Skip to main content
SpringerLink
Log in

Comparative histochemistry of a flatfish fin muscle and of other vertebrate muscles used for ultrastructural studies

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

Summary

Because of the high degree of filament order in the myofibrils of fish skeletal muscles, and the resulting usefulness of such preparations (particularly flatfish fin muscles) in structural studies of muscular contraction, the fibre type composition of plaice fin muscle has been determined by conventional histochemical tests. As controls, and for comparison, fibre type distributions have also been studied in several other vertebrate skeletal muscles which are widely used for ultrastructural and mechanical studies. In view of the importance of single fibres in such studies and because much of the published information on fibre types is rather difficult to collate, we summarize here the fibre compositions of several muscles; comparable enzyme tests have been carried out on cryostat sections of rabbit psoas muscle, frog sartorius and semitendinosus muscles and plaice fin muscles. On this basis all four muscles are composed of more than one fibre type. We confirm that frog sartorius muscle is mainly a random mixture of two fast fibre types and show that there is also a third group of fibres which are small, metabolically rich and dark under acid m-ATPase tests. We confirm that the semitendinosus is composed of three fibre types, in three non-exclusive, concentric regions and that rabbit psoas muscle contains a mixture of at least three fibre types.

The principal new findings of this work are that plaice fin muscle can be divided into four regions, some of which are composed of more than one fibre type, on the basis of its histochemical reactions. This division into regions changes seasonally. The system of classification devised by Dubowitz & Brooke (1973) for mammalian muscle, and which can be applied approximately to frog muscle, can also be applied to the fibres of plaice fin muscle provided that the test for lactate dehydrogenase is carried out in the presence of polyvinyl alcohol. These fibres do not easily fit the division into red, white and intermediate types normally used for fish myotomal muscles.

Since none of these muscles is homogeneous, their complex nature must be borne in mind if they are to be used satisfactorily in structural and mechanical studies of muscular contraction involving the use of single fibres.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Arnold, G. P. (1969) The reactions of the plaice (Pleuronectes platessa L.) to water currents.J. exp. Biol. 51, 681–97.

    Google Scholar 

  • Bauer, H. P., Reichmann, H. &Hofer, H. W. (1986) Perfusion of the psoas muscle of the rabbit. Metabolism of a homogeneous muscle composed of “fast glycolytic” fibres.Int. J. Biochem. 18, 67–72.

    PubMed  Google Scholar 

  • Bone, Q., Johnston, I. A., Pulsford, A. &Ryan, K. P. (1986) Contractile properties and ultrastructure of three types of muscle fibre in the dogfish myotome.J. Musc. Res. Cell Motility 7, 47–56.

    Google Scholar 

  • Brenner, B. &Squire, J. M. (1987) Rapid stiffness of single skinned fish muscle fibres: no detectable crossbridge attachment at low ionic strength. (abstract).J. Musc. Res. Cell Motility 8, 66–7.

    Google Scholar 

  • Brenner, B. &Yu, L. C. (1985) Equatorial X-ray diffraction from single skinned rabbit psoas fibres at various degrees of activation. Changes in intensities and lattice spacing.Biophys. J. 48, 829–34.

    PubMed  Google Scholar 

  • Brumback, R. A. &Leech, R. W. (1984)Colour Atlas of Muscle Histochemistry. Littleton, Massachusetts: PSG Publishing Company.

    Google Scholar 

  • Cantino, M. &Squire, J. M. (1986) Resting myosin cross-bridge configuration in frog muscle thick filaments.J. Cell Biol. 102, 610–8.

    PubMed  Google Scholar 

  • Carpene, E., Veggetti, A. &Mascarello, F. (1982) Histochemical fibre types in the lateral muscle of fishes in fresh, brackish and salt water.J. Fish Biol. 20, 379–96.

    Google Scholar 

  • Chayen, N., Freundlich, A. &Squire, J. M. (1987) Histochemical fibre typing of plaice fin muscle (abstract).J. Musc. Res. Cell Motility 8, 84.

    Google Scholar 

  • Dahl, H. A. &Mellgren, S. I. (1970) The effect of polyvinyl alcohol and polyvinyl pyrrollidone on diffusion artefacts in lactate dehydrogenase histochemistry.Histochemie 24, 354–70.

    PubMed  Google Scholar 

  • Davison, W. (1983) The lateral musculature of the common bully,Gobiomorphus cotidianus, a freshwater fish from New Zealand.J. Fish Biol. 23, 143–51.

    Google Scholar 

  • Dubowitz, V. &Brooke, M. H. (1973)Muscle Biopsy: A Modern Approach. London: W. B. Saunders.

    Google Scholar 

  • Edman, A. C., Squire, J. M. &Sjostrom, M. (1987) Fine structure of the A-band in cryosections. Diversity of M-band structure in chicken breast muscle (submitted for publication).

  • Engel, W. K. &Irwin, A. L. (1967) A histochemical-physiological correlation of frog skeletal muscle fibres.Am. J. Physiol. 213 (2), 511–8.

    PubMed  Google Scholar 

  • Gill, H. S., Weatherley, A. H. &Bhesania, T. (1982) Histochemical characterization of myotomal muscle in the bluntnose minnow,Pimephales notatus Rafinesque.J. Fish Biol. 21, 205–14.

    Google Scholar 

  • Harford, J. J. (1984)Diffraction analysis of vertebrate muscle crossbridge arrangements. Ph.D. thesis, University of London.

  • Harford, J. J. &Squire, J. M. (1986) “Crystalline” myosin crossbridge array in relaxed bony fish muscle.Biophys. J. 50, 145–55.

    PubMed  Google Scholar 

  • Henderson, B., Loveridge, N. &Robertson, W. R. (1978) A quantitative study of the effects of different grades of polyvinyl alcohol on certain enzyme activities in unfixed tissue sections.Histochem. J. 10, 453–63.

    PubMed  Google Scholar 

  • Huxley, H. E. &Brown, W. (1967) The low-angle X-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor.J. molec. Biol. 30, 383–434.

    PubMed  Google Scholar 

  • 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. molec. Biol. 158, 637–84.

    PubMed  Google Scholar 

  • Johnston, I. A. (1981) Quantitative analysis of muscle breakdown during starvation in the marine flatfishPleuronectes platessa.Cell Tissue Res. 214, 369–86.

    PubMed  Google Scholar 

  • Johnston, I. A., Davison, W. &Goldspink, G. (1977) Energy metabolism in carp swimming muscles.J. comp. Physiol. 114, 203–16.

    Google Scholar 

  • Johnston, I. A., Patterson, S., Ward, P. &Goldspink, G. (1974) The histochemical demonstration of myofibrillar adenosine triphosphatase activity in fish muscle.Can. J. Zool. 52, 871–7.

    PubMed  Google Scholar 

  • Korneliussen, H., Dahl, H. A. &Paulsen, J. E. (1978) Histochemical definition of muscle fibre types in the trunk musculature of a teleost fish.Histochemistry 55, 1–16.

    PubMed  Google Scholar 

  • Kryvi, H. &Totland, G. K. (1978) Fibre types in locomotory muscles of the cartilaginous fishChimaera monstrosa.J. Fish Biol. 12, 257–65.

    Google Scholar 

  • Lannergren, J. &Hoh, J. F. Y. (1984) Myosin isoenzymes in single muscle fibres ofXenopus laevis: analysis of five different functional types.Proc. Roy. Soc. Lond. Ser. B. 222, 401–8.

    Google Scholar 

  • Lannergren, J., Lindblom, P. &Johansson, B. (1982) Contractile properties of two varieties of twitch muscle fibres inXenopus laevis.Acta physiol. scand. 114, 523–35.

    PubMed  Google Scholar 

  • Lannergren, J. &Smith, R. S. (1966) Types of muscle fibres in toad skeletal muscle.ibid. 68, 263–74.

    Google Scholar 

  • Luther, P. K. &Crowther, R. A. (1984) Three-dimensional reconstruction from tilted sections of fish muscle M-band.Nature 307, 566–8.

    PubMed  Google Scholar 

  • Luther, P. K. &Squire, J. M. (1980) Three-dimensional structure of the vertebrate muscle A-band. II. The myosin filament superlattice.J. molec. Biol. 141, 409–39.

    PubMed  Google Scholar 

  • Luther, P. K., Munro, P. M. G. &Squire, J. M. (1981) Three-dimensional structure of the vertebrate muscle A-band. III. M-region structure and myosin filament symmetry.J. molec. Biol. 151, 703–30.

    PubMed  Google Scholar 

  • Nemeth, P. &Pette, D. (1981) Succinate dehydrogenase activity in fibres classified by myosin ATPase in three hind limb muscles of rat.J. Physiol. 320, 73–80.

    PubMed  Google Scholar 

  • Pette, D. &Schnez, U. (1977) Myosin light chain patterns of individual fast and slow-twitch fibres of rabbit muscles.Histochemistry 54, 97–107.

    PubMed  Google Scholar 

  • Putnam, R. W. &Bennett, A. F. (1983) Histochemical, enzymatic, and contractile properties of skeletal muscles of three anuran amphibians.Am. J. Physiol. 244, R558–67.

    PubMed  Google Scholar 

  • Rowlerson, A. &Spurway, N. C. (1985) How many fibre types in amphibian limb muscles? A comparison ofRana andXenopus. J. Physiol. 358, 78P.

    Google Scholar 

  • Rowlerson, A., Scapolo, P. A., Mascarello, F., Carpene, E. &Veggetti, A. (1985) Comparative study of myosins present in the lateral muscle of some fish: species variations in myosin isoforms and their distribution in red, pink and white muscle.J. Musc. Res. Cell Motility 6, 601–40.

    Google Scholar 

  • Schoenberg, N. &Eisenberg, E. (1985) Muscle crossbridge kinetics in rigor and in the presence of ATP analogues.Biophys. J. 48, 863–71.

    PubMed  Google Scholar 

  • Skorobovichuk, N. F. &Chizhova, N. A. (1976) Distribution of three types of muscle fibres in skeletal muscles of the frogRana temporaria.J. Evol. Biochem. Physiol. 12, 133–9.

    Google Scholar 

  • Spamer, C. &Pette, D. (1977) Activity patterns of phosphofructokinase, glyceraldehydephosphate dehydrogenase, lactate dehydrogenase and malate dehydrogenase in microdissected fast and slow fibres from rabbit psoas and soleus muscle.Histochemistry 52, 201–16.

    PubMed  Google Scholar 

  • Spamer, C. &Pette, D. (1979) Activities of malate dehydrogenase, 3-hydroxyacyl-CoA dehydrogenase and fructose-1,6-diphosphatase with regard to metabolic subpopulations of fast- and slow-twitch fibres in rabbit muscles.Histochemistry 60, 9–19.

    PubMed  Google Scholar 

  • Spurway, N. C. (1984) Quantitative histochemistry of frog skeletal muscles.J. Physiol. 346, 62P.

    Google Scholar 

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

    Google Scholar 

  • Squire, J. M., Podolsky, R. J., Yu, L. C. &Brenner, B. (1987) Equatorial X-ray diffraction from resting skinned single fibres of fish muscle: little evidence for crossbridge attachment at low ionic strength. (abstract).J. Musc. Res. Cell Motility 8, 66.

    Google Scholar 

  • Walesby, N. J. &Johnston, I. A. (1980) Fibre types in the locomotory muscles of an antarctic teleost,Notothenia rossii.Cell Tissue Res. 208, 143–64.

    PubMed  Google Scholar 

  • Weeds, A. G., Hall, R. &Spurway, N. C. S. (1975) Characterization of myosin light chains from histochemically identified fibres of rabbit psoas muscle.FEBS Lett. 49, 320–4.

    PubMed  Google Scholar 

  • Wilson, M. G. A. &Woledge, R. C. (1985) Lack of correlation between twitch contraction time and velocity of unloaded shortening in fibres of frog anterior tibialis muscle.J. Physiol. 358, 81P.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biophysics Section, Blackett Laboratory, Imperial College, London SW7, UK

    Naomi Chayen, Alan Freundlich & John M. Squire

Authors
  1. Naomi Chayen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alan Freundlich
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John M. Squire
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chayen, N., Freundlich, A. & Squire, J.M. Comparative histochemistry of a flatfish fin muscle and of other vertebrate muscles used for ultrastructural studies. J Muscle Res Cell Motil 8, 358–371 (1987). https://doi.org/10.1007/BF01568892

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01568892

Keywords

Search

Navigation