Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1982;329:527–540.1. doi: 10.1113/jphysiol.1982.sp014317

Calcium- and length-dependent force production in rat ventricular muscle

M G Hibberd 1,*, B R Jewell 1,
PMCID: PMC1224794  PMID: 7143258

Abstract

1. Trabeculae from the right ventricles of rat hearts were `skinned' by immersion for 30 min in a solution containing the non-ionic detergent Brij-58 at a concentration of 1%.

2. The average sarcomere length in the central region of the relaxed preparation was estimated by laser diffraction and set at pre-determined values within the range of 1·9-2·4 μm by adjustment of muscle length. Isometric contractions were then induced by raising the Ca2+ concentration under carefully controlled chemical conditions.

3. The dependence of Ca2+-activated force production on sarcomere length over the ascending limb of the length—force relation was examined at Ca2+ concentrations giving partial and full activation of the contractile system of the muscle.

4. The dependence of Ca2+-activated force on Ca2+ concentration was compared at sarcomere lengths on the ascending limb and plateau of the length—force relation.

5. The results obtained from both kinds of experiment showed that the sensitivity of the contractile system to Ca2+ increases with sarcomere length over the ascending limb of the length—force relation.

6. Possible explanations for this observation have been discussed.

Full text

PDF
527

Images in this article

Selected References

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

  1. Allen D. G., Blinks J. R. Calcium transients in aequorin-injected frog cardiac muscle. Nature. 1978 Jun 15;273(5663):509–513. doi: 10.1038/273509a0. [DOI] [PubMed] [Google Scholar]
  2. Allen D. G., Jewell B. R., Murray J. W. The contribution of activation processes to the length-tension relation of cardiac muscle. Nature. 1974 Apr 12;248(449):606–607. doi: 10.1038/248606a0. [DOI] [PubMed] [Google Scholar]
  3. Allen D. G., Kurihara S. Calcium transients at different muscle lengths in rat ventricular muscle [proceedings]. J Physiol. 1979 Jul;292:68P–69P. [PubMed] [Google Scholar]
  4. Allen D. G., Kurihara S. The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. J Physiol. 1982 Jun;327:79–94. doi: 10.1113/jphysiol.1982.sp014221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ashley C. C., Moisescu D. G. Effect of changing the composition of the bathing solutions upon the isometric tension-pCa relationship in bundles of crustacean myofibrils. J Physiol. 1977 Sep;270(3):627–652. doi: 10.1113/jphysiol.1977.sp011972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brandt P. W., Cox R. N., Kawai M. Can the binding of Ca2+ to two regulatory sites on troponin C determine the steep pCa/tension relationship of skeletal muscle? Proc Natl Acad Sci U S A. 1980 Aug;77(8):4717–4720. doi: 10.1073/pnas.77.8.4717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brandt P. W., Reuben J. P., Grundfest H. Regulation of tension in the skinned crayfish muscle fiber. II. Role of calcium. J Gen Physiol. 1972 Mar;59(3):305–317. doi: 10.1085/jgp.59.3.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bremel R. D., Weber A. Cooperation within actin filament in vertebrate skeletal muscle. Nat New Biol. 1972 Jul 26;238(82):97–101. doi: 10.1038/newbio238097a0. [DOI] [PubMed] [Google Scholar]
  9. Dobson J. G., Jr, Schwab G. E., Ross J., Jr, Mayer S. E. Comparison of the biochemical composition of four preparations of contracting cardiac muscle. Am J Physiol. 1974 Dec;227(6):1452–1457. doi: 10.1152/ajplegacy.1974.227.6.1452. [DOI] [PubMed] [Google Scholar]
  10. Ellis D., Thomas R. C. Direct measurement of the intracellular pH of mammalian cardiac muscle. J Physiol. 1976 Nov;262(3):755–771. doi: 10.1113/jphysiol.1976.sp011619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. FURCHGOTT R. F., LEE K. S. High energy phosphates and the force of contraction of cardiac muscle. Circulation. 1961 Aug;24:416–432. doi: 10.1161/01.cir.24.2.416. [DOI] [PubMed] [Google Scholar]
  12. Fabiato A., Fabiato F. Contractions induced by a calcium-triggered release of calcium from the sarcoplasmic reticulum of single skinned cardiac cells. J Physiol. 1975 Aug;249(3):469–495. doi: 10.1113/jphysiol.1975.sp011026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fabiato A., Fabiato F. Dependence of the contractile activation of skinned cardiac cells on the sarcomere length. Nature. 1975 Jul 3;256(5512):54–56. doi: 10.1038/256054a0. [DOI] [PubMed] [Google Scholar]
  14. Fabiato A., Fabiato F. Myofilament-generated tension oscillations during partial calcium activation and activation dependence of the sarcomere length-tension relation of skinned cardiac cells. J Gen Physiol. 1978 Nov;72(5):667–699. doi: 10.1085/jgp.72.5.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ford L. E., Huxley A. F., Simmons R. M. Tension responses to sudden length change in stimulated frog muscle fibres near slack length. J Physiol. 1977 Jul;269(2):441–515. doi: 10.1113/jphysiol.1977.sp011911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fozzard H. A., Lee C. O. Influence of changes in external potassium and chloride ions on membrane potential and intracellular potassium ion activity in rabbit ventricular muscle. J Physiol. 1976 Apr;256(3):663–689. doi: 10.1113/jphysiol.1976.sp011345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fuchs F. Cooperative interactions between calcium-binding sites on glycerinated muscle fibers. The influence of cross-bridge attachment. Biochim Biophys Acta. 1977 Nov 17;462(2):314–322. doi: 10.1016/0005-2728(77)90130-x. [DOI] [PubMed] [Google Scholar]
  18. Fuchs F. The binding of calcium to glycerinated muscle fibers in rigor. The effect of filament overlap. Biochim Biophys Acta. 1977 Apr 25;491(2):523–531. doi: 10.1016/0005-2795(77)90297-5. [DOI] [PubMed] [Google Scholar]
  19. Goodship-Patience R., Hibberd M. G., Jewell B. R. Apparatus for studying the mechanical properties of skinned muscle fibres [proceedings]. J Physiol. 1979 May;290(2):13P–14P. [PubMed] [Google Scholar]
  20. Gordon A. M., Pollack G. H. Effects of calcium on the sarcomere length-tension relation in rat cardiac muscle. Implications for the Frank-Starling mechanism. Circ Res. 1980 Oct;47(4):610–619. doi: 10.1161/01.res.47.4.610. [DOI] [PubMed] [Google Scholar]
  21. Hibberd M. G., Jewell B. R. Length-dependence of the sensitivity of the contractile system to calcium in rat ventricular muscle [proceedings]. J Physiol. 1979 May;290(2):30P–31P. [PubMed] [Google Scholar]
  22. Holroyde M. J., Robertson S. P., Johnson J. D., Solaro R. J., Potter J. D. The calcium and magnesium binding sites on cardiac troponin and their role in the regulation of myofibrillar adenosine triphosphatase. J Biol Chem. 1980 Dec 25;255(24):11688–11693. [PubMed] [Google Scholar]
  23. Huntsman L. L., Stewart D. K. Length-dependent calcium inotropism in cat papillary muscle. Circ Res. 1977 Apr;40(4):366–371. doi: 10.1161/01.res.40.4.366. [DOI] [PubMed] [Google Scholar]
  24. Johnson J. D., Charlton S. C., Potter J. D. A fluorescence stopped flow analysis of Ca2+ exchange with troponin C. J Biol Chem. 1979 May 10;254(9):3497–3502. [PubMed] [Google Scholar]
  25. Lakatta E. G., Jewell B. R. Length-dependent activation: its effect on the length-tension relation in cat ventricular muscle. Circ Res. 1977 Mar;40(3):251–257. doi: 10.1161/01.res.40.3.251. [DOI] [PubMed] [Google Scholar]
  26. Maughan D. W., Low E. S., Alpert N. R. Isometric force development, isotonic shortening, and elasticity measurements from Ca2+-activated ventricular muscle of the guinea pig. J Gen Physiol. 1978 Apr;71(4):431–451. doi: 10.1085/jgp.71.4.431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Moisescu D. G. Kinetics of reaction in calcium-activated skinned muscle fibres. Nature. 1976 Aug 12;262(5569):610–613. doi: 10.1038/262610a0. [DOI] [PubMed] [Google Scholar]
  28. Moisescu D. G., Thieleczek R. Sarcomere length effects on the Sr2+- and Ca2+-activation curves in skinned frog muscle fibres. Biochim Biophys Acta. 1979 Apr 11;546(1):64–76. doi: 10.1016/0005-2728(79)90170-1. [DOI] [PubMed] [Google Scholar]
  29. Orentlicher M., Reuben J. P., Grundfest H., Brandt P. W. Calcium binding and tension development in detergent-treated muscle fibers. J Gen Physiol. 1974 Feb;63(2):168–186. doi: 10.1085/jgp.63.2.168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Parmley W. W., Chuck L. Length-dependent changes in myocardial contractile state. Am J Physiol. 1973 May;224(5):1195–1199. doi: 10.1152/ajplegacy.1973.224.5.1195. [DOI] [PubMed] [Google Scholar]
  31. Polimeni P. I., Page E. Magnesium in heart muscle. Circ Res. 1973 Oct 5;33(4):367–374. doi: 10.1161/01.res.33.4.367. [DOI] [PubMed] [Google Scholar]
  32. Thames M. D., Teichholz L. E., Podolsky R. J. Ionic strength and the contraction kinetics of skinned muscle fibers. J Gen Physiol. 1974 Apr;63(4):509–530. doi: 10.1085/jgp.63.4.509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. ter Keurs H. E., Rijnsburger W. H., van Heuningen R., Nagelsmit M. J. Tension development and sarcomere length in rat cardiac trabeculae. Evidence of length-dependent activation. Circ Res. 1980 May;46(5):703–714. doi: 10.1161/01.res.46.5.703. [DOI] [PubMed] [Google Scholar]

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

RESOURCES