Axon withdrawal during synapse elimination at the neuromuscular junction is accompanied by disassembly of the postsynaptic specialization and withdrawal of Schwann cell processes

Journal of Neuroscience

Volumn 18, Issue 13, 1998, Pages 4953-4965

  Culican, Susan M ^a   Nelson, Carla C ^a   Lichtman, Jeff W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AChR; Neuromuscular junction; Postsynaptic specialization; Schwann cell; Synapse elimination; Synaptic competition

Indexed keywords

CHOLINERGIC RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNOCYTOCHEMISTRY; MOUSE; NERVE ENDING; NERVE FIBER; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR DENSITY; REINNERVATION; SCHWANN CELL; SYNAPSE;

EID: 0032125483     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-13-04953.1998     Document Type: Article

References (49)

1. Adams ME, Butler MH, Dwyer TM, Peters MF, Murnane AA, Froehner SC (1993) Two forms of mouse syntrophin, a 58k dystrophin-associated protein, differ in primary structure and tissue distribution. Neuron 11:531-540.
2. Balice-Gordon RJ, Lichtman JW (1993) In vivo observations of presyn aptic and postsynaptic changes during the transition from multiple to single innervation at developing neuromuscular junctions. J Neurosci 13:834-855.
3. Balice-Gordon RJ, Licht man JW (1994) Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372:519-524.
4. Balice-Gordon RJ, Chua C, Nelson CC, Lichtman JW (1993) Gradual loss of synaptic cartels precedes axon withdrawal at developing neuromuscular junctions. Neuron 11:801-815.
5. Bridgman PC, Carr C, Pedersen SE, Cohen JB (1989) Visualization of the cytoplasmic surface of torpedo postsynaptic membrane by freezeetch and immunoclcetron microscopy. J Cell Biol 105:1829-1846.
6. Brown MC, Jansen JKS, Van Essen D (1976) Polyneuronal innervation of skeletal muscle in new-born rats and its elimination during maturation. J Physiol (Lond) 261:387-422.
7. Carr C, Fischbach GD, Cohen JB (1989) A novel 87,000-Mr protein associated with acetylcholine receptors in Torpedo electric organ and vertebrate skeletal muscle. J Cell Biol 109:1753-1764.
8. Colman H, Nabekura J, Lichtman JW (1997) Alterations in synaptic strength preceding axon withdrawal. Science 275:356-361.
9. Covault J, Sanes JR (1985) Neural cell adhesion molecule (N-CAM) accumulates in denervated and paralyzed skeletal muscles. Proc Natl Acad Sci USA 82:4544-4548.
10. Covault J, Sanes JR (1986) Distribution of N-CAM in synaptic and extrasynaptic portions of developing and adult skeletal muscle. J Cell Biol 102:716-730.
11. Dai Z, Scotland PB, Froehner SC, Peng HB (1993) Expression of the postsynaptic 43K protein in Xenopus embryonic cells and its association with phosphotyrosine. Soc Neurosci Abstr 19:1273.
12. Dechiara TM, Bowen DC, Valenzuela DM, Simmons M, Poueymirou WT, Thomas S, Kinetz E, Compton DL, Rojas E, Park JS, Smith C, Distefano PS, Glass DJ, Burden SJ, Yancopoulos GD (1996) The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85:501-512.
13. Froehner SC (1991) The submembrane machinery for nicotinic acetylcholine receptor clustering. J Cell Biol 114:1-7.
14. Froehner SC, Murnane AA, Tobler M, Peng HB, Sealock R (1987) A postsynaptic Mr 58,000 (58K) protein concentrated at acetylcholine receptor-rich sites in Torpedo electroplaques and skeletal muscle. J Cell Biol 104:1633-1646.
15. Froehner SC, Luetje CW, Scotland PB, Patrick J (1990) The postsynaptic 43K protein clusters muscle nicotinic acetylcholine receptors in Xenopus oocytes. Neuron 5:403-410.
16. Gautam M, Noakes PG, Mudd J, Nichol M, Chu GC, Sanes JR, Merlie JP (1995) Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377:232-236.
17. Gu Y, Hall ZW (1988) Immunological evidence for a change in subunits of the acetylcholine receptor in developing and denervated rat muscle. Neuron 1:117-125.
18. Hill RR, Robbins NJ, Fang Z-P (1991) Plasticity of presynaptic and postsynaptic elements of neuromuscular junctions repeatedly observed in living adult mice. J Neurocytol 19:85-99.
19. Hunter DD, Porter BE, Bulock JW, Adams SP, Merlia JP, Sanes JR (1989a) Primary sequence of a motor neuron-selective adhesive site in the synaptic basal lamina protein S-laminin. Cell 59:905-913.
20. Hunter DD, Shah V, Merlie JP, Sanes JR (1989b) A laminin-like adhesive protein concentrated in the synaptic cleft of the neuromuscular junction. Nature 338:229-233.
21. Krause M, Wernig A (1985) The distribution of acetylcholine receptors in the normal and denervated junction of the frog. J Neurocytol 14:765-780.
22. Lichtman JW (1980) On the predominantly single innervation of submandibular ganglion cells in the rat. J Physiol (Lond) 302:121-130.
23. Lichtman JW (1995) Synapse disassembly at the neuromuscular junction. Semin Dev Biol 6:195-206.
24. Lichtman JW, Magrassi L, Purves D (1987) Visualization of neuromuscular junctions over periods of several months in living mice. J Neurosci 7:1215-1222.
25. Lingle CJ, Steinbach JH (1988) Neuromuscular blocking agents. Int Anesthesiol Clin 26:288-301.
26. MacArdle JJ (1975) Complex end-plate potentials at the regenerating neuromuscular junction of the rat. Exp Neurol 49:629-638.
27. Miner JH, Lewis RM, Sanes JR (1995) Molecular cloning of a novel laminin chain, alpha 5, and widespread expression in adult mouse tissues. J Biol Chem 270:28523-28526.
28. Missias AC, Chu GC, Klocke BJ, Sanes JR, Merlie JP (1996) Maturation of the acetylcholine receptor in skeletal muscle: regulation of the AChR gamma-to-epsilon switch. Dev Biol 179:223-238.
29. Noakes PG, Gautam M, Mudd J, Sanes JR, Merlie JP (1995) Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/ laminin beta 2. Nature 374:258-262.
30. Ohlendieck K, Ervasti JM, Matsumura K, Kahl SD, Leveille CJ, Campbell KP (1991) Dystrophin-related protein is localized to neuromuscular junctions of adult skeletal muscle. Neuron 7:499-508.
31. Peters MF, Kramarcy NR, Sealock R, Froehner SC (1994) Beta-2-syntrophin: localization at the neuromuscular junction in skeletal muscle. NcuroReport 5:1577-1580.
32. Phillips WD, Kopta C, Blount P, Gardner PD, Steinbach JH, Merlie JP (1991) ACh receptor-rich membrane domains organized in fibroblasts by recombinant 43-kilodalton protein. Science 251:568-570.
33. Phillips WD, Noakes PG, Roberds SL, Campbell KP, Merlie JP (1993) Clustering and immobilization of acetylcholine receptors by the 43 kDa protein: a possible role for Dystrophin-related protein. J Cell Biol 123:729-740.
34. Qu Z, Moritz E, Huganir RL (1990) Regulation of tyrosine phosphorylation of the nicotinic acetylcholine receptor at the rat neuromuscular junction. Neuron 2:367-378.
35. Qu Z, Doherty C, Hoffman P, Huganir RL (1994) Regulation of tyrosine phosphorylation of the nicotinic acetylcholine receptor by the postsynaptic 43k protein. Neuroscience Abstr 20:841.
36. Redfern PA (1970) Neuromuscular transmission in new-born rats. J Physiol (Lond) 209:701-709.
37. Rich MM, Lichtman JW (1989a) In Vivo visualization of presynaptic and postsynaptic changes during synapse elimination in reinnervated mouse muscle. J Neurosci 9:1781-1805.
38. Rich MM, Lichtman JW (1989b) Motor nerve terminal loss from degenerating muscle fibers. Neuron 3:677-688.
39. Scott LJC, Bacou F, Sanes JR (1988) A synapse-specific carbohydrate at the neuromuscular junction: association with both acetylcholinesterase and a glycolipid. J Neurosci 8:932-944.
40. Sealock R, Butler MH, Kramarcy NR, Gao KX, Murnane AA, Douville K, Froehner SC (1991) Localization of dystrophin relative to acetylcholine receptor domains in electric tissue and adult and cultured skeletal muscle. J Cell Biol 113:1133-1144.
41. Son YJ, Thompson WJ (1995a) Schwann cell processes guide regeneration of peripheral axons. Neuron 14:125-132.
42. Son YJ, Thompson WJ (1995b) Nerve sprouting in muscle is induced and guided by processes extended by Schwann cells. Neuron 14:133-141.
43. Trachtenberg JT, Thompson WJ (1997) Nerve terminal withdrawal from rat neuromuscular junctions induced by neuregulin and Schwann cells. Neuroscience 17:6243-6255.
44. Turney SG, Culican SM, Lichtman JW (1996) A quantitative fluorescence-imaging technique for studying acetylcholine receptor turnover at neuromuscular junctions in living animals. J Neurosci Methods 64:199-208.
45. van Mier P, Balice-Gordon R, Lichtman J (1994) Synaptic plasticity studied in vivo using vital dyes, lasers, and computer-assisted fluorescence microscopy. Neuroprotocols 5:91-101.
46. Wallace BG, Qu Z, Huganir RL (1991) Agrin induces phosphorylation of the nicotinic acetylcholine receptor. Neuron 6:869-878.
47. Werle MJ, Sojka AM (1996) Antiagrin staining is absent at abandoned synaptic sites of frog neuromuscular junctions. J Neurobiol 30:293-302.
48. Wigston D (1989) Remodeling of neuromuscular junctions in adult mouse soleus. J Neurosci 9:639-647.
49. Woolf CJ, Reynolds ML, Chong MS, Emson P, Irwin N, Benowitz LI (1992) Denervation of the motor endplate results in the rapid expression by terminal Schwann cells of the growth-associated protein GAP-43. J Neurosci 12:3999-4010.