Muscle fibre loss and reinnervation after long-term denervation
Rent the article at a discountRent now
* Final gross prices may vary according to local VAT.Get Access
Cutaneus pectoris muscles of frog (Rana temporaria) were investigated 19.5–40 months after denervation. On whole mounts a heavy reduction in size and number of muscle fibres is noticed; in two muscles studied with semithin and ultrathin sections the number of remaining muscle fibres is 149 and around 120, while one of the contralateral muscles contains 250 and control muscles of equal sized frogs between 220 and 320 (n=18) fibres. By electron microscopy muscle fibres undergoing degeneration or phagocytosis can be seen (3 of 20 muscle fibres present in a single ultrathin cross-section). On the other hand several profiles contained within one common basal lamina sheath are present in 14 of 20 fibres, indicating satellite cell proliferation. In one preparation 40 months after denervation not a single muscle fibre or axon is present, suggesting that eventually, without nerve supply, muscle fibres entirely disappear.
Upon spontaneous reinnervation or implantation of the hypoglossal nerve 16 months after denervation, synapses are formed with the remaining muscle fibres. When studied 3.5–24 months after nerve implantation muscles innervated by few axons only (< 10, 10–20 axons) contain a low number of muscle fibres (mean 44 ± 41sd,n=6), while all muscles with a larger number of axons have more than 150 muscle fibres (n=6). This indicates that unless large numbers of axons regenerate and/or when reinnervation is delayed muscle fibre loss continues to occur. The presence in one muscle of motor axons but only six muscle fibres 24 months after nerve implantation indicates that muscle fibre loss cannot be reversed, or recovery is extremely slow. This observation is interpreted as evidence for the exhaustibility of the satellite cell pool.
- Anz1l, A. P., Bieser, A. &Wernig, A. (1984) Light and electron microscopic identification of nerve terminal sprouting and retraction in normal adult frog muscle.Journal of Physiology 350, 393–9.
- Burden, S. J., Sargent, P. B. &McMahan, U. J. (1979) Acetylcholine receptors in regenerating muscle accumulate at original synaptic sites in the absence of the nerve.Journal of Cell Biology 82, 412–25.
- Cardasis, C. A. (1983) Ultrastructural evidence of continued reorganization at the ageing (11–26 months) rat soleus neuromuscular junction.Anatomical Record 207, 399–415.
- Carpenter, S. &Karpati, G. (1979) Duchenne muscular dystrophy: plasma membrane loss initiates muscle cell necrosis unless it is repaired.Brain 102, 147–61.
- Carpenter, S. &Karpati, G. (1984)Pathology of Skeletal Muscle. New York, Edinburgh, London, Melbourne: Churchill Livingstone.
- Carraro, U., Morale, D., Mussini, I., Lucke, S., Cantini, M., Betto, R., Catani, C., Libera, L. D., Betto, D. D. &Noventa, D. (1985) Chronic denervation of rat hemidiaphragm: maintenance of fibre heterogeneity with associated increasing uniformity of myosine isoforms.Journal of Cell Biology 100, 161–74.
- Cazzato, G. (1970) Myopathic changes in denervated muscle. A study of biopsy material in various neuromuscular diseases. InMuscle Diseases (edited byWalton, J. M., Canal, D. &Scarlato, G.), pp. 392–401. Amsterdam: Excerpta Medica.
- Darr, K. C. &Schultz, E. (1987) Exercise-induced satellite cell activation in growing and mature skeletal muscle.Journal of Applied Physiology 63, 1816–21.
- Diaz, J. &Pécot-Dechavassine, M. (1988) Electrophysiological and morphological study of polyneuronal innervation in the cutaneus pectoris muscle of adult frog (Rana esculenta).Journal of Neurocytology 17, 279–92.
- Drachman, D. B., Murphy, S. A., Nigam, M. P. &Hills, J. R. (1967) ‘Myopathie’ changes in chronically denervated muscles.Archives of Neurology 16, 14–24.
- Duchen, L. W. &Strich, S. J. (1968) The effects of botulinum toxin on the pattern of innervation of skeletal muscle in the mouse.Quarterly Journal of Experimental Physiology 53, 84–9.
- Glicksman, M. A. &Sanes, J. R. (1983) Differentiation of motor nerve terminals formed in the absence of muscle fibres.Journal ofNeurocytology 12, 661–71.
- Gutmann, E. (1948) Effect of delay of innervation on recovery of muscle after nerve lesions.Journal of Neurophysiology 11, 279–94.
- Gutmann, E. &Young, J. Z. (1944) The re-innervation of muscle after various periods of atrophy.Journal of Anatomy 78, 15–43.
- Gutmann, E. &Zelena, J. (1962) Morphological changes in the denervated muscle. InThe Denervated Muscle (edited byGutmann, E.), pp. 57–102. Prague: Publishing House of the Czechoslovak Academy of Sciences.
- Hunter, D. D., Shah, V., Merlie, J. P. &Sanes, J. R. (1989) A laminin-like adhesive protein concentrated in the synaptic cleft of the neuromuscular junction.Nature 388, 229–34.
- Irintchev, A. &Wernig, A. (1987) Muscle damage and repair in voluntarily running mice: strain and muscle differences.Cell and Tissue Research 249, 509–21.
- Jans, H., Salzmann, R. &Wernig, A. (1986) Sprouting and nerve retraction in frog neuromuscular junction during ontogenesis and environmental changes.Neuroscience 18, 773–81.
- Karnovsky, M. J. &Roots, L. (1964) A ‘direct-coloring’ thiocholine method for cholinesterases.Journal of Histochemistry and Cytochemistry 12, 219–21.
- Karpati, G. &Carpenter, S. (1989) The deficiency of a sarcolemmal cytoskeletal protein (dystrophin) leads to the necrosis of skeletal muscle fibres in Duchenne-Becker dystrophy. InNeuromuscular Junction (edited bySellin, L. C., Libelius, R. &Thesleff, S.), pp. 429–36. Amsterdam, New York, Oxford: Elsevier.
- Ko, Ch.-P. (1984) Regeneration of the active zone at the frog neuromuscular junction.Journal of Cell Biology 98, 1685–95.
- Konigsberg, U. R., Lipton, B. H. &Konigsberg, I. R. (1975) The regenerative response of single mature muscle fibres isolatedin vitro.Developmental Biology 45, 260–75.
- Krause, M. &Wernig, A. (1985) The distribution of acetylcholine receptors in the normal and denervated neuromuscular junction of the frog.Journal of Neurocytology 14, 765–80.
- Lomo, T., Pockett, S. &Sommerschild, H. (1988) Control of number and distribution of synapses during ectopic synapse formation in adult rat soleus muscles.Neuroscience 24, 673–86.
- Magill, C., Reist, N. E., Fallon, J. R., Nitkin, R. M., Wallace, B. G. &McMahan, U. J. (1987) Agrin.Progress in Brain Research 71, 391–6.
- McMahan, U. J., Edg1ngton, D. R. &Kuffler, D. P. (1980) Factors that influence regeneration of the neuromuscular junction.Journal of Experimental Biology 89, 31–42.
- Miledi, R. &Slater, C. R. (1969) Electron microscopic structure of denervated skeletal muscle.Proceedings of the Royal Society of London B 174, 253–69.
- Ontell, M. (1974) Muscle satellite cells: a validated technique for light microscopic identification and a quantitative study of changes in their population following denervation.Anatomical Record 18, 211–28.
- Rutishauser, U. &Jessell, T. M. (1988) Cell adhesion molecules in vertebrate neural development.Physiological Reviews 68, 819–57.
- Sanes, J. R., Marshall, L. M. &McMahan, U. J. (1978) Reinnervation of muscle fibre basal lamina after removal of myofibres. Differentiation of regenerating axons at original synaptic sites.Journal of Cell Biology 78, 176–98.
- Sayers, H. &Tonge, D. A. (1982) Differences between foreign and original innervation of skeletal muscle in the frog.Journal of Physiology 330, 57–68.
- Sayers, H. &Tonge, D. A. (1986) A study of factors influencing synapse formation by a foreign nerve in skeletal muscle ofRana pipiens.Journal of Physiology 375, 449–60.
- Schmalbruch, H. (1984) Regenerated muscle fibres in Duchenne muscular dystrophy: a serial section study.Neurology 34, 60–5.
- Schultz, E. (1978) Changes in the satellite cells of growing muscle following denervation.Anatomical Record 190, 299–312.
- Wernig, A., Pécot-Dechavassine, M. &Stöver, H. (1980) Sprouting and regression of the nerve at the frog neuromuscular junction in normal conditions and after prolonged paralysis with curare.Journal of Neurocytology 9, 277–303.
- Wernig, A. &Herrera, A. A. (1986) Sprouting and remodelling at the nerve-muscle junction.Progress in Neurobiology 27, 251–91.
- Wernig, A. &Irintchev, A. (1988) Muscle reinnervation and recovery after long-term denervation.Pflügers Archiv 412 (Supplement 1), R74.
- Wernig, A. &Irintchev, A. (1989) Intermittent voluntary running causes changes in muscle fibre type composition and in contractile muscle force in the mouse.Pflügers Archiv 413 (Supplement 1), R33.
- Muscle fibre loss and reinnervation after long-term denervation
Journal of Neurocytology
Volume 18, Issue 6 , pp 833-845
- Cover Date
- Print ISSN
- Online ISSN
- Kluwer Academic Publishers
- Additional Links