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Nonlinear summation of contractions in striated muscle. II. Potentiation of intracellular Ca2+ movements in single barnacle muscle fibres

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Summary

Nonlinear summation of contractions is studied in single barnacle (Balanus nubilus) muscle fibres, loaded with the photoprotein aequorin. The results indicate that nonlinear summation of aequorin transients is indeed present and for short interpulse intervals (25–250 ms), a more-than-linear summation of transients, which suggest an increase of the cytosolic Ca2+ concentration in the second response, is observed. This augmented Ca2+ concentration is not merely due to summation with the preceding conditioning transient, but to an enlargement of the second transient in its own right. Furthermore, the enlargement of the second Ca2+ response is not the result of prolonged release, or slowing of re-uptake by intracellular organelles. On the contrary, Ca2+ release is found to be enhanced and for short depolarizations (20 ms), its time to half re-uptake is reduced. The intensified Ca2+ release, triggered by the second standard depolarization, is related to the level of cytosolic Ca2+ concentration reached in the conditioning response and, for example, appears to be larger in the presence of Dantrolene-sodium, which is known to reduce Ca2+ movements in a single twitch. It is concluded that contractile potentiation observed during nonlinear summation of contractions, is associated with a potentiation of intracellular Ca2+ movements, which interact to regulate the cytosolic Ca2+ concentration during contraction.

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References

  1. Ashley, C. C. (1983) Calcium in muscle. InCalcium in Biological Systems (edited bySpiro, T.), pp. 107–73. New York: Wiley.

  2. Ashley, C. C. &Lignon, J. (1981) Aequorin responses during relaxation of tension of single muscle fibres stimulated by voltage clamp.J. Physiol., Lond. 318, 10–11p.

  3. Ashley, C. C. &Moisescu, D. G. (1972) Model for the action of calcium in muscle.Nature, Lond. 237, 208–11.

  4. Ashley, C. C. &Ridgway, E. B. (1970) On the relationships between membrane potential, calcium transient and tension in single barnacle muscle fibres.J. Physiol., Lond. 209, 105–30.

  5. Ashley, C. C. &Thomas, M. V. (1983) Ca2+ indicators in voltage-clamped single muscle fibres.J. Musc. Res. Cell Motility 3, 505–6.

  6. Blinks, J. R., Rüdel, R. &Taylor, S. R. (1978) Calcium transients in isolated amphibian skeletal muscle fibres: detection with aequorin.J. Physiol., Lond. 277, 291–323.

  7. Carafoli, E., Clementi, F., Drabikowski, W. &Margreth, A. (eds) (1975)Calcium Transport in Contraction and Secretion, p 588. Amsterdam: North-Holland Publishing Company.

  8. Cooper, S. &Eccles, J. C. (1930) The isometric responses of mammalian muscles.J. Physiol., Lond. 69, 377–85.

  9. Desmedt, J. E. &Hainaut, K. (1968) Kinetics of myofilament activation in potentiated contraction: the staircase phenomenon in human skeletal muscle.Nature, Lond. 217, 529–32.

  10. Duchateau, J. &Hainaut, K. (1986) Nonlinear summation of contractions in striated muscle. I. Twitch potentiation in human muscle.J. Musc. Res. Cell Motility 7, 11–17.

  11. Ebashi, S. (1976) Excitation-contraction coupling.A. Rev. Physiol. 38, 293–313.

  12. Ebashi, S. &Endo, M. (1968) Calcium ion and muscle contraction.Prog. Biophys. molec. Biol. 18, 123–83.

  13. Fatt, P. &Katz, B. (1953) The electrical properties of crustacean muscle fibres.J. Physiol., Lond. 120, 171–204.

  14. Ford, L. E. &Podolsky, R. J. (1970) Regenerative calcium release within muscle cells.Science, N. Y. 167, 58–9.

  15. Hainaut, K. &Desmedt, J. E. (1974a) Calcium ionophore A 23187 potentiates twitch and intracellular calcium release in single muscle fibres.Nature, Lond. 252, 407–8.

  16. Hainaut, K. &Desmedt, J. E. (1974b) Effect of Dantrolene sodium on calcium movements in single muscle fibres.Nature, Lond. 252, 728–30.

  17. Hoyle, G. &Smith, T. (1963) Neuromuscular physiology of giant muscle fibres of a barnacle,Balanus nubilus Darwin.Comp. Biochem. Physiol. 10, 291–314.

  18. Katz, B. (1969)The Release of Neural Transmitter Substances, p. 60. Liverpool: University Press.

  19. Makinose, M. (1975) The mechanism of rapid calcium exchange between the inside and outside of the sarcoplasmic membrane. InCalcium Transport in Contraction and Secretion (edited byCarafoli, E., Clementi, F., Drabikowski, W. andMargreth, A.), pp. 367–72. Amsterdam: North-Holland Publishing Company.

  20. Parmiggiani, F. &Stein, R. B. (1981) Nonlinear summation of contractions in cat muscles. II. Later facilitation and stiffness changes.J. gen. Physiol. 78, 295–311.

  21. Stein, R. B. &Parmiggiani, F. (1981) Nonlinear summation of contractions in cat muscles. I. Early depression.J. gen. Physiol. 78, 277–93.

  22. Ritchie, J. M. &Wilkie, D. R. (1955) The effect of previous stimulation on the active state of muscle.J. Physiol. Lond. 130, 488–96.

  23. Ridgway, E. B. &Gordon, A. M. (1984) Effect of post-stimulus length changes in single fibers.J. gen. Physiol. 83, 75–103.

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Correspondence to K. Hainaut.

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Duchateau, J., Hainaut, K. Nonlinear summation of contractions in striated muscle. II. Potentiation of intracellular Ca2+ movements in single barnacle muscle fibres. J Muscle Res Cell Motil 7, 18–24 (1986). https://doi.org/10.1007/BF01756198

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Keywords

  • Striate Muscle
  • Muscle Fibre
  • Intracellular Organelle
  • Prolonged Release
  • Interpulse Interval