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The Journal of Physiological Sciences

, Volume 62, Issue 1, pp 1–9 | Cite as

The effect of high-intensity intermittent swimming on post-exercise glycogen supercompensation in rat skeletal muscle

  • Akiko Sano
  • Keiichi Koshinaka
  • Natsuki Abe
  • Masashi Morifuji
  • Jinichiro Koga
  • Emi Kawasaki
  • Kentaro Kawanaka
Original Paper

Abstract

A single bout of prolonged endurance exercise stimulates glucose transport in skeletal muscles, leading to post-exercise muscle glycogen supercompensation if sufficient carbohydrate is provided after the cessation of exercise. Although we recently found that short-term sprint interval exercise also stimulates muscle glucose transport, the effect of this type of exercise on glycogen supercompensation is uncertain. Therefore, we compared the extent of muscle glycogen accumulation in response to carbohydrate feeding following sprint interval exercise with that following endurance exercise. In this study, 16-h-fasted rats underwent a bout of high-intensity intermittent swimming (HIS) as a model of sprint interval exercise or low-intensity prolonged swimming (LIS) as a model of endurance exercise. During HIS, the rats swam for eight 20-s sessions while burdened with a weight equal to 18% of their body weight. The LIS rats swam with no load for 3 h. The exercised rats were then refed for 4, 8, 12, or 16 h. Glycogen levels were almost depleted in the epitrochlearis muscles of HIS- or LIS-exercised rats immediately after the cessation of exercise. A rapid increase in muscle glycogen levels occurred during 4 h of refeeding, and glycogen levels had peaked at the end of 8 h of refeeding in each group of exercised refed rats. The peak glycogen levels during refeeding were not different between HIS- and LIS-exercised refed rats. Furthermore, although a large accumulation of muscle glycogen in response to carbohydrate refeeding is known to be associated with decreased insulin responsiveness of glucose transport, and despite the fact that muscle glycogen supercompensation was observed in the muscles of our exercised rats at the end of 4 h of refeeding, insulin responsiveness was not decreased in the muscles of either HIS- or LIS-exercised refed rats compared with non-exercised fasted control rats at this time point. These results suggest that sprint interval exercise enhances muscle glycogen supercompensation in response to carbohydrate refeeding as well as prolonged endurance exercise does. Furthermore, in this study, both HIS and LIS exercise prevented insulin resistance of glucose transport in glycogen supercompensated muscle during the early phase of carbohydrate refeeding. This probably led to the enhanced muscle glycogen supercompensation after exercise.

Keywords

Insulin Glucose uptake Akt Exercise Epitrochlearis 

Notes

Acknowledgments

We are grateful to Dr. Tadaomi Takenawa (Kobe University, Kobe, Japan) for providing the SKIP antibodies used in this study. This research was supported by the Uehara Memorial Foundation (Tokyo, Japan), the Nakatomi Foundation (Tosu, Japan), a Grant-in-Aid from Niigata University of Health and Welfare, and a Grant-in-Aid for Scientific Research (KAKENHI) (C) no. 16500426 from the Japan Society for the Promotion of Science. K. Koshinaka was supported by Postdoctoral Fellowships from the Japan Society for the Promotion of Science.

References

  1. 1.
    Wallberg-Henriksson H, Constable SH, Young DA, Holloszy JO (1988) Glucose transport into rat skeletal muscle: interaction between exercise and insulin. J Appl Physiol 65:909–913PubMedGoogle Scholar
  2. 2.
    Cartee GD, Douen AG, Ramlal T, Klip A, Holloszy JO (1991) Stimulation of glucose transport in skeletal muscle by hypoxia. J Appl Physiol 70:1593–1600PubMedGoogle Scholar
  3. 3.
    Gulve EA, Cartee GD, Zierath JR, Corpus VM, Holloszy JO (1990) Reversal of enhanced muscle glucose transport after exercise: roles of insulin and glucose. Am J Physiol 259:E685–E691PubMedGoogle Scholar
  4. 4.
    Richter EA, Garetto LP, Goodman MN, Ruderman NB (1982) Muscle glucose metabolism following exercise in the rat. Increased sensitivity to insulin. J Clin Invest 69:785–793PubMedCrossRefGoogle Scholar
  5. 5.
    Bergstrom J, Hultman E (1966) Muscle glycogen synthesis after exercise: an enhancing factor localized to the muscle cells in man. Nature 210:309–310PubMedCrossRefGoogle Scholar
  6. 6.
    Koshinaka K, Sano A, Howlett KF, Yamazaki T, Sasaki M, Sakamoto K, Kawanaka K (2008) Effect of high intensity intermittent swimming on post-exercise insulin sensitivity in rat epitrochlearis muscle. Metabolism 57:749–756PubMedCrossRefGoogle Scholar
  7. 7.
    Koshinaka K, Kawasaki E, Hokari F, Kawanaka K (2009) Effect of acute high intensity intermittent swimming on post-exercise insulin responsiveness in epitrochlearis of fed rats. Metabolism 58:246–253PubMedCrossRefGoogle Scholar
  8. 8.
    Derave W, Hansen BF, Lund S, Kristiansen S, Richter EA (2000) Muscle glycogen content affects insulin-stimulated glucose transport and protein kinase B activity. Am J Physiol 279:E947–E955Google Scholar
  9. 9.
    Host HH, Hansen PA, Nolte LA, Chen MM, Holloszy JO (1998) Glycogen supercompensation masks the effect of a training-induced increase in GLUT-4 on muscle glucose transport. J Appl Physiol 85:133–138PubMedGoogle Scholar
  10. 10.
    Kawanaka K, Han D-H, Nolte LA, Hansen PA, Nakatani A, Holloszy JO (1999) Decreased insulin-stimulated GLUT4 translocation in glycogen supercompensated muscles of exercised rats. Am J Physiol 276:E907–E912PubMedGoogle Scholar
  11. 11.
    Kawanaka K, Tabata I, Higuchi M (1998) Effects of high-intensity intermittent swimming on glucose transport in rat epitrochlearis muscle. J Appl Physiol 84:1852–1857PubMedGoogle Scholar
  12. 12.
    Ueyama A, Sato T, Yoshida H, Magata K, Koga N (2000) Nonradioisotope assay of glucose uptake activity in rat skeletal muscle using enzymatic measurement of 2-deoxyglucose 6-phosphate in vitro and in vivo. Biol Signals Recept 9:267–274PubMedCrossRefGoogle Scholar
  13. 13.
    Passonneau JV, Lowry OH (1993) Enzymatic analysis: a practical guide. Humana, TotowaGoogle Scholar
  14. 14.
    Hansen PA, Gulve EA, Holloszy JO (1994) Suitability of 2-deoxyglucose for in vitro measurement of glucose transport activity in skeletal muscle. J Appl Physiol 76:979–985PubMedGoogle Scholar
  15. 15.
    Passonneau JV, Lauderdale VR (1974) A comparison of three methods of glycogen measurements in tissue. Anal Biochem 60:405–412PubMedCrossRefGoogle Scholar
  16. 16.
    Margolis B, Bellot F, Honegger AM, Ullrich A, Schlessinger J, Zilberstein A (1990) Tyrosine kinase activity is essential for the association of phospholipase C-γ with the epidermal growth factor receptor. Mol Cell Biol 10:435–441PubMedGoogle Scholar
  17. 17.
    Holloszy JO, Hansen PA (1996) Reviews of physiology, biochemistry and pharmacology. In: Blaustein MP, Grunicke H, Habermann E, Pette D, Schultz G, Schweiger M (eds) Regulation of glucose transport into skeletal muscle. Spinger, BerlinGoogle Scholar
  18. 18.
    Kawanaka K, Nolte LA, Han D-H, Hansen PA, Holloszy JO (2000) Mechanism underlying impaired GLUT4 translocation in glycogen supercompensated muscles of exercised rats. Am J Physiol 279:E1311–E1318Google Scholar
  19. 19.
    Cho H, Mu J, Kim JK, Thorvaldsen JL, Chu Q, Crenshaw EB III et al (2001) Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science 292:1728–1731PubMedCrossRefGoogle Scholar
  20. 20.
    Garofalo RS, Orena SJ, Rafidi K, Torchia AJ, Stock JL, Hildebrandt AL et al (2003) Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKB beta. J Clin Invest 112:197–208PubMedGoogle Scholar
  21. 21.
    McCurdy CE, Cartee GD (2005) Akt2 is essential for the full effect of calorie restriction on insulin-stimulated glucose uptake in skeletal muscle. Diabetes 54:1349–1356PubMedCrossRefGoogle Scholar
  22. 22.
    Scheid MP, Marignani PA, Woodgett JR (2002) Multiple phosphoinositide 3-kinase-dependent steps in activation of protein kinase B. Mol Cell Biol 22:6247–6260PubMedCrossRefGoogle Scholar
  23. 23.
    Clement S, Krause U, Desmedt F, Tanti JF, Behrends J, Pesesse X, Sasaki T, Penninger J, Doherty M, Malaisse W, Dumont JE, Le Marchand-Brustel Y, Erneux C, Hue L, Schurmans S (2001) The lipid phosphatase SHIP2 controls insulin sensitivity. Nature 409:92–97PubMedCrossRefGoogle Scholar
  24. 24.
    Ijuin T, Yu YE, Mizutani K, Pao A, Tateya S, Tamori Y, Bradley A, Takenawa T (2008) Increased insulin action in SKIP heterozygous knockout mice. Mol Cell Biol 28:5184–5195PubMedCrossRefGoogle Scholar
  25. 25.
    Kagawa S, Soeda Y, Ishihara H, Oya T, Sasahara M, Yaguchi S, Oshita R, Wada T, Tsuneki H, Sasaoka T (2008) Impact of transgenic overexpression of SH2-containing inositol 5’-phosphatase 2 on glucose metabolism and insulin signaling in mice. Endocrinology 149:642–650PubMedCrossRefGoogle Scholar
  26. 26.
    Wijesekara N, Konrad D, Eweida M, Jefferies C, Liadis N, Giacca A, Crackower M, Suzuki A, Mak TW, Kahn CR, Klip A, Woo M (2005) Muscle-specific Pten deletion protects against insulin resistance and diabetes. Mol Cell Biol 25:1135–1145PubMedCrossRefGoogle Scholar

Copyright information

© The Physiological Society of Japan and Springer 2011

Authors and Affiliations

  • Akiko Sano
    • 1
  • Keiichi Koshinaka
    • 1
  • Natsuki Abe
    • 1
  • Masashi Morifuji
    • 2
  • Jinichiro Koga
    • 2
  • Emi Kawasaki
    • 1
  • Kentaro Kawanaka
    • 1
  1. 1.Department of Health and NutritionNiigata University of Health and WelfareNiigataJapan
  2. 2.Food and Health R&D LaboratoriesMeiji Seika Kaisha LtdSakadoJapan

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