Formation of synaptic specializations in the inner plexiform layer of the developing chick retina

Molecular and Cellular Neurosciences

Volumn 8, Issue 1, 1996, Pages 1-13

  Mann, Sabine ^a   Kröger, Stephan ^a  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AGRIN; CHOLINERGIC RECEPTOR; CARRIER PROTEIN; GEPHYRIN; MEMBRANE PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; BRAIN DEVELOPMENT; CHICKEN; IMMUNOCYTOCHEMISTRY; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; RETINA CELL; RETINA DEVELOPMENT; ANIMAL; ANTIBODY SPECIFICITY; AUTORADIOGRAPHY; BIOSYNTHESIS; CELL CULTURE; CHEMISTRY; CHICK EMBRYO; CYTOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; METABOLISM; RETINA; SERODIAGNOSIS; SYNAPSE; ULTRASTRUCTURE;

ANIMALIA; GALLUS GALLUS;

AGRIN; ANIMALS; ANTIBODY SPECIFICITY; AUTORADIOGRAPHY; CARRIER PROTEINS; CELLS, CULTURED; CHICK EMBRYO; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; NEUROMUSCULAR JUNCTION; PRECIPITIN TESTS; RECEPTORS, CHOLINERGIC; RETINA; SYNAPSES;

EID: 0030200234     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1006/mcne.1996.0039     Document Type: Article

References (63)

1. Altschuler, R. A., Betz, H., Parakkal, M. H., Reeks, K. A., and Wenthold, R. J. (1986). Identification of glycinergic synapses in the cochlear nucleus through immunocytochemical localization of the postsynaptic receptor. Brain Res. 369: 316-320.
2. Béchade, C., Colin, I., Kirsch, J., Betz, H., and Triller, A. (1996). Expression of glycine receptor a subunits and gephyrin in cultured spinal cord neurons. Eur. J. Neurosci. 8: 429-435.
3. Bird, M. M. (1986). An ultrastructural study of embryonic chick retinal neurons in culture. Cell Tissue Res. 245: 563-577.
4. Bowe, M. A., and Fallon, J. R. (1995). The role of agrin in synapse formation. Annu. Rev. Neurosci. 18: 443-462.
5. Cohen, M. W., and Godfrey, E. W. (1992). Early appearance of and neuronal contribution to agrin-like molecules at embryonic frog nerve-muscle synapses formed in culture. J. Neurosci. 12: 2982-2992.
6. Crisanti-Combes, P., Privat, A., Pessac, B., and Calothy, G. (1996). Differentiation of chick embryo neuroretina cells in monolayer cultures: An ultrastructural study. Cell Tissue Res. 185: 159-173.
7. Daniels, M. P., and Vogel, Z. (1980). Localization of alpha-bungarotoxin binding sites in synapses of the developing chick retina. Brain Res. 201: 45-56.
8. Denzer, A. J., Gesemann, M., Schumacher, B., and Ruegg, M. A. (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.
9. Dowling, J. E., and Boycott, B. B. (1966). Organization of the primate retina: Electron microscopy. Proc. R. Soc. London B. Biol. Sci. 166: 80-111.
10. Fallon, J. R., and Gelfman, C. E. (1989). Agrin-related molecules are concentrated at acetylcholine receptor clusters in normal and aneural developing muscle. J. Cell Biol. 108: 1527-1535.
11. Ferns, M., Hoch, W., Campanelli, J. T., Rupp, F., Hall, Z. W., and Scheller, R. H. (1992). RNA splicing regulates agrin-mediated acetylcholine receptor clustering activity on cultured myotubes. Neuron 8: 1079-1086.
12. Ferns, M. J., Campanelli, J. T., Hoch, W., Scheller, R. H., and Hall, Z. W. (1993). The ability of agrin to cluster AChRs depends on alternative splicing and on cell surface proteoglycans. Neuron 11: 491-502.
13. 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.
14. Gleason, E., and Wilson, M. (1989). Development of synapses between chick retinal neurons in dispersed culture. J. Comp. Neurol. 287: 213-224.
15. Gleason, E., Borges, S., and Wilson, M. (1993). Synaptic transmission between pairs of retinal amacrine cells in culture. J. Neurosci. 13: 2359-2370.
16. Godfrey, E. W. (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.
17. Godfrey, E. W., Siebenlist, R. E., Wallskog, P. A., Walters, L. M., Bolender, D. L., and Yorde, D. E. (1988). Basal lamina components are concentrated in premuscle masses and at early acetylcholine receptor clusters in chick embryo hindlimb muscles. Dev. Biol. 130: 471-486.
18. Graham, F. L., Smiley, J., Russell, W. C., and Nairu, R. (1977). Characteristics of human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol. 36: 59-77.
19. Greferath, U., Brandstätter, J. H., Wässle, H., Kirsch, J., Kuhse, J., and Grunert, U. (1994). Differential expression of glycine receptor subunits in the retina of the rat: A study using immunohistochemistry and in situ hybridization. Visual Neurosci. 11: 721-729.
20. Grünert, U., and Wässle, H. (1993). Immunocytochemical localization of glycine receptors in the mammalian retina. J. Comp. Neurol. 335: 523-537.
21. Halfter, W. (1993). A heparan sulfate proteoglycan in developing avian axonal tracts. J. Neurosci. 13: 2863-2873.
22. Halfter, W., and Fua, C. S. (1987). Immunohistochemical localization of laminin, neural cell adhesion molecule, collagen type IV and T-61 antigen in the embryonic retina of the Japanese quail by in vivo injection of antibodies. Cell Tissue Res. 249: 487-496.
23. Hall, Z. W., and Sanes, J. R. (1993). Synaptic structure and development: The neuromuscular junction. Cell/Neuron 72/10(Suppl.): 99-121.
24. Hamburger, V., and Hamilton, H. L. (1951). A series of normal stages in the development of the chick embryo. J. Morphol. 88: 48-92.
25. Hering, H., and Kröger, S. (1996). Formation of synaptic specializations in the inner plexiform layer of the developing chick retina. J. Comp. Neurol, in press.
26. Hoch, W., Ferns, M., Campanelli, J. T., Hall, Z. W., and Scheller, R. H. (1993). Developmental regulation of highly active alternatively spliced forms of agrin. Neuron 11: 479-490.
27. Hughes, W. F., and LaVelle, A. (1974). On the synaptogenic sequence in the chick retina. Anat. Rec. 179: 297-302.
28. Keyser, K. T., Britto, L. R. G., Schoepfer, R., Whiting, P., Cooper, J., Conroy, W., Brozozowska-Prechtl, A., Karten, H. J., and Lindstrom, J. (1993). Three subtypes of α-bungarotoxin-sensitive nicotinic acetylcholine receptors are expressed in chick retina. J. Neurosci. 13: 442-454.
29. Kirsch, J., and Betz, H. (1993). Widespread expression of gephyrin, a putative glycine receptor-tubulin linker protein, in rat brain. Brain Res. 621: 301-310.
30. Kirsch, J., and Betz, H. (1995). The postsynaptic localization of the glycine receptor-associated protein gephyrin is regulated by the cytoskeleton. J. Neurosci. 15: 4148-4156.
31. Kirsch, J., and Kröger, S. (1996). Postsynaptic anchoring of receptors: A cellular approach to neuronal and muscular sensitivity. Neuroscientist 2: 101-109.
32. Kirsch, J., Wolters, I., Triller, A., and Betz, H. (1993). Gephyrin antisense oligonucleotides prevent glycine receptor clustering in spinal neurons. Nature 366: 745-748.
33. Kröger, S., and Mann, S. (1996). Biochemical and functional characterization of basal lamina-bound agrin in the chick central nervous system. Eur. J. Neurosci. 8: 500-509.
34. Kröger, S., Horton, S. E., and Honig, L. S. (1996). The developing avian retina expresses agrin isoforms during synaptogenesis. J. Neurobiol. 29: 165-182.
35. Ma, E., Morgan, R., and Godfrey, E. W. (1994). Distribution of agrin mRNAs in the chick embryo nervous system. J. Neurosci. 14: 2943-2952.
36. Magill-Solc, C., and McMahan, U. J. (1988). Motor neurons contain agrin-like molecules. J. Cell Biol. 107: 1825-1833.
37. Magill-Solc, C., and McMahan, U. J. (1990). Synthesis and transport of agrin-like molecules in motor neurons. J. Exp. Biol. 153: 1-10.
38. McMahan, U. J. (1990). The agrin hypothesis. Cold Spring Harbor Symp. Quant. Biol. 55: 407-418.
39. Meyer, G., Kirsch, J., Betz, H., and Langosch, D. (1995). Identification of a gephyrin binding motif on the glycine receptor b subunit. Neuron 15: 563-572.
40. Nitkin, R. M., Smith, M. A., Magill, C., Fallon, J. R., Yao, Y. 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.
41. O'Connor, L. T., Lauterborn, J. C., Gall, C. M., and Smith, M. A. (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.
42. Pfeiffer, E., 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. Natl. Acad. Sci. USA 81: 7224-7227.
43. Reist, N. E., Magill, C., and McMahan, U. J. (1987). Agrin-like molecules at synaptic sites in normal, denervated, and damaged skeletal muscles. J. Cell Biol. 105: 2457-2469.
44. Ruegg, M. A., Tsim, K. W., Horton, S. E., Kröger, 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.
45. Rupp, F., Payan, D. G., Magill-Solc, C., Cowan, D. M., and Scheller, R. H. (1991). Structure and expression of a rat agrin. Neuron 6: 811-823.
46. Sassoé-Pognetto, M., Wässle, H., and Grünert, U. (1994). Glycinergic synapses in the rod pathway of the rat retina: Cone bipolar cells express the alpha 1 subunit of the glycine receptor. J. Neurosci. 14: 5131-5146.
47. Sassoé-Pognetto, M., Kirsch, J., Grünert, U., Greferath, U., Fritschy, J. M., Möhler, H., Betz, H., and Wässle, H. (1995). Colocalization of gephyrin and GABAA-receptor subunits in the rat retina. J. Comp. Neurol. 357: 1-14.
48. r 93,000 polypeptide of the postsynaptic glycine receptor complex is a peripheral membrane protein. Biochemistry 26: 805-811.
49. Schwartz, M., Vogel, Z., and Kalcheim, C. (1981). Goldfish brain extract induces aggregation of acetylcholine receptors on cultured myotubes: Increased activity following optic nerve axotomy. Neurosci. Lett. 27: 165-170.
50. Shadiack, A. M., and Nitkin, R. M. (1991). Agrin induces alpha-actinin, filamin, and vinculin to co-localize with AChR clusters on cultured chick myotubes. J. Neurobiol. 22: 617-628.
51. Smith, M. A., Magill-Solc, C., Rupp, F., Yao, Y. M., Schilling, J. W., Snow, P., and McMahan, U. J. (1992). Isolation and characterization of a cDNA that encodes an agrin homolog in the marine ray. Mol. Cell Neurosci. 3: 406-417.
52. Thomas, W. S., O'Dowd, D. K., and Smith, M. A. (1993). Developmental expression and alternative splicing of chick agrin RNA. Dev. Biol. 158: 523-535.
53. Thompson, J. M., and Rapoport, S. I. (1988). Retinal neurons lack an acetylcholine receptor aggregating factor. Synapse 2: 7-10.
54. Todd, A. J., Watt, C., Spike, R. C., and Sieghart, W. (1996). Colocalization of GABA, glycine, and their receptors at synapses in the rat spinal cord. J. Neurosci. 16: 974-982.
55. 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.
56. 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.
57. Trisler, D., Bekenstein, J., and Daniels, M. P. (1986). Antibody to a molecular marker of cell position inhibits synapse formation in retina. Proc. Natl. Acad. Sci. USA 83: 4194-4198.
58. Tsen, G., Napier, A., Halfter, W., and Cole, G. L. (1995a). Identification of a novel alternatively spliced agrin mRNA that is preferentially expressed in non-neuronal cells. J. Biol. Chem. 270: 15934-15937.
59. Tsen, G., Halfter, W., Kröger, S., and Cole, G. J. (1995b). Agrin is a heparan-sulfate proteoglycan. J. Biol. Chem. 270: 3392-3399.
60. Tsim, K. W., Ruegg, M. A., Escher, G., Kröger, S., and McMahan, U. J. (1992). cDNA that encodes active agrin. Neuron 8: 677-689.
61. van den Pol, A. N., and Gorcs, 4T. (1988). Glycine and glycine receptor immunoreactivity in brain and spinal cord. J. Neurosci. 8: 472-492.
62. Wallace, B. G. (1989). Agrin-induced specializations contain cytoplasmic, membrane, and extracellular matrix-associated components of the postsynaptic apparatus. J. Neurosci. 9: 1294-1302.
63. Wässle, H., and Boycott, B. B. (1991). Functional architecture of the mammalian retina. Physiol. Rev. 71: 447-480.