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. 1979 Mar;288:45–70.

The extracellular compartments of frog skeletal muscle.

M C Neville, R T Mathias
PMCID: PMC1281414  PMID: 313982

Abstract

1. Detailed studies of solute efflux from frog sartorius muscle and single muscle fibres were carried out in order to characterize a 'special region' (Harris, 1963) in the extracellular space of muscle and determine whether this 'special region' is the sarcoplasmic reticulum. 2. The efflux of radioactive Na, Cl, glusose, 3-O-methylglucose, xylose, glycine, leucine, cycloleucine, Rb, K, inulin (mol. wt. 5000) and dextran (mol. wt. 17,000) from previously loaded muscles was studied. In all cases except dextran the curve had three components, a rapid (A) component which could be equated with efflux from the extracellular space proper, a slow (C) component representing cellular solute and an intermediate (B) component. The distribution space for the B component was 8% of muscle volume in summer frogs and 12% in winter frogs and appeared to be equal for all compounds studied. We tested the hypothesis that the B component originated from the sarcoplasmic reticulum. 3. The C component was missing from the dextran curves. Both dextran and inulin entered the compartment of origin of the B component (compartment B) to the same extent as small molecules. 4. For all compounds studies, the efflux rate constant for the A component could be predicted from the diffusion coefficient. For the B component the efflux rate constant was 6--10 times slower than that for the A component but was still proportional to the diffusion coefficient for the solute in question. 5. When Na and sucrose efflux from single fibres was followed, a B component was usually observed. The average distribution space for this component was small, averaging 1.5% of fibre volume. There was no difference between the average efflux rate constants for Na and sucrose. 6. In an appendix, the constraints placed on the properties of a hypothetical channel between the sarcoplasmic reticulum and the T-system by the linear electrical parameters of frog skeletal muscle are derived. It is shown that the conductance of such a channel must be less than 0.06 x 10(-3) mohs/cm2 of fibre membrane. 7. The conductance between compartment B and the extracellular space can be calculated from the efflux rate constants for Na, K and Cl. The value obtained was 5 x 10(-3) mhos/cm2 of fibre membrane or 100 times the limiting value for the conductance of the T-SR junction. 8. The finding that there is a B component in the efflux curves for large molecular weight substances like inulin and dextran and the small size of the B component in efflux curves from single muscle fibres indicate that the 'speical region' of the extra-cellular space of frog muscle is not the sarcoplasmic reticulum. This conclusion is confirmed by a calculation of the conductance between the B compartment and the extracellular space. The value obtained is incompatible with predicted electrical properteis of the SR-T-tubule junction...

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Selected References

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

  1. ADRIAN R. H. Internal chloride concentration and chloride efflux of frog muscle. J Physiol. 1961 May;156:623–632. doi: 10.1113/jphysiol.1961.sp006698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adrian R. H., Almers W. Membrane capacity measurements on frog skeletal muscle in media of low ion content. J Physiol. 1974 Mar;237(3):573–605. doi: 10.1113/jphysiol.1974.sp010499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BLINKS J. R. INFLUENCE OF OSMOTIC STRENGTH ON CROSS-SECTION AND VOLUME OF ISOLATED SINGLE MUSCLE FIBRES. J Physiol. 1965 Mar;177:42–57. doi: 10.1113/jphysiol.1965.sp007574. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Birks R. I., Davey D. F. Osmotic responses demonstrating the extracellular character of the sarcoplasmic reticulum. J Physiol. 1969 May;202(1):171–188. doi: 10.1113/jphysiol.1969.sp008802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boyle P. J., Conway E. J., Kane F., O'reilly H. L. Volume of interfibre spaces in frog muscle and the calculation of concentrations in the fibre water. J Physiol. 1941 Jun 30;99(4):401–414. doi: 10.1113/jphysiol.1941.sp003911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Case R., Creese R., Dixon W. J., Massey F. J., Taylor D. B. Movement of labelled decamethonium in muscle fibres of the rat. J Physiol. 1977 Nov;272(2):283–294. doi: 10.1113/jphysiol.1977.sp012044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chandler W. K., Rakowski R. F., Schneider M. F. Effects of glycerol treatment and maintained depolarization on charge movement in skeletal muscle. J Physiol. 1976 Jan;254(2):285–316. doi: 10.1113/jphysiol.1976.sp011233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Costantin L. L. Contractile activation in skeletal muscle. Prog Biophys Mol Biol. 1975;29(2):197–224. doi: 10.1016/0079-6107(76)90023-7. [DOI] [PubMed] [Google Scholar]
  9. DESMEDT J. E. Electrical activity and intracellular sodium concentration in frog muscle. J Physiol. 1953 Jul;121(1):191–205. doi: 10.1113/jphysiol.1953.sp004940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. DYDYNSKA M., WILKIE D. R. THE OSMOTIC PROPERTIES OF STRIATED MUSCLE FIBERS IN HYPERTONIC SOLUTIONS. J Physiol. 1963 Nov;169:312–329. doi: 10.1113/jphysiol.1963.sp007258. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dell R. B., Sciacca R., Lieberman K., Case D. B., Cannon P. J. A weighted least-squares technique for the analysis of kinetic data and its application to the study of renal xenon washout in dogs and man. Circ Res. 1973 Jan;32(1):71–84. doi: 10.1161/01.res.32.1.71. [DOI] [PubMed] [Google Scholar]
  12. Eisenberg B., Eisenberg R. S. Selective disruption of the sarcotubular system in frog sartorius muscle. A quantitative study with exogenous peroxidase as a marker. J Cell Biol. 1968 Nov;39(2):451–467. doi: 10.1083/jcb.39.2.451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Eisenberg R. S., Gage P. W. Ionic conductances of the surface and transverse tubular membranes of frog sartorius fibers. J Gen Physiol. 1969 Mar;53(3):279–297. doi: 10.1085/jgp.53.3.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Endo M. Entry of fluorescent dyes into the sarcotubular system of the frog muscle. J Physiol. 1966 Jul;185(1):224–238. doi: 10.1113/jphysiol.1966.sp007983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. HARRIS E. J. Distribution and movement of muscle chloride. J Physiol. 1963 Apr;166:87–109. doi: 10.1113/jphysiol.1963.sp007092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. HILL D. K. THE SPACE ACCESSIBLE TO ALBUMIN WITHIN THE STRIATED MUSCLE FIBRE OF THE TOAD. J Physiol. 1964 Dec;175:275–294. doi: 10.1113/jphysiol.1964.sp007517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. HODGKIN A. L., HOROWICZ P. Movements of Na and K in single muscle fibres. J Physiol. 1959 Mar 3;145(2):405–432. doi: 10.1113/jphysiol.1959.sp006150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. JOHNSON J. A. Kinetics of release of radioactive sodium, sulfate and sucrose from the frog sartorius muscle. Am J Physiol. 1955 May;181(2):263–268. doi: 10.1152/ajplegacy.1955.181.2.263. [DOI] [PubMed] [Google Scholar]
  19. Kirby A. C., Lindley B. D., Picken J. R. Calcium content and exchange in frog skeletal muscle. J Physiol. 1975 Dec;253(1):37–52. doi: 10.1113/jphysiol.1975.sp011178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kulczycky S., Mainwood G. W. Evidence for a functional connection between the sarcoplasmic reticulum and the extracellular space in frog sartorius muscle. Can J Physiol Pharmacol. 1972 Feb;50(2):87–98. doi: 10.1139/y72-015. [DOI] [PubMed] [Google Scholar]
  21. Ling G. N. Cell membrane and cell permeability. Ann N Y Acad Sci. 1966 Jul 14;137(2):837–859. doi: 10.1111/j.1749-6632.1966.tb50204.x. [DOI] [PubMed] [Google Scholar]
  22. Ling G. N., Kromash M. H. The extracellular space of voluntary muscle tissues. J Gen Physiol. 1967 Jan;50(3):677–694. doi: 10.1085/jgp.50.3.677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Macdonald R. L., Mann J. E., Jr, Sperelakis N. Derivation of general equations describing tracer diffusion in any two-compartment tissue with application to ionic diffusion in cylindrical muscle bundles. J Theor Biol. 1974 May;45(1):107–130. doi: 10.1016/0022-5193(74)90046-0. [DOI] [PubMed] [Google Scholar]
  24. Mathias R. T., Eisenberg R. S., Valdiosera R. Electrical properties of frog skeletal muscle fibers interpreted with a mesh model of the tubular system. Biophys J. 1977 Jan;17(1):57–93. doi: 10.1016/S0006-3495(77)85627-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mobley B. A., Eisenberg B. R. Sizes of components in frog skeletal muscle measured by methods of stereology. J Gen Physiol. 1975 Jul;66(1):31–45. doi: 10.1085/jgp.66.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. NARAHARA H. T., OZAND P. Studies of tissue permeability. IX. The effect of insulin on the penetration of 3-methylglucose-H3 in frog muscle. J Biol Chem. 1963 Jan;238:40–49. [PubMed] [Google Scholar]
  27. Neville M. C. Solute concentration gradients in frog muscles at 0 degree C: active transport or adsorption? Science. 1972 Apr 21;176(4032):302–303. doi: 10.1126/science.176.4032.302. [DOI] [PubMed] [Google Scholar]
  28. Neville M. C., White S. Extracellular space of frog skeletal muscle in vivo and in vitro: relation to proton magnetic resonance relaxation times. J Physiol. 1979 Mar;288:71–83. [PMC free article] [PubMed] [Google Scholar]
  29. Peachey L. D. The sarcoplasmic reticulum and transverse tubules of the frog's sartorius. J Cell Biol. 1965 Jun;25(3 Suppl):209–231. doi: 10.1083/jcb.25.3.209. [DOI] [PubMed] [Google Scholar]
  30. Revel J. P., Karnovsky M. J. Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J Cell Biol. 1967 Jun;33(3):C7–C12. doi: 10.1083/jcb.33.3.c7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rogus E., Zierler K. L. Sodium and water contents of sarcoplasm and sarcoplasmic reticulum in rat skeletal muscle: effects of anisotonic media, ouabain and external sodium. J Physiol. 1973 Sep;233(2):227–270. doi: 10.1113/jphysiol.1973.sp010307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rubio R., Sperelakis N. Penetration of horseradish peroxidase into the terminal cisternae of frog skeletal muscle fibers and blockade of caffeine contracture by Ca ++ depletion. Z Zellforsch Mikrosk Anat. 1972;124(1):57–71. [PubMed] [Google Scholar]
  33. Schneider M. F., Chandler W. K. Effects of membrane potential on the capacitance of skeletal muscle fibers. J Gen Physiol. 1976 Feb;67(2):125–163. doi: 10.1085/jgp.67.2.125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sjodin R. A., Beaugé L. A. An analysis of the leakages of sodium ions into and potassium ions out of striated muscle cells. J Gen Physiol. 1973 Feb;61(2):222–250. doi: 10.1085/jgp.61.2.222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Somlyo A. V., Shuman H., Somlyo A. P. Composition of sarcoplasmic reticulum in situ by electron probe X-ray microanalysis. Nature. 1977 Aug 11;268(5620):556–558. doi: 10.1038/268556a0. [DOI] [PubMed] [Google Scholar]
  36. Somlyo A. V., Shuman H., Somlyo A. P. Elemental distribution in striated muscle and the effects of hypertonicity. Electron probe analysis of cryo sections. J Cell Biol. 1977 Sep;74(3):828–857. doi: 10.1083/jcb.74.3.828. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sperelakis N., Valle R., Orozco C., Martínez-Palomo A., Rubio R. Electromechanical uncoupling of frog skeletal muscle by possible change in sarcoplasmic reticulum content. Am J Physiol. 1973 Oct;225(4):793–800. doi: 10.1152/ajplegacy.1973.225.4.793. [DOI] [PubMed] [Google Scholar]
  38. TASKER P., SIMON S. E., JOHNSTONE B. M., SHANKLY K. H., SHAW F. H. The dimensions of the extracellular space in sartorius muscle. J Gen Physiol. 1959 Sep;43:39–53. doi: 10.1085/jgp.43.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Vinogradova N. A., Nikol'skii N. N., Troshin A. S. Raspredelenie sakharov mezhdu portniazhnymi myshtsami liagushki i sredoi. Tsitologiia. 1967 Jun;9(6):658–665. [PubMed] [Google Scholar]
  40. Vinogradova N. A. Raspredelenie inulina, sakharozy i fruktozy v portniazhnykh myshtsakh liagushki. Tsitologiia. 1967 Jul;9(7):781–790. [PubMed] [Google Scholar]
  41. Vinogradova N. A. Raspredelenie nepronikaiushchikh sakharov v portniazhnykh myshtsakh liagushki v usloviiakh giopo- i gipertonii. Tsitologiia. 1968 Jul;10(7):831–838. [PubMed] [Google Scholar]
  42. Winegrad S. The intracellular site of calcium activaton of contraction in frog skeletal muscle. J Gen Physiol. 1970 Jan;55(1):77–88. doi: 10.1085/jgp.55.1.77. [DOI] [PMC free article] [PubMed] [Google Scholar]

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