Skip to main content
SpringerLink
Log in

Calcium and strontium activation characteristics of skeletal muscle fibres from the small marsupialSminthopsis macroura

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

Summary

Mechanically skinned skeletal muscle fibres from the soleus and tibialis anterior muscles of the small marsupialSminthopsis macroura were activated by Ca2+ and Sr2+ so that their isometric force properties could be determined. The properties characterized were the shape, slope and positions of the curves generated by plotting isometric force vs. pCa (−log10[Ca2+]) and pSr (−log10[Sr2+]), the maximum Ca2+-activated and Sr2+-activated tension (Ncm−2) and the frequency of force oscillations of myofibrillar origin during submaximal activations. The effect of caffeine on force activation was also studied. Apart from the fibres which exhibited physiological characteristics similar to those observed previously in mammalian fibres, a large proportion of fibres exhibited characteristics or combinations of characteristics which have not previously been described from healthy adult mammals. The results from 32 soleus fibres showed that only 23 could be categorized as either typical fast-twitch or slow-twitch fibres. The rest possessed unusual physiological characteristics which suggested the co-existence in the same fibre of Ca2+-regulatory and contractile properties from different categories of fast-twitch and slow-twitch fibres. We could distinguish two major fast twitch populations of tibialis anterior fibres which occurred in similar proportions. There were significant differences in the maximum tension produced by some of these groups of fibres. The tibialis anterior population fibres produced the highest maximum tension (T Cao 44.6±4.6 Ncm−2, n=7) while the soleus combined type fibres produced the lowest maximum tension (T Cao 18.1±2.1 Ncm−2, n=8). Our physiological observations of the Ca2+-activation and Sr2+-activation properties of soleus fibres in this study provide new evidence that there can be combinations of characteristics in single fibres and a continuum of properties between fibre types in normal mammalian skeletal muscles. These animals can therefore be used as a source of fibres with a wide range of properties.

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

  • Ashley, C. C. &Moisescu, D. G. (1977) The effect of changing the composition of the bathing solutions upon the isometric tension-pCa relationship in bundles of crustacean myofibrils.J. Physiol. 270, 627–52.

    PubMed  Google Scholar 

  • Billeter, R., Weber, H., Lutz, H., Howald, H., Eppenberger, H. M. &Jenny, E. (1980) Myosin types in human skeletal muscle fibers.Histochem. 65, 249–59.

    Google Scholar 

  • Brandt, P. W., Diamond, M. S., Rutchik, J. S. &Schachat, F. H. (1987) Co-operative interactions between troponin-tropomyosin units extend the length of the thin filament in skeletal muscle.J. Molec. Biol. 195, 885–96.

    Google Scholar 

  • Brandt, P. W., Diamond, M. S. &Schachat, F. H. (1984) The thin filament of vertebrate skeletal muscle co-operatively activates as a unit.J. Molec. Biol. 180, 379–84.

    PubMed  Google Scholar 

  • Bridge, D. T. &Allbrook, D. (1970) Growth of striated muscle in an Australian marsupial (Setonix brachyurus).J. Anat. 106, 285–95.

    PubMed  Google Scholar 

  • Brooke, M. H. &Kaiser, K. K. (1970) Muscle fiber types: how many and what kind?Arch. Neurol. 23, 369–79.

    PubMed  Google Scholar 

  • Close, R. I. (1972) Dynamic properties of mammalian skeletal muscles.Physiol. Revs. 52,129–97.

    Google Scholar 

  • Close, R. I. (1974) Specialization among fast-twitch muscles. InExploratory concepts in muscular dystrophy II, edited byMilhorat, A. T., pp. 309–18. Amsterdam: Excerpta Medica.

    Google Scholar 

  • Fink, R. H. A., Stephenson, D. G. &Williams, D. A. (1986a) Potassium and ionic strength effects on the isometric force of skinned twitch muscle fibres of the rat and toad.J. Physiol. 370, 317–37.

    PubMed  Google Scholar 

  • Fink, R. H. A., Stephenson, D. G. &Williams, D. A. (1986b) Calcium and strontium activation of single skinned muscle fibres of normal and dystrophic mice.J. Physiol. 373, 513–25.

    PubMed  Google Scholar 

  • Fitzsimons, R. B. &Hoh, J. F. Y. (1983). Myosin Isoenzymes in fast-twitch and slow-twitch muscles of normal and dystrophic mice.J. Physiol. 343, 539–50.

    PubMed  Google Scholar 

  • Goldspink, G. (1980) Growth of muscle. InDevelopment and specialization of skeletal muscle, edited byGoldspink, D. F., pp. 19–35. Cambridge: Cambridge University Press.

    Google Scholar 

  • Gundersen, K., Leberer, E., Lomo, T., Pette, D. &Staron, R. S. (1988) Fibre types, calcium sequestering proteins and metabolic enzymes in denervated and chronically stimulated muscles of the rat.J. Physiol. 398, 177–89.

    PubMed  Google Scholar 

  • Hill, J. C. &Hill, W. C. O. (1955) The growth stages of the pouch young of the native cat (Daryurus viverrinus) together with observations of the anatomy of the new-born young.Trans. Zool. Soc. London 28, 349–452.

    Google Scholar 

  • Hoar, P. E., Potter, J. D. &Kerrick, D. L. (1988). Skinned ventricular fibres: troponin C extraction is species-dependent and its replacement with skeletal troponin C changes Sr2+ activation properties.J. Muscle Res. Cell Motil. 9, 165–73.

    PubMed  Google Scholar 

  • Jolesz, F. &Sreter, F. A. (1981) Development, innervation, and activity-pattern induced changes in skeletal muscle.Ann. Revs. Physiol. 43, 531–52.

    Google Scholar 

  • Joubert, D. M. (1955) Growth of muscle fibre in the foetal sheep.Nature 175, 936–37.

    PubMed  Google Scholar 

  • Julian, F. J. (1971) The effect of calcium on the force-velocity relation of briefly glycerinated frog muscle fibres.J. Physiol. 218, 117–45.

    PubMed  Google Scholar 

  • Julian, F. J., Rome, L. C., Stephenson, D. G. &Striz, S. (1986) The maximum speed of shortening in living and skinned frog muscle fibres.J. Physiol. 370, 181–99.

    PubMed  Google Scholar 

  • Kerrick, W. G. L., Hoar, P. E., Malencik, D. A., Stamps, L. &Fischer, E. H. (1979) Characterization of Ca2+- and Sr2+-activated tension in functionally skinned chicken fibers of normal and dystrophic skeletal and normal cardiac muscle.Pflugers Arch. 381, 53–62.

    PubMed  Google Scholar 

  • Kerrick, W. G. L., Malencik, D. A., Hoar, P. E., Potter, J. D., Coby, R. L., Pocinwong, S. &Fischer, E. H. (1980). Ca2+ and Sr2+ activation: comparison of cardiac and skeletal muscle contraction models.Pflugers Arch. 386, 207–13.

    PubMed  Google Scholar 

  • Kerrick, W. G. L., Secrist, D., Coby, R. &Lucas, S. (1976) Development of difference between red and white muscles in sensitivity to Ca2+ in the rabbit from embryo to adult.Nature 260, 440–41.

    PubMed  Google Scholar 

  • Kerrick, W. G. L., Zot, H. G., Hoar, P. E. &Potter, J. D. (1985) Evidence that the Sr2+-activation properties of cardiac troponin C are altered when substituted into skinned skeletal muscle fibres.J. Biol. Chem. 260, 15687–93.

    PubMed  Google Scholar 

  • Lannergren, J. &Westerblad, H. (1987) The temperature dependence of isometric contractions of single, intact fibres dissected from a mouse foot muscle.J. Physiol. 390, 285–93.

    PubMed  Google Scholar 

  • Lewis, O. J. (1962) The phylogeny of the crural and pedal flexor musculature.Proc. Zool. Soc. London 138, 77–109.

    Google Scholar 

  • Luff, A. R. (1981) Dynamic properties of the inferior rectus, extensor digitorum longus, diaphragm and soleus muscles of the mouse.J. Physiol. 313, 161–71.

    PubMed  Google Scholar 

  • Miller, D. J. &Smith, G. L. (1984) EGTA purity and the buffering of Ca ions in physiological solutions.Am. J. Physiol. 246, C160–6.

    PubMed  Google Scholar 

  • Mizusawa, H., Takagi, A., Sugita, H. &Toyokura, Y. (1982). Coexistence of fast and slow types of myosin light chains in a single fibre of rat soleus muscle.J. Biochem. 91, 423–5.

    PubMed  Google Scholar 

  • Moisescu, D. G. (1976) Kinetics of reaction in Ca-activated skinned muscle fibres.Nature 262, 610–3.

    PubMed  Google Scholar 

  • Moisescu, D. G. &Thieleczek, R. (1978) Calcium and strontium concentration changes within skinned muscle preparations following a change in the external bathing solution.J. Physiol. 275, 241–62.

    PubMed  Google Scholar 

  • Moisescu, D. G. &Thieleczek, R. (1979) Sarcomere length effects on the Sr2+ and Ca2+ activation curves in skinned frog muscle fibres.Biochim. Biophys. Acta 546, 64–76.

    PubMed  Google Scholar 

  • Moore, G. E. &Schachat, F. H. (1985) Molecular heterogeneity of histochemical fibre types: a comparison of fast fibres.J. Muscle Res. Cell Motil. 6, 513–24.

    PubMed  Google Scholar 

  • Morton, S. R. (1983) Stripe-faced dunnart. InThe complete book of Australian mammals, edited byStrahan, R., pp. 63–4. Sydney: Angus & Robertson.

    Google Scholar 

  • Moss, R. L., Giulian, G. G. &Greaser, M. L. (1985) The effects of partial extraction of TnC upon the tension-pCa relationship in rabbit skinned skeletal muscle fibers.J. gen. Physiol. 86, 585–600.

    PubMed  Google Scholar 

  • Moss, R. L., Lauer, M. R., Giulian, G. G. &Greaser, M. L. (1986) Altered Ca2+-dependence of tension development in skinned skeletal muscle fibers following modification of troponin by partial substitution with cardiac troponin C.J. Biol. Chem. 261, 6096–99.

    PubMed  Google Scholar 

  • Reiser, P. J., Moss, R. L., Guilian, G. G. &Greaser, M. L. (1985a) Shortening velocity in single fibers from adult rabbit soleus is correlated with myosin heavy chain composition.J. Biol. Chem. 260, 9077–80.

    PubMed  Google Scholar 

  • Reiser, P. J., Moss, R. L., Giulian, G. G. &Greaser, M. L. (1985b). Shortening velocity and myosin heavy chains of developing rabbit muscle fibers.J. Biol. Chem. 260, 14403–05.

    PubMed  Google Scholar 

  • Schachat, F. H., Diamond, M. S. &Brandt, P. W. (1987) Effect of different troponin T-tropomyosin combinations on thin filament activation.J. Molec. Biol. 198, 551–4.

    Google Scholar 

  • Schantz, P. G. (1986) Plasticity of human skeletal muscle.Acta Physiol. Scand. Supplementum 558.

  • Staron, R. S., Hikida, R. S. &Hagerman, F. C. (1983) Reevaluation of human muscle fast-twitch subtypes: evidence for a continuum.Histochem. 78, 33–9.

    Google Scholar 

  • Staron, R. S. &Pette, D. (1987a). The multiplicity of combinations of myosin light chains and heavy chains in histochemically typed single fibres: rabbit soleus muscle.Biochem. J. 243, 687–93.

    PubMed  Google Scholar 

  • Staron, R. S. &Pette, D. (1987b) The multiplicity of combinations of myosin light chains and heavy chains in histochemically typed single fibres: rabbit tibialis anterior muscle.Biochem. J. 243, 695–9.

    PubMed  Google Scholar 

  • Staron, R. S. &Pette, D. (1987c). Nonuniform myosin expression along single fibers of chronically stimulated and contralateral rabbit tibialis anterior muscles.Pflugers Arch. 409, 67–73.

    PubMed  Google Scholar 

  • Stephenson, D. G. &Forrest, Q. G. (1980) Different isometric force-[Ca2+] relationships in slow and fast twitch skinned muscle fibres of the rat.Biochim. Biophys. Acta 589, 358–62.

    PubMed  Google Scholar 

  • Stephenson, D. G., Stewart, A. W. &Wilson, G. J. (1989) Dissociation of force from myofibrillar MgATPase and stiffness at short sarcomere lengths in rat and toad skeletal muscle.J. Physiol. 410, 351–66.

    PubMed  Google Scholar 

  • Stephenson, D. G. &Williams, D. A. (1981) Calcium-activated force responses in fast- and slow-twitch skinned muscle fibres of the rat at different temperatures.J. Physiol. 317, 281–302.

    PubMed  Google Scholar 

  • Stephenson, D. G. &Williams, D. A. (1982) Effects of sarcomere length on the force-pCa relation in fast- and slow-twitch skinned muscle fibres from the rat.J. Physiol. 333, 637–53.

    PubMed  Google Scholar 

  • Takagi, A. (1981) Single muscle fibres of Duchenne Muscular Dystrophy (DMD): sensitivity to strontium and composition of contractile protein.Clin. Neurol. 21, 1088–91.

    Google Scholar 

  • Takagi, A. &Endo, M. (1977) Guinea pig soleus and extensor digitorum longus: a study on single-skinned fibers.Exp. Neurol. 55, 95–101.

    PubMed  Google Scholar 

  • Takagi, A., Ishiura, S., Nonaka, I. &Sugita, H. (1982) Myosin light chain components in single muscle fibres of Duchenne muscular dystrophy.Muscle and Nerve 5, 399–404.

    PubMed  Google Scholar 

  • Takagi, A., Yonemoto, K. &Sugita, H. (1978) Single-skinned human muscle fibres: activation by calcium and strontium.Neurol. 28, 497–9.

    Google Scholar 

  • Vrbova, G. (1980) Innervation and differentiation of muscle fibres. InDevelopment and specialization of skeletal muscle, edited byGoldspink, D. F., pp. 37–50. Cambridge: Cambridge University Press.

    Google Scholar 

  • Wendt, I. R. &Stephenson, D. G. (1983) Effects of caffeine on Ca-activated force production in skinned cardiac and skeletal muscle fibres of the rat.Pflugers Arch. 398, 210–16.

    PubMed  Google Scholar 

  • Wilson, G. J. &Stephenson, D. G. (1987) Ca++- and Sr++-activation of force in skinned skeletal muscle fibres ofSminthopsis macroura reveals the existence of single fibres with fast-twitch, intermediate, slow-twitch and combined regulatory characteristics.Proc. Aust. Physiol. Pharmacol. Soc. 18, 47P.

    Google Scholar 

  • Windle, B. C. &Parsons, F. G. (1903) On the muscles of the Ungulata — Part II.Proc. Zool. Soc. London 1903, 261–98.

    Google Scholar 

Download references

Author information

Author notes

  1. G. J. Wilson

    Present address: Cardiovascular Research Institute and Department of Biochemistry and Biophysics, University of California, 94143-0524, San Fransisco, CA., USA

Authors and Affiliations

  1. Department of Zoology, La Trobe University, Bundoora, 3083, Melbourne, Victoria, Australia

    G. J. Wilson & D. G. Stephenson

Authors
  1. G. J. Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. G. Stephenson
    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

Wilson, G.J., Stephenson, D.G. Calcium and strontium activation characteristics of skeletal muscle fibres from the small marsupialSminthopsis macroura . J Muscle Res Cell Motil 11, 12–24 (1990). https://doi.org/10.1007/BF01833322

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01833322

Keywords

Search

Navigation