AMPA amd NMDA receptors: Similarities and differences in their synaptic distribution

Current Opinion in Neurobiology

Volumn 10, Issue 3, 2000, Pages 337-341

  Nusser, Zoltan ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POSTSYNAPTIC RECEPTOR; RECEPTOR SUBTYPE; SYNAPSE RECEPTOR;

HUMAN; HUMAN CELL; IMMUNOGOLD STAINING; PRIORITY JOURNAL; REVIEW; SYNAPSE; ANIMAL; CHEMISTRY; NERVE CELL;

ANIMALS; NEURONS; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 0033625432     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(00)00086-6     Document Type: Review

References (46)

1. Hollmann M., Heinemann S. Cloned glutamate receptors. Annu Rev Neurosci. 17:1994;31-108.
2. Seeburg P.H. The molecular biology of mammalian glutamate receptor channels. Trends Neurosci. 16:1993;359-365.
3. Nakanishi S. Metabotropic glutamate receptors: synaptic transmission, modulation, and plasticity. Neuron. 13:1994;1031-1037.
4. Pin J.P., Duvoisin R. The metabotropic glutamate receptors: structure and functions. Neuropharmacology. 34:1995;1-26.
5. Seeburg P.H. The role of RNA editing in controlling glutamate receptor channel properties. J Neurochem. 66:1996;1-5.
6. 125I-labeled α bungarotoxin binding at mouse motor endplates. Proc Natl Acad Sci USA. 71:1974;1376-1378.
7. Moriyoshi K., Masu M., Ishii T., Shigemoto R., Mizuno N., Nakanishi S. Molecular cloning and characterization of the rat NMDA receptor. Nature. 354:1991;31-37.
8. Hollmann M., O'Shea-Greenfield A., Rogers S.W., Heinemann S. Cloning by functional expression of a member of the glutamate receptor family. Nature. 342:1989;643-648.
9. Rogers S.W., Hughes T.E., Hollmann M., Gasic G.P., Deneris E.S., Heinemann S. The characterization and localization of the glutamate receptor subunit GluR1 in the rat brain. J Neurosci. 11:1991;2713-2724.
10. Wenthold R.J., Yokotani N., Doi K., Wada K. Immunochemical characterization of the non-NMDA glutamate receptor using subunit-specific antibodies. J Biol Chem. 267:1992;501-507.
11. Molnar E., Baude A., Richmond S.A., Patel P.B., Somogyi P., McIlhinney R.A.J. Biochemical and immunocytochemical characterization of antipeptide antibodies to a cloned GluR1 glutamate receptor subunit: cellular and subcellular distribution in the rat forebrain. Neuroscience. 53:1993;307-326.
12. Martin L.J., Blackstone C.D., Levey A.I., Huganir R.L., Price D.L. AMPA glutamate receptor subunits are differentially distributed in rat brain. Neuroscience. 53:1993;327-358.
13. Nusser Z., Mulvihill E., Streit P., Somogyi P. Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localization. Neuroscience. 61:1994;421-427.
14. Baude A., Nusser Z., Molnar E., McIlhinney R.A.J., Somogyi P. High-resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and non-synaptic sites in rat hippocampus. Neuroscience. 69:1995;1031-1055.
15. Phend K.D., Rustioni A., Weinberg R.J. An osmium-free method of Epon embedment that preserves both ultrastucture and antigenicity for post-embedding immunocytochemistry. J Histochem Cytochem. 43:1995;283-292.
16. Matsubara A., Laake J.H., Davanger S., Usami S., Ottersen O.P. Organization of AMPA receptor subunits at a glutamate synapse: a quantitative immunogold analysis of hair cell synapses in the rat organ of Corti. J Neurosci. 16:1996;4457-4467.
17. Craig A.M., Blackstone C.D., Huganir R.L., Banker G. The distribution of glutamate receptors in cultured rat hippocampal neurons: postsynaptic clustering of AMPA-selective subunits. Neuron. 10:1993;1055-1068.
18. Craig A.M., Blackstone C.D., Huganir R.L., Banker G. Selective clustering of glutamate and γ-aminobutyric acid receptors opposite terminals releasing the corresponding neurotransmitters. Proc Natl Acad Sci USA. 91:1994;12373-12377.
19. Somogyi P., Tamas G., Lujan R., Buhl E.H. Salient features of synaptic organisation in the cerebral cortex. Brain Res Rev. 26:1998;113-135.
20. Kharazia V.N., Weinberg R.J. Tangential synaptic distribution of NMDA and AMPA receptors in rat neocortex. Neurosci Lett. 238:1997;41-44.
21. Baude A., Molnar E., Latawiec D., McIlhinney R.A.J., Somogyi P. Synaptic and nonsynaptic localization of the GluR1 subunit of the AMPA-type excitatory amino acid receptor in the rat cerebellum. J Neurosci. 14:1994;2830-2843.
22. Nusser Z., Lujan R., Laube G., Roberts J.D.B., Molnar E., Somogyi P. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron. 21:1998;545-559. Quantitative immunogold localization of synaptic AMPA receptors showed that the amount of AMPA receptors at a given glutamatergic synapse is governed by both pre- and postsynaptic elements. The high sensitivity of the applied immunogold localization was demonstrated after functional calibration. On average, less than three functional receptors are represented by a gold particle, indicating that immunonegative synapses contain a maximum of two functional receptors. The AMPA receptor number per mossy fiber to CA3 pyramidal cell synapse ranges from 12 to 200, with a mean of 80, and that for C/A synapses on CA3 pyramidal cell spines ranges from <3 to 135, with a mean of 10.
23. 2, did not contain a detectable amount of AMPA receptors. In the rest of the synapses, the number of AMPA receptors is linearly correlated with synaptic area, whereas NMDA receptor number is linearly correlated with the diameter of the synapse. Thus, these results demonstrate that the ratio of the number of AMPA to NMDA receptors depends on the size of the synapses.
24. Petralia R.S., Wang Y.X., Wenthold R.J. The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J Neurosci. 14:1994;6102-6120.
25. Petralia R.S., Yokotani N., Wenthold R.J. Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J Neurosci. 14:1994;667-696.
26. Siegel S.J., Brose N., Janssen W.G., Gasic G.P., Jahn R., Heinemann S.F., Morrison J.H. Regional, cellular, and ultrastructural distribution of N-methyl-D-aspartate receptor subunit 1 in monkey hippocampus. Proc Natl Acad Sci USA. 91:1994;564-568.
27. Huntley G.W., Vickers J.C., Morrison J.H. Cellular and synaptic localization of NMDA and non-NMDA receptor subunits in neocortex: organizational features related to cortical circuitry, function and disease. Trends Neurosci. 17:1994;536-543.
28. -/- brains. However, protease digestion, a newly developed antigen-retrieval method, transformed the strong intracellular labeling into a punctate staining of the hippocampal neuropile with cell bodies and apical dendrites almost devoid of labeling.
29. A receptor were concentrated around axon initial segments of hippocampal pyramidal cells consistent with electron microscopic immunogold localization. Similarly, a diffuse, mainly intracellular labeling for NMDA receptor subunits were replaced by numerous, intensely immunopositive puncta in the neuropile, indicating a preferential synaptic location of NMDA receptors.
30. Kharazia V.N., Weinberg R.J. Immunogold localization of AMPA and NMDA receptors in somatic sensory cortex of albino rat. J Comp Neurol. 412:1999;292-302.
31. Kharazia V.N., Phend K.D., Rustioni A., Weinberg R.J. EM colocalization of AMPA and NMDA receptor subunits at synapses in rat cerebrat cortex. Neurosci Lett. 210:1996;37-40.
32. Petralia R.S., Esteban J.A., Wang Y.X., Partridge J.G., Zhao H.M., Wenthold R.J., Malinow R. Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat Neurosci. 2:1999;31-36. The proportion of Schaffer collateral synapses on CA1 pyramidal cells that are immunopositive for AMPA receptors increases during postnatal development, whereas that for NMDA receptors does not change. The authors also show that as development progresses, immunopositive synapses contain increasing numbers of AMPA receptors, with very little change in NMDA receptor number.
33. Clarke N.P., Bolam J.P. Distribution of glutamate receptor subunits at neurochemically characterized synapses in the entopeduncular nucleus and subthalamic nucleus of the rat. J Comp Neurol. 397:1998;403-420.
34. Rubio M.E., Wenthold R.J. Glutamate receptors are selectively targeted to postsynaptic sites in neurons. Neuron. 18:1997;939-950.
35. Harris K.M., Kater S.B. Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu Rev Neurosci. 17:1994;341-371.
36. A receptor number underlie variation in GABA mini amplitude. Neuron. 19:1997;697-709.
37. A receptors underlies potentiation at hippocampal inhibitory synapses. Nature. 395:1998;172-177.
38. A, NMDA and AMPA receptors: a developmentally regulated 'menage a trois'. Trends Neurosci. 20:1997;523-529.
39. Racca C., Stephenson F.A., Streit P., Roberts J.D.B., Somogyi P. NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area. J Neurosci. 20:2000;2512-2522. Every synapse made by Schaffer collaterals onto CA1 pyramidal cell spines contains NMDA receptors, but only 85% of them has a detectable level of AMPA receptors in adult rats. Furthermore, the variability in the number of synaptic NMDA receptors is much smaller than that of AMPA receptors. These results indicate that the regulation of expression of these two types of receptor is not closely linked.
40. Stevens C.F., Wang Y. Changes in reliability of synaptic function as a mechanism for plasticity. Nature. 371:1994;704-707.
41. Bolshakov V.Y., Siegelbaum S.A. Regulation of hippocampal transmitter release during development and long-term potentiation. Science. 269:1995;1730-1734.
42. Larkman A., Hannay T., Stratford K., Jack J. Presynaptic release probability influences the locus of long-term potentiation. Nature. 360:1992;70-73.
43. Malinow R. Transmission between pairs of hippocampal slice neurons: quantal levels, oscillations, and LTP. Science. 252:1991;722-724.
44. Malenka R.C., Nicoll R.A. Silent synapses speak up. Neuron. 19:1997;473-476.
45. Toni N., Buchs P.A., Nikonenko I., Bron C.R., Muller D. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature. 402:1999;421-425.
46. Markram H., Tsodyks M. Redistribution of synaptic efficacy between neocortical pyramidal neurons. Nature. 382:1996;807-810.