Localization of components of glycinergic synapses during rat spinal cord development

Journal of Comparative Neurology

Volumn 398, Issue 3, 1998, Pages 359-372

  Colin, I ^a,b   Rostaing, P ^a   Augustin, A ^a   Triller, A ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

GABA; Glycine; Glycine receptor; Immunogold; Inhibition; Synaptic transmission

Indexed keywords

4 AMINOBUTYRIC ACID; GEPHYRIN; GLYCINE; GLYCINE RECEPTOR; MONOCLONAL ANTIBODY; POSTSYNAPTIC RECEPTOR;

ADOLESCENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; RAT; RECEPTOR DENSITY; SPINAL CORD; SPINAL CORD VENTRAL HORN; SYNAPSE;

ANIMALS; CARRIER PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; GLYCINE; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA; RECEPTORS, GLYCINE; RECEPTORS, PRESYNAPTIC; SPINAL CORD; SYNAPSES;

EID: 0032585033     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980831)398:3<359::AID-CNE5>3.0.CO;2-Z     Document Type: Article

References (63)

1. Balice-Gordon, R.J., C.K. Chua, C.C. Nelson, and J.W. Lichtman (1993) Gradual loss of synaptic cartel precedes axon withdrawal at developing neuromuscular junctions. Neuron 77:801-815.
2. Balice-Gordon, R. J. and J.W. Lichtman (1990) In vivo visualization of the growth of pre- and postsynaptic elements of neuromuscular junction in the mouse. J. Neurosci. 70:894-908.
3. Baude, A., Z. Nusser, E. Molnar, R.A. Mcilhinney, and P. Somogyi (1995) High-resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and non-synaptic sites in rat hippocampus. Neuroscience 69:1031-1055.
4. Béchade, C., I. Colin, J. Kirsch, H. Betz, and A. Triller (1996) Expression of glycine receptor α subunits and gephyrin in cultured spinal neurons. Eur. J. Neurosci. 8:429-435.
5. Béchade, C., C. Sur, and A. Triller (1994) The inhibitory neuronal glycine receptor. Bioessays 16:735-744.
6. - natal development. ETIBO J. 7:3317-3726.
7. Bevan, S. and J.H. Steinbach (1977) The distribution of α-bungarotoxin binding sites on mammalian skeletal muscle developing in vivo. J. Physiol. (Lond.) 267:195-213.
8. A-receptors at GABAergic synaptic contacts demonstrated by triple immunofluorescence staining. Brain Res. 642:59-69.
9. Bourgeois, J.P., P.S. Goldman-Rakic, and P. Rakic (1994) Synaptogenesis in the prefrontal cortex of Rhesus monkeys. Cereb. Cortex 4:78-96.
10. Bruning, G., R. Bauer, and H.G. Baumgarten (1990) Postnatal development of [3H]flunitrazepam and [3H]strychnine binding sites in rat spinal cord localized by quantitative autoradiography. Neurosci. Lett. 110:6-10.
11. Cabot, J.B., A. Brushnell, V. Alesi, and N.R. Mendell (1995) Postsynaptic gephyrin immunoreactivity exhibits a nearly one-to-one correspondence with γ-aminobutyric acid-like immunogold-labeled synaptic inputs to sympathetic preganglionic neurons. J. Comp. Neurol. 256:418-432.
12. Cartaud, J. and J.-P. Changeux (1993) Post-transcriptional compartmentalization of acetylcholine receptor biosynthesis in the subneural domain of muscle and electrocyte junctions. Eur. J. Neurosci. 5:191-202.
13. Changeux, J.-P., P. Courrège, and A. Danchin (1973) A theory of the epigenesis of neuronal networks by selective stabilization of synapses. Proc. Natl. Acad. Sci. USA 70:2974-2978.
14. Changeux, J.P. and A. Danchin (1976) Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks. Nature 264:705-712.
15. Colin, I., P. Rostaing, and A. Triller (1996) Gephyrin accumulates at specific plasmalemma loci during neuronal maturation in vitro. J. Comp. Neurol. 374:467-479.
16. Conradi, S. and L.-O. Ronevi (1975) Spontaneous elimination of synapses on cat spinal motoneurons after birth: Do half of the synapses on the cell bodies disappear? Brain Res. 92:505-510.
17. Craig, A.M., G. Banker, W. Chang, M.E. McGrath, and A.S. Serpinskaia (1996) Clustering of gephyrin and GABAergic but not glutamatergic synapses in cultured rat hippocampal neurons. J. Neurosci. 16:3166-3177.
18. Craig, A.M., C.D. Blackstone, R.L. Huganir, and G. Banker (1994) Selective clustering of glutamate and γ-aminobutyric acid receptors opposite terminals releasing the corresponding neurotransmitters. Proc. Natl. Acad. Sci. USA 91:12373-12377.
19. A-receptor α-subunit is an essential prerequisite for receptor formation in vivo. Neuroscience 81:1043-1053.
20. A-receptors subtypes during postnatal development: An immunocytochemical study. J. Neurosci. 14:5302-5324.
21. Froehner, S.C. (1993) Regulation of ion channel distribution at synapses. Annu. Rev. Neurosci. 16:347-368.
22. Holstein, G., T. Pasik, P. Pasik, and J. Hamori (1985) Early postnatal development of the monkey visual system: II. Elimination of retinogeniculate synapses. Dev. Brain. Res. 20:15-31.
23. Jakowec, M.W., A.J. Fox, L.J. Martin, K.R. G (1995) Quantitative and qualitative changes in AMPA receptor expression during spinal cord development. Neuroscience 64:893-907.
24. Kalb, R.G., M.S. Lidow, M.J. Halsted and S. Hockfield (1992) N-methyl-D-aspartate receptors are transiently expressed in the developing spinal ventral horn. Proc. Natl. Acad. Sci. USA89:8502-8506.
25. Kirsch, J. and H. Betz (1993) Widespread expression of gephyrin, a putative receptor-tubulin linker protein, in rat brain. Brain Res. 621:301-310.
26. Kirsch, J. and H. Betz (1995) The postsynaptic localization of the glycine receptor-associated protein gephyrin is regulated by the cytoskeleton. J. Neurosci. 15:4148-4156.
27. Kirsch, J., F. Kuhse and H. Betz (1995) Targeting of glycine receptor subunit to getzrin-ride domains in transfected human autophic Iniderney cells. Molec. and Cell. Neurose. 6:450-461.
28. Kirsch, J., D. Langosch, P. Prior, U.Z. Littauer, and H. Betz (1991) The 93-kDa glycine receptor-associated protein binds to tubulin. J. Biol. Chem. 266:22242-22245.
29. Kirsch, J., M.-L. Malosio, I. Wolters, and H. Betz (1993a) Distribution of gephyrin transcripts in the adult and developing rat brain. Eur. J. Neurosci. 5:1109-1117.
30. Kirsch, J., I. Wolters, A. Triller, and H. Betz (1993b) Gephyrin antisense oligonucleotides prevent glycine receptor clustering in spinal cord. Nature 366:745-748.
31. Kolston, J., K.K. Osen, C.M. Hackney, O.P. Ottersen, and J. Storm-Mathisen (1992) An atlas of glycine- and GABA-like immunoreactivity and colocalization in the cochlear nuclear complex of the guinea pig. Anat. Embryol. 186:443-465.
32. Langosch, D., L. Thomas, and H. Betz (1988) Conserved quaternary structure of ligand-gated ion channels: The postsynaptic glycine receptor is a pentamer. Proc. Natl. Acad. Sci. USA 85:7394-7398.
33. Lohof, A.M., N. Delhaye-Bouchaud, and J. Mariani (1996) Synapse elimination in the central nervous system: Functional significance and cellular mechanisms. Rev. Neurosci. 7:85-101.
34. Ma, W., T. Behar, and J.L. Barker (1992) Transient expression of GABA immunoreactivity in the developing rat spinal cord. J. Comp. Neurol. 325:271-290.
35. Malosio, M.L., B. Marquèze-Pouey, J. Kuhse, and H. Betz (1991) Widespread expression of glycine receptor subunit mRNAs in the adult and developing rat brain. EMBO J. 10:2401-2409.
36. Mandler, R.N., A.E. Schaffner, E.A. Novotny, G.D. Lange, S.V. Smith, and J.L. Barker (1990) Electrical and chemical excitability appear one week before birth in the embryonic rat spinal cord. Brain Res. 522:46-54.
37. May, M.K. and T.J. Biscoe (1975) An investigation of the foetal rat spinal cord. II. An ultrastructural study on the development of synapses with the aid of observations on some electrophysiological properties. Cell Tissue Res. 158:251-268.
38. Meyer, G., J. Kirsch, H. Betz, and D. Langosh (1995) Identification of a gephyrin binding motif on the glycine receptor § subunit. Neuron 15:563-572.
39. Mitchell, K., R.C. Spike, and A.J. Todd (1993) An immunocytochemical study of glycine receptor and GABA in lamina I-III of rat spinal dorsal horn. J. Neurosci. 13:2371-2381.
40. Nicola, M.A., C.M. Becker, and A. Triller (1992) Development of glycine receptor α subunit in cultivated rat spinal neurons: An immunocytochemical study. Neurosci. Lett. 138:173-178.
41. Noakes, P.G., W.D. Phillips, T.A. Hanley, J.R. Sanas, and J.P. Merlie (1993) 43K protein and acetylcholine receptors colocalize during the initial stages of neuromuscular synapse formation in vivo. Dev. Biol. 155:275-280.
42. A receptor to specific GABAergic synapses in the Dentate Gyrus. Eur. J. Neurosci. 7:630-646.
43. A receptors on cerebellar granule cells as determined by a quantitative immunogold method. J. Neurosci. 15:2948-2960.
44. Pfeiffer, F., D. Graham, and H. Betz (1982) Purification by affinity chromatography of the glycine receptor of rat spinal cord. J. Biol. Chem. 257:9389-9393.
45. Pfeiffer, F., R. Simler, G. Grenningloh, and H. Betz (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.
46. Prior, P., B. Schmitt, G. Grenningloh, I. Pribilla, G. Multaup, K. Beyreuther, Y. Maulet, P. Werner, D. Langosch, J. Kirsch, and H. Betz (1992) Primary structure and alternative splice variants of gephyrin, a putative glycine receptor-tubulin linker protein. Neuron 8:1161-1170.
47. Reynolds, E.S. (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol. 17:208-212.
48. Sassoè-Pognetto, M., J. Kirsch, U. Grünert, U. Greferath, J.M. Fritschy, H. Möhler, H. Betz, and H. W ssle (1995) Colocalization of gephyrin and GABAA-receptor subunits in the rat retina. J. Comp. Neurol. 357:1-14.
49. Schaffner, A.E., T. Behar, S. Nadi, and J.L. Barker (1993) Quantitative analysis of transient GABA expression in embryonic and early postnatal rat spinal cord neurons. Dev. Brain. Res. 72:265-276.
50. Schröder, S., W. Hoch, C.-M. Becker, G. Grenningloh, and H. Betz (1991) Mapping of antigenic epitopes on the α1 subunit of the inhibitory glycine receptor. Biochemistry 30:42-47.
51. Seguela, P., M. Geffard, R.M. Buijs, and M. Le Moal (1984) Antibodies against γ-aminobutyric acid: Specificity studies and immunocytochemical results. Proc. Natl. Acad. Sci. USA 81:3888-3892.
52. Seitanidou, T., M.-A. Nicola, A. Triller, and H. Korn (1992) Partial glycinergic denervation induces changes in the distribution of a glycine receptor-associated protein in a central neuron. J. Neurosci. 12:116-131.
53. Shupliakov, O., G. Ornung, L. Brodin, B. Ulfhake, O.P. Ottersen, J. Storm-Mathisen, and S. Cullheim (1993) Immunocytochemical localization of amino acid neurotransmitter candidates in the ventral horn of the cat spinal cord: A light microscopic study. Exp. Brain Res. 96:404-418.
54. Srinivasan, Y., A.P. Guzikowski, R.P. Haugland, and K.J. Angelides (1990) Distribution and lateral mobility of glycine receptors on cultured spinal cord neurons. J. Neurosci. 10:985-995.
55. Storm-Mathisen, J. and O.P. Ottersen (1990) Antibodies and fixatives for the immunocytochemical localization of glycine. In O.P. Ottersen and J. Storm-Mathisen (eds): Glycine Neurotransmission. New York: John Wiley & Sons, pp. 281-302.
56. Takahashi, T. and A. Momiyama (1991) Single-channel currents underlying glycinergic inhibitory postsynaptic responses in spinal cord. Neuron 7:965-969.
57. Takahashi, T., A. Nokiyaona, K. Hirai, F. Hishinuma, and H. Agara (1992) Functional correlation of fetal and adult forms of glycine receptor with developmental changes in inhibitory receptor channels. Neuron 9:1155-1161.
58. Todd, A.J., R.C. Spike, D. Chong, and M. Neilson (1995) The relationship between glycine and gephyrin in synapses of the rat spinal cord. Eur. J. Neurosci. 7:1-11.
59. Todd, A.J., C. Watt, R.C. Spike, and W. Sieghart (1996) Colocalization of GABA, glycine, and their receptors at synapses in the rat spinal cord. J. Neurosci. 16:974-982.
60. Triller, A., F. Cluzeaud, and H. Korn (1987) γ-Aminobutyric acid-containing terminals can be apposed to glycine receptors at central synapses. J. Cell Biol. 104:947-956.
61. Triller, A., F. Cluzeaud, F. Pfeiffer, H. Betz, and H. Korn (1985) Distribution of glycine receptors at central synapses: An immunoelectron microscopy study. J. Cell Biol. 101:683-688.
62. Triller, A., C. Sur, and H. Korn (1993a) Heterogeneous distribution of glycinergic and GABAergic afferents on an identified central neuron. J. Comp. Neurol. 338:83-96.
63. Triller, A., C. Sur, J. Storm-Mathissen, O.P. Ottersen, and H. Korn (1993b) Glycine and GABA coexist in the same presynaptic boutons of rat spinal cord. 16th European Neurological Association Meeting, Madrid.