Cellular and synaptic distribution of NR2A and NR2B in macaque monkey and rat hippocampus as visualized with subunit-specific monoclonal antibodies

Experimental Neurology

Volumn 191, Issue SUPPL. 1, 2005, Pages

  Janssen, William G M ^a   Vissavajjhala, Prabakhar ^a   Andrews, Ginelle ^a   Moran, Thomas ^a   Hof, Patrick R ^a   Morrison, John H ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Electron microscopy; Excitatory synapse; Glutamate; Immunogold; NMDA receptor; Spinophilin

Indexed keywords

COMPLEMENTARY DNA; HYBRID PROTEIN; MONOCLONAL ANTIBODY; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; CONTROLLED STUDY; EMBRYO; GENETIC TRANSFECTION; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOGOLD ELECTRON MICROSCOPY; IMMUNOREACTIVITY; MACACA; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SYNAPSE; ULTRASTRUCTURE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; CELL LINE; GENE TRANSFER TECHNIQUES; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; KIDNEY; MACACA FASCICULARIS; NEOCORTEX; NEURONS; PROTEIN SUBUNITS; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 11344258408     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2004.08.020     Document Type: Article

References (71)

1. M.M. Adams, R.A. Shah, W.G. Janssen, and J.H. Morrison Different modes of hippocampal plasticity in response to estrogen in young and aged female rats Proc. Natl. Acad. Sci. U. S. A. 98 2001 8071 8076
2. M.M. Adams, S.E. Fink, W.G. Janssen, R.A. Shah, and J.H. Morrison Estrogen modulates synaptic N-methyl-d-aspartate receptor subunit distribution in the aged hippocampus J. Comp. Neurol. 474 2004 419 426
3. C. Aoki, S. Fujisawa, V. Mahadomrongkul, P.J. Shah, K. Nader, and A. Erisir NMDA receptor blockade in intact adult cortex increases trafficking of NR2A subunits into spines, postsynaptic densities, and axon terminals Brain Res. 963 2003 139 149
4. E.A. Barnard Ionotropic glutamate receptors: new types and new concepts Trends Pharmacol. Sci. 18 1997 141 148
5. A. Barria, and R. Malinow Subunit-specific NMDA receptor trafficking to synapses Neuron 35 2002 345 353
6. J.C. Brimecombe, F.A. Boeckman, and E. Aizenman Functional consequences of NR2 subunit composition in single recombinant N-methyl-d-aspartate receptors Proc. Natl. Acad. Sci. U. S. A. 94 1997 11019 11024
7. A.L. Buller, H.C. Larson, B.E. Schneider, J.A. Beaton, R.A. Morrisett, and D.T. Monaghan The molecular basis of NMDA receptor subtypes: native receptor diversity is predicted by subunit composition J. Neurosci. 14 1994 5471 5484
8. N. Burnashev, H. Monyer, P.H. Seeburg, and B. Sakmann Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit Neuron 8 1992 189 198
9. J.P. Charton, M. Herkert, C.M. Becker, and H. Schroder Cellular and subcellular localization of the 2B-subunit of the NMDA receptor in the adult rat telencephalon Brain Res. 816 1999 609 617
10. F.A. Chaudhry, K.P. Lehre, M. van Lookeren Campagne, O.P. Ottersen, N.C. Danbolt, and J. Storm-Mathisen Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry Neuron 15 1995 711 720
11. N. Chen, T. Luo, and L.A. Raymond Subtype-dependence of NMDA receptor channel open probability J. Neurosci. 19 1999 6844 6854
12. F. Conti, P. Barbaresi, M. Melone, and A. Ducati Neuronal and glial localization of NR1 and NR2A/B subunits of the NMDA receptor in the human cerebral cortex Cereb. Cortex 9 1999 110 120
13. A. Erisir, and J.L. Harris Decline of the critical period of visual plasticity is concurrent with the reduction of NR2B subunit of the synaptic NMDA receptor in layer 4 J. Neurosci. 23 2003 5208 5218
14. J. Feng, Z. Yan, A. Ferreira, K. Tomizawa, J.A. Liauw, M. Zhuo, P.B. Allen, C.C. Ouimet, and P. Greengard Spinophilin regulates the formation and function of dendritic spines Proc. Natl. Acad. Sci. U. S. A. 97 2000 9287 9292
15. J.M. Fritschy, O. Weinmann, A. Wenzel, and D. Benke Synapse-specific localization of NMDA and GABA(A) receptor subunits revealed by antigen-retrieval immunohistochemistry J. Comp. Neurol. 390 1998 194 210
16. S. Fujisawa, and C. Aoki In vivo blockade of N-methyl-d-aspartate receptors induces rapid trafficking of NR2B subunits away from synapses and out of spines and terminals in adult cortex Neuroscience 121 2003 51 63
17. A. Gardiol, C. Racca, and A. Triller Dendritic and postsynaptic protein synthetic machinery J. Neurosci. 19 1999 168 179
18. A.H. Gazzaley, S.J. Siegel, J.H. Kordower, E.J. Mufson, and J.H. Morrison Circuit-specific alterations of N-methyl-d-aspartate receptor subunit 1 in the dentate gyrus of aged monkeys Proc. Natl. Acad. Sci. U. S. A. 93 1996 3121 3125
19. A.H. Gazzaley, D.L. Benson, G.W. Huntley, and J.H. Morrison Differential subcellular regulation of NMDAR1 protein and mRNA in dendrites of dentate gyrus granule cells after perforant path transection J. Neurosci. 17 1997 2006 2017
20. K.M. Harris, and S.B. Kater Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function Annu. Rev. Neurosci. 17 1994 341 371
21. L.M. Hawkins, P.L. Chazot, and F.A. Stephenson Biochemical evidence for the co-association of three N-methyl-d-aspartate (NMDA) R2 subunits in recombinant NMDA receptors J. Biol. Chem. 274 1999 27211 27218
22. S.D. Hess, L.P. Daggett, J. Crona, C. Deal, C.C. Lu, A. Urrutia, L. Chavez-Noriega, S.B. Ellis, E.C. Johnson, and G. Velicelebi Cloning and functional characterization of human heteromeric N-methyl-d-aspartate receptors J. Pharmacol. Exp. Ther. 278 1996 808 816
23. O.P. Hjelle, F.A. Chaudhry, and O.P. Ottersen Antisera to glutathione: characterization and immunocytochemical application to the rat cerebellum Eur. J. Neurosci. 6 1994 793 804
24. M. Hollmann, and S. Heinemann Cloned glutamate receptors Annu. Rev. Neurosci. 17 1994 31 108
25. K. Ikeda, M. Nagasawa, H. Mori, K. Araki, K. Sakimura, M. Watanabe, Y. Inoue, and M. Mishina Cloning and expression of the epsilon 4 subunit of the NMDA receptor channel FEBS Lett. 313 1992 34 38
26. T. Ishii, K. Moriyoshi, H. Sugihara, K. Sakurada, H. Kadotani, M. Yokoi, C. Akazawa, R. Shigemoto, N. Mizuno, and M. Masu Molecular characterization of the family of the N-methyl-d-aspartate receptor subunits J. Biol. Chem. 268 1993 2836 2843
27. T. Iwamoto, Y. Yamada, K. Hori, Y. Watanabe, K. Sobue, and M. Inui Differential modulation of NR1-NR2A and NR1-NR2B subtypes of NMDA receptor by PDZ domain-containing proteins J. Neurochem. 89 2004 100 108
28. J.N. Kew, J.G. Richards, V. Mutel, and J.A. Kemp Developmental changes in NMDA receptor glycine affinity and ifenprodil sensitivity reveal three distinct populations of NMDA receptors in individual rat cortical neurons J. Neurosci. 18 1998 1935 1943
29. G. Krapivinsky, L. Krapivinsky, Y. Manasian, A. Ivanov, R. Tyzio, C. Pellegrino, Y. Ben-Ari, D.E. Clapham, and I. Medina The NMDA receptor is coupled to the ERK pathway by a direct interaction between NR2B and RasGRF1 Neuron 40 2003 775 784
30. S.S. Kumar, and J.R. Huguenard Pathway-specific differences in subunit composition of synaptic NMDA receptors on pyramidal neurons in neocortex J. Neurosci. 23 2003 10074 10083
31. T. Kutsuwada, N. Kashiwabuchi, H. Mori, K. Sakimura, E. Kushiya, K. Araki, H. Meguro, H. Masaki, T. Kumanishi, and M. Arakawa Molecular diversity of the NMDA receptor channel Nature 358 1992 36 41
32. D.J. Laurie, I. Bartke, R. Schoepfer, K. Naujoks, and P.H. Seeburg Regional, developmental and interspecies expression of the four NMDAR2 subunits, examined using monoclonal antibodies Brain Res., Mol. Brain Res. 51 1997 23 32
33. J. Luo, Y. Wang, R.P. Yasuda, A.W. Dunah, and B.B. Wolfe The majority of N-methyl-d-aspartate receptor complexes in adult rat cerebral cortex contain at least three different subunits (NR1/NR2A/NR2B) Mol. Pharmacol. 51 1997 79 86
34. S.J. Martin, P.D. Grimwood, and R.G. Morris Synaptic plasticity and memory: an evaluation of the hypothesis Annu. Rev. Neurosci. 23 2000 649 711
35. H. Meguro, H. Mori, K. Araki, E. Kushiya, T. Kutsuwada, M. Yamazaki, T. Kumanishi, M. Arakawa, K. Sakimura, and M. Mishina Functional characterization of a heteromeric NMDA receptor channel expressed from cloned cDNAs Nature 357 1992 70 74
36. H. Monyer, R. Sprengel, R. Schoepfer, A. Herb, M. Higuchi, H. Lomeli, N. Burnashev, B. Sakmann, and P.H. Seeburg Heteromeric NMDA receptors: molecular and functional distinction of subtypes Science 256 1992 1217 1221
37. H. Monyer, N. Burnashev, D.J. Laurie, B. Sakmann, and P.H. Seeburg Developmental and regional expression in the rat brain and functional properties of four NMDA receptors Neuron 12 1994 529 540
38. K. Moriyoshi, M. Masu, T. Ishii, R. Shigemoto, N. Mizuno, and S. Nakanishi Molecular cloning and characterization of the rat NMDA receptor Nature 354 1991 31 37
39. N. Nakanishi, R. Axel, and N.A. Shneider Alternative splicing generates functionally distinct N-methyl-d-aspartate receptors Proc. Natl. Acad. Sci. U. S. A. 89 1992 8552 8556
40. G. Nase, J. Weishaupt, P. Stern, W. Singer, and H. Monyer Genetic and epigenetic regulation of NMDA receptor expression in the rat visual cortex Eur. J. Neurosci. 11 1999 4320 4326
41. Z. Nusser, R. Lujan, G. Laube, J.D. Roberts, E. Molnar, and P. Somogyi Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus Neuron 21 1998 545 559
42. J.M. Parker, D. Guo, and R.S. Hodges New hydrophilicity scale derived from high-performance liquid chromatography peptide retention data: correlation of predicted surface residues with antigenicity and X-ray-derived accessible sites Biochemistry 25 1986 5425 5432
43. R.S. Petralia, Y.X. Wang, and R.J. Wenthold The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1 J. Neurosci. 14 1994 6102 6120
44. J.P. Pierce, K. van Leyen, and J.B. McCarthy Translocation machinery for synthesis of integral membrane and secretory proteins in dendritic spines Nat. Neurosci. 3 2000 311 313
45. C. Portera-Cailliau, D.L. Price, and L.J. Martin N-methyl-d-aspartate receptor proteins NR2A and NR2B are differentially distributed in the developing rat central nervous system as revealed by subunit-specific antibodies J. Neurochem. 66 1996 692 700
46. E.M. Quinlan, B.D. Philpot, R.L. Huganir, and M.F. Bear Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo Nat. Neurosci. 2 1999 352 357
47. E.M. Quinlan, D. Lebel, I. Brosh, and E. Barkai A molecular mechanism for stabilization of learning-induced synaptic modifications Neuron 41 2004 185 192
48. C. Racca, F.A. Stephenson, P. Streit, J.D. Roberts, and P. Somogyi NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area J. Neurosci. 20 2000 2512 2522
49. E.B. Roberts, and A.S. Ramoa Enhanced NR2A subunit expression and decreased NMDA receptor decay time at the onset of ocular dominance plasticity in the ferret J. Neurophysiol. 81 1999 2587 2591
50. S.H. Shi, Y. Hayashi, R.S. Petralia, S.H. Zaman, R.J. Wenthold, K. Svoboda, and R. Malinow Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation Science 284 1999 1811 1816
51. S.J. Siegel, N. Brose, W.G. Janssen, G.P. Gasic, R. Jahn, S.F. Heinemann, and J.H. Morrison Regional, cellular, and ultrastructural distribution of N-methyl-d-aspartate receptor subunit 1 in monkey hippocampus Proc. Natl. Acad. Sci. U. S. A. 91 1994 564 568
52. J. Spacek, and K.M. Harris Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat J. Neurosci. 17 1997 190 203
53. P. Stern, P. Behe, R. Schoepfer, and D. Colquhoun Single-channel conductances of NMDA receptors expressed from cloned cDNAs: comparison with native receptors Proc. R. Soc. London, B Biol. Sci. 250 1992 271 277
54. P. Stern, M. Cik, D. Colquhoun, and F.A. Stephenson Single channel properties of cloned NMDA receptors in a human cell line: comparison with results from Xenopus oocytes J. Physiol. 476 1994 391 397
55. O. Steward, and W.B. Levy Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus J. Neurosci. 2 1982 284 291
56. O. Steward, and T.M. Reeves Protein-synthetic machinery beneath postsynaptic sites on CNS neurons: association between polyribosomes and other organelles at the synaptic site J. Neurosci. 8 1988 176 184
57. Y.P. Tang, E. Shimizu, G.R. Dube, C. Rampon, G.A. Kerchner, M. Zhuo, G. Liu, and J.Z. Tsien Genetic enhancement of learning and memory in mice Nature 401 1999 63 69
58. H. Tiedge, F.E. Bloom, and D. Richter RNA, whither goest thou? Science 283 1999 186 187
59. K.R. Tovar, and G.L. Westbrook The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro J. Neurosci. 19 1999 4180 4188
60. K.R. Tovar, and G.L. Westbrook Mobile NMDA receptors at hippocampal synapses Neuron 34 2002 255 264
61. G.M. Vaitaitis, R.J. Sanderson, E.J. Kimble, N.D. Elkins, and S.C. Flores Modification of enzyme-conjugated streptavidin-biotin Western blot technique to avoid detection of endogenous biotin-containing proteins BioTechniques 26 1999 854 858
62. J.G. Valtschanoff, A. Burette, R.J. Wenthold, and R.J. Weinberg Expression of NR2 receptor subunit in rat somatic sensory cortex: synaptic distribution and colocalization with NR1 and PSD-95 J. Comp. Neurol. 410 1999 599 611
63. M. van Lookeren Campagne, A.B. Oestreicher, T.P. van der Krift, W.H. Gispen, and A.J. Verkleij Freeze-substitution and Lowicryl HM20 embedding of fixed rat brain: suitability for immunogold ultrastructural localization of neural antigens J. Histochem. Cytochem. 39 1991 1267 1279
64. M.A. Varney, C. Jachec, C. Deal, S.D. Hess, L.P. Daggett, R. Skvoretz, M. Urcan, J.H. Morrison, T. Moran, E.C. Johnson, and G. Velicelebi Stable expression and characterization of recombinant human heteromeric N-methyl-d-aspartate receptor subtypes NMDAR1A/2A and NMDAR1A/2B in mammalian cells J. Pharmacol. Exp. Ther. 279 1996 367 378
65. S. Vicini, J.F. Wang, J.H. Li, W.J. Zhu, Y.H. Wang, J.H. Luo, B.B. Wolfe, and D.R. Grayson Functional and pharmacological differences between recombinant N-methyl-d-aspartate receptors J. Neurophysiol. 79 1998 555 566
66. P. Vissavajjhala, W.G. Janssen, Y. Hu, A.H. Gazzaley, T. Moran, P.R. Hof, and J.H. Morrison Synaptic distribution of the AMPA-GluR2 subunit and its colocalization with calcium-binding proteins in rat cerebral cortex: an immunohistochemical study using a GluR2-specific monoclonal antibody Exp. Neurol. 142 1996 296 312
67. Y.H. Wang, T.Z. Bosy, R.P. Yasuda, D.R. Grayson, S. Vicini, T. Pizzorusso, and B.B. Wolfe Characterization of NMDA receptor subunit-specific antibodies: distribution of NR2A and NR2B receptor subunits in rat brain and ontogenic profile in the cerebellum J. Neurochem. 65 1995 176 183
68. P. Washbourne, J.E. Bennett, and A.K. McAllister Rapid recruitment of NMDA receptor transport packets to nascent synapses Nat. Neurosci. 5 2002 751 759
69. M. Watanabe, M. Fukaya, K. Sakimura, T. Manabe, M. Mishina, and Y. Inoue Selective scarcity of NMDA receptor channel subunits in the stratum lucidum (mossy fibre-recipient layer) of the mouse hippocampal CA3 subfield Eur. J. Neurosci. 10 1998 478 487
70. A. Wenzel, J.M. Fritschy, H. Mohler, and D. Benke NMDA receptor heterogeneity during postnatal development of the rat brain: differential expression of the NR2A, NR2B, and NR2C subunit proteins J. Neurochem. 68 1997 469 478
71. M. Yamazaki, H. Mori, K. Araki, K.J. Mori, and M. Mishina Cloning, expression and modulation of a mouse NMDA receptor subunit FEBS Lett. 300 1992 39 45