Skip to main content
Log in

The movement of muscle precursor cells between adjacent regenerating muscles in the mouse

  • Original Articles
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Summary

Regeneration of mature skeletal muscle fibers involves the formation of new multinucleate muscle fibres by the fusion together of mononucleate muscle precursor cells. Such precursor cells appear to be largely or entirely derived from satellite cells, located between the basement membrane and the sarcolemma of the muscle fibre. We have previously presented evidence that precursor cells which contribute to regenerating muscle in a region of muscle damage are not all locally derived but that some migrate in from exogenous sources. The present study examines the possibility that a regenerating muscle might receive muscle precursor cells from neighbouring muscles. To do this we have made whole muscle allografts in the mouse and used the two murine isoenzyme allotypes of the dimeric enzyme Glucose-6-Phosphate Isomerase (GPI) as markers to demonstrate whether there is movement of muscle precursor cells between these allografts and adjacent host muscles. In host muscles adjacent to some allografts, a “hybrid” form of GPI was detected, each molecule consiting of one donor and one host GPI subunit. Such heterodimers can form only where host and donor nuclei share a common cytoplasm: in muscles this means that mosaic host/donor muscle fibres are present. The presence of such fibres implies that muscle precursor cells must have migrated into the host muscle from the neighbouring allograft.

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

  • Abercrombie M (1977) Concepts in morphogenesis. Proc R Soc B 199:337–344

    Google Scholar 

  • Bateson RG, Woodrow DF, Sloper JC (1967) Circulating cell as a source of myoblasts in regenerating injured mammalian skeletal muscle. Nature 213:1035–1036

    Google Scholar 

  • Billingham RE, Brent L, Medawar PB (1956) Quantitative studies on tissue transplantation immunity. III: Actively acquired tolerance. Phil Trans R Soc Lond (Series B Biological Sciences) 239:357–424

    Google Scholar 

  • Carlson BM (1973) The regeneration of skeletal muscle—a review. Am J Anat 137:119–150

    Google Scholar 

  • Carlson BM (1976) A quantitative study of muscle fibre survival and regeneration in normal, predenervated and marcaine treated free muscle grafts in the rat. Exp neurol 52:421–432

    Google Scholar 

  • Carlson BM, Gutmann E (1975) Regeneration in free grafts of normal and denervated muscles of the rat. Anat Rec (Abstract) 175:284

    Google Scholar 

  • Carter ND, Parr CW (1967) Isoenzymes of phosphoglucose isomerase in mice. Nature 216:511

    Google Scholar 

  • Curtis ASG (1960) Area and volume measurements by random sampling. Med Biol Illust 10:261–266

    Google Scholar 

  • Elson J (1929) Auto- and homoio transplantation of cross-striated muscle tissue in the rat. Am J Pathol 5:425–438

    Google Scholar 

  • Faulkner JA, Maxwell LC, Mufti SA, Carlson BM (1976) Skeletal muscle fibre regeneration following heterotopic autotransplantation in cats. Life Sci 19:289–296

    Google Scholar 

  • Gearhart JD, Mintz B (1972) Clonal origin of somites and their muscle derivatives — Evidence from allophenic mice. Dev Biol 29:27–37

    Google Scholar 

  • Ghins E, Colson-van Schloor M, Maréchal G (1984) The origin of muscle stem cells in rat triceps surae regenerating after mincing. J Muscle Res Cell Motil 5:711–722

    Google Scholar 

  • Grounds MD (1984) Skeletal muscle precursors do not arise from bone marrow cells. Cell Tissue Res 234:713–722

    Google Scholar 

  • Grounds MD, McGeachie JK (1986) 3H-thymidine reutilization at high (170 μCi) an low (25 μCi) dosage, in studies of regenerating skeletal muscle. Cell Tissue Res (in press)

  • Grounds MD, Partridge TA, Sloper JC (1980) The contribution of exogenous cells to regenerating skeletal muscle allografts in mice. J Pathol 132:325–341

    Google Scholar 

  • Grounds MD, Partridge TA (1983) Isoenzyme studies of whole muscle grafts and movements of muscle precursor cells. Cell Tissue Res 230:677–688

    Google Scholar 

  • Hall-Craggs ECB (1974) Rapid degeneration and regeneration of a whole skeletal muscle following treatment with bupivacaine (marcain). Exp Neurol 43:349–358

    Google Scholar 

  • Hansen-Smith FM, Carlson BM (1979) Cellular responses to free grafting of the extensor digitorum longus muscle of the rat. J neurol Sci 41:149–173

    Google Scholar 

  • Hsu L, Trupin GL, Roisen FJ (1979) The role of satellite cells and myonuclei during myogenesis in vitro. In: Mauro A (ed) Muscle Regeneration. Raven, New York, pp 115–120

    Google Scholar 

  • Jacob M, Christ B, Jacob HL (1978) On the migration of myogenic stem cells into the prospective wing region of chick embryos. A scanning and transmission electron microscope study. Anat Embryol 153:179–193

    Google Scholar 

  • Jockusch J (1982) Muscle transplantation in mammals: a tool to study neuromuscular mutations and specificity of innervation. In: Jaenicke L (ed) Biochemistry of differentiation and morphogenesis. Springer-Verlag, Berlin, pp 195–198

    Google Scholar 

  • Klein-Ogus K, Harris JB (1983) Preliminary observations of satellite cells in the undamaged fibres of the rat soleus muscle assaulted by a snakevenom toxin. Cell Tissue Res 230:671–676

    Google Scholar 

  • Konigsberg IR (1979) Regeneration of single muscle fibres in culture and in vivo. In: Mauro A (ed) Muscle regeneration. Raven, New York, pp 41–56

    Google Scholar 

  • Lipton BH, Schultz E (1979) Developmental fate of skeletal muscle satellite cells. Science 205:1292–1294

    Google Scholar 

  • Mauro A (1961) Satellite cells of skeletal muscle fibres. J Biophys Biochem Cytol 9:493–495

    Google Scholar 

  • Moss FP, Leblonde CP (1971) Satellite cells as a source of nuclei in muscles of growing rats. Anat Rec 170:421–436

    Google Scholar 

  • Partridge TA, Sloper JC (1977) A host contribution to the regeneration of muscle grafts. J Neurol Sci 33:425–435

    Google Scholar 

  • Partridge TA, Grounds M, Sloper JC (1978) Evidence of fusion between host and donor myoblasts in skeletal muscle grafts. Nature 273:306–308

    Google Scholar 

  • Partridge T, Morgan J, Coulton G (1986) Repopulation of dead muscles by live muscle precursor cells. Muscle Nerve [Suppl] 9, Abstract No. 31.7, 171

    Google Scholar 

  • Schultz E, Jaryszak DL, Gibson MC, Albright DJ (1986) Contribution of exogenous myogenic cells to regeneration of frozen skeletal muscle. Muscle Nerve [Suppl] 9, Abstract No 31.8, 171

    Google Scholar 

  • Snow MH (1978) An autoradiographic study of satellite cell differentiation into regenerating myotubes following transplantation of muscles in young rats. Cell Tissue Res 180:535–540

    Google Scholar 

  • Studitsky AN (1964) Free auto and homografts of mucle tissue in experimental animals. Ann NY Acad Sci 120:789–801

    Google Scholar 

  • Turner DC, Carbonetto ST (1984) Model systems for studying the functions of extracellular matrix molecules in muscle development. Exp Biol Med 9:72–79

    Google Scholar 

  • Watt DJ (1982) Factors which affect fusion of allogeneic muscle precursor cells in vivo. Neuropathol Appl Neurobiol 8:135–147

    Google Scholar 

  • Venkatasubramanian K, Solursh M (1984) Chemotactic behaviour of myoblasts. Dev Biol 104:428–433

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Watt, D.J., Morgan, J.E., Clifford, M.A. et al. The movement of muscle precursor cells between adjacent regenerating muscles in the mouse. Anat Embryol 175, 527–536 (1987). https://doi.org/10.1007/BF00309688

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00309688

Key words

Navigation