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Isoenzyme studies of whole muscle grafts and movement of muscle precursor cells

Summary

Isoenzymes of glucose-6-phosphate isomerase (GPI: E.C. 5.3.1.9) were used as markers to determine the origin of cells which give rise to new muscle formed in allografts of whole intact muscle. GPI isoenzymes were also employed to see whether host precursor cells, which have been shown to contribute to muscle formation in grafts of minced muscle, can be derived from muscle lying adjacent to grafts.

Excellent muscle regeneration was found in allografts of extensor digitorum longus (EDL) muscle examined after 58 days: 12 of 16 grafts contained 80% or more new muscle. Isoenzyme analysis showed that most, and in 2 instances all, new muscle was derived from implanted donor cells; however, there was strong evidence that in 5 grafts some, or all, new muscle must have resulted from host cells moving into the graft. Although hybrid isoenzyme was not detected this was attributed to factors associated with host tolerance which appear to interfere with fusion between host and donor myoblasts.

Isografts of minced muscle were placed next to whole EDL muscle allografts to see if cells from allografts moved into adjacent regenerating tissue. Unfortunately, muscle regeneration in minced isografts was poor; only 3 contained 50% or more new muscle and most contained large amounts of fibrous connective tissue. Only a single isoenzyme band was detected in 11 isografts, but in five instances, the presence of a second band showed that cells from EDL allografts were also present. As no hybrid isoenzyme was detected, it is not known whether these cells which had moved into the regenerating minced grafts were muscle precursors, fibroblasts or some other cell types.

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References

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

  2. Billingham RE, Brent L (1959) Quantitative studies on tissue transplantation. IV. Induction of tolerance in newborn mice and studies on the phenomenon of runt disease. Phil Trans Roy Soc Lond B 242:439–477

  3. Bradley WG (1973) Discussion Myogenesis. In Kakulas BA (ed) Basic research in myology. Excerpta Medica, Amsterdam, p 451–453

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

  5. Carlson BM (1976) A quantitative study of muscle fibre survival and regeneration in normal predenervated and marcain-treated free muscle grafts in the rat. Exp Neurol 52:421–4132

  6. Castillo de Maruenda E, Franzini-Armstrong C (1978) Satellite and invasive cells in frog sartorius muscle. Tissue Cell 10:749–772

  7. Constantinides PG, Jones PA, Gevers W (1977) Functional striated muscle cells from non-myoblast precursors following 5-azacytidine treatment. Nature 267:364–366

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

  9. Darmon M, Serrero G, Rizzino A, Sato G (1981) Isolation of myoblastic fibroadipogenic, and fibroblastic clonal cell lines from a common precursor and study of their requirements for growth and differentiation. Exp Cell Res 132:313–327

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

  11. Freschi JE, Parfitt AG, Shain WG (1979) Electrophysiology and pharmacology of striated muscle fibres cultured from dissociated neonatal rat pineal glands. J Physiol 293:1–10

  12. Freund-Molbert E, Ketelsen UP (1973) The regeneration of human striated muscle cell. Beitr Pathol 148:35–54

  13. Gearhart JD, Mintz B (1979) Contact mediated myogenesis and increased acetylcholinesterase activity in primary cultures of mouse teratocarcinoma cells. Proc Natl Acad Sci (Wash) 71:1734–1738

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

  15. Gutmann E, Mares V, Stichova J (1976) Fate of 3H-thymidine labelled myogenic cells in regeneration of muscle isografts. Cell Tissue Res 167:117–123

  16. Hansen-Smith FM, Carlson BM (1979) Cellular responses to free grafting of extensor digitorum longus muscle of the rat. J Neurol Sci 41:149–73

  17. Konigsberg UR, Lipton BH, Konigsberg IR (1975) The regenerative response of single mature muscle fibres isolated in vitro. Dev Biol 45:260–275

  18. Lennon HA, Petersen S, Schubert D (1979) Neurectoderm markers retained in phenotypical skeletal muscle cells arising from a glial cell line. Nature 281:586–588

  19. Lipton BH (1977) A fine-structural analysis of normal and modulated cells in myogenic cultures. Dev Biol 60:26–47

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

  21. Mintz B, Illmensee K (1975) Normally genetically mosaic mice produced from malignant teratocarcinoma cells. Proc Natl Acad Sci (Wash) 72:3585–3589

  22. Mufti SA, Carlson BM, Maxwell LC, Faulkner JA (1977) The free autografting of entire limb muscles in the cat: Morphology. Anat Rec 188:417–430

  23. Neerunjun J (1975) Pathogenesis of murine muscular dystrophy: studies on skeletal muscle transplanted between normal and dystrophic mice. PhD Thesis, University of London

  24. Neerunjun J, Dubowitz V (1974) Isoenzyme studies in the identification of transplanted muscle in the mouse. Clin Sci Mol Med 46:555–558

  25. Partridge TA (1982) Cellular interactions in the development and maintenance of skeletal muscle. In: Bellairs R, Curtis A, Dunn G (eds) Cell Behav. Cambridge University Press, Great Britain p 555–581

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

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

  28. Reznik M, Betz EH (1967) Influence de l'irradiation locate prealable sur les capacities régénératrices du muscle strié squellettique. Pathol Eur 2:69–80

  29. Rolston JLL (1970) Further studies on the orthotopic transplantation of skeletal muscle. Texas Rep Biol Med 28:97–104

  30. Schiaffino S, Sjostrom M, Thornell LE, Nystrom B, Hackelius L (1975) The process of survival of denervated and freely autotransplanted skeletal muscle. Experientia 31:1328–1330

  31. Schultz E (1978) Changes in the satellite cells of growing muscle following denervation. Anat Rec 190:299–312

  32. Snow MH (1978) An autoradiographic study of satellite cell differentiation into regenerating myotubes following transplantation of muscles in young rats. Cell Tissue Res 186:535–540

  33. Toto PH, O'Malley JJ, Anguizola C, Hilgers C (1967) Histogenesis of myotubes in regenerating skeletal muscle. J Dent Res 46:331–336

  34. Trupin GL (1979) The identification of myogenic cells in regenerating skeletal muscle. Dev Biol 68:59–71

  35. Walker BE (1963) Skeletal muscle regeneration in young rats. Am J Anat 133:369–378

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

  37. Watt DJ, Partridge TA, Sloper JC (1981) Cyclosporin A as a means of preventing rejection of skeletal muscle allografts in mice. Transplantation 31:266–271

  38. Werkerle H, Paterson B, Ketelsen UP, Feldman M (1975) Striated muscle fibres differentiate in monolayer cultures of adult thymus reticulum. Nature 256:493–494

  39. Yarom R, Bebar AJ, Yanko L, Hall TA, Peters PH (1976) Gold tracer studies of muscle regeneration. J Neuropath Exp Neurol 35:445–457

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Correspondence to Dr. M. D. Grounds.

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Grounds, M.D., Partridge, T.A. Isoenzyme studies of whole muscle grafts and movement of muscle precursor cells. Cell Tissue Res. 230, 677–688 (1983). https://doi.org/10.1007/BF00216211

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Key words

  • Muscle
  • Grafts
  • Regeneration
  • Precursor cells
  • Isoenzymes