Journal of Muscle Research & Cell Motility

, Volume 14, Issue 6, pp 573–584

Contraction-induced movements of water in single fibres of frog skeletal muscle

  • Károly Trombitás
  • Peter Baatsen
  • John Schreuder
  • Gerald H. Pollack
Papers

Summary

Although X-ray diffraction measurements imply almost constant filament separation during isometric contraction, such constancy does not hold at the level of the isolated cell; cell cross-section increases substantially during isometric contraction. This expansion could arise from accumulation of water drawn from other fibre regions, or from water drawn into the cell from outside. To distinguish between these hypotheses, we froze single fibres of frog skeletal muscle that were jacketed by a thin layer of water. Frozen fibres were freeze-substituted, sectioned transversely, and examined in the electron microscope. In fibres frozen during contraction, we found large amounts of water just beneath the sarcolemma, less in deeper regions, and almost none in the fibre core. Such gradients were absent or diminished in fibres frozen in the relaxed state. The water was not confined to the myofibril space alone; we found large water spaces between myofibrils, particularly near mitochondria. Accumulation of water between myofibrils and around mitochondria implies that the driving force for water movement probably lies outside the filament lattice, and may therefore be osmotic. The fact that the distribution was nonuniform-highest near the sarcolemma and lowest in the core-implies that the water was likely drawn from the thin jacket surrounding the cell. Thus, the contractile cycle appears to be associated with water entry into and exit from the cell.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. ABBOTT, B. C. & BASKIN, J. R. (1962) Volume changes in frog muscle during contraction. J. Physiol. 161, 379–91.Google Scholar
  2. APRIL, E. W., BRANDT, P. W. & ELLIOTT, G. E. (1971) The myofilament lattice: studies on isolated fibers. J. Cell Biol. 51, 71–82.Google Scholar
  3. BAATSEN, P. H. (1991) Ultrastructural Aspects of Skeletal Muscle Revealed by Quick-Freezing Methods. Doctoral dissertation, University of Washington, Seattle, WA.Google Scholar
  4. BROWN, L. & HILL, L. (1982) Mercuric chloride in alcohol and chloroform used as a rapidly acting fixative for contracting muscle fibres. J. Microsc. 125, 319–36.Google Scholar
  5. BROWN, L. M., CONZÁLEZ-SERRATOS, H. & HUXLEY, A. F. (1984) Structural studies of the waves in striated muscle fibres shortened passively below their slack length. J. Muscle Res. Cell Motil. 5, 273–92.Google Scholar
  6. CECCHI, G., BAGNI, M. A., GRIFFITHS, P. J., ASHLEY, C. C. & MAÉDA, Y. (1990) Detection of radial crossbridge force by lattice spacing changes in intact single muscle fibers. Science 250, 1409–11.Google Scholar
  7. EDELMANN, L. (1988) The cell water problem posed by electron microscopic studies of ion binding in muscle. Scanning Microscopy 2(2), 851–65.Google Scholar
  8. EDMAN, K. A. P. & LOU, F. (1990) Changes in force and stiffness induced by fatigue and intracellular acidification in frog muscle fibres. J. Physiol. 424, 133–49.Google Scholar
  9. EDMAN, K. A. P. & LOU, F. (1992) Myofibrillar fatigue versus failure of activation during repetitive stimulation of frog muscle fibres. J. Physiol. 457, 655–73.Google Scholar
  10. ELLIOTT, G. F., LOWY, J. & MILLMAN, B. M. (1967) Low-angle X-ray diffraction studies of living striated muscle during contraction. J. Mol. Biol. 25, 31–45.Google Scholar
  11. GRANZIER, H. L. M. (1988) Sarcomere Mechanics and the Mechanism of Muscle Contraction. Doctoral dissertation, University of Washington, Seattle, WA.Google Scholar
  12. GRANZIER, H. L. M. & POLLACK, G. H. (1989) Effect of active pre-shortening on isometric and isotonic performance of single frog muscle fibres. J. Physiol. 415, 299–327.Google Scholar
  13. HASELGROVE, J. C. & HUXLEY, H. E. (1973) X-ray evidence for radial cross-bridge movement and for the sliding filament model in actively contracting skeletal muscle. J. Mol. Biol. 77, 549–68.Google Scholar
  14. IRVING, M., WOLEDGE, R. C. & YAMADA, K. (1979) The heat produced by frog muscle in a series of contractions with shortening. J. Physiol. 293, 103–18.Google Scholar
  15. LÄNNERGREN, J., WESTERBLAD, H. & FLOCK, B. (1990) Transient appearance of vacuoles in fatigued Xenopus muscle fibers. Acta Physiol. Scand. 140, 437–45.Google Scholar
  16. LÄNNERGREN, J. & NOTH, J. (1973) Tension in isolated frog muscle fibres induced by hypertonic solutions. J. Gen. Physiol. 61, 158–75.Google Scholar
  17. LING, G. N. (1992) A Revolution in the Physiology of the Living Cell, Malabar, FL: Krieger Publication Co.Google Scholar
  18. LING, G. N. & OCHSENFELD, M. M. (1992) The majority of potassium ions in muscle cells is adsorbed on β- and γ-carboxyl groups of myosin: potassium-ion-adsorbing carboxyl groups on myosin heads engage in cross-bridge formation during contraction. Physiol. Chem. Phys. Med. NMR 23, 133–60.Google Scholar
  19. MATSUBARA, I. &ELLIOTT, G. F. (1972) X-ray diffraction studies on skinned single fibres of frog skeletal muscle. J. Mol. Biol. 72, 657–69.Google Scholar
  20. MAUGHAN, D. & RECCHIA, C. (1985) Diffusible sodium, potassium, magnesium, calcium and phosphorus in frog skeletal muscle. J. Physiol. 368, 545–63.Google Scholar
  21. MÜLLER, M., MARTI, T. & KRIZ, S. (1980) Improved structural preservation by freeze substitution. In Electron Microscopy (ed. BREDEROO, P. & DEPRIESTER, W.) pp. 720–1 Leiden: Seventh European Congress on Electron Microscopy Foundation.Google Scholar
  22. NEERING, I. R., QUESENBERRY, L. A., MORRIS, V. A. & TAYLOR, S. R. (1991) Nonuniform volume changes during muscle contraction. Biophys. J. 59, 926–32.Google Scholar
  23. NOTH, J. (1974) Osmotic water movement across the sarcolemma of frog skeletal muscle fibers. J. Membrane Biol. 17, 367–82.Google Scholar
  24. PADRÓN, R., ALAMO, L., CRAIG, R. & CAPUTO, C. (1988) A method for quick-freezing live muscles at known instants during contraction with simultaneous recordings of mechanical tension. J. Microsc. 151, 81–102.Google Scholar
  25. PERIASAMY, A., BURNS, D. H., HOLDREN, D. N., POLLACK, G. H. & TROMBITÁS, K. (1990) A-band shortening in single fibers of frog skeletal muscle. Biophys. J. 57, 815–28.Google Scholar
  26. PLATTNER, H. & BACHMANN, L. (1982) Cryofixation: a tool in biological ultrastructural research. Int. Rev. 79, 237–304.Google Scholar
  27. POLLACK, G. H. (1990) Muscles and Molecules: Uncovering the Principles of Biological Motion. Seattle: Ebner & Sons.Google Scholar
  28. RASMUSSEN, D. H. Ice formation in aqueous systems. J. Microsc. 128, 167–74.Google Scholar
  29. TASAKI, I. & BYRNE, P. M. (1988) Volume expansion of nonmyelinated nerve fibres during impulse conduction. Biophys. J. 57, 633–5.Google Scholar
  30. TASAKI, I. (1988) A macromolecular approach to excitation phenomena: mechanical and thermal changes in nerve during excitation. Physiol. Chem. Phys. Med. NMR 20, 251–68.Google Scholar
  31. TAYLOR, S. R., NEERING, I. R., QUESENBERRY, L. A. & MORRIS, V. A. (1992) Volume changes during contraction of isolated frog muscle fibres. In: Excitation-Contraction Coupling in Skeletal, Cardiac and Smooth Muscle (edited by FRANK, G. B.) pp. 91–101. New York: Plenum Press.Google Scholar
  32. TSUKITA, S. (1988) Dynamic aspects of sarcoplasmic reticulum detected by rapid-freeze method. Seibutsu Butsari 28, 167–70.Google Scholar
  33. WESTERBLAD, H. & LÄNNERGREN, J. (1991) Slowing of relaxation during fatigue in single muscle fibres. J. Physiol. 434, 323–36.Google Scholar
  34. YAGI, N., ITO, H., NAKAJIMA, T., IZUMI, T. & MATSUBARA, I. (1977) Return of myosin heads to thick filaments after muscle contraction. Science 197, 685–7.Google Scholar

Copyright information

© Chapman & Hall 1993

Authors and Affiliations

  • Károly Trombitás
    • 1
  • Peter Baatsen
    • 1
  • John Schreuder
    • 1
  • Gerald H. Pollack
    • 1
  1. 1.Center for Bioengineering WD-12University of WashingtonSeattleUSA

Personalised recommendations