The developing avian retina expresses agrin isoforms during synaptogenesis

Journal of Neurobiology

Volumn 29, Issue 2, 1996, Pages 165-182

  Kröger, Stephan ^a   Horton, Sharon E ^b   Honig, Lawrence S ^b,c  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

agrin; chick; extracellular matrix; retina; synaptogenesis

Indexed keywords

AGRIN; IMMUNOGLOBULIN F(AB) FRAGMENT;

ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; EXTRACELLULAR MATRIX; GENE EXPRESSION; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; NERVOUS SYSTEM DEVELOPMENT; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; RETINA DEVELOPMENT; RETINA GANGLION CELL; SYNAPTIC MEMBRANE; SYNAPTOGENESIS;

AGRIN; ANIMALS; AXONS; CHICK EMBRYO; EXTRACELLULAR SPACE; IMMUNOGLOBULIN FAB FRAGMENTS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; ISOMERISM; NERVE FIBERS; OPTIC NERVE; POLYMERASE CHAIN REACTION; RETINA; RETINAL GANGLION CELLS; RNA, MESSENGER; SYNAPSES; VITREOUS BODY;

EID: 0030032097     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(199602)29:2<165::AID-NEU4>3.3.CO;2-G     Document Type: Article

References (55)

1. AOKI, C., JOH, T. H., and PICKEL, V. M. (1987). Ultrastructural localization of β-adrenergic receptor-like immunoreactivity in the cortex and neostriatum of rat brain. Brain Res. 437:264-282.
2. BAUDE, A., NUSSER, Z., ROBERTS, J. D., MULVIHILL, E., MCILHINNEY, R. A., and SOMOGYI, P. (1993). The metabotropic glutamate receptor (mGluR1 alpha) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11:771-787.
3. BIROC, S. L., PAYAN, D. G., and FISHER, J. M. (1993). Isoforms of agrin are widely expressed in the developing rat and may function as protease inhibitors. Dev Brain Res. 75:119-129.
4. 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.
5. COLE, G. J., LOEWY, A., and GLASER, L. (1986). Neuronal cell-cell adhesion depends on interactions of N-CAM with heparin-like molecules. Nature 320:445-447
6. 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.
7. DOWLING, J. E. and BOYCOTT, B. B. (1966). Organization of the primate retina: electron microscopy. Proc. R. Soc. Lond. 166:80-111.
8. 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.
9. 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.
10. 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.
11. 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.
12. GODFREY, E. W., DIETZ, M. E., MORSTAD, A. L., WALLSKOG, P. A., and YORDE, D. E. (1988). Acetylcholine receptor-aggregating proteins are associated with the extracellular matrix of many tissues in Torpedo. J. Cell Biol. 106:1263-1272.
13. HALFTER, W. (1993). A heparan sulfate proteoglycan in developing avian axonal tracts. J Neurosci. 13:2863-2873.
14. 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,
15. HALFTER, W., NEWGREEN, D. F., SAUTER, J., and SCHWARZ, U. J. (1983). Oriented axon outgrowth from avian embryonic retinae in culture. Dev. Biol. 95:56-64.
16. HALFTER, W., RECKHAUS, W., and KRÖGER, S. (1987). Nondirected axonal growth on basal lamina from avian embryonic neural retina. J. Neurosci. 7:3712-3722.
17. HALL, Z. W. and SANES, J. R. (1993). Synaptic structure and development: the neuromuscular junction. Cell 72/Neuron 10 (Suppl):99-121.
18. HAMBURGER, V. and HAMILTON, H. L. (1951). A series of normal stages in the development of the chick embryo. J Morphol. 88:48-92.
19. 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.
20. HOCH, W., CAMPANELLI, J. T., HARRISON, S., and SCHELLER, R. H. (1994). Structural domains of agrin required for clustering of nicotinic acetylcholine receptors. EMBO J. 13:2814-2821.
21. HONIG, L. S., STONE, D., NIKOLICS, K., and MCMAHAN, U. J. (1993). Agrin isoforms in developing chick motor neurons. Soc. Neurosci. Abstr. 19:1272.
22. HUANG, Q., ZHOU, D., CHASE, K., GUSELLA, J. F., ARONIN, N., and DIFIGLIA, M. (1992). Immunohistochemical localization of the D1 dopamine receptor in rat brain reveals its axonal transport, pre- and postsynaptic localization, and prevalence in the basal ganglia, limbic system, and thalamic reticular nucleus. Proc. Natl. Acad. Sci. USA 89:11988-11992.
23. HUGHES, W. F. and LA VELLE, A. (1974). On the synaptogenic sequence in the chick retina. Anat. Rec. 179: 297-302.
24. HUNTLEY, G. W., ROGERS, S. W., MORAN, T., JANSSEN, W., ARCHIN, N., VICKERS, J. C., CAULEY, K., HEINEMANN, S. F., and MORRISON, J. H. (1993). Selective distribution of kainate receptor subunit immunoreactivity in monkey neocortex revealed by a monoclonal antibody that recognizes glutamate receptor subunits GluR5/6/7. J. Neurosci. 13:2965-2981.
25. KAMAKURA, K., TADANO, Y., KAWAI, M., ISHIURA, S., NAKAMURA, R., MIYAMOTO, K., NAGATA, N., and SUGITA, H. (1994). Dystrophin-related protein is found in the central-nervous-system of mice at various developmental stages, especially at the postsynaptic membrane. J. Neurosci. Res. 37:728-734.
26. KIRSCH, J., WOLTERS, I., TRILLER, A., and BETZ, H. (1993). Gephyrin antisense oligonucleotides prevent glycine receptor clustering in spinal neurons. Nature 366:745-748.
27. LENTZ, T. L., and CHESTER, J. (1977). Localization of acetylcholine receptors in central synapses. J. Cell Biol. 75:258-267.
28. LIDOV, H. G., BYERS, T. J., WATKINS, S. C., and KUNKEL, L. M. (1990). Localization of dystrophin to postsynaptic regions of central nervous system cortical neurons. Nature 348:725-728.
29. MA, E., MORGAN, R., and GODFREY, E. W. (1994). Distribution of agrin messenger-RNAs in the chick embryo nervous system. J. Neurosci. 14:2943-2952.
30. MA, E., MORGAN, R., and GODFREY, E. W. (1995). Agrin variants are differentially regulated in the developing chick embryo spinal cord and sensory ganglia. J. Neurobiol. 26:585-597.
31. MAGILL-SOLC, C. and MCMAHAN, U. J. (1988). Motor neurons contain agrin-like molecules. J. Cell Biol. 107:1825-1833.
32. MAGILL-SOLC, C. and MCMAHAN, U. J. (1990). Synthesis and transport of agrin-like molecules in motor neurons. J. Exp Biol. 153:1-10.
33. MCMAHAN, U. J. (1990). The agrin hypothesis. Cold Spring Harb. Symp. Quant. Biol. 55:407-418.
34. MCMAHAN, U. J., HORTON, S. E., WERLE, M. J., HONIG, L. S., KRÖGER, S., RUEGG, M. A., and ESCHER, G. (1992). Agrin isoforms and their role in synaptogenesis. Curr. Opin Cell Biol. 4:869-874.
35. 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.
36. NOMURA, A., SHIGEMOTO, R., NAKAMURA, Y., OKAMOTO, N., MIZUNO, N., and NAKANISHI, S. (1994). Developmentally-regulated postsynaptic localization of a metabotropic glutamate-receptor in rat rod bipolar cells. Cell 77:361-369.
37. O'CONNOR, L. T., LAUTERBORN, J. C., GALL, C. M., and SMITH, M. A. (1994). Localization and alternative splicing of agrin messenger-RNA in adult rat brain - transcripts encoding isoforms that aggregate acetylcholine receptors are not restricted to cholinergic regions. J. Neurosci. 14:1141-1152.
38. PETRALIA, R. S., YOKOTANI, N., and WENTHOLD, R. J. (1994). Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J. Neurosci. 14:667-696.
39. PRADA, C., PUGA, J., PEREZ-MENDEZ, L., LOPEZ, R., and RAMIREZ, G. (1991). Spatial and temporal patterns of neurogenesis in the chick retina. Eur. J. Neurosci. 3:559-569.
40. RAGER, G. (1976). Morphogenesis and physiogenesis of the retino-tectal connection in the chicken. I. The retinal ganglion cells and their axons. Proc. R. Soc. Lond. B. 192:331-352.
41. RAGER, G., and VON QEYNHAUSEN, B. (1979). Ingrowth and ramification of retinal fibers in the developing optic tectum of the chick embryo. Exp. Brain Res 35:213-227.
42. RAMON Y CAJAL, S. (1893). La rétine des vertébrés. Cellule 9:119-255.
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. REIST, N. E., WERLE, M. J., and MCMAHAN, U. J. (1992). Agrin released by motor neurons induces the aggregation of acetylcholine receptors at neuromuscular junctions. Neuron 8:865-868.
45. RICHARDS, J. G., SCHOCH, P., HARING, P., TAKAC, B., and MÖHLER, H. (1987). Resolving GABAA/ benzodiazepine receptors: cellular and subcellular localization in the CNS with monoclonal antibodies. J. Neurosci 7:1866-1886.
46. 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.
47. 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.
48. SMITH, M. A. and O'DOWD, D. K. (1994). Cell-specific regulation of agrin RNA splicing in the chick ciliary ganglion. Neuron 12:795-804.
49. 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.
50. 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.
51. 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.
52. 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.
53. TSEN, G., HALFTER, W., KRÖGER, S., and COLE, G. J. (1995). Agrin is a heparan sulfate proteoglycan. J. Biol. Chem. 270:3392-3399.
54. TSIM, K. W., RUEGG, M. A., ESCHER, G., KRÖGER, S., and MCMAHAN, U. J. (1992). cDNA that encodes active agrin. Neuron 8:677-689.
55. WISDEN, W., MORRIS, B. J., and HUNT, S. P. (1991). In situ hybridization with synthetic DNA probes. In: Molecular Neurobiology: A Practical Approach. J. Chad and H. Wheal, Eds. Oxford University Press, New York, pp. 205-225.