GABA and GABAA receptors at hippocampal mossy fibre synapses

European Journal of Neuroscience

Volumn 18, Issue 4, 2003, Pages 931-941

  Bergersen, Linda ^a   Ruiz, Arnaud ^b,c   Bjaalie, Jan G ^a   Kullmann, Dimitri M ^b   Gundersen, Vidar ^a,d  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c University of Bordeaux   (France)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Exocytosis; GABA; Glutamate; Immunocytochemistry; Rat; Receptors

Indexed keywords

2 (2,3 DICARBOXYCYCLOPROPYL)GLYCINE; 2 AMINO 5 PHOSPHONOVALERIC ACID; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; AMPA RECEPTOR; AMPA RECEPTOR ANTAGONIST; GLUTAMATE RECEPTOR AGONIST; GLUTAMATE RECEPTOR ANTAGONIST; GLUTAMIC ACID; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; PICROTOXIN; POSTSYNAPTIC RECEPTOR; PRESYNAPTIC RECEPTOR;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; FACILITATION; FREQUENCY MODULATION; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IMMUNOGOLD STAINING; MALE; NERVE ENDING; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RECEPTOR SENSITIVITY; SIGNAL TRANSDUCTION; SYNAPSE VESICLE; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; ANIMAL; EXCITATORY POSTSYNAPTIC POTENTIAL; IMMUNOHISTOCHEMISTRY; METABOLISM; ORGAN CULTURE TECHNIQUE; PATCH CLAMP; PHYSIOLOGY; ULTRASTRUCTURE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIALS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, ELECTRON; MOSSY FIBERS, HIPPOCAMPAL; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; RATS; RECEPTORS, AMPA; RECEPTORS, GABA-A; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 0042819698     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02828.x     Document Type: Article

References (50)

1. Acsády, L., Kamondi, A., Sik, A., Freund, T. & Buzsaki, G. (1998) GABAergic cells are the major postsynaptic targets of mossy fibres in the rat hippocampus. J. Neurosci., 18, 3386-3403.
2. Amaral, D.G. (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat. J. Comp. Neurol., 182, 851-914.
3. Ben-Ari, Y., Rovira, C. Gaiarsa, J.L., Corradetti, R., Robain, O. & Cherubini, E. (1990) GABAergic mechanisms in the CA3 hippocampal region during early postnatal life. Prog. Brain. Res., 83, 313-321.
4. Bergersen, L., Waerhaug, O., Helm, J., Thomas, M., Laake, P., Davies, A.J., Wilson, M.C. Halestrap, A.P. & Ottersen, O.P. (2001) A novel postsynaptic density protein: the monocarboxylate transporter MCT2 is co-localized with delta-glutamate receptors in postsynaptic densities of parallel fibre-Purkinje cell synapses. Exp. Brain Res., 136, 523-534.
5. Bramham, C.R., Torp, R., Zhang, N., Storm-Mathisen, J. & Ottersen, O.P. (1990) Distribution of glutamate-like immunoreactivity in excitatory hippocampal pathways: a semiquantitative electron microscopic study in rats. Neuroscience, 39, 405-417.
6. Broman, J., Anderson, S. & Ottersen, O.P. (1993) Enrichment of glutamate-like immunoreactivity in primary afferent terminals throughout the spinal cord dorsal horn. Eur. J. Neurosci., 5, 1050-1061.
7. Buckmaster, P.S., Wenzel, H.J., Kunkel, D.D. & Schwartzkroin, P.A. (1996) Axon arbors and synaptic connections of hippocampal mossy cells in the rat in vivo. J. Comp. Neurol., 366, 271-292.
8. Chaudhry, F.A., Lehre, K.P., Van Lookeren Campagne, M., Ottersen, O.P., Danbolt, N.C. & Storm-Mathisen, J. (1995) Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron, 14, 711-720.
9. Chaudhry, F.A., Reimer, R.J., Bellocchio, E.E., Danbolt, N.C., Osen, K.K., Edwards, R.H. & Storm-Mathisen, J. (1998) The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycingergic as well as GABAergic neurons. J. Neurosci., 18, 9733-9750.
10. Cotman, C.W. & Storm-Mathisen, J. (1986) Excitatory amino acids and receptor interactions. Adv. Exp. Med. Biol., 203, 317-318.
11. Ewert, M., Shivers, B.D., Luddens, H., Mohler, H. & Seeburg, P.H. (1990) Subunit selectivity and epitope characterization of mAbs directed against the GABAA/benzodiazepine receptor. J. Cell Biol., 110, 2043-2048.
12. Fremeau, R.T. Jr, Troyer, M.D., Pahner, I., Nygaard, G.O., Tran, C.H., Reimer, R.J., Bellocchio, E.E., Fortin, D., Storm-Mathisen, J. & Edwards, R.H. (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron, 31, 247-260.
13. Fujiyama, F., Fritschy, J.M., Stephenson, F.A. & Bolam, J.P. (2000) Synaptic localization of GABA(A) receptor subunits in the striatum of the rat. J. Comp. Neurol., 416, 158-172.
14. Gundersen, H.J., Bendtsen, T.F., Korbo, L., Marcussen, N., Moller, A., Nielsen, K., Nyengaard, J.R., Pakkenberg, B. Sorensen F.B. & Vesterby, A. (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS, 96, 379-394.
15. Gundersen, V., Chaudhry, F.A., Bjaalie, J.G., Fonnum, F., Ottersen, O.P. & Storm-Mathisen, J. (1998) Synaptic vesicular localization and exocytosis of 1-aspartate in excitatory nerve terminals: a quantitative immunogold analysis in rat hippocampus. J. Neurosci., 18, 6059-6070.
16. Gundersen, V., Fonnum, F., Ottersen, O.P. & Storm-Mathisen, J. (2001) Redistribution of neuroactive amino acids in hippocampus and striatum during hypoglycemia: a quantitative immunogold study. J. Cereb. Blood Flow Metab., 21, 41-51.
17. Gutierrez, R. (2000) Seizures induce simultaneous GABAergic and glutamatergic transmission in the dentate gyrus-CA3 system. J. Neurophysiol., 84, 3088-3090.
18. Gutierrez, R. (2002) Activity-dependent expression of simultaneous glutamatergic and GABAergic neurotransmission from the mossy fibres in vitro. J. Neurophysiol., 87, 2562-2570.
19. Gutierrez, R. & Heinemann, U. (2001) Kindling induces transient fast inhibition in the dentate gyrus - CA3 projection. Eur. J. Neurosci., 13, 1371-1379.
20. Haring, P., Stahli, C., Schoch, P., Takacs, B., Staehelin, T. & Mohler, H. (1985) Monoclonal antibodies reveal structural homogeneity of gamma-aminobutyric acid/benzodiazepine receptors in different brain areas. Proc. Natl Acad. Sci. U.S.A., 82, 4837-4841.
21. Henze, D.A., Urban, N.N. & Barrionuevo, G. (2000) The multifarious hippocampal mossy fiber pathway: a review. Neuroscience, 98, 407-427.
22. Jackson, M.B. & Scharfman, H.E. (1996) Positive feedback from hilar mossy cells to granule cells in the dentate gyrus revealed by voltage-sensitive dye and microelectrode recording. J. Neurophysiol., 76, 601-616.
23. Ji, Z., Aas, J.E., Laake, J., Walberg, F. & Ottersen, O.P. (1991) An electron microscopic, immunogold analysis of glutamate and glutamine in terminals of rat spinocerebellar fibres. J. Comp. Neurol., 307, 296-310.
24. Jonas, P., Bischofberger, J. & Sandkuhler, J. (1998) Corelease of two fast neurotransmitters at a central synapse. Science, 281, 419-424.
25. von Kitzing, E., Jonas, P. & Sakmann, B. (1994) Quantal analysis of excitatory postsynaptic currents at the hippocampal mossy fibre-CA3 pyramidal cell synapse. Adv. Sec. Mess. Phosphoprot. Res., 29, 235-260.
26. Laake, J.H., Gundersen, V., Nordbø, G., Ottersen, O.P. & Storm-Mathisen, J. (1986) An antiserum against glutamine. In Roberts, P.J., Storm-Mathisen, J. & Bradford, H.F. (Eds), Excitatory Amino Acids. Macmillan, London, pp. 448-450.
27. Lamas, M., Gomez-Lira, G. & Gutierrez, R. (2001) Vesicular GABA transporter mRNA expression in the dentate gyrus and in mossy fibre synaptosomes. Brain Res. Mol. Brain Res., 93, 209-214.
28. Leergaard, T.B. & Bjaalie, J.G. (1995) Semi-automatic data acquisition for quantitative neuroanatomy. MicroTrace - computer programme for recording of the spatial distribution of neuronal populations. Neurosci. Res., 22, 231-243.
29. Min, M.Y., Rusakov, D.A. & Kullmann, D.M. (1998) Activation of AMPA, kainate, and metabotropic receptors at hippocampal mossy fibre synapses: role of glutamate diffusion. Neuron, 21, 561-570.
30. Murakawa, R. & Kosaka, T. (2001) Structural features of mossy cells in the hamster dentate gyrus, with special reference to somatic thorny excrescences. J. Comp. Neurol., 429, 113-126.
31. Nagelhus, E.A., Veruki, M.L., Torp, R., Haug, F.M., Laake, J.H., Nielsen, S., Agre, P. & Ottersen, O.P. (1998) Aquaporin-4 water channel protein in the rat retina and optic nerve: polarized expression in Muller cells and fibrous astrocytes. J. Neurosci., 18, 2506-2519.
32. Nusser, Z., Sieghart, W. & Somogyi, P. (1998) Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J. Neurosci., 18, 1693-1703.
33. Ottersen, O.P. (1987) Postembedding light- and electron microscopic immunocytochemistry of amino acids: description of a new model system allowing identical conditions for specificity testing and tissue processing. Exp. Brain Res., 69, 167-174.
34. Ottersen, O.P. (1988) Quantitative assessment of taurine-like immunoreactivity in different cell types and processes in rat cerebellum: an electronmicroscopic study based on a postembedding immunogold labelling procedure. Anat. Embryol. (Berl.), 178, 407-421.
35. Ottersen, O.P. (1989) Quantitative electron microscopic immunocytochemistry of amino acids. Anat. Embryol. (Berl.), 180, 1-15.
36. Park, J., Osei, Y.D. & Churchich, J.E. (1993) Isolation and characterization of recombinant mitochondrial 4-aminobutyrate aminotransferase. J. Biol. Chem., 15 (268), 7636-7639.
37. Petralia, R.S. & Wenthold, R.J. (1992) Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J. Comp. Neurol., 318, 329-354.
38. Reijnierse, G.L., Veldstra, H. & Van den Berg, C.J. (1975) Subcellular localization of gamma-aminobutyrate transaminase and glutamate dehydrogenase in adult rat brain. Evidence for at least two small glutamate compartments in brain. Biochem. J., 152, 469-475.
39. Romo-Parra, H., Vivar, C., Maqueda, J., Morales, M.A. & Gutierrez, R. (2003) Activity-dependent induction of multitransmitter signaling onto pyramidal cells and interneurons of hippocampal area CA3. Neurophysiology, 89, 3155-3167.
40. Sandler, R. & Smith, A.D. (1991) Coexistence of GABA and glutamate in mossy fibre terminals of the primate hippocampus: an ultrastructural study. J. Comp. Neurol., 303, 177-192.
41. Shigemoto, R., Kinoshita, A., Wada, E., Nomura, S., Ohishi, H., Takada, M., Flor, P.J., Neki, A., Abe, T., Nakanishi, S. et al. (1997) Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J. Neurosci., 17, 7503-7522.
42. Sloviter, R.S., Dichter, M.A., Rachinsky, T., Dean, E., Goodman, J.H., Sollas, A.L. & Martin, D.L. (1996) Basal expression and induction of glutamate decarboxylase and GABA in excitatory granule cells of the rat and monkey hippocampal dentate gyrus. J. Comp. Neurol., 373, 593-618.
43. Somogyi, P., Fritschy, J.M., Benke, D., Roberts, J.D. & Sieghart, W. (1996) The gamma 2 subunit of the GABAA receptor is concentrated in synaptic junctions containing the alpha 1 and beta 2/3 subunits in hippocampus, cerebellum and globus pallidus. Neuropharmacology, 35, 1425-1444.
44. Storm-Mathisen, J., Leknes, A.K., Bore, A., Vaaland, J.L., Edminson, P., Haug, F.M.S. & Ottersen, O.P. (1983) First visualization of glutamate and GABA in neurones by immunocytochemistry. Nature, 301, 517-520.
45. Storm-Mathisen, J. & Ottersen, O.P. (1990) Immunocytochemistry of glutamate at the synaptic level. J. Histochem. Cytochem., 38, 1733-1743.
46. Takumi, Y., Ramirez-Leon, V., Laake, P., Rinvik, E. & Ottersen, O.P. (1999) Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nature Neurosci., 2, 618-624.
47. Valtschanoff, J.G. & Weinberg, R.J. (2001) Laminar organization of the NMDA receptor complex within the postsynaptic density. J. Neurosci., 21, 1211-1217.
48. Walker, M.C., Ruiz, A. & Kullmann, D.M. (2001) Monosynaptic GABAergic signaling from dentate to CA3 with a pharmacological and physiological profile typical of mossy fibre synapses. Neuron, 29, 703-715.
49. Walker, M.C., Ruiz, A. & Kullmann, D.M. (2002) Do mossy fibres release GABA? Epilepsia, 43, 196-202.
50. Wang, B.L. & Larsson, L.I. (1985) Simultaneous demonstration of multiple antigens by indirect immunofluorescence or immunogold staining. Novel light and electron microscopical double and triple staining method employing primary antibodies from the same species. Histochemistry, 83, 47-56.