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European Journal of Applied Physiology

, Volume 89, Issue 2, pp 142–149 | Cite as

Effect of endurance training and acute exercise on sarcoplasmic reticulum function in rat fast- and slow-twitch skeletal muscles

  • Shuichiro Inashima
  • Satoshi Matsunaga
  • Toshihiro Yasuda
  • Masanobu Wada
Original Article

Abstract

Following 10 weeks of endurance training and in age-matched sedentary rats, sarcoplasmic reticulum (SR) Ca2+-uptake, Ca2+-release, and Ca2+-stimulated adenosinetriphosphatase (ATPase) activity were examined in homogenates of the plantaris and soleus muscles from rats subjected to moderate-intensity treadmill running to exhaustion. In order to examine the effects of acute exercise and/or training on SR Ca2+-handling capacity, comparisons between exhausted and non-exercised rats and between trained and untrained rats were performed. Our data confirm that Ca2+-sequestration by the SR from fast-twitch muscles is depressed after training. Immediately after exhaustive running, decreases in SR function occurred in both muscles, but were more pronounced in the soleus. In the plantaris, reductions in SR Ca2+-uptake rate and Ca2+-ATPase activity were observed in untrained rats only, while in the soleus they were adversely affected irrespective of training status. Although the average run time to exhaustion varied markedly between untrained and trained animals (untrained: 253.0 min; trained: 559.4 min), no differences existed with regard to the magnitude of decreases in SR function in the soleus after exercise. The mean rate of decline in SR Ca2+-handling capacity during acute exercise, as estimated from the run time and the extent of the decline, was more than twofold higher in untrained than in trained soleus. From the present study, it is unclear whether there exists a causal relationship between muscular fatigue and SR function because the run time to exhaustion was not significantly correlated with any of parameters indicative of SR Ca2+-handling capacity, but suggested that endurance training may be capable of delaying a progression of the deterioration in SR function that occurs during exercise.

Keywords

Ca2+-uptake and release muscle fatigue Ca2+-ATPase Ca2+-sensitive fluorescent dye myosin heavy chain 

Notes

Acknowledgement

This study was supported by Grants-in-Aid for Scientific Research of Japan, 11680032.

References

  1. Belcastro AN (1987) Myofibril and sarcoplasmic reticulum changes during muscle development: activity vs. inactivity. Int J Biochem 19:945–948PubMedGoogle Scholar
  2. Bonner HW, Leslie SW, Combs AB, Tate CA (1976) Effects of exercise training and exhaustion on 45Ca uptake by rat skeletal muscle mitochondria and sarcoplasmic reticulum. Res Commun Chem Pathol Pharmacol 14:767–770PubMedGoogle Scholar
  3. Byrd SK, Bode AK, Klug GA (1989) Effects of exercise of varying duration on sarcoplasmic reticulum function. J Appl Physiol 66:1383–1389PubMedGoogle Scholar
  4. Chin ER, Green HJ, Grange F, Dossett-Mercer J, O'Brien PO (1995) Effects of prolonged low frequency stimulation on skeletal muscle sarcoplasmic reticulum. Can J Physiol Pharmacol 73:1154–1164PubMedGoogle Scholar
  5. Dux L (1993) Muscle relaxation and sarcoplasmic reticulum function in different muscle types. Rev Physiol Biochem Pharmacol 122:70–147Google Scholar
  6. Eberstein A, Sandow A (1976) Fatigue mechanisms in muscle fibers. In: Guttman E, Hnik P (eds) The effect of use and disuse in neuromuscular function. Elsevier, Amsterdam, pp 515–526Google Scholar
  7. Favero TG (1999) Sarcoplasmic reticulum Ca2+ release and muscle fatigue. J Appl Physiol 87:471–483PubMedGoogle Scholar
  8. Favero TG, Pessah IN, Klug GA (1993) Prolonged exercise reduces Ca2+ release in rat skeletal muscle sarcoplasmic reticulum. Pflügers Arch 422:472–475Google Scholar
  9. Favero TG, Colter D, Hooper PF, Abramson JJ (1998) Hypochlorous acid inhibits Ca2+-ATPase from skeletal muscle sarcoplasmic reticulum. J Appl Physiol 84:425–430PubMedGoogle Scholar
  10. Fitts RH (1994) Cellular mechanisms of muscle fatigue. Physiol Rev 74:49–94PubMedGoogle Scholar
  11. Fitts RH, Courtright JB, Kim DH, Witzmann FA (1982) Muscle fatigue with prolonged exercise: contractile and biochemical alterations. Am J Physiol 242:C65-C73PubMedGoogle Scholar
  12. Green HJ, Klug GA, Reichmann H, Seedorf U, Wiehrer W, Pette D (1984) Exercise-induced fibre type transitions with regard to myosin, parvalbumin, and sarcoplasmic reticulum in muscles of the rat. Pflugers Arch 400:432–438PubMedGoogle Scholar
  13. Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescent properties. J Biol Chem 260:3440–3450PubMedGoogle Scholar
  14. Herrmann-Frank A, Richter M, Sardor S, Mohr U, Lehmann-Horn F (1996) 4-chloro-m-cresol, a potent and specific activator of the skeletal muscle ryanodine receptor. Biochim Biophys Acta 1289:31–40CrossRefPubMedGoogle Scholar
  15. Hill CA, Thompson MW, Ruell PA, Thom JM, White MJ (2001) Sarcoplasmic reticulum function and muscle contractile character following exercise in humans. J Physiol (Lond) 531:871–878Google Scholar
  16. Kim DH, Wible GS, Witzmann FA, Fitts RH (1981) The effect of exercise-training on sarcoplasmic reticulum function in fast and slow skeletal muscle. Life Sci 28:2671–2677CrossRefPubMedGoogle Scholar
  17. Klebl BM, Ayoub AT, Pette D (1998) Protein oxidation, tyrosine nitration, and inactivation of sarcoplasmic reticulum Ca2+-ATPase in low-frequency stimulated rabbit muscle. FEBS Lett 422:381–384CrossRefPubMedGoogle Scholar
  18. Lamb GD, Cellini MA (1999) High intracellular [Ca2+] alters sarcoplasmic reticulum function in skinned skeletal muscle fibres of the rat. J Physiol (Lond) 519:815–827Google Scholar
  19. Leberer E, Härtner K-T, Pette D (1987) Reversible inhibition of sarcoplasmic reticulum Ca-ATPase by altered neuromuscular activity in rabbit fast-twitch muscle. Eur J Biochem 162:555–561PubMedGoogle Scholar
  20. Li JL, Wang XN, Fraser SF, Carey MF, Wrigley TV, McKenna MJ (2002) Effects of fatigue and training on sarcoplasmic reticulum Ca2+ regulation in human skeletal muscle. J Appl Physiol 92:912–922PubMedGoogle Scholar
  21. Lowry OH, Passonneau JV (1972) A flexible system of enzymatic analysis. Academic, New YorkGoogle Scholar
  22. Okumoto T, Imoto T, Katsuta S, Wada M (1996) Severe endurance training fails to change myosin heavy-chain distribution of diaphragm. Respir Physiol 104:39–43CrossRefPubMedGoogle Scholar
  23. Powers SK, Criswell D, Lawler J, Ji LL, Martin D, Herb RA, Dudley G (1994) Influence of exercise and fiber type on antioxidant enxyme activity in rat skeletal muscle. Am J Physiol 266:R375-R380PubMedGoogle Scholar
  24. Saitoh A, Okumoto T, Nakano H, Wada M, Katsuta S (1999) Age effect on expression of myosin heavy- and light-chain isoforms in suspended rat soleus muscle. J Appl Physiol 86:1483–1489PubMedGoogle Scholar
  25. Saltin B, Gollnick PD (1983) Skeletal muscle adaptability: significance for metabolism and performance. In: Peachey LD (ed) Handbook of physiology, section 10 skeletal muscle. American Physiological Society, Bethesda, pp 555–631Google Scholar
  26. Simonides WS, van Hardeveld C (1990) An assay for sarcoplasmic reticulum Ca2+-ATPase activity in muscle homogenate. Anal Biochem 191:321–331PubMedGoogle Scholar
  27. Srere PA (1969) Citrate synthase. Methods Enzymol 13:3–5Google Scholar
  28. Szentesi P, Zaremba R, Mechelen WV, Stienen GJ (2001) ATP utilization for calcium uptake and force production in different types of human skeletal muscle fibres. J Physiol (Lond) 531:393–403Google Scholar
  29. Tupling R, Green H, Senisterra G, Lepock J, McKee N (2001) Effects of ischemia on sarcoplasmic reticulum Ca2+ uptake and Ca2+ release in rat skeletal muscle. Am J Physiol 281:E224-E232Google Scholar
  30. Wada M, Okumoto T, Toro K, Masuda K, Fukubayashi T, Kikuchi K, Niihata S, Katsuta S (1996) Expression of hybrid isomyosins in human skeletal muscle. Am J Physiol 271:C1250-C1255PubMedGoogle Scholar
  31. Ward CW, Spangenburg EE, Diss LM, Williams JH (1998) Effects of varied fatigue protocols on sarcoplasmic reticulum uptake and release. Am J Physiol 275:R99-R104PubMedGoogle Scholar
  32. Yasuda T, Inashima S, Sasaki S, Kikuchi K, Niihata S, Wada M, Katsuta S (1999) Effects of exhaustive exercise on biochemical characteristics of sarcoplasmic reticulum from rat soleus muscle. Acta Physiol Scand 165:45–50CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Shuichiro Inashima
    • 1
  • Satoshi Matsunaga
    • 2
  • Toshihiro Yasuda
    • 3
  • Masanobu Wada
    • 4
  1. 1.Graduate School of Biosphere ScienceHiroshima UniversityHigashihiroshima-shi, Hiroshima-kenJapan
  2. 2.Institute of Health Sciences and Physical EducationOsaka City UniversityOsaka-shi, Osaka-fuJapan
  3. 3.Faculty of EducationFukushima UniversityFukushima-shi. Fukushima-kenJapan
  4. 4.Faculty of Integrated Arts and SciencesHiroshima UniversityHigashihiroshima-shi, Hiroshima-kenJapan

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