Neural impacts on the regeneration of skeletal muscles.
Languages of publication
The regeneration of skeletal muscles is a suitable model to study the development and differentiation of contractile tissues. Neural effects are one of the key factors in the regulation of this process. In the present work, effects of different reinnervation protocols (suture or grafting) were studied upon the regenerative capacity of rat soleus muscles treated with the venom of the Australian tiger snake, notexin, which is known to induce complete necrosis and subsequent regeneration of muscles. Morphological and motor endplate analysis indicated that the regenerative capacity of denervated, and thereafter surgically reinnervated muscles remains impaired compared to that of normally innervated muscles, showing differences in the muscle size, fiber type pattern and motor endplate structure, even 35 days after the notexin injection. A lack or deficiency of secreted neural factors, deterioration of satellite cells and/or incomplete recovery of the sutured or grafted nerves may be the cause of these discrepancies in the regeneration process.
- Department of Traumatology, Faculty of Medicine, University of Szeged, Szeged, Hungary
- Institute of Biochemistry, Faculty of Medicine, University of Szeged, Szeged, Hungary
- Institute of Biochemistry, Faculty of Medicine, University of Szeged, Szeged, Hungary
- Alnot JY. (1995) Traumatic brachial plexus lesions in adult: indications and results. Microsurgery.; 16: 22-9.
- Asakura A, Seale P, Girgis-Gabardo A, Rudnicki MA. (2002) Myogenic specification of side population cells in skeletal muscle. J Cell Biol.; 159: 123-34.
- Berger A, Brenner P. (1995) Secondary surgery following brachial plexus injuries. Microsurgery.; 16: 43-7.
- Bischoff R. (1993) The satellite cell and muscle regeneration. In Myology. Basic and clinical. Engel AG, Franzini-Armstrong C, eds, vol. 1, pp 97-118. 2nd edn. McGraw-Hill, Inc.
- Borisov AB, Dedkov E, Carlson BM. (2001) Interrelations of myogenic response, progressive atrophy of muscle fibers, and cell death in denervated skeletal muscle. Anat Rec.; 264: 203-18.
- Davis CE, Harris JB, Nicholson LV. (1991) Myosin isoform transitions and physiological properties of regenerated and re-innervated soleus muscles of the rat. Neuromusc Disord.; 1: 411-21.
- Doi K, Hattori Y, Kuwata N, Soo-heong T, Kawakami F, Otsuka K, Watanbe M. (1998) Free muscle transfer can restore hand function after injuries of the lower brachial plexus. J Bone Joint Surg Br.; 80: 117-20.
- Dux L, Cooper BJ, Sewry CA, Dubowitz V. (1993) Notechis scutatus venom increases the yield of proliferating muscle cells from biopsies of normal and dystrophic canine muscle - a possible source for myoblast transfer studies. Neuromusc Disord.; 3: 23-9.
- Germinario E, Esposito A, Megighian A, Midrio M, Biral D, Betto R, Danieli-Betto D. (2002) Early changes of type 2B fibers after denervation of rat EDL skeletal muscle. J Appl Physiol.; 92: 2045-52.
- Grubb BD, Harris JB, Schofield IS. (1991) Neuromuscular transmission at newly formed neuromuscular junctions in the regenerating soleus muscle of the rat. J Physiol.; 441: 405-21.
- Gutmann E, Zelena J. (1962) Morphological changes in the denervated muscle. In The denervated muscle. Gutmann E, ed, pp 341-71. Prague Publishing House of the Czechoslovak Academy of Sciences, Prague.
- Harris JB, Johnson MA, Karlsson E. (1975) Pathological responses of rat skeletal muscle for a single subcutaneous injection of a toxin isolated from the venom of the Australian tiger snake, Notechis scutatus. Clin Exp Pharmacol Physiol.; 2: 383-404.
- Harris JB, Johnson MA. (1978) Further observations on the pathological responses of rat skeletal muscle to toxins isolated from the venom of the Australian tiger snake. Clin Exp Pharmacol Physiol.; 5: 587-600.
- Ijkema-Paassen J, Meek MF, Gramsbergen A. (2001a) Muscle differentiation after sciatic nerve transection and reinnervation in adult rats. Ann Anat.; 183: 369-77.
- Ijkema-Paassen J, Meek MF, Gramsbergen A. (2001b) Transection of the sciatic nerve and reinnervation in adult rats: muscle and endplate morphology. Equine Vet J Suppl.; 33: 41-5.
- Lefaucheur JP, Sebille A. (1995) The cellular events of injured muscle regeneration depend on the nature of the injury. Neuromusc Disord.; 5: 501-9.
- Louboutin JP, Fichter-Gagnepain V, Noireaud J. (1995) Comparison of contractile properties between developing and regenerating soleus muscle: influence of external calcium concentration upon contractility. Muscle Nerve.; 18: 1292-9.
- Mackinnon SE. (1993) Peripheral nerve injuries. Curr Opin Orthoped.; 4: 61-7.
- Maier A, Zhou Z, Bornemann A. (2002) The expression profile of myogenic transcription factors in satellite cells from denervated rat muscle. Brain Pathol.; 12: 170-7.
- Mauro A. (1961) Satellite cells of skeletal muscle fibers. J Biophys Biochem Cytol.; 9: 493-5.
- Mendler L, Zádor E, Dux L, Wuytack F. (1998a) mRNA levels of myogenic regulatory factors in rat slow and fast muscles regenerating from notexin-induced necrosis. Neuromusc Disord.; 8: 533-41.
- Mendler L, Szakonyi G, Zádor E, Görbe A, Dux L, Wuytack F. (1998b) Expression of sarcoplasmic/endoplasmic reticulum Ca2+ ATPases in the rat extensor digitorum longus (EDL) muscle regenerating from notexin-induced necrosis. J Muscle Res Cell Motil.; 19: 777-85.
- Mendler L, Zádor E, Ver Heyen M, Dux L, Wuytack F. (2000) Myostatin in regenerating rat muscles and in myogenic cell cultures. J Muscle Res Cell Motil., 21: 551-63.
- Nnodim JO. (2001) Testosterone mediates satellite cell activation in denervated rat levator ani muscle. Anat Rec.; 263: 19-24.
- Pette D, Staron R. (1990) Cellular and molecular diversities of mammalian skeletal muscle fibers. Rev Physiol Biochem Pharmacol.; 116: 1-76.
- Pette D, Vrbová G. (1992) Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation. Rev Physiol Biochem Pharmacol.; 120: 115-202.
- Preston SA, Davis CE, Harris JB. (1990) The assessment of muscle fibre loss after the injection of the venom of Notechis scutatus (Australian tiger sanke). Toxicon.; 28: 201-14.
- Saito Y, Nonaka I (1994) Initiation of satellite cell replication in bupivacaine-induced myonecrosis. Acta Neuropathol.; 88: 252-7.
- Sesodia S, Cullen MJ. (1991) The effect of denervation on the morphology of regenerating rat soleus muscles. Acta Neuropathol.; 82: 21-32.
- Sesodia S, Choksi RM, Nemeth PM. (1994) Nerve-dependent recovery of metabolic pathways in regenerating soleus muscles. J Muscle Res Cell Motil.; 15: 573-81.
- Sewry CA, Wilson LA, Dux L, Dubowitz V, Cooper JB. (1992) Experimetal regeneration in canine muscular dystrophy 1. Immunocytochemical evaluation of dystrophin and beta-spectrin expression. Neuromusc Disord.; 2: 331-42.
- Sunderland S, Ray LJ. (1950) Denervation changes in mammalian striated muscles. J Neurol Neurosurg Psychiatry.; 13: 159-77.
- Tago H, Kimura H, Maeda T. (1986) Visualization of detailed acetylcholinesterase: fiber and neuron staining in rat brain by a sensitive histochemical procedure. J Histochem Cytochem.; 34: 1431-8.
- Vater R, Cullen MJ, Harris JB. (1992) The fate of desmin and titin during the degeneration and regeneration of the soleus muscle of the rat. Acta Neuropathol.; 84: 278-88.
- Wang L, Copray S, Brouwer N, Meek M, Kernell D. (2002) Regional distribution of slow-twitch muscle fibers after reinnervation in adult rat hindlimb muscles. Muscle Nerve.; 25: 805-15.
- Whalen RG, Harris JB, Butler-Browne GS, Sesodia S. (1990) Expression of myosin isoforms during notexin-induced regeneration of rat soleus muscles. Dev Biol.; 141: 24-40.
- Wilson LA, Cooper BJ, Dux L, Dubowitz V, Sewry CA. (1994a) Expression of utrophin (dystrophin related protein) during regeneration and maturation of skeletal muscle in canine x-linked muscular dystrophy. Neuropathol Appl Neurobiol.; 20: 359-67.
- Wilson LA, Dux L, Cooper BJ, Dubowitz V, Sewry CA. (1994b) Experimental regeneration in canine muscular dystrophy - 2. Expression of myosin heavy chain isoforms. Neuromusc Disord.; 4: 25-37.
- Zádor E, Mendler L, Ver Heyen M, Dux L, Wuytack F. (1996) Changes in mRNA levels of the sarcoplasmic/endoplasmic-reticulum Ca2+-ATPase isoforms in the rat soleus muscle regenerating from notexin-induced necrosis. Biochem J.; 320: 107-13.
- Zádor E, Szakonyi G, Rácz G, Mendler L, Ver Heyen M, Lebacq J, Dux L, Wuytack F. (1998) Expression of the sarco/endoplasmic reticulum Ca2+-transport ATPase protein isoforms during regeneration from notexin induced necrosis of rat muscle. Acta Histochem.; 100: 355-69.
- Zádor E, Dux L, Wuytack F. (1999) Prolonged passive stretch of rat soleus muscle provokes an increase in the mRNA levels of the muscle regulatory factors distributed along the entire length of the fibers. J Muscle Res Cell Motil.; 20: 395-402.
- Zádor E, Mendler L, Takács V, De Bleecker J, Wuytack F. (2001) Regenerating soleus and EDL muscles of the rat show elevated levels of TNF-α and its receptors, TNFR-60 and TNFR-80. Muscle Nerve.; 24: 1058-67.
- Zádor E, Bottka S, Wuytack F. (2002) Antisense inhibition of myoD expression in regenerating rat soleus muscle is followed by an increase in the mRNA levels of myoD, myf-5 and myogenin and by a retarded regeneration. Biochim Biophys Acta.; 1590: 52-63.
- Zádor E, Wuytack F. (2003) Expression of SERCA2a is independent of innervation in regenerating soleus muscle. Am J Physiol Cell Physiol.; 285: C853-61.
Publication order reference