Nerve terminal growth remodels neuromuscular synapses in mice following regeneration of the postsynaptic muscle fiber

Journal of Neuroscience

Volumn 31, Issue 37, 2011, Pages 13191-13203

  Li, Yue ^a   Thompson, Wesley J ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINERGIC RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GLIA CELL; LASER; MALE; MOTONEURON; MOUSE; MUSCLE CELL; MUSCLE REGENERATION; NERVE ENDING; NERVE GROWTH; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; STERNOCLEIDOMASTOID MUSCLE;

ANIMALS; FEMALE; LASERS, GAS; MALE; MICE; MICE, INBRED C57BL; MOTOR NEURONS; MUSCLE, STRIATED; NERVE ENDINGS; NEUROGLIA; NEUROMUSCULAR JUNCTION; RECEPTORS, CHOLINERGIC; REGENERATION; SYNAPSES;

EID: 80052930004     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2953-11.2011     Document Type: Article

References (45)

1. Akaaboune M, Culican SM, Turney SG, Lichtman JW (1999) Rapid and reversible effects of activity on acetylcholine receptor density at the neu-romuscular junction in vivo. Science 286:503-507.
2. Balice-Gordon RJ, Lichtman JW (1994) Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372:519-524.
3. Balice-Gordon RJ, Breedlove SM, Bernstein S, Lichtman JW (1990) Neuro-muscular junctions shrink and expandasmuscle fiber size ismanipulated: in vivo observations in the androgen-sensitive bulbocavernosus muscle of mice. J Neurosci 10:2660-2671.
4. Brooks SV, Faulkner JA (1990) Contraction-induced injury: recovery of skeletal muscles in young and old mice. Am J Physiol 258:C436-C442.
5. Burden SJ, Sargent PB, McMahan UJ (1979) Acetylcholine receptors in regenerating muscle accumulate at original synaptic sites in the absence of the nerve. J Cell Biol 82:412-425.
6. Carlson BM (1973) The regeneration of skeletal muscle. A review. Am J Anat 137:119-149.
7. Couteaux R, Mira JC, d'Albis A (1988) Regeneration of muscles after car-diotoxin injury. I. Cytological aspects. Biol Cell 62:171-182.
8. Duchen LW, Excell BJ, Patel R, SmithB (1974) Changesin motor end-plates resulting from muscle fibre necrosis and regeneration. A light and electron microscopic study of the effects of the depolarizing fraction (cardio-toxin) of Dendroaspis jamesoni venom. J Neurol Sci 21:391-417.
9. Dunaevsky A, Connor EA (1995) Long-term maintenance of presynaptic function in the absence of target muscle fibers. J Neurosci 15:6137-6144.
10. Dunaevsky A, Connor EA (1998) Stability of frog motor nerve terminals in the absence of target muscle fibers. Dev Biol 194:61-71.
11. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51.
12. Gatchalian CL, Schachner M, Sanes JR (1989) Fibroblasts that proliferate near denervated synaptic sites in skeletal muscle synthesize the adhesive molecules tenascin(J1), N-CAM, fibronectin, and a heparan sulfate pro-teoglycan. J Cell Biol 108:1873-1890.
13. 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, Notechis scutatus scutatus. Clin Exp Pharmacol Physiol 5:587-600.
14. JenningsC (1994) Developmental neurobiology. Deathofasynapse. Nature 372:498-499.
15. Jirmanová I (1975) Ultrastructure of motor end-plates during pharmacologically-induced degeneration and subsequent regeneration of skeletal muscle. J Neurocytol 4:141-155.
16. Jones KH, Senft JA (1985) An improved method to determine cell viability by simultaneous staining with fluorescein diacetate-propidium iodide. J Histochem Cytochem 33:77-79.
17. Kang H, Tian L, Thompson W (2003) Terminal Schwann cells guide the reinnervation of muscle after nerve injury. J Neurocytol 32:975-985.
18. Kummer TT, Misgeld T, Lichtman JW, Sanes JR (2004) Nerve-independent formation of a topologically complex postsynaptic apparatus. J Cell Biol 164:1077-1087.
19. Le Grand F, Rudnicki MA (2007) Skeletal muscle satellite cells and adult myogenesis. Curr Opin Cell Biol 19:628-633.
20. Letinsky MS, Fischbeck KH, McMahan UJ (1976) Precision of reinnerva-tionoforiginal postsynaptic sitesin frog muscle afteranerve crush. JNeu-rocytol 5:691-718.
21. Lichtman JW, Magrassi L, Purves D (1987) Visualization of neuromuscular junctions over periods of several months in living mice. J Neurosci 7:1215-1222.
22. Liley AW (1956) An investigation of spontaneous activity at the neuromus-cular junction of the rat. J Physiol 132:650-666.
23. Lingle CJ, Steinbach JH (1988) Neuromuscular blocking agents. Int Anes-thesiol Clin 26:288-301.
24. Love FM, Thompson WJ (1998) Schwann cells proliferate at rat neuromus-cular junctions during development and regeneration. J Neurosci 18:9376-9385.
25. Lyons PR, Slater CR (1991) Structure and function of the neuromuscular junction in young adult mdx mice. J Neurocytol 20:969-981.
26. Magrassi L, Purves D, Lichtman JW (1987) Fluorescent probes that stain living nerve terminals. J Neurosci 7:1207-1214.
27. Marques MJ, Mendes ZT, Minatel E, Santo Neto H (2005) Acetylcholine receptors and nerve terminal distribution at the neuromuscular junction of long-term regenerated muscle fibers. J Neurocytol 34:387-396.
28. Marshall LM, Sanes JR, McMahan UJ (1977) Reinnervation of original syn-aptic sites on muscle fiber basement membrane after disruption of the muscle cells. Proc Natl Acad Sci U S A 74:3073-3077.
29. McCann CM, Nguyen QT, Santo Neto H, Lichtman JW (2007) Rapid synapse elimination after postsynaptic protein synthesis inhibition in vivo. J Neurosci 27:6064-6067.
30. McMahan UJ, Slater CR (1984) The influence of basal lamina on the accumulation of acetylcholine receptors at synaptic sites in regenerating muscle. J Cell Biol 98:1453-1473.
31. McMahan UJ, Sanes JR, Marshall LM (1978) Cholinesterase is associated with the basal lamina at the neuromuscular junction. Nature 271:172-174.
32. Misgeld T, Kummer TT, Lichtman JW, Sanes JR (2005) Agrin promotes synaptic differentiation by counteracting an inhibitory effect of neu-rotransmitter. Proc Natl Acad Sci U S A 102:11088-11093.
33. Papadimitriou JM, Robertson TA, Mitchell CA, Grounds MD (1990) The process of new plasmalemma formation in focally injured skeletal muscle fibers. J Struct Biol 103:124-134.
34. Peng HB, Xie H, Rossi SG, Rotundo RL (1999) Acetylcholinesterase clustering at the neuromuscular junction involves perlecan and dystroglycan. J Cell Biol 145:911-921.
35. Ribchester RR (2009) Mammalian neuromuscular junctions: modern tools to monitor synaptic form and function. Curr Opin Pharmacol 9:297-305.
36. Rich M, Lichtman JW (1989a) Motor nerve terminal loss from degenerating muscle fibers. Neuron 3:677-688.
37. Rich MM, Lichtman JW (1989b) In vivo visualization of pre- and postsyn-aptic changes during synapse elimination in reinnervated mouse muscle. J Neurosci 9:1781-1805.
38. Sanes JR, Lichtman JW (2001) Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2:791-805.
39. Slater CR, Allen EG (1985) Acetylcholine receptor distribution on regenerating mammalian muscle fibers at sites of mature and developing nerve-muscle junctions. J Physiol (Paris) 80:238-246.
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. Valdez G, Tapia JC, Kang H, Clemenson GD Jr, Gage FH, Lichtman JW, Sanes JR (2010) Attenuation of age-related changes in mouse neuromuscular synapses by caloric restriction and exercise. Proc Natl Acad Sci U S A 107:14863-14868.
42. van Mier P, Lichtman JW (1994) Regenerating muscle fibers induce directional sprouting from nearby nerve terminals: studies in living mice. J Neurosci 14:5672-5686.
43. Wernig A, Pécot-Dechavassine M, Stöver H (1980) Sprouting and regres-sionofthe nerveatthe frog neuromuscular junctioninnormal conditions and after prolonged paralysis with curare. J Neurocytol 9:277-303.
44. Yao YM (1988) Maintenance of axon terminals at synaptic sites in the absence of muscle fibers. In: Current issues in neural regeneration research (Reier PJ, Bunge RP, Seil FJ, eds), pp 167-178. New York: Alan R. Liss.
45. Zuo Y, Lubischer JL, Kang H, Tian L, Mikesh M, Marks A, Scofield VL, Maika S, Newman C, Krieg P, Thompson WJ (2004) Fluorescent proteins expressed in mouse transgenic lines mark subsets of glia, neurons, macrophages, and dendritic cells for vital examination. J Neurosci 24:10999-11009.