To build a synapse: Signaling pathways in neuromuscular junction assembly

Development

Volumn 137, Issue 7, 2010, Pages 1017-1033

  Wu, Haitao ^a   Xiong, Wen C ^a   Mei, Lin ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Neural development; Neuromuscular junction; Retrograde signaling; Synapse formation

Indexed keywords

AGRIN; BETA CATENIN; BETA1 INTEGRIN; CHOLINERGIC RECEPTOR; COLLAGEN; FIBROBLAST GROWTH FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; LAMININ; LRP4 PROTEIN; MUSK PROTEIN; PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WNT PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; PROTEIN TYROSINE KINASE;

BRAIN; CELL INTERACTION; CELL MATURATION; GLIA CELL; HUMAN; MOTONEURON; MUSCLE CELL; MUSCULAR DYSTROPHY; NERVE CELL; NERVE FIBER; NERVE GROWTH; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTOGENESIS; VERTEBRATE; ANIMAL; CYTOLOGY; GLIA; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT; SKELETAL MUSCLE; SYNAPTIC TRANSMISSION; ULTRASTRUCTURE;

ANIMALIA;

AGRIN; ANIMALS; COLLAGEN; FIBROBLAST GROWTH FACTORS; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; LAMININ; MOTOR NEURONS; MUSCLE FIBERS, SKELETAL; NEUROGLIA; NEUROMUSCULAR JUNCTION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, CHOLINERGIC; RECEPTORS, LDL; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION; WNT PROTEINS;

EID: 77950462859     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.038711     Document Type: Review

References (220)

1. Aberle, H., Haghighi, A. P., Fetter, R. D., McCabe, B. D., Magalhaes, T. R. and Goodman, C. S. (2002). wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 33, 545-558. (Pubitemid 34188431)
2. Adams, L., Carlson, B. M., Henderson, L. and Goldman, D. (1995). Adaptation of nicotinic acetylcholine receptor, myogenin, and MRF4 gene expression to long-term muscle denervation. J. Cell Biol. 131, 1341-1349.
3. Adams, M. E., Kramarcy, N., Fukuda, T., Engel, A. G., Sealock, R. and Froehner, S. C. (2004). Structural abnormalities at neuromuscular synapses lacking multiple syntrophin isoforms. J. Neurosci. 24, 10302-10309. (Pubitemid 39552613)
4. Akaaboune, M., Culican, S. M., Turney, S. G. and Lichtman, J. W. (1999). Rapid and reversible effects of activity on acetylcholine receptor density at the neuromuscular junction in vivo. Science 286, 503-557.
5. Anderson, M. J. and Cohen, M. W. (1977). Nerve-induced and spontaneous redistribution of acetylcholine receptors on cultured muscle cells. J. Physiol. 268, 757-773. (Pubitemid 8154323)
6. Antolik, C., Catino, D. H., Resneck, W. G. and Bloch, R. J. (2006). The tetratricopeptide repeat domains of rapsyn bind directly to cytoplasmic sequences of the muscle-specific kinase. Neuroscience 141, 87-100.
7. Apel, E. D., Roberds, S. L., Campbell, K. P. and Merlie, J. P. (1995). Rapsyn may function as a link between the acetylcholine receptor and the agrin-binding dystrophin-associated glycoprotein complex. Neuron 15, 115-126.
8. Apel, E. D., Glass, D. J., Moscoso, L. M., Yancopoulos, G. D. and Sanes, J. R. (1997). Rapsyn is required for MuSK signaling and recruits synaptic components to a MuSK-containing scaffold. Neuron 18, 623-635.
9. Apel, E. D., Lewis, R. M., Grady, R. M. and Sanes, J. R. (2000). Syne-1, a dystrophin- and Klarsicht-related protein associated with synaptic nuclei at the neuromuscular junction. J. Biol. Chem. 275, 31986-31995.
10. Arikawa-Hirasawa, E., Rossi, S. G., Rotundo, R. L. and Yamada, Y. (2002). Absence of acetylcholinesterase at the neuromuscular junctions of perlecan-null mice. Nat. Neurosci. 5, 119-123. (Pubitemid 34121578)
11. Ataman, B., Ashley, J., Gorczyca, D., Gorczyca, M., Mathew, D., Wichmann, C., Sigrist, S. J. and Budnik, V. (2006). Nuclear trafficking of Drosophila Frizzled-2 during synapse development requires the PDZ protein dGRIP. Proc. Natl. Acad. Sci. USA 103, 7841-7846. (Pubitemid 43752868)
12. Aucott, R., Bullwinkel, J., Yu, Y., Shi, W., Billur, M., Brown, J. P., Menzel, U., Kioussis, D., Wang, G., Reisert, I. et al. (2008). HP1-beta is required for development of the cerebral neocortex and neuromuscular junctions. J. Cell Biol. 183, 597-606.
13. Augustin, H., Grosjean, Y., Chen, K., Sheng, Q. and Featherstone, D. E. (2007). Nonvesicular release of glutamate by glial xCT transporters suppresses glutamate receptor clustering in vivo. J. Neurosci. 27, 111-123. (Pubitemid 46089965)
14. Awatramani, R., Shumas, S., Kamholz, J. and Scherer, S. S. (2002). TGFbeta1 modulates the phenotype of Schwann cells at the transcriptional level. Mol. Cell Neurosci. 19, 307-319. (Pubitemid 34293455)
15. Banks, G. B., Chamberlain, J. S. and Froehner, S. C. (2009). Truncated dystrophins can influence neuromuscular synapse structure. Mol. Cell Neurosci. 40, 433-441.
16. Baudet, C., Pozas, E., Adameyko, I., Andersson, E., Ericson, J. and Ernfors, P. (2008). Retrograde signaling onto Ret during motor nerve terminal maturation. J. Neurosci. 28, 963-975. (Pubitemid 351159003)
17. Bevan, S. and Steinbach, J. H. (1977). The distribution of alpha-bungarotoxin binding sites of mammalian skeletal muscle developing in vivo. J. Physiol. 267, 195-213. (Pubitemid 8090831)
18. Bezakova, G., Helm, J. P., Francolini, M. and Lomo, T. (2001). Effects of purified recombinant neural and muscle agrin on skeletal muscle fibers in vivo. J. Cell Biol. 153, 1441-1452. (Pubitemid 34286128)
19. Bishop, D. L., Misgeld, T., Walsh, M. K., Gan, W. B. and Lichtman, J. W. (2004). Axon branch removal at developing synapses by axosome shedding. Neuron 44, 651-661. (Pubitemid 39531229)
20. Bloch, R. J. (1986). Actin at receptor-rich domains of isolated acetylcholine receptor clusters. J. Cell Biol. 102, 1447-1458.
21. Borges, L. S. and Ferns, M. (2001). Agrin-induced phosphorylation of the acetylcholine receptor regulates cytoskeletal anchoring and clustering. J. Cell Biol. 153, 1-12.
22. Braithwaite, A. W. and Harris, A. J. (1979). Neural influence on acetylcholine receptor clusters in embryonic development of skeletal muscles. Nature 279, 549-551.
23. Brandon, E. P., Lin, W., D'Amour, K. A., Pizzo, D. P., Dominguez, B., Sugiura, Y., Thode, S., Ko, C. P., Thal, L. J., Gage, F. H. et al. (2003). Aberrant patterning of neuromuscular synapses in choline acetyltransferase- deficient mice. J. Neurosci. 23, 539-549. (Pubitemid 36139553)
24. Bromann, P. A., Weiner, J. A., Apel, E. D., Lewis, R. M. and Sanes, J. R. (2004). A putative ariadne-like E3 ubiquitin ligase (PAUL) that interacts with the muscle-specific kinase (MuSK). Gene Expr. Patterns 4, 77-84.
25. Bruneau, E., Sutter, D., Hume, R. I. and Akaaboune, M. (2005). Identification of nicotinic acetylcholine receptor recycling and its role in maintaining receptor density at the neuromuscular junction in vivo. J. Neurosci. 25, 9949-9959. (Pubitemid 41528033)
26. Burden, S. J. (2000). Wnts as retrograde signals for axon and growth cone differentiation. Cell 100, 495-497.
27. Burden, S. J., DePalma, R. L. and Gottesman, G. S. (1983). Crosslinking of proteins in acetylcholine receptor-rich membranes: association between the beta-subunit and the 43 kd subsynaptic protein. Cell 35, 687-692.
28. Burden, S. J., Jo, S. A., Tang, J., Zhu, X., Yeadon, J. E. and Simon, A. M. (1995). Polarity in skeletal muscle cells is induced by innervation. Sem. Dev. Biol. 6, 59-65.
29. Campanelli, J. T., Hoch, W., Rupp, F., Kreiner, T. and Scheller, R. H. (1991). Agrin mediates cell contact-induced acetylcholine receptor clustering. Cell 67, 909-916. (Pubitemid 121001505)
30. Cao, G. and Ko, C. P. (2007). Schwann cell-derived factors modulate synaptic activities at developing neuromuscular synapses. J. Neurosci. 27, 6712-6722. (Pubitemid 46983427)
31. Cartaud, A., Strochlic, L., Guerra, M., Blanchard, B., Lambergeon, M., Krejci, E., Cartaud, J. and Legay, C. (2004). MuSK is required for anchoring acetylcholinesterase at the neuromuscular junction. J. Cell Biol. 165, 505-515. (Pubitemid 38679616)
32. Chen, F., Qian, L., Yang, Z. H., Huang, Y., Ngo, S. T., Ruan, N. J., Wang, J., Schneider, C., Noakes, P. G., Ding, Y. Q. et al. (2007). Rapsyn interaction with calpain stabilizes AChR clusters at the neuromuscular junction. Neuron 55, 247-260. (Pubitemid 47048911)
33. Chen, F., Sugiura, Y., Myers, K. G., Liu, Y. and Lin, W. (2010). Ubiquitin carboxyl-terminal hydrolase L1 is required for maintaining the structure and function of the neuromuscular junction. Proc. Natl. Acad. Sci. USA 107, 1636-1641.
34. Chen, P. C., Qin, L. N., Li, X. M., Walters, B. J., Wilson, J. A., Mei, L. and Wilson, S. M. (2009). The proteasome-associated deubiquitinating enzyme Usp14 is essential for the maintenance of synaptic ubiquitin levels and the development of neuromuscular junctions. J. Neurosci. 29, 10909-10919.
35. Cheusova, T., Khan, M. A., Schubert, S. W., Gavin, A. C., Buchou, T., Jacob, G., Sticht, H., Allende, J., Boldyreff, B., Brenner, H. R. et al. (2006). Casein kinase 2-dependent serine phosphorylation of MuSK regulates acetylcholine receptor aggregation at the neuromuscular junction. Genes Dev. 20, 1800-1816. (Pubitemid 43992888)
36. Christopherson, K. S., Ullian, E. M., Stokes, C. C., Mullowney, C. E., Hell, J. W., Agah, A., Lawler, J., Mosher, D. F., Bornstein, P. and Barres, B. A. (2005). Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120, 421-433. (Pubitemid 40222435)
37. Creazzo, T. L. and Sohal, G. S. (1983). Neural control of embryonic acetylcholine receptor and skeletal muscle. Cell Tissue Res. 228, 1-12.
38. Dai, Z., Luo, X., Xie, H. and Peng, H. B. (2000). The actin-driven movement and formation of acetylcholine receptor clusters. J. Cell Biol. 150, 1321-1334.
39. DeChiara, T. M., Bowen, D. C., Valenzuela, D. M., Simmons, M. V., Poueymirou, W. T., Thomas, S., Kinetz, E., Compton, D. L., Rojas, E., Park, J. S. et al. (1996). The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85, 501-512. (Pubitemid 26157189)
40. Derynck, R. and Zhang, Y. E. (2003). Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425, 577-584. (Pubitemid 37280136)
41. Dobbins, G. C., Luo, S., Yang, Z., Xiong, W. C. and Mei, L. (2008). alpha-Actinin interacts with rapsyn in agrin-stimulated AChR clustering. Mol. Brain 1, 18.
42. Dong, X. P., Li, X. M., Gao, T. M., Zhang, E. E., Feng, G. S., Xiong, W. C. and Mei, L. (2006). Shp2 is dispensable in the formation and maintenance of the neuromuscular junction. Neurosignals 15, 53-63. (Pubitemid 44260253)
43. Dudu, V., Bittig, T., Entchev, E., Kicheva, A., Julicher, F. and Gonzalez-Gaitan, M. (2006). Postsynaptic mad signaling at the Drosophila neuromuscular junction. Curr. Biol. 16, 625-635.
44. Edwards, C. and Frisch, H. L. (1976). A model for the localization of acetylcholine receptors at the muscle endplate. J. Neurobiol. 7, 377-381.
45. Edwards, D. C., Sanders, L. C., Bokoch, G. M. and Gill, G. N. (1999). Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat. Cell. Biol. 1, 253-259.
46. Engel, A. G., Shen, X. M., Selcen, D. and Sine, S. M. (2008). Further observations in congenital myasthenic syndromes. Ann. New York Acad. Sci. 1132, 104-113. (Pubitemid 351841379)
47. Escher, P., Lacazette, E., Courtet, M., Blindenbacher, A., Landmann, L., Bezakova, G., Lloyd, K. C., Mueller, U. and Brenner, H. R. (2005). Synapses form in skeletal muscles lacking neuregulin receptors. Science 308, 1920-1923. (Pubitemid 40941877)
48. Evers, J., Laser, M., Sun, Y. A., Xie, Z. P. and Poo, M. M. (1989). Studies of nerve-muscle interactions in Xenopus cell culture: analysis of early synaptic currents. J. Neurosci. 9, 1523-1539. (Pubitemid 19146250)
49. Feng, X. H. and Derynck, R. (2005). Specificity and versatility in tgf-beta signaling through Smads. Annu. Rev. Cell Dev. Biol. 21, 659-693.
50. Feng, Z. and Ko, C. P. (2008). Schwann cells promote synaptogenesis at the neuromuscular junction via transforming growth factor-beta1. J. Neurosci. 28, 9599-9609.
51. Finn, A. J., Feng, G. and Pendergast, A. M. (2003). Postsynaptic requirement for Abl kinases in assembly of the neuromuscular junction. Nat. Neurosci. 6, 717-723.
52. Fischbach, G. D. and Rosen, K. M. (1997). ARIA: a neuromuscular junction neuregulin. Annu. Rev. Neurosci. 20, 429-458.
53. Flanagan-Steet, H., Fox, M. A., Meyer, D. and Sanes, J. R. (2005). Neuromuscular synapses can form in vivo by incorporation of initially aneural postsynaptic specializations. Development 132, 4471-4481. (Pubitemid 41632226)
54. Fox, M. A., Sanes, J. R., Borza, D. B., Eswarakumar, V. P., Fassler, R., Hudson, B. G., John, S. W., Ninomiya, Y., Pedchenko, V., Pfaff, S. L. et al. (2007). Distinct target-derived signals organize formation, maturation, and maintenance of motor nerve terminals. Cell 129, 179-193. (Pubitemid 46507579)
55. Franciscovich, A. L., Mortimer, A. D., Freeman, A. A., Gu, J. and Sanyal, S. (2008). Overexpression screen in Drosophila identifies neuronal roles of GSK-3 beta/shaggy as a regulator of AP-1-dependent developmental plasticity. Genetics 180, 2057-2071.
56. Franco, B., Bogdanik, L., Bobinnec, Y., Debec, A., Bockaert, J., Parmentier, M. L. and Grau, Y. (2004). Shaggy, the homolog of glycogen synthase kinase 3, controls neuromuscular junction growth in Drosophila. J. Neurosci. 24, 6573-6577. (Pubitemid 38971706)
57. Froehner, S. C. (1993). Regulation of ion channel distribution at synapses. Ann. Rev. Neuro. 16, 347-368.
58. Fu, A. K., Ip, F. C., Fu, W. Y., Cheung, J., Wang, J. H., Yung, W. H. and Ip, N. Y. (2005). Aberrant motor axon projection, acetylcholine receptor clustering, and neurotransmission in cyclin-dependent kinase 5 null mice. Proc. Natl. Acad. Sci. USA 102, 15224-15229. (Pubitemid 41513363)
59. Fuentes-Medel, Y., Logan, M. A., Ashley, J., Ataman, B., Budnik, V. and Freeman, M. R. (2009). Glia and muscle sculpt neuromuscular arbors by engulfing destabilized synaptic boutons and shed presynaptic debris. PLoS Biol. 7, e1000184.
60. Fuhrer, C., Sugiyama, J. E., Taylor, R. G. and Hall, Z. W. (1997). Association of muscle-specific kinase MuSK with the acetylcholine receptor in mammalian muscle. EMBO J. 16, 4951-4960. (Pubitemid 27348404)
61. Gautam, M., Noakes, P. G., Mudd, J., Nichol, M., Chu, G. C., Sanes, J. R. and Merlie, J. P. (1995). Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377, 232-236.
62. Gautam, M., Noakes, P. G., Moscoso, L., Rupp, F., Scheller, R. H., Merlie, J. P. and Sanes, J. R. (1996). Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85, 525-535. (Pubitemid 26157191)
63. Gendrel, M., Rapti, G., Richmond, J. E. and Bessereau, J. L. (2009). A secreted complement-control-related protein ensures acetylcholine receptor clustering. Nature 461, 992-996.
64. Gesemann, M., Denzer, A. J. and Ruegg, M. A. (1995). Acetylcholine receptor-aggregating activity of agrin isoforms and mapping of the active site. J. Cell Biol. 128, 625-636.
65. Glass, D. J., Bowen, D. C., Stitt, T. N., Radziejewski, C., Bruno, J., Ryan, T. E., Gies, D. R., Shah, S., Mattsson, K., Burden, S. J. et al. (1996). Agrin acts via a MuSK receptor complex. Cell 85, 513-523. (Pubitemid 26157190)
66. Godfrey, E. W., Nitkin, R. M., Wallace, B. G., Rubin, L. L. and McMahan, U. J. (1984). Components of Torpedo electric organ and muscle that cause aggregation of acetylcholine receptors on cultured muscle cells. J. Cell Biol. 99, 615-627.
67. Gogel, S., Wakefield, S., Tear, G., Klambt, C. and Gordon-Weeks, P. R. (2006). The Drosophila microtubule associated protein Futsch is phosphorylated by Shaggy/Zeste-white 3 at an homologous GSK3beta phosphorylation site in MAP1B. Mol. Cell Neurosci. 33, 188-199. (Pubitemid 44430060)
68. Gordon, K. J. and Blobe, G. C. (2008). Role of transforming growth factor-beta superfamily signaling pathways in human disease. Biochim. Biophys. Acta 1782, 197-228.
69. Grady, R. M., Zhou, H., Cunningham, J. M., Henry, M. D., Campbell, K. P. and Sanes, J. R. (2000). Maturation and maintenance of the neuromuscular synapse: genetic evidence for roles of the dystrophin-glycoprotein complex. Neuron 25, 279-293.
70. Grady, R. M., Akaaboune, M., Cohen, A. L., Maimone, M. M., Lichtman, J. W. and Sanes, J. R. (2003). Tyrosine-phosphorylated and nonphosphorylated isoforms of alpha-dystrobrevin: roles in skeletal muscle and its neuromuscular and myotendinous junctions. J. Cell Biol. 160, 741-752. (Pubitemid 36298269)
71. Hall, A. C., Lucas, F. R. and Salinas, P. C. (2000). Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 100, 525-535.
72. Hall, Z. W. and Sanes, J. R. (1993). Synaptic structure and development: the neuromuscular junction. Cell 72, 99-121.
73. Hamburger, V. (1934). The effects of wing bud extirpation on the development of the central nervous system in chick embryos. J. Exp. Zool. 68, 449-494.
74. Hayworth, C. R., Moody, S. E., Chodosh, L. A., Krieg, P., Rimer, M. and Thompson, W. J. (2006). Induction of neuregulin signaling in mouse schwann cells in vivo mimics responses to denervation. J. Neurosci. 26, 6873-6884. (Pubitemid 44315248)
75. Henriquez, J. P., Webb, A., Bence, M., Bildsoe, H., Sahores, M., Hughes, S. M. and Salinas, P. C. (2008). Wnt signaling promotes AChR aggregation at the neuromuscular synapse in collaboration with agrin. Proc. Natl. Acad. Sci. USA 105, 18812-18817.
76. Herbst, R. and Burden, S. J. (2000). The juxtamembrane region of MuSK has a critical role in agrin-mediated signaling. EMBO J. 19, 67-77. (Pubitemid 30009226)
77. Herbst, R., Iskratsch, T., Unger, E. and Bittner, R. E. (2009). Aberrant development of neuromuscular junctions in glycosylation-defective Large(myd) mice. Neuromuscul. Disord. 19, 366-378.
78. Herz, J. and Bock, H. H. (2002). Lipoprotein receptors in the nervous system. Annu. Rev. Biochem. 71, 405-434.
79. Hess, D. M., Scott, M. O., Potluri, S., Pitts, E. V., Cisterni, C. and Balice-Gordon, R. J. (2007). Localization of TrkC to Schwann cells and effects of neurotrophin-3 signaling at neuromuscular synapses. J. Comp. Neurol. 501, 465-482. (Pubitemid 46622490)
80. Heupel, K., Sargsyan, V., Plomp, J. J., Rickmann, M., Varoqueaux, F., Zhang, W. and Krieglstein, K. (2008). Loss of transforming growth factor-beta 2 leads to impairment of central synapse function. Neural Dev. 3, 25.
81. Hoang, B. and Chiba, A. (2001). Single-cell analysis of Drosophila larval neuromuscular synapses. Dev. Biol. 229, 55-70. (Pubitemid 32061714)
82. Inaki, M., Yoshikawa, S., Thomas, J. B., Aburatani, H. and Nose, A. (2007). Wnt4 is a local repulsive cue that determines synaptic target specificity. Curr. Biol. 17, 1574-1579. (Pubitemid 47380398)
83. Jennings, C. G. B., Dyer, S. M. and Burden, S. J. (1993). Muscle-specific trk-related receptor with a kringle domain defines a distinct class of receptor tyrosine kinases. Proc. Natl. Acad. Sci. USA 90, 2895-2899.
84. Jevsek, M., Jaworski, A., Polo-Parada, L., Kim, N., Fan, J., Landmesser, L. T. and Burden, S. J. (2006). CD24 is expressed by myofiber synaptic nuclei and regulates synaptic transmission. Proc. Natl. Acad. Sci. USA 103, 6374-6379.
85. Jiang, Y., McLennan, I. S., Koishi, K. and Hendry, I. A. (2000). Transforming growth factor-beta 2 is anterogradely and retrogradely transported in motoneurons and up-regulated after nerve injury. Neuroscience 97, 735-742. (Pubitemid 30332180)
86. Jin, Y. and Garner, C. C. (2008). Molecular mechanisms of presynaptic differentiation. Annu. Rev. Cell Dev. Biol. 24, 237-262.
87. Jing, L., Lefebvre, J. L., Gordon, L. R. and Granato, M. (2009). Wnt signals organize synaptic prepattern and axon guidance through the zebrafish unplugged/MuSK receptor. Neuron 61, 721-733.
88. Johnson, E. B., Hammer, R. E. and Herz, J. (2005). Abnormal development of the apical ectodermal ridge and polysyndactyly in Megf7-deficient mice. Hum. Mol. Genet. 14, 3523-3538.
89. Jones, G., Meier, T., Lichtsteiner, M., Witzemann, V., Sakmann, B. and Brenner, H. R. (1997). Induction by agrin of ectopic and functional postsynaptic-like membrane in innervated muscle. Proc. Natl. Acad. Sci. USA 94, 2654-2659. (Pubitemid 27136931)
90. Jones, N., Hardy, W. R., Friese, M. B., Jorgensen, C., Smith, M. J., Woody, N. M., Burden, S. J. and Pawson, T. (2007). Analysis of a Shc family adaptor protein, ShcD/Shc4, that associates with muscle-specific kinase. Mol. Cell. Biol. 27, 4759-4773. (Pubitemid 47016129)
91. Jorgensen, E. and Nonet, M. L. (1995). Neuromuscular junctions in teh nematode C. elegans. Semin. Dev. Biol. 6, 207-220.
92. Kawasaki, Y., Senda, T., Ishidate, T., Koyama, R., Morishita, T., Iwayama, Y., Higuchi, O. and Akiyama, T. (2000). Asef, a link between the tumor suppressor APC and G-protein signaling. Science 289, 1194-1197. (Pubitemid 30650732)
93. Keller-Peck, C. R., Feng, G., Sanes, J. R., Yan, Q., Lichtman, J. W. and Snider, W. D. (2001). Glial cell line-derived neurotrophic factor administration in postnatal life results in motor unit enlargement and continuous synaptic remodeling at the neuromuscular junction. J. Neurosci. 21, 6136-6146. (Pubitemid 32737746)
94. Keshishian, H., Broadie, K., Chiba, A. and Bate, M. (1996). The drosophila neuromuscular junction: a model system for studying synaptic development and function. Annu. Rev. Neurosci. 19, 545-575. (Pubitemid 26080839)
95. Kim, C. H., Xiong, W. C. and Mei, L. (2003). Regulation of MuSK expression by a novel signaling pathway. J. Biol. Chem. 278, 38522-38527. (Pubitemid 37221747)
96. Kim, N. and Burden, S. J. (2008). MuSK controls where motor axons grow and form synapses. Nat. Neurosci. 11, 19-27.
97. Kim, N., Stiegler, A. L., Cameron, T. O., Hallock, P. T., Gomez, A. M., Huang, J. H., Hubbard, S. R., Dustin, M. L. and Burden, S. J. (2008). Lrp4 is a receptor for Agrin and forms a complex with MuSK. Cell 135, 334-342.
98. Kishi, M., Kummer, T. T., Eglen, S. J. and Sanes, J. R. (2005). LL5beta: a regulator of postsynaptic differentiation identified in a screen for synaptically enriched transcripts at the neuromuscular junction. J. Cell Biol. 169, 355-366. (Pubitemid 40656572)
99. Klassen, M. P. and Shen, K. (2007). Wnt signaling positions neuromuscular connectivity by inhibiting synapse formation in C. elegans. Cell 130, 704-716.
100. Kulkarni, A. B. and Karlsson, S. (1993). Transforming growth factor-beta 1 knockout mice. A mutation in one cytokine gene causes a dramatic inflammatory disease. Am. J. Pathol. 143, 3-9.
101. Kummer, T. T., Misgeld, T. and Sanes, J. R. (2006). Assembly of the postsynaptic membrane at the neuromuscular junction: paradigm lost. Curr. Opin. Neurobiol. 16, 74-82. (Pubitemid 43221856)
102. Lain, E., Carnejac, S., Escher, P., Wilson, M. C., Lomo, T., Gajendran, N. and Brenner, H. R. (2009). A novel role for embigin to promote sprouting of motor nerve terminals at the neuromuscular junction. J. Biol. Chem. 284, 8930-8939.
103. LaRochelle, W. J. and Froehner, S. C. (1986). Determination of the tissue distributions and relative concentrations of the postsynaptic 43-kDa protein and the acetylcholine receptor in Torpedo. J. Biol. Chem. 261, 5270-5274.
104. Lee, C. W., Han, J., Bamburg, J. R., Han, L., Lynn, R. and Zheng, J. Q. (2009). Regulation of acetylcholine receptor clustering by ADF/cofilin-directed vesicular trafficking. Nat. Neurosci. 12, 848-856.
105. Lemke, G. (1993). Transcriptional regulation of the development of neurons and glia. [Review]. Curr. Opin. Neurobiol. 3, 703-708. (Pubitemid 23303373)
106. Levi-Montalcini, R. (1987). The nerve growth factor 35 years later. Science 237, 1154-1162. (Pubitemid 17124912)
107. Li, X. M., Dong, X. P., Luo, S. W., Zhang, B., Lee, D. H., Ting, A. K., Neiswender, H., Kim, C. H., Carpenter-Hyland, E., Gao, T. M. et al. (2008). Retrograde regulation of motoneuron differentiation by muscle beta-catenin. Nat. Neurosci. 11, 262-268. (Pubitemid 351311800)
108. Lichtman, J. W. and Colman, H. (2000). Synapse elimination and indelible memory. Neuron 25, 269-278.
109. Liebl, F. L., Wu, Y., Featherstone, D. E., Noordermeer, J. N., Fradkin, L. and Hing, H. (2008). Derailed regulates development of the Drosophila neuromuscular junction. Dev. Neurobiol. 68, 152-165. (Pubitemid 351199414)
110. Lin, S., Landmann, L., Ruegg, M. A. and Brenner, H. R. (2008). The role of nerve- versus muscle-derived factors in mammalian neuromuscular junction formation. J. Neurosci. 28, 3333-3340. (Pubitemid 351469317)
111. Lin, W., Sanchez, H. B., Deerinck, T., Morris, J. K., Ellisman, M. and Lee, K. F. (2000). Aberrant development of motor axons and neuromuscular synapses in erbB2-deficient mice. Proc. Natl. Acad. Sci. USA 97, 1299-1304. (Pubitemid 30080853)
112. Lin, W., Burgess, R. W., Dominguez, B., Pfaff, S. L., Sanes, J. R. and Lee, K. F. (2001). Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature 410, 1057-1064. (Pubitemid 32391032)
113. Lin, W., Dominguez, B., Yang, J., Aryal, P., Brandon, E. P., Gage, F. H. and Lee, K. F. (2005). Neurotransmitter acetylcholine negatively regulates neuromuscular synapse formation by a Cdk5-dependent mechanism. Neuron 46, 569-579. (Pubitemid 40797382)
114. Linnoila, J., Wang, Y., Yao, Y. and Wang, Z. Z. (2008). A mammalian homolog of Drosophila tumorous imaginal discs, Tid1, mediates agrin signaling at the neuromuscular junction. Neuron 60, 625-641.
115. Liu, Y., Padgett, D., Takahashi, M., Li, H., Sayeed, A., Teichert, R. W., Olivera, B. M., McArdle, J. J., Green, W. N. and Lin, W. (2008). Essential roles of the acetylcholine receptor gamma-subunit in neuromuscular synaptic patterning. Development 135, 1957-1967. (Pubitemid 351943360)
116. Liu, Y., Oppenheim, R. W., Sugiura, Y. and Lin, W. (2009). Abnormal development of the neuromuscular junction in Nedd4-deficient mice. Dev. Biol. 330, 153-166.
117. Lu, B. and Je, H. S. (2003). Neurotrophic regulation of the development and function of the neuromuscular synapses. J. Neurocytol. 32, 931-941. (Pubitemid 39011270)
118. Lu, Y., Tian, Q. B., Endo, S. and Suzuki, T. (2007a). A role for LRP4 in neuronal cell viability is related to apoE-binding. Brain Res. 1177, 19-28. (Pubitemid 47561888)
119. Lu, Z., Je, H. S., Young, P., Gross, J., Lu, B. and Feng, G. (2007b). Regulation of synaptic growth and maturation by a synapse-associated E3 ubiquitin ligase at the neuromuscular junction. J. Cell Biol. 177, 1077-1089. (Pubitemid 46955711)
120. Luo, S., Zhang, B., Dong, X. P., Tao, Y., Ting, A., Zhou, Z., Meixiong, J., Luo, J., Chiu, F. C., Xiong, W. C. et al. (2008). HSP90 beta regulates rapsyn turnover and subsequent AChR cluster formation and maintenance. Neuron 60, 97-110.
121. Luo, Z., Wang, Q., Zhou, J., Wang, J., Liu, M., He, X., Wynshaw-Boris, A., Xiong, W., Lu, B. and Mei, L. (2002). Regulation of AChR Clustering by Dishevelled Interacting with MuSK and PAK1. Neuron 35, 489-505. (Pubitemid 34879948)
122. Luo, Z., Wang, Q., Dobbins, G. C., Levy, S., Xiong, W. C. and Mei, L. (2003a). Signaling complexes for postsynaptic differentiation. J. Neurocytol. 32, 697-708.
123. Luo, Z. G., Je, H. S., Wang, Q., Yang, F., Dobbins, G. C., Yang, Z. H., Xiong, W. C., Lu, B. and Mei, L. (2003b). Implication of geranylgeranyltransferase I in synapse formation. Neuron 40, 703-717.
124. Macdonald, B. T., Semenov, M. V. and He, X. (2007). SnapShot: Wnt/beta-catenin signaling. Cell 131, 1204.
125. Marques, G., Bao, H., Haerry, T. E., Shimell, M. J., Duchek, P., Zhang, B. and O'Connor, M. B. (2002). The Drosophila BMP type II receptor Wishful Thinking regulates neuromuscular synapse morphology and function. Neuron 33, 529-543. (Pubitemid 34188430)
126. Marrus, S. B. and DiAntonio, A. (2004). Preferential localization of glutamate receptors opposite sites of high presynaptic release. Curr. Biol. 14, 924-931.
127. Mathew, D., Ataman, B., Chen, J., Zhang, Y., Cumberledge, S. and Budnik, V. (2005). Wingless signaling at synapses is through cleavage and nuclear import of receptor DFrizzled2. Science 310, 1344-1347. (Pubitemid 41698869)
128. McCabe, B. D., Marques, G., Haghighi, A. P., Fetter, R. D., Crotty, M. L., Haerry, T. E., Goodman, C. S. and O'Connor, M. B. (2003). The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction. Neuron 39, 241-254. (Pubitemid 36897547)
129. McCabe, B. D., Hom, S., Aberle, H., Fetter, R. D., Marques, G., Haerry, T. E., Wan, H., O'Connor, M. B., Goodman, C. S. and Haghighi, A. P. (2004). Highwire regulates presynaptic BMP signaling essential for synaptic growth. Neuron 41, 891-905. (Pubitemid 38429733)
130. McLennan, I. S. and Koishi, K. (2002). The transforming growth factor-betas: multifaceted regulators of the development and maintenance of skeletal muscles, motoneurons and Schwann cells. Int. J. Dev. Biol. 46, 559-567.
131. McMahan, U. J. (1990). The agrin hypothesis. Cold Spring Harb. Symp. Quant. Biol. 55, 407-418.
132. Megeath, L. J. and Fallon, J. R. (1998). Intracellular calcium regulates agrin-induced acetylcholine receptor clustering. J. Neurosci. 18, 672-678.
133. Menon, K. P., Andrews, S., Murthy, M., Gavis, E. R. and Zinn, K. (2009). The translational repressors Nanos and Pumilio have divergent effects on presynaptic terminal growth and postsynaptic glutamate receptor subunit composition. J. Neurosci. 29, 5558-5572.
134. Merlie, J. P. and Sanes, J. R. (1985). Concentration of acetylcholine receptor mRNA in synaptic regions of adult muscle fibres. Nature 317, 66-68.
135. Miech, C., Pauer, H. U., He, X. and Schwarz, T. L. (2008). Presynaptic local signaling by a canonical wingless pathway regulates development of the Drosophila neuromuscular junction. J. Neurosci. 28, 10875-10884.
136. Millard, T. H., Sharp, S. J. and Machesky, L. M. (2004). Signalling to actin assembly via the WASP (Wiskott-Aldrich syndrome protein)-family proteins and the Arp2/3 complex. Biochem. J. 380, 1-17.
137. Misgeld, T., Burgess, R. W., Lewis, R. M., Cunningham, J. M., Lichtman, J. W. and Sanes, J. R. (2002). Roles of neurotransmitter in synapse formation: development of neuromuscular junctions lacking choline acetyltransferase. Neuron 36, 635-648. (Pubitemid 35346757)
138. Mittaud, P., Marangi, P. A., Erb-Vogtli, S. and Fuhrer, C. (2001). Agrin-induced activation of acetylcholine receptor-bound Src family kinases requires Rapsyn and correlates with acetylcholine receptor clustering. J. Biol. Chem. 276, 14505-14513. (Pubitemid 37391845)
139. Mohamed, A. S., Rivas-Plata, K. A., Kraas, J. R., Saleh, S. M. and Swope, S. L. (2001). Src-class kinases act within the agrin/MuSK pathway to regulate acetylcholine receptor phosphorylation, cytoskeletal anchoring, and clustering. J. Neurosci. 21, 3806-3818.
140. Moransard, M., Borges, L. S., Willmann, R., Marangi, P. A., Brenner, H. R., Ferns, M. J. and Fuhrer, C. (2003). Agrin regulates rapsyn interaction with surface acetylcholine receptors, and this underlies cytoskeletal anchoring and clustering. J. Biol. Chem. 278, 7350-7359. (Pubitemid 36800738)
141. Morris, J. K., Lin, W., Hauser, C., Marchuk, Y., Getman, D. and Lee, K. F. (1999). Rescue of the cardiac defect in ErbB2 mutant mice reveals essential roles of ErbB2 in peripheral nervous system development. Neuron 23, 273-283. (Pubitemid 29315723)
142. Moseley, J. B., Bartolini, F., Okada, K., Wen, Y., Gundersen, G. G. and Goode, B. L. (2007). Regulated binding of adenomatous polyposis coli protein to actin. J. Biol. Chem. 282, 12661-12668. (Pubitemid 47100645)
143. Nguyen, Q. T., Parsadanian, A. S., Snider, W. D. and Lichtman, J. W. (1998). Hyperinnervation of neuromuscular junctions caused by GDNF overexpression in muscle. Science 279, 1725-1729.
144. Nishimune, H., Sanes, J. R. and Carlson, S. S. (2004). A synaptic laminin-calcium channel interaction organizes active zones in motor nerve terminals. Nature 432, 580-587. (Pubitemid 39626258)
145. Nishimune, H., Valdez, G., Jarad, G., Moulson, C. L., Muller, U., Miner, J. H. and Sanes, J. R. (2008). Laminins promote postsynaptic maturation by an autocrine mechanism at the neuromuscular junction. J. Cell Biol. 182, 1201-1215.
146. Nizhynska, V., Neumueller, R. and Herbst, R. (2007). Phosphoinositide 3-kinase acts through RAC and Cdc42 during agrin-induced acetylcholine receptor clustering. Dev. Neurobiol. 67, 1047-1058. (Pubitemid 47343748)
147. Noakes, P. G., Gautam, M., Mudd, J., Sanes, J. R. and Merlie, J. P. (1995). Aberrant differentiation of neuromuscular junctions in mice lacking slaminin/laminin beta 2. Nature 374, 258-262.
148. Okada, K., Inoue, A., Okada, M., Murata, Y., Kakuta, S., Jigami, T., Kubo, S., Shiraishi, H., Eguchi, K., Motomura, M. et al. (2006). The muscle protein Dok-7 is essential for neuromuscular synaptogenesis. Science 312, 1802-1805. (Pubitemid 43962899)
149. Oppenheim, R. W., Houenou, L. J., Johnson, J. E., Lin, L. F., Li, L., Lo, A. C., Newsome, A. L., Prevette, D. M. and Wang, S. (1995). Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. Nature 373, 344-346.
150. Packard, M., Koo, E. S., Gorczyca, M., Sharpe, J., Cumberledge, S. and Budnik, V. (2002). The Drosophila Wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation. Cell 111, 319-330. (Pubitemid 35341387)
151. Panzer, J. A., Gibbs, S. M., Dosch, R., Wagner, D., Mullins, M. C., Granato, M. and Balice-Gordon, R. J. (2005). Neuromuscular synaptogenesis in wild-type and mutant zebrafish. Dev. Biol. 285, 340-357. (Pubitemid 41394024)
152. Park, S. J., Suetsugu, S., Sagara, H. and Takenawa, T. (2007). HSP90 cross-links branched actin filaments induced by N-WASP and the Arp2/3 complex. Genes Cells 12, 611-622. (Pubitemid 46824959)
153. Paterson, I. C., Matthews, J. B., Huntley, S., Robinson, C. M., Fahey, M., Parkinson, E. K. and Prime, S. S. (2001). Decreased expression of TGF-beta cell surface receptors during progression of human oral squamous cell carcinoma. J. Pathol. 193, 458-467. (Pubitemid 32266814)
154. Peng, H. B., Xie, H. and Dai, Z. (1997). Association of cortactin with developing neuromuscular specializations. J. Neurocytol. 26, 637-650. (Pubitemid 27449001)
155. Peng, H. B., Xie, H., Rossi, S. G. and Rotundo, R. L. (1999). Acetylcholinesterase clustering at the neuromuscular junction involves perlecan and dystroglycan. J. Cell Biol. 145, 911-921. (Pubitemid 29240865)
156. Polo-Parada, L., Bose, C. M., Plattner, F. and Landmesser, L. T. (2004). Distinct roles of different neural cell adhesion molecule (NCAM) isoforms in synaptic maturation revealed by analysis of NCAM 180 kDa isoform-deficient mice. J. Neurosci. 24, 1852-1864. (Pubitemid 38292796)
157. Rawson, J. M., Lee, M., Kennedy, E. L. and Selleck, S. B. (2003). Drosophila neuromuscular synapse assembly and function require the TGF-beta type I receptor saxophone and the transcription factor Mad. J. Neurobiol. 55, 134-150. (Pubitemid 36423155)
158. Reddy, L. V., Koirala, S., Sugiura, Y., Herrera, A. A. and Ko, C. P. (2003). Glial cells maintain synaptic structure and function and promote development of the neuromuscular junction in vivo. Neuron 40, 563-580. (Pubitemid 37494705)
159. Reist, N. E., Werle, M. J. and McMahan, U. J. (1992). Agrin released by motor neurons induces the aggregation of acetylcholine receptors at neuromuscular junctions. Neuron 8, 865-868.
160. Reynolds, M. L. and Woolf, C. J. (1992). Terminal Schwann cells elaborate extensive processes following denervation of the motor endplate. J. Neurocytol. 21, 50-66.
161. Riethmacher, D., Sonnenberg-Riethmacher, E., Brinkmann, V., Yamaai, T., Lewin, G. R. and Birchmeier, C. (1997). Severe neuropathies in mice with targeted mutations in the ErbB3 receptor. Nature 389, 725-730. (Pubitemid 27458958)
162. Rival, T., Soustelle, L., Cattaert, D., Strambi, C., Iche, M. and Birman, S. (2006). Physiological requirement for the glutamate transporter dEAAT1 at the adult Drosophila neuromuscular junction. J. Neurobiol. 66, 1061-1074. (Pubitemid 44264931)
163. Roos, J., Hummel, T., Ng, N., Klambt, C. and Davis, G. W. (2000). Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron 26, 371-382.
164. Ruegg, M. A. and Bixby, J. L. (1998). Agrin orchestrates synaptic differentiation at the vertebrate neuromuscular junction. Trends Neurosci. 21, 22-27.
165. Ruegg, M. A., Tsim, K. W., Horton, S. E., Kroger, S., Escher, G., Gensch, E. M. and McMahan, U. J. (1992). The agrin gene codes for a family of basal lamina proteins that differ in function and distribution. Neuron 8, 691-699.
166. Ruggiu, M., Herbst, R., Kim, N., Jevsek, M., Fak, J. J., Mann, M. A., Fischbach, G., Burden, S. J. and Darnell, R. B. (2009). Rescuing Z+ agrin splicing in Nova null mice restores synapse formation and unmasks a physiologic defect in motor neuron firing. Proc. Natl. Acad. Sci. USA 106, 3513-3518.
167. Rushton, E., Rohrbough, J. and Broadie, K. (2009). Presynaptic secretion of mind-the-gap organizes the synaptic extracellular matrix-integrin interface and postsynaptic environments. Dev. Dyn. 238, 554-571.
168. Saiga, T., Fukuda, T., Matsumoto, M., Tada, H., Okano, H. J., Okano, H. and Nakayama, K. I. (2009). Fbxo45 forms a novel ubiquitin ligase complex and is required for neuronal development. Mol. Cell. Biol. 29, 3529-3543.
169. Salpeter, M. M. and Loring, R. H. (1985). Nicotinic acetylcholine receptors in vertebrate muscle: properties, distribution and neural control. Prog. Neurobiol. 25, 297-325.
170. Salpeter, M. M., Cooper, D. L. and Levitt-Gilmour, T. (1986). Degradation rates of acetylcholine receptors can be modified in the postjunctional plasma membrane of the vertebrate neuromuscular junction. J. Cell Biol. 103, 1399-1403.
171. Sanes, J. R. and Lichtman, J. W. (2001). Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat. Rev. Neurosci. 2, 791-805.
172. Schaeffer, L., de Kerchove d'Exaerde, A. and Changeux, J. P. (2001). Targeting transcription to the neuromuscular synapse. Neuron 31, 15-22.
173. Schwander, M., Shirasaki, R., Pfaff, S. L. and Muller, U. (2004). Beta1 integrins in muscle, but not in motor neurons, are required for skeletal muscle innervation. J. Neurosci. 24, 8181-8191. (Pubitemid 39280838)
174. Sealock, R., Wray, B. E. and Froehner, S. C. (1984). Ultrastructural localization of the Mr 43,000 protein and the acetylcholine receptor in Torpedo postsynaptic membranes using monoclonal antibodies. J. Cell Biol. 98, 2239-2244. (Pubitemid 14121855)
175. Shen, K. and Bargmann, C. I. (2003). The immunoglobulin superfamily protein SYG-1 determines the location of specific synapses in C. elegans. Cell 112, 619-630. (Pubitemid 36331775)
176. Shen, K., Fetter, R. D. and Bargmann, C. I. (2004). Synaptic specificity is generated by the synaptic guidepost protein SYG-2 and its receptor, SYG-1. Cell 116, 869-881. (Pubitemid 38410731)
177. Shi, L., Butt, B., Ip, F. C. F., Dai, Y., Jiang, L., Yung, W. H., Greenberg, M. E., Fu, A. K. Y. and Ip, N. Y. (2010). Ephexin1 is required for structural maturation and neurotransmission at the neuromuscular junction. Neuron 65, 204-216.
178. Shull, M. M., Ormsby, I., Kier, A. B., Pawlowski, S., Diebold, R. J., Yin, M., Allen, R., Sidman, C., Proetzel, G., Calvin, D. et al. (1992). Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 359, 693-699.
179. Simon-Chazottes, D., Tutois, S., Kuehn, M., Evans, M., Bourgade, F., Cook, S., Davisson, M. T. and Guenet, J. L. (2006). Mutations in the gene encoding the low-density lipoprotein receptor LRP4 cause abnormal limb development in the mouse. Genomics 87, 673-677.
180. Smith, C. L., Mittaud, P., Prescott, E. D., Fuhrer, C. and Burden, S. J. (2001). Src, Fyn, and Yes are not required for neuromuscular synapse formation but are necessary for stabilization of agrin-induced clusters of acetylcholine receptors. J. Neurosci. 21, 3151-3160. (Pubitemid 32323497)
181. Son, Y. J. and Thompson, W. J. (1995a). Nerve sprouting in muscle is induced and guided by processes extended by Schwann cells. Neuron 14, 133-141.
182. Son, Y. J. and Thompson, W. J. (1995b). Schwann cell processes guide regeneration of peripheral axons. Neuron 14, 125-132.
183. Soosairajah, J., Maiti, S., Wiggan, O., Sarmiere, P., Moussi, N., Sarcevic, B., Sampath, R., Bamburg, J. R. and Bernard, O. (2005). Interplay between components of a novel LIM kinase-slingshot phosphatase complex regulates cofilin. EMBO J. 24, 473-486. (Pubitemid 40343250)
184. Stetzkowski-Marden, F., Gaus, K., Recouvreur, M., Cartaud, A. and Cartaud, J. (2006). Agrin elicits membrane lipid condensation at sites of acetylcholine receptor clusters in C2C12 myotubes. J. Lipid Res. 47, 2121-2133. (Pubitemid 44936123)
185. Strochlic, L., Cartaud, A., Labas, V., Hoch, W., Rossier, J. and Cartaud, J. (2001). MAGI-1c: a synaptic MAGUK interacting with muSK at the vertebrate neuromuscular junction. J. Cell Biol. 153, 1127-1132. (Pubitemid 34289250)
186. Strochlic, L., Cartaud, A., Mejat, A., Grailhe, R., Schaeffer, L., Changeux, J. P. and Cartaud, J. (2004). 14-3-3 gamma associates with muscle specific kinase and regulates synaptic gene transcription at vertebrate neuromuscular synapse. Proc. Natl. Acad. Sci. USA 101, 18189-18194. (Pubitemid 40054095)
187. Tang, H., Sun, Z. and Goldman, D. (2001). CaM kinase II-dependent suppression of nicotinic acetylcholine receptor delta-subunit promoter activity. J. Biol. Chem. 276, 26057-26065. (Pubitemid 37412815)
188. Ten Dijke, P., Miyazono, K. and Heldin, C. H. (2000). Signaling inputs converge on nuclear effectors in TGF-beta signaling. Trends Biochem. Sci. 25, 64-70. (Pubitemid 30100368)
189. Tian, Q. B., Suzuki, T., Yamauchi, T., Sakagami, H., Yoshimura, Y., Miyazawa, S., Nakayama, K., Saitoh, F., Zhang, J. P., Lu, Y. et al. (2006). Interaction of LDL receptor-related protein 4 (LRP4) with postsynaptic scaffold proteins via its C-terminal PDZ domain-binding motif, and its regulation by Ca/calmodulin-dependent protein kinase II. Eur. J. Neurosci. 23, 2864-2876. (Pubitemid 43882865)
190. Trachtenberg, J. T. and Thompson, W. J. (1996). Schwann cell apoptosis at developing neuromuscular junctions is regulated by glial growth factor. Nature 379, 174-177.
191. Umemori, H. and Sanes, J. R. (2008). Signal regulatory proteins (SIRPS) are secreted presynaptic organizing molecules. J. Biol. Chem. 283, 34053-34061.
192. Umemori, H., Linhoff, M. W., Ornitz, D. M. and Sanes, J. R. (2004). FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain. Cell 118, 257-270. (Pubitemid 38962580)
193. Valenzuela, D. M., Stitt, T. N., DiStefano, P. S., Rojas, E., Mattsson, K., Compton, D. L., Nunez, L., Park, J. S., Stark, J. L., Gies, D. R. 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, 573-584.
194. Vock, V. M., Ponomareva, O. N. and Rimer, M. (2008). Evidence for muscle-dependent neuromuscular synaptic site determination in mammals. J. Neurosci. 28, 3123-3130.
195. Wang, C. Y., Yang, F., He, X. P., Je, H. S., Zhou, J. Z., Eckermann, K., Kawamura, D., Feng, L., Shen, L. and Lu, B. (2002). Regulation of neuromuscular synapse development by glial cell line-derived neurotrophic factor and neurturin. J. Biol. Chem. 277, 10614-10625. (Pubitemid 34968186)
196. Wang, J., Jing, Z., Zhang, L., Zhou, G., Braun, J., Yao, Y. and Wang, Z. Z. (2003). Regulation of acetylcholine receptor clustering by the tumor suppressor APC. Nat. Neurosci. 6, 1017-1018. (Pubitemid 37186190)
197. Wang, J., Ruan, N. J., Qian, L., Lei, W. L., Chen, F. and Luo, Z. G. (2008). Wnt/beta-catenin signaling suppresses Rapsyn expression and inhibits acetylcholine receptor clustering at the neuromuscular junction. J. Biol. Chem. 283, 21668-21675.
198. Wang, P., Yang, G., Mosier, D. R., Chang, P., Zaidi, T., Gong, Y. D., Zhao, N. M., Dominguez, B., Lee, K. F., Gan, W. B. et al. (2005). Defective neuromuscular synapses in mice lacking amyloid precursor protein (APP) and APP-Like protein 2. J. Neurosci. 25, 1219-1225. (Pubitemid 40268964)
199. Wang, Q., Zhang, B., Wang, Y. E., Xiong, W. C. and Mei, L. (2008). The Ig1/2 domain of MuSK binds to muscle surface and is involved in acetylcholine receptor clustering. Neurosignals 16, 246-253. (Pubitemid 351263229)
200. Watanabe, T., Wang, S., Noritake, J., Sato, K., Fukata, M., Takefuji, M., Nakagawa, M., Izumi, N., Akiyama, T. and Kaibuchi, K. (2004). Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev. Cell 7, 871-883. (Pubitemid 39654731)
201. Weatherbee, S. D., Anderson, K. V. and Niswander, L. A. (2006). LDL-receptor-related protein 4 is crucial for formation of the neuromuscular junction. Development 133, 4993-5000. (Pubitemid 46085064)
202. Webb, B. A., Zhou, S., Eves, R., Shen, L., Jia, L. and Mak, A. S. (2006). Phosphorylation of cortactin by p21-activated kinase. Arch. Biochem. Biophys. 456, 183-193.
203. Weston, C., Yee, B., Hod, E. and Prives, J. (2000). Agrin-induced Acetylcholine Receptor Clustering Is Mediated by the Small Guanosine Triphosphatases Rac and Cdc42. J. Cell Biol. 150, 205-212. (Pubitemid 30480238)
204. Weston, C., Gordon, C., Teressa, G., Hod, E., Ren, X. D. and Prives, J. (2003). Cooperative regulation by Rac and Rho of agrin-induced acetylcholine receptor clustering in muscle cells. J. Biol. Chem. 278, 6450-6455. (Pubitemid 36800904)
205. Willmann, R., Pun, S., Stallmach, L., Sadasivam, G., Santos, A. F., Caroni, P. and Fuhrer, C. (2006). Cholesterol and lipid microdomains stabilize the postsynapse at the neuromuscular junction. EMBO J. 25, 4050-4060. (Pubitemid 44338746)
206. Woldeyesus, M. T., Britsch, S., Riethmacher, D., Xu, L., Sonnenberg-Riethmacher, E., Abou-Rebyeh, F., Harvey, R., Caroni, P. and Birchmeier, C. (1999). Peripheral nervous system defects in erbB2 mutants following genetic rescue of heart development. Genes Dev. 13, 2538-2548. (Pubitemid 29489645)
207. Wolpowitz, D., Mason, T. B., Dietrich, P., Mendelsohn, M., Talmage, D. A. and Role, L. W. (2000). Cysteine-rich domain isoforms of the neuregulin-1 gene are required for maintenance of peripheral synapses. Neuron 25, 79-91. (Pubitemid 30316512)
208. Yamaguchi, Y. L., Tanaka, S. S., Kasa, M., Yasuda, K., Tam, P. P. and Matsui, Y. (2006). Expression of low density lipoprotein receptor-related protein 4 (Lrp4) gene in the mouse germ cells. Gene Expr. Patterns 6, 607-612. (Pubitemid 43758643)
209. Yang, X., Li, W., Prescott, E. D., Burden, S. J. and Wang, J. C. (2000). DNA topoisomerase IIbeta and neural development. Science 287, 131-134. (Pubitemid 30033236)
210. Yang, X., Arber, S., William, C., Li, L., Tanabe, Y., Jessell, T. M., Birchmeier, C. and Burden, S. J. (2001). Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 30, 399-410. (Pubitemid 32530584)
211. Yuan, L. L. and Ganetzky, B. (1999). A glial-neuronal signaling pathway revealed by mutations in a neurexin-related protein. Science 283, 1343-1345. (Pubitemid 129507223)
212. Yumoto, N., Wakatsuki, S., Kurisaki, T., Hara, Y., Osumi, N., Frisen, J. and Sehara-Fujisawa, A. (2008). Meltrin beta/ADAM19 interacting with EphA4 in developing neural cells participates in formation of the neuromuscular junction. PLoS ONE 3, e3322.
213. Zhang, B., Luo, S., Dong, X. P., Zhang, X., Liu, C., Luo, Z., Xiong, W. C. and Mei, L. (2007). Beta-catenin regulates acetylcholine receptor clustering in muscle cells through interaction with rapsyn. J. Neurosci. 27, 3968-3973. (Pubitemid 46597140)
214. Zhang, B., Luo, S., Wang, Q., Suzuki, T., Xiong, W. C. and Mei, L. (2008). LRP4 serves as a coreceptor of agrin. Neuron 60, 285-297.
215. Zhang, J., Lefebvre, J. L., Zhao, S. and Granato, M. (2004). Zebrafish unplugged reveals a role for muscle-specific kinase homologs in axonal pathway choice. Nat. Neurosci. 7, 1303-1309. (Pubitemid 41057752)
216. Zhang, X., Xu, R., Zhu, B., Yang, X., Ding, X., Duan, S., Xu, T., Zhuang, Y. and Han, M. (2007). Syne-1 and Syne-2 play crucial roles in myonuclear anchorage and motor neuron innervation. Development 134, 901-908. (Pubitemid 46795681)
217. Zhou, H., Glass, D. J., Yancopoulos, G. D. and Sanes, J. R. (1999). Distinct domains of MuSK mediate its abilities to induce and to associate with postsynaptic specializations. J. Cell Biol. 146, 1133-1146. (Pubitemid 29430453)
218. Zhu, D., Xiong, W. C. and Mei, L. (2006). Lipid rafts serve as a signaling platform for nicotinic acetylcholine receptor clustering. J. Neurosci. 26, 4841-4851. (Pubitemid 44315325)
219. Zhu, D., Yang, Z., Luo, Z., Luo, S., Xiong, W. C. and Mei, L. (2008). Muscle-specific receptor tyrosine kinase endocytosis in acetylcholine receptor clustering in response to agrin. J. Neurosci. 28, 1688-1696. (Pubitemid 351287032)
220. Ziskind-Conhaim, L. and Bennett, J. I. (1982). The effects of electrical inactivity and denervation on the distribution of acetylcholine receptors in developing rat muscle. Dev. Biol. 90, 185-197. (Pubitemid 12104835)