Synapse-specific localization of NMDA and GARA(A) receptor subunits revealed by antigen-retrieval immunohistochemistry

Journal of Comparative Neurology

Volumn 390, Issue 2, 1998, Pages 194-210

  Fritschy, Jean Marc ^a   Weinmann, Oliver ^a   Wenzel, Andreas ^a   Benke, Dietmar ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

aminobutyric acid; Glutamate; Ionotropic neurotransmitter receptor; Subunit specific antibody; Synapse

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ANTIGEN; CYTOSKELETON PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROFILAMENT PROTEIN; RECEPTOR SUBUNIT; SYNAPSE RECEPTOR;

ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN MAPPING; CORPUS STRIATUM; DENTATE GYRUS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MICROWAVE IRRADIATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

ANIMALS; ANTIGEN-ANTIBODY REACTIONS; FIXATIVES; IMMUNOHISTOCHEMISTRY; MALE; MICROWAVES; PEPTIDE FRAGMENTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 0031975271     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980112)390:2<194::AID-CNE3>3.0.CO;2-X     Document Type: Article

References (67)

1. Ainley, C.D., and J.W. Ironside (1994) Microwave technology in diagnostic neuropathology. J. Neurosci. Methods 55:183-190.
2. Baude, A., Z. Nusser, E. Molnar, R.A.J. McIlhinney, and P. Somogyi (1995) High-resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and non-synaptic sites in rat hippocampus. Neurosci. 69:1031-1055.
3. Benke, D., A. Wenzel, L. Scheurer, J.M. Fritschy, and H. Mohler (1995) Immunobiochemical characterization of the NMDA-receptor subunit NR1 in the developing and adult rat brain. J. Recept. Res. 15:393-411.
4. Blackstad, T.W. (1963) Ultrastructural studies on the hippocampal region. Prog. Brain Res. 3:122-148.
5. Boon, M.E., P.O. Gerrits, H.E. Moorlag, P. Nieuwenhuis, and L.P. Kok (1988) Formaldehyde fixation and microwave irradiation. Histochem. J. 20:313-322.
6. Bravo, H., and H.J. Karten (1992) Pyramidal neurons of the rat cerebral cortex, immunoreactive to nicotinic acetylcholine receptors, project mainly to subcortical targets. J. Comp. Neurol. 320:62-68.
7. Brose, N., G.P. Gasic, D.E. Vetter, J.M. Sullivan, and S.F. Heinemann (1993) Protein chemical characterization and immunocytochemical localization of the NMDA receptor subunit NMDA R1. J. Biol. Chem. 268:22663-22671.
8. Cattoretti, G., S. Pileri, C. Parravicini, M.H.G. Becker, S. Poggi, C. Bifulco, G. Key, L. D'Amato, E. Sabattini, E. Feudale, F. Reynolds, J. Gerdes, and F. Rilke (1993) Antigen unmasking on formalin-fixed, paraffin-embedded tissue sections. J. Pathol. 171:83-98.
9. Craig, A.M., C.D. Blackstone, R.L. Huganir, and G. Banker (1993) The distribution of glutamate receptors in cultured rat hippocampal neurons: Postsynaptic clustering of AMPA-selective subunits. Neuron 10:1055-1068.
10. 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.
11. Del Toro, E.D., J.M. Juiz, X. Peng, J. Lindstrom, and M. Criado (1994) Immunocytochemical localization of the α7 subunit of the nicotinic acetylcholine receptor in the rat central nervous system. J. Comp. Neurol. 349:325-342.
12. Eccles, J.C. (ed) (1964) The Physiology of Synapses. Berlin: Springer Verlag.
13. Evers, P., and H.B.M. Uylings (1994a) Effects of microwave pretreatment on immunocytochemical staining of vibratome sections and tissue blocks of human cerebral cortex stored in formaldehyde fixative for long periods. J. Neurosci. Methods 55:163-172.
14. Evers, P., and H.B.M. Uylings (1994b) Microwave-stimulated antigen retrieval is pH and temperature dependent. J. Histochem. Cytochem. 42:1555-1563.
15. Farb, C.R., C. Aoki, and J.E. Ledoux (1995) Differential localization of NMDA and AMPA receptor subunits in the lateral and basal nuclei of the amygdala: A light and electron microscopic study. J. Comp. Neurol. 362:86-108.
16. Flint, A.C., U.S. Maisch J.H. Weishaupt, A.R. Kriegstein, and H. Monyer (1997) NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J. Neurosci. 17:2469-2476.
17. A-receptor heterogeneity in the adult rat brain: Differential regional and cellular distribution of seven major subunits. J. Comp. Neurol. 359:154-194.
18. A-receptors containing the α1-subunit to neurochemically distinct subpopulations of hippocampal interneurons. Eur. J. Neurosci. 6:837-853.
19. A-receptor subtypes in cholinergic and parvalbumin-positive neurons of the rat and marmoset medial-septum-diagonal band complex. Neurosci. 65:101-117.
20. Gottmann K., A. Mehrle, G. Gisselmann, and H. Hatt (1997) Presynaptic control of subunit composition of NMDA receptors mediating synaptic plasticity. J. Nourosci. 17:2766-2774.
21. Gray, E.G. (1969) Electron microscopy of excitatory and inhibitory synapses: A brief review. Prog. Brain Res. 31:141-155.
22. A-receptor subunits have differential distributions in the rat retina: In situ hybridization and immunohistochemistry. J. Comp. Neurol. 353:553-571.
23. A receptor in the rat brain. J. Neurosci. 74:7168-7179.
24. Hartveit, E., J.H. Brandstätter, M. Sassoé-Pognetto, D.J. Laurie, P.H. Seeburg, and H. Wässle (1994) Localization and developmental expression of the NMDA receptor subunit NR2A in the mammalian retina. J. Comp. Neurol. 348:570-582.
25. Hazelbag, H.M., L.J.C.M. van den Broek, E.B.L. van Dorst, G.J.A. Offerhaus, G.J. Fleuren, and P.C.W. Hogendoorn (1995) Immunostaining of chain-specific keratins on formalin-fixed, paraffin-embedded tissues: A comparison of various antigen retrieval systems using microwave heating and proteolytic pre-treatments. J. Histochem. Cytochem. 43: 429-437.
26. A receptor subunit immunoreactivity in primate visual cortex: Distribution in macaques and humans and regulation by visual input in adulthood. J. Neurosci. 14:2383-2401.
27. Hof, P.R., P. Vissavajjhala, R.E. Rosenthal, G. Fiskum, and J.H. Morrison (1996) Distribution of glutamate receptor subunit proteins GluR2(4), GluR5/6/7, and NMDAR1 in the canine and primate cerebral cortex - A comparative immunohistochemical analysis. Brain Res. 723:77-89.
28. Hsu, S.M., L. Raine, and H. Fanger (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. J. Histochem. Cytochem. 29:577-580.
29. Huntley, G.W., J.C. Vickers, W. Janssen, N. Brose, S.F. Heinemann, and J.H. Morrison (1994) Distribution and synaptic localization of immunocytochemically identified NMDA receptor subunit proteins in sensory-motor and visual cortices of monkey and man. J. Neurosci. 14:3603-3619.
30. Ishii, T., K. Moriyoshi, H. Sugihara, K. Sakurada, H. Kadotani, M. Yokoi, C. Akazawa, R. Shigemoto, N. Mizuno, M. Masu, and S. Nakanishi (1993) Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J. Biol. Chem. 268:2836-2843.
31. Johnson, R.R., X.P. Jiang, and A. Burkhalter (1996) Regional and laminar differences in synaptic localization of NMDA receptor subunit NR1 splice variants in rat visual cortex and hippocampus. J. Comp. Neurol. 368:335-355.
32. Kharazia, V.N., K.D. Phend, A. Rustioni, and R.J. Weinberg (1996) EM colocalization of AMPA and NMDA receptor subunits at synapses in rat cerebral cortex. Neurosci. Lett. 210:37-40.
33. Kirson, E.D., and Y. Yaari (1996) Synaptic NMDA receptors in developing mouse hippocampal neurones - Functional properties and sensitivity to ifenprodil. J. Physiol. (Lond.) 497:437-455.
34. Kosaka, T. (1980) The axon initial segment as a synaptic site: Ultrastructure and synaptology of the initial segment of the pyramidal cell in the rat hippocampus (CA3 region). J. Neuroeytol. 9:861-882.
35. A and glycine receptors in the mammalian retina. J. Neurosci. 16:2127-2140.
36. Laurie, D.J., and P.H. Seeburg (1994) Ligand affinities at recombinant N-methyl-D-aspartate receptors depend on subunit composition. Eur. J. Pharmacol. 268:335-345.
37. Login, G.R., and A.M. Dvorak (1994) Application of microwave fixation techniques in pathology to neuroscience studies: A review. J. Neurosci. Methods 55:173-182.
38. Marani, E., and R.W. Horobin (1994) Overview of microwave applications in the neurosciences. J. Neurosci. Methods 55:111-117.
39. Monyer, H., N. Burnashev, D.J. Laurie, B. Sakmann, and P.H. Seeburg (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540.
40. A receptor in the rat brain. J. Comp. Neurol. 350:260-271.
41. Nakayama, H., S. Shioda, H. Okuda, T. Nakashima, and Y. Nakai (1995) Immunocytochemical localization of nicotinic acetylcholine receptor in rat cerebral cortex. Mol. Brain. Res. 32:321-328.
42. Nusser, Z., E. Mulvihill, P. Streit, and P. Somogyi (1994) Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localization. Neurosci. 61:421-427.
43. A receptor in relation to specific GABAergic synapses in the dentate gyrus. Eur. J. Neurosci. 7:630-646.
44. A receptors on cerebellar granule cells as determined by a quantitative immunogold method. J. Neurosci. 15:2948-2960.
45. Nusser, Z., W. Sieghart, D. Benke, J.M. Fritschy, and P. Somogyi (1996) Differential synaptic localization of two major γ-aminobutyric acid type A receptor alpha subunits on hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. USA 93:11939-11944.
46. A receptor subunits in the rat CNS. J. Comp. Neurol. 326:193-216.
47. Petralia, R.S., Y.X. Wang, and R.J. Wenthold (1994a) The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J. Neurosci. 14:6102-6120.
48. Petralia, R.S., N. Yokotani, and R.J. Wenthold (1994b) 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.
49. Priestley, T., P. Laughton, J. Myers, B. Lebourdelies, J. Derby, and P. Whiting (1995) Pharmacological properties of recombinant human N-methyl-D-aspartate receptors comprising NR1a/NR2A and NR1a/ NR2B subunit assemblies expressed in permanently transfected mouse fibroblast cells. Mol. Pharmacol. 48:415-421.
50. Rema, V., and F.F. Ebner (1996) Postnatal changes in NMDAR1 subunit expression in the rat trigeminal pathway to barrel field cortex. J. Comp. Neurol. 368:165-184.
51. A-receptor subunits in the rat retina. J. Comp. Neurol. 357:1-14.
52. Schroder, H. (1992) Immunohistochemistry of cholinergic receptors. Anat. Embryol, 186:407-429.
53. Shi, S.R., M.E. Key, and K.L. Kalra (1991) Antigen retrieval in formalin-fixed, paraffin-embedded tissues: An enhancement method for immunohistochemical staining based on microwave oven heating of tissue sections. J. Histochem. Cytochem. 39:741-748.
54. Shi, S.R., A. Imam, L. Young, R.J. Cote, and C.R. Taylor (1995) Antigen retrieval immunohistochemistry under the influence of pH using monoclonal antibodies. J. Histochem. Cytochem. 43:193-201.
55. Somogyi, P., and H. Takagi (1982) A note on the use of picric acid-paraformaldehyde-glutaraldehyde fixative for correlated light and electron microscopic immunocytochemistry. Neurosci. 7:1779-1783.
56. Somogyi, P., M.G. Nunzi, A. Gorio, and A.D. Smith (1983a) A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells. Brain Res. 259:137-142.
57. Somogyi, P., A.D. Smith, M.G. Nunzi, A. Gorio, H. Takagi, and J.Y. Wu (1983b) Glutamate decarboxylase immunoreactivity in the hippocampus of the cat: Distribution of immunoreactive synaptic terminals with special reference to the axon initial segment of pyramidal neurons. J. Neurosci. 3:1450-1468.
58. A-receptor is concentrated in synaptic junctions containing the α1 and β2/3 subunits in hippocampus, cerebellum and globus pallidus. Neuropharmacology 35:1425-1444.
59. Standaert, D.G., G.B. Lanwehrmeyer, J.A. Kerner, J.B. Penney, and A.B. Young (1996) Expression of NMDAR2D glutamate receptor subunit mRNA in neurochemically identified interneurons in the rat neostriatum, neocortex and hippocampus. Mol. Brain. Res. 42:89-102.
60. Van der Zee, E.A., C. Streefland, A.D. Strosberg, H. Schroder, and P.G.M. Luiten (1992) Visualization of cholinoceptive neurons in the rat neocortex: Colocalization of masearinic and nicotinic acetylcholine receptors. Mol. Brain. Res. 14:326-336.
61. Watanabe, M., Y. Inoue, K. Sakiwura, and M. Mishina (1993) Distinct distributions of five N-niethyl-D-aspartate receptor channel subunit mRNAs in the forebrain. J. Comp. Neurol 338:377-390.
62. Wenzel, A., L. Scheurer, R. Kunzi, J.M. Fritschy, H. Mohler, and D. Benke (1995) Distribution of NMDA receptor subunit proteins NR2A, 2B, 2C and 2D in rat brain. Neuroreport 7:45-48.
63. Wenzel, A., J.M. Fritschy, H. Mohler, and D. Benke (1997) NMDA receptor heterogeneity during postnatal development of the rat brain: Differential expression of the NR2A, NR2B, and NR2C subunit proteins. J. Neurochem. 68:469-478.
64. Werner, M., R.von Wasielewski, and P. Komminoth (1996) Antigen retrieval, signal amplification and intensification in immunohistochemistry. Histochem. Cell Biol. 105:253-260.
65. A receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J. Neurosci. 12:1040-1062.
66. Wyllie, D.A.J., P. Behe, M. Nassar, R. Schoepfer, and D. Colquhoun (1996) Single-channel currents from recombinant NMDA NR1a/NB2D receptors expressed in Xenopus oocytes. Proc. R. Soc. Lond. B 263:1079-1086
67. A receptor in the rat brain. Neurosci. Lett. 127:125-128.