N-acetyllactosamine and the CT carbohydrate antigen mediate agrin- dependent activation of MuSK and acetylcholine receptor clustering in skeletal muscle

Molecular and Cellular Neurosciences

Volumn 15, Issue 4, 2000, Pages 380-397

  Parkhomovskiy, Natasha ^a   Kammesheidt, Anja ^a   Martin, Paul T ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGRIN; CARBOHYDRATE; CARBOHYDRATE ANTIGEN; CHOLINERGIC RECEPTOR; MUCIN; N ACETYLGALACTOSAMINE; PEANUT AGGLUTININ; PHOSPHOTRANSFERASE; SIALIDASE;

ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CELL STRAIN COS1; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MOUSE; NEUROMUSCULAR SYNAPSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ANIMALIA; ARACHIS HYPOGAEA; MAMMALIA;

EID: 0034028291     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1006/mcne.2000.0835     Document Type: Article

References (52)

1. Bowen D. C., Sugiyama J., Ferns M., Hall Z. W. Neural agrin activates a high-affinity receptor in C2 muscle cells that is unresponsive to muscle agrin. J. NeuroScience 16:1996;3791-3797
2. Burgess R. W., Nguyen Q. T., Son Y. J., Lichtman J. W., Sanes J. R. Alternatively spliced isoforms of nerve- and muscle-derived agrin: Their roles at the neuromuscular junction. Neuron. 23:1999;23-44
3. Burkin D. J., Gu M., Hodges B., Campanelli J. T., Kaufman S. J. A functional role for specific-spliced variants of the α7β1 integrin in acetylcholine receptor clustering. J. Cell Biol. 143:1998;1067-1075
4. Campanelli J. T., Roberds S. L., Campbell K. P., Scheller R. H. A role for dystrophin-associated glycoproteins and utrophin in agrin-induced AChR clustering. Cell. 77:1994;663-674
5. Campanelli J. T., Gayer G. G., Scheller R. H. Alternative RNA splicing that determines agrin activity regulates binding to heparin and alpha dystroglycan. Development. 122:1996;1663-1672
6. Cheresh D. A., Klier F. G. Disialoganglioside GD2 distributes preferentially into substrate-associated microprocesses on human melanoma cells during their attachment to fibronectin. J. Cell Biol. 102:1986;1887-1897
7. Cheresh D. A., Pytela R., Pierschbacher M. D., Klier F. G., Ruoslahti E., Reisfeld R. A. An Arg-Gly-Asp-directed receptor on the surface of human melanoma cells exists in a divalent cation-dependent functional complex with the disialoganglioside GD2. J. Cell Biol. 105:1987;1163-1173
8. Chiba A. Structures of sialylated O-linked oligosaccharides of bovine peripheral nerve α dystroglycan. J. Biol. Chem. 272:1997;2156-2162
9. Chomczynski P., Sacchi N. Single-step method of RNA isolation of acid-guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159
10. Conzelman A., Lefrancois L. Monoclonal antibodies specific for T cell-associated carbohydrate determinants react with human blood group antigens Cad and Sda. J. Exp. Med. 167:1988;119-131
11. Cornish T., Chi J., Johnson S., Lu Y., Campanelli J. T. Globular domains of agrin are functional units that collaborate to induce acetylcholine receptor clustering. J. Cell Science 112:1999;1213-1223
12. DeChiara T. M. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell. 85:1996;501-512
13. Decastel M., Tran A.-T., Frenoy J.-P. Binding of 4-methylumbelliferyl-galactosides to peanut agglutinin. Biochem. Biophys. Res. Commun. 106:1982;838-643
14. Ervasti J. M., Burwell A. L., Geissler A. L. Tissue-specific heterogeneity in α-dystroglycan sialoglycosylation. J. Biol. Chem. 272:1997;22315-22321
15. Ferns M. J., Campanelli J. T., Hoch W., Scheller R. H., Hall Z. W. The ability of agrin to cluster AChRs depends on alternative splicing and on cell surface proteoglycans. Neuron. 11:1993;491-502
16. Gautam M., Noakes P. G., Moscoso L., Rupp F., Scheller R. H., Merlie J. P., Sanes J. R. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell. 85:1996;525-535
17. Gesemann M., Denzer A. J., Ruegg M. A. Acetylcholine receptor aggregating activity of agrin isoforms and mapping of the active site. J. Cell Biol. 128:1995;625-636
18. Gesemann M., Cavalli V., Denzer A. J., Brancaccio A., Schumacher B., Ruegg M. A. Alternative splicing of agrin alters its binding to heparin, dystroglycan, and the putative agrin receptor. Neuron. 16:1996;755-767
19. Ghattas I. R., Sanes J. R., Majors J. E. The encephalomyocarditis virus ribosome entry site allows efficient coexpression of two genes from a recombinant provirus in cultured cells and embryos. Mol. Cell Biol. 11:1991;5848-5859
20. Glass D. J. Agrin acts via a MuSK receptor complex. Cell. 85:1996;513-523
21. Hoch W., Ferns M., Campanelli J. T., Hall Z. W., Scheller R. H. Developmental regulation of highly active alternatively spliced forms of agrin. Neuron. 11:1993;479-490
22. Hoch W., Campanelli J. T., Harrison S., Scheller R. H. Structural domains of agrin required for clustering of nicotinic acetylcholine receptors. EMBO J. 13:1994;2814-2821
23. Hopf C., Hoch W. Tyrosine phosphorylation of the muscle-specific kinase is exclusively induced by acetylcholine receptor-aggregating agrin fragments. Eur. J. Biochem. 253:1998;382-389
24. Hopp T. P. A short polypeptide marker sequence useful for recombinant protein identification and purification. Biotechnology. 6:1988;1204-1210
25. Huet G. GalNAc-α-O-benzyl inhibits NeuAcα2-3 glycosylation and blocks the intracellular transport of apical glycoproteins and mucus in differentiated HT-29 cells. J. Cell Biol. 141:1998;1411-1322
26. Lefrancois L. Carbohydrate differentiation antigens of murine T cells: Expression on intestinal lymphocytes and intestinal epithelium. J. Immunol. 138:1987;3375-3384
27. Lefrancois L., Bevan M. J. Novel antigenic determinants of the T200 glycoprotein expressed preferentially by activated cytotoxic T lymphocytes. J. Immunol. 135:1985a;374-383
28. Lefrancois L., Bevan M. J. Functional modification of cytotoxic T-lymphocyte T200 glycoprotein recognized by monoclonal antibodies. Nature. 314:1985b;449-452
29. Martin P. T., Sanes J. R. Role for a synapse-specific carbohydrate in agrin-induced clustering of acetylcholine receptors. Neuron. 14:1995;743-754
30. Martin P. T., Ettinger A. J., Sanes J. R. A synaptic localization domain in the synaptic cleft protein laminin β2 (S-laminin). Science. 269:1995;413-416
31. Martin P. T., Sanes J. R. Integrins mediate adhesion to agrin and modulate agrin signaling. Development. 124:1997;3909-3917
32. Martin P. T., Scott L. J. C., Porter B. E., Sanes J. R. Distinct structures and functions of related pre- and postsynaptic carbohydrates at the mammalian neuromuscular junction. Mol. Cell. NeuroScience 13:1999;105-118
33. Montanaro F., Gee S. H., Jacobson C., Lindenbaum M. H., Froehner S. C., Carbonetto S. Laminin and α-dystroglycan mediate acetylcholine receptor aggregation via a MuSK-independent pathway. J. NeuroScience 18:1998;1250-1260
34. Neurohr K. J., Young N. M., Mantsch H. H. Determination of the carbohydrate-binding properties of peanut agglutinin by ultraviolet difference spectroscopy. J. Biol Chem. 255:1980;9205-9209
35. Neurohr K. J., Young N. M., Smith I. C. P., Mantsch H. H. Kinetics of binding of methyl-α and β- d -galactopyranoside to peanut agglutinin: A carbon-13 nuclear magnetic resonance study. Biochemistry. 20:1981;3499-3504
36. Obata K., Oide M., Handa S. Effects of glycolipids on in vitro development of neuromuscular junction. Nature. 266:1977;369-371
37. Reist N. E., Werle M. J., McMahan U. J. Agrin released by motor neurons induces the aggregation of acetylcholine receptors at neuromuscular junctions. Neuron. 8:1992;865-868
38. Repraeger A. C., Krufka A., Olwin B. B. Requirement of heparin sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science. 252:1991;1705-1707
39. Rupp F., Payan D. G., Magill-Solc C., Cowan D. M., Scheller R. H. Structure and expression of a rat agrin. Neuron. 6:1991;811-823
40. Sanes J. R., Cheney J. M. Lectin binding reveals a synapse-specific carbohydrate in skeletal muscle. Nature. 300:1982;646-647
41. Sasaki T., Yamada H., Matsumura K., Shimizu T., Kobata A., Endo T. Detection of O-mannosyl glycans in rabbit skeletal muscle α-dystroglycan. Biochim. Biophys. Acta. 1425:1998;599-606
42. Scott L. J. C., Bacou F., Sanes J. R. A synapse-specific carbohydrate at the neuromuscular junction: Association with both acetylcholinesterase and a glycolipid. J. NeuroScience 8:1988;932-944
43. Smalheiser N. R., Haslam S. M., Sutton-Smith M., Morris H. R., Dell A. Structural analysis of sequences O-linked to mannose reveals a novel Lewis X structure in cranin (dystroglycan) purified from sheep brain. J. Biol. Chem. 273:1998;23698-23703
44. Smith P. L., Lowe J. B. Molecular cloning of a murine N-acetylgalactosamine transferase cDNA that determines expression of the T lymphocyte-specific CT oligosaccharide differentiation antigen. J. Biol. Chem. 269:1994;15162-15171
45. Sugiyama J., Bowen D. C., Hall Z. W. Dystroglycan binds nerve and muscle agrin. Neuron. 13:1994;103-115
46. Sugiyama J. E., Glass D. J., Yancopoulos G. D., Hall Z. W. Laminin-induced acetylcholine receptor clustering: An alternative pathway. J. Cell Biol. 139:1997;181-191
47. Tsim K. W. K., Ruegg M. A., Escher G., Kroger S., McMahan U. J. cDNA that encodes active agrin. Neuron. 8:1992;677-689
48. Valenzuela D. M. Receptor tyrosine kinase specific for skeletal muscle lineage: Expression in embryonic muscle, at the neuromuscular junction, and after injury. Neuron. 15:1995;573-584
49. Varki A. Sialic acids as ligands in recognition phenomena. FASEB J. 11:1997;248-255
50. Wallace B. G. Inhibition of agrin-induced acetylcholine receptor aggregation by heparin, heparin sulfate, and other polyanions. J. NeuroScience 10:1990;3576-3582
51. Yaffe D., Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 270:1977;725-727
52. Yayon A., Klagsbrun M., Esko J. D., Leder P., Ornitz D. M. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell. 64:1991;841-848