Development of the vertebrate neuromuscular junction

Annual Review of Neuroscience

Volumn 22, Issue , 1999, Pages 389-442

  Sanes, Joshua R ^a   Lichtman, Jeff W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acetylcholine receptor; Regeneration; Synapse elimination; Synapse formation; Synapse maintenance

Indexed keywords

CHOLINERGIC RECEPTOR;

EMBRYO; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTOGENESIS; VERTEBRATE;

ANIMALS; GLYCOPROTEINS; NERVE REGENERATION; NEUREGULINS; NEUROMUSCULAR JUNCTION; PRESYNAPTIC TERMINALS; SIGNAL TRANSDUCTION; SYNAPSES; TRANSCRIPTION, GENETIC; VERTEBRATES;

EID: 0032936983     PISSN: 0147006X     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.neuro.22.1.389     Document Type: Review

References (400)

1. Adams L, Goldman D. 1998. A role for calcium from the sarcoplasmic reticulum in coupling muscle activity to nicotonic acetylcholine receptor gene expression in rat. J. Neurobiol. 35:245-57
2. Aframian D, Grinnell AD. 1988. Destabilization of junctional ACh receptors by a reinnervating frog motor nerve. Puerto Rico Health Sci. J. 7:80-86
3. Altiok N, Altiok S, Changeux JP. 1997. Heregulin-stimulated acetylcholine receptor gene expression in muscle: requirement for MAP kinase and evidence for a parallel inhibitory pathway independent of electrical activity. EMBO J. 16:717-25
4. Altiok N, Bessereau JL, Changeux, JP. 1995. ErbB3 and ErbB2/neu mediate the effect of heregulin on acetylcholine receptor gene expression in muscle: differential expression at the endplate. EMBO J. 14:4258-66
5. Anderson MJ, Cohen MW. 1977. Nerve-induced and spontaneous redistribution of acetylcholine receptors on cultured muscle cells. J. Physiol. 268:757-73
6. Antony C, Huchet M, Changeux JP, Cartaud J. 1995. Developmental regulation of membrane traffic organization during synaptogenesis in mouse diaphragm muscle. J. Cell Biol. 130:959-68
7. Apel Ed, Glass DJ, Moscoso LM, Yancopoulos GD, Sanes JR. 1997. Rapsyn is required for MuSK signaling and recruits synaptic components to a MuSK-containing scaffold. Neuron 18:623-35
8. Apel ED, Roberds SL, Campbell KP, Merlie JP. 1995. Rapsyn may function as a link between the acetylcholine receptor and the agrin-binding dystrophin-associated glycoprotein complex. Neuron 15:115-26
9. Arce V, Pollock RA, Phillippe JM, Pennica D, Henderson CE, deLapeyriere O. 1998. Synergistic effects of Schwann-derived and muscle-derived factors on motoneuron survival involve glial cell line-derived neurotrophic factor (GDNF) and cardiotrophin (CT-1). J. Neurosci. 18:1-9
10. Astrow SH, Pitaevski V, Herrera AA. 1996. Precision of reinnervation and synaptic remodeling observed in neuromuscular junctions of living frogs. J. Neurosci. 16:5130-40
11. Balice-Gordon RJ, Breedlove SM, Bernstein S, Lichtman JW. 1990. Neuromuscular junctions shrink and expand as muscle fiber size is manipulated: in vivo observations in the androgen-sensitive bulbocavernosus muscle of mice. J. Neurosci. 10:2660-71
12. Balice-Gordon RJ, Chua CK, Nelson CC, Lichtman JW. 1993. Gradual loss of synaptic cartels precedes axon withdrawal at developing neuromuscular junctions. Neuron 11:801-15
13. Balice-Gordon RJ, Lichtman JW. 1990. In vivo visualization of the growth of pre- and postsynaptic elements of neuromuscular junctions in the mouse. J. Neurosci. 10:894-908
14. 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. 13:834-55
15. Balice-Gordon RJ, Lichtman JW. 1994. Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372:519-24
16. Balice-Gordon RJ, Thompson WJ. 1988. Synaptic rearrangements and alterations in motor unit properties in neonatal rat extensor digitorum longus muscle. J. Physiol. 398:191-210
17. Barker D, Ip MC. 1966. Sprouting and degeneration of mammalian motor axons in normal and de-afferentated skeletal muscle. Proc. R. Soc. Lond. (Biol.) 163:538-54
18. Barry JA, Ribchester RR. 1995. Persistent polyneuronal innervation in partially denervated rat muscle after reinnervation and recovery from prolonged nerve conduction block. J. Neurosci. 15:6327-39
19. Bennett MR, Pettigrew AG. 1976. The formation of neuromuscular synapses. Cold Spring Harbor Symp. Quart. Biol. 40:409-24
20. Bennett MR, Lavidis NA. 1984. Development of the topographical projection of motor neurons to a rat muscle accompanies loss of polyneuronal innervation. J. Neurosci. 4:2204-12
21. Bennett M, Ho S. 1988. The formation of topographical maps in developing rat gastrocnemius muscle during synapse elimination. J. Physiol. 396:471-96
22. Bessereau J-L, Laudenbach V, Le Poupon C, Changeux J-P. 1998. Nonmyogenic factors bind nicotinic acetylcholine receptor promoter elements required for response to denervation. J. Biol. Chem. 273:12786-93
23. Betz WJ, Ribchester RR, Ridge RM. 1990. Competitive mechanisms underlying synapse elimination in the lumbrical muscle of the rat. J. Neurobiol. 21:1-17
24. Bevan S, Steinbach JH. 1977. The distribution of a α-bungarotoxin binding sites on mammalian skeletal muscle developing in vivo. J. Physiol. 267:195-213
25. Bewick GS, Young C, Slater CR. 1996. Spatial relationships of utrophin, dystrophin, β-dystroglycan and β-spectrin to acetylcholine receptor clusters during postnatal maturation of the rat neuromuscular junction. J. Neurocytol. 25:367-79
26. Biroc SL, Payan DG, Fisher JM. 1993. Isoforms of agrin are widely expressed in the developing rat and may function as protease inhibitors. Dev. Brain Res. 75:119-29
27. Bixby JL. 1981. Ultrastructural observations on synapse elimination in neonatal rabbit skeletal muscle. Neurocytol. 10:81-100
28. Bloch RJ, Steinbach JH, Merlie JP, Heinemann S. 1986. Collagenase digestion alters the organization and turnover of junctional acetylcholine receptors. Neurosci. Lett. 66:113-19
29. Boaro SN, Soares JC, Konig B. 1998. Comparative structural analysis of neuromuscular junctions in mice at different ages. Ann. Anat. 180:173-79
30. Bowe MA, Deyst KA, Leszyk JD, Fallon JR. 1994. Identification and purification of an agrin receptor from Torpedo postsynaptic membranes: a heteromeric complex related to the dystroglycans. Neuron 12:1173-80
31. Bowe MA, Fallon JR. 1995. The role of agrin in synapse formation. Annu. Rev. Neurosci. 18:443-62
32. Bowen DC, Sugiyama J, Ferns M, Hall ZW. 1996. Neural agrin activates a high-affinity receptor in C2 muscle cells that is unresponsive to muscle agrin. J. Neurosci. 16:3791-97
33. Brand-Saberi B, Wilting J, Ebebsperger C, Christ B. 1996. The formation of somite compartments in the avian embryo. Int. J. Dev. Biol. 40:411-20
34. Brenner HR, Herczeg A, Slater CR. 1992. Synapse-specific expression of acetylcholine receptor genes and their products at original synaptic sites in rat soleus muscle fibres regenerating in the absence of innervation. Development 116:41-53
35. Brown MC, Booth CM. 1983. Postnatal development of the adult pattern of motor axon distribution in rat muscle. Nature 304:741-42
36. Brown MC, Holland RL, Hopkins WG. 1981. Motor nerve sprouting. Annu. Rev. Neurosci. 4:17-42
37. 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
38. Buchanan J, Sun YA, Poo MD. 1989. Studies of nerve-muscle interactions in Xenopus cell culture: fine structure of early functional contacts. J. Neurosci. 9:1540-54
39. Burden S. 1977. Development of the neuromuscular junction in the chick embryo: the number, distribution, and stability of acetylcholine receptors. Dev. Biol. 57:317-29
40. Burden SJ, DePalma RL, Gottesman GS. 1983. Crosslinking of proteins in acetylcholine receptor-rich membranes: associated between the β-subunit and the 43 kd subsynaptic protein. Cell 35:687-92
41. 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. 82:412-25
42. Burgess RW, Nguyen Q, Lichtman JW, Sanes JR. 1998. A genetic analysis of agrin. Neurosci. Abstr. 24:1534
43. Cajal S, Ramon Y. 1928. Reprinted 1991. Degeneration and Regeneration of the Nervous System. London: Oxford Univ. Press
44. Calakos N, Scheller RH. 1996. Synaptic vesicle biogenesis, docking, and fusion: a molecular description. Physiol. Rev. 76:1-29
45. Callaway EM, Soha JM, Van Essen DC. 1989. Differential loss of neuromuscular connections according to activity level and spinal position of neonatal rabbit soleus motor neurons. J. Neurosci. 9:1806-24
46. Campagna JA, Prevette D, Oppenheim RW, Bixby JL. 1997a. Target contact regulates expression of synaptotagmin genes in spinal motor neurons in vivo. Mol. Cell. Neurosci. 8:377-88
47. Campagna JA, Ruegg MA, Bixby JL. 1995. Agrin is a differentiation-inducing "stop signal" for motoneurons in vitro. Neuron 15:1365-74
48. Campagna JA, Ruegg MA, Bixby JL. 1997b. Evidence that agrin directly influences presynaptic differentiation at neuromuscular junctions in vitro. Eur J. Neurosci. 9:2269-83
49. Campanelli JT, Gayer GG, Scheller RH. 1996. Alternative RNA splicing that determines agrin activity regulates binding to heparin and α-dystroglycan. Development 122:1663-72
50. Campanelli JT, Roberds SL, Campbell KP, Scheller RH. 1994. A role for dystrophin-associated glycoproteins and utrophin in agrin-induced AChR clustering. Cell 77:663-74
51. Cardasis CA, Padykula HA. 1981. Ultrastructural evidence indicating reorganization at the neuromuscular junction in the normal rat soleus muscle. Anat. Rec. 200:41-59
52. Caroni P. 1997. Intrinsic neuronal determinants that promote axonal sprouting and elongation. BioEssays 19:767-75
53. Caroni P, Aigner L, Schneider C. 1997. Intrinsic neuronal determinants locally regulate extrasynaptic and synaptic growth at the adult neuromuscular junction. J. Cell Biol. 136:679-92
54. Caroni P, Becker M. 1992. The downregulation of growth-associated proteins in motoneurons at the onset of synapse elimination is controlled by muscle activity and IGF-1. J. Neurosci. 12:3849-61
55. Caroni P, Rotzler S, Britt JC, Brenner HR. 1993. Calcium influx and protein phosphorylation mediate the metabolic stabilization of synaptic acetylcholine receptors in muscle. J. Neurosci. 13:1315-25
56. Caroni P, Schneider C. 1994. Signaling by insulin-like growth factors in paralyzed skeletal muscle: rapid induction of IGF-1 expression in muscle fibers and prevention of interstitial cell proliferation by IGF-BP5 and IGF-BP4. J. Neurosci. 14:3378-88
57. Caroni P, Schneider C, Kiefer MC, Zapf J. 1994. Role of muscle insulin-like growth factors in nerve sprouting: suppression of terminal sprouting in paralyzed muscle by IGF-binding protein 4. J. Cell Biol. 125:893-902
58. Chahine KG, Walker W, Goldman D. 1992. A 102 base pair sequence of the nicotinic acetylcholine receptor delta-subunit gene confers regulation by muscle electrical activity. Development 115:213-19
59. Chang D, Woo JS, Campanelli J, Scheller RH, Ignatius MJ. 1997. Agrin inhibits neurite outgrowth but promotes attachment of embryonic motor and sensory neurons. Dev. Biol. 181:21-35
60. Changeux JP, Duclert A, Sekine S. 1992. Calcitonin gene-related peptides and neuromuscular interactions. Ann. NY Acad. Sci. 657:361-78
61. Chen L, Ko CP. 1994. Extension of synaptic extracellular matrix during nerve terminal sprouting in living frog neuromuscular junctions. J. Neurosci. 14:796-808
62. Chen LL, Folsom DB, Ko CP. 1991. The remodeling of synaptic extracellular matrix and its dynamic relationship with nerve terminals at living frog neuromuscular junctions. J. Neurosci. 11:2920-30
63. Chiu AY, Sanes JR. 1984. Development of basal lamina in synaptic and extrasynaptic portions of embryonic rat muscle. Dev. Biol. 103:456-67
64. Chow I, Poo MM. 1985. Release of acetylcholine from embryonic neurons upon contact with muscle cell. J. Neurosci. 5:1076-82
65. Chu GC, Moscoso LM, Sliwkowski MX, Merlie JP. 1995. Regulation of the acetylcholine receptor ε subunit gene by recombinant ARIA: an in vitro model for transynaptic gene regulation. Neuron 14:329-39
66. Cohen I, Rimer M, Lomo T, McMahan UJ. 1997. Agrin-induced postsynaptic-like apparatus in skeletal muscle fibers in vivo. Mol. Cell. Neurosci. 9:237-53
67. Cohen MW, Godfrey EW. 1992. Early appearance of and neuronal contribution to agrin-like molecules at embryonic frog nerve-muscle synapses formed in culture. J. Neurosci. 12:2982-92
68. Colman H, Lichtman JW. 1993. Interactions between nerve and muscle: synapse elimination at the developing neuromuscular junction. Dev. Biol. 156:1-10
69. Colman H, Nabekura J, Lichtman JW. 1997. Alterations in synaptic strength preceding axon withdrawal. Science 275:356-61
70. Connold AL, Evers JV, Vrbova G. 1986. Effect of low calcium and protease inhibitors on synapse elimination during postnatal development in the rat soleus muscle. Brain Res. 393:99-107
71. Connor EA. 1997. Developmental regulation of interstitial cell density in bullfrog skeletal muscle. J. Neurocytol. 26:23-32
72. Connor EA, McMahan UJ. 1987. Cell accumulation in the junctional region of denervated muscle. J. Cell Biol. 104:109-20
73. Courtney J, Steinbach JH. 1981. Age changes in neuromuscular junction morphology and acetylcholine receptor distribution on rat skeletal muscle fibres. J. Physiol. 320:435-47
74. Couteaux R. 1973. Motor endplate structure. In Structure and Function of Muscle, Vol. 2, ed. GH Bourne, pp. 483-530. New York: Academic
75. Covault J, Sanes JR. 1985. Neural cell adhesion molecule (N-CAM) accumulates in denervated and paralyzed skeletal muscles. Proc. Natl. Acad. Sci. USA 82:4544-48
76. Covault J, Sanes JR. 1986. Distribution of N-CAM in synaptic and extrasynaptic portions of developing and adult skeletal muscle. J. Cell Biol. 102:716-30
77. 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. 18:4953-65
78. Daggett DF, Cohen MW, Stone D, Nikolics K, Rauvala H, Peng HB. 1996. The role of an agrin-growth factor interaction in acetylcholine receptor clustering. Mol. Cell. Neurosci. 8:272-85
79. Dai Z, Peng HB. 1993. Elevation in presynaptic Ca++ level accompanying initial nervemuscle contact in tissue culture. Neuron 10:827-37
80. Dai Z, Peng HB. 1995. Presynaptic differentiation induced in cultured neurons by local application of basic fibroblast growth factor. J. Neurosci. 15:5466-75
81. Dai Z, Peng HB. 1996. From neurite to nerve terminal: induction of presynaptic differentiation by target-derived signals. Semin. Neurosci. 8:97-106
82. Dai Z, Peng HB. 1998. A role of tyrosine phosphatase in acetylcholine receptor cluster dispersal and formation. J. Cell Biol. 141:1613-24
83. Dale HH, Feldberg W, Vogt M. 1936. Release of acetylcholine at voluntary motor nerve endings. J. Physiol. 86:353-80
84. Day NC, Wood SJ, Ince PG, Volsen SG, Smith W, et al. 1997. Differential localization of voltage-dependent calcium channel α1 subunits at the human and rat neuromuscular junction. J. Neurosci. 17:6226-35
85. DeChiara TM, Bowen DC, Valenzuela DM, Simmons MV, Poueymirou WT, et al. 1996. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85:501-12
86. Deconinck AE, Potter AC, Tinsley JM, Wood SJ, Vater R, et al. 1997. Postsynaptic abnormalities at the neuromuscular junctions of utrophin deficient mice. J. Cell Biol. 36:883-94
87. DeKoninck P, Cooper E. 1995. Differential regulation of neuronal nicotinic acetylcholine receptor subunit genes in cultured neonatal rat sympathetic neurons: specific induction of α-7 by membrane depolarization through a Ca2+/calmodulin-dependent kinase pathway. J. Neurosci. 15:7966-78
88. Dennis MJ. 1981. Development of the neuromuscular junction: inductive interactions between cells. Annu. Rev. Neurosci. 4:43-68
89. Denzer AJ, Brandenberger R, Gesemann M, Chiquet M, Ruegg MA. 1997. Agrin binds to the nerve-muscle basal lamina via laminin. J. Cell Biol. 137:671-83
90. Denzer AJ, Gesemann M, Schumacher B, Ruegg MA. 1995. An amino-terminal extension is required for the secretion of chick agrin and its binding to extracellular matrix. J. Cell Biol. 131:1547-60
91. Desaki J, Uehara Y. 1987. Formation and maturation of subneural apparatuses at neuromuscular junctions in postnatal rats: a scanning and transmission electron microscopical study. Dev. Biol. 119:390-401
92. DiMario JX, Stockdale FE. 1997. Both myoblast lineage and innervation determine fiber type and are required for expression of the slow myosin heavy chain 2 gene. Dev. Biol. 188:167-180
93. Donahue SP, English AW. 1989. Selective elimination of cross-compartmental innervation in rat lateral gastrocnemius muscle. J. Neurosci. 9:1621-27
94. Dong Z, Brennan A, Liu N, Yarden Y, Lefkowitz G, et al. 1995. Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron 15:585-96
95. Donoghue MJ, Lewis RM, Merlie JP, Sanes JR. 1996. An eph kinase ligand, AL-1, is expressed by rostral muscles and inhibits outgrowth from caudal neurons. Mol. Cell. Neurosci. 8:185-98
96. Donoghue MJ, Morris-Valero R, Johnson YR, Merlie JP, Sanes JR. 1992. Mammalian muscle cells bear a cell-autonomous, heritable memory of their rostrocaudal position. Cell 69:67-77
97. Donoghue MJ, Sanes JR. 1994. All muscles are not created equal. Trends Genet. 10:396-401
98. Duclert A, Changeux JP. 1995. Acetylcholine receptor gene expression at the developing neuromuscular junction. Physiol. Rev. 75:339-68
99. Duclert A, Savatier N, Schaeffer L, Changeux JP. 1996. Identification of an element crucial for the sub-synaptic expression of the acetylcholine receptor ε-subunit gene. J. Biol. Chem. 271:17433-38
100. Dunaevsky A, Connor EA. 1998. Stability of frog motor nerve terminals in the absence of target muscle fibers. Dev. Biol. 194:61-71
101. Dunia R, Herrera AA. 1993. Synapse formation and elimination during growth of the pectoral muscle in Xenopus laevis. J. Physiol. 469:501-9
102. Duxson MJ, Vrbova G. 1985. Inhibition of acetylcholinesterase accelerates axon terminal withdrawal at the developing rat neuromuscular junction. J. Neurocytol. 14:337-63
103. Eftimie R, Brenner HR, Buonanno A. 1991. Myogenin and MyoD join a family of skeletal muscle genes regulated by electrical activity. Proc. Natl. Acad. Sci. USA 88:1349-53
104. Eisen JS. 1994. Development of motoneuronal phenotype. Annu. Rev. Neurosci. 17:1-30
105. Elizalde A, Huerta M, Stefani E. 1983. Selective reinnervation of twitch and tonic muscle fibres of the frog. J. Physiol. 340:513-24
106. Engel AG. 1994. The neuromuscular junction. In Myology: Basic and Clinical, Vol. 1, ed. AG Engel, C Franzini-Armstrong, pp. 261-302. New York: McGraw-Hill
107. English AW. 1990. Development of compartmentalized innervation of the rat gluteus maximus muscle. J. Comp. Neurol. 301:104-13
108. English AW, Schwartz G. 1995. Both basic fibroblast growth factor and ciliary neurotrophic factor promote the retention of polyneuronal innervation of developing skeletal muscle fibers. Dev. Biol. 169:57-64
109. Evers J, Laser M, Sun YA, Xie ZP, Poo MM. 1989. Studies of nerve-muscle interactions in Xenopus cell culture: analysis of early synaptic currents. J. Neurosci. 9:1523-39
110. Fahim MA. 1989. Rapid neuromuscular remodeling following limb immobilization. Anat. Rec. 224:102-9
111. Fallon JR, Gelfman CE. 1989. Agrin-related molecules are concentrated at acetylcholine receptor clusters in normal and aneural developing muscle. J. Cell Biol. 108:1527-35
112. Falls DL, Rosen KM, Corfas G, Lane WS, Fischbach GD. 1993. ARIA, a protein that stimulates acetylcholine receptor synthesis, is a member of the neu ligand family. Cell 72:801-15
113. Fambrough DM. 1979. Control ofacetylcholine receptors in skeletal muscle. Physiol. Rev. 59:165-227
114. Feng G, Steinbach JH, Sanes JR. 1998. Rapsyn clusters neuronal acetylcholine receptors but is inessential for formation of an interneuronal cholinergic synapse. J. Neurosci. 18:4166-76
115. Ferns MJ, Campanelli JT, Hoch W, Scheller RH, Hall ZW. 1993. The ability of agrin to cluster AChRs depends on alternative splicing and on cell surface proteoglycans. Neuron 11:491-502
116. Ferns M, Hoch W, Campanelli JT, Rupp F, Hall ZW, Scheller RH. 1992. RNA splicing regulates agrin-mediated acetylcholine receptor clustering activity in cultured myotubes. Neuron 8:1079-86
117. Ferns M, Deiner M, Hall Z. 1996. Agrin-induced acetylcholine receptor clustering in mammalian muscle requires tyrosine phosphorylation. J. Cell Biol. 132:937-44
118. Fischbach GD, Rosen KM. 1997. ARIA: A neuromuscular junction neuregulin. Annu. Rev. Neurosci. 20:429-58
119. Fitzsimonds RM, Poo MM. 1998. Retrograde signaling in the development and modification of synapses. Physiol. Rev. 78:143-70
120. Flanagan JG, Vanderhaeghen P. 1998. The ephrins and eph receptors in neural development. Annu. Rev. Neurosci. 21:309-45
121. Flucher BE, Daniels MP. 1989. Distribution of Na+ channels and ankyrin in neuromuscular junctions is complementary to that of acetylcholine receptors and the 43 kd protein. Neuron 3:163-75
122. Fontaine B, Klarsfeld A, Changeux JP. 1987. Calcitonin gene-related peptide and muscle activity regulate acetylcholine receptor α-subunit mRNA levels by distinct intracellular pathways. J. Cell Biol. 105:1337-42
123. Fontaine B, Klarsfeld A, Hokfelt T, Changeux JP. 1986. Calcitonin gene-related peptide, a peptide present in spinal cord motoneurons, increases the number of acetylcholine receptors in primary cultures of chick embryo myotubes. Neurosci. Lett. 71:59-65
124. Frail DE, Mudd J, Shah V, Carr C, Cohen JB, Merlie JP. 1987. cDNAs for the postsynaptic 43-kDa protein of Torpedo electric organ encode two proteins with different carboxy I termini. Proc. Natl. Acad. Sci. USA 84:6302-6
125. Frank E, Fischbach GD. 1979. Early events in neuromuscular junction formation in vitro: induction of acetylcholine receptor clusters in the postsynaptic membrane and morphology of newly formed synapses. J. Cell Biol. 83:143-58
126. Frank E, Gautvik K, Sommerschild H. 1976. Persistence of junctional acetylcholine receptors following denervation. Cold Spring Harbor Symp. Quant. Biol. 40:275-81
127. Frank E, Jansen JK, Lomo T, Westgaard RH. 1975. The interaction between foreign and original motor nerves innervating the soleus muscle of rats. J. Physiol. 247:725-43
128. Froehner SC, Luetje CW, Scotland PB, Patrick J. 1990. The postsynaptic 43K protein clusters muscle nicotinic acetylcholine receptors in Xenopus oocytes. Neuron 5:403-10
129. Fromm L, Burden SJ. 1998. Synapse-specific and neuregulin-induced transcription require an ETS site that binds GABPα/GABPβ. Genes Dev. In press
130. Fuhrer C, Hall ZW. 1996. Functional interaction of src family kinases with the acetylcholine receptor in C2 myotubes. J. Biol. Chem. 271:32474-81
131. Fuhrer C, Sugiyama JE, Taylor RG, Hall ZW. 1997. Association of muscle-specific kinase MuSK with the acetylcholine receptor in mammalian muscle. EMBO J. 16:4951-60
132. Gan W-B, Lichtman JW. 1998. Synaptic segregation at the developing neuromuscular junction. Science. In press
133. Ganju P, Walls E, Brennan J, Reith AD. 1995. Cloning and developmental expression of Nsk2, a novel receptor tyrosine kinase implicated in skeletal myogenesis. Oncogene 11:281-90
134. Gao FB. 1998. Messenger RNAs in dendrites: localization, stability, and implications for neuronal function. BioEssays 20:70-78
135. Gardiner PF. 1993. Physiological properties of motoneurons innervating different muscle unit types in rat gastrocnemius. J. Neurophysiol. 69:1160-70
136. 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 proteoglycan. J. Cell Biol. 108:1873-90
137. Gates HJ, Betz WJ. 1993. Spatial distribution of muscle fibers in a lumbrical muscle of the rat. Anat. Rec. 236:381-89
138. Gautam M, Noakes PG, Moscoso L, Rupp F, Scheller RH, et al. 1996. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85:525-35
139. Gautam M, Noakes PG, Mudd J, Nichol M, Chu GC, et al. 1995. Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377:232-36
140. Gee SH, Montanaro F, Lindenbaum MH, Carbonetto S. 1994. Dystroglycan-a, a dystrophin-associated glycoprotein, is a functional agrin receptor. Cell 77:675-86
141. Gesemann M, Cavalli V, Denzer AJ, Brancaccio A, Schumacher B, Ruegg MA. 1996. Alternative splicing of agrin alters its binding to heparin, dystroglycan, and the putative agrin receptor. Neuron 16:755-67
142. Gesemann M, Denzer AJ, Ruegg MA. 1995. Acetylcholine receptor-aggregating activity of agrin isoforms and mapping of the active site. J. Cell Biol. 128:625-36
143. Gillespie SK, Balasubramanian S, Fung ET, Huganir RL. 1996. Rapsyn clusters and activates the synapse-specific receptor tyrosine kinase MuSK. Neuron 16:953-62
144. Glass DJ, Apel ED, Shah S, Bowen DC, DeChiara TM, et al. 1997. MuSK kinase domain sufficient for phosphorylation but not clustering of acetylcholine receptors. Proc. Natl. Acad. Sci. USA 94:8848-53
145. Glass DJ, Bowen DC, Stitt TN, Radziejewski C, Bruno J, et al. 1996. Agrin acts via a MuSK receptor complex. Cell 85:513-23
146. Glazner GW, Yadav K, Fitzgerald S, Coven E, Brenneman DE, Nelson PG. 1997. Cholinergic stimulation increases thrombin activity and gene expression in cultured mouse muscle. Dev. Brain Res. 99:148-54
147. Glicksman MA, Sanes JR. 1983. Differentiation of motor nerve terminals formed in the absence of muscle fibres. J. Neurocytol. 12:661-71
148. Godfrey EW, Nitkin RM, Wallace BG, Rubin LL, McMahan UJ. 1984. Components of Torpedo electric organ and muscle that cause aggregation of acetylcholine receptors on cultured muscle cells. J. Cell Biol. 99:615-27
149. Goldman D, Brenner HR, Heinemann S. 1988. Acetylcholine receptor, α, β, γ, σ subunit mRNA levels are regulated by muscle activity. Neuron 1:329-33
150. Goldman D, Staple J. 1989. Spatial and temporal expression of acetylcholine receptor RNAs in innervated and denervated rat soleus muscle. Neuron 3:219-28
151. Goldman DB, Carlson M, Staple J. 1991. Induction of adult-type nicotinic acetylcholine receptor gene expression in noninnervated regenerating muscle. Neuron 7:649-58
152. Goodearl AD, Yee AG, Sandrock AW Jr, Corfas G, Fischbach GD. 1995. ARIA is concentrated in the synaptic basal lamina of the developing chick neuromuscular junction. J. Cell Biol. 130:1423-34
153. Grady RM, Merlie JP, Sanes JR. 1997a. Subtle neuromuscular defects in utrophin-deficient mice. J. Cell Biol. 136:871-82
154. Grady RM, Teng H, Nichol MC, Cunningham JC, Wilkinson RS, Sanes JR. 1997b. Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 90:729-38
155. Gramolini AO, Burton EA, Tinsley JM, Ferns MJ, Cartaud A, et al. 1998. Muscle and neural isoforms of agrin increase utrophin expression in cultured myotubes via a transcriptional regulatory mechanism. J. Biol. Chem. 273:1-8
156. Grinnell AD. 1995. Dynamics of nerve-muscle interaction in developing and mature neuromuscular junctions. Physiol. Rev. 75:789-824
157. Grinspan JB, Marchionni MA, Reeves M, Coulaloglou M, Scherer SS. 1996. Axonal interactions regulate Schwann cell apoptosis in developing peripheral nerve: neuregulin receptors and the role of neuregulins. J. Neurosci. 16:6107-18
158. Gu Y, Hall ZW. 1988. Immunological evidence for a change in subunits of the acetylcholine receptor in developing and denervated rat muscle. Neuron. 1:117-25
159. Gundersen K, Sanes JR, Merlie JP. 1993. Neural regulation of muscle acetylcholine receptor α- and ε-subunit gene promoters in transgenic mice. J. Cell Biol. 123:1535-44
160. Gurney ME, Yamamoto H, Kwon Y. 1992. Induction of motor neuron sprouting in vivo by ciliary neurotrophic factor and basic fibroblast growth factor. J. Neurosci. 12:3241-47
161. Hall ZW, Sanes JR. 1993. Synaptic structure and development: the neuromuscular junction. Cell 72:99-121
162. Hardman VJ, Brown MC. 1987. Accuracy of reinnervation of rat intercostal muscles by their own segmental nerves. J. Neurosci. 7:1031-36
163. Herrera AA, Werle MJ. 1990. Mechanisms of elimination, remodeling, and competition at frog neuromuscular junctions. J. Neurobiol. 21:73-98
164. Hesselmans LF, Jennekens FG, Van Den Oord CJ, Veldman H, Vincent A. 1993. Development of innervation of skeletal muscle fibers in man: relation to acetylcholine receptors. Anat. Rec. 236:553-62
165. Hirata K, Zhou C, Nakamura K, Kawabuchi M. 1997. Postnatal development of Schwann cells at neuromuscular junctions, with special reference to synapse elimination. J. Neurocytol. 26:799-809
166. Hoch W, Ferns M, Campanelli JT, Hall ZW, Scheller RH. 1993. Developmental regulation of highly active alternatively spliced forms of agrin. Neuron 11:479-90
167. Hopf C, Hoch W. 1996. Agrin binding to α-dystroglycan. Domains of agrin necessary to induce acetylcholine receptor clustering are overlapping but not identical to the α-dystroglycan-binding region. J. Biol. Chem. 271:5231-36
168. Hopf C, Hoch W. 1998a. Dimerization of the muscle-specific kinase induces tyrosine phosphorylation of acetylcholine receptors and their aggregation on the surface of myotubes. J. Biol. Chem. 273:6467-73
169. Hopf C, Hoch W. 1998b. Tyrosine phosphorylation of the muscle-specific kinase is exclusively induced by acetylcholine receptor-aggregating agrin fragments. Eur J. Biochem. 253:382-89
170. Huang CF, Flucher B, Schmidt M, Stroud SK, Schmidt J. 1994a. Depolarization-transcription signals in skeletal muscle use calcium flux through L channels, but bypass the sarcoplasmic reticulum. Neuron 13:167-77
171. Huang CF, Lee YS, Schmidt MM, Schmidt J. 1994b. Rapid inhibition of myogenindriven acetylcholine receptor subunit gene transcription. EMBO J. 13:634-40
172. Huang CF, Tong J, Schmidt J. 1992. Protein kinase C couples membrane excitation to acetylcholine receptor gene inactivation in chick skeletal muscle. Neuron 9:671-78
173. Hume RI, Role LW, Fischbach GD. 1983. Acetylcholine release from growth cones detected with patches of acetylcholine receptor-rich membranes. Nature 305:632-34
174. Hunter DD, Shah V, Merlie JP, Sanes JR. 1989. A laminin-like adhesive protein concentrated in the synaptic cleft of the neuromuscular junction. Nature 338:229-34
175. Ide C. 1996. Peripheral nerve regeneration. Neurosci. Res. 25:101-21
176. Imaizumi-Scherrer T, Faust DM, Benichou JC, Hellio R, Weiss MC. 1996. Accumulation in fetal muscle and localization to the neuromuscular junction of cAMP-dependent protein kinase A regulatory and catalytic subunits RI α and C α. J. Cell Biol. 134:1241-54
177. Jansen JK, Fladby T. 1990. The perinatal reorganization of the innervation of skeletal muscle in mammals. Prog. Neurobiol. 34:39-90
178. Jasmin BJ, Antony C, Changeux JP, Cartaud J. 1995. Nerve-dependent plasticity of the golgi complex in skeletal muscle fibres: compartmentalization within the subneural sarcoplasm. Eur. J. Neurosci. 7:470-79
179. Jennings CG, Dyer SM, Burden SJ. 1993. Muscle-specific trk-related receptor with a kringle domain defines a distinct class of receptor tyrosine kinases. Proc. Natl. Acad. Sci. USA 90:2895-99
180. Jessell TM, Siegel RE, Fischbach GD. 1979. Induction of acetylcholine receptors on cultured skeletal muscle by a factor extracted from brain and spinal cord. Proc. Natl. Acad Sci. USA 76:5397-401
181. Jo SA, Burden SJ. 1992. Synaptic basal lamina contains a signal for synapse-specific transcription. Development 115:673-80
182. Jo SA, Zhu X, Marchionni MA, Burden SJ. 1995. Neuregulins are concentrated at nerve-muscle synapses and activate ACh-receptor gene expression. Nature 373:158-61
183. Jones G, Herczeg A, Ruegg MA, Lichsteiner M, Kroger S, Brenner HR. 1996. Substrate-bound agrin induces expression of acetylcholine receptor ε-subunit gene in cultured mammalian muscle cells. Proc. Natl. Acad. Sci. USA
184. Jones G, Meier T, Lichtsteiner M, Witzemann V, Sakmann B, Brenner HR. 1997. Induction by agrin of ectopic and functional postsynaptic-like membrane in innervated muscle. Proc. Natl. Acad. Sci. USA 94:2654-59
185. Jordan CL. 1996a. Ciliary neurotrophic factor may act in target musculature to regulate developmental synapse elimination. Dev. Neurosci. 18:185-98
186. Jordan CL. 1996b. Morphological effects of ciliary neurotrophic factor treatment during neuromuscular synapse elimination. J. Neurobiol. 31:29
187. Jordan CL, Watamura S, Arnold AP. 1995. Androgenic, not estrogenic, steroids alter neuromuscular synapse elimination in the rat levator ani. Dev. Brain Res. 84:215-24
188. Katz B. 1966. Nerve, Muscle and Synapse. New York: McGraw-Hill
189. Kawabuchi M, Zhou C, Nakamura K, Hirata K. 1995. Morphological features of collateral innervation and supernumerary innervation in the skeletal muscles of presenile rats. Anat. Anz. 177:251-65
190. Kelly AM, Zacks SI. 1969. The fine structure of motor endplate morphogenesis. J. Cell Biol. 42:154-69
191. Keshishian H, Broadie K, Chiba A, Bate M. 1996. The drosophila neuromuscular junction: a model system for studying synaptic development and function. Annu. Rev. Neurosci. 19:545-75
192. Kidokoro Y, Yeh E 1982. Initial synaptic transmission at the growth cone in Xenopus nerve-muscle cultures. Proc. Natl. Acad. Sci. USA 79:6727-31
193. Kirsch J, Meyer G, Betz H. 1996. Synaptic targeting of ionotropic neurotransmitter receptors. Mol. Cell. Neurosci. 8:93-98
194. Klarsfeld A, Bessereau JL, Salmon AM, Triller A, Babinet C, Changeux JP. 1991. An acetylcholine receptor α-subunit promoter conferring preferential synaptic expression in muscle of transgenic mice. EMBO J. 10:625-32
195. Klarsfeld A, Changeux JP. 1985. Activity regulates the levels of acetylcholine receptor α-subunit mRNA in cultured chick myotubes. Proc. Natl. Acad. Sci. USA 82:4558-62
196. Klarsfeld A, Laufer R, Fontaine B, Devillers-Thiery A, Dubreuil C, Changeux JP. 1989. Regulation of the muscle AChR α-subunit gene expression by electrical activity: involvement of protein kinase C and Ca++. Neuron 2:1229-36
197. Ko CP. 1985. Formation of the active zone at developing neuromuscular junctions in larval and adult bullfrogs. J. Neurocytol. 14:487-512
198. Ko CP, Chen L. 1996. Synaptic remodeling revealed by repeated in vivo observations and electron microscopy of identified frog neuromuscular junctions. J. Neurosci. 16:1780-90
199. Koike S, Schaeffer L, Changeux JP. 1995. Identification of DNA element determining synaptic expression of the mouse acetylcholine receptor σ-subunit gene. Proc. Natl. Acad. Sci. USA 92:10624-28
200. Krejci E, Thomine S, Boschetti N, Legay C, Sketelj J, Massoulie J. 1997. The mammalian gene of acetylcholinesterase-associated collagen. J. Biol. Chem. 272:22840-47
201. Kuffler D, Thompson W, Jansen JK. 1977. The elimination of synapses in multiply-innervated skeletal muscle fibres of the rat: dependence on distance between endplates. Brain Res. 138:353-58
202. Kuffler DR. 1986. Accurate reinnervation of motor endplates after disruption of sheath cells and muscle fibers. J. Comp. Neurol. 250:228-35
203. Kuffler DP, Thompson WJ, Jansen JK. 1980. The fate of foreign endplates in cross-innervated rat soleus muscle. Proc. R. Soc. London (Biol.) 208:189-222
204. Kullberg RW, Lentz TL, Cohen MW. 1977. Development of the myotomal neuromuscular junction in Xenopus laevis: an electrophysiological and fine-structural study. Dev. Biol. 60:101-29
205. Kwon YW, Abbondanzo SJ, Stewart CL, Gurney ME. 1995. Leukemia inhibitory factor influences the timing of programmed synapses withdrawal from neonatal muscles. J. Neurobiol. 28:35-50
206. Kwon YW, Gurney ME. 1994. Systemic injections of ciliary neurotrophic factor induce sprouting by adult motor neurons. NeuroReport 5:789-92
207. Kwon YW, Gurney ME. 1996. Brain-derived neurotrophic factor transiently stabilizes silent synapses on developing neuromuscular junctions. J. Neurobiol. 29:503-16
208. Lance-Jones C, Landmesser L. 1981. Pathway selection by embryonic chick motoneurons in an experimentally altered environment. Proc. R. Soc. London (Biol.) 214:19-52
209. Landau BR, Akert K, Roberts TS. 1962. Studies on the innervation of the diaphragm. J. Comp. Neurol. 119:1-10
210. Langenfeld-Oster B, Dorlochter M, Wernig A. 1993. Regular and photodamage-enhanced remodelling in vitally stained frog and mouse neuromuscular junctions. J. Neurocytol. 22:517-30
211. Laskowski MB, Colman H, Nelson C, Lichtman JW. 1998a. Synaptic competition during the reformation of a neuromuscular map. J. Neurosci. 18:7328-35
212. Laskowski MB, Feng G, Nichol M, Sanes JR. 1998b. Overexpression of ephrin A5 in muscle disrupts neuromuscular topography. Neurosci. Abstr. 24:791
213. Laskowski MB, Owens JL. 1994. Embryonic expression of motoneuron topography in the rat diaphragm muscle. Dev. Biol. 166:502-8
214. Laskowski MB, Sanes JR. 1987. Topographic mapping of motor pools onto skeletal muscles. J. Neurosci. 7:252-60
215. Laskowski MB, Sanes JR. 1988. Topographically selective reinnervation of adult mammalian skeletal muscles. J. Neurosci. 8:3094-99
216. Leber SM, Breedlove SM, Sanes JR. 1990. Lineage, arrangement, and death of clonally related motoneurons in chick spinal cord. J. Neurosci. 10:2451-62
217. Lemke G. 1996. Neuregulins in development. Mol. Cell. Neurosci. 7:247-62
218. Lichtman JW, Wilkinson RS, Rich MD. 1985. Multiple innervation of tonic endplates revealed by activity-dependent uptake of fluorescent probes. Nature 314:357-59
219. Lichtman JW, Magrassi L, Purves D. 1987. Visualization of neuromuscular junctions over periods of several months in living mice. J. Neurosci. 7:1215-22
220. Lichtman JW, Balice-Gordon RJ. 1990. Understanding synaptic competition in theory and in practice. J. Neurobiol. 21:99-106
221. Linden DC, Jerian SM, Letinsky MS. 1988. Neuromuscular junction development in the cutaneous pectoris muscle of Rana catesbeiana. Exp. Neurol. 99:735-60
222. Liu Y, Fields RD, Festoff BW, Nelson PG. 1994. Proteolytic action of thrombin is required for electrical activity-dependent synapse reduction. Proc. Natl. Acad Sci. USA 91:10300-4
223. Loeb JA, Fischbach GD. 1995. ARIA can be released from extracellular matrix through cleavage of a heparin-binding domain. J. Cell Biol. 130:127-35
224. Lohof AM, Delhaye-Bouchaud N, Mariana J. 1996. Synapse elimination in the central nervous system: functional significance and cellular mechanisms. Rev. Neurosci. 7:85-101
225. Lomo T, Westgaard RH. 1975. Control of ACh sensitivity in rat muscle fibers. Cold Spring Harbor Symp. Quant. Biol. 40:263-74
226. Lou XJ, Bixby JL. 1995. Patterns of presynaptic gene expression define two stages of synaptic differentiation. Mol. Cell. Neurosci. 6:252-62
227. Lu B, Czernik AJ, Popov S, Wang T, Poo MM, Greengard P. 1996. Expression of synapsin I correlates with maturation of the neuromuscular synapse. Neuroscience 74:1087-97
228. Lu B, Figurov A. 1997. Role of neurotrophins in synapse development and plasticity. Rev. Neurosci. 8:1-12
229. Ludatscher RM, Silbermann M, Gershon D, Reznick A. 1985. Evidence of Schwann cell degeneration in the aging mouse motor end-plate region. Exp. Gerontol. 20:81-91
230. Lupa MT, Gordon H, Hall ZW. 1990. A specific effect of muscle cells on the distribution of presynaptic proteins in neurites and its absence in a C2 muscle cell variant. Dev. Biol. 142:31-43
231. Lupa MT, Hall ZW. 1989. Progressive restriction of synaptic vesicle protein to the nerve terminal during development of the neuromuscular junction. J. Neurosci. 9:3937-45
232. Mann S, Kroger S. 1996. Agrin is synthesized by retinal cells and colocalizes with gephyrin. Mol. Cell. Neurosci. 8:1-13
233. Martin D, Merkel E, Tucker KK, McManaman JL, Albert D, et al. 1996. Cachectic effect of ciliary neurotrophic factor on innervated skeletal muscle. Am. J. Physiol. 271:R1422-R1428
234. Martin PT, Ettinger AJ, Sanes JR. 1995. A synaptic localization domain in the synaptic cleft protein laminin β2 (s-laminin). Science 269:413-16
235. Martin PT, Kaufman SJ, Kramer RH, Sanes JR. 1996. Synaptic integrins in developing, adult, and mutant muscle: selective association of α1, α7A, and α7B integrins with the neuromuscular junction. Dev. Biol. 174:125-39
236. Martin PT, Sanes JR. 1995. Role for a synapse-specific carbohydrate in agrin-induced clustering of acetylcholine receptors. Neuron 14:743-54
237. Martin PT, Sanes JR. 1997. Integrins mediate adhesion to agrin and modulate agrin signaling. Development 124:3909-17
238. Martinou JC, Falls DL, Fischbach GD, Merlie JP. 1991. Acetylcholine receptor-inducing activity stimulates expression of the ε-subunit gene of the muscle acetylcholine receptor. Proc. Natl. Acad. Sci. USA 88:7669-73
239. Martinou JC, Merlie JP. 1991. Nerve-dependent modulation of acetylcholine recepfor ε-subunit gene expression. J. Neurosci. 11:1291-99
240. Massoulie J, Pezzementi L, Bon S, Krejci E, Vallette FM. 1993. Molecular and cellular biology of cholinesterases. Prog. Neurobiol. 41:31-91
241. Matsuoka I, Nakane A, Kurihara K. 1997. Induction of LIF-mRNA by TGF-β1 in Schwann cells. Brain Res. 776:170-80
242. McMahan UJ. 1990. The agrin hypothesis. Cold Spring Harbor Symp. Quant. Biol. 55:407-18
243. Megeath LJ, Fallon JR. 1998. Intracellular calcium regulates agrin-induced acetylcholine receptor clustering. J. Neurosci. 18:672-78
244. Meier T, Gesemann M, Cavalli V, Ruegg MA, Wallace BG. 1996. AChR phosphorylation and aggregation induced by an agrin fragment that lacks the binding domain for α-dystroglycan. EMBO J. 15:2625-31
245. Meier T, Hauser DM, Chiquet M, Landmann L, Ruegg MA, Brenner HR. 1997. Neural agrin induces ectopic postsynaptic specializations in innervated muscle fibers. J. Neurosci. 17:6534-44
246. Meier T, Masciulli F, Moore C, Schoumacher F, Eppenberger U, et al. 1998. Agrin can mediate acetylcholine receptor gene expression in muscle by aggregation of muscle-derived neuregulins. J. Cell Biol. 141:715-26
247. Merlie JP. 1984. Biogenesis of the acetylcholine receptor, a multisubunit integral membrane protein. Cell 36:573-75
248. Merlie JP, Isenberg KE, Russell SD, Sanes JR. 1984. Denervation supersensitivity in skeletal muscle: analysis with a cloned cDNA probe. J. Cell Biol. 99:332-35
249. Merlie JP, Sanes JR. 1985. Concentration of acetylcholine receptor mRNA in synaptic regions of adult muscle fibres. Nature 317:66-68
250. Meyer D, Birchmeier C. 1995. Multiple essential functions of neuregulin in development. Nature 378:386-90
251. Miner JH, Sanes JR. 1994. Collagen IV α3, α4, and α5 chains in rodent basal laminae: sequence, distribution, association with laminins, and developmental switches. J. Cell Biol. 127:879-91
252. Mirsky R, Jessen KR. 1996. Schwann cell development, differentiation and myelination. Curr. Opin. Neurobiol. 6:89-96
253. Mishina M, Takai T, Imoto K, Noda M, Takahashi T, et al. 1986. Molecular distinction between fetal and adult forms of muscle acetylcholine receptor. Nature 321:406-11
254. Missias AC, Chu GC, Klöcke B, Sanes JR, Merlie JP. 1996. Maturation of the acetylcholine receptor in developing skeletal muscle: regulation of the AChR γ-to-ε-switch. Dev. Biol. 179:223-38
255. Missias AC, Mudd J, Cunningham JM, Steinbach JH, Merlie JP, Sanes JR. 1997. Deficient development and maintenance of postsynaptic specializations in mutant mice lacking an "adult" acetylcholine receptor subunit. Development 124:5075-86
256. Montanaro F, Gee SH, Jacobson C, Lindenbaum MH, Froehner SC, Carbonetto S. 1998. Laminin and α-dystroglycan mediate acetylcholine receptor aggregation via a MuSK-independent pathway. J. Neurosci. 18:1250-60
257. Mook-Jung I, Gordon H. 1995. Acetylcholine receptor clustering in C2 muscle cells requires chondroitin sulfate. J. Neurobiol. 28:482-92
258. Moscoso LM, Chu GC, Gautam M, Noakes PG, Merlie JP, Sanes JR. 1995a. Synapse-associated expression of an acetylcholine receptor-inducing protein, ARIA/heregulin, and its putative receptors, ErbB2 and ErbB3, in developing mammalian muscle. Dev. Biol. 172:158-69
259. Moscoso LM, Cremer H, Sanes JR. 1998. Formation and regeneration of neuromuscular junctions in mice lacking N-CAM, tenascin-C, or FGF-5. J. Neurosci. 18:1465-77
260. Moscoso LM, Merlie JP, Sanes JR. 1995b. N-CAM, 43k-rapsyn, and S-laminin mRNAs are concentrated at synaptic sites in muscle fibers. Mol. Cell. Neurosci. 6:80-89
261. Moss BL, Schuetze SM. 1987. Development of rat soleus endplate membrane following denervation at birth. J. Neurobiol. 18:101-18
262. Nakajima Y, Kidokoro Y, Klier FG. 1980. The development of functional neuromuscular junctions in vitro: an ultrastructural and physiological study. Dev. Biol. 77:52-72
263. Namba T, Scheller RH. 1996. Inhibition of agrin-mediated acetylcholine receptor clustering by utrophin C-terminal peptides. Genes to Cells 1:755-64
264. New HV, Mudge AW. 1986. Calcitonin gene-related peptide regulates muscle acetylcholine receptor synthesis. Nature 323:809-11
265. Nguyen QT, Lichtman JW. 1996. Mechanism of synapse disassembly at the developing neuromuscular junction. Curr. Opin. Neurobiol. 6:104-12
266. Nguyen QT, Parsadanian AS, Snider WD, Lichtman JW. 1998. Hyperinnervation of neuromuscular junctions caused by GDNF overexpression in muscle. Science 279:1725-29
267. Nitkin RM, Smith MA, Magill C, Fallon JR, Yao YM, et al. 1987. Identification of agrin, a synaptic organizing protein from Torpedo electric organ. J. Cell Biol. 105:2471-78
268. Noakes PG, Gautam M, Mudd J, Sanes JR, Merlie JR. 1995. Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin β2. Nature 374:258-62
269. Noakes PG, Phillips WD, Hanley TA, Sanes JR, Merlie JP. 1993. 43K protein and acetylcholine receptors colocalize during the initial stages of neuromuscular synapse formation in vivo. Dev. Biol. 155:275-80
270. Nystrom B. 1968. Histochemical studies of end-plate bound esterases in "slow-red" and "fast-white" cat muscles during postnatal development. Acta Neurol. Scand. 44:295-317
271. Ogata T. 1988. Structure of motor endplates in the different fiber types of vertebrate skeletal muscles. Arch. Histol. Cytol. 51:385-424
272. O'Malley JP, Moore CT, Salpeter MM. 1997. Stabilization of acetylcholine receptors by exogenous ATP and its reversal by cAMP and calcium. J. Cell Biol. 138:159-65
273. Ontell M, Ontell MP. 1995. Muscle-specific gene expression during myogenesis in the mouse. Microsc. Res. Tech. 30:354-65
274. Oppenheim RW. 1996. Neurotrophic survival molecules for motoneurons: an embarrassment of riches. Neuron 17:195-97
275. Ostberg AJ, Vrbova G, O'Brien RA. 1986. Reinnervation of fast and slow mammalian muscles by a superfluous number of motor axons. Neuroscience 18:205-13
276. O'Toole JJ, Deyst KA, Bowe MA, Nastuk MA, McKechnie BA, Fallon JR. 1996. Alternative splicing of agrin regulates its binding to heparin, α-dystroglycan, and the cell surface. Proc. Natl. Acad. Sci. USA 93:7369-74
277. Ozaki M, Sasner M, Yano R, Lu HS, Buonanno A. 1997. Neuregulin-β induces expression of an NMDA-receptor subunit. Nature 390:691-94
278. Pachter BR, Spielholz NI. 1990. Tenotomy-induced motor endplate alterations in rat soleus muscle, Anat. Rec. 228:104-8
279. Patton BL, Chiu AY, Sanes JR. 1998. Synaptic laminin prevents glial entry into the synaptic cleft. Nature 393:698-701
280. Patton BL, Liu J, Sanes JR. 1995. The synaptic cleft protein s-laminin/laminin β2 promotes synaptic responses by motoneurons, muscle cells, and Schwann cells in vitro. Neurosci. Abstr. 20:799
281. Patton BL, Miner JH, Chiu AY, Sanes JR. 1997. Localization, regulation and function of laminins in the neuromuscular system of developing, adult and mutant mice. J. Cell Biol. 139:1507-21
282. Peng HB, Ali AA, Dai Z, Daggett DF, Raulo E, Rauvala H. 1995. The role of heparin-binding growth-associated molecule (HB-GAM) in the postsynaptic induction in cultured muscle cells. J. Neurosci. 15:3027-38
283. Peng HB, Baker LP, Chen Q. 1991. Induction of synaptic development in cultured muscle cells by basic fibroblast growth factor. Neuron 6:237-46
284. Peters MF, Sadoulet-Puccio HM, Grady M, Kramarcy NR, Kunkel LM, et al. 1998. Differential membrane localization and intermolecular associations of α-dystrobrevin isoforms in skeletal muscle. J. Cell Biol. 142:1269-78
285. Pette D, Staron RS. 1997. Mammalian skeletal muscle fiber type transitions. Int. Rev. Cytol. 170:143-223
286. Pfrieger FW, Barres BA. 1997. Synaptic efficacy enhanced by glial cells in vitro. Science 277:1684-87
287. Phillips WD, Kopta C, Blount P, Gardner PD, Steinbach JH, Merlie JP. 1991. ACh receptor-rich membrane domains organized in fibroblasts by recombinant 43-kildalton protein. Science 251:568-70
288. Piette J, Bessereau JL, Huchet M, Changeux JP. 1990. Two adjacent MyoD1-binding sites regulate expression of the acetylcholine receptor α-subunit gene. Nature 345:353-55
289. Plantinga LC, Verhaagen J, Edwards PM, Hol EM, Bar PR, Gispen WH. 1993. The expression of B-50/GAP-43 in Schwann cells is upregulated in degenerating peripheral nerve stumps following nerve injury. Brain Res. 602:69-76
290. Plunkett JA, Baccus SA, Bixby JL. 1998. Differential regulation of synaptic vesicle protein genes by target and synaptic activity. J. Neurosci. 18:5832-38
291. Porter BE, Weis J, Sanes JR. 1995. A motoneuron-selective stop signal in the synaptic protein S-laminin. Neuron 14:549-59
292. Porter JD, Baker RS. 1996. Muscles of a different 'color': the unusual properties of the extraocular muscles may predispose or protect them in neurogenic and myogenic disease. Neurology 46:30-37
293. Prody CA, Merlie JP. 1992. The 5′-flanking region of the mouse muscle nicotinic acetylcholine receptor β-subunit gene promotes expression in cultured muscles cells and is activated by MRF4, myogenin and myoD. Nucleic Acids Res. 20:2367-72
294. Purves D, Lichtman JW. 1980. Elimination of synapses in the developing nervous system. Science 210:153-57
295. Purves D, Lichtman JW. 1987. Synaptic sites on reinnervated nerve cells visualized at two different times in living mice. J. Neurosci. 7:1492-97
296. Ramarao MK, Cohen JB. 1998. Mechanism of nicotinic acetylcholine receptor cluster formation by rapsyn. Proc. Natl. Acad. Sci. USA 95:4007-12
297. Rao A, Kim E, Sheng M, Craig AM. 1998. Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture. J. Neurosci. 18:1217-29
298. Rauvala H, Peng HB. 1997. HB-GAM (heparin-binding growth-associated molecule) and heparin-type glycans in the development and plasticity of neuron-target contacts. Prog. Neurobiol, 52:127-44
299. Redfern PA. 1970. Neuromuscular transmission in new-born rats. J. Physiol. 209:701-9
300. Reist NE, Werle MJ, McMahan UJ. 1992. Agrin released by motor neurons induces the aggregation of acetylcholine receptors at neuromuscular junctions. Neuron 8:865-68
301. Reynolds ML, Woolf CJ. 1992. Terminal Schwann cells elaborate extensive processes following denervation of the motor endplate. J. Neurocytol. 21:50-66
302. Ribchester RR. 1988. Activity-dependent and -independent synaptic interactions during reinnervation of partially denervated rat muscle. J. Physiol. 401:53-75
303. Rich MM, Lichtman JW. 1989a. In vivo visualization of pre- and postsynaptic changes during synapse elimination in reinnervated mouse muscle. J. Neurosci. 9:1781-1805
304. Rich M, Lichtman JW. 1989b. Motor nerve terminal loss from degenerating muscle fibers. Neuron 3:677-88
305. Ridge RM. 1971. Different types of extrafusal muscle fibres in snake costocutaneous muscles. J. Physiol. 217:393-418
306. Ridge RM, Betz WJ. 1984. The effect of selective chronic stimulation on motor unit size in developing rat muscle. J. Neurosci. 4:2614-20
307. Ridge RM, Rowlerson A. 1996. Motor units of juvenile rat lumbrical muscles and fibre type compositions of the glycogen-depleted component. J. Physiol. 497:199-210
308. Riethmacher D, Sonnenbergriethmacher E, Brinkmann V, Yamaai T, Lewin GR, Birchmeier C. 1997. Severe neuropathies in mice with targeted mutations in the ERBB3 receptor. Nature 389:725-30
309. Riley DA. 1981. Ultrastructural evidence for axon retraction during the spontaneous elimination of polyneuronal innervation of the rat soleus muscle. J. Neurocytol. 10:425-40
310. Rimer M, Mathiesen I, Lomo T, McMahon UJ. 1997. γ-AChR/ε-AChR switch at agrin-induced postsynaptic-like apparatus in skeletal muscle. Mol. Cell. Neurosci. 9:254-63
311. Robitaille R, Garcia ML, Kaczorowski GJ, Charlton MP. 1993. Functional colocalization of calcium and calcium-gated potassium channels in control of neurotransmitter release. Neuron 11:645-55
312. Rosenheimer JL, Smith DO. 1985. Differential changes in the end-plate architecture of functionally diverse muscles during aging. J. Neurophysiol. 53:1567-81
313. Rosenthal JL, Taraskevich PS. 1977. Reduction of multiaxonal innervation at the neuromuscular junction of the rat during development. J. Physiol. 270:299-310
314. Rotundo RL, Rossi SG, Anglister L. 1997. Transplantation of quail collagen-tailed acetylcholinesterase molecules onto the frog neuromuscular synapse. J. Cell Biol. 136:367-74
315. Rudnicki MA, Jaenisch R. 1995. The MyoD family of transcription factors and skeletal myogenesis. BioEssays 17:203-9
316. Ruegg MA, Tsim KW, Horton SE, Kroger S, Escher G, et al. 1992. The agrin gene codes for a family of basal lamina proteins that differ in function and distribution. Neuron 8:691-99
317. Rupp F, Payan DG, Magill-Solc C, Cowan DM, Scheller RH. 1991. Structure and expression of a rat agrin. Neuron 6:811-23
318. Salpeter MM, Loring RH. 1985. Nicotinic acetylcholine receptors in vertebrate muscle: properties, distribution and neural control. Prog. Neurobiol. 25:297-325
319. Salpeter MM, Marchaterre M, Harris R. 1988. Distribution of extrajunctional acetylcholine receptors on a vertebrate muscle: evaluated by using a scanning electron microscope autoradiographic procedure. J. Cell Biol. 106:2087-93
320. Sandrock AW, Dryer SE, Rosen KM, Gozani SN, Kramer R, et al. 1997. Maintenance of acetylcholine receptor number by neuregulins. Science 276:599-603
321. Sanes JR. 1995. The synaptic cleft of the neuromuscular junction. Semin. Dev. Biol. 6:163-73
322. Sanes JR, Apel ED, Gautam M, Glass D, Grady RM, et al. 1998. Agrin receptors at the skeletal neuromuscular junction. Ann. NY Acad. Sci. In Press
323. Sanes JR, Johnson YR, Kotzbauer PT, Mudd J, Hanley T, et al. 1991. Selective expression of an acetylcholine receptor-lacZ transgene in synaptic nuclei of adult muscle fibers. Development 113:1181-91
324. Sanes JR, Marshall LM, McMahan UJ. 1978. Reinnervation of muscle fiber basal lamina after removal of myofibers. Differentiation of regenerating axons at original synaptic sites. J. Cell Biol. 78:176-98
325. Sanes JR, Schachner M, Covault J. 1986. Expression of several adhesive macromolecules (N-CAM, L1, J1, NILE, uvomorulin, laminin, fibronectin, and a heparan sulfate proteoglycan) in embryonic, adult, and denervated adult skeletal muscle. J. Cell Biol. 102:420-31
326. Sanes JR, Scheller RH. 1997. Synapse formation: a molecular perspective. In Developmental Neurobiology, ed. WM Cowan, SL Zipursky, TM Jessel, pp. 179-219. New York: Oxford Univ. Press
327. Sapru MK, Florance SK, Kirk C, Goldman D. 1998. Identification of a neuregulin and protein-tyrosine phosphatase response element in the nicotinic acetylcholine receptor ε-subunit gene: regulatory role of an Ets transcription factor. Proc. Natl. Acad. Sci. USA 95:1-6
328. Schaeffer L, Duclert N, Huchetdymanus M, Changeux JP. 1998. Implication of a multisubunit ETS-related transcription factor in synaptic expression of the nicotinic acetylcholine receptor. EMBO J. 17:3078-90
329. Schiaffino S, Reggiani C. 1996. Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol. Rev. 76:371-423
330. Schuetze SM, Role LW. 1987. Developmental regulation of nicotinic acetylcholine receptors. Annu. Rev. Neurosci. 10:403-57
331. Scott LJ, Bacou F, Sanes JR. 1988. A synapse-specific carbohydrate at the neuromuscular junction: association with both acetylcholinesterase and a glycolipid. J. Neurosci. 8:932-44
332. Sealock R, Wray BE, Froehner SC. 1984. Ultrastructural localization of the Mr 43,000 protein and the acetylcholine receptor in Torpedo postsynaptic membranes using monoclonal antibodies. J. Cell Biol. 98:2239-44
333. Serpinskaya AS, Feng G, Sanes JR, Craig AM. 1997. Synapse formation between agrin-deficient neurons. Neurosci. Abstr. 23:33
334. Sheard PW, Duxson MJ. 1997. The transient existence of 'en passant' nerve terminals in normal embryonic rat skeletal muscle. Dev. Brain Res. 98:259-64
335. Shyng SL, Xu R, Salpeter MD. 1991. Cyclic AMP stabilizes the degradation of original junctional acetylcholine receptors in denervated muscle. Neuron 6:469-75
336. Si J, Miller DS, Mei L. 1997. Identification of an element required for acetylcholine receptor-inducing activity (ARIA)-induced expression of the acetylcholine receptor ε-subunit gene. J. Biol. Chem. 272:10367-71
337. Si JT, Luo ZJ, Mei L. 1996. Induction of acetylcholine receptor gene expression by ARIA requires activation of mitogen-activated protein kinase. J. Biol. Chem. 271:19752-59
338. Simon AM, Burden SJ. 1993. An E box mediates activation and repression of the acetylcholine receptor α-subunit gene during myogenesis. Mol. Cell. Biol. 13:5133-40
339. Simon AM, Hoope P, Burden SJ. 1992. Spatial restriction of AChR gene expression to subsynaptic nuclei. Development 114:545-53
340. Slater CR. 1982. Postnatal maturation of nerve-muscle junctions in hindlimb muscles of the mouse. Dev. Biol. 94:11-22
341. Smith DO, Rosenheimer JL. 1982. Decreased sprouting and degeneration of nerve terminals of active muscles in aged rats. J. Neurophysiol. 48:100-9
342. Snider WD, Lichtman JW. 1996. Are neurotrophins synaptotrophins? Mol. Cell. Neurosci. 7:433-42
343. Son YJ, Thompson WJ. 1995a. Schwann cell processes guide regeneration of peripheral axons. Neuron 14:125-32
344. Son YJ, Thompson WJ. 1995b. Nerve sprouting in muscle is induced and guided by processes extended by Schwann cells. Neuron 14:133-41
345. Son YJ, Trachtenberg JT, Thompson WJ. 1996. Schwann cells induce and guide sprouting and reinnervation of neuromuscular junctions. Trends Neurosci. 19:280-85
346. Stanco AM, Werle MJ. 1997. Agrin and acetylcholine receptors are removed from abandoned synaptic sites at reinnervated frog neuromuscular junctions. J. Neurobiol: 999-1018
347. Steinbach JH. 1981. Developmental changes in acetylcholine receptor aggregates at rat skeletal neuromuscular junctions. Dev. Biol. 84:267-76
348. Stockdale FE. 1992. Myogenic cell lineages. Dev. Biol. 154:284-98
349. Storms SD, Kim AC, Tran BH, Cole GJ, Murray BA. 1996. NCAM-mediated adhesion of transfected cells to agrin. Cell Adhes. Commun. 3:497-509
350. Sudhof TC. 1995. The synaptic vesicle cycle: a cascade of protein-protein. Nature 375:645-53
351. Sugiura Y, Woppmann A, Miljanich GP, Ko CP. 1995. A novel w-conopeptide for the presynaptic localization of calcium channels at the mammalian neuromuscular junction. J. Neurocytol. 24:15-27
352. Sugiyama J, Bowen DC, Hall ZW. 1994. Dystroglycan binds nerve and muscle agrin. Neuron 13:103-15
353. Sugiyama JE, Glass DJ, Yancopoulos GD, Hall ZW. 1997. Laminin-induced acetylcholine receptor clustering: an alternative pathway. J. Cell Biol. 139:181-91
354. Swanson GJ, Vrbova G. 1987. Effects of low calcium and inhibition of calcium-activiated neutral protease (CANP) on mature nerve terminal structure in the rat sternocostalis muscle. Brain Res. 430:199-203
355. Takahashi T, Nakajimi Y, Hirosawa K, Nakajimi S, Onodera K. 1987. Structure and physiology of developing neuromuscular synapses in culture. J. Neurosci. 7:473-81
356. Tal M, Rotshenker S. 1983. Recycling of synaptic vesicles in motor nerve endings separated from their target muscle fibers. Brain Res. 270:131-33
357. Tanabe Y, Jessell TM. 1996. Diversity and pattern in the developing spinal cord. Science 274:1115-23
358. Tang J, Jo SA, Burden SJ. 1994. Separate pathways for synapse-specific and electrical activity-dependent gene expression in skeletal muscle. Development 120:1799-1804
359. Taniuchi M, Clark HB, Schweitzer JB, Johnson EM Jr. 1988. Expression of nerve growth factor receptors by Schwann cells of axotomized peripheral nerves: ultrastructural location, suppression by axonal contact, and binding properties. J. Neurosci. 8:664-81
360. Tansey MG, Chu GC, Merlie JP. 1996. ARIA/HRG regulates AChR ε-subunit gene expression at the neuromuscular synapse via activation of phosphatidylinositol 3-kinase and RAS/MAPK pathway. J. Cell Biol. 134:465-76
361. Tessier-Lavigne M, Goodman CS. 1996. The molecular biology of axon guidance. Science 274:1123-33
362. Thompson WJ. 1983. Synapse elimination in neonatal rat muscle is sensitive to pattern of muscle use. Nature 302:614-616
363. Thompson WJ. 1985. Activity and synapse elimination at the neuromuscular junction. Cell. Mol. Neurobiol. 5:167-82
364. Thompson WJ, Condon K, Astrow SH. 1990. The origin and selective innervation of early muscle fiber types in the rat. J. Neurobiol. 21:212-22
365. Trachtenberg JT, Thompson WJ. 1996. Schwann cell apoptosis at developing neuromuscular junctions in regulated by glial growth factor. Nature 379:174-77
366. Trachtenberg JT, Thompson WJ. 1997. Nerve terminal withdrawal from rat neuromuscular junctions induced by neuregulin and Schwann cells. J. Neurosci. 17:6243-55
367. Tsay HJ, Schmidt J. 1989. Skeletal muscle denervation activates acetylcholine receptor genes. J. Cell Biol. 108:1523-26
368. Tsen G, Halfter W, Kroger S, Cole GJ. 1995. Agrin is a heparan sulfate proteoglycan. J. Biol. Chem. 270:3392-99
369. Tyc F, Vrbova G. 1995. Stabilisation of neuromuscular junctions by leupeptin increases motor unit size in partially denervated rat muscles. Dev. Brain Res. 88:186-93
370. Uchida S, Yamamoto H, Iio S, Matsumoto N, Wang XB, et al. 1990. Release of calcitonin gene-related peptide-like immunoreactive substance from neuromuscular junction by nerve excitation and its action on striated muscle. J. Neurochem. 54:1000-3
371. Usdin TB, Fischbach G. 1986. Purification and characterization of a polypeptide from chick brain that promotes the accumulation of acetylcholine receptors in chick myotubes. J. Cell Biol. 103:493-507
372. Valenzuela DM, Stitt TN, DiStefano PS, Rojas E, Mattsson K, et al. 1995. Receptor tyrosine kinase specific for the skeletal muscle lineage: expression in embryonic muscle, at the neuromuscular junction, and after injury. Neuron 15:573-84
373. Vaughn JE. 1989. Fine structure of synaptogenesis in the vertebrate central nervous system. Synapse 3:255-85
374. Villarroel A, Sakmann B. 1996. Calcium permeability increase of endplate channels in rat muscle during postnatal development. J. Physiol. 496:331-38
375. Walke W, Xiao G, Goldman D. 1996a. Identification and characterization of a 47 base pair activity-dependent enhancer of the rat nicotinic acetylcholine receptor delta-subunit promoter. J. Neurosci. 16:3641-51
376. Walke W, Xiao G, Goldman D. 1996b. A dual function activity-dependent, muscle-specific enhancer from rat nicotinic acetylcholine receptor σ-subunit gene. J. Neurobiol. 31:359-69
377. Wallace BG. 1989. Agrin-induced specializations contain cytoplasmic, membrane, and extracellular matrix-associated components of the postsynaptic apparatus. J. Neurosci. 9:1294-302
378. Wallace BG. 1995. Regulation of the interaction of nicotinic acetylcholine receptors with the cytoskeleton by agrin-activated protein tyrosine kinase. J. Cell Biol. 128:1121-29
379. Wallace BG, Qu Z, Huganir RL. 1991. Agrin induces phosphorylation of the nicotinic acetylcholine receptor. Neuron 6:869-78
380. Wang X-H, Berninger B, Poo M-M. 1998. Localized synaptic actions of neurotrophin-4. J. Neurosci. 18:4985-92
381. Werle MJ, Herrera AA. 1991. Elevated levels of polyneuronal innervation persist for as long as two years in reinnervated frog neuromuscular junctions. J. Neurobiol. 22:97-103
382. Werle MJ, Sojka AM. 1996. Anti-agrin staining is absent at abandoned synaptic sites of frog neuromuscular junctions. J. Neurobiol. 30:293-302
383. Wernig A, Herrera AA. 1986. Sprouting and remodeling at the nerve-muscle junction. Prog. Neurobiol. 27:251-91
384. Wigston DJ. 1986. Selective innervation of transplanted limb muscles by regenerating motor axons in the axolotl. J. Neurosci. 6:2757-63
385. Wigston DJ. 1990. Repeated in vivo visualization of neuromuscular junctions in adult mouse lateral gastrocnemius. J. Neurosci. 10:1753-61
386. Wigston DJ, Kennedy PR. 1987. Selective reinnervation of transplanted muscles by their original motoneurons in the axolotl. J. Neurosci. 7:1857-65
387. Wigston DJ, Sanes JR. 1982. Selective reinnervation of adult mammalian muscle by axons from different segmental levels. Nature 299:464-67
388. Wigston DJ, Sanes JR. 1985. Selective reinnervation of rat intercostal muscles transplanted from different segmental levels to a common site. J. Neurosci. 5:1208-21
389. Wood SJ, Slater CR. 1997. The contribution of postsynaptic folds to the safety factor for neuromuscular transmission in rat fast- and slow-twitch muscles. J. Physiol. 500:165-76
390. Wood SJ, Slater CR. 1998. Beta-spectrin is colocalized with both voltage-gated sodium channels and ankyrin(g) at the adult rat neuromuscular junction. J. Cell Biol. 140:675-84
391. Xie ZP, Poo MM. 1986. Initial events in the formation of neuromuscular synapse: rapid induction of acetylcholine release from embryonic neuron. Proc. Natl. Acad. Sci. USA 83:7069-73
392. Xu R, Salpeter MM. 1997. Acetylcholine receptors in innervated muscles of dystrophic mdx mice degrade as after denervation. J. Neurosci. 17:8194-8200
393. Yee WC, Pestronk A, Alderson K, Yuan CM. 1988. Regional heterogeneity in the distal motor axon: three zones with distinctive intrinsic components. J. Neurocytol. 17:649-56
394. You S, Petrov T, Chung PH, Gordon T. 1997. The expression of the low affinity nerve growth factor receptor in long-term denervated Schwann cells. Glia 20:87-100
395. Young SH, Poo MM. 1983. Spontaneous release of transmitter from growth cones of embryonic neurones. Nature 305:634-37
396. Zhang M, McLennan IS. 1995. During secondary myotube formation, primary, myotubes preferentially absorb new nuclei at their ends. Dev. Dynam. 204:168-77
397. Zhou H, Grady RM, Sanes JR. 1998. Muscular dystrophy and impaired aggregation of acetylcholine receptors in α-dystrobrevin-deficient mutant mice. Neurosci. Abstr. 24:1534
398. Zhou H, Muramatsu T, Halfter W, Tsim KW, Peng HB. 1997. A role of midkine in the development of the neuromuscular junction. Mol. Cell. Neurosci. 10:56-70
399. Zhu X, Lai C, Thomas S, Burden SJ. 1995. Neuregulin receptors, erbB3 and erbB4, are localized at neuromuscular synapses. EMBO J. 14:5842-48
400. Zoubine MN, Ma JY, Smirnova IV, Citron BA, Festoff BW. 1996. A molecular mechanism for synapse elimination: novel inhibition of locally generated thrombin delays synapse loss in neonatal mouse muscle. Dev. Biol. 179:447-57