Localization of the clustering protein gephyrin at GABAergic synapses in the main olfactory bulb of the rat

Journal of Comparative Neurology

Volumn 395, Issue 2, 1998, Pages 231-244

  Giustetto, Maurizio ^a   Kirsch, Joachim ^b   Fritschy, Jean Marc ^c   Cantino, Dario ^a   Sassoè Pognetto, Marco ^a,d  

^a UNIVERSITY OF TURIN   (Italy)

^b MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d Dipto Anat Farmacol Med L   (Italy)

Author keywords

Electron microscopy; GABA(A) receptor; Glycine receptor; Immunocytochemistry; Receptor clustering

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; BINDING PROTEIN; GEPHYRIN; GLYCINE RECEPTOR; RECEPTOR SUBTYPE; RECEPTOR SUBUNIT; TUBULIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; FEMALE; GABAERGIC SYSTEM; MALE; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SPINAL CORD NERVE CELL; SYNAPSE; SYNAPTIC MEMBRANE;

ANIMALS; ANTIBODIES, MONOCLONAL; CARRIER PROTEINS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE PROTEINS; OLFACTORY BULB; RATS; RATS, WISTAR; RECEPTORS, GABA-A; SYNAPSES; TISSUE EMBEDDING;

EID: 0032103933     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980601)395:2<231::AID-CNE7>3.0.CO;2-3     Document Type: Article

References (84)

1. Altschuler, R.A., H. Betz, M.H. Parakkal, K.A. Reeks, and R.J. Wenthold (1986) Identification of glycinergic synapses in the cochlear nucleus through immunocytochemical localization of the postsynaptic receptor. Brain Res. 369:316-320.
2. Alvarez, F.J., D.E. Dewey, D.H. Harrington, and R.E.W. Fyffe (1997) Cell-type specific organization of glycine receptor clusters in the mammalian spinal cord. J. Comp. Neurol. 379:150-170.
3. Basbaum, A. (1988) Distribution of the glycine receptor immunoreactivity in the spinal cord of the rat: Cytochemical evidence for a differential glycinergic control of lamina I and V nociceptive neurons. J. Comp. Neurol. 278:330-336.
4. A-receptor in the rat brain. J. Receptor Res. 11:407-424.
5. Berkowicz, D.A., P.Q. Trombley, and G.M. Shepherd (1994) Evidence for glutamate as the olfactory receptor cell neurotransmitter. J. Neurophysiol. 71:2557-2561.
6. A receptors at GABAergic synaptic contacts demonstrated by triple immunofluorescence staining. Brain Res. 642:59-69.
7. Bormann, J., N. Rundström, H. Betz, and D. Langosch (1993) Residues within transmembrane segment M2 determine chloride conductance of glycine receptor homo- and hetero-oligomers. EMBO J. 12:3729-3337.
8. Cabot, J.B., A. Bushnell, V. Alessi, and N.R. Mendell (1995) Postsynaptic gephyrin immunoreactivity exhibits a nearly one-to-one correspondence with gamma-aminobutyric acid-like immunogold-labeled synaptic inputs to sympathetic preganglionic neurons. J. Comp. Neurol. 356:418-432.
9. Chen, S. and D.E. Hillman (1993) Colocalization of neurotransmitters in the deep cerebellar nuclei. J. Neurocytol. 22:81-91.
10. Craig, A.M., G. Banker, W.R. Chang, M.E. Mcgrath, and A.S. Serpinskaya (1996) Clustering of gephyrin at GABAergic but not glutamatergic synapses in cultured rat hippocampal neurons. J. Neurosci. 16:3166-3177.
11. Ennis, M., L.A. Zimmer, and M.T. Shipley (1996) Olfactory nerve stimulation activates rat mitral cells via NMDA and non-NMDA receptors in vitro. NeuroReport 7:989-992.
12. Felix, D. and H. McLennan (1971) The effect of bicuculline on the inhibition of the mitral cells of the olfactory bulb. Brain Res. 25:661-664.
13. A-receptor heterogeneity in the adult rat brain: Differential regional and cellular distribution of seven major subunits. J. Comp. Neurol. 359:154-194.
14. Gall, C.M., S.H.C. Hendry, K.B. Seroogy, E.G. Jones, and J.W. Haycock (1987) Evidence for coexistence of GABA and dopamine in neurons of the rat olfactory bulb. J. Comp. Neurol. 266:307-318.
15. Giustetto, M., P. Bovolin, A. Fasolo, M. Bonino, D. Cantino, and M. Sassoè-Pognetto (1997) Glutamate receptors in the olfactory bulb synaptic circuitry: Heterogeneity and synaptic localization of the NR1 and GluR1 subunits. Neuroscience 76:787-798.
16. Godfrey, D.A., C.D. Ross, J.A. Carter, O.H. Lowry, and F.M. Matschinsky (1980) Effect of intervening lesions on amino acid distributions in rat olfactory cortex and olfactory bulb. J. Histochem. Cytochem. 28:1157-1169.
17. Graham, D., F. Pfeiffer, R. Simler, and H. Betz (1985) Purification and characterization of the glycine receptor of pig spinal cord. Biochemistry 24:990-994.
18. Grünert, U. and H. Wässle (1993) Immunocytochemical localization of glycine receptors in the mammalian retina. J. Comp. Neurol. 335:523-537.
19. Halasz, N., Å. Ljungdahl, and T. Hökfelt (1978) Transmitter histochemistry in the rat olfactory bulb-II. Fluorescence histochemical, autoradiographic and electron microscopic localization of monoamines. Brain Res. 154:253-271.
20. Hsu, S.M., L. Raine, and H. Fanyer (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques. J. Histochem. Cytochem. 29:577-580.
21. Jacobson, I. and A. Hamberger (1986) Effects of kynurenic acid on evoked extracellular field potentials in the rat olfactory bulb in vivo. Brain Res. 386:389-392.
22. Jacobson, I., S. Butcher, and A. Hamberger (1986) An analysis of the effects of the excitatory amino acid receptor antagonists on evoked field potentials in the olfactory bulb. Neuroscience 19:267-273.
23. Jacobson, I., A. Hamberger, and C.D. Richards (1990) Ketamine and MK801 attenuate paired pulse inhibition in the olfactory bulb of the rat. Exp. Brain Res. 80:409-414.
24. Jahr, C.E. and R.A. Nicoll (1982) An intracellular analysis of dendrodendritic inhibition in the turtle in vitro olfactory bulb. J. Physiol. Lond. 326:213-234.
25. Kirsch, J. and H. Betz (1993) Widespread expression of gephyrin, a putative glycine 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 cytosckeleton. J. Neurosci. 15:4148-4156.
27. Kirsch, J., D. Langosch, P. Prior, U.Z. Littauer, B. Schmitt, and H. Betz (1991) The 93-kDa glycine receptor-associated protein binds to tubulin. J. Biol. Chem. 266:22242-22245.
28. 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.
29. Kirsch, J., I. Wolters, A. Triller, and H. Betz (1993b) Gephyrin antisense oligonucleotides prevent glycine receptor clustering in spinal neurons. Nature 366:745-748.
30. Kirsch, J., J. Kuhse, and H. Betz (1995) Targeting of glycine receptor subunits to gephyrin-rich domains in transfected human embryonic kidney cells. Mol. Cell. Neurosci. 6:450-461.
31. Kirsch, J., G. Meyer, and H. Betz (1996) Synaptic targeting of ionotropic neurotransmitter receptors. Mol. Cell. Neurosci. 8:93-98.
32. Kosaka, T., K. Kosaka, C.W. Heizmann, I. Nagatsu, J. Wu, N. Yanaihara, and K. Hama (1987) An aspect of the organization of the GABAergic system in the rat main olfactory bulb: Laminar distribution of immunohistochemically defined subpopulations of GABAergic neurons. Brain Res. 411:373-378.
33. A and glycine receptors in the mammalian retina. J. Neurosci. 16:2127-2140.
34. Kuhse, J., H. Betz, and J. Kirsch (1995) The inhibitory glycine receptor: Architecture, synaptic localization and molecular pathology of a postsynaptic ion-channel complex. Curr. Opin. Neurobiol. 5:318-323.
35. Langosch, D., C.-M. Becker, and H. Betz (1990) The inhibitory glycine receptor: A ligand-gated chloride channel of the central nervous system. Eur. J. Biochem. 194:1-8.
36. A receptor subunit mRNAs in the rat brain. II. Olfactory bulb and cerebellum. J. Neurosci. 12:1063-1076.
37. 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.
38. Meyer, G., J. Kirsch, H. Betz, and D. Langosch (1995) Identification of a gephyrin binding motif on the glycine receptor β 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 laminae I-III of rat spinal dorsal horn. J. Neurosci. 13:2371-2381.
40. Mori, K., M.C. Nowycky, and G.M. Shepherd (1981) Analysis of a long duration inhibitory potential in mitral cells in the isolated turtle olfactory bulb. J. Physiol. Lond. 314:311-320.
41. Mugnaini, E., W.H. Oertel, and F.F. Wouterlood (1984) Immunocytochemical localization of GABA neurons and dopamine neurons in the rat main and accessory olfactory bulb. Neurosci. Lett. 47:221-226.
42. Nicola, M.-A., C.-M. Becker, and A. Triller (1992) Development of glycine receptor alpha subunit in cultivated rat spinal neurons: An immunocytochemical study. Neurosci. Lett. 138:173-178.
43. Nicoll, R.A. (1971) Pharmacological evidence for GABA as the transmitter in granule cell inhibition in the olfactory bulb. Brain Res. 35:137-149.
44. Nowycky, M.C., K. Mori, and M.G. Shepherd (1981) GABAergic mechanisms of dendrodendritic synapses in isolated turtle olfactory bulb. J. Neurophysiol. 46:639-648.
45. A receptors on cerebellar granule cells as determined by a quantitative immunogold method. J. Neurosci. 15:2948-2960.
46. Nusser, Z., W. Sieghart, D. Benke, J.-M. Fritschy, and P. Somogyi (1996a) Differential synaptic localization of two major γ-aminobutyric acid type A receptor α subunits on hippocampal pyramidal cells. Proc. Natl. Acad. Sci. USA 93:11939-11944.
47. A receptor is concentrated in both inhibitory and excitatory synapses on cerebellar granule cells. J. Neurosci. 16:103-114.
48. Osborne, R.H., I.R. Duce, and P. Keen (1976) Amino acids in "light" and "heavy" synaptosome fractions from rat olfactory lobes and their release by electrical stimulation. J. Neurochem. 27:1483-1488.
49. A receptor subunits in the rat CNS. J. Comp. Neurol. 326:193-216.
50. Pfeiffer, F., D. Graham, and H. Betz (1982) Purification by affinity chromatography of the glycine receptor of the rat spinal cord. J. Biol. Chem. 257:9389-9393.
51. 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.
52. Phend, K.D., R.J. Weinberg, and A. Rustioni (1992) Techniques to optimize post-embedding single and double staining for amino acid neurotransmitters. J. Histochem. Cytochem. 40:1011-1020.
53. Pinching, A.J. and T.P.S. Powell (1971) The neuropil of the glomeruli of the olfactory bulb. J. Cell Sci. 9:305-345.
54. Pourcho, R.G. and M.T. Owczarzak (1991) Glycine receptor immunoreactivity is localized at amacrine synapses in cat retina. Vis. Neurosci. 7:611-618.
55. Pribilla, I., T. Takagi, D. Langosh, J. Bormann, and H. Betz (1992) The atypical M2 segment of the beta subunit confers picrotoxinin resitance to inhibitory glycine receptor channels. Neuron 9:1155-1161.
56. Price, J.L. and T.P.S. Powell (1970a) The morphology of granule cells of the olfactory bulb. J. Cell Sci. 7:91-123.
57. Price, J. L. and T.P.S. Powell (1970b) The synaptology of the granule cells of the olfactory bulb. J. Cell Sci. 7:125-155.
58. Prior, P., B. Schmitt, G. Grenningloh, I. Pribilla, G. Malthaup, 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.
59. Probst, A., R. Cortes, and J.M. Palacios (1986) The distribution of glycine receptors in the human brain. A light microscopic autoradiographic study using [3H]strychnine. Neuroscience 17:11-35.
60. Ribak, C.E., J.E. Vaughn, K. Saito, R. Barber, and E. Roberts (1977) Glutamate decarboxylase localization in neurons in the olfactory bulb. Brain Res. 126:1-18.
61. Rundström, N., V. Schmieden, H. Betz, J. Bormann, and D. Langosch (1994) Cyanotriphenylborate: Subtype-specific blocker of glycine receptor chloride channels. Proc. Natl. Acad. Sci. USA 91:8950-8954.
62. Sassoè-Pognetto, M., D. Cantino, P. Panzanelli, L. Verdun di Cantogno, M. Giustetto, F.L. Margolis, S. De Biasi, and A. Fasolo (1993) Presynaptic co-localization of carnosine and glutamate in olfactory neurons. NeuroReport 5:7-10.
63. Sassoè-Pognetto, M., H. Wässle, and U. Grünert (1994) Glycinergic synapses in the rod pathway of the rat retina: Cone bipolar cells express the α1 subunit of the glycine receptor. J. Neurosci. 14:5131-5146.
64. A-receptor subunits in the rat retina. J. Comp. Neurol. 357:1-14.
65. A receptors, and the anchoring protein gephyrin. J. Comp. Neurol. 381:158-174.
66. Schmitt, B., P. Knaus, C.-M. Becker, and H. Betz (1987) The M 93,000 polypeptide of the postsynaptic glycine receptor complex is a peripheral membrane protein. Biochemistry 26:805-811.
67. Shepherd, G.M. and C.A. Greer (1998) Olfactory bulb. In G.M. Shepherd (ed): The synaptic organization of the brain. Fourth Edition. New York: Oxford UP, pp 159-203.
68. Shipley, M.T. and M. Ennis (1996) Functional organization of olfactory system. J. Neurobiol 30:123-176.
69. A-receptors subtypes. Trends Neurosci. 19:386.
70. Sigel, E., F.A. Stephenson, C. Mamalaki, and E.A. Barnard (1983) A gamma-aminobutyric acid/benzodiazepine receptor complex of bovine cerebral cortex. J. Biol. Chem. 258:6965-6971.
71. A receptors in the cerebellum of rat, cat, and monkey using monoclonal antibodies. J. Neurosci. 9:2197-2209.
72. A receptor but the α1 polypeptide is the principal site of the agonist benzodiazepine photoaffinity labeling reaction. J. Biol. Chem. 265:21160-21165.
73. 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.
74. 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.
75. 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.
76. Trombley, P.Q. and G.M. Shepherd (1992) Noradrenergic inhibition of synaptic transmission between mitral and granule cells in mammalian olfactory bulb cultures. J. Neurosci. 12:3985-3991.
77. Trombley, P.Q. and G.M. Shepherd (1993) Synaptic transmission and modulation in the olfactory bulb. Curr. Opin. Neurobiol. 3:540-547.
78. Trombley, P.Q. and G.M. Shepherd (1994) Glycine exerts potent inhibitory actions on mammalian olfactory bulb neurons. J. Neurophysiol. 71:761-767.
79. Trombley, P.Q. and G.M. Shepherd (1996) Differential modulation by zinc and copper of amino acid receptors from rat olfactory bulb neurons. J. Neurophysiol. 76:2536-2546.
80. Trombley, P.Q. and G.L. Westbrook (1990) Excitatory synaptic transmission in cultures of rat olfactory bulb. J. Neurophysiol. 64:598-606.
81. van den Pol, A.N. and T. Gorcs (1988) Glycine and glycine receptor immunoreactivity in brain and spinal cord. J. Neurosci. 8:472-492.
82. Wenthold, R.J., M.H. Parakkal, M.D. Oberdorfer, and R.A. Altschuler (1988) Glycine receptor immunoreactivity in the ventral cochlear nucleus of the guinea pig. J. Comp. Neurol. 276:423-435.
83. Yokoi, M., K. Mori, and S. Nakanishi S (1995) Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc. Natl. Acad. Sci. USA 92:3371-3375.
84. Zarbin, M.A., J.K. Wamsley, and M.J. Kuhar (1981) Glycine receptor: Light microscopic autoradiographic localization with [3H] strychnine. J. Neurosci. 1:532-547.