Neuromuscular synaptogenesis: Clustering of acetylcholine receptors revisited

Cellular and Molecular Life Sciences

Volumn 59, Issue 8, 2002, Pages 1296-1316

  Willmann, R ^a   Fuhrer, C ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Acetylcholine receptor; Agrin; Clustering; MuSK; Neuromuscular junction; Postsynaptic preassembly; Rapsyn

Indexed keywords

AGRIN; CHOLINERGIC RECEPTOR; PROTEIN TYROSINE KINASE; RAPSYN;

CELL COMMUNICATION; HUMAN; MOTONEURON; NERVE ENDING; NEUROMUSCULAR SYNAPSE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PROTEIN ASSEMBLY; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SYNAPTOGENESIS;

ANIMALS; HUMANS; NEUROMUSCULAR JUNCTION; RECEPTORS, CHOLINERGIC;

EID: 0036693564     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00018-002-8509-4     Document Type: Review

References (165)

1. Development of the vertebrate neuromuscular junction
2. Clustering of nicotinic acetylcholine receptors: From the neuromuscular junction to interneuronal synapses
3. The formation of neuromuscular synapses
4. Formation of the neuromuscular junction. Agrin and its unusual receptors
5. Formation of the neuromuscular junction: Molecules and mechanisms
6. Induction, assembly, maturation and maintenance of a postsynaptic apparatus
7. Agrin orchestrates synaptic differentiation at the vertebrate neuromuscular junction
8. DNA topoisomerase IIbeta and neural development
9. Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse
10. Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation
11. The agrin hypothesis
12. The agrin gene codes for a family of basal lamina proteins that differ in function and distribution
13. RNA splicing regulates agrin-mediated acetylcholine receptor clustering activity on cultured myotubes
14. An amino-terminal extension is required for the secretion of chick agrin and its binding to extracellular matrix
15. Agrin isoforms with distinct amino termini: Differential expression, localization, and function
16. An alternative amino-terminus expressed in the central nervous system converts agrin to a type II transmembrane protein
17. Structure and expression of a rat agrin
18. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice
19. Alternatively spliced isoforms of nerve- and muscle-derived agrin: Their roles at the neuromuscular junction
20. Agrin-induced postsynaptic-like apparatus in skeletal muscle fibers in vivo
21. Neural agrin induces ectopic postsynaptic specializations in innervated muscle fibers
22. Induction by agrin of ectopic and functional postsynaptic-like membrane in innervated muscle
23. Neuregulins and erbB receptors at neuromuscular junctions and at agrin- induced postsynaptic-like apparatus in skeletal muscle
24. gamma-AChR/epsilon-AChR switch at agrin-induced postsynaptic-like apparatus in skeletal muscle
25. Induction of multiple signaling loops by MuSK during neuromuscular synapse formation
26. Agrin is a differentiation-inducing 'stop signal' for motoneurons in vitro
27. Muscle-specific trk-related receptor with a kringle domain defines a distinct class of receptor tyrosine kinases
28. Receptor tyrosine kinase specific for the skeletal muscle lineage: Expression in embryonic muscle, at the neuromuscular junction, and after injury
29. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo
30. Agrin acts via a MuSK receptor complex
31. Constitutively active MuSK is clustered in the absence of agrin and induces ectopic postsynaptic-like membranes in skeletal muscle fibers
32. Distinct domains of MuSK mediate its abilities to induce and to associate with postsynaptic specializations
33. Agrin binding to alpha-dystroglycan. Domains of agrin necessary to induce acetylcholine receptor clustering are overlapping but not identical to the alpha-dystroglycan-binding region
34. Alternative splicing of agrin alters its binding to heparin, dystroglycan, and the putative agrin receptor
35. Tyrosine phosphorylation of the muscle-specific kinase is exclusively induced by acetylcholine receptor-aggregating agrin fragments
36. alpha-Dystroglycan functions in acetylcholine receptor aggregation but is not a coreceptor for agrin-MuSK signaling
37. Role for a synapse-specific carbohydrate in agrin-induced clustering of acetylcholine receptors
38. N-acetyllactosamine and the CT carbohydrate antigen mediate agrin- dependent activation of MuSK and acetylcholine receptor clustering in skeletal muscle
39. Modulation of agrin binding and activity by the CT and related carbohydrate antigens
40. The in vitro and in vivo phosphotyrosine map of activated MuSK
41. The juxtamembrane region of MuSK has a critical role in agrin-mediated signaling
42. MAGI-1 c: A synaptic MAGUK interacting with muSK at the vertebrate neuromuscular junction
43. Distinct protein components from Torpedo marmorata membranes carry the acetylcholine receptor site and the binding site for local anesthetics and histrionicotoxin
44. Crosslinking of proteins in acetylcholine receptor-rich membranes: Association between the beta-subunit and the 43 kd subsynaptic protein
45. Characterization and localization of the Mr=43,000 proteins associated with acetylcholine receptor-rich membranes
46. Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice
47. Rapsyn is required for MuSK signaling and recruits synaptic components to a MuSK-containing scaffold
48. ACh receptor-rich membrane domains organized in fibroblasts by recombinant 43-kildalton protein
49. Rapsyn clusters and activates the synapse-specific receptor tyrosine kinase MuSK
50. Rapsyn may function as a link between the acetylcholine receptor and the agrin-binding dystrophin-associated glycoprotein complex
51. The postsynaptic 43K protein clusters muscle nicotinic acetylcholine receptors in Xenopus oocytes
52. To muster a cluster: Anchoring neurotransmitter receptors at synapses
53. Mutagenesis of the 43-kD postsynaptic protein defines domains involved in plasma membrane targeting and AChR clustering
54. Mechanism of nicotinic acetylcholine receptor cluster formation by rapsyn
55. Role of rapsyn tetratricopeptide repeat and coiled-coil domains in self- association and nicotinic acetylcholine receptor clustering
56. The intracellular domain of the nicotinic acetylcholine receptor alpha subunit mediates its coclustering with rapsyn
57. Evidence for in sim and in vitro association between betadystroglycan and the subsynaptic 43K rapsyn protein. Consequence for acetylcholine receptor clustering at the synapse
58. Interactions of the rapsyn RING-H2 domain with dystroglycan
59. Comparison of the postsynaptic 43-kDa protein from muscle cells that differ in acetylcholine receptor clustering activity
60. Determination of the tissue distributions and relative concentrations of the post-synaptic 43-kDa protein and the acetylcholine receptor in Torpedo
61. Increased expression of the 43-kD protein disrupts acetylcholine receptor clustering in myotubes
62. Overexpression of rapsyn inhibits agrin-induced acetylcholine receptor clustering in muscle cells
63. Overexpression of rapsyn modifies the intracellular trafficking of acetylcholine receptors
64. The myristoylated protein rapsyn is cotargeted with the nicotinic acetylcholine receptor to the post-synaptic membrane via the exocytic pathway
65. Differential targeting of components of the dystrophin complex to the postsynaptic membrane
66. Acetylcholine receptors are required for agrin-induced clustering of postsynaptic proteins
67. Agrin-induced phosphorylation of the acetylcholine receptor regulates cytoskeletal anchoring and clustering
68. Agrin-induced activation of AChR-bound Src family kinases requires rapsyn and correlates with AChR clustering
69. Src-class kinases act within the agrin/MuSK pathway to regulate acetylcholine receptor phosphorylation, cytoskeletal anchoring, and clustering
70. Src, Fyn and Yes are not required for neuromuscular synapse formation but are necessary for stabilization of agrin-induced clusters of acetylcholine receptors
71. Mechanism of agrin-induced acetylcholine receptor aggregation
72. Agrin-induced acetylcholine receptor clustering in mammalian muscle requires tyrosine phosphorylation
73. The submembrane machinery for nicotinic acetylcholine receptor clustering
74. Immobilization of nicotinic acetylcholine receptors in mouse C2 myotubes by agrin-induced protein tyrosine phosphorylation
75. Staurosporine inhibits agrin-induced acetylcholine receptor phosphorylation and aggregation
76. Regulation of the interaction of nicotinic acetylcholine receptors with the cytoskeleton by agrin-activated protein tyrosine kinase
77. Recruitment of a nicotinic acetylcholine receptor mutant lacking cytoplasmic tyrosine residues in its beta subunit into agrin-induced aggregates
78. Association of muscle-specific kinase MuSK with the acetylcholine receptor in mammalian muscle
79. Functional interaction of Src family kinases with the acetylcholine receptor in C2 myotubes
80. Molecular cloning of two abundant protein tyrosine kinases in Torpedo electric organ that associate with the acetylcholine receptor
81. Acetylcholine receptors are required for postsynaptic aggregation driven by the agrin signalling pathway
82. Paralytic zebrafish lacking acetylcholine receptors fail to localize rapsyn clusters to the synapse
83. Pathfinding and synapse formation in a zebrafish mutant lacking functional acetylcholine receptors
84. Roles of rapsyn and agrin in interaction of postsynaptic proteins with acetylcholine receptors
85. Accumulation of acetylcholine receptors is a necessary condition for normal accumulation of acetylcholinesterase during in vitro neuromuscular synaptogenesis
86. Acetylcholinesterase clustering at the neuromuscular junction involves perlecan and dystroglycan
87. Absence of acetylcholinesterase at the neuromuscular junctions of perlecan-null mice
88. Deficient development and maintenance of postsynaptic specializations in mutant mice lacking an 'adult' acetylcholine receptor subunit
89. Different functions of fetal and adult AChR subtypes for the formation and maintenance of neuromuscular synapses revealed in epsilon-subunit-deficient mice
90. Rapid formation and remodeling of postsynaptic densities in developing dendrites
91. Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin
92. Assembly of presynaptic active zones from cytoplasmic transport packets
93. Assembling the presynaptic active zone: A characterization of an active zone precursor vesicle
94. Intracellular calcium regulates agrin-induced acetylcholine receptor clustering
95. Dual role for calcium in agrin signaling and acetylcholine receptor clustering
96. Agrin-induced acetylcholine receptor clustering is mediated by the small guanosine triphosphatases Rac and Cdc42
97. The actin-driven movement and formation of acetylcholine receptor clusters
98. Subtle neuromuscular defects in utrophin-deficient mice
99. Nitric oxide is a downstream mediator of agrin-induced acetylcholine receptor aggregation
100. Nitric oxide synthase (NOS-1) coclustered with agrin-induced AChR-specializations on cultured skeletal myotubes
101. Nitric oxide controls src kinase activity through a sulfhydryl group modification-mediated Tyr-527-independent and Tyr-416-linked mechanism
102. ARIA: A neuromuscular junction neuregulin
103. Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction in vivo
104. Regulation by ARIA/neuregulin of acetylcholine receptor gene transcription at the neuromuscular junction
105. Targeting transcription to the neuromuscular synapse
106. Synapse-associated expression of an acetylcholine receptor-inducing protein, ARIA/heregulin, and its putative receptors, ErbB2 and ErbB3, in developing mammalian muscle
107. Neuregulin receptors, erbB3 and erbB4, are localized at neuromuscular synapses
108. The Agrin/MuSK signaling pathway is spatially segregated from the neuregulin/ErbB receptor signaling pathway at the neuromuscular junction
109. Induction of acetylcholine receptor gene expression by ARIA requires activation of mitogen-activated protein kinase
110. Heregulin-stimulated acetylcholine receptor gene expression in muscle: Requirement for MAP kinase and evidence for a parallel inhibitory pathway independent of electrical activity
111. Neuregulin-increased expression of acetylcholine receptor epsilon- subunit gene requires ErbB interaction with Shc
112. AR1A/HRG regulates AChR epsilon subunit gene expression at the neuromuscular synapse via activation of phosphatidylinositol 3-kinase and Ras/MAPK pathway
113. Essential roles of c-JUN and c-JUN N-terminal kinase (JNK) in neuregulin-increased expression of the acetylcholine receptor epsilon subunit
114. Implication of a multisubunit Ets-related transcription factor in synaptic expression of the nicotinic acetylcholine receptor
115. The Ets transcription factor GABP is required for postsynaptic differentiation in vivo
116. Synapse-specific and neuregulin-induced transcription require an ets site that binds GABPalpha/GABPbeta
117. Identification of a DNA element determining synaptic expression of the mouse acetylcholine receptor delta-subunit gene
118. Identification of an element crucial for the sub-synaptic expression of the acetylcholine receptor epsilon-subunit gene
119. Protein-tyrosine phosphatases specifically regulate muscle adult-type nicotinic acetylcholine receptor gene expression
120. Regulation of neuregulin-mediated acetylcholine receptor synthesis by protein tyrosine phosphatase SHP2
121. Cdk5 is involved in neuregulin-induced AChR expression at the neuromuscular junction
122. N-CAM, 43K-rapsyn and S-laminin mRNAs are concentrated at synaptic sites in muscle fibers
123. Compartmentalization of acetylcholinesterase mRNA and enzyme at the vertebrate neuromuscular junction
124. Local transcriptional control of utrophin expression at the neuromuscular synapse
125. Induction of utrophin gene expression by heregulin in skeletal muscle cells: Role of the N-box motif and GA binding protein
126. An intronic enhancer containing an N-box motif is required for synapse- and tissue-specific expression of the acetylcholinesterase gene in skeletal muscle fibers
127. Substrate-bound agrin induces expression of acetylcholine receptor epsilon-subunit gene in cultured mammalian muscle cells
128. MuSK induces in vivo acetylcholine receptor clusters in a ligand-independent manner
129. Agrin can mediate acetylcholine receptor gene expression in muscle by aggregation of muscle-derived neuregulins
130. Cloning and characterization of muscle-specific kinase in chicken
131. Neural influence on acetylcholine receptor clusters in embryonic development of skeletal muscles
132. Embryonic growth and innervation of rat skeletal muscles. III. Neural regulation of junctional and extrajunctional acetylcholine receptor clusters
133. Challenging the neurocentric view of neuromuscular synapse formation
134. Synapse formation revisited
135. Patterning of skeletal muscle
136. Laminin-induced acetylcholine receptor clustering: An alternative pathway
137. Laminin and alpha-dystroglycan mediate acetylcholine receptor aggregation via a MuSK-independent pathway
138. Laminin and α7β1 integrin regulate agrin-induced clustering of acetylcholine receptors
139. Distribution and function of laminins in the neuromuscular system of developing, adult, and mutant mice
140. Laminin redistributes postsynaptic proteins and requires rapsyn, tyrosine phosphorylation, and Src and Fyn to stably cluster acetylcholine receptors
141. Synapse elimination and indelible memory
142. From plaque to pretzel: Fold formation and acetylcholine receptor loss at the developing neuromuscular junction
143. Muscular dystrophies and the dystrophin-glycoprotein complex
144. Three muscular dystrophies: Loss of cytoskeleton-extracellular matrix linkage
145. Assembly of the postsynaptic apparatus
146. Characterisation of alpha-dystrobrevin in muscle
147. Syntrophin isoforms at the neuromuscular junction: Developmental time course and differential localization
148. Postsynaptic abnormalities at the neuromuscular junctions of utrophin-deficient mice
149. Structure and function of the neuromuscular junction in young adult mdx mice
150. The mutant mdx: Inherited myopathy in the mouse. Morphological studies of nerves, muscles and end-plates
151. Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: A model for Duchenne muscular dystrophy
152. Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy
153. Chimaeric mice deficient in dystroglycans develop muscular dystrophy and have disrupted myoneural synapses
154. The dystroglycan complex is necessary for stabilization of acetylcholine receptor clusters at neuromuscular junctions and formation of the synaptic basement membrane
155. Maturation and maintenance of the neuromuscular synapse: Genetic evidence for roles of the dystrophin-glycoprotein complex
156. Role for alpha-dystrobrevin in the pathogenesis of dystrophin-dependent muscular dystrophies
157. Absence of alpha-syntrophin leads to structurally aberrant neuromuscular synapses deficient in utrophin
158. alpha1-syntrophin gene disruption results in the absence of neuronal-type nitric-oxide synthase at the sarcolemma but does not induce muscle degeneration
159. c-Src enhances the spreading of src-/- fibroblasts on fibronectin by a kinase-independent mechanism
160. SH2- and SH3-mediated interactions between focal adhesion kinase and Src
161. Disruption of Trkb-mediated signaling induces disassembly of postsynaptic receptor clusters at neuromuscular junctions
162. Association of the Src family tyrosine kinase Fyn with TrkB
163. Neurotrophins regulate agrin-induced post-synaptic differentiation
164. The 87K postsynaptic membrane protein from Torpedo is a protein-tyrosine kinase substrate homologous to dystrophin
165. Acetylcholine receptor epsilon-subunit deletion causes muscle weakness and atrophy in juvenile and adult mice