Journal of Muscle Research & Cell Motility

, Volume 10, Issue 4, pp 297–311 | Cite as

The ‘catch’ mechanism in molluscan muscle: an electron microscopy study of freeze-substituted anterior byssus retractor muscle ofMytilus edulis

  • Pauline M. Bennett
  • Arthur Elliott


A method for quick-freezing muscles while observing their mechanical properties until the moment of freezing is described. This method was used to freeze the anterior byssus retractor muscle (ABRM) ofMytilus edulis. Intact muscle in the presence of sucrose as a cryoprotectant was freeze-substituted in acetone, fixed and embedded for electron microscopy. ABRM was frozen in a number of mechanical states including ‘catch’, the state of high passive tension particularly associated with some molluscan muscles. Transverse sections were examined to determine the distribution of filaments in the muscle cells. In the relaxed muscle thick and thin filaments are fairly randomly distributed. Groups of thin filaments and of thick filaments are often seen, and there is no obvious association between the two types of filaments. In contrast, in rigor muscles, both glycerol-extracted and intact, most of the thin filaments were found to lie in rings or rosettes around the thick filaments. In some places bridges between thick and thin filaments could be distinguished. In actively contracting muscle (phasic contraction) the appearance is intermediate between that of the relaxed and rigor muscles. Many thick filaments are surrounded by rosettes of thin filaments but many of the thin filaments are grouped and have no connections with thick filaments. The ‘catch’ state, left after a period of tonic contraction, is similar in its distributrion of thick and thin filaments to the active state, many of the thin filaments lying between the thick. Frequently thick and thin filaments seem to be closer together than in other states of the muscle where a pronounced exclusion zone is present around the thick filaments. There is no evidence for association between the thick filaments.

The different distribution of thin filaments in the different states is consistent with the previously described X-ray diffraction data if it is assumed that most of the contribution to the equatorial reflection at 12 nm comes from the groups of thin filaments. Our data support a model for catch in which there is a change in the association between thick and thin filaments, rather than one in which thick filaments are clumped.


Mechanical State Transverse Section Electron Microscopy Study Thin Filament High Passive 
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. Achazi, R. K. (1979) Phosphorylation of molluscan paramyosin.Pflüegers Arch. ges. Physiol. 379, 197–201.Google Scholar
  2. Achazi, R. K. (1982) Catch Muscle InBasic Biology of Muscles: A Comparative Approach (edited byTwarog, B. M., Levine, R. J. C. &Dewey, M. M.) 291–308. New York: Raven Press.Google Scholar
  3. Bennett, P. M. &Elliott, A. (1981) The structure of the paramyosin core in molluscan thick filaments.J. Musc. Res. Cell Motility 2, 65–81.Google Scholar
  4. Cambridge, G. W., Holgate, J. A. &Sharp, J. A. (1959) A pharmocological analysis of the contractile mechanism ofMytilus muscle.J. Physiol. (Lond.) 148, 451–464.Google Scholar
  5. Castellani, L. &Cohen, C. (1987a) Myosin rod phosphorylation and the catch state of molluscan muscles.Science 235, 334–7.Google Scholar
  6. Castellani, L. &Cohen, C. (1987b) Rod phosphorylation favours folding in a catch muscle myosin.Proc. nain. Acad. Sci. U.S.A. 84, 4058–62.Google Scholar
  7. Cohen, C. (1982) Matching molecules in the catch mechanism.Proc. nain. Acad. Sci. U.S.A. 79, 3176–8.Google Scholar
  8. Cooley, L. B., Johnson, W. H. &Krause, S. (1979) Phosphorylation of paramyosin and its possible role in the catch mechanism.J. biol. Chem. 254, 2195–8.Google Scholar
  9. Cornelius, F. &Lowy, J. (1978) Tension-length behaviour of a molluscan smooth muscle related to filament organisation.Acta Physiol. Scand. 102, 167–80.Google Scholar
  10. Elliott, A. (1965) The use of toroidal reflecting surfaces in X-ray diffraction cameras.J. Sci. Inst. 42, 312–6.Google Scholar
  11. Elliott, A. &Bennett, P. M. (1984) Molecular organization of paramyosin in the core of molluscan thick filamentsJ. molec. Biol. 176, 477–93.Google Scholar
  12. Elliott, G. F. &Lowy, J. (1961) Low-angle X-ray reflections from living molluscan muscles.J. molec. Biol. 3, 41–6.Google Scholar
  13. Gilloteaux, J. &Baguet, F. (1977) Contractile filaments organization in functional states of the anterior byssus retractor muscle (ABRM) ofMytilus edulis L.Cytobiologie 15, 192–220.Google Scholar
  14. Haas, D. J. (1966) Studies of cross-linked lysozyme crystals.Acta Crystallogr. 21, A159–60.Google Scholar
  15. Handley, D. A., Alexander, J. T. &Chien, S. (1981) The design and use of a simple device for rapid quench-freezing of biological samples.J. Micros. 121, 273–82.Google Scholar
  16. Hanson, J. &Lowy, J. (1961) The structure of the muscle fibres in the translucent part of the oyster Crassostrea angulata. Proc. R. Soc. Lond.B154, 173–96.Google Scholar
  17. Hauck, R. &Achazi, R. K. (1987) The ultrastructure of a molluscan catch muscle during a contraction-catchrelaxation cycle.Eur. J. Cell Biol. 45, 30–5.Google Scholar
  18. Heuser, J. E., Reese, T. S., Dennis, M. J., Jan, Y., Jan, L. &Evans, L. (1979) Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release.J. Cell Biol. 81, 275–300.Google Scholar
  19. Jehl, B., Bauer, R., Dörge, A. &Rick, R. (1981) The use of propane/isopentane mixtures for the rapid feezing of biological specimens.J. Micros. 123, 307–9.Google Scholar
  20. Jewell, B. R. (1959) The nature of the phasic and the tonic responses of the anterior byssal retractor muscle of Mytillus.J. Physiol. (Lond.) 149, 154–77.Google Scholar
  21. Johnson, W. H. (1962) Tonic Mechanisms in Smooth Muscles.Physiol. Rev. 42, Suppl. 5, 113–43.Google Scholar
  22. Johnson, W. H., Kahn, J. S. &Szent-Györgyi, A. G. (1959) Paramyosin and contraction of ‘catch muscles’.Science 130, 160–1.Google Scholar
  23. Lowy, J. &Millman, B. M. (1963) The contractile mechanism of the Anterior Byssus Retractor muscle ofMytilus edulis. Phil. Trans. R. Soc. Lond. B246, 105–48.Google Scholar
  24. Lowy, J. &Poulsen, F. R. (1982) Time-resolved X-ray diffraction studies of the structural behaviour of myosin heads in a living contracting unstriated muscleNature 299, 308–12.Google Scholar
  25. Lowy, J. &Vibert, P. J. (1967) Structure and organization of actin in a molluscan smooth muscle.Nature 215, 1254–5.Google Scholar
  26. Lowy, J. &Vibert, P. J. (1972) Studies of the low-angle X-ray pattern of a molluscan smooth muscle during tonic contraction and rigor.Cold Spring Harb. Symp. quant. Biol. 37, 353–9.Google Scholar
  27. Miller, A. (1968) A short periodicity in the thick filaments of theanterior byssus retractor muscle ofMytilus edulis J. molec. Biol. 32, 687–8.Google Scholar
  28. Millman, B. M. &Elliott, G. F. (1973) An X-ray diffraction study of contracting molluscan smooth muscle.Biophys. J. 12, 1405–14.Google Scholar
  29. Potts, W. T. W. (1958) The inorganic and amino acid composition of some lamellibranch muscles.J. exp. Biol. 35, 749–64.Google Scholar
  30. Rebhun, L. I. (1972) Freeze-substitution and freeze-drying, InPrinciples and Techniques of Electron Microscopy Vol. 2, (edited byHayat, M. A.) pp. 3–42. New York: van Nostrand Rheinhold Co.Google Scholar
  31. Rüegg, J. C. (1958) The possible function of invertebrate tropomyosinBiochem. J. 69, 46P.Google Scholar
  32. Rüegg, J. C. (1961) On the tropomyosin-paramyosin system in relation to the viscous tone of lamellibranch ‘catch’ muscle.Proc. R. Soc. Lond. B154, 224–49.Google Scholar
  33. Rüegg, J. C. (1971) Smooth Muscl Tone.Physiol. Rev. 51, 201–48.Google Scholar
  34. Sobieszek, A. (1973) The fine structure of the contractile apparatus of theanterior byssus retractor muscle ofMytilus edulis.J. Ulstrastruct. Res. 43, 313–43.Google Scholar
  35. Svendsen, K. H. (1982) Ultrastructure of a molluscan smooth muscle during phasic contractions and in the relaxed state.Int. J. Biol. Macromol 4, 43–9.Google Scholar
  36. Szent-Györgyi, A. G., Cohen, C. &Kendrick-Jones, J. (1971) Paramyosin and the filaments of molluscan ‘catch’ muscles II. Native filaments: Isolation and characterization.J. molec Biol. 56, 239–58.Google Scholar
  37. Twarog, B. M., Muneoka, Y. &Ledgere, M. (1977) Serotonin and dopamine as neurotransmitters inMytilus: block of serotonin receptors by an organic mercurialJ. Pharmac. exp. Therapeut. 201, 350–6.Google Scholar
  38. Ward, R. &Murray, J. M. (1987) Natural propane cryogen for frozen-hydrated biological specimens.J. Electron Micros. Tech. 5, 275–8.Google Scholar

Copyright information

© Chapman and Hall Ltd. 1989

Authors and Affiliations

  • Pauline M. Bennett
    • 1
  • Arthur Elliott
    • 1
  1. 1.MRC Cell Biophysics Unit and Department of Biophysics, Cell and Molecular BiologyKing's College LondonLondonUK

Personalised recommendations