Skip to main content
Log in

The role of innervation in the establishment of the topographical distribution of primary myotube types during development

  • Published:
Journal of Neurocytology

Summary

Many avian muscles contain a characteristic topographical distribution of fibre types. In order to study the role of nerves in the establishment and distribution of these fibre types, monoclonal antibodies (McAb) to the heavy chain subunit of myosin (MHC) were produced. The anti-fast McAb (2B12) bound to adult fast MHC and cross-reacted with the embryonic isoform of MHC. The anti-slow McAb (3D1) bound specifically to the heavy chain of slow myosin 2. By indirect immunofluorescence, anti-fast (2B12) stained all myotubes in the anterior latissimus dorsi and triceps and biceps muscles at stage 37 (11 days embryonic), whilst anti-slow (3D1) staining was largely restricted to the future slow fibres of these muscles. Brachial levels of the neural tube were surgically removed at stage 12 (2 days embryonic) so that muscles developed aneurally. Muscles at aneural stage 37 were smaller than normal, but the distribution of myotube types was not altered; all myotubes present still stained with anti-fast antibody while anti-slow staining was restricted to the anterior latissimus dorsi and myotubes in the deep parts of the triceps brachii pars scapularis, triceps brachii par humeralis and biceps brachii muscles (the future slow fibres of normal muscles). The results suggest that despite an overall reduction in MHC in aneural muscles, specialized fast and slow primary myotubes arise independently of the nerve in appropriate regions of the muscle.

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

  • Bader, D., Masaki, T. &Fischman, D. A. (1982) Immunochemical analysis of myosin heavy chain during avian myogenesisin vivo andin vitro.Journal of Cell Biology 95, 763–70.

    Google Scholar 

  • Bandman, E. (1985) Continued expression of neonatal myosin heavy chain in adult dystrophic skeletal muscle.Science 227, 780–2.

    Google Scholar 

  • Bandman, E., Matsuda, R. &Strohman, R. C. (1982) Developmental appearance of myosin heavy and light chain isoformsin vivo andin vitro in chicken skeletal muscle.Developmental Biology 93, 508–18.

    Google Scholar 

  • Brown, W. E., Salmons, S. &Whalen, R. G. (1983) The sequential replacement of myosin subunit isoforms during muscle type transformation induced by long term electrical stimulation.Journal of Biological Chemistry 258, 14686–92.

    Google Scholar 

  • Burke, R. E. &Edgerton, V. R. (1975) Motor unit properties and selective involvement in movement. InExercise and Sport Science Reviews Vol. 3 (edited byKeogh, J. F. &Wilmore, J. H.), pp. 31–81. New York: Academic Press.

    Google Scholar 

  • Butler, J. &Cosmos, E. (1981) Differentiation of the avian latissimus dorsi primordium: analysis of fiber type expression using the myosin ATPase histochemical reaction.Journal of Experimental Zoology 218, 219–32.

    Google Scholar 

  • Butler, J., Cosmos, E. &Brierly, J. (1982) Differentiation of muscle fiber types in aneurogenic brachial muscles of the chick embryo.Journal of Experimental Zoology 224, 65–80.

    Google Scholar 

  • Dahl, D. &Bignami, A. (1977) Preparation of antisera to neurofilament protein from chicken brain and human sciatic nerve.Journal of Comparative Neurology 176, 645–58.

    Google Scholar 

  • Dhoot, G. K. (1985) Initiation of differentiation into skeletal muscle fiber types.Muscle and Nerve 8, 307–16.

    Google Scholar 

  • Everett, A. W., Clark, W. A., Chizzonite, R. A. &Zak, R. (1983) Change in synthesis rates of α- and β-myosin heavy chains in rabbit heart after treatment with thyroid hormone.Journal of Biological Chemistry 258, 2421–5.

    Google Scholar 

  • Gambke, B. &Rubinstein, N. A. (1984) A monoclonal antibody to the embryonic myosin heavy chain of rat skeletal muscle.Journal of Biological Chemistry 259, 12092–100.

    Google Scholar 

  • Gauthier, G. F. (1967) On the localization of sarcotubular ATPase activity in mammalian skeletal muscle.Histochemie 11, 97–111.

    Google Scholar 

  • Gauthier, G. F., Burke, R. E., Lowey, S. &Hobbs, A. W. (1983) Myosin isozymes in normal and cross-reinnervated cat skeletal muscle fibers.Journal of Cell Biology 97, 756–71.

    Google Scholar 

  • Gauthier, G. F., Lowey, S., Benfield, P. A. &Hobbs, A. W. (1982) Distribution and properties of myosin isozymes in developing avian and mammalian skeletal muscle fibers.Journal of Cell Biology 92, 471–84.

    Google Scholar 

  • Gauthier, G. F., Ono, R. D. &Hobbs, A. W. (1984) Curare-induced transformation of myosin pattern in developing skeletal muscle fibers.Developmental Biology 105, 144–54.

    Google Scholar 

  • Gordon, H. &Van Essen, D. C. (1985) Specific innervation of muscle fiber types in a developmentally polyinnervated muscle.Developmental Biology 111, 42–50.

    Google Scholar 

  • Guth, L. (1973) Fact or artifact in the histochemical procedure for myofibrillar ATPase.Experimental Neurology 41, 440–50.

    Google Scholar 

  • Hamburger, V. &Hamilton, H. L. (1951) A series of normal stages in the development of the chick embryo.Journal of Morphology 88, 49–92.

    Google Scholar 

  • Hoh, J. F. Y. (1975) Neural regulation of mammalian fast and slow muscle myosins: an electrophoretic analysis.Biochemistry 14, 742–7.

    Google Scholar 

  • Hoh, J. F. Y. (1978) Light chain distribution of chicken skeletal muscle myosin isoenzymes.FEBS Letters 90, 297–300.

    Google Scholar 

  • Hoh, J. F. Y. (1979) Developmental changes in chicken skeletal myosin isoenzymes.FEBS Letters 98, 267–70.

    Google Scholar 

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

    Google Scholar 

  • Hoh, J. F. Y. &Yeoh, G. P. S. (1979) Rabbit skeletal myosin isoenzymes from fetal, fast-twitch and slow-twitch muscles.Nature 280, 321–3.

    Google Scholar 

  • Kelly, A. M. &Rubinstein, N. A. (1980) Why are fetal muscles slow?Nature 288, 266–9.

    Google Scholar 

  • Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Nature 277, 680–5.

    Google Scholar 

  • Laing, N. G. &Lamb, A. H. (1983) The distribution of muscle fibre types in chick embryo wings transplanted to the pelvic region is normal.Journal of Embryology and Experimental Morphology 78, 67–82.

    Google Scholar 

  • Lowey, S., Benfield, P. A., Le Blanc, D. D. &Waller, G. S. (1983) Myosin isozymes in avian skeletal muscles. I. Sequential expression of myosin isozymes in developing chicken pectoralis muscles.Journal of Muscle Research and Cell Motility 4, 695–716.

    Google Scholar 

  • Lowey, S., Benfield, P. A., Le Blanc, D. D., Waller, G. S., Winkelmann, D. A. &Gauthier, G. F. (1982) Characterisation of myosins from embryonic and developing chicken pectoralis muscle. InMuscle Development: Molecular and Cellular Control (edited byPearson, M. L. &Epstein, H. F.), pp. 15–24. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory.

    Google Scholar 

  • Lowey, S., Benfield, P. A., Silberstein, L. &Lang, L. M. (1979) Distribution of light chains in fast skeletal myosin.Nature 282, 522–4.

    Google Scholar 

  • Lyons, G. E., Haselgrove, J., Kelly, A. M. &Rubinstein, N. A. (1983) Myosin transitions in developing fast and slow muscles of the rat hindlimb.Differentiation 25, 168–75.

    Google Scholar 

  • Masaki, T. &Yoshizaki, C. (1974) Differentiation of myosin in chick embryos.Journal of Biochemistry (Tokyo) 76, 123–31.

    Google Scholar 

  • Matsuda, R., Bandman, E. &Strohman, R. C. (1982) The two myosin isoenzymes of chicken anterior latissimus dorsi muscle contain different myosin heavy chains encoded by separate mRNAs.Differentiation 23, 36–42.

    Google Scholar 

  • Matsuda, R., Spector, D. H. &Strohman, R. C. (1983) Regenerating adult chicken skeletal muscle and satellite cell cultures express embryonic patterns of myosin and tropomyosin isoforms.Developmenatal Biology 100, 478–88.

    Google Scholar 

  • McLennan, I. S. (1983a) Differentiation of muscle fiber types in the chicken hindlimb.Developmental Biology 97, 222–8.

    Google Scholar 

  • McLennan, I. S. (1983b) The development of the pattern of innervation in chicken hindlimb muscles: evidence for specification of nerve-muscle connections.Developmental Biology 97, 229–38.

    Google Scholar 

  • McLennan, I. S. (1983c) Neural dependence and independence of myotube production in chicken hindlimb muscles.Developmental Biology 98, 287–94.

    Google Scholar 

  • Navarette, R. &Vrbova, G. (1983) Changes of activity pattern in slow and fast muscles during postnatal development.Developmental Brain Research 8, 11–19.

    Google Scholar 

  • Phillips, W. D. &Bennett, M. R. (1984) Differentiation of fiber types in wing muscles during embryonic development: effect of neural tube removal.Developmental Biology 106, 457–68.

    Google Scholar 

  • Phillips, W. D., Lai, K. &Bennett, M. R. (1985) Spatial distribution and size of acetylcholine receptor clusters determined by motor nerves in developing chick muscles.Journal of Neurocytology 14, 309–25.

    Google Scholar 

  • Rubinstein, N. A. &Kelly, A. M. (1981) Development of muscle fiber specialization in the rat hindlimb.Journal of Cell Biology 90, 128–44.

    Google Scholar 

  • Rubinstein, N. A., Mabuchi, K., Pepe, F., Salmons, S., Gergely, J. &Sreter, F. (1978) Use of type-specific antimyosins to demonstrate the transformation of individual fibers in chronically stimulated rabbit fast muscles.Journal of Cell Biology 79, 252–61.

    Google Scholar 

  • Rushbrook, J. I. &Stracker, A. (1979) Comparison of adult, embryonic, and dystrophic myosin heavy chains from chicken muscle by sodium dodecyl sulfate/polyacrylamide gel electrophoresis and peptide mapping.Proceedings of the National Academy of Sciences USA 76, 4331–4.

    Google Scholar 

  • Samaha, F. J. &Yunis, E. J. (1973) Quantitative and histochemical demonstration of a calcium activated mitochondrial ATPase in skeletal muscle.Experimental Neurology 41, 431–9.

    Google Scholar 

  • Sohal, G. S. &Holt, R. K. (1980) Role of innervation on the embryonic development of skeletal muscle.Cell and Tissue Research 210, 383–93.

    Google Scholar 

  • Sreter, F., Gergely, J., Salmons, S. &Romanul, F. (1973) Synthesis by fast muscle of myosin light chains characteristic of slow muscle in response to long term stimulation.Nature 241, 17–18.

    Google Scholar 

  • Thompson, W. J., Sutton, L. A. &Riley, D. A. (1984) Fibre type composition of single motor units during synapse elimination in neonatal rat soleus muscle.Nature 309, 709–11.

    Google Scholar 

  • Whalen, R. G., Schwartz, K., Bouveret, P., Sell, S. M. &Gros, F. (1979) Contractile protein isozymes in muscle development: identification of an embryonic form of myosin heavy chain.Proceedings of the National Academy of Sciences USA 76, 5197–201.

    Google Scholar 

  • Whalen, R. G., Sell, S. M., Butler-Browne, G., Schwartz, K., Bouveret, P. &Pinset-Harstrom, I. (1981) Three myosin heavy-chain isozymes appear sequentially in rat muscle development.Nature 292, 805–9.

    Google Scholar 

  • Winkelmann, D. A., Lowey, S. &Press, J. L. (1983) Monoclonal antibodies localize changes on myosin heavy chain isozymes during avian myogenesis.Cell 34, 295–306.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Phillips, W.D., Everett, A.W. & Bennett, M.R. The role of innervation in the establishment of the topographical distribution of primary myotube types during development. J Neurocytol 15, 397–405 (1986). https://doi.org/10.1007/BF01611441

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01611441

Keywords

Navigation