A role for the juxtamembrane domain of β-dystroglycan in agrin-induced acetylcholine receptor clustering

Journal of Neuroscience

Volumn 23, Issue 2, 2003, Pages 392-402

  Kahl, Joanna ^a   Campanelli, James T ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Acetylcholine receptor; Agrin; Dystroglycan; Dystrophin; Juxtamembrane; Neuromuscular junction

Indexed keywords

AGRIN; CHOLINERGIC RECEPTOR; DYSTROGLYCAN;

ANIMAL CELL; ARTICLE; BETA CHAIN; CELL DIFFERENTIATION; GENE DELETION; GENE OVEREXPRESSION; MUTAGENESIS; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RECEPTOR UPREGULATION; STIMULUS RESPONSE; SYNAPTIC TRANSMISSION;

EID: 0037439662     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-02-00392.2003     Document Type: Article

References (74)

1. Andrews DW, Young JC, Mirels LF, Czarnota GJ (1992) The role of the N region in signal sequence and signal-anchor function. J Biol Chem 267:7761-7769.
2. 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 18:623-635.
3. Barker PA, Barbee G, Misko TP, Shooter EM (1994) The low affinity neurotrophin receptor, p75LNTR, is palmitoylated by thioester formation through cysteine 279. J Biol Chem 269:30645-30650.
4. Bartoli M, Ramarao MK, Cohen JB (2001) Interactions of the rapsyn RING-H2 domain with dystroglycan. J Biol Chem 276:24911-24917.
5. Ben-Tal N, Honig B, Peitzsch RM, Denisov G, McLaughlin S (1996) Binding of small basic peptides to membranes containing acidic lipids: theoretical models and experimental results. Biophys J 71:561-575.
6. Bewick GS, Nicholson LV, Young C, O'Donnell E, Slater CR (1992) Different distributions ofdystrophin and related proteins at nerve-muscle junctions. NeuroReport 3:857-860.
7. Blake DJ, Weir A, Newey SE, Davies KE (2002) Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 82:291-329.
8. Borges LS, Ferns M (2001) Agrin-induced phosphorylation of the acetylcholine receptor regulates cytoskeletal anchoring and clustering. J Cell Biol 153:1-12.
9. Bretscher A, Chambers D, Nguyen R, Reczek D (2000) ERM-merlin and EBP50 protein families in plasma membrane organization and function. Annu Rev Cell Dev Biol 16:113-143.
10. Burgess RW, Nguyen QT, Son YJ, Lichtman JW, Sanes JR (1999) Alternatively spliced isoforms of nerve- and muscle-derived agrin: their roles at the neuromuscular junction. Neuron 23:33-44.
11. Byers TJ, Kunkel LM, Watkins SC (1991) The subcellular distribution of dystrophin in mouse skeletal, cardiac, and smooth muscle. J Cell Biol 115:411-421.
12. Campanelli JT, Hoch W, Rupp F, Kreiner T, Scheller RH (1991) Agrin mediates cell contact-induced acetylcholine receptor clustering. Cell 67:909-916.
13. Campanelli JT, Roberds SL, Campbell KP, Scheller RH (1994) A role for dystrophin-associated glycoproteins and utrophin in agrin-induced AChR clustering. Cell 77:663-674.
14. Campanelli JT, Gayer GG, Scheller RH (1996) Alternative RNA splicing that determines agrin activity regulates binding to heparin and alpha-dystroglycan. Development 122:1663-1672.
15. Cartaud A, Coutant S, Petrucci TC, Cartaud J (1998) Evidence for in situ and in vitro association between beta-dystroglycan and the subsynaptic 43K rapsyn protein. Consequence for acetylcholine receptor clustering at the synapse. J Biol Chem 273:11321-11326.
16. Cavaldesi M, Macchia G, Barca S, Defilippi P, Tarone G, Petrucci TC (1999) Association of the dystroglycan complex isolated from bovine brain synaptosomes with proteins involved in signal transduction. J Neurochem 72:1648-1655.
17. Chung W, Campanelli JT (1999) WW and EF hand domains of dystrophin-family proteins mediate dystroglycan binding. Mol Cell Biol Res Commun 2:162-171.
18. Comer FI, Parent CA (2002) PI 3-kinase and PTEN: how opposites chemoattract. Cell 109:541-544.
19. Cornish T, Chi J, Johnson S, Lu Y, Campanelli JT (1999) Globular domains of agrin are functional units that collaborate to induce acetylcholine receptor clustering. J Cell Sci 112:1213-1223.
20. Cote PD, Moukhles H, Lindenbaum M, Carbonetto S (1999) Chimaeric mice deficient in dystroglycans develop muscular dystrophy and have disrupted myoneural synapses. Nat Genet 23:338-342.
21. Couchman JR, Woods A (1999) Syndecan-4 and integrins: combinatorial signaling in cell adhesion. J Cell Sci 112:3415-3420.
22. Dai Z, Luo X, Xie H, Peng HB (2000) The actin-driven movement and formation of acetylcholine receptor clusters. J Cell Biol 150:1321-1334.
23. DeChiara TM, Bowen DC, Valenzuela DM, Simmons MV, Poueymirou WT, Thomas S, Kinetz E, Compton DL, Rojas E, Park JS, Smith C, DiStefano PS, Glass DJ, Burden SJ, Yancopoulos GD (1996) The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85:501-512.
24. Ferns M, Deiner M, Hall Z (1996) Agrin-induced acetylcholine receptor clustering in mammalian muscle requires tyrosine phosphorylation. J Cell Biol 132:937-944.
25. Fuhrer C, Sugiyama JE, Taylor RG, Hall ZW (1997) Association of muscle-specific kinase MuSK with the acetylcholine receptor in mammalian muscle. EMBO J 16:4951-4960.
26. Gautam M, Noakes PG, Mudd J, Nichol M, Chu GC, Sanes JR, Merlie JP (1995) Failure ofpostsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377:232-236.
27. Gautam M, DeChiara TM, Glass DJ, Yancopoulos GD, Sanes JR (1999) Distinct phenotypes of mutant mice lacking agrin, MUSK, or rapsyn. Brain Res Dev Brain Res 114:171-178.
28. Gee SH, Montanaro F, Lindenbaum MH, Carbonetto S (1994) Dystroglycan-alpha, a dystrophin-associated glycoprotein, is a functional agrin receptor. Cell 77:675-686.
29. Gesemann M, Denzer AJ, Ruegg MA (1995) Acetylcholine receptor-aggregating activity of agrin isoforms and mapping of the active site. J Cell Biol 128:625-636.
30. Glass DJ, Apel ED, Shah S, Bowen DC, DeChiara TM, Stitt TN, Sanes JR, Yancopoulos GD (1997) Kinase domain of the muscle-specific receptor tyrosine kinase (MuSK) is sufficient for phosphorylation but not clustering of acetylcholine receptors: required role for the MuSK MUSK ectodomain? Proc Natl Acad Sci USA 94:8848-8853.
31. Grady RM, Zhou H, Cunningham JM, Henry MD, Campbell KP, Sanes JR (2000) Maturation and maintenance of the neuromuscular synapse: genetic evidence for roles of the dystrophin-glycoprotein complex. Neuron 25:279-293.
32. Harder T, Kuhn M (2000) Selective accumulation of raft-associated membrane protein LAT in T cell receptor signaling assemblies. J Cell Biol 151:199-208.
33. Heathcote RD, Ekman JM, Campbell KP, Godfrey EW (2000) Dystroglycan overexpression in vivo alters acetylcholine receptor aggregation at the neuromuscular junction. Dev Biol 227:595-605.
34. Heiska L, Alfthan K, Gronholm M, Vilja P, Vaheri A, Carpen O (1998) Association of ezrin with intercellular adhesion molecule-1 and -2 (ICAM-1 and ICAM-2). Regulation by phosphatidylinositol 4,5-bisphosphate. J Biol Chem 273:21893-21900.
35. Henry MD, Campbell KP (1999) Dystroglycan inside and out. Curr Opin Cell Biol 11:602-607.
36. Hobert M, Carlin C (1995) Cytoplasmic juxtamembrane domain of the human EGF receptor is required for basolateral localization in MDCK cells. J Cell Physiol 162:434-446.
37. Hopf C, Hoch W (1996) 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. J Biol Chem 271:5231-5236.
38. Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, Slaughter CA, Sernett SW, Campbell KP (1992) Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355:696-702.
39. Jacobson C, Montanaro F, Lindenbaum M, Carbonetto S, Ferns M (1998) α-Dystroglycan functions in acetylcholine receptor aggregation but is not a coreceptor for agrin-MuSK signaling. J Neurosci 18:6340-6348.
40. James M, Nuttall A, Iisley JL, Ottersbach K, Tinsley JM, Sudol M, Winder SJ (2000) Adhesion-dependent tyrosine phosphorylation of (beta)-dystroglycan regulates its interaction with utrophin. J Cell Sci 113:1717-1726.
41. Jones MA, Werle MJ (2000) Nitric oxide is a downstream mediator of agrin-induced acetylcholine receptor aggregation. Mol Cell Neurosci 16:649-660.
42. Jung D, Yang B, Meyer J, Chamberlain JS, Campbell KP (1995) Identification and characterization of the dystrophin anchoring site on beta-dystroglycan. J Biol Chem 270:27305-27310.
43. Khan AA, Bose C, Yam LS, Soloski MJ, Rupp F (2001) Physiological regulation of the immunological synapse by agrin. Science 292:1681-1686.
44. Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua NH (1999) Rac homologues and compartmentalized phosphatidylinositol 4,5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 145:317-330.
45. Koziak K, Kaczmarek E, Kittel A, Sevigny J, Blusztajn JK, Schulte Am Esch J, Imai M, Guckelberger O, Goepfert C, Qawi I, Robson SC (2000) Palmitoylation targets CD39/endothelial ATP diphosphohydrolase to caveolae. J Biol Chem 275:2057-2062.
46. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
47. Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451-461.
48. Legg JW, Isacke CM (1998) Identification and functional analysis of the ezrin-binding site in the hyaluronan receptor, CD44. Curr Biol 8:705-708.
49. Luck G, Hoch W, Hopf C, Blottner D (2000) Nitric oxide synthase (NOS-1) coclustered with agrin-induced AChR-specializations on cultured skeletal myotubes. Mol Cell Neurosci 16:269-281.
50. Marchand S, Stetzkowski-Marden F, Cartaud J (2001) Differential targeting of components of the dystrophin complex to the postsynaptic membrane. Eur J Neurosci 13:221-229.
51. McMahan UJ (1990) The agrin hypothesis. Cold Spring Harb Symp Quant Biol 55:407-418.
52. Megeath LJ, Fallon JR (1998) Intracellular calcium regulates agrin-induced acetylcholine receptor clustering. J Neurosci 18:672-678.
53. Misra S, Hurley JH (1999) Crystal structure of a phosphatidylinositol 3-phosphate-specific membrane-targeting motif, the FYVE domain of Vps27p. Cell 97:657-666.
54. Mohamed AS, Rivas-Plata KA, Kraas JR, Saleh SM, Swope SL (2001) Src-class kinases act within the agrin/MuSK pathway to regulate acetylcholine receptor phosphorylation, cytoskeletal anchoring, and clustering. J Neurosci 21:3806-3818.
55. Phillips WD, Noakes PG, Roberds SL, Campbell KP, Merlie JP (1993) Clustering and immobilization of acetylcholine receptors by the 43-kD protein: a possible role for dystrophin-related protein. J Cell Biol 123:729-740.
56. Qu Z, Huganir RL (1994) Comparison of innervation and agrin-induced tyrosine phosphorylation of the nicotinic acetylcholine receptor. J Neurosci 14:6834-6841.
57. Ren Q, Bennett V (1998) Palmitoylation of neurofascin at a site in the membrane-spanning domain highly conserved among the L1 family of cell adhesion molecules. J Neurochem 70:1839-1849.
58. Rentschler S, Linn H, Deininger K, Bedford MT, Espanel X, Sudol M (1999) The WW domain of dystrophin requires EF-hands region to interact with beta-dystroglycan. Biol Chem 380:431-442.
59. Rohatgi R, Ho HY, Kirschner MW (2000) Mechanism of N-WASP activation by CDC42 and phosphatidylinositol 4,5-bisphosphate. J Cell Biol 150:1299-1310.
60. Russo K, Di Stasio E, Macchia G, Rosa G, Brancaccio A, Petrucci TC (2000) Characterization of the beta-dystroglycan-growth factor receptor 2 (Grb2) interaction. Biochem Biophys Res Commun 274:93-98.
61. Saito F, Masaki T, Kamakura K, Anderson LV, Fujita S, Fukuta-Ohi H, Sunada Y, Shimizu T, Matsumura K (1999) Characterization of the transmembrane molecular architecture of the dystroglycan complex in Schwann cells. J Biol Chem 274:8240-8246.
62. Sander A, Hesser BA, Witzemann V (2001) MuSK induces in vivo acetylcholine receptor clusters in a ligand-independent manner. J Cell Biol 155:1287-1296.
63. Sanes JR, Lichtman JW (2001) Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2:791-805.
64. Snyers L, Umlauf E, Prohaska R (1999) Cysteine 29 is the major palmitoylation site on stomatin. FEBS Lett 449:101-104.
65. Sotgia F, Lee JK, Das K, Bedford M, Petrucci TC, Macioce P, Sargiacomo M, Bricarelli FD, Minetti C, Sudol M, Lisanti MP (2000) Caveolin-3 directly interacts with the C-terminal tail of beta-dystroglycan. Identification of a central WW-like domain within caveolin family members. J Biol Chem 275:38048-38058.
66. Sugiyama J, Bowen DC, Hall ZW (1994) Dystroglycan binds nerve and muscle agrin. Neuron 13:103-115.
67. Wahlberg JM, Spiess M (1997) Multiple determinants direct the orientation of signal-anchor proteins: the topogenic role of the hydrophobic signal domain. J Cell Biol 137:555-562.
68. Wallace BG (1995) Regulation of the interaction of nicotinic acetylcholine receptors with the cytoskeleton by agrin-activated protein tyrosine kinase. J Cell Biol 128:1121-1129.
69. Weston C, Yee B, Hod E, Prives J (2000) Agrin-induced acetylcholine receptor clustering is mediated by the small guanosine triphosphatases rac and cdc42. J Cell Biol 150:205-212.
70. Yang B, Jung D, Motto D, Meyer J, Koretzky G, Campbell KP (1995) SH3 domain-mediated interaction of dystroglycan and Grb2. J Biol Chem 270:11711-11714.
71. Yonemura S, Hirao M, Doi Y, Takahashi N, Kondo T, Tsukita S (1998) Ezrin/radixin/moesin (ERM) proteins bind to a positively charged amino acid cluster in the juxta-membrane cytoplasmic domain of CD44, CD43, and ICAM-2. J Cell Biol 140:885-895.
72. Yoon SO, Soltoff SP, Chao MV (1997) A dominant role of the juxtamembrane region of the TrkA nerve growth factor receptor during neuronal cell differentiation. J Biol Chem 272:23231-23238.
73. Zhang W, Trible RP, Samelson LE (1998) LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation. Immunity 9:239-246.
74. Zhang W, Irvin BJ, Trible RP, Abraham RT, Samelson LE (1999) Functional analysis of LAT in TCR-mediated signaling pathways using a LAT-deficient Jurkat cell line. Int Immunol 11:943-950.