Age-dependent synapse withdrawal at axotomised neuromuscular junctions in Wlds mutant and Ube4b/Nmnat transgenic mice

Journal of Physiology

Volumn 543, Issue 3, 2002, Pages 739-755

  Gillingwater, Thomas H ^a   Thomson, Derek ^a   Mack, Till G A ^b   Soffin, Ellen M ^a   Mattison, Richard J ^a   Coleman, Michael P ^b   Ribchester, Richard R ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEIN; FLUORESCENT DYE; NICOTINAMIDE MONONUCLEOTIDE ADENYLYL TRANSFERASE; UNCLASSIFIED DRUG; CYAN FLUORESCENT PROTEIN;

AGE; CONTROLLED STUDY; ENDPLATE POTENTIAL; GENE EXPRESSION; GENE OVEREXPRESSION; MOUSE; MOUSE MUTANT; NERVE DEGENERATION; NERVE ENDING; NERVE FIBER TRANSECTION; NERVE REGENERATION; NEUROMUSCULAR SYNAPSE; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; TRANSGENIC MOUSE; WILD TYPE; ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; GENE; NERVE CELL DEGENERATION; REINNERVATION; WLD GENE; YOUNG ADULT;

AGING; ANIMALS; AXONS; AXOTOMY; FUNGAL PROTEINS; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON; MUSCLE, SKELETAL; NERVE REGENERATION; NEUROMUSCULAR JUNCTION; NICOTINAMIDE-NUCLEOTIDE ADENYLYLTRANSFERASE; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; SYNAPSES; UBIQUITIN-CONJUGATING ENZYMES; WALLERIAN DEGENERATION;

EID: 0037106522     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2002.022343     Document Type: Review

References (64)

1. Balice-Gordon, R. J., Chua, C. K., Nelson, C. C. & Lichtman, J. W. (1993). Gradual loss of synaptic cartels precedes axon withdrawal at developing neuromuscular junctions. Neuron 11, 801-815.
2. Balice-Gordon, R. J. & Lichtman, J. W. (1993). In vivo observations of pre- and postsynaptic changes during the transition from multiple to single innervation at developing neuromuscular junctions. Journal of Neuroscience 13, 834-855.
3. Balice-Gordon, R. J. & Lichtman, J. W. (1994). Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372, 519-524.
4. Barry, J. A. & Ribchester, R. R. (1995). Persistent polyneuronal innervation in partially denervated rat muscle after reinnervation and recovery from prolonged nerve conduction block. Journal of Neuroscience 15, 6327-6339.
5. Betz, W. J., Caldwell, J. H. & Ribchester, R. R. (1979). The size of motor units during post-natal development of rat lumbrical muscle. Journal of Physiology 297, 463-478.
6. Betz, W. J., Caldwell, J. H. & Ribchester, R. R. (1980). The effects of partial denervation at birth on the development of muscle fibres and motor units in rat lumbrical muscle. Journal of Physiology 303, 265-279.
7. Birks, R., Katz, B. & Miledi, R. (1960). Physiological and structural changes at the amphibian myoneural junction, in the course of nerve degeneration. Journal of Physiology 150, 145-168.
8. Bixby, J. L. (1981). Ultrastructural observations on synapse elimination in neonatal rabbit skeletal muscle. Journal of Neurocytology 10, 81-100.
9. Brown, M. C. & Ironton, R. (1978). Sprouting and regression of neuromuscular synapses in partially denervated mammalian muscles. Journal of Physiology 278, 325-348.
10. Brown, M. C., Jansen, J. K. S. & Van Essen, D. C. (1976). Polyneuronal innervation of skeletal muscle in new-born rats and its elimination during maturation. Journal of Physiology 261, 387-422.
11. Brown, M. C., Lunn, E. R. & Perry, V. H. (1992). Consequences of slow Wallerian degeneration for regenerating motor and sensory axons. Journal of Neurobiology 23, 521-536.
12. + levels. European Journal of Neuroscience 7, 1596-1602.
13. Chang, Q. & Balice-Gordon, R. J. (2000). Highwire, rpm-1, and futsch: Balancing synaptic growth and stability. Neuron 26, 287-290.
14. Changeux, J. P. (2001). Cajal on neurons, molecules, and consciousness. Annals of the New York Academy of Sciences 929, 147-151.
15. s) mouse. Proceedings of the National Academy of Sciences of the USA 95, 9985-9990.
16. Colman, H., Nabekura, J. & Lichtman, J. W. (1997). Alterations in synaptic strength preceding synaptic withdrawal. Science 275, 356-361.
17. s) mouse. Proceedings of the National Academy of Sciences of the USA 97, 11377-11382.
18. Costanzo, E. M., Barry, J. A. & Ribchester, R. R. (1999). Coregulation of synaptic efficacy at stable polyneuronally innervated neuromuscular junctions in reinnervated rat muscle. Journal of Physiology 521, 365-374.
19. Costanzo, E. M., Barry, J. A. & Ribchester, R. R. (2000). Competition at silent synapses in reinnervated skeletal muscle. Nature Neuroscience 3, 694-700.
20. Crawford, T. O., Hsieh, S.-T., Schryer, B. L. & Glass, J. D. (1995). Prolonged axonal survival in transected nerves of C57Bl/Ola mice is independent of age. Journal of Neurocytology 24, 333-340.
21. Deckwerth, T. L. & Johnson, E. M. (1994). Neurites can remain viable after the destruction of the neuronal soma by programmed cell death. Developmental Biology 165, 63-72.
22. DiAntonio, A., Haghighi, A. P., Portman, S. L., Lee, J. D., Amaranto, A. M. & Goodman, C. S. (2001). Ubiquitin-dependent mechanisms regulate synaptic growth and function. Nature 412, 449-452.
23. Feng, G., Mellor, R. H., Bernstein, M., Keller-Peck, C., Nguyen, Q. T., Wallace, M., Gross, J., Nerbonne, J. M., Lichtman, J. W. & Sanes, J. R. (2000). Imaging neuronal subsets in transgenic mice expressing multiple variants of GFP. Neuron 28, 41-51.
24. Fladby, T. & Jansen, J. K. S. (1987). Postnatal loss of synaptic terminals in the partially denervated mouse soleus muscle. Acta Physiologica Scandinavica 129, 239-246.
25. s mutant mice. Journal of Physiology 523.P, 53P.
26. s mutant mouse. Journal of Physiology 534, 627-639.
27. Gorio, A., Carmignoto, G., Finesso, M., Polato, P. & Nunzi, M. G. (1983). Muscle reinnervation - II. Sprouting, synapse formation and repression. Neuroscience 8, 403-415.
28. Herdegen, T. & Leah, J. D. (1998). Inducible and constitutive transcription factors in the mammalian nervous system: Control of gene expression by jun, fos and krox, and creb/atf proteins. Brain Research Reviews 28, 370-490.
29. Hoffman, H. (1953). The persistence of hyperneurotized end-plates in mammalian muscles. Journal of Comparative Neurology 99, 331-345.
30. Keller-Peck, C. R., Walsh, M. K., Gan, W.-B., Feng, G., Sanes, J. R. & Lichtman, J. W. (2001). Asynchronous synapse elimination in neonatal motor units: Studies using GFP transgenic mice. Neuron 31, 381-394.
31. Kopp, D. M., Perkel, D. J. & Balice-Gordon, R. J. (2000). Disparity in neurotransmitter release probability among competing inputs during neuromuscular synapse elimination. Journal of Neuroscience 20, 8771-8779.
32. Korneliussen, H. & Jansen, J. K. S. (1976). Morphological aspects of the elimination of polyneuronal innervation of skeletal muscle fibres in newborn rats. Journal of Neurocytology 5, 591-604.
33. Lichtman, J. W. & Fraser, S. E. (2001). The neuronal naturalist: watching neurons in their native habitat. Nature Neuroscience 4, 1215-1220.
34. Lunn, E. R., Perry, V. H., Brown, M. C., Rosen, H. & Gordon, S. (1989). Absence of Wallerian degeneration does hinder regeneration in peripheral nerve. European Journal of Neuroscience 1, 27-33.
35. Lyon, M. F., Ogunkolade, B. W., Brown, M. C., Atherton, D. J. & Perry, V. H. (1993). A gene affecting Wallerian nerve degeneration maps distally on mouse chromosome 4. Proceedings of the National Academy of Sciences of the USA 90, 9717-9720.
36. Mack, T. G. A., Reiner, M., Beirowski, B., Mi, W., Emanuelli, M., Wagner, D., Thomson, D., Gillingwater, T., Court, F., Conforti, L., Shama Fernando, F., Tarlton, A., Andressen, C., Addicks, K., Magni, G., Ribchester, R. R., Perry, V. H. & Coleman, M. P. (2001). Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nature Neuroscience 4, 1199-1206.
37. Mattson, M. P., Keller, J. N. & Begley J. G. (1998a). Evidence for synaptic apoptosis. Experimental Neurology 153, 35-48.
38. Mattson, M. P., Partin, J. & Begley, J. G. (1998b). Amyloid β-peptide induces apoptosis-related events in synapses and dendrites. Brain Research 807, 167-176.
39. McArdle, J. J. (1975). Complex end-plate potentials at the regenerating neuromuscular junction of the rat. Experimental Neurology 49, 629-638.
40. s) for axons. Journal of Neuroscience Methods 113, 215-218.
41. Miledi, R. & Slater, C. R. (1970). On the degeneration of rat neuromuscular junctions after nerve section. Journal of Physiology 207, 507-528.
42. Nicholls, J. G., Martin, A. R. & Wallace, B. G. (1992). From Neuron to Brain, 3rd edn, pp. 389. Sinauer Associates Massachusetts, USA.
43. s). European Journal of Neuroscience 9, 1586-1592.
44. Perry, V. H., Brown, M. C. & Lunn, E. R. (1990a). Very slow retrograde and Wallerian degeneration in the CNS of C57Bl/Ola mice. European Journal of Neuroscience 3, 102-105.
45. Perry, V. H., Brown, M. C. & Tsao, J. W. (1992). The effectiveness of the gene which slows the rate of Wallerian degeneration in C57Bl/Ola mice declines with age. European Journal of Neuroscience 4, 1000-1002.
46. Perry, V. H., Lunn, E. R., Brown, M. C., Cahusac, S. & Gordon, S. (1990b). Evidence that the rate of Wallerian degeneration is controlled by a single autosomal dominant gene. European Journal of Neuroscience 2, 408-413.
47. Pun, S., Sigrist, M., Santos, A. F., Ruegg, M. A., Sanes, J. R., Jessell, T. M., Arber, S. & Caroni, P. (2002). An intrinsic distinction in neuromuscular junction assembly and maintenance in different skeletal muscles. Neuron 34, 357-370.
48. Raff, M. C., Whitmore, A. V. & Finn, J. T. (2002). Axonal self-degeneration and neurodegeneration. Science 296, 868-871.
49. Ribchester, R. R. (2001). Development and plasticity of neuromuscular connections. In Brain and Behaviour in Human Neural Development, ed. A. F. Kalverboer & A. Gramsbergen, pp. 261-341. Kluwer Academic Press, London.
50. s mice. European Journal of Physiology 443, 183S
51. Ribchester, R. R., Mao, F. & Betz, W. J. (1994). Optical measurements of activity-dependent membrane recycling in motor nerve terminals of mammalian skeletal muscle. Proceedings of the Royal Society B 255, 61-66.
52. s mutant mouse skeletal muscle. Journal of Physiology 520.P, 76P.
53. s). European Journal of Neuroscience 7, 1641-1650.
54. Rich, M. M. & Lichtman, J. W. (1989). In vivo visualization of presynaptic and postsynaptic changes during synapse elimination in reinnervated mouse muscle. Journal of Neuroscience 9, 1781-1805.
55. Riley, D. A. (1977). Spontaneous elimination of nerve terminals from the endplates of developing skeletal myofibers. Brain Research 134, 279-285.
56. Roden, R. L., Donahue, S. P., Schwartz, G. A., Wood, J. G. & English, A. W. (1991). 200kD neurofilament protein and synapse elimination in the rat soleus. Synapse 9, 239-243.
57. Rosenthal, J. L. & Taraskevich, P. S. (1977). Reduction of multiaxonal innervation at the neuromuscular junction of the rat during development. Journal of Physiology 270, 299-310.
58. Tello, J. F. (1907). Degeneration et regeneration des plaques motrices après la section des nerfs. Travaux du Laboratoire de Recherches Biologiques de l'Université de Madrid 5, 117-149.
59. Thompson, W. & Jansen, J. K. S. (1977). The extent of sprouting of remaining motor units in partly denervated immature and adult rat soleus muscle. Neuroscience 2, 523-535.
60. Tsao, J. W., Brown, M. C., Carden, M. J., McLean, W. G. & Perry, V. H. (1994). Loss of the compound action potential: an electrophysiological, biochemical and morphological study of early events in axonal degeneration in the C57Bl/Ola mouse. European Journal of Neuroscience 6, 516-524.
61. Wan, H. I., Diantonio, A., Fetter, R. D., Bergstrom, K., Strauss, R. & Goodman, C. S. (2000). Highwire regulates synaptic growth in Drosophila. Neuron 26, 313-329.
62. Watson, D. F., Glass, J. D. & Griffin, J. W. (1993). Redistribution of cytoskeletal proteins in mammalian axons disconnected from their cell bodies. Journal of Neuroscience 13, 4354-4360.
63. Winlow, W. & Usherwood, P. N. R. (1975). Ultrastructural studies of normal and degenerating mouse neuromuscular junctions. Journal of Neurocytology 4, 377-394.
64. Wood, S. J. & Slater, C. R. (1997). The contribution of postsynaptic folds to the safety factor for neuromuscular transmission in rat fast- and slow-twitch muscles. Journal of Physiology 500, 165-176.