Summary
Rat soleus muscles were autografted from right to left legs, and regeneration following necrosis of all original myofibres was studied after 7 to 250 days. The best regenerates were from grafts replacing all calf muscles and sutured to the tendon stumps. After 30 days the size of such regenerates was equal to those from minced gastrocnemius muscles: the cross sectional area of muscle tissue was 30% (1.7 mm2) and the number of fibres was 180% (4500) of normal soleus muscles; the fibre diameters were 10 to 40 μm. To increase the number of myoblasts before grafting some muscles were injured by Ringer solution of 70° C and transplanted after 2 days. Nevertheless, this did not influence regeneration.
After 7 days clusters of myotubes occurred in the periphery of the muscle. These myotubes originated from myoblasts growing like endothelial cells on the inner face of the persisting basal lamina tubes of necrotic fibres. After 30 days the muscles were vascularized. Fibres formed in a common basal lamina detached and so looked “split”. Satellite cells of new fibres came from undifferentiated cells associated with myotubes, i.e. from myoblasts. After 30 days and more regenerates contained three sorts of fibres. 1. Thin (5 to 20 μm) fibres resembling fetal muscle fibres. They were most prominent after 30 days, and probably not yet innervated. 2. Thin (10 μm) degenerating fibres as in long-time denervated muscles. 3. Thick (more than 30 μm) mature looking fibres which were innervated and revealed end-plates.
Half of the grafts studied after 30 and 60 days contained unmyelinated and myelinated axons which had grown along strands of surviving Schwann cells. After 250 days, only two muscles were studied which both lacked innervation. Almost all regenerates contained muscle spindles, which, however, were not innervated. Within the persisting spindle capsules new muscle fibres had been formed from satellite cells of the former intrafusal fibres.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aloisi, M.: Patterns of muscle regeneration. In: Regeneration of striated muscle, and myogenesis (A. Mauro, S.A. Shafiq, A.T. Milhorat, eds.), pp. 180–193. Amsterdam: Excerpta Medica 1970
Aloisi, M.: Discussion of Studitsky's paper. In: Exploratory concepts in muscular dystrophy II (A.T. Milhorat, ed.), p. 367. Amsterdam: Excerpta Medica 1974
Bennett, M.R., Florin, T., Woog, R.: The formation of synapses in regenerating mammalian striated muscle. J. Physiol. (Lond.) 238, 79–92 (1974)
Bischoff, R.: Enzymatic liberation of myogenic cells from adult rat muscle. Anat. Rec. 180, 645–662 (1974)
Carlson, B.M.: The regeneration of minced muscles. Basel: Karger 1972
Carlson, B.M.: The regeneration of skeletal muscle — a review. Amer. J. Anat. 137, 119–150 (1973)
Carlson, B.M., Gutmann, E.: Development of contractile properties of minced muscle regenerates in the rat. Exp. Neurol. 36, 239–249 (1972)
Corvaja, N., Magherini, P.C., Pompeiano, O.: Ultrastructure of glycogen-membrane complexes in sensory nerve fibres of cat muscle spindles. Z. Zellforsch. 121, 199–217 (1971)
Editorial: Successful transplant of cat muscle. Sci. News 107, 268 (1975)
Elson, J.: Auto- and homoio-transplantation of cross-striated muscle tissue in the rat. Amer. J. Path. 5, 425–438 (1929)
Fischman, D.A.: An electron microscope study of myofibril formation in embryonic chick skeletal muscle. J. Cell Biol. 32, 557–575 (1967)
Franzini-Armstrong, C.: Membranous systems in muscle fibres. In: The structure and function of muscle. 2nd ed., Vol. II (G.H. Bourne, ed.), pp. 531–619. New York: Academic Press 1973
Hikida, R.S., Lombardo, J.A.: Regeneration of pigeon fast and slow muscle fibre types after partial excision and mincing. J. Cell Biol. 61, 414–426 (1974)
Holtzer, H., Jones, K.W., Yaffe, D.: Research group on neuromuscular diseases: A report on various aspects of myogenic cell culture with particular reference to studies on the muscular dystrophies. J. neurol. Sci. 26, 115–124 (1975)
Ishikawa, H.: Formation of elaborate networks of T-system tubules in cultured skeletal muscle with special reference to the T-system formation. J. Cell Biol. 38, 51–66 (1968)
Kelly, A.M., Zacks, S.I.: The histogenesis of rat intercostal muscle. J. Cell Biol. 42, 135–153 (1969)
Mair, W.G.P., Tomé, F.M.S.: Atlas of the ultrastructure of diseased human muscle. Edinburgh and London: Churchill Livingstone 1972
Mastaglia, F.L., Dawkins, R.L., Papadimitriou, J.M.: Morphological changes in skeletal muscle after transplantation. J. neurol. Sci. 25, 227–247 (1975)
Mauro. A.: Satellite cell of skeletal muscle fibers. J. biophys. biochem. Cytol. 9, 493–495 (1961)
Miledi, R., Slater, C.R.: Electron-microscopic structure of denervated skeletal muscle. Proc. roy. Soc. B 174, 253–269 (1969)
Rumpelt, HJ., Schmalbruch, H.: Zur Morphologie der Bauelemente von Muskelspindeln bei Mensch und Ratte. Z. Zellforsch. 102, 601–630 (1969)
Salafsky, B.: Functional studies of regenerated muscles from normal and dystrophic mice. Nature (Lond.) 229, 270–272 (1971)
Schmalbruch, H.: “Rote” Muskelfasern. Z. Zellforsch. 119, 120–146 (1971)
Schmalbruch, H.: Muscle fibre splitting and regeneration in diseased human muscle. Neuropath. appl. Neurobiol. 2, 3–19 (1976a)
Schmalbruch, H.: The morphology of regeneration of skeletal muscles in rat. Tissue and Cell 8 (IV) (1976b) (in press)
Schmid, W., Siess, M.: Über Grenzbedingungen von Zelleben und spezifische Zellfunktion am isolierten Muskel. Pflügers Arch. ges. Physiol. 263, 492–510 (1956)
Schröder, J.M.: Degeneration and regeneration of myelinated nerve fibers in experimental neuropathies. In: Peripheral Neuropathy. Vol. I (P.J. Dyck, P.K. Thomas, E.H. Lambert, eds.), pp. 337–362. Philadelphia: Saunders 1975
Studitsky, A.N.: Dynamics of the development of myogenic tissue under conditions of explantation and transplantation. In: Cinemicrography in cell biology (G.G. Rose, ed.), pp. 171–200. New York: Academic Press 1963
Studitsky, A.N.: Free auto- and homografts of muscle tissue in experiments in animals. Ann. N.Y. Acad. Sci. 120, 789–801 (1964)
Studitsky, A.N.: The neural factor in the development of transplanted muscles. In: Exploratory concepts in muscular dystrophy II (A.T. Milhorat, ed.), pp. 351–366. Amsterdam: Excerpta Medica 1974
Walker, S.M., Schrodt, G.R., Currier, G.J., Yuen, J.W.: Development of the triadic junction in skeletal muscle fibres of fetal and postnatal rats. Amer. J. phys. Med. 54, 61–79 (1975)
Zhenevskaya, R.P., Rumyantseva, O.N., Novocyelova, I.L., Proshlyakova, E.V.: Regenerative processes in transplants of intact muscles in young rats (Russian). Zhur. Obsch. Biol. 26, 569–576 (1965) (after Carlson, 1972)
Author information
Authors and Affiliations
Additional information
This study was supported by grants from the Danish Medical Research Council, and the National Danish Association against Rheumatic Diseases. I wish to thank Miss U. Hellhammer for valuable technical help and Dr. T. Tobias for correcting my English
Rights and permissions
About this article
Cite this article
Schmalbruch, H. Regeneration of soleus muscles of rat autografted in toto as studied by electron microscopy. Cell Tissue Res. 177, 159–180 (1977). https://doi.org/10.1007/BF00221079
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00221079