Axonal targeting of agrin in cultured rat dorsal horn neurons

Journal of Cell Science

Volumn 109, Issue 13, 1996, Pages 2959-2966

  Escher, Gérard ^a   Béchade, Catherine ^b   Levi, Sabine ^b   Triller, Antoine ^b  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

Agrin; Axon; Central nervous system; Gephyrin; Spinal cord

Indexed keywords

AGRIN; GEPHYRIN; MESSENGER RNA;

ANIMAL CELL; ANTIBODY LABELING; ARTICLE; CELLULAR DISTRIBUTION; FLUORESCENCE MICROSCOPY; NERVE CELL CULTURE; NERVE FIBER; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RAT; SPINAL CORD DORSAL HORN;

AGRIN; ANIMALS; AXONS; CELLS, CULTURED; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SPINAL CORD;

EID: 0030449156     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (54)

1. A benzodiazepine receptor complex in granule cells of the cerebellar complex. Neuroscience 51, 739-748.
2. Béchade, C., Sur, C. and Triller, A. (1994). The inhibitory neuronal glycine receptor. BioEssays 16, 735-744.
3. Béchade, C., Colin, I., Kirsch, J., Betz, H. and Triller, A. (1996). Expression of glycine receptor α subunits and gephyrin in cultured spinal neurons. Eur. J. Neurosci. 8, 429-435.
4. Binder, L., Frankfurter, A., Kim, H., Caceres, A., Payne, M. and Rebhun, L. (1984). Heterogeneity of microtubule-associated protein 2 during rat brain development. Proc. Nat. Acad. Sci. USA 81, 5613-5617.
5. Binder, L., Frankfurter, A. and Rebhun, L. (1985). The distribution of tau polypeptides in the mammalian central nervous system. J. Cell Biol. 101, 1371-1378.
6. Biroc, S., Payan, D. and Fisher, J. (1993). Isoforms of agrin are widely expressed in the developing rat and may function as protease inhibitors. Dev. Brain. Res. 75, 119-129.
7. Burg, M., Halfter, W. and Cole, J. (1995). Analysis of proteoglycan expression in developing chicken brain: characterization of a heparan proteoglycan that interacts with the neural cell adhesion molecule. J. Neurosci. 41, 49-64.
8. Campagna, J., Ruegg, M. and Bixby, J. (1995). Agrin is a differentiation-inducing 'stop signal' for motoneurons in vitro. Neuron 15, 1365-1374.
9. Campanelli, J. T., Hoch, W., Rupp, F., Kreiner, T. and Scheller, R. (1991). Agrin mediates cell-contact-induced acetylcholine receptor clustering. Cell 67, 906-916.
10. Colin, I., Rostaing, P. and Triller, A. (1996). Gephyrin accumulates at specific plasmalemma loci during neuronal maturation in vitro. J. Comp. Neurol. (in press).
11. Denzer, A., Gesemann, M., Schumacher, B. and Ruegg, M. (1995). An amino-terminal extension is required for the secretion of chick agrin and its binding to extracellular matrix. J. Cell Biol. 131, 1547-1560.
12. Ferns, M., Hoch, W., Campanelli, J., Rupp, F., Hall, Z. W. and Scheller, R. (1992). RNA splicing regulates agrin-mediated acetylcholine receptor clustering activity on cultured myotubes. Neuron 8, 1079-1086.
13. Ferns, M. J., Campanelli, J. T., Hoch, W., Scheller, R. H. and Hall, Z. (1993). The ability of agrin to cluster AChRs depends on alternative splicing and on cell surface proteoglycans. Neuron 11, 491-502.
14. Ferns, M., Deiner, M. and Hall, Z. (1996). Agrin-induced acetylcholine receptor clustering in mammalian muscle requires tyrosine phosphorylation. J. Cell Biol. 132, 937-944.
15. Gautam, M., Noakes, P., Moscoso, L., Rupp, F., Scheller, R., Merlie, J. and Sanes, J. (1996). Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85, 525-535.
16. Gesemann, M., Denzer, A. and Ruegg, M. (1995). Acetylcholine receptor-aggregating activity of agrin isoforms and mapping of the active site. J. Cell Biol. 128, 625-636.
17. Glass, D. J., Bowen, D. C., Stitt, T., Radziejewski, C., Bruno, J., Ryan, T. E., Gies, D. R., Shah, S., Mattson, K., Burden, S., Distefano, P., Valenzuela, D., DeChiara, T. and Yancopulos, G. (1996). Agrin acts via a MuSK receptor complex. Cell 85, 513-523.
18. Godfrey, E. (1991). Comparison of agrin like proteins from the extracellular matrix of chicken kidney and muscle with neural agrin. a synapse organizing protein. Exp. Cell Res. 195, 99-109.
19. Hall, Z. W. and Sanes, J. R. (1993). Synaptic structure and development: the neuromuscular junction. Cell/Neuron 72/10, 99-121.
20. Henderson, C. E., Camu, W., Mettling, C., Gouin, A., Poulsen, K., Karihaloo, M., Rullamas, J., Evans, T., McMahon, S. B., Armanini, M. P., Berkemeier, L., Philips, H. S. and Rosenthal, A. (1993). Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 363, 266-270.
21. Hoch, W., Ferns, M., Campanelli, J. T., Hall, Z. and Scheller, R. (1993). Developmental regulation of highly active alternatively spliced forms of agrin. Neuron 11, 479-490.
22. Jackson, M. B., Lecar, H., Brenneman, D. E., Fitzgerald, S. and Nelson, P. G. (1982). Electrical development in spinal cord cell culture. J. Neurosci. 2, 1052-1061.
23. Kirsch, J., Wolters, I., Triller, A. and Betz, H. (1993). Gephyrin antisense oligonucleotides prevent glycine receptor clustering in spinal cord. Nature 366, 745-748.
24. Kröger, S., Horton, S. and Honig, L. (1995). The developing avian retina expresses agrin isoforms during synaptogenesis. J. Neurobiol. 29, 165-181.
25. Kröger, S. and Mann, S. (1996). Biochemical and functional characterization of basal lamina-bound agrin in the chick central nervous system. Eur. J. Neurosci.
26. Lafont, F., Rouget, M., Triller, A., Prochianz, A. and Rousselet, A. (1992). In vitro control of neuronal polarity by glycosaminoglycans. Development 114, 17-29.
27. Ma, E., Morgan, R. and Godfrey, E. W. (1994). Distribution of agrin mRNAs in the chick embryo nervous system. J. Neurosci. 14, 2943-2952.
28. Ma, E., Morgan, R. and Godfrey, E. (1995). Agrin mRNA variants are differentially regulated in developing chick embryo spinal cord and sensory ganglia. J. Neurobiol. 585-597.
29. Magill-Solc, C. and McMahan, U. (1988). Motor neurons contain agrin-like molecules. J. Cell Biol. 107, 1825-1833.
30. Magill-Solc, C. and McMahan, U. (1990). Synthesis and transport of agrin-like molecules in motor neurons. J. Exp. Biol. 153, 1-10.
31. McMahan, U. (1990). The agrin hypothesis. Cold Spring Habor Symp. Quant. Biol. 55, 407-418.
32. McMahan, U., Horton, S., Werle, M., Honig, L., Kröger, S., Ruegg, M. and Escher, G. (1992). Agrin isoforms and their role in synaptogenesis. Curr. Opin. Cell Biol. 4, 869-874.
33. Meier, T., Perez, G. M. and Wallace, B. G. (1995). Immobilization of nicotinic acetylcholine receptors in mouse C2 myotubes by agrin-induced protein tyrosine phosphorylation. J Cell Biol. 131, 441-451.
34. Nicola, M. A., Becker, C. M. and Triller, A. (1992). Development of glycine receptor alpha subunit in cultivated rat spinal neurons: an immunocytochemical study. Neurosci. Lett. 138, 173-178.
35. Nitkin, R. M., Smith, M. A., Magill, C., Fallon, J. R., Yao, Y.-M. M., Wallace, B. G. and McMahan, U. J. (1987). Identification of agrin, a synaptic organizing protein from Torpedo electric organ. J. Cell Biol. 105, 2471-2478.
36. O'Connor, L., Lauterborn, J., Gall, C. and Smith, M. (1994). Localization and alternative splicing of agrin mRNA in adult rat brain: transcripts encoding isoforms that aggregate acetylcholine receptors are not restricted to cholinergic regions. J. Neurosci. 14, 1141-1152.
37. Patthy, L. and Nikolics, K. (1993). Functions of agrin and agrin-related proteins. Trends Neurosci. 16, 76-81.
38. Petralia, R. S. and Wenthold, R. J. (1992). Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J. Comp. Neurol. 318, 329-354.
39. Pfeiffer, F., Simler, R., Grenningloh, G. and Betz, H. (1984). Monoclonal antibodies and peptide mapping reveal structural similarities between the subunits of the glycine receptor of rat spinal cord. Proc. Nat. Acad. Sci. USA 81, 7224-7227.
40. Qu, Z. and Huganir, R. L. (1994). Comparison of innervation and agrin-induced tyrosine phosphorylation of the nicotinic acetylcholine receptor. J. Neurosci. 14, 6834-6841.
41. Ruegg, M., Tsim, K., Horton, S., Kröger, S., Escher, G., Gensh, E. and McMahan, U. (1992). The agrin gene codes for a family of a basal lamina proteins that differ in function and distribution. Neuron 8, 691-699.
42. Ruegg, M. (1996). Agrin, laminin b2 (s-laminin) and ARIA: their role in neuromuscular development. Curr. Opin. Neurobiol. 6, 97-103.
43. Rupp, F., Payan, D., Magill-Soc, C., Cowan, D. and Scheller, R. (1991). Structure and expression of a rat agrin. Neuron 6, 811-823.
44. Rupp, F., Özçellik, T., Linial, M., Peterson, K., Francke, U. and Scheller, R. (1992). Structure and chromosomal localization of the mammalian agrin gene. J. Neurosci. 12, 3535-3544.
45. Smith, M., Magill-Solc, C., Rupp, F., Yao, M. Y.-M, Schilling, J., Snow, P. and McMahan, U. (1992). Isolation and characterization of a cDNA that encodes an agrin homolog in the marine ray. Mol. Cell. Neurosci. 3, 406-417.
46. Smith, M. and O'Dowd, D. (1994). Cell-specific regulation of agrin RNA splicing in the chick ciliary ganglion. Neuron 12, 794-804.
47. So, K., Pun, S., Wan, D. and Tsim, K. (1996). Cerebellar granule cells express a specific isoform of agrin that lacks the acetylcholine receptor aggregating activity. FEBS Lett. 379, 63-68.
48. Stone, D. and Nikolics, K. (1995). Tissue- and age specific expression patterns of alternatively spliced agrin mRNA transcripts in embryonic rat suggest novel developmental roles. J. Neurosci. 15, 6767-6778.
49. Triller, A., Cluzeaud, F., Pfeiffer, F., Betz, H. and Korn, H. (1985). Distribution of glycine receptors at central synapses: an immunoelectron microscopy study. J. Cell Biol. 101, 683-688.
50. Triller, A., Cluzeaud, F. and Korn, H. (1987). Gamma-aminobutyric acid-containing terminals can be apposed to glycine receptors at central synapses. J. Cell Biol. 104, 947-956.
51. Tsen, G., Halfter, W., Kröger, S. and Cole, G. (1995a). Agrin is a heparan sulfate proteoglycan. J. Biol. Chem. 270, 3392-3399.
52. Tsen, G., Napier, A., Halfter, W. and Cole, G. (1995b). Identification of a novel spliced agrin mRNA that is preferentially expressed in non-neuronal cells. J. Biol. Chem. 270, 15934-15937.
53. Tsim, K., Ruegg, M., Escher, G., Kroger, S. and McMahan, U. (1992). cDNA that encodes active agrin. Neuron 8, 677-689.
54. Wallace, B. G. (1994). Staurosporin inhibits agrin-induced acetylcholine receptor phosphorylation and aggregation. J. Cell Biol. 125, 661-668.