Terminal Schwann cells participate in the competition underlying neuromuscular synapse elimination

Journal of Neuroscience

Volumn 33, Issue 45, 2013, Pages 17724-17736

  Smith, Ian W ^a   Mikesh, Michelle ^b   Lee, Young Il ^a   Thompson, Wesley J ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINERGIC RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ELECTRON MICROSCOPY; FLUORESCENCE MICROSCOPY; GLIA CELL; MOTONEURON; MOUSE; MUSCLE CELL; NERVE CELL DIFFERENTIATION; NERVE FIBER; NEUROMUSCULAR SYNAPSE ELIMINATION; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; SCHWANN CELL; SYNAPTIC TRANSMISSION; SYNAPTOSOME;

ANIMALS; AXONS; MICE; NEUROMUSCULAR JUNCTION; RECEPTORS, CHOLINERGIC; SCHWANN CELLS;

EID: 84887105788     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3339-13.2013     Document Type: Article

References (43)

1. Awasaki T, Ito K (2004) Engulfing action of glial cells is required for programmed axon pruning during Drosophila metamorphosis. Curr Biol 14:668-677. CrossRef Medline
2. Balice-Gordon RJ, Lichtman JW (1993) In vivo observations of pre- and postsynaptic changes during the transition from multiple to single innervation at developing neuromuscular junctions. J Neurosci 13:834-855. Medline
3. Balice-Gordon RJ, Lichtman JW (1994) Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372:519-524. CrossRef Medline
4. Bishop DL, Misgeld T, Walsh MK, Gan WB, Lichtman JW (2004) Axon branch removal at developing synapses by axosome shedding. Neuron 44:651-661. CrossRef Medline
5. Bixby JL (1981) Ultrastructural observations on synapse elimination in neonatal rabbit skeletal muscle. J Neurocytol 10:81-100. CrossRef Medline
6. Brill MS, Lichtman JW, Thompson W, Zuo Y, Misgeld T (2011) Spatial constraints dictate glial territories at murine neuromuscular junctions. J Cell Biol 195:293-305. CrossRef Medline
7. Brown MC, Jansen JK, Van Essen D (1976) Polyneuronal innervation of skeletal muscle in new-born rats and its elimination during maturation. J Physiol 261:387-422. Medline
8. Buffelli M, Burgess RW, Feng G, Lobe CG, Lichtman JW, Sanes JR (2003) Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition. Nature 424:430-434. CrossRef Medline
9. Culican SM, Nelson CC, Lichtman JW (1998) Axon withdrawal during synapse elimination at the neuromuscular junction is accompanied by disassembly of the postsynaptic specialization and withdrawal of Schwann cell processes. J Neurosci 18:4953-4965. Medline
10. Fiala JC (2005) Reconstruct: a free editor for serial section microscopy. J Microsc 218:52-61. CrossRef Medline
11. Fuentes-Medel Y, Logan MA, Ashley J, Ataman B, Budnik V, Freeman MR (2009) Glia and muscle sculpt neuromuscular arbors by engulfing destabilized synaptic boutons and shed presynaptic debris. PLoS Biol 7:e1000184. CrossRef Medline
12. Hayworth CR, Moody SE, Chodosh LA, Krieg P, Rimer M, Thompson WJ (2006) Induction of neuregulin signaling in mouse Schwann cells in vivo mimics responses to denervation. J Neurosci 26:6873-6884. CrossRef Medline
13. Jirmanová I, Thesleff S (1972) Ultrastructural study of experimental muscle degeneration and regeneration in the adult rat. Z Zellforsch Mikrosk Anat 131:77-97. CrossRef Medline
14. Kang H, Tian L, Son YJ, Zuo Y, Procaccino D, Love F, Hayworth C, Trachtenberg J, Mikesh M, Sutton L, Ponomareva O, Mignone J, Enikolopov G, Rimer M, Thompson W (2007) Regulation of the intermediate filament protein nestin at rodent neuromuscular junctions by innervation and activity. J Neurosci 27:5948-5957. CrossRef Medline
15. Kasthuri N, Lichtman JW (2003) The role of neuronal identity in synaptic competition. Nature 424:426-430. CrossRef Medline
16. Keller-Peck CR, Walsh MK, Gan WB, Feng G, Sanes JR, Lichtman JW (2001) Asynchronous synapse elimination in neonatal motor units: studies using GFP transgenic mice. Neuron 31:381-394. CrossRef Medline
17. Kelly AM, Zacks SI (1969) The fine structure of motor endplate morphogenesis. J Cell Biol 42:154-169. CrossRef Medline
18. Korneliussen H, Jansen JK (1976) Morphological aspects of the elimination of polyneuronal innervation of skeletal muscle fibres in newborn rats. J Neurocytol 5:591-604. CrossRef Medline
19. Kummer TT, Misgeld T, Lichtman JW, Sanes JR (2004) Nerve-independent formation of a topologically complex postsynaptic apparatus. J Cell Biol 164:1077-1087. CrossRef Medline
20. Lee YI, Mikesh M, Smith I, Rimer M, Thompson W (2011) Muscles in a mouse model of spinal muscular atrophy show profound defects in neuromuscular development even in the absence of failure in neuromuscular transmission or loss of motor neurons. Dev Biol 356:432-444. CrossRef Medline
21. Love FM, Thompson WJ (1998) Schwann cells proliferate at rat neuromuscular junctions during development and regeneration. J Neurosci 18: 9376-9385. Medline
22. Marques MJ, Conchello JA, Lichtman JW (2000) From plaque to pretzel: fold formation and acetylcholine receptor loss at the developing neuromuscular junction. J Neurosci 20:3663-3675. Medline
23. Matthews-Bellinger JA, Salpeter MM (1983) Fine structural distribution of acetylcholine receptors at developing mouse neuromuscular junctions. J Neurosci 3:644-657. Medline
24. Miledi R, Slater CR (1970) On the degeneration of rat neuromuscular junctions after nerve section. J Physiol 207:507-528. Medline
25. Njå A, Purves D (1978) The effects of nerve growth factor and its antiserum on synapses in the superior cervical ganglion of the guinea-pig. J Physiol 277:53-75. Medline
26. Ontell M, Bourke D, Hughes D (1988) Cytoarchitecture of the fetal murine soleus muscle. Am J Anat 181:267-278. CrossRef Medline
27. Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, Giustetto M, Ferreira TA, Guiducci E, Dumas L, Ragozzino D, Gross CT (2011) Synaptic pruning by microglia is necessary for normal brain development. Science 333:1456-1458. CrossRef Medline
28. Peters A, Muir AR (1959) The relationship between axons and Schwann cells during development of peripheral nerves in the rat. J Exp Physiol 44:117-130. Medline
29. Reddy LV, Koirala S, Sugiura Y, Herrera AA, Ko CP (2003) Glial cells maintain synaptic structure and function and promote development of the neuromuscular junction in vivo. Neuron 40:563-580. CrossRef Medline
30. Riley DA (1977) Spontaneous elimination of nerve terminals from the endplates of developing skeletal myofibers. Brain Res 134:279-285. CrossRef Medline
31. Riley DA (1981) Ultrastructural evidence for axon retraction during the spontaneous elimination of polyneuronal innervation of the rat soleus muscle. J Neurocytol 10:425-440. CrossRef Medline
32. Ronnevi LO (1978) Origin of the glial processes responsible for the spontaneous postnatal phagocytosis of boutons on cat spinal motoneurons. Cell Tissue Res 189:203-217. Medline
33. Rosenthal JL, Taraskevich PS (1977) Reduction of multiaxonal innervation at the neuromuscular junction of the rat during development. J Physiol 270:299-310. Medline
34. Sanes JR, Lichtman JW (2001) Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2:791-805. CrossRef Medline
35. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B (2012) Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74:691-705. CrossRef Medline
36. Slater CR (1982) Postnatal maturation of nerve-muscle junctions in hindlimb muscles of the mouse. Dev Biol 94:11-22. CrossRef Medline
37. Song JW, Misgeld T, Kang H, Knecht S, Lu J, Cao Y, Cotman SL, Bishop DL, Lichtman JW (2008) Lysosomal activity associated with developmental axon pruning. J Neurosci 28:8993-9001. CrossRef Medline
38. Tapia JC, Wylie JD, Kasthuri N, Hayworth KJ, Schalek R, Berger DR, Guatimosim C, Seung HS, Lichtman JW (2012) Pervasive synaptic branch removal in the mammalian neuromuscular system at birth. Neuron 74: 816-829. CrossRef Medline
39. Teräväinen H (1968) Development of the myoneural junction in the rat. Z Zellforsch 87:249-265. CrossRef Medline
40. Turney SG, Lichtman JW (2012) Reversing the outcome of synapse elimination at developing neuromuscular junctions in vivo: evidence for synaptic competition and its mechanism. PLoS Biol 10:e1001352. CrossRef Medline
41. Walsh MK, Lichtman JW (2003) In vivo time-lapse imaging of synaptic takeover associated with naturally occurring synapse elimination. Neuron 37:67-73. CrossRef Medline
42. Watts RJ, Schuldiner O, Perrino J, Larsen C, Luo L (2004) Glia engulf degenerating axons during developmental axon pruning. Curr Biol 14:678-684. CrossRef Medline
43. Wolpowitz D, Mason TB, Dietrich P, Mendelsohn M, Talmage DA, Role LW (2000) Cysteine-rich domain isoforms of the neuregulin-1 gene are required for maintenance of peripheral synapses. Neuron 25:79-91. CrossRef Medline