Skip to main content
Log in

Fibre types inLimulus telson muscles: morphology and histochemistry

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

Summary

Using a variety of techniques, we have demonstrated the presence of at least two fibre types inLimulus median telson levator muscle. By light and electron microscopy, large (21 56 μm2 mean cross-sectional area) fibres have A-bands of 4.1 μm, one-half I bands of 2.15 μm and Z lines ⩽ 0.5 μm in width. Few mitochondria are found in these fibres, which comprise 54% of those present in a given microscope field and which occupy 82% of the total cross-sectional area. Small fibres (484 μm2 mean cross-sectional area) have A bands of 6.3 μm, one-half I bands of 3.1 μm and Z lines between 0.5 and 1.0 μm in width and are rich in mitochondria. Although small fibres comprise nearly one-half (46%) of the fibres in a field, they occupy only 18% of the total cross-sectional area.

Histochemical staining for alkaline-stable myofibrillar ATPase activity and mitochondrial reduced β-nicotinamide adenine nucleotide (β-NADH) tetrazolium reductase activity confirms the presence of two fibre types. The large fibres react positively for the myofibrillar ATPase activity and negatively for the mitochondrial enzyme activity. The reverse is seen with the small fibres. Some fibres of intermediate size, having intermediate staining characteristics, were also observed. Native gel electrophoresis of both myofibrillar and purified myosin preparations supports the observed differences in myofibrillar ATPase activity in that two myosin isozymes are resolved on pyrophosphate gels. Although the thick filaments isolated from unstimulated small fibres are longer (>6.0 μm) than those isolated from unstimulated large fibres (4.26 μm), all have a similar appearance with respect to the arrangement of myosin heads on their surfaces, and similar diameters. The implications of the observed heterogeneity of fibre types is discussed with reference to previously reported phenomena inLimulus telson muscle, including changes in length of thick filaments on fibre stimulation and the shape of the length-tension curve obtained from fibre bundles.

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

  • Brooke, M. H. &Kaiser, K. K. (1969) Some comments on the histochemical characterization of muscle adenosine triphosphatase.J. Histochem. Cytochem. 17, 431–2.

    PubMed  Google Scholar 

  • Crowther, R. A., Padron, R. &Craig, R. (1985) Arrangement of the heads of myosin in relaxed thick filaments from tarantula muscleJ. molec. Biol. 184, 429–39.

    PubMed  Google Scholar 

  • Davidheiser, S. &Davies, R. E. (1982) Energy utilization ofLimulus telson muscle at different sarcomere and A-band lengths.Am. J. Physiol. 242, R394-R400.

    PubMed  Google Scholar 

  • Davidheiser, S., Levine, R. J. C. &Davies, R. E. (1982) Two different fibre types inLimulus muscle.Fedn Proc. Am. Soc. exp. Biol. 41, 1522 (abstract).

    Google Scholar 

  • De Villafranca, G. W. (1961) The A- and I-band lengths in stretched or contracted horseshoe crab skeletal muscle.J. Ultrastruct. Res. 5, 109–15.

    PubMed  Google Scholar 

  • De Villafranca, G. W. &Marschhaus, C. M. (1963) Contraction of the A-bandJ. Ultrastruct. Res. 9, 157–65.

    Google Scholar 

  • Dewey, M. M., Levine, R. J. C. &Colflesh, D. E. (1973) Structure ofLimulus striated muscle. The contractile apparatus at various sarcomere lengths.J. Cell. Biol. 58, 574–93.

    PubMed  Google Scholar 

  • Dewey, M. M., Walcott, B., Colflesh, D. E., Terry, H. &Levine, R. J. C. (1977) Changes in thick filament length inLimulus striated muscle.J. Cell. Biol. 75, 366–80.

    PubMed  Google Scholar 

  • Eisenberg, B. (1983) Quantitative ultrastructure of mammalian skeletal muscle. In:Handbook of Physiology (edited byPeachey, L. D.), pp. 73–112. Bethesda: Am, Physiol. Soc.

    Google Scholar 

  • Franzini-Armstrong, C. (1970) Natural variability in the length of thin and thick filaments in single fibres from a crab,Portunus depurator.J. Cell Sci. 6, 559–92.

    PubMed  Google Scholar 

  • Hoh, J. F., McGrath, P. A. &White, R. I. (1976) Electrophoretic analysis of multiple forms of myosin in fast-twitch and slow-twitch muscles of the chick.Biochem. J. 157, 87–95.

    PubMed  Google Scholar 

  • Kensler, R. W. &Levine, R. J. C. (1982a) An electron microscopic and optical diffraction analysis of the structure ofLimulus thick filaments.J. Cell Biol. 92, 443–51.

    PubMed  Google Scholar 

  • Kensler, R. W. &Levine, R. J. C. (1982b) Determination of the hand of the crossbridge helix ofLimulus thick filaments.J. Mus. Res. Cell. Motil. 3, 349–61.

    Google Scholar 

  • Kensler, R. W., Levine, R. J. C. &Stewart, M. (1985) Electron microscopic and optical diffraction analysis of the structure of scorpion muscle thick filaments.J. Cell. Biol. 101, 395–401.

    PubMed  Google Scholar 

  • Kensler, R. W. &Stewart, M. (1986) An ultrastructural study of crossbridge arrangement in the frog thigh muscle thick filament.Biophys. J. 49, 343–51.

    PubMed  Google Scholar 

  • Lehman, W., Kendrick-Jones, J. &Szent-Gyorgyi, A. G. (1973) Myosin-linked regulatory systems: comparative studies.Cold Spring Harb. Symp. Quant. Biol. 37, 319–30.

    Google Scholar 

  • Levine, R. J. C. (1986) Effects of myosin light chain phosphorylation onLimulus thick filaments.J. Cell. Biol. 103, 118a (abstr).

    Google Scholar 

  • Levine, R. J. C., Davidheiser, S., Kensler, R. W., Kelly, A. M. &Davies, R. E. (1986) Fiber types inLimulus muscle.Biophys. J. 49, 259a (abstr).

    Google Scholar 

  • Levine, R. J. C., Dewey, M. M. &De Villafranca, G. W. (1972) Immunohistochemical localization of contractile proteins inLimulus striated muscle.J. Cell Biol. 55, 221–36.

    PubMed  Google Scholar 

  • Levine, R. J. C. &Kensler, R. W. (1985) Structure of short thick filaments fromLimulus muscle.J. molec. Biol. 182, 347–52.

    PubMed  Google Scholar 

  • Levine, R. J. C., Kensler, R. W., Reedy, M. C., Hofmann, W. &King, H. A. (1983) Structure and paramyosin content of tarantula thick filaments.J. Cell Biol. 97, 186–95.

    PubMed  Google Scholar 

  • Levine, R. J. C. &Woodhead, J. L. (1987) Structural effects ofLimulus myosin light chain phosphorylation.Biophys. J. 51, 324a (abstr).

    Google Scholar 

  • Maruyama, K., Sawada, H., Kimura, S., Ohashi, K., Higuchi, H. &Umazume, Y. (1984) Connectin filaments in stretched skinned fibres of frog skeletal muscle,J. Cell. Biol. 99, 1391–7.

    PubMed  Google Scholar 

  • Mcneil, P. A. &Hoyle, G. (1967) Evidence for superthin filaments.Am. Zool. 7, 483–98.

    Google Scholar 

  • Ogonowski, M. M. &Lang, F. (1979) Histochemical evidence for enzyme differences in crustacean fast and slow muscle.J. exp. Zool. 207, 143–54.

    Google Scholar 

  • Padykula, H. A. &Herman, E. (1955) The specificity of the histochemical method for adenosine triphosphatase.J. Histochem. Cytochem. 3, 170–83.

    PubMed  Google Scholar 

  • Rudel, R. &Zite-Ferenczy, F. (1979) Interpretation of light diffraction by cross-striated muscle as a Bragg reflexion of light by the lattice of contractile proteins.J. Physiol., Lond. 290, 317–30.

    Google Scholar 

  • Sellers, J. R. (1981) Phosphorylation-dependent regulation ofLimulus myosin.J. biol. Chem. 256, 9274–8.

    PubMed  Google Scholar 

  • Stewart, M., Kensler, R. W. &Levine, R. J. C. (1981) Structure ofLimulus telson muscle thick filaments.J. molec. Biol. 153, 781–90.

    PubMed  Google Scholar 

  • Stewart, M., Kensler, R. W. &Levine, R. J. C. (1985) Three-dimensional reconstruction of thick filaments fromLimulus and scorpion muscle.J. Cell Biol. 101, 402–11.

    PubMed  Google Scholar 

  • Trinick, J., Knight, P. &Whiting, A. (1984) Purification and properties of native titin.J. molec. Biol. 180, 331–56.

    PubMed  Google Scholar 

  • Walcott, B. &Dewey, M. M. (1980) Length-tension relation inLimulus striated muscle.J. Cell Biol. 87, 204–8.

    PubMed  Google Scholar 

  • Wang, K. &Ramirez-Mitchell, R. (1983) A network of transverse and longitudinal intermediate filaments is associated with sarcomeres of adult vetebrate skeletal muscle.J. Cell Biol. 96, 562–70.

    PubMed  Google Scholar 

  • Wang, K. &Williamson, C. L. (1980) Identification of an N2 line protein of striated muscle.Proc. Natn. Acad. Sci. U.S.A. 77, 3254–8.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Levine, R.J.C., Davidheiser, S., Kelly, A.M. et al. Fibre types inLimulus telson muscles: morphology and histochemistry. J Muscle Res Cell Motil 10, 53–66 (1989). https://doi.org/10.1007/BF01739856

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01739856

Keywords

Navigation