Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 1977 Aug;19(2):103–116. doi: 10.1016/S0006-3495(77)85573-2

Swelling of Skinned Muscle Fibers of the Frog

Experimental Observations

Robert E Godt, David W Maughan
PMCID: PMC1473314  PMID: 18220

Abstract

Frog skeletal muscle fibers, mechanically skinned under water-saturated silicone oil, swell upon transfer to aqueous relaxing medium (60 mM KCl; 3 mM MgCl2; 3 mM ATP; 4 mM EGTA; 20 mM Tris maleate; pH = 7.0; ionic strength 0.15 M). Their cross-sectional areas, estimated with an elliptical approximation, increase 2.32-fold (±0.54 SD). Sarcomere spacing is unaffected by this swelling. Addition of 200 mM sucrose to relaxing medium had no effect on fiber dimensions, whereas decreasing pH to 5.0 caused fibers to shrink nearly to their original (oil) size. Decreasing MgCl2 to 0.3 mM caused fibers to swell 10%, and increasing MgCl2 to 9 mM led to an 8% shrinkage. Increasing ionic strength to 0.29 M with KCl caused a 26% increase in cross-sectional area; decreasing ionic strength to 0.09 M had no effect. Swelling pressure was estimated with long-chain polymers, which are probably excluded from the myofilament lattice. Shrinkage in dextran T10 (number average mol wt 6,200) was transient, indicating that this polymer may penetrate into the fibers. Shrinkage in dextran T40 (number average mol wt 28,000), polyvinylpyrrolidone (PVP) K30 (number average mol wt 40,000) and dextran T70 (number average mol wt 40,300) was not transient, indicating exclusion. Maximal calcium-activated tension is decreased by 21% in PVP solutions and by 31% in dextran T40 solutions. Fibers were shrunk to their original size with 8 × 10-2 g/cm3 PVP K30, a concentration which, from osmometric data, corresponds to an osmotic pressure (II/RT) of 10.5 mM. As discussed in the text, we consider this our best estimate of the swelling pressure. We find that increasing ionic strength to 0.39 M with KCl decreases swelling pressure slightly, whereas decreasing ionic strength to 0.09 M has no effect. We feel these data are consistent with the idea that swelling arises from the negatively charged nature of the myofilaments, from either mutual filamentary repulsion or a Donnan-osmotic mechanism.

Full text

PDF
103

Selected References

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

  1. April E. W., Brandt P. W., Elliott G. F. The myofilament lattice: studies on isolated fibers. I. The constancy of the unit-cell volume with variation in sarcomere length in a lattice in which the thin-to-thick myofilament ratio is 6:1. J Cell Biol. 1971 Oct;51(1):72–82. doi: 10.1083/jcb.51.1.72. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. April E. W., Brandt P. W., Elliott G. F. The myofilament lattice: studies on isolated fibers. II. The effects of osmotic strength, ionic concentration, and pH upon the unit-cell volume. J Cell Biol. 1972 Apr;53(1):53–65. doi: 10.1083/jcb.53.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. April E. W., Brandt P. W. The myofilament lattice: studies on isolated fibers. 3. The effect of myofilament spacing upon tension. J Gen Physiol. 1973 Apr;61(4):490–508. doi: 10.1085/jgp.61.4.490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. April E. W. The myofilament lattice: studies on isolated fibers. IV. Lattice equilibria in striated muscle. J Mechanochem Cell Motil. 1975;3(2):111–121. [PubMed] [Google Scholar]
  5. Beinfeld M. C., Bryce D. A., Kochavy D., Martonosi A. The binding of divalent cations to myosin. J Biol Chem. 1975 Aug 25;250(16):6282–6287. [PubMed] [Google Scholar]
  6. Collins E. W., Jr, Edwards C. Role of Donnan equilibrium in the resting potentials in glycerol-extracted muscle. Am J Physiol. 1971 Oct;221(4):1130–1133. doi: 10.1152/ajplegacy.1971.221.4.1130. [DOI] [PubMed] [Google Scholar]
  7. Edman K. A., Andersson K. E. The variation in active tension with sarcomere length in vertebrate skeletal muscle and its relation to fibre width. Experientia. 1968 Feb 15;24(2):134–136. doi: 10.1007/BF02146942. [DOI] [PubMed] [Google Scholar]
  8. Elliott G. F. Donnan and osmotic effects in muscle fibres without membranes. J Mechanochem Cell Motil. 1973 May;2(1):83–89. [PubMed] [Google Scholar]
  9. Endo M. Calcium release from the sarcoplasmic reticulum. Physiol Rev. 1977 Jan;57(1):71–108. doi: 10.1152/physrev.1977.57.1.71. [DOI] [PubMed] [Google Scholar]
  10. Godt R. E. Calcium-activated tension of skinned muscle fibers of the frog. Dependence on magnesium adenosine triphosphate concentration. J Gen Physiol. 1974 Jun;63(6):722–739. doi: 10.1085/jgp.63.6.722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gordon A. M., Godt R. E., Donaldson S. K., Harris C. E. Tension in skinned frog muscle fibers in solutions of varying ionic strength and neutral salt composition. J Gen Physiol. 1973 Nov;62(5):550–574. doi: 10.1085/jgp.62.5.550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hellam D. C., Podolsky R. J. Force measurements in skinned muscle fibres. J Physiol. 1969 Feb;200(3):807–819. doi: 10.1113/jphysiol.1969.sp008723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. MARTONOSII A., MOLINO C. M., GERGELY J. THE BINDING OF DIVALENT CATIONS TO ACTIN. J Biol Chem. 1964 Apr;239:1057–1064. [PubMed] [Google Scholar]
  14. Matsubara I., Elliott G. F. X-ray diffraction studies on skinned single fibres of frog skeletal muscle. J Mol Biol. 1972 Dec 30;72(3):657–669. doi: 10.1016/0022-2836(72)90183-0. [DOI] [PubMed] [Google Scholar]
  15. Okada R. D., Gordon A. M. Excitation, contraction, and excitation-contraction coupling of frog muscles in hypotonic solutions. Life Sci I. 1972 May 1;11(9):449–460. doi: 10.1016/0024-3205(72)90117-8. [DOI] [PubMed] [Google Scholar]
  16. Rome E. Relaxation of glycerinated muscle: low-angle x-ray diffraction studies. J Mol Biol. 1972 Mar 28;65(2):331–345. doi: 10.1016/0022-2836(72)90285-9. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES