Neuromuscular Activity Impairs Axonal Sprouting in Partially Denervated Muscles by Inhibiting Bridge Formation of Perisynaptic Schwann Cells

Journal of Neurobiology

Volumn 57, Issue 2, 2003, Pages 221-234

  Tam, S L ^a   Gordon, T ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Axonal sprouting; Partial denervation; Perisynaptic Schwann cells; Physiological running exercise

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXERCISE; FEMALE; IMMUNOHISTOCHEMISTRY; MUSCLE DENERVATION; NERVE ENDING; NERVE SPROUTING; NEUROMUSCULAR FUNCTION; NONHUMAN; PRIORITY JOURNAL; RAT; SCHWANN CELL; SIGNAL TRANSDUCTION; TIBIALIS ANTERIOR MUSCLE;

ANIMALS; FEMALE; HINDLIMB; IMMUNOHISTOCHEMISTRY; MOTOR ACTIVITY; MOTOR ENDPLATE; MUSCLE DENERVATION; MUSCLE, SKELETAL; NERVE REGENERATION; RATS; RATS, SPRAGUE-DAWLEY; SCHWANN CELLS; TIME FACTORS;

EID: 0142072037     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10276     Document Type: Article

References (48)

1. Brown MC, Holland RL. 1979. A central role for denervated tissues in causing nerve sprouting. Nature 282:724-726.
2. Brown MC, Holland RL, Hopkins WG. 1981. Motor nerve sprouting. Ann Rev Neurosci 4:17-42.
3. Brown MC, Holland RL, Ironton R. 1978. Degenerating nerve products affect innervated muscle fibres. Nature 275:652-654.
4. Brown MC, Ironton R. 1977. Motor neurone sprouting induced by prolonged tetrodotoxin block of nerve action potential. Nature 265:459-461.
5. Brown MC, Ironton R. 1978. Sprouting and regression of neuromuscular synapses in partially denervated mammalian muscles. J Physiol (London) 278:325-348.
6. Cangiano A, Magherini PC, Pasino E, Pellegrino M, Risaliti R. 1984. Interaction of inactivity and nerve breakdown products in the origin of acute denervation changes in rat skeletal muscle. J Physiol (London) 355:345-365.
7. Caroni P, Grandes P. 1990. Nerve sprouting in innervated adult skeletal muscle induced by exposure to elevated levels of insulin-like growth factors. J Cell Biol 110:1307-1317.
8. Cohan CS, Connor JA, Kater SB. 1987. Electrically and chemically mediated increases in intracellular calcium in neuronal growth cones. J Neurosci 7:3588-3699.
9. Collins F, Schmidt MF, Guthrie PB, Kater SB. 1991. Sustained increase in intracellular calcium promotes neuronal survival. J Neurosci 11:2582-2587.
10. Connold AL, Vrbová G. 1990. The effect of muscle activity on motor unit size in partially denervated rat soleus muscles. Neurosci 34:525-532.
11. Connold AL, Vrbová G. 1991. Temporary loss of activity prevents the increase of motor unit size in partially denervated rat soleus muscles. J Physiol (London) 434:107-119.
12. Connor JA, Kater SB, Cohan C, Fink L. 1990. Ca2+ dynamics in neuronal growth cones: regulation and changing patterns of Ca2+ entry. Cell Calcium 11:233-239.
13. Einsiedel LJ, Luff AR. 1994. Activity and motor unit size in partially denervated rat medial gastrocnemius. J Appl Physiol 76:2663-2671.
14. Gardiner PF, Michel RN, Iadeluca G. 1984. Previous exercise training influences functional sprouting of rat hindlimb motoneurons in response to partially denervation. Neurosci Lett 45:123-127.
15. Georgiou J, Robitaille R, Charlton MP. 1999. Muscarinic control of cytoskeleton in perisynaptic glia. J Neurosci 19:3836-3846.
16. Gordon T, Pattullo MC. 1993. Plasticity of muscle fiber and motor unit types. Exercise Sport Sci Rev 21:331-362.
17. Gutmann E, Jakoubek B. 1963. Effect of increased motor activity on regeneration of the peripheral nerve in young rats. Physiologia Bohemoslovenica 12:463-468.
18. Halstead LS. 1998. Post-polio syndrome. Sci Am 278:42-47.
19. Halstead LS, Wiechers DO. 1987. Research and clinical aspects of the late effects of poliomyelitis. White Plains, NY: March of Dimes Birth Defects Foundation. 363 p.
20. Holland RL, Brown MC. 1980. Postsynaptic transmission block can cause terminal sprouting of a motor nerve. Science 207:649-651.
21. Jahromi BS, Robitaille R, Charlton MP. 1992. Transmitter release increases intracellular calcium in perisynaptic Schwann cells in situ. Neuron 8:1069-1077.
22. Kater SB, Mattson MP, Cohan CS, Connor JA. 1988. Calcium regulation of the neuronal growth cone. TINS 11:315-320.
23. Kater SB, Mattson MP, Guthrie PB. 1989. Calcium-induced neuronal degeneration: a normal growth cone regulating signal gone away (?). Ann NY Acad Sci 568:252-261.
24. Kater SB, Mills LR. 1991. Regulation of growth cone behavior by calcium. J Neurosci 11:891-899.
25. Lömo T. 1976. The role of activity in the control of membrane and contractile properties of skeletal muscle. In: Thesleff S, editor. Motor innervation of muscle. London: Academic Press, p 289-321.
26. Love FM, Son YJ, Thompson WJ. 2003. Activity alters muscle reinnervation and terminal sprouting by reducing the number of Schwann cell pathways that grow to link synaptic sites. J Neurobiol 54:566-576.
27. Love FM, Thompson WJ. 1999. Glial cells promote muscle reinnervation by responding to activity-dependent postsynaptic signals. J Neurosci 19:10390-10396.
28. Mattson MP, Kater SB. 1987. Calcium regulation of neurite elongation and growth cone motility. J Neurosci 7:4034-4042.
29. Mattson MP, Taylor-Hunter A, Kater SB. 1988. Neurite outgrowth in individual neurons of a neuronal population is differentially regulated by calcium and cyclic AMP. J Neurosci 8:1704-1711.
30. Mehta A, Reynolds ML, Woolf CJ. 1993. Partial denervation of the medial gastrocnemins muscle results in growth-associated protein-43 immunoreactivity in sprouting axons and Schwann cells. Neurosci 57:433-442.
31. Pockett S, Slack JR. 1982. Source of the stimulus for nerve terminal sprouting in partially denervated muscle. Neurosci 7:3173-3176.
32. Rabben I, Bezálová G, Lömo T. 1997. Distribution of extrajunctional acetylcholine receptors in rat skeletal muscle after inactivation by botulinum toxin (abstract). Soc Neurosci Abstr 23:154.2.
33. Rafuse VF, Gordon T, Orozco R. 1992. Proportional Enlargement of Motor Units After Partial Denervation of Cat Triceps Surae Muscles. J Neurophysiol 68:1261-1275.
34. Rehder V, Kater SB. 1992. Regulation of neuronal growth cone filopodia by intracellular calcium. J Neurosci 12:3175-3186.
35. Reynolds ML, Woolf CJ. 1992. Terminal Schwann cells elaborate extensive processes following denervation of the motor endplate. J Neurocytol 21:50-66.
36. Ribchester RR. 1988. Activity-dependent and independent synaptic interactions during reinnervation of partially denervated rat muscle. J Physiol (London) 401:53-75.
37. Rochon D, Rousse I, Robitaille R. 2001. Synaptic-glia interactions at the mammalian neuromuscular junction. J Neurosci 21:3819-3829.
38. Rodnight R, Goncalves CA, Wofchuk ST, Leal R. 1997. Control of the phosphorylation of the astrocyte marker glial fibrillary acidic protein (GFAP) in the immature rat hippocampus by glutamate and calcium ions: possible key factor in astrocytic plasticity. Braz J Med Biol Res 30:325-338.
39. Slack JR, Pockett S. 1981. Terminal sprouting of motoneurones is a local response to a local stimulus. Brain Res 217:368-374.
40. Son YJ, Thompson WJ. 1995. Nerve sprouting in muscle is induced and guided by processes extended by Schwann cells. Neuron 14:133-141.
41. Son YJ, Trachtenberg JT, Thompson WJ. 1996. Schwann cells induce and guide sprouting and reinnervation of neuromuscular junctions. Trends Neurosci 19:280-285.
42. Soucy M, Seburn K, Gardiner P. 1996. Is increased voluntary motor activity beneficial or detrimental during the period of motor nerve regeneration/reinnervation. Can J Appl Physiol 21:218-224.
43. Tam SL, Archibald V, Tyreman N, Gordon T. 2002. Effect of exercise on stability of chronically enlarged motor units. Muscle Nerve 25:359-369.
44. Tam SL, Archibald V, Tyreman N, Jassar B, Gordon T. 2001. Increased neuromuscular activity reduces sprouting in partially denervated muscles. J Neurosci 21:654-667.
45. Tam SL, Gordon T. 1998a. Detrimental effect of neuromuscular activity on the ability of terminal Schwann cells to induce sprouting in extensively denervated tibialis anterior muscle (abstract). Soc Neurosci Abstr 24:413.16.
46. Tam SL, Gordon T. 2003. Mechanisms controlling axonal sprouting at the neuromuscular junction. J Neurocytol (Invited Review). In press.
47. Thompson WJ, Jansen JK. 1977. The extent of sprouting of remaining motor units in partly denervated immature and adult rat soleus muscle. Neurosci 2:523-535.
48. Yang JF, Stein RB, Jhamandas J, Gordon T. 1990. Motor unit numbers and contractile properties after spinal cord injury. Ann Neurol 28:496-502.