Skip to main content
Log in

Prolonged exercise potentiates sarcoplasmic reticulum Ca2+ uptake in rat diaphragm

  • Original Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

The effects of a single bout of prolonged treadmill exercise [mean=81 (13) min] on sarcoplasmic reticulum (SR) Ca2+ release, uptake and ATPase activity were determined in the costal region of rat diaphragm (D) and red gastrocnemius (RG). Glycogen depletion measurements made immediately following exercise suggested that treadmill running substantially recruited the fibers throughout both muscles. SR Ca2+ ATPase activity, measured in isolated SR vesicles, decreased in the RG by 33% but remained unchanged in D in response to the exercise bout. This effect in RG was matched by a 37% decline in Ca2+ uptake and a 28% depression in Ca2+ release when measured in muscle homogenates. Conversely, Ca2+ uptake increased between 157% and 263% in the D in the absence of any change in Ca2+ release. These data show that the attenuation of SR function that has been consistently observed in limb muscle over the last several decades is absent in diaphragm despite the fact that its fibers appear to experience sufficient activity to deplete their glycogen. In fact, the large increase in Ca2+ uptake in D shows that prolonged activity actually potentiates the ability of SR vesicles to sequester Ca2+ in the absence of any increase in energy cost. Thus, it appears necessary to re-evaluate the role of exercise in regulating Ca2+ sequestration by the SR as different muscles may respond in ways that are dictated by their function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

References

  • Byrd SK, Bode AK, Klug GA (1989a) Effects of exercise of varying duration on sarcoplasmic reticulum function. J Appl Physiol 66:1383–1389

    CAS  PubMed  Google Scholar 

  • Byrd SK, McCutcheon LJ, Hodgson DR, Gollnick PD (1989b) Altered sarcoplasmic reticulum function after high-intensity exercise. J Appl Physiol 67:2072–2077

    CAS  PubMed  Google Scholar 

  • Chin ER, Allen DG (1997) Effects of reduced muscle glycogen concentration on force, Ca2+ release and contractile protein function in intact mouse skeletal muscle. J Physiol (Lond) 498:17–29

    Google Scholar 

  • Daiho T, Yamasaki K, Saino T, Kamidochi M, Satoh K, Iizuka H, Suzuki H (2001) Mutations of either or both Cys876 and Cys888 residues of sarcoplasmic reticulum Ca2+-ATPase result in a complete loss of Ca2+ transport activity without a loss of Ca2+-dependent ATPase Activity:role of the Cys876-Cys888 disulfide bond. J Biol Chem 276: 32771–32778.

    Article  CAS  PubMed  Google Scholar 

  • DeTroyer A, Sampson M, Sigrist S, Macklem PT (1981) The diaphragm: two muscles. Science 213:237–238

    CAS  PubMed  Google Scholar 

  • Favero TG, Pessah IN, Klug GA (1993) Prolonged exercise reduces Ca2+ release in rat skeletal muscle sarcoplasmic reticulum. Pflügers Arch 422:472–475

    Google Scholar 

  • Favero TG, Zable AC, Colter D, Abramson JJ (1997) Lactate inhibits Ca2+-activated Ca2+-channel activity from skeletal muscle sarcoplasmic reticulum. J Appl Physiol 82:447–452

    CAS  PubMed  Google Scholar 

  • Ferrington DA, Reijneveld JC, Bar PR, Bigelow DJ (1996) Activation of the sarcoplasmic reticulum Ca2+-ATPase induced by exercise. Biochim Biophys Acta 1279:203–213

    Article  CAS  PubMed  Google Scholar 

  • Fitts RH (1994) Cellular mechanisms of muscle fatigue. Physiol Rev 74:49–94

    CAS  PubMed  Google Scholar 

  • Fitts RH, Courtright JB, Kim GH, Witzmann FA (1982) Muscle fatigue with prolonged exercise: contractile and biochemical alterations. Am J Physiol 242:C65–73

    CAS  PubMed  Google Scholar 

  • Gauthier AP, Faltus RE, Macklem PT, Bellemare F (1993) Effects of fatigue on the length-tetanic force relationship of the rat diaphragm. J Appl Physiol 74:326–332

    CAS  PubMed  Google Scholar 

  • Gollnick PD, Karlsson J, Piehl K, Saltin B (1974a) Selective glycogen depletion in skeletal muscle fibres of man following sustained contractions. J Physiol (Lond)241:59–67

    Google Scholar 

  • Gollnick PD, Piehl K, Saltin B (1974b) Selective glycogen depletion pattern in human muscle fibres after exercise of varying intensity and at varying pedaling rates. J Physiol (Lond) 241:45–57

    Google Scholar 

  • Grassino A, Macklem PT (1984) Respiratory muscle fatigue and ventilatory failure. Annu Rev Med 35:625–647

    Article  CAS  PubMed  Google Scholar 

  • Gray H (1995) Gray's anatomy, 3rd edn. Churchill Livingstone, New York

  • Green HJ (1991) How important is endogenous muscle glycogen to fatigue in prolonged exercise? Can J Physiol Pharmacol 69:290–297

    CAS  PubMed  Google Scholar 

  • Hervé P, Lecarpentier Y, Brenot F, Clergue M, Chemla D, Duroux P (1988) Relaxation of the diaphragm muscle: influence of ryanodine and fatigue. J Appl Physiol 65:1950–1956

    PubMed  Google Scholar 

  • Hood DA, Parent G (1991) Metabolic and contractile responses of rat fast-twitch muscle to 10-Hz stimulation. Am J Physiol 260:C832–840

    CAS  PubMed  Google Scholar 

  • Howell S (1996) Compartmental analysis of Ca2+ kinetics in long-lasting diaphragm fatigue: loss of t-tubular membrane Ca2+. J Appl Physiol 80:2009–2018

    Article  CAS  PubMed  Google Scholar 

  • Howell S, Zhan W-Z, Sieck GC (1997) Diaphragm disuse reduces Ca2+ uptake capacity of sarcoplasmic reticulum. J Appl Physiol 82:164–171

    CAS  PubMed  Google Scholar 

  • Inesi G, Hill T (1983) Calcium and proton dependence of sarcoplasmic reticulum ATPase. Biophys J 44:271–280

    CAS  PubMed  Google Scholar 

  • Johnson BD, Sieck GC (1993) Differential susceptibility of diaphragm muscle fibers to neuromuscular transmission failure. J Appl Physiol 75:341–348

    CAS  PubMed  Google Scholar 

  • Kirtley ME, Sumbilla C, Inesi G (1990) Mechanisms of calcium uptake and release by sarcoplasmic reticulum. In: Bronner F (ed) Intracellular calcium regulation. Wiley-Liss, New York, pp 249–270

  • Luckin KA, Favero TG, Klug GA (1991) Prolonged exercise induces structural changes in SR Ca2+-ATPase of rat muscle. Biochem Med Metabol Biol 46:391–405

  • McCarthy JJ, Klug GA (1995) Phosphorylation kinetics of the sarcoplasmic reticulum Ca2+- Mg2+ - ATPase following exercise. Med Sci Sport Exerc 27: S141

    Google Scholar 

  • Metzger JM, Fitts, RH (1986) Fatigue from high- and low-frequency muscle stimulation: role of sarcolemma action potentials. Exp Neurol 93:320–333

    CAS  PubMed  Google Scholar 

  • Road J, Vahi R, Del Rio P, Grassino A (1987) In vivo contractile properties of fatigued diaphragm. J Appl Physiol 63:471–478

    CAS  PubMed  Google Scholar 

  • Roussos C, Macklem PT (1977) Diaphragmatic fatigue in man. J Appl Physiol 43:189–197

    CAS  PubMed  Google Scholar 

  • Rüegg JC (1992) Calcium In Muscle Contraction. Springer, Berlin Heidelberg New York

  • Sen CK, Das DK (eds) (2000) Antioxidants & redox signaling 2:2. Mary Ann Liebert, New York

    Google Scholar 

  • Ward CW, Spangenburg EE, Liss LM, Williams JH (1998) Effects of varied fatigue protocols on sarcoplasmic reticulum calcium uptake and release rates. Am J Physiol 275:R99-R104

    CAS  PubMed  Google Scholar 

  • Weidekamm E, Brdiczka D (1975) Excitation and localization of a (Ca2+ + Mg2+)-stimulated ATPase in human eruthrocute spectrin. Biochim Biophys Acta 401:51–58

    CAS  PubMed  Google Scholar 

  • Westerblad H, Lee JA, Lännergren J, Allen DG (1991) Cellular mechanisms of fatigue in skeletal muscle. Am J Physiol 261:C195-C209

    CAS  PubMed  Google Scholar 

  • Williams JH (1997) Contractile apparatus and sarcoplasmic reticulum function: effects of fatigue 'recovery' and elevated Ca2+. J Appl Physiol 83:444–450

    CAS  PubMed  Google Scholar 

  • Williams JH, Klug GA (1995) Calcium exchange hypothesis of skeletal muscle fatigue: a brief review. Muscle Nerve 18:421–434

    CAS  PubMed  Google Scholar 

  • Williams JH, Ward CW, Klug GA (1993) Fatigue-induced alterations in Ca2+ and caffeine sensitivities of skinned muscle fibers. J Appl Physiol 75:586–593

    CAS  PubMed  Google Scholar 

  • Xu KY, Becker LC (1998) Ultrastuctural localization of glycolytic enzymes on sarcoplasmic reticulum vesicles. J Histochem Cytochem 46:419–427

Download references

Acknowledgements

This work was supported by the Eugene Evonuk Memorial Graduate Scholarship and the National Institutes of Health grant AR 41727.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stasinos Stavrianeas.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stavrianeas, S., Spangenburg, E., Batts, T. et al. Prolonged exercise potentiates sarcoplasmic reticulum Ca2+ uptake in rat diaphragm. Eur J Appl Physiol 89, 63–68 (2003). https://doi.org/10.1007/s00421-002-0761-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-002-0761-7

Keywords

Navigation