A synaptic balancing act: Local and global signaling in the clustering of ACh receptors at vertebrate neuromuscular junctions

Journal of Neurocytology

Volumn 32, Issue 5-8, 2003, Pages 685-696

  Madhavan, Raghavan ^a   Peng, H Benjamin ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; AGRIN; CHOLINERGIC RECEPTOR; F ACTIN; MUSK; PROTEIN TYROSINE KINASE; RAPSYN;

CYTOSKELETON; ENZYME ACTIVATION; MOLECULAR MECHANICS; MUSCLE INNERVATION; NERVE ENDING; NEUROMUSCULAR SYNAPSE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CHEMISTRY; HUMAN; METABOLISM; PHYSIOLOGY; SYNAPSE;

VERTEBRATA;

ACTINS; ANIMALS; HUMANS; NEUROMUSCULAR JUNCTION; RECEPTORS, CHOLINERGIC; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 3042524749     PISSN: 03004864     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:NEUR.0000020617.05656.68     Document Type: Review

References (102)

1. ALI, D. W. & SALTER, M. W. (2001) NMDA receptor regulation by Src kinase signalling in excitatory synaptic transmission and plasticity. Current Opinion in Neurobiology 11, 336-342.
2. APEL, E. D., GLASS, D. J., MOSCOSO, L. M., YANCOPOULOS, G. D. & SANES, J. R. (1997) Rapsyn is required for MuSK signaling and recruits synaptic components to a MuSK-containing scaffold. Neuron 18, 623-635.
3. APEL, E. D., ROBERDS, S. L., CAMPBELL, K. P. & 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.
4. BAKER, L. P., DAGGETT, D. F. & PENG, H. B. (1994) Concentration of pp125 focal adhesion kinase (FAK) at the myotendinous junction. Journal of Cell Science 107, 1485-1497.
5. BAKER, L. P. & PENG, H. B. (1993) Tyrosine phosphorylation and acetylcholine receptor cluster formation in cultured Xenopus muscle cells. Journal of Cell Biology 120, 185-195.
6. BALASUBRAMANIAN, S., FUNG, E. T. & HUGANIR, R. L. (1998) Characterization of the tyrosine phosphorylation and distribution of dystrobrevin isoforms. FEBS Letters 432, 133-140.
7. BARTOLI, M., RAMARAO, M. K. & COHEN, J. B. (2001) Interactions of the rapsyn RING-H2 domain with dystroglycan. Journal of Biological Chemistry 276, 24911-24917.
8. BLOCH, R. J. (1986) Actin at receptor-rich domains of isolated acetylcholine receptor clusters. Journal of Cell Biology 102, 1447-1458.
9. BLOCH, R. J. & HALL, Z. W. (1983) Cytoskeletal components of the vertebrate neuromuscular junction: Vinculin, a-actinin, and filamin. Journal of Cell Biology 97, 217-223.
10. BORGES, L. S., LEE, Y. & FERNS, M. (2002) Dual role for calcium in agrin signaling and acetylcholine receptor clustering. Journal of Neurobiology 50, 69-79.
11. CARTAUD, A., COUTANT, S., PETRUCCI, T. C. & CARTAUD, J. (1998) Evidence for in situ and in vitro association between β-dystroglycan and the subsynaptic 43K rapsyn protein - Consequence for acetylcholine receptor clustering at the synapse. Journal of Biological Chemistry 273, 11321-11326.
12. CHETKOVICH, D. M., CHEN, L., STOCKER, T. J., NICOLL, R. A. & BREDT, D. S. (2002) Phosphorylation of the postsynaptic density-95 (PSD-95)/discs large/zona occludens-1 binding site of stargazin regulates binding to PSD-95 and synaptic targeting of AMPA receptors. Journal of Neuroscience 22, 5791-5796.
13. CHOI, J., KO, J., PARK, E., LEE, J. R., YOON, J., LIM, S. & KIM, E. (2002) Phosphorylation of stargazin by protein kinase A regulates its interaction with PSD-95. Journal of Biological Chemistry 277, 12359-12363.
14. CHUNG, H. J., XIA, J., SCANNEVIN, R. H., ZHANG, X. & HUGANIR, R. L. (2000) Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins. Journal of Neuroscience 20, 7258-7267.
15. COHEN, N. A., BRENMAN, J. E., SNYDER, S. H. & BREDT, D. S. (1996) Binding of the inward rectifier K+ channel Kir 2.3 to PSD-95 is regulated by protein kinase A phosphorylation. Neuron 17, 759-767.
16. CONNOLLY, J. A. (1984) Role of the cytoskeleton in the formation, stabilization and removal of acetylcholine receptor clusters in cultured muscle cells. Journal of Cell Biology 99, 148-154.
17. CORY, G. O., GARG, R., CRAMER, R. & RIDLEY, A. J. (2002) Phosphorylation of tyrosine 291 enhances the ability of WASp to stimulate actin polymerization and filopodium formation. Wiskott-Aldrich Syndrome protein. Journal of Biological Chemistry 277, 45115-45121.
18. DAI, Z., LUO, X., XIE, H. & PENG, H. B. (2000) The actin-driven movement and formation of acetylcholine receptor clusters. Journal of Cell Biology 150, 1321-1334.
19. DAI, Z. & PENG, H. B. (1998) A role of tyrosine phosphatase in acetylcholine receptor cluster dispersal and formation. Journal of Cell Biology 141, 1613-1624.
20. DAI, Z. & PENG, H. B. (2001) Fluorescent imaging of nicotinic receptors during neuromuscular junction development. In Ion Channel Localization Methods and Protocols (edited by LOPATIN, A. & NICHOLS, C. G.) pp. 119-143. Totowa, NJ: Humana Press.
21. 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., SMITH, C., DISTEFANO, P. S., GLASS, D. J., BURDEN, S. J. & YANCOPOULOS, G. D. (1996) The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo Cell 85, 501-512.
22. EDWARDS, C. & FRISCH, H. L. (1976) A model for the localization of acetylcholine receptors at the muscle endplate. Journal of Neurobiology 7, 377-381.
23. ETIENNE-MANNEVILLE, S. & HALL, A. (2002) Rho GT-Pases in cell biology. Nature 420, 629-635.
24. FERNS, M. & CARBONETTO, S. (2001) Challenging the neurocentric view of neuromuscular synapse formation. Neuron 30, 311-314.
25. FERTUCK, H. C. & SALPETER, M. M. (1976) Quantitation of junctional and extrajunctional acetylcholine receptors by electron microscope autoradiography after 125I-alpha-bungarotoxin binding at mouse neuromuscular junctions. Journal of Cell Biology 69, 144-158.
26. FROEHNER, S. C., LUETJE, C. W., SCOTLAND, P. B. & PATRICK, J. (1990) The postsynaptic 43K protein clusters muscle nicotinic acetylcholine receptors in Xenopus oocytes. Neuron 5, 403-410.
27. FUHRER, C. & HALL, Z. W. (1996) Functional interaction of Src family kinases with the acetylcholine receptor in C2 myotubes. Journal of Biological Chemistry 271, 32474-32481.
28. FUHRER, C., SUGIYAMA, J. E., TAYLOR, R. G. & HALL, Z. W. (1997) Association of muscle-specific kinase MuSK with the acetylcholine receptor in mammalian muscle. EMBO Journal 16, 4951-4960.
29. FUKAZAWA, Y., SAITOH, Y., OZAWA, F., OHTA, Y., MIZUNO, K. & INOKUCHI, K. (2003) Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 38, 447-460.
30. GALKIN, V. E., ORLOVA, A., VANLOOCK, M. S., RYBAKOVA, I. N., ERVASTI, J. M. & EGELMAN, E. H. (2002) The utrophin actin-binding domain binds F-actin in two different modes: Implications for the spectrin superfamily of proteins. Journal of Cell Biology 157, 243-251.
31. GANJU, P., WALLS, E., BRENNAN, J. & REITH, A. D. (1995) Cloning and developmental expression of Nsk2, a novel receptor tyrosine kinase implicated in skeletal myogenesis. Oncogene 11, 281-290.
32. GAUTAM, M., NOAKES, P. G., MOSCOSO, L., RUPP, F., SCHELLER, R. H., MERLIE, J. P. & SANES, J. R. (1996) Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85, 525-535.
33. GAUTAM, M., NOAKES, P. G., MUDD, J., NICHOL, M., CHU, G. C., SANES, J. R. & MERLIE, J. P. (1995) Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377, 232-236.
34. 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., DISTEFANO, P. S., VALENZUELA, D. M., DECHIARA, T. M. & YANCOPOULOS, G. D. (1996) Agrin acts via a MuSK receptor complex. Cell 85, 513-523.
35. GLASS, D. J. & YANCOPOULOS, G. D. (1997) Sequential roles of agrin, MuSK and rapsyn during neuromuscular junction formation. Current Opinion in Neurobiology 7, 379-384.
36. GRADY, R. M., ZHOU, H., CUNNINGHAM, J. M., HENRY, M. D., CAMPBELL, K. P. & SANES, J. R. (2000) Maturation and maintenance of the neuromuscular synapse: Genetic evidence for roles of the dystrophin - glycoprotein complex. Neuron 25, 279-293.
37. HALL, Z. W. & SANES, J. R. (1993) Synaptic structure and development: The neuromuscular junction. Neuron 10(Suppl.), 99-121.
38. HALPAIN, S., HIPOLITO, A. & SAFFER, L. (1998) Regulation of F-actin stability in dendritic spines by glutamate receptors and calcineurin. Journal of Neuroscience 18, 9835-9844.
39. HARRIS, K. M. (1999) Structure, development, and plasticity of dendritic spines. Current Opinion in Neurobiology 9, 343-348.
40. HERBST, R. & BURDEN, S. J. (2000) The juxtamembrane region of MuSK has a critical role in agrin-mediated signaling. EMBO Journal 19, 67-77.
41. HIGGS, H. N. & POLLARD, T. D. (2001) Regulation of actin filament network formation through ARP2/3 complex: Activation by a diverse array of proteins. Annual Review of Biochemistry 70, 649-676.
42. HOPF, C. & HOCH, W. (1998) Dimerization of the muscle-specific kinase induces tyrosine phosphorylation of acetylcholine receptors and their aggregation on the surface of myotubes. Journal of Biological Chemistry 273, 6467-6473.
43. JONES, M. A. & WERLE, M. J. (2000) Nitric oxide is a down-stream mediator of agrin-induced acetylcholine receptor aggregation. Mol. Cell Neurosci. 16, 649-660.
44. KAKSONEN, M., PENG, H. B. & RAUVALA, H. (2000) Association of cortactin with dynamic actin in lamellipodia and on endosomal vesicles. Journal of Cell Science 113, 4421-4426.
45. KENNEDY, M. B. (2000) Signal-processing machines at the postsynaptic density. Science 290, 750-754.
46. KIDOKORO, Y. & BRASS, B. (1985) Redistribution of acetylcholine receptors during neuromuscular junction formation in Xenopus cultures. Journal of Physiology Paris 80, 212-220.
47. LEI, G., XUE, S., CHERY, N., LIU, Q., XU, J., KWAN, C. L., FU, Y. P., LU, Y. M., LIU, M., HARDER, K. W. & YU, X. M. (2002) Gain control of N-methyl-D-aspartate receptor activity by receptor-like protein tyrosine phosphatase alpha. EMBO Journal 21, 2977-2989.
48. LIN, W., BURGESS, R. W., DOMINGUEZ, B., PFAFF, S. L., SANES, J. R. & LEE, K. F. (2001) Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature 410, 1057-1064.
49. LISMAN, J. E. & ZHABOTINSKY, A. M. (2001) A model of synaptic memory: A CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly. Neuron 31, 191-201.
50. LUO, G., ZHANG, J. Q., NGUYEN, T. P., HERRERA, A. H., PATERSON, B. & HOROWITS, R. (1997) Complete cDNA sequence and tissue localization of N-RAP, a novel nebulin-related protein of striated muscle. Cell Motility and the Cytoskeleton 38, 75-90.
51. LUO, Z. G., WANG, Q., ZHOU, J. Z., WANG, J., LUO, Z., LIU, M., HE, X., WYNSHAW-BORIS, A., XIONG, W. C., LU, B. & MEI, L. (2002) Regulation of AChR clustering by Dishevelled interacting with MuSK and PAK1. Neuron 35, 489-505.
52. MADHAVAN, R., CHAN, F., ZHAO, X. T., WU, Z. & PENG, H. B. (2003) The involvement of calcineurin in acetylcholine receptor dispersal and clustering. Mol. Cell Neurosci. 23, 8587-8599.
53. MCMAHAN, U. J. (1990) The agrin hypothesis. Cold Spring Harbor Symp. 50, 407-418.
54. MEGEATH, L. J. & FALLON, J. R. (1998) Intracellular calcium regulates agrin-induced acetylcholine receptor aggregation. Journal of Neuroscience 18, 672-678.
55. MEIER, T., PEREZ, G. M. & WALLACE, B. G. (1995) Immobilization of nicotinic acetylcholine receptors in mouse C2 myotubes by agrin-induced protein tyrosine phosphorylation. Journal of Cell Biology 131, 441-451.
56. MENG, Y., ZHANG, Y., TREGOUBOV, V., JANUS, C., CRUZ, L., JACKSON, M., LU, W. Y., MACDONALD, J. F., WANG, J. Y., FALLS, D. L. & JIA, Z. (2002) Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron 35, 121-133.
57. MITTAUD, P., MARANGI, P. A., ERB-VOGTLI, S. & FUHRER, C. (2001) Agrin-induced activation of acetylcholine receptor-bound Src family kinases requires rapsyn and correlates with acetylcholine receptor clustering. Journal of Biological Chemistry 276, 14505-14513.
58. MOHAMED, A. S., RIVAS-PLATA, K. A., KRAAS, J. R., SALEH, S. M. & SWOPE, S. L. (2001) Src-class kinases act within the agrin/MuSK pathway to regulate acetylcholine receptor phosphorylation, cytoskeletal anchoring, and clustering. Journal of Neuroscience 21, 3806-3818.
59. MOHAMED, A. S. & SWOPE, S. L. (1999) Phosphorylation and cytoskeletal anchoring of the acetylcholine receptor by src class protein-tyrosine kinases. Activation by rapsyn. Journal of Biological Chemistry 274, 20529-20539.
60. MOODY-CORBETT, F. & COHEN, M. W. (1982) Influence of nerve on the formation and survival of acetylcholine receptor and cholinesterase patches on embryonic Xenopus muscle cells in culture. Journal of Neuroscience 2, 633-646.
61. MURASE, S., MOSSER, E. & SCHUMAN, E. M. (2002) Depolarization drives beta-Catenin into neuronal spines promoting changes in synaptic structure and function. Neuron 35, 91-105.
62. NAWROTZKI, R., LOH, N. Y., RUEGG, M. A., DAVIES, K. E. & BLAKE, D. J. (1998) Characterisation of alpha-dystrobrevin in muscle. Journal of Cell Science 111, 2595-2605.
63. NIMCHINSKY, E. A., SABATINI, B. L. & SVOBODA, K. (2002) Structure and function of dendritic spines. Ann. Rev. Physiol. 64, 313-353.
64. OLAZABAL, I. M. & MACHESKY, L. M. (2001) Abp1p and cortactin, new "hand-holds" for actin. Journal of Cell Biology 154, 679-682.
65. PAK, D. T., YANG, S., RUDOLPH-CORREIA, S., KIM, E. & SHENG, M. (2001) Regulation of dendritic spine morphology by SPAR, a PSD-95-associated RapGAP. Neuron 31, 289-303.
66. PANTALONI, D., LE CLAINCHE, C. & CARLIER, M. F. (2001) Mechanism of actin-based motility. Science 292, 1502-1506.
67. PENG, H. B. (1986) Elimination of preexistent acetylcholine receptor clusters induced by the formation of new clusters in the absence of nerve. Journal of Neuroscience 6, 581-589.
68. PENG, H. B., ALI, A. A., DAI, Z., DAGGETT, D. F., RAULO, E. & RAUVALA, H. (1995) The role of heparin-binding growth-associated molecule (HB-GAM) in the postsynaptic induction in cultured muscle cells. Journal of Neuroscience 15, 3027-3038.
69. PENG, H. B. & PHELAN, K. A. (1984) Early cytoplasmic specialization at the presumptive acetylcholine receptor cluster: A meshwork of thin filaments. Journal of Cell Biology 99, 344-349.
70. PENG, H. B., XIE, H. & DAI, Z. (1997) The association of cortactin with developing neuromuscular specializations. Journal of Neurocytology 26, 637-650.
71. PERKINS, G. A., WANG, L., HUANG, L. J., HUMPHRIES, K., YAO, V. J., MARTONE, M., DEERINCK, T. J., BARRACLOUGH, D. M., VIOLIN, J. D., SMITH, D., NEWTON, A., SCOTT, J. D., TAYLOR, S. S. & ELLISMAN, M. H. (2001) PKA, PKC, and AKAP localization in and around the neuromuscular junction. BMC Neuroscience 2, 17.
72. PETERS, M. F., SADOULET-PUCCIO, H. M., GRADY, M. R., KRAMARCY, N. R., KUNKEL, L. M., SANES, J. R., SEALOCK, R. & FROEHNER, S. C. (1998) Differential membrane localization and intermolecular associations of alpha-dystrobrevin isoforms in skeletal muscle. Journal of Cell Biology 142, 1269-1278.
73. PHILLIPS, W. D., KOPTA, C., BLOUNT, P., GARDNER, P. D., STEINBACH, J. H. & MERLIE, J. P. (1991) ACh receptor-rich membrane domains organized in fibroblasts by recombinant 43-kilodalton protein. Science 251, 568-570.
74. POLLARD, T. D. & BELTZNER, C. C. (2002) Structure and function of the Arp2/3 complex. Curr. Opin. Struct. Biol. 12, 768-774.
75. POO, M.-M. (1985) Mobility and localization of proteins in excitable membranes. Ann. Rev. Neurosci. 8, 369-406.
76. ROCHLIN, M. W., CHEN, Q., TOBLER, M., TURNER, C. E., BURRIDGE, K. & PENG, H. B. (1989) The relationship between talin and acetylcholine receptor clusters in Xenopus muscle cells. Journal of Cell Science 92, 461-472.
77. SANES, J. R. & LICHTMAN, J. W. (1999) Development of the vertebrate neuromuscular junction. Annual Revew of Neuroscience 22, 389-442.
78. SANES, J. R. & LICHTMAN, J. W. (2001) Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nature Reviews Neuroscience 2, 791-805.
79. SEALOCK, R., PASCHAL, B., BECKERLE, M. & BURRIDGE, K. (1986) Talin is a post-synaptic component of the rat neuromuscular junction. Experimental Cell Research 163, 143-150.
80. SHENG, M. & KIM, E. (2000) The Shank family of scaffold proteins. Journal of Cell Science 113, 1851-1856.
81. SHENG, M. & KIM, M. J. (2002) Postsynaptic signaling and plasticity mechanisms. Science 298, 776-780.
82. STRACK, S., BARBAN, M. A., WADZINSKI, B. E. & COLBRAN, R. J. (1997) Differential inactivation of postsynaptic density-associated and soluble Ca2+/calmodulin-dependent protein kinase II by protein phosphatases 1 and 2A. J. Neurochem. 68, 2119-2128.
83. SUETSUGU, S., HATTORI, M., MIKI, H., TEZUKA, T., YAMAMOTO, T., MIKOSHIBA, K. & TAKENAWA, T. (2002) Sustained activation of N-WASP through phosphorylation is essential for neurite extension. Developmental Cell 3, 645-658.
84. TEZUKA, T., UMEMORI, H., AKIYAMA, T., NAKANISHI, S. & YAMAMOTO, T. (1999) PSD-95 promotes Fyn-mediated tyrosine phosphorylation of the N-methyl-D-aspartate receptor subunit NR2A. Proc. Natl. Acad. Sci. USA 19, 435-440.
85. TILL, J. H., BECERRA, M., WATTY, A., LU, Y., MA, Y., NEUBERT, T. A., BURDEN, S. J. & HUBBARD, S. R. (2002) Crystal structure of the MuSK tyrosine kinase: Insights into receptor autoregulation. Structure (Cambridge) 10, 1187-1196.
86. TOGASHI, H., ABE, K., MIZOGUCHI, A., TAKAOKA, K., CHISAKA, O. & TAKEICHI, M. (2002) Cadherin regulates dendritic spine morphogenesis. Neuron 35, 77-89.
87. TURING, A. M. (1990) The chemical basis of morphogenesis. 1953. Bulletin of Mathematical Biology 52, 153-197.
88. TURNER, C. E., KRAMARCY, N., SEALOCK, R. & BURRIDGE, K. (1991) Localization of paxillin, a focal adhesion protein, to smooth muscle dense plaques, and the myotendinous and neuromuscular junctions of skeletal muscle. Experimental Cell Research 192, 651-655.
89. 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., THOMAS, S., LE BEAU, M. M., FERNALD, A. A., COPELAND, N. G., JENKINS, N. A., BURDEN, S. J., GLASS, D. J. & YANCOPOULOS, G. D. (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.
90. 1, associated with acetylcholine receptor containing membrane fragments is an actin-binding protein. EMBO Journal 3, 2287-2296.
91. WALLACE, B. G. (1994) Staurosporine inhibits agrin-induced acetylcholine receptor phosphorylation and aggregation. Journal of Cell Biology 125, 661-668.
92. WALLACE, B. G., QU, Z. & HUGANIR, R. L. (1991) Agrin induces phosphorylation of the nicotinic acetylcholine receptor. Neuron 6, 869-878.
93. WEED, S. A. & PARSONS, J. T. (2001) Cortactin: Coupling membrane dynamics to cortical actin assembly. Oncogene 20, 6418-6434.
94. WEISS, J. N., QU, Z. & GARFINKEL, A. (2003) Understanding biological complexity: Lessons from the past. FASEB Journal 17, 1-6.
95. WESTON, C., YEE, B., HOD, E. & PRIVES, J. (2000) Agrin-induced acetylcholine receptor clustering is mediated by the small guanosine triphosphatases Rac and Cdc42. Journal of Cell Biology 150, 205-212.
96. WU, H., REYNOLDS, A. B., KANNER, S. B., VINES, R. R. & PARSONS, J. T. (1991) Identification and characterization of a novel cytoskeleton-associated pp60src substrate. Molecular and Cellular Biology 11, 5113-5124.
97. WYSZYNSKI, M., KHARAZIA, V., SHANGHVI, R., RAO, A., BEGGS, A. H., CRAIG, A. M., WEINBERG, R. & SHENG, M. (1998) Differential regional expression and ultrastructural localization of alpha-actinin-2, a putative NMDA receptor-anchoring protein, in rat brain. Journal of Neuroscience 18, 1383-1392.
98. WYSZYNSKI, M., LIN, J., RAO, A., NIGH, E., BEGGS, A. H., CRAIG, A. M. & SHENG, M. (1997) Competitive binding of alpha-actinin and calmodulin to the NMDA receptor. Nature 385, 439-442.
99. XIE, M. H., YUAN, J., ADAMS, C. & GURNEY, A. (1997) Direct demonstration of MuSK involvement in acetylcholine receptor clustering through identification of agonist ScFv. Nature Biotechnology 15, 768-771.
100. YANG, X., ARBER, S., WILLIAM, C., LI, L., TANABE, Y., JESSELL, T. M., BIRCHMEIER, C. & BURDEN, S. J. (2001) Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 30, 399-110.
101. YU, X. M., ASKALAN, R., KEIL, G. J. & SALTER, M. W. (1997) NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science 275, 674-678.
102. ZHU, D.-L. & PENG, H. B. (1988) Increase in intracellular calcium induced by the polycation-coated latex bead, a stimulus that causes postsynaptic-type differentiation in cultured muscle cells. Developmental Biology 126, 63-70.