Skip to main content
PMC home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1973 Nov 1;62(5):550–574. doi: 10.1085/jgp.62.5.550

Tension in Skinned Frog Muscle Fibers in Solutions of Varying Ionic Strength and Neutral Salt Composition

A M Gordon 1, R E Godt 1, S K B Donaldson 1, C E Harris 1
PMCID: PMC2226133  PMID: 4543066

Abstract

The maximal calcium-activated isometric tension produced by a skinned frog single muscle fiber falls off as the ionic strength of the solution bathing this fiber is elevated declining to zero near 0.5 M as the ionic strength is varied using KCl. When other neutral salts are used, the tension always declines at high ionic strength, but there is some difference between the various neutral salts used. The anions and cations can be ordered in terms of their ability to inhibit the maximal calcium-activated tension. The order of increasing inhibition of tension (decreasing tension) at high ionic strength for anions is propionate- ≃ SO4 -- < Cl- < Br-. The order of increasing inhibition of calcium-activated tension for cations is K+ ≃ Na+ ≃ TMA+ < TEA+ < TPrA+ < TBuA+. The decline of maximal calcium-activated isometric tension with elevated salt concentration (ionic strength) can quantitatively explain the decline of isometric tetanic tension of a frog muscle fiber bathed in a hypertonic solution if one assumes that the internal ionic strength of a muscle fiber in normal Ringer's solution is 0.14–0.17 M. There is an increase in the base-line tension of a skinned muscle fiber bathed in a relaxing solution (no added calcium and 3 mM EGTA) of low ionic strength. This tension, which has no correlate in the intact fiber in hypotonic solutions, appears to be a noncalcium-activated tension and correlates more with a declining ionic strength than with small changes in [MgATP], [Mg], pH buffer, or [EGTA]. It is dependent upon the specific neutral salts used with cations being ordered in increasing inhibition of this noncalcium-activated tension (decreasing tension) as TPrA+ < TMA+ < K+ ≃ Na+. Measurements of potentials inside these skinned muscle fibers bathed in relaxing solutions produced occasional small positive values (<6 mV) which were not significantly different from zero.

Full Text

The Full Text of this article is available as a PDF (1.5 MB).

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. 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]
  2. April E., Brandt P. W., Reuben J. P., Grundfest H. Muscle contraction: the effect of ionic strength. Nature. 1968 Oct 12;220(5163):182–184. doi: 10.1038/220182a0. [DOI] [PubMed] [Google Scholar]
  3. Ashley C. C., Ridgway E. B. On the relationships between membrane potential, calcium transient and tension in single barnacle muscle fibres. J Physiol. 1970 Jul;209(1):105–130. doi: 10.1113/jphysiol.1970.sp009158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Buller A. J., Mommaerts W. F., Seraydarian K. Enzymic properties of myosin in fast and slow twitch muscles of the cat following cross-innervation. J Physiol. 1969 Dec;205(3):581–597. doi: 10.1113/jphysiol.1969.sp008984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. CONWAY E. J. Nature and significance of concentration relations of potassium and sodium ions in skeletal muscle. Physiol Rev. 1957 Jan;37(1):84–132. doi: 10.1152/physrev.1957.37.1.84. [DOI] [PubMed] [Google Scholar]
  7. Caputo C. Caffeine- and potassium-induced contractures of frog striated muscle fibers in hypertonic solutions. J Gen Physiol. 1966 Sep;50(1):129–139. doi: 10.1085/jgp.50.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Dancker P., Hasselbach W. Dependence of actomyosin ATPase activity on ionic strength and its modification by thiol group substitution. FEBS Lett. 1971 Sep 1;16(4):272–274. doi: 10.1016/0014-5793(71)80367-8. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Gibbs C. L., Ricchiuti N. V., Mommaerts W. F. Activation heat in frog sartorius muscle. J Gen Physiol. 1966 Jan;49(3):517–535. doi: 10.1085/jgp.49.3.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gordon A. M., Godt R. E. Some effects of hypertonic solutions on contraction and excitation-contraction coupling in frog skeletal muscles. J Gen Physiol. 1970 Feb;55(2):254–275. doi: 10.1085/jgp.55.2.254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gordon A. M., Huxley A. F., Julian F. J. The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol. 1966 May;184(1):170–192. doi: 10.1113/jphysiol.1966.sp007909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. HILL A. V. The priority of the heat production in a muscle twitch. Proc R Soc Lond B Biol Sci. 1958 Mar 18;148(932):397–402. doi: 10.1098/rspb.1958.0033. [DOI] [PubMed] [Google Scholar]
  15. HODGKIN A. L., HOROWICZ P. Potassium contractures in single muscle fibres. J Physiol. 1960 Sep;153:386–403. doi: 10.1113/jphysiol.1960.sp006541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. HOWARTH J. V. The behaviour of frog muscle in hypertonic solutions. J Physiol. 1958 Nov 10;144(1):167–175. doi: 10.1113/jphysiol.1958.sp006093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Jacobs H. K., Guthe K. F. Anions and the contraction of glycerol-extracted muscle fibers. Arch Biochem Biophys. 1970 Jan;136(1):36–40. doi: 10.1016/0003-9861(70)90323-1. [DOI] [PubMed] [Google Scholar]
  19. Kaldor G., Chowrashi P. K., Hsu Q. S. Studies on the interaction of actomyosin with polyions. Arch Biochem Biophys. 1968 Oct;128(1):261–268. doi: 10.1016/0003-9861(68)90030-1. [DOI] [PubMed] [Google Scholar]
  20. Katz A. M. Effects of alkali metal ions on the Mg2+-activated ATPase activity of reconstituted actomyosin. Biochim Biophys Acta. 1968 Jul 16;162(1):79–85. doi: 10.1016/0005-2728(68)90216-8. [DOI] [PubMed] [Google Scholar]
  21. Katz A. M. Purification and properties of a tropomyosin-containing protein fraction that sensitizes reconstituted actomyosin to calcium-binding agents. J Biol Chem. 1966 Apr 10;241(7):1522–1529. [PubMed] [Google Scholar]
  22. Kerrick W. G., Donaldson S. K. The effects of Mg 2+ on submaximum Ca 2+ -activated tension in skinned fibers of frog skeletal muscle. Biochim Biophys Acta. 1972 Jul 12;275(1):117–122. doi: 10.1016/0005-2728(72)90030-8. [DOI] [PubMed] [Google Scholar]
  23. Kominz D. R. Studies of adenosine triphosphatase activity and turbidity in myofibril and actomyosin suspensions. Biochemistry. 1970 Apr 14;9(8):1792–1801. doi: 10.1021/bi00810a019. [DOI] [PubMed] [Google Scholar]
  24. Kushmerick M. J., Podolsky R. J. Ionic mobility in muscle cells. Science. 1969 Dec 5;166(3910):1297–1298. doi: 10.1126/science.166.3910.1297. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. McLaughlin S. G., Szabo G., Eisenman G. Divalent ions and the surface potential of charged phospholipid membranes. J Gen Physiol. 1971 Dec;58(6):667–687. doi: 10.1085/jgp.58.6.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Miyamoto M., Hubbard J. I. On the inhibition of muscle contraction caused by exposure to hypertonic solutions. J Gen Physiol. 1972 Jun;59(6):689–700. doi: 10.1085/jgp.59.6.689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Muir J. R., Weber A., Olson R. E. Cardiac myofibrillar ATPase: a comparison with that of fast skeletal actomyosin in its native and in an altered conformation. Biochim Biophys Acta. 1971 May 11;234(2):199–209. doi: 10.1016/0005-2728(71)90075-2. [DOI] [PubMed] [Google Scholar]
  29. Nakano J., Moore S. E. Effect of different alcohols on the contractile force of the isolated guinea-pig myocardium. Eur J Pharmacol. 1972 Dec;20(3):266–270. doi: 10.1016/0014-2999(72)90184-7. [DOI] [PubMed] [Google Scholar]
  30. Ogawa Y. The apparent binding constant of glycoletherdiaminetetraacetic acid for calcium at neutral pH. J Biochem. 1968 Aug;64(2):255–257. doi: 10.1093/oxfordjournals.jbchem.a128887. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Portzehl H., Zaoralek P., Gaudin J. The activation by Ca2+ of the ATPase of extracted muscle fibrilsith variation of ionic strength, pH and concentration of MgATP. Biochim Biophys Acta. 1969;189(3):440–448. doi: 10.1016/0005-2728(69)90175-3. [DOI] [PubMed] [Google Scholar]
  33. WEBER A., HERZ R. The binding of calcium to actomyosin systems in relation to their biological activity. J Biol Chem. 1963 Feb;238:599–605. [PubMed] [Google Scholar]
  34. Warren J. C., Stowring L., Morales M. F. The effect of structure-disrupting ions on the activity of myosin and other enzymes. J Biol Chem. 1966 Jan 25;241(2):309–316. [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES