Journal of Muscle Research & Cell Motility

, Volume 13, Issue 4, pp 406–419 | Cite as

Interpretation of the X-ray diffraction pattern from relaxed skeletal muscle and modelling of the thick filament structure

  • S. B. Malinchik
  • V. V. Lednev


The first part of this paper is devoted to the model-building studies of our high resolution meridional X-ray diffraction patterns (in the region from 1/500 to 1/50 Å−1) obtained from relaxed frog muscle. A one-dimensional model of thick filament was proposed which basically consists of two symmetrical arrays of 50 crossbridge crown projections. In the proximate and central zones of the filament the crossbridge crowns are regularly shifted with a 429 Å period and appear as triplets with a 130 Å distance between crowns, while the crowns in the distal parts of filament are regularly ordered with a 143 Å repeat. The centre-to-centre distance between regions with crossbridge perturbations is 7050 Å. The length of each crown projection is about 125 Å. The model includes also (1) C-protein component represented in each half of the filament by seven stripes of about 350 Å long and located 429 Å apart, (2) a uniform density of filament backbone of about 1.5 μm length, and (3) 13 high density stripes in a central zone located with 223 Å period. The final model explains very well the positions and intensities of the main meridional reflections. A three-dimensional model of crossbridge configuration is described in the second part of the work. The model was constructed by using the intensity profiles of the first six myosin layer lines of the X-ray pattern from stretched muscle and taking into account the crossbridge perturbations and the axial size of crossbridge crown obtained from the one-dimensional studies. It was found that both myosin heads are tilted in opposite directions along the filament and wrap around the filament backbone. This crossbridge configuration corresponds well to the findings of Haselgrove. To take into account interference effects between thick filaments we proposed a model of the filament hexagonal lattice with disorder of the second kind. The cross-sectional width of crystalline domains in stretched muscle was estimated to be about 0.11 μm. The models presented may be helpful in the interpretation of the X-ray diffraction patterns from contracting muscle.


Central Zone Myosin Head Contracting Muscle Layer Line Thick Filament 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bennett, P. M., Starr, R., Elliott, A. &Offer, G. (1985) The structure of C-protein and X-protein molecules and a polymer of X-protein.J. Mol. Biol. 184, 297–309.PubMedGoogle Scholar
  2. Bennett, P. M., Craig, R., Starr, R. &Offer, G. (1986) The ultrastructural location of C-protein and H-protein in rabbit muscle.J. Muscle Res. Cell Motil. 7, 550–67.PubMedGoogle Scholar
  3. Borejdo, J., Assulin, O., Ando, T. &Putnam, S. (1982) Crossbridge orientation in skeletal muscle measured by linear dichroism of an extrinsic chromophore.J. Mol. Biol. 158, 391–414.PubMedGoogle Scholar
  4. Cantino, M. &Squire, J. M. (1986) Resting myosin crossbridge conformation in frog muscle thick filaments.J. Cell Biol. 102, 610–18.PubMedGoogle Scholar
  5. Craig, R. (1977) Structure of A-segments from frog and rabbit skeletal muscle.J. Mol. Biol. 109, 69–81.PubMedGoogle Scholar
  6. Crowther, R. A., Padron, R. &Craig, R. (1985) Arrangement of heads of myosin in relaxed thick filaments from tarantula muscle.J. Mol. Biol. 184 429–39.PubMedGoogle Scholar
  7. Edman, A., Squire, J. &Sjostrom, M. (1988) Fine structure of the A-band in cryo-sections.J. Ultrastruct. Mol. Struct. Res. 100, 1–12.PubMedGoogle Scholar
  8. Elliott, G. F., Lowy, J. &Worthington, C. R. (1963) An X-ray 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
  9. Harford, J. &Squire, J. (1986) The ‘crystalline’ myosin crossbridge array in relaxed bony fish muscle: low-angle X-ray diffraction from plaice fin muscle and its interpretation.Biophys. J. 50, 145–55.PubMedGoogle Scholar
  10. Haselgrove, J. C. (1975) X-ray evidence for conformational changes in the myosin filaments of vertebrate striated muscle.J. Mol. Biol. 92, 113–43.Google Scholar
  11. Haselgrove, J. C. (1980) A model of myosin crossbridge structure consistent with the low angle X-ray diffraction pattern of vertebrate muscle.J. Muscle Res. Cell Motil. 1, 177–91.PubMedGoogle Scholar
  12. Haselgrove, J. C. &Huxley, H. E. (1973) X-Ray evidence for radial crossbridge movement and for the sliding filament model in actively contracting skeletal muscle.J. Mol. Biol. 77, 549–68.PubMedGoogle Scholar
  13. Hosemann, R. &Bagchi, S. N. (1962).Direct Analysis of Diffraction by Matter, Amsterdam: North-Holland.Google Scholar
  14. Huxley, H. E. &Brown, W. (1967). The low-angle X-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor.J. Mol. Biol. 30, 383–434.PubMedGoogle Scholar
  15. Huxley, H. E., Faruqi, A. R., Kress, M., Bordas, J. &Koch, M. H. J. (1982) Time-resolved X-ray diffraction studies of the myosin layer-line reflections during muscle contraction.J. Mol. Biol. 158, 637–84.PubMedGoogle Scholar
  16. Huxley, H. E., Simmons, R. M., Faruqi, A. R., Kress, M., Boras, J. &Koch, M. H. J. (1983) Changes in the X-ray reflections from contracting muscle during rapid mechanical transients and their structural implications.J. Mol. Biol. 169, 496–506.Google Scholar
  17. Kensler, R. W. &Stewart, M. (1986) An ultrastructural study of crossbridge arrangement in the frog thigh muscle thick filament.Biophys. J. 49, 343–51.PubMedGoogle Scholar
  18. Lednev, V. V., Srebnitskaya, L. K., Kornev, A. N., Khromov, A. S. &Malinchik, S. B. (1981) Localization of minor proteins and structural changes in myosin filaments of vertebrate skeletal muscles.Biofizika 26, 739–48 (in Russian).PubMedGoogle Scholar
  19. Malinchik, S. B. &Lednev, V. V. (1986) Interpretation of the X-ray meridional diffraction pattern of frog skeletal muscle in resting state.Doklady Academii Nauk USSR 289, 1258–62 (in Russian).Google Scholar
  20. Malinchik, S. B. &Lednev, V. V. (1987) Interpretation of the X-ray diffraction pattern of skeletal muscle in resting state: 3D-model of thick filament.Doklady Academii Nauk USSR 293, 238–42 (in Russian).Google Scholar
  21. Miller, A. &Tregear, R. T. (1972) Structure of insect fibrillar flight muscle in the presence and absence of ATP.J. Mol. Biol. 70, 85–104.PubMedGoogle Scholar
  22. Offer, G., Moos, C. S. &Starr, R. (1973) A new protein of the thick filaments of vertebrate skeletal myofibrils. Extraction, purification and characterization.J. Mol. Biol. 74, 653–76.PubMedGoogle Scholar
  23. Poulsen, F. R. &Lowy, J. (1983) Small-angle X-ray scattering from myosin heads in relaxed and rigor frog skeletal muscle.Nature (Lond.) 303, 146–52.Google Scholar
  24. Poulsen, F. R. &Lowy, J. (1984) Application of potential energy calculations to the determination of muscle structure from X-ray data with special reference to the configuration of myosin heads.J. Mol. Biol. 174, 239–47.PubMedGoogle Scholar
  25. Rome, E., Offer, G. &Pepe, F. A. (1973) X-ray diffraction of muscle labelled with antibody to C-protein.Nature New Biology 244, 152–4.PubMedGoogle Scholar
  26. Shimizu, T., Dennis, J., Masaki, T. &Fischman, D. (1985) Axial arrangement of the myosin rod in vertebrate thick filaments: immunoelectron microscopy with a monoclonal antibody to light meromyosin.J. Cell Biol. 101, 115–23.Google Scholar
  27. Sjostrom, M. &Squire, J. M. (1977) Fine structure of the A-band in cryo-sections.J. Mol. Biol. 109, 49–68.PubMedGoogle Scholar
  28. Squire, J. M. (1975) Muscle filament structure and muscle contraction.Ann. Rev. Biophys. Bioeng. 4, 291–323.Google Scholar
  29. Squire, J. M. (1981).The Structural Basis of Muscle Contraction, London: Plenum Press.Google Scholar
  30. Squire, J. M., Harford, J. J., Edman, A. C. &Sjostrom, M. (1982) Fine structure of the A-band in cryo-sections. III. Crossbridge distribution and the axial structure of the human C-zone.J. Mol. Biol. 155, 467–94.PubMedGoogle Scholar
  31. Stewart, M. &Kensler, R. W. (1986) Arrangement of myosin heads in relaxed thick filaments from frog skeletal muscle.J. Mol. Biol. 192, 831–51.PubMedGoogle Scholar
  32. Stewart, M., Kensler, R. W. &Levine, R. J. C. (1985) Threedimensional reconstruction of thick filaments fromLimulus and scorpion muscle.J. Cell Biol. 101, 402–11.PubMedGoogle Scholar
  33. Thomas, D. D. &Cooke, R. (1980) Orientation of spin-labelled myosin heads in glycerinated muscle fibres.Biophys. J. 32, 891–906.PubMedGoogle Scholar
  34. Thomas, D. D., Ishiwata, S., Seidel, J. C. &Gergely, J. (1980) Submillisecond rotational dynamics of spin-labelled myosin heads in myofibrils.Biophys. J. 32, 873–90.PubMedGoogle Scholar
  35. Trombitas, K., Baatsen, P. H. W. W. &Pollack, G. H. (1988) I-bands of striated muscle contain lateral struts.J. Ultra struct. Mol Struct. Res. 100, 13–30.Google Scholar
  36. Vainstein, B. M. (1966).Diffraction of X-rays by Chain Molecules, Amsterdam: Elsevier.Google Scholar
  37. Yagi, N., O'Brien, E. J. &Matsubara, I. (1981) Changes of thick filament structure during contraction of frog striated muscle.Biophys. J. 33, 121–38.PubMedGoogle Scholar
  38. Yu, L. C., Steven, A. C., Naylor, G. R. S., Gamble, R. C. &Podolsky, R. J. (1985) Distribution of mass in relaxed frog skeletal muscle and its redistribution upon activation.Biophys. J. 47, 311–21.PubMedGoogle Scholar

Copyright information

© Chapman & Hall 1992

Authors and Affiliations

  • S. B. Malinchik
    • 1
  • V. V. Lednev
    • 1
  1. 1.Institute of Biological PhysicsAcademy of SciencesPushchinoRussia

Personalised recommendations