Skip to main content
Log in

Location of paramyosin in relation to the subfilaments within the thick filaments of scallop striated muscle

  • Papers
  • Published:
Journal of Muscle Research & Cell Motility Aims and scope Submit manuscript

Summary

Myosin co-assembles with paramyosin in the thick filaments of invertebrate muscles. The molar ratio of the two proteins varies greatly but where sufficient paramyosin is present it forms the filament core with myosin arranged on its surface. In the fastest acting striated muscles, paramyosin is present in small amounts, and neither its location nor the nature of its interactions with myosin has previously been established. Antibodies to paramyosin have now been used in an attempt to locate the protein in thick filaments that have been isolated from the striated adductor muscle of the scallop and then frayed apart into their constituent subfilaments. Using a gold-conjugated secondary antibody, the location of paramyosin in relation to the subfilaments has been determined by electron microscopy of negatively stained samples. The labelling indicates that paramyosin extends throughout the length of the scallop filaments and appears to be associated with each subfilament, raising the possibility that in these filaments paramyosin may not be confined to a central core domain.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Atkinson, S. J. &Stewart, M. (1991) Molecular basis of myosin assembly: coiled-coil interactions and the role of charge periodicities.J. Cell Sci. 14 (Suppl.), 7–10.

    Google Scholar 

  • Beinbrech, G., Meller, U. &Sasse, W. (1985). Paramyosin content and thick filament structure in insect muscles.Cell and Tissue Res. 241, 607–14.

    Google Scholar 

  • Bullard, B., Luke, B. &Winkelman, L. (1973) The paramyosin of insect flight muscle.J. Mol. Biol. 75, 359–67.

    Google Scholar 

  • Bullard, B., Hammond, K. S. &Luke, B. M. (1977) The site of paramyosin in insect flight muscle and the presence of an unidentified protein between myosin filaments and Z-line.J. Mol. Biol. 115, 417–40.

    Google Scholar 

  • Castellani, L. &Cohen, C. (1987) Rod phosphorylation favours folding in a catch muscle myosin.Proc. Nail. Acad. Sci. USA 84, 4058–62.

    Google Scholar 

  • Castellani, L., Vibert, P. &Cohen, C. (1983) Structure of myosin/paramyosin filaments from a molluscan smooth muscle.J. Mol. Biol. 167, 853–72.

    Google Scholar 

  • Cohen, C. (1982) Matching molecules in the catch mechanism.Proc. Natl. Acad. Sci. USA 79, 3176–89.

    Google Scholar 

  • Cohen, C. &Holmes, K. C. (1963) X-ray diffraction evidence for α-helical coiled coils in native muscle.J. Mol. Biol. 6, 423–32.

    Google Scholar 

  • Cohen, C. &Castellani, L. (1988) New perspectives on catch.Comp. Biochem. Physiol. 91C, 31–3.

    Google Scholar 

  • Cohen, C., Szent-Györgyi, A. G. &Kendrick Jones, J. (1971) Paramyosin and the filaments of molluscan ‘catch’ muscles. I. Paramyosin structure and assembly.J. Mol. Biol. 56, 223–37.

    Google Scholar 

  • Cohen, C., Lanar, D. E. &Parry, D. A. D. (1987) Amino acid sequence and structural repeats in schistosome paramyosin match those of myosin.Biosci. Rep. 7, 11–16.

    Google Scholar 

  • Collins, J. H. &Kork E. D. (1980) Actin activation of Ca2+-sensitive Mg2+-ATPase activity ofAcanthamoeba myosin II is enhanced by dephosphorylation of its heavy chains.J. Biol. Chem. 255, 8011–14.

    Google Scholar 

  • 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 

  • Craig, R., Padrón, R. &Alamo, L. (1991) Direct determination of myosin filament symmetry by rapid freezing and freeze-substitution electron microscopy.J. Mol. Biol. 220, 125–32.

    Google Scholar 

  • Davis, J. S. (1988) Assembly processes in vertebrate skeletal thick filament formation.Ann. Rev. Biophys. Chem. 17, 217–39.

    Google Scholar 

  • Elliott, A. &Bennett, P. M. (1984) Molecular organization of paramyosin in the core of molluscan thick filaments.J. Mol. Biol. 176, 477–93.

    Google Scholar 

  • Epstein, H. F. (1988) Modulation of myosin assembly.BioEssays 9, 197–200.

    Google Scholar 

  • Epstein, H. F., Miller, D. M., Ortiz, I. &Berliner, G. C. (1985) Myosin and paramyosin are organized about a newly identified core structure.J. Cell Biol. 100, 904–15.

    Google Scholar 

  • Epstein, H. F., Ortiz, I. &Berliner, G. C., (1987) Assemblages of multiple thick filaments in nematode mutants.J. Muscle Res. Cell Motil. 8, 527–36.

    Google Scholar 

  • Epstein, H. F., Berliner, G. C., Casey, D. L. &Ortiz, I. (1988) Purified thick filaments from the nematodeCaenorhabditis elegans; evidence for multiple proteins associated with core structures.J. Cell Biol. 106, 1985–95.

    Google Scholar 

  • Gengyo-Ando, K. &Kagawa, H. (1991) Single charge change on the helical surface of the paramyosin rod dramatically disrupts thick filament assembly inCaenorhabditis elegans.J. Mol. Biol. 219, 429–41.

    Google Scholar 

  • Hanson, J. &Lowy.J. (1961) The structure of the muscle fibres in the translucent part of the adductor of the oysterCrassostrea angulata.Proc. Roy. Soc. Series B. 154, 173–96.

    Google Scholar 

  • Hardwicke, P. M. D. &Hanson, J. (1971) Separation of thick and thin myofilaments.J. Mol. Biol. 59, 509–16.

    Google Scholar 

  • Kagawa, H., Gengyo, K., McLachlan, A. D., Brenner, S. &Karn, J. (1989) Paramyosin gene (unc-15) ofCaenorhabditis elegans. Molecular cloning, nucleotide sequence and models for thick filament structure.J. Mol. Biol. 207, 311–33.

    Google Scholar 

  • Kiehart, D. P. &Pollard, T. D. (1984) Stimulation ofAcanthamoeba actomyosin ATPase activity by myosin-II polymerization.Nature 308, 864–6.

    Google Scholar 

  • Levine, R. J. C., Elfvin, M., Dewey, M. M., &Walcott, B. (1976) Paramyosin in invertebrate muscles. II. Content in relation to structure and function.J. Cell Biol. 71, 273–9.

    Google Scholar 

  • Levine, R. J. C., Kensler, R. W., Stewart, M. &Haselgrove, J. C. (1982) Molecular organization ofLimulus thick filaments. InBasic Biology of Muscles: a Comparative Approach (edited by Twarog, B. M., Levine, R. J. C. & Dewey, M. M.) pp. 37–52. New York: Raven Press.

    Google Scholar 

  • Levine, R. J. C., Kensler, R. W. &Levitt, P. (1986) Crossbridge and backbone structure of invertebrate thick filaments.Biophys. J. 49, 135–8.

    Google Scholar 

  • Levine, R. J. C., Chantler, P. D. &Kensler, R. W. (1988) Arrangement of myosin heads onLimulus thick filaments.J. Cell Biol. 107, 1739–47.

    Google Scholar 

  • Lowey, S., Kucera, J. &Holtzer, A. M. (1963) On the structure of the paramyosin molecule.J. Mol. Biol. 7, 234–44.

    Google Scholar 

  • Mackenzie, J. M. Jr. &Epstein, H. F. (1980) Paramyosin is necessary for determination of nematode thick filament length.Cell 22, 747–55.

    Google Scholar 

  • Miller, D. M., Ortiz, I., Berliner, G. C. &Epstein, H. F. (1983) Differential localization of two myosins within nematode thick filaments.Cell 34, 477–90.

    Google Scholar 

  • Millman, B. M. &Bennett, P. M. (1976) Structure of the cross-striated adductor muscle of the scallop.J. Mol. Biol. 103, 439–67.

    Google Scholar 

  • Nonomura, Y. (1974) Fine structure of the thick filament in molluscan catch muscle.J. Mol. Biol. 88, 445–55.

    Google Scholar 

  • Nunzi, M. G. &Franzini-Armstrong, C. (1981) The structure of smooth and striated portions of the adductor muscles of the valves in a scallop.J. Ultrastruct. Res. 76, 134–48.

    Google Scholar 

  • Nyitray, L., Mocz, G., Szilagyi, L., Balint, M., Lu, R. C., Wong, A. &Gergely, J. (1983) The proteolytic substructure of light meromyosin: localization of a region responsible for the low ionic strength insolubility of myosin.J. Biol. Chem. 258, 13213–20.

    Google Scholar 

  • Pepe, F. A., Ashton, F. T., Street, C. &Weisel, J. (1986) The myosin filament. X. Observation of nine subfilaments in transverse sections.Tissue Cell 18, 499–508.

    Google Scholar 

  • Sinard, J. H., Rimm, D. L. &Pollard, T. D. (1990) Identification of functional regions on one tail ofAcanthamoeba myoxin-II using recombinant fusion proteins. II. Assembly properties of tails with NH2- and COOHterminal deletions.J. Cell Biol. 111, 2417–26.

    Google Scholar 

  • Sohn, R. &Leinward, R. (1990) Sequence requirements for myosin filament assembly.J. Cell. Biochem. 14A, 14 (Abstract).

    Google Scholar 

  • Squire, J. M. (1981)The Structural Basis of Muscular Contraction. pp. 698. New York: Plenum Press.

    Google Scholar 

  • 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. Mol. Biol. 56, 239–58.

    Google Scholar 

  • Vibert, P. J. &Craig, R. W. (1983) Electron microscopy and image analysis of myosin filaments from scallop striated muscle.J. Mol. Biol. 165, 303–20.

    Google Scholar 

  • Vibert, P. &Craig. R. (1985) Structural changes that occur in scallop myosin filaments upon activation.J. Cell Biol. 101, 830–7.

    Google Scholar 

  • Vibert, P. &Castellani, L. (1989) Substructure and Accessory proteins in scallop myosin filaments.J. Cell Biol. 109, 539–47.

    Google Scholar 

  • Wallimann, T. &Szent-Györgyi, A. G. (1981) An immunological approach to myosin light-chain function in thick filament linked regulation. 1. Characterization, specificity and cross-reactivity of anti-scallop myosin heavy- and light-chain antibodies by competitive, solid-phase radioimmunoassay.Biochemistry 20, 1176–87.

    Google Scholar 

  • Waterston, R. H., Epstein, H. F. &Brenner, S. (1974) Paramyosin ofCaenorhabditis elegans.J. Mol. Biol. 90, 285–90.

    Google Scholar 

  • Wray, J. S. (1979) Structure of the backbone in myosin filaments of muscle.Nature (Lond.) 277, 37–40.

    Google Scholar 

  • Wray, J. S., Vibert, P. J. &Cohen, C. (1975) Diversity of crossbridge configurations in invertebrate muscles.Nature 257, 561–4.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Castellani, L., Vibert, P. Location of paramyosin in relation to the subfilaments within the thick filaments of scallop striated muscle. J Muscle Res Cell Motil 13, 174–182 (1992). https://doi.org/10.1007/BF01874154

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01874154

Keywords

Navigation