Skip to main content
Log in

Skeletal muscle regeneration induced by chorio-allantoic grafting

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

Abstract

To examine whether the expression pattern of fast-muscle type troponin-T (TnT) isoforms was fixed in cell lineage, breast muscle pieces (pectoralis major) from chick embryos and young and adult chickens were grafted on to chorio-allantoic membrane of 9-day-old chick embryos and cultured until the host embryos hatched out. Muscle fibre formation of the grafts was investigated by histological and immunohistochemical methods with anti-fast-muscle type and anti-slow-muscle type TnT sera, and the expression of fast-muscle type TnT in the grafts from chick embryos and young chickens was studied by SDS-polyacrylamide gel electrophoresis (SDS-PAGE), two-dimensional SDS-PAGE, and immunoblotting. In the chorio-allantoic grafting, the breast muscle initially degenerated forming pyknotic nuclei and hyaline cytoplasm. The surviving cells, which were supposed to be satellite cells, regenerated new muscle fibres of the same type as those of the grafted muscle in respect of TnT isoform expression. Therefore, we considered that the ability to express specific isoforms of TnT was fixed in the satellite cells, and that chorio-allantoic grafting was a useful technique for studying muscle differentiation.

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

  • ALLBROOK, D. (1981) Skeletal muscle regeneration. Muscle & Nerve4, 234–45.

    Article  CAS  Google Scholar 

  • ANDREW, A. & RAWDON, B. B. (1987) The embryonic origin of connective tissue mast cells. J. Anat.150, 219–27.

    PubMed  CAS  Google Scholar 

  • ARMAND, O. & KIENY, M. (1984) Ontogeny of the myo-satellite cell. Arch. Anat. Microsc.73, 75–90.

    Google Scholar 

  • BENOIT, P. W. & BELT, W. D. (1970) Destruction and regeneration of skeletal muscle after treatment with a local anaesthetic, bupivacaine (Marcaine). J. Anat.107, 547–56.

    PubMed  CAS  Google Scholar 

  • BODINE-FOWLER, S. (1994) Skeletal muscle regeneration after injury: an overview. J. Voice.8, 53–62.

    Article  PubMed  CAS  Google Scholar 

  • BONNER, P. H. (1975) Clonal analysis of vertebrate myogenesis. V. Nerve-muscle interaction in chick limb bud chorio-allantoic membrane grafts. Dev. Biol. 47, 222–7.

    Article  PubMed  CAS  Google Scholar 

  • BRADLEY, S. J. (1970) An analysis of self-differentiation of chick limb buds in chorio-allantoic grafts. J. Anat.107, 479–90.

    PubMed  CAS  Google Scholar 

  • CAMPION, D. R. (1984) The muscle satellite cell: a review. Int. Rev. Cytol.87, 225–51.

    PubMed  CAS  Google Scholar 

  • CARLSON, B. M. (1973) The regeneration of skeletal muscle. A review. Am. J. Anat. 137, 119–50.

    Article  PubMed  CAS  Google Scholar 

  • CARLSON, B. M. & GUTMANN, E. (1975) Regeneration in free grafts of normal and denervated muscles in the rat: morphology and histochemistry. Anat. Rec.183, 47–62.

    Article  PubMed  CAS  Google Scholar 

  • EBASHI, S., WAKABAYASHI, T. & EBASHI, F. (1971) Troponin and its components. J. Biochem.69, 441–5.

    PubMed  CAS  Google Scholar 

  • FELDMAN, J. L. & STOCKDALE, F. E. (1991) Skeletal muscle satellite cell diversity: satellite cells from fibers of different types in cell culture. Dev. Biol.143, 320–34.

    Article  PubMed  CAS  Google Scholar 

  • FRANKE, W. W., HEID, H. W., GROUND, C., WINTER, S., FREUDENSTEIN, C., SCHMID, E., JARASCH, E. & KEENAN, T. W. (1981) Antibodies to the major insoluble milk fat globule membrane-associated protein: specific location in apical regions of lactating epithelial cells. J. Cell Biol.89, 485–94.

    Article  PubMed  CAS  Google Scholar 

  • HALL-CRAGGS, E. C. B. (1974) Rapid degeneration and regeneration of a whole skeletal muscle following treatment with bupivacaine (Marcain). Exp. Neurol.43, 349–58.

    Article  PubMed  CAS  Google Scholar 

  • HARTLEY, R. S., BANDMAN, E. & YABLONKA-REUVENI, Z. (1992) Skeletal muscle satellite cells appear during late chicken embryogenesis. Dev. Biol.153, 206–16.

    Article  PubMed  CAS  Google Scholar 

  • HIRABAYASHI, T. (1981) Two-dimensional gel electrophoresis of chicken skeletal muscle proteins with agarose gels in the first dimension. Anal. Biochem.117, 443–51.

    Article  PubMed  CAS  Google Scholar 

  • HUNT, E. A. (1932) The differentiation of chick limb buds in chorio-allantoic grafts, with special reference to the muscles. J. Exp. Zool.62, 57–91.

    Article  Google Scholar 

  • LAEMMLI, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227, 680–85.

    Article  PubMed  CAS  Google Scholar 

  • MASTAGLIA, F. L., PAPADIMITRIOU, J. M. & KAKULAS, B. A. (1970) Regeneration of muscle in Duchenne muscular dystrophy: an electron microscope study. J. Neurol. Sci.11, 425–44.

    Article  PubMed  CAS  Google Scholar 

  • MAURO, A. (1961) Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol.9, 493–5.

    Article  PubMed  CAS  Google Scholar 

  • MAURO, A. (1979) Muscle Regeneration. New York: Raven.

    Google Scholar 

  • MIKAWA, T., TAKEDA, S., SHIMIZU, T. & KITAURA, T. (1981) Gene expression of myofibrillar proteins in single muscle fibers of adult chicken: micro two-dimensional gel electrophoretic analysis. J. Biochem.89, 1951–62.

    PubMed  CAS  Google Scholar 

  • NAKAMURA, M., IMAI, H. & HIRABAYASHI, T. (1989) Coordinate accumulation of troponin subunits in chicken breast muscle. Dev. Biol.132, 389–97.

    Article  PubMed  CAS  Google Scholar 

  • NEWGREEN, D. F., JAHNKE, I., ALLAN, I. J. & GIBBINS, I.L. (1980) Differentiation of sympathetic and enteric neurons of the fowl embryo in grafts to the chorio-allantoic membrane. Cell Tissue Res.208, 1–19.

    Article  PubMed  CAS  Google Scholar 

  • NIJWEIDE, P. J., VAN IPEREN-VAN GENT, A. S., KAWILARANG-DE HAAS, E. W. M., VAN DER PLAS, A. & WASSENAAR, A. M. (1982) Bone formation and calcification by isolated osteoblastlike cells. J. Cell Biol.93, 318–23.

    Article  PubMed  CAS  Google Scholar 

  • PERRY, S. V. & COLE, H. A. (1974) Phosphorylation of troponin and the effects of interactions between the components of the complex. Biochem. J.141, 733–43.

    PubMed  CAS  Google Scholar 

  • RISAU, W., HALLMANN, R., ALBRECHT, U. & HENKEFAHLE, S. (1986) Brain induces the expression of an early cell surface marker for blood-brain barrier-specific endothelium. EMBO J.5, 3179–83.

    PubMed  CAS  Google Scholar 

  • SCHULTZ, E. (1976) Fine structure of satellite cells in growing skeletal muscle. Am. J. Anat.147, 49–70.

    Article  PubMed  CAS  Google Scholar 

  • SCHULTZ, E. & MCCORMICK, K. M. (1994) Skeletal muscle satellite cells. Rev. Physiol. Biochem. Pharmacol.123, 213–57.

    Article  PubMed  CAS  Google Scholar 

  • SNOW, M. H. (1977) Myogenic cell formation in regenerating rat skeletal muscle injured by mincing. I. A fine structural study. Anat. Rec.188, 181–200.

    Article  PubMed  CAS  Google Scholar 

  • STEWART, M. E. & TEREPKA A. R. (1969) Transport functions of the chick chorio-allantoic membrane. I. Normal histology and evidence for active electrolyte transport from the allantoic fluid, in vivo. Exp. Cell Res.58, 93–106.

    Article  CAS  Google Scholar 

  • TOWBIN, H., STAEHELIN, T. & GORDON, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl Acad. Sci. USA76, 4350–54.

    Article  PubMed  CAS  Google Scholar 

  • WILLIER, B. H. & RAWLES, M. E. (1931) The relation of Hensen's node to the differentiating capacity of whole chick blastoderms as studied in chorio-allantoic grafts. J. Exp. Zool.59, 429–65.

    Article  Google Scholar 

  • WILKINSON, J. M. (1978) The components of troponin from chicken fast skeletal muscle. Biochem. J.169, 229–38.

    PubMed  CAS  Google Scholar 

  • WILKINSON, J. M. & GRAND, R. J. A. (1978) Comparison of amino acid sequence of troponin I from different striated muscle. Nature271, 31–5.

    Article  PubMed  CAS  Google Scholar 

  • YAO, Y., MIYAZAKI, J-I. & HIRABAYASHI, T. (1994) Coexistence of fast-muscle-type and slow-muscle-type troponin T isoforms in single chimeric muscle fibers induced by muscle transplantation. Exp. Cell Res.214, 400–407.

    Article  PubMed  CAS  Google Scholar 

  • YAO, Y., NAKAMURA, M., MIYAZAKI, J-I., KIRINOKI, M. & HIRABAYASHI, T. (1992) Expression pattern of skeletal muscle troponin T isoforms is fixed in cell lineage. Dev. Biol.151, 531–40.

    Article  PubMed  CAS  Google Scholar 

Download references

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

NAKADA, K., YAO, Y., MASHIMA, J. et al. Skeletal muscle regeneration induced by chorio-allantoic grafting. J Muscle Res Cell Motil 19, 169–177 (1998). https://doi.org/10.1023/A:1005312729381

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1005312729381

Keywords

Navigation