unbiased Stereology. Three-dimensional measurement in Microscopy. Bios Scientific Publishers, OxfordGoogle Scholar
  10. Jacobs I, Westlin N, Karlsson J, Rasmusson M, Houghton B (1982) Muscle glycogen and diet in elite soccer players. Eur J Appl Physiol Occup Physiol 48:297–302PubMedCrossRefGoogle Scholar
  11. Krustrup P, Ørtenblad N, Nielsen J, Nybo L, Gunnarsson TP, Iaia FM, Madsen K, Stephens F, Greenhaff P, Bangsbo J (2011) 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 111(12):2987–2995PubMedCrossRefGoogle Scholar
  12. Lin LI (1989) A concordance correlation coefficient to evaluate reproducibility. Biometrics 45:255–268PubMedCrossRefGoogle Scholar
  13. Marchand I, Chorneyko K, Tarnopolsky M, Hamilton S, Shearer J, Potvin J, Graham TE (2002) Quantification of subcellular glycogen in resting human muscle: granule size, number, and location. J Appl Physiol 93:1598–1607PubMedGoogle Scholar
  14. Marchand I, Tarnopolsky M, Adamo KB, Bourgeois JM, Chorneyko K, Graham TE (2007) Quantitative assessment of human muscle glycogen granules size and number in subcellular locations during recovery from prolonged exercise. J Physiol 580:617–628PubMedCrossRefGoogle Scholar
  15. Nielsen JN, Derave W, Kristiansen S, Ralston E, Ploug T, Richter EA (2001) Glycogen synthase localization and activity in rat skeletal muscle is strongly dependent on glycogen content. J Physiol 531:757–769PubMedCrossRefGoogle Scholar
  16. Nielsen J, Schrøder HD, Rix CG, Ørtenblad N (2009) Distinct effects of subcellular glycogen localization on tetanic relaxation time and endurance in mechanically skinned rat skeletal muscle fibres. J Physiol 587:3679–3690PubMedCrossRefGoogle Scholar
  17. Nielsen J, Mogensen M, Vind BF, Sahlin K, Højlund K, Schrøder HD, Ørtenblad N (2010a) Increased subsarcolemmal lipids in type 2 diabetes: effect of training on localization of lipids, mitochondria, and glycogen in sedentary human skeletal muscle. Am J Physiol Endocrinol Metab 298:E706–E713PubMedCrossRefGoogle Scholar
  18. Nielsen J, Suetta C, Hvid LG, Schrøder HD, Aagaard P, Ørtenblad N (2010b) Subcellular localization-dependent decrements in skeletal muscle glycogen and mitochondria content following short-term disuse in young and old men. Am J Physiol Endocrinol Metab 299:E1053–E1060PubMedCrossRefGoogle Scholar
  19. Nielsen J, Holmberg HC, Schroder HD, Saltin B, Ortenblad N (2011) Human skeletal muscle glycogen utilization in exhaustive exercise: role of subcellular localization and fibre type. J Physiol 589:2871–2885PubMedCrossRefGoogle Scholar
  20. Ørtenblad N, Nielsen J, Saltin B, Holmberg HC (2011) Role of glycogen availability in sarcoplasmic reticulum Ca2+ kinetics in human skeletal muscle. J Physiol 589:711–725PubMedCrossRefGoogle Scholar
  21. Prats C, Cadefau JA, Cusso R, Qvortrup K, Nielsen JN, Wojtaszewski JF, Hardie DG, Stewart G, Hansen BF, Ploug T (2005) Phosphorylation-dependent translocation of glycogen synthase to a novel structure during glycogen resynthesis. J Biol Chem 280:23165–23172PubMedCrossRefGoogle Scholar
  22. Prats C, Helge JW, Nordby P, Qvortrup K, Ploug T, Dela F, Wojtaszewski JF (2009) Dual regulation of muscle glycogen synthase during exercise by activation and compartmentalization. J Biol Chem 284:15692–15700PubMedCrossRefGoogle Scholar
  23. Prats C, Gomez-Cabello A, Hansen AV (2011) Intracellular compartmentalization of skeletal muscle glycogen metabolism and insulin signalling. Exp Physiol 96:385–390PubMedCrossRefGoogle Scholar
  24. Rampinini E, Bosio A, Ferraresi I, Petruolo A, Morelli A, Sassi A (2011) Match-related fatigue in soccer players. Med Sci Sports Exerc 43:2161–2170PubMedCrossRefGoogle Scholar
  25. Robinson TM, Sewell DA, Hultman E, Greenhaff PL (1999) Role of submaximal exercise in promoting creatine and glycogen accumulation in human skeletal muscle. J Appl Physiol 87:598–604PubMedGoogle Scholar
  26. Sjöström M, Ängquist KA, Bylund AC, Fridén J, Gustavsson L, Schersten T (1982a) Morphometric analyses of human muscle fiber types. Muscle Nerve 5:538–553PubMedCrossRefGoogle Scholar
  27. Sjöström M, Fridén J, Ekblom B (1982b) Fine structural details of human muscle fibres after fibre type specific glycogen depletion. Histochemistry 76:425–438PubMedCrossRefGoogle Scholar
  28. Skurat AV, Lim SS, Roach PJ (1997) Glycogen biogenesis in rat 1 fibroblasts expressing rabbit muscle glycogenin. Eur J Biochem 245:147–155PubMedCrossRefGoogle Scholar
  29. Thorlund JB, Aagaard P, Madsen K (2009) Rapid muscle force capacity changes after soccer match play. Int J Sports Med 30:273–278PubMedCrossRefGoogle Scholar
  30. Wanson JC, Drochmans P (1968) Rabbit skeletal muscle glycogen. A morphological and biochemical study of glycogen beta-particles isolated by the precipitation-centrifugation method. J Cell Biol 38:130–150PubMedCrossRefGoogle Scholar
  31. Weibel ER (1980) Stereological methods. In: Theoretical foundations vol 2, Academic Press, LondonGoogle Scholar
  32. Widrick JJ, Costill DL, McConell GK, Anderson DE, Pearson DR, Zachwieja JJ (1992) Time course of glycogen accumulation after eccentric exercise. J Appl Physiol 72:1999–2004PubMedGoogle Scholar
  33. Wyss M, Kaddurah-Daouk R (2000) Creatine and creatinine metabolism. Physiol Rev 80:1107–1213PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Joachim Nielsen
    • 1
    Email author
  • Peter Krustrup
    • 3
    • 4
  • Lars Nybo
    • 3
  • Thomas P. Gunnarsson
    • 3
  • Klavs Madsen
    • 5
  • Henrik Daa Schrøder
    • 2
  • Jens Bangsbo
    • 3
  • Niels Ørtenblad
    • 1
  1. 1.Institute of Sports Science and Clinical BiomechanicsUniversity of Southern DenmarkOdense MDenmark
  2. 2.Institute of PathologyUniversity of Southern DenmarkOdense MDenmark
  3. 3.Section of Human Physiology, Department of Exercise and Sport SciencesUniversity of CopenhagenCopenhagenDenmark
  4. 4.Sport and Health Sciences, College of Life and Environmental SciencesUniversity of ExeterExeterUK
  5. 5.Department of Sport ScienceAarhus UniversityAarhusDenmark

Personalised recommendations