Journal of Muscle Research & Cell Motility

, Volume 13, Issue 1, pp 100–105

Z-line/I-band and A-band lattices of intact frog sartorius muscle at altered interfilament spacing

  • Thomas C. Irving
  • Barry M. Millman
Papers

Summary

Muscle contraction has long been known to be affected by the osmolarity of the bathing solution. Part of this effect is caused by changes in interfilament spacing in the A-band. We have investigated the variation in spacing of the square lattice of thin filaments within and near the Z-line (the Z-line/I-band or Z-I lattice) in intact frog sartorius muscle over a wide range of osmolarities and compared it with the corresponding changes in the A-band lattice. Both lattices have a lower limit for compression and an upper limit for swelling. The spacing of the Z-I lattice is nearly proportional to that of the A-band, but shows a 2–3% variation at extreme shrinkage or swelling. In normal intact muscle, the osmotically-inactive volume of both lattices is between 20 and 30%. Thesein vivo measurements of lattice spacing differ significantly from those observed in electron micrographs. With moderate variations in osmolarity, lattice spacing and muscle fibre width show similar behaviour, but at extreme osmolarities, the lattice spacing changes less than the fibre width. An equatorial reflection was observed in intact muscle, previously identified in skinned muscle, which does not index on the A-band and which changes with osmolarity in a manner different from that observed for the A-band and Z-I lattices. This reflection may arise from changes in the ordering of the Z-I lattice or may involve components additional to the thick and thin filaments.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bergman, R. A. (1983) Ultrastructural configuration of sarcomeres in passive and contracted frog sartorius muscle.Amer. J. Anat. 166, 209–22.PubMedGoogle Scholar
  2. Boyle, P. J. &Conway, E. J. (1941) Potassium accumulation in muscle and associated changes.J. Fhysiol. 100, 1–63.Google Scholar
  3. Elliott, G. F. &Lowy, J. (1968) Organization of actin in a mammalian smooth muscle.Nature 219, 156–7.PubMedGoogle Scholar
  4. Elliott, G. F., Lowy, J. &Worthington, C. R. (1963) An X-ray diffraction and light diffraction study of the filament lattice of striated muscle in the living state and in rigor.J. Mol. Biol. 6, 295–305.Google Scholar
  5. 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.PubMedGoogle Scholar
  6. Goldstein, M. A., Michael, L. H., Schroeter, J. P. &Sass, R. L. (1987) Z-band dynamics as a function of sarcomere length and the contractile state of muscle.FASEB J. 1, 133–42.PubMedGoogle Scholar
  7. Gulati, J. &Babu, A. (1982) Tonicity effects on intact single muscle fibres: relation between force and cell volume.Science 215, 1109–12.PubMedGoogle Scholar
  8. Gulati, J. &Babu, A. (1984) Intrinsic shortening speed of temperature-jump-activated intact muscle fibres.Biophys. J. 45, 431–45.PubMedGoogle Scholar
  9. Gulati, J. &Babu, A. (1985) Critical dependence of calciumactivated force on width in highly compressed skinned fibres of the frog.Biophys. J. 48, 781–7.PubMedGoogle Scholar
  10. Higuchi, H. (1987) Lattice swelling with selective digestion of elastic components in single skinned fibres of the frog.Biophys. J. 52, 29–32.PubMedGoogle Scholar
  11. Higuchi, H. &Umazume, Y. (1986) Lattice shrinkage with increasing resting tension in stretched, single-skinned fibres of frog muscle.Biophys. J. 50, 385–9.PubMedGoogle Scholar
  12. Irving, T. C. (1989) Analysis of the equatorial X-ray diffraction pattern of vertebrate striated muscle. PhD Thesis, University of Guelph, Ontario, Canada.Google Scholar
  13. Irving, T. C. &Millman, B. M. (1989) Changes in thick filament structure during compression of the filament lattice in frog sartorius muscle.J. Muscle Res. Cell Motil. 10, 385–96.PubMedGoogle Scholar
  14. Lowy, J. &Vtbert, P. J. (1967) Structure and organization of actin in a molluscan smooth muscle.Nature 215, 1254–5.PubMedGoogle Scholar
  15. Magid, A. &Reedy, M. K. (1980) X-ray diffraction observations of chemically-skinned frog skeletal muscle processed by an improved method.Biophys. J. 30, 27–40.PubMedGoogle Scholar
  16. Mansson, A. (1989) The effects of tonicity on tension and stiffness of tentanized skeletal muscle fibres of the frog.Acta Physiol. Scand. 136, 205–16.PubMedGoogle Scholar
  17. Matsubara, I. &Elliott, G. F. (1972) X-ray diffraction studies on skinned single fibres of frog skeletal muscle.J. Mol. Biol. 72, 657–69.PubMedGoogle Scholar
  18. Matsubara, I., Goldman, Y. E. &Simmons, R. M. (1984) Changes in the lateral filament spacing of skinned muscle fibres when crossbridges attach.J. Mol. Biol. 173, 15–33.PubMedGoogle Scholar
  19. Millman, B. M. &Nickel, B. G. (1980) Electrostatic forces in muscle and cylindrical gel systems.Biophys. J. 32, 49–63.PubMedGoogle Scholar
  20. Millman, B. M. &Bell, R. M. (1983) Lateral forces between actin filaments in muscle.Biophys. J. 41, 253a.Google Scholar
  21. Millman, B. M. &Irving, T. C. (1988) Filament lattice of frog striated muscle. Radial forces, lattice stability and filament compression in the A-band of relaxed and rigor muscle.Biophys. J. 54, 437–47.PubMedGoogle Scholar
  22. Millman, B. M., Racey, T. J. &Matsubara, I. (1981) Effects of hyperosmotic solutions on the filament lattice of intact frog skeletal muscle.Biophys. J. 33, 189–201.PubMedGoogle Scholar
  23. Millman, B. M., Wakabayashi, K. &Racey, T. J. (1983) Lateral forces in the filament lattice of vertebrate striated muscle in the rigor state.Biophys. J. 41, 259–67.PubMedGoogle Scholar
  24. Rome, E. M. (1968) X-ray diffraction studies of the filament lattice of striated muscle in various bathing media.J. Mol. Biol. 37, 331–44.PubMedGoogle Scholar
  25. Rome, E. M. (1972) Relaxation of glycerinated muscle: low-angle X-ray diffraction studies.J. Mol. Biol. 65, 331–45.PubMedGoogle Scholar
  26. Williams, B. A. (1989) Filament lattice spacing in the A-band of frog sartorius muscles in the relaxed and contracting states. MSc Thesis, Univeristy of Guelph, Ontario, Canada.Google Scholar
  27. Yamaguchi, M., Izumimoto, M., Robson, R. M. &Stromer, M. H. (1985) Fine structure of wide and narrow vertebrate muscle Z-lines. A proposed model and computer simulation of Z-line architecture.J. Mol. Biol. 184, 621–44.PubMedGoogle Scholar
  28. Yu, L. C., Lymn, R. W. &Podolsky, R. J. (1977) Characterization of a non-indexible equatorial X-ray reflection from frog sartorius muscle.J. Mol. Biol. 115, 445–64.Google Scholar
  29. Yu, L. C., Arata, I., Steven, A. C., Naylor, G. R. S., Gamble, R. C. &Podolsky, R. J. (1984) Structural studies of muscle during force development in various states.Adv. Exp. Med. Biol. 170, 207–20.PubMedGoogle Scholar

Copyright information

© Chapman & Hall 1992

Authors and Affiliations

  • Thomas C. Irving
    • 1
  • Barry M. Millman
    • 1
  1. 1.Biophysics Interdepartmental Group, Department of PhysicsUniversity of GuelphGuelphCanada
  2. 2.MacCHESS, Department of Biochemistry, Biotechnology BuildingCornell UniversityIthecaUSA

Personalised recommendations