Skip to main content
Log in

Myogenic and neurogenic regulation of myosin gene expression in cat jaw-closing muscles regenerating in fast and slow limb muscle beds

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

Summary

Immunocytochemical techniques were used to study changes in myosin gene expression during the regeneration of the cat posterior temporalis muscle transplanted into the bed of either the fast extensor digitorum longus (EDL) or the slow soleus muscle. Strips of the posterior temporalis, a homogeneously superfast muscle, were treated with Marcaine and then transplanted into limb muscle beds which had been completely cleared of host muscle fibres. The regenerates were examined 6 to 224 days after surgery. Early regenerates in both muscle beds reacted with antibodies against the heavy chain of foetal, slow and superfast myosins, but not with antibodies against fast myosin. In the long-term, regenerates innervated by the EDL nerve expressed only superfast myosin whereas in the regenerates innervated by the soleus nerve most fibres expressed only slow myosin and only a few fibres reacted exclusively with the anti-superfast myosin antibody even after 210 days. In contrast, EDL and soleus muscles regenerating in their own beds expressed foetal, slow and fast myosin, but did not express superfast myosin. The isometric contraction times of the various types of regenerates reflected the types of myosin synthesized. It is concluded that jaw and limb muscle cells exist as two distinct allotypes, each having a distinct repertoire for the expression of adult isomyosins, and that within that repertoire isomyosin gene expression can be modulated by the nerve. Thus, myosin gene expression in skeletal muscle fibres is regulated by both myogenic and neurogenic mechanisms.

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

  • Bárány, M. (1967) ATPase activity of myosin correlated with speed of muscle shortening.J. Gen. Physiol. 50, 197–218.

    PubMed  Google Scholar 

  • Bárány, M. &Close, I. (1971) The transformation of myosin in cross-innervated rat muscles.J. Physiol. (Lond.) 213, 455–474.

    Google Scholar 

  • Bonner, P. H. &Hauschka, S. D. (1974) Clonal analysis of vertebrate myogenesis. I. Early developmental events in the chick limb.Devl. Biol. 37, 317–328.

    Google Scholar 

  • Bosley, M. &Rowlerson, A. (1980) A new myosin associated with the fast fibre type in the cat jaw-closer muscles?J. Physiol. (Lond.) 306, 18P.

    Google Scholar 

  • Buchthal. F. &Schmalbruch, H. (1980) Motor unit of mammalian muscle.Physiol. Revs. 60, 90–142.

    Google Scholar 

  • Buller, A. J., Eccles, J. C. &Eccles, R. M. (1960) Interactions between motoneurones and muscles in respect of the characteristic speeds of their responses. J.Physiol. (Lond.) 150, 417–439.

    Google Scholar 

  • Burden, S. J., Sargent, P. B. &Mcmahan, U. J. (1979) Acetylcholine receptors in regenerating muscle accumulate at original synaptic sites in the absence of the nerve.J. Cell. Biol. 82, 412–425.

    PubMed  Google Scholar 

  • Carlson, B. M. &Faulkner, J. A. (1983) The regeneration of skeletal muscle fibres following injury: a review.Med. Sci. Sports Exercise 15, 187–198.

    Google Scholar 

  • Close, R. (1969) Dynamic properties of fast and slow skeletal muscles of the rat after nerve cross-union.J. Physiol. (Lond.) 204, 331–346.

    Google Scholar 

  • Crow, M. T. &Stockdale, F. E. (1986) Myosin expression and specialization among the earliest muscle fibres of the developing avian limb.Devl. Biol. 113, 238–254.

    Google Scholar 

  • Fitzsimons, R. B. &Hoh, J. F. Y. (1981) Embryonic and foetal myosins in human skeletal muscle.J. Neurol. Sci. 52, 367–384.

    PubMed  Google Scholar 

  • Hansen-Smith, F. M. &Carlson, B. M. (1979) Cellular responses to free grafting of the extensor digitorum longus muscle of the rat.J. Neurol. Sci. 41, 149–173.

    PubMed  Google Scholar 

  • Hennig, R. &Lømo, T. (1985) Firing patterns of motor units in normal rats.Nature (Lond.) 314, 164–166.

    Google Scholar 

  • Hoh, J. F. Y. (1975) Neural regulation of mammalian fast and slow muscle myosins: an electrophoretic study.Biochemistry 14, 742–747.

    PubMed  Google Scholar 

  • Hoh, J. F. Y. &Hughes, S. (1986) Myosin gene expression in cat temporalis muscle regenerating in the absence of a nerve.Proc. Aust. Physiol. Pharm. Soc. 17, 142P.

    Google Scholar 

  • Hoh, J. F. Y., Hughes, S., Hale, P. T. &Fitzsimons, R. B. (1988a) Immunocytochemical and electrophoretic analyses of changes in myosin gene expression in cat limb fast and slow muscles during postnatal development.J. Musc. Res. Cell Motility 9, 30–47.

    Google Scholar 

  • Hoh, J. F. Y., Hughes, S., Chow, C., Hale, P. T. &Fitzsimons, R. B. (1988b) Immunocytochemical and electrophoretic analyses of changes in myosin gene expression in cat posterior temporalis muscle during postnatal development.J. Musc. Res. Cell Motility 9, 48–58.

    Google Scholar 

  • Hoh, J. F. Y., Kwan, B. T. S., Dunlop, C. &Kim, B. H. (1980) Effects of nerve cross-union and cordotomy on myosin isoenzymes in fast-twitch and slow-twitch muscles of the rat. InPlasticity of Muscle (edited byPette, D.), pp. 339–352. Berlin. New York: Walter de Gruyter & Co.

    Google Scholar 

  • Hughes, S. &Hoh, J. F. Y. (1985) Myotubes grown in tissue culture from juvenile cat jaw and limb muscles express a slow myosin epitope.Proc. Aust. Physiol. Pharm. Soc. 16, 260P.

    Google Scholar 

  • Jockusch, H., Fuchtbauer, E-M., Fuchtbauer, A., Leger, J. J., Maldonado, C. A. &Forssmann, W-G. (1986) Long-term expression of isomyosins and myoendocrine functions in ectopic grafts of atrial tissue.Proc. Nat. Acad. Sci. (Wash.) 83, 7325–7329.

    Google Scholar 

  • Jolesz, F. &Sréter, F. A. (1981) Development, innervation, and activity-pattern induced changes in skeletal muscle.Ann. Rev. Physiol. 43, 531–552.

    Google Scholar 

  • Lømo, T., Westgaard, R. H. &Dahl, H. A. (1974) Contractile properties of muscle: control by pattern of muscle activity in the rat.Proc. R. Soc. Lond. Ser. B 187, 99–103.

    Google Scholar 

  • Lubetzki-Korn, I., Ovadia, H., Vlodavsky, I., Fuks, Z. &Abramsky, O. (1983) Enhanced growth and morphological differentiation of isolated adult rat oligodendrocytesin vitro: use of a naturally produced extracellular matrix.Brain Res. 267, 151–155.

    PubMed  Google Scholar 

  • Maréchal, G., Schwartz, K., Beckers-Bleukx, G. &Ghins, E. (1984) Isozymes of myosin in growing and regenerating rat muscles.Eur. J. Biochem. 138, 421–428.

    PubMed  Google Scholar 

  • Miller, J. B. &Stockdale, F. E. (1986) Developmental origins of skeletal muscle fibres: clonal analysis of myogenic cell lineages based on expression of fast and slow myosin heavy chains.Proc. Nat. Acad. Sci. (Wash.) 83, 3860–3864.

    Google Scholar 

  • Pette, D. &Vrbová, G. (1985) Invited review: neural control of phenotypic expression in mammalian muscle fibres.Muscle Nerve 8, 676–689.

    PubMed  Google Scholar 

  • Pierobon-Bormioli, S., Sartore, S., Dalla Libera, L., Vitadello, M. &Schiaffino, S. (1981) “Fast” isomyosins and fibre types in mammalian skeletal muscle.J. Histochem. Cytochem. 29, 1179–1188.

    PubMed  Google Scholar 

  • Rowlerson, A., Mascarello, F., Veggetti, A. &Carpene, E. (1983) The fibre-type composition of the first branchial arch muscles in Carnivora and Primates.J. Musc. Res. Cell Motility 4, 443–472.

    Google Scholar 

  • Rowlerson, A., Pope, B., Murray, J., Whalen, R. B. &Weeds, A. G.(1981) A novel myosin present in cat jaw-closing muscles.J. Musc. Res. Cell Motility 2, 415–438.

    Google Scholar 

  • Rutz, R. &Hauschka, S. (1982) Clonal anlysis of vertebrate myogenesis. VII. Heritability of muscle colony type through sequential subclonal passages in vitro.Devl. Biol. 91, 103–110.

    Google Scholar 

  • Salmons, S. &Sréter, F. A. (1976) Significance of impulse activity in the transformation of skeletal muscle type.Nature (Lond.) 263, 30–34.

    Google Scholar 

  • Sanes, J. R. (1983) Roles of extracellular matrix in neural development.Ann. Rev. Physiol. 45, 581–600.

    Google Scholar 

  • Sanes, J. R., Marshall, L. M. &Mcmahan, U. J. (1978) Reinnervation of muscle fibre basal lamina after removal of myofibres.J. Cell Biol. 78, 176–198.

    PubMed  Google Scholar 

  • Sartore, S., Gorza, L. &Schiaffino, S. (1982) Foetal myosin heavy chains in regenerating muscle.Nature (Lond.) 298, 294–296.

    Google Scholar 

  • Taylor, A., Cody, F. W. Y. &Bosley, M. A. (1973) Histochemical and mechanical properties of the jaw muscles of the cat.Expl. Neurol. 38, 99–109.

    Google Scholar 

  • Vlodavsky, I., Levi, A., Lax, I., Fuks, Z. &Schlessinger, J. (1982) Induction of cell attachment and morphological differentiation in a phaeochromocytoma cell line and embryonal sensory cells by the extracellular matrix.Devl. Biol. 93, 285–300.

    Google Scholar 

  • White, N. K., Bonner, P. H., Nelson, D. R. &Hauschka, S. D. (1975) Clonal analysis of vertebrate myogenesis. IV. Medium-dependent classification of colony-forming cells.Devl. Biol. 44, 346–361.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hoy, J.F.Y., Hughes, S. Myogenic and neurogenic regulation of myosin gene expression in cat jaw-closing muscles regenerating in fast and slow limb muscle beds. J Muscle Res Cell Motil 9, 59–72 (1988). https://doi.org/10.1007/BF01682148

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01682148

Keywords

Navigation