Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1993 May;464:699–710. doi: 10.1113/jphysiol.1993.sp019658

Effects of repeated tetanic stimulation on excitation-contraction coupling in cut muscle fibres of the frog.

S Györke 1
PMCID: PMC1175409  PMID: 8229825

Abstract

1. The effects of prolonged intermittent fatiguing stimulation were studied on various steps of excitation-contraction (E-C) coupling in cut single frog muscle fibres using the triple Vaseline voltage clamp and the fluorescent Ca2+ indicator rhod-2. 2. There were two phases of changes in amplitude of Ca2+ transients during fatiguing stimulation: first a 5-10% increase, then a larger decrease. The decrease in amplitude of Ca2+ transients was accompanied by a slowing down of the rate of decay of the transients and by an increase in resting [Ca2+]. 3. A complete recovery of both amplitude and time course of Ca2+ transients as well as of the resting [Ca2+] occurred within 1-3 min after cessation of fatiguing stimulation. 4. The changes in Ca2+ release signals during fatiguing stimulation were accompanied by decreases in the amplitude and the rate of decay of the action potentials as well as by a decrease in resting potential. However, these alterations are not likely to contribute to fatigue significantly, since fibres stimulated under voltage-clamp conditions, when the T-tubule voltage sensor is activated directly by applied voltage steps, showed similar fatiguability to fibres stimulated by action potentials under current-clamp conditions. 5. Simultaneous measurements of intramembrane charge movement and [Ca2+] revealed that the decrease in sarcoplasmic reticulum (SR) Ca2+ release during fatiguing stimulation is not accompanied by any significant change in charge movement. 6. These results suggest that fatigue caused by repeated tetanic stimulation develops primarily at the level of SR Ca2+ release with only small possible additional effects at the level of membrane excitability and action potential propagation along the surface/T-tubule membrane. The T-tubule voltage sensor with this type of stimulation is virtually fatigue resistant.

Full text

PDF
699

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allen D. G., Lee J. A., Westerblad H. Intracellular calcium and tension during fatigue in isolated single muscle fibres from Xenopus laevis. J Physiol. 1989 Aug;415:433–458. doi: 10.1113/jphysiol.1989.sp017730. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cooke R., Pate E. The effects of ADP and phosphate on the contraction of muscle fibers. Biophys J. 1985 Nov;48(5):789–798. doi: 10.1016/S0006-3495(85)83837-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Curtin N. A. Effects of carbon dioxide and tetanus duration on relaxation of frog skeletal muscle. J Muscle Res Cell Motil. 1986 Jun;7(3):269–275. doi: 10.1007/BF01753560. [DOI] [PubMed] [Google Scholar]
  4. Dawson M. J., Gadian D. G., Wilkie D. R. Muscular fatigue investigated by phosphorus nuclear magnetic resonance. Nature. 1978 Aug 31;274(5674):861–866. doi: 10.1038/274861a0. [DOI] [PubMed] [Google Scholar]
  5. Garcia M. C., Gonzalez-Serratos H., Morgan J. P., Perreault C. L., Rozycka M. Differential activation of myofibrils during fatigue in phasic skeletal muscle cells. J Muscle Res Cell Motil. 1991 Oct;12(5):412–424. doi: 10.1007/BF01738326. [DOI] [PubMed] [Google Scholar]
  6. Godt R. E., Nosek T. M. Changes of intracellular milieu with fatigue or hypoxia depress contraction of skinned rabbit skeletal and cardiac muscle. J Physiol. 1989 May;412:155–180. doi: 10.1113/jphysiol.1989.sp017609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Grabowski W., Lobsiger E. A., Lüttgau H. C. The effect of repetitive stimulation at low frequencies upon the electrical and mechanical activity of single muscle fibres. Pflugers Arch. 1972;334(3):222–239. doi: 10.1007/BF00626225. [DOI] [PubMed] [Google Scholar]
  8. Györke S., Palade P. Calcium-induced calcium release in crayfish skeletal muscle. J Physiol. 1992 Nov;457:195–210. doi: 10.1113/jphysiol.1992.sp019373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Han J. W., Thieleczek R., Varsányi M., Heilmeyer L. M., Jr Compartmentalized ATP synthesis in skeletal muscle triads. Biochemistry. 1992 Jan 21;31(2):377–384. doi: 10.1021/bi00117a010. [DOI] [PubMed] [Google Scholar]
  10. Hille B., Campbell D. T. An improved vaseline gap voltage clamp for skeletal muscle fibers. J Gen Physiol. 1976 Mar;67(3):265–293. doi: 10.1085/jgp.67.3.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Klein M. G., Simon B. J., Szucs G., Schneider M. F. Simultaneous recording of calcium transients in skeletal muscle using high- and low-affinity calcium indicators. Biophys J. 1988 Jun;53(6):971–988. doi: 10.1016/S0006-3495(88)83178-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kovács L., Ríos E., Schneider M. F. Calcium transients and intramembrane charge movement in skeletal muscle fibres. Nature. 1979 May 31;279(5712):391–396. doi: 10.1038/279391a0. [DOI] [PubMed] [Google Scholar]
  13. Lamb G. D., Recupero E., Stephenson D. G. Effect of myoplasmic pH on excitation-contraction coupling in skeletal muscle fibres of the toad. J Physiol. 1992 Mar;448:211–224. doi: 10.1113/jphysiol.1992.sp019037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lamb G. D., Stephenson D. G. Effect of Mg2+ on the control of Ca2+ release in skeletal muscle fibres of the toad. J Physiol. 1991 Mar;434:507–528. doi: 10.1113/jphysiol.1991.sp018483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lee J. A., Westerblad H., Allen D. G. Changes in tetanic and resting [Ca2+]i during fatigue and recovery of single muscle fibres from Xenopus laevis. J Physiol. 1991 Feb;433:307–326. doi: 10.1113/jphysiol.1991.sp018427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lännergren J., Westerblad H. Force decline due to fatigue and intracellular acidification in isolated fibres from mouse skeletal muscle. J Physiol. 1991 Mar;434:307–322. doi: 10.1113/jphysiol.1991.sp018471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lännergren J., Westerblad H. Maximum tension and force-velocity properties of fatigued, single Xenopus muscle fibres studied by caffeine and high K+. J Physiol. 1989 Feb;409:473–490. doi: 10.1113/jphysiol.1989.sp017508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Maylie J., Irving M., Sizto N. L., Boyarsky G., Chandler W. K. Calcium signals recorded from cut frog twitch fibers containing tetramethylmurexide. J Gen Physiol. 1987 Jan;89(1):145–176. doi: 10.1085/jgp.89.1.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Meissner G., Darling E., Eveleth J. Kinetics of rapid Ca2+ release by sarcoplasmic reticulum. Effects of Ca2+, Mg2+, and adenine nucleotides. Biochemistry. 1986 Jan 14;25(1):236–244. doi: 10.1021/bi00349a033. [DOI] [PubMed] [Google Scholar]
  20. Nassar-Gentina V., Passonneau J. V., Vergara J. L., Rapoport S. I. Metabolic correlates of fatigue and of recovery from fatigue in single frog muscle fibers. J Gen Physiol. 1978 Nov;72(5):593–606. doi: 10.1085/jgp.72.5.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Palade P., Vergara J. Arsenazo III and antipyrylazo III calcium transients in single skeletal muscle fibers. J Gen Physiol. 1982 Apr;79(4):679–707. doi: 10.1085/jgp.79.4.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Renaud J. M. The effect of lactate on intracellular pH and force recovery of fatigued sartorius muscles of the frog, Rana pipiens. J Physiol. 1989 Sep;416:31–47. doi: 10.1113/jphysiol.1989.sp017747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Saks V. A., Ventura-Clapier R., Huchua Z. A., Preobrazhensky A. N., Emelin I. V. Creatine kinase in regulation of heart function and metabolism. I. Further evidence for compartmentation of adenine nucleotides in cardiac myofibrillar and sarcolemmal coupled ATPase-creatine kinase systems. Biochim Biophys Acta. 1984 Apr 16;803(4):254–264. doi: 10.1016/0167-4889(84)90115-0. [DOI] [PubMed] [Google Scholar]
  24. Schneider M. F., Chandler W. K. Voltage dependent charge movement of skeletal muscle: a possible step in excitation-contraction coupling. Nature. 1973 Mar 23;242(5395):244–246. doi: 10.1038/242244a0. [DOI] [PubMed] [Google Scholar]
  25. Takasago T., Imagawa T., Furukawa K., Ogurusu T., Shigekawa M. Regulation of the cardiac ryanodine receptor by protein kinase-dependent phosphorylation. J Biochem. 1991 Jan;109(1):163–170. doi: 10.1093/oxfordjournals.jbchem.a123339. [DOI] [PubMed] [Google Scholar]
  26. Westerblad H., Allen D. G. Myoplasmic free Mg2+ concentration during repetitive stimulation of single fibres from mouse skeletal muscle. J Physiol. 1992;453:413–434. doi: 10.1113/jphysiol.1992.sp019236. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Westerblad H., Lee J. A., Lamb A. G., Bolsover S. R., Allen D. G. Spatial gradients of intracellular calcium in skeletal muscle during fatigue. Pflugers Arch. 1990 Mar;415(6):734–740. doi: 10.1007/BF02584013. [DOI] [PubMed] [Google Scholar]
  28. Westerblad H., Lee J. A., Lännergren J., Allen D. G. Cellular mechanisms of fatigue in skeletal muscle. Am J Physiol. 1991 Aug;261(2 Pt 1):C195–C209. doi: 10.1152/ajpcell.1991.261.2.C195. [DOI] [PubMed] [Google Scholar]
  29. Westerblad H., Lännergren J. Force and membrane potential during and after fatiguing, intermittent tetanic stimulation of single Xenopus muscle fibres. Acta Physiol Scand. 1986 Nov;128(3):369–378. doi: 10.1111/j.1748-1716.1986.tb07990.x. [DOI] [PubMed] [Google Scholar]
  30. Westerblad H., Lännergren J. The relation between force and intracellular pH in fatigued, single Xenopus muscle fibres. Acta Physiol Scand. 1988 May;133(1):83–89. doi: 10.1111/j.1748-1716.1988.tb08383.x. [DOI] [PubMed] [Google Scholar]
  31. Zhu Y., Nosek T. M. Intracellular milieu changes associated with hypoxia impair sarcoplasmic reticulum Ca2+ transport in cardiac muscle. Am J Physiol. 1991 Sep;261(3 Pt 2):H620–H626. doi: 10.1152/ajpheart.1991.261.3.H620. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES