Ontogeny of postsynaptic density proteins at glutamatergic synapses

Molecular and Cellular Neuroscience

Volumn 29, Issue 3, 2005, Pages 436-452

  Petralia, Ronald S ^a   Sans, Nathalie ^a   Wang, Ya Xian ^a   Wenthold, Robert J ^a  

^a NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CADHERIN; CATENIN; GLUTAMIC ACID; MEMBRANE PROTEIN; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; POSTSYNAPTIC DENSITY PROTEIN; POSTSYNAPTIC DENSITY PROTEIN 95; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; HIPPOCAMPUS; IMMUNOBLOTTING; IMMUNOGOLD ELECTRON MICROSCOPY; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RAT; SYNAPSE;

ANIMALS; ANIMALS, NEWBORN; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CARRIER PROTEINS; CELL DIFFERENTIATION; GLUTAMIC ACID; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; NERVE TISSUE PROTEINS; NEURONS; NEUROPEPTIDES; RATS; RECEPTORS, AMPA; RECEPTORS, GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC MEMBRANES; SYNAPTIC TRANSMISSION;

ANIMALIA;

EID: 20444397745     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2005.03.013     Document Type: Article

References (106)

1. S.E. Ahmari, J. Buchanan, and S.J. Smith Assembly of presynaptic active zones from cytoplasmic transport packets Nat. Neurosci. 3 2000 445 451
2. P. Alberts, and T. Galli The cell outgrowth secretory endosome (COSE): a specialized compartment involved in neuronal morphogenesis Biol. Cell 95 2003 419 424
3. F. Ango, G. de Cristo, H. Higashiyama, V. Bennett, P. Wu, and Z.J. Huang Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at Purkinje axon initial segment Cell 119 2004 257 272
4. C. Aoki, K. Wu, A. Elste, G.-W. Len, S.-Y. Lin, G. McAuliffe, and I.B. Black Localization of brain-derived neurotrophic factor and TrkB receptors to postsynaptic densities of adult rat cerebral cortex J. Neurosci. Res. 59 2000 454 463
5. F. Appel, J. Holm, J. Conscience, F. von Bohlen und Halbach, A. Faissner, P. James, and M. Schachner Identification of the border between fibronectin type III homologous repeats 2 and 3 of the neural cell adhesion molecule L1 as a neurite outgrowth promoting and signal-transducing domain J. Neurobiol. 28 1995 297 312
6. K.-U. Bayer, J. Löhler, H. Schulman, and K. Harbers Developmental expression of the CaM kinase II isoforms: ubiquitous γ- and δ-CaM kinase II are the early isoforms and most abundant in the developing nervous system Mol. Brain Res. 70 1999 147 154
7. K.D. Beck, F. Lamballe, R. Klein, M. Barbacid, P.E. Schauwecker, T.H. McNeill, C.E. Finch, F. Hefti, and J.R. Day Induction of noncatalytic TrkB neurotrophin receptors during axonal sprouting in the adult hippocampus J. Neurosci. 13 1993 4001 4014
8. D.L. Benson, and H. Tanaka N-cadherin redistribution during synaptogenesis in hippocampal neurons J. Neurosci. 18 1998 6892 6904
9. D.S. Bredt, and R.A. Nicoll AMPA receptor trafficking at excitatory synapses Neuron 40 2003 361 379
10. T. Bresler, M. Shapira, T. Boeckers, T. Dresbach, M. Futter, C.C. Garner, K. Rosenblum, E.D. Gundelfinger, and N.E. Ziv Postsynaptic density assembly is fundamentally different from presynaptic active zone assembly J. Neurosci. 24 2004 1507 1520
11. J. Broman, B. Hassel, E. Rinvik, and O.P. Ottersen Biochemistry and anatomy of transmitter glutamate O.P. Ottersen J. Storm-Mathisen Handbook of Chemical Neuroanatomy Glutamate vol. 18 2000 Elsevier New York 1 44
12. O. Bukalo, N. Fentrop, A.Y.W. Lee, B. Salmen, J.W.S. Law, C.T. Wotjak, M. Schweizer, A. Dityatev, and M. Schachner Conditional ablation of the neural cell adhesion molecule reduces precision of spatial learning, long-term potentiation, and depression in the CA1 subfield of mouse hippocampus J. Neurosci. 24 2004 1565 1577
13. L.K. Crossin, and L.A. Krushel Cellular signaling by neural cell adhesion molecules of the immunoglobulin superfamily Dev. Dyn. 218 2000 260 279
14. M. Darstein, R.S. Petralia, G.T. Swanson, R.J. Wenthold, and S.F. Heinemann Distribution of kainate receptor subunits at hippocampal mossy fiber synapses J. Neurosci. 23 2003 8013 8019
15. G.P. Demyanenko, M. Schachner, E. Anton, R. Schmid, G. Feng, J. Sanes, and P.F. Maness Close homolog of L1 modulates area-specific neuronal positioning and dendrite orientation in the cerebral cortex Neuron 44 2004 423 437
16. V.D. Di Giorgi Gerevini, A. Caruso, I. Cappuccio, L. Ricci Vitiani, S. Romeo, C. Della Rocca, R. Gradini, D. Melchiorri, and F. Nicoletti The mGlu5 metabotropic glutamate receptor is expressed in zones of active neurogenesis of the embryonic and postnatal brain Dev. Brain Res. 150 2004 17 22
17. S. Dieni, and S. Rees Distribution of brain-derived neurotrophic factor and TrkB receptor proteins in the fetal and postnatal hippocampus and cerebellum of the guinea pig J. Comp. Neurol. 454 2002 229 240
18. A. Dosemeci, J.-H. Tao-Cheng, L. Vinade, C.A. Winters, L. Pozzo-Miller, and T.S. Reese Glutamate-induced transient modification of the postsynaptic density Proc. Natl. Acad. Sci. 98 2001 10428 10432
19. C.T. Drake, T.A. Milner, and S.L. Patterson Ultrastructural localization of full-length trkB immunoreactivity in rat hippocampus suggests multiple roles in modulating activity-dependent synaptic plasticity J. Neurosci. 19 1999 8009 8026
20. T. Dresbach, A. Neeb, G. Meyer, E.D. Gundelfinger, and N. Brose Synaptic targeting of neuroligin is independent of neurexin and SAP90/PSD95 binding Mol. Cell. Neurosci. 27 2004 227 235
21. G.M. Durand, Y. Kovalchuk, and A. Konnerth Long-term potentiation and functional synapse induction in developing hippocampus Nature 381 1996 71 75
22. M.U. Ehrengruber, A. Kato, K. Inokuchi, and S. Hennou Homer/Vesl proteins and their roles in CNS neurons Mol. Neurobiol. 29 2004 213 227
23. S.B. Elmariah, M.A. Crumling, T.D. Parsons, and R.J. Balice-Gordon Postsynaptic TrkB-mediated signaling modulates excitatory and inhibitory neurotransmitter receptor clustering at hippocampal synapses J. Neurosci. 24 2004 2380 2393
24. A. Erisir, and J.L. Harris Decline in 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
25. 2+/calmodulin-dependent protein kinase in rat brain J. Neurosci. 5 1985 3270 3277
26. E. Escandón, D. Soppet, A. Rosenthal, J.-L. Mendoza-Ramirez, E. Szönyi, L.E. Burton, C.E. Henderson, L.F. Parada, and K. Nikolics Regulation of neurotrophin receptor expression during embryonic and postnatal development J. Neurosci. 14 1994 2054 2068
27. C. Faivre-Sarrailh, J. Falk, E. Pollerberg, M. Schachner, and G. Rougon NrCAM, cerebellar granule cell receptor for the neuronal adhesion molecule F3, displays an actin-dependent mobility in growth cones J. Cell Sci. 112 1999 3015 3027
28. J.C. Fiala, M. Feinberg, V. Popov, and K.M. Harris Synaptogenesis via dendritic filopodia in developing hippocampal area CA1 J. Neurosci. 18 1998 8900 8911
29. C.C. Fink, K.-U. Bayer, J.W. Myers, J.E. Ferrell Jr., H. Schulman, and T. Meyer Selective regulation of neurite extension and synapse formation by the β but not the α isoform of CaMKII Neuron 39 2003 283 297
30. R.H. Fryer, D.R. Kaplan, S.C. Feinstein, M.J. Radeke, D.R. Grayson, and L.F. Kromer Developmental and mature expression of full-length and truncated TrkB receptors in the rat forebrain J. Comp. Neurol. 374 1996 21 40
31. C.M. Fux, M. Krug, A. Dityatev, T. Schuster, and M. Schachner NCAM180 and glutamate receptor subtypes in potentiated spine synapses: an immunogold electron microscope study Mol. Cell. Neurosci. 24 2003 939 950
32. C.C. Garner, R.G. Zhai, E.D. Gundelfinger, and N.E. Ziv Molecular mechanisms of CNS synaptogenesis Trends Neurosci. 25 2002 243 250
33. Y. Goda, and G.W. Davis Mechanisms of synapse assembly and disassembly Neuron 40 2003 243 264
34. R.A. Gomes, C.M. Hampton, and A.K. McAllister Subcellular localization of TrkB in developing cortical neurons Soc. Neurosci. 2003 Abs. #783-9
35. M. Gonzalez, F.P. Ruggiero, Q. Chang, Y.-J. Shi, M.M. Rich, S. Kraner, and R.J. Balice-Gordon Disruption of TrkB-mediated signaling induces disassembly of postsynaptic receptor clusters at neuromuscular junctions Neuron 24 1999 567 583
36. K. Hashimoto, M. Fukaya, X. Qiao, K. Sakimura, M. Watanabe, and M. Kano Impairment of AMPA receptor function in cerebellar granule cells of ataxic mutant mouse Stargazer J. Neurosci. 19 1999 6027 6036
37. M. Hortsch Structural and functional evolution of the L1 family: are four adhesion molecules better than one? Mol. Cell. Neurosci. 15 2000 1 10
38. A. Kato, F. Ozawa, Y. Saitoh, K. Hirai, and K. Inokuchi Vesl, a gene encoding VASP/Ena family related protein, is upregulated during seizure, long-term potentiation and synaptogenesis FEBS Lett. 412 1997 183 189
39. J.F. Kayyem, J.M. Roman, E.J. de la Rosa, U. Schwarz, and W.J. Dreyer Bravo/Nr-CAM is closely related to the cell adhesion molecules L1 and Ng-CAM and has a similar heterodimer structure J. Cell Biol. 118 1992 1259 1270
40. P.T. Kelly, and P. Vernon Changes in the subcellular distribution of calmodulin-kinase II during brain development Dev. Brain Res. 18 1985 211 224
41. E. Kim, S. Naisbitt, Y.-P. Hsueh, A. Rao, A. Rothschild, A.M. Craig, and M. Sheng GKAP, a novel synaptic protein that interacts with the guanylate kinase-like domain of the PSD-95/SAP90 family of channel clustering molecules J. Cell Biol. 136 1997 669 678
42. J.H. Kim, D. Liao, L.-F. Lau, and R.L. Huganir SynGAP: a synaptic RasGAP that associates with the PSD-95/SAP90 protein family Neuron 20 1998 683 691
43. S.J. Kim, Y.S. Kim, J.P. Yuan, R.S. Petralia, P.F. Worley, and D.J. Linden Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1 Nature 426 2003 285 291
44. J.W.S. Law, A.Y.W. Lee, M. Sun, A.G. Nikonenko, S.K. Chung, A. Dityatev, M. Schachner, and F. Morellini Decreased anxiety, altered place learning, and increased CA1 basal excitatory synaptic transmission in mice with conditional ablation of the neural cell adhesion molecule L1 J. Neurosci. 23 2003 10419 10432
45. Z. Li, and M. Sheng Some assembly required: the development of neuronal synapses Nat. Rev., Mol. Cell Biol. 4 2003 833 841
46. S. Lim, S. Naisbitt, J. Yoon, J.-I. Hwang, P.-G. Suh, M. Sheng, and E. Kim Characterization of the Shank family of synaptic proteins J. Biol. Chem. 274 1999 29510 29518
47. X.-B. Liu, K.D. Murray, and E.G. Jones Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development J. Neurosci. 24 2004 8885 8895
48. G. López-Bendito, R. Shigemoto, A. Fairén, and R. Luján Differential distribution of group 1 metabotropic glutamate receptors during rat cortical development Cereb. Cortex 12 2002 368 625
49. M. Lustig, L. Erskine, C.A. Mason, M. Grumet, and T. Sakurai Nr-CAM expression in the developing mouse nervous system: ventral midline structures, specific fiber tracts, and neuropilar regions J. Comp. Neurol. 434 2001 13 28
50. E. Margotti, S. Covaceuszach, E. Tongiorgi, A. Cattaneo, and L. Domenici TRKB signaling controls the expression of N-methyl-d-aspartate receptors in the visual cortex Eur. J. Neurosci. 16 2002 1067 1074
51. A. Matsubara, J.H. Laake, S. Davanger, S. Usami, and O.P. Ottersen 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
52. K. Matsumoto-Miyai, A. Ninomiya, H. Yamasaki, H. Tamura, Y. Nakamura, and S. Shiosaka NMDA-dependent proteolysis of presynaptic adhesion molecule L1 in the hippocampus by neuropsin J. Neurosci. 23 2003 7727 7736
53. M. Montcouquiol, J. Valat, C. Travo, and A. Sans A role for BDNF in early postnatal rat vestibular epithelia maturation: implication of supporting cells Eur. J. Neurosci. 10 1998 598 606
54. S. Naisbitt, E. Kim, R.J. Weinberg, A. Rao, F.-C. Yang, A.M. Craig, and M. Sheng Characterization of guanylate kinase-associated protein, a postsynaptic density protein at excitatory synapses that interacts directly with postsynaptic density-95/synapse-associated protein 90 J. Neurosci. 17 1997 5687 5696
55. S. Naisbitt, E. Kim, J.C. Tu, B. Xiao, C. Sala, J. Valtschanoff, R.J. Weinberg, P.F. Worley, and M. Sheng Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin Neuron 23 1999 569 582
56. S. Oshima, M. Fukaya, N. Masabumi, T. Shirakawa, H. Oguchi, and M. Watanabe Early onset of NMDA receptor GluRε1 (NR2A) expression and its abundant postsynaptic localization in developing motoneurons of the mouse hypoglossal nucleus Neurosci. Res. 43 2002 239 250
57. D.T.S. Pak, and M. Sheng Targeted protein degradation and synapse remodeling by an inducible protein kinase Science 302 2003 1368 1373
58. D.T.S. Pak, S. Yang, S. Rudolph-Correia, E. Kim, and M. Sheng Regulation of dendritic spine morphology by SPAR, a PSD-95-associated RapGAP Neuron 31 2001 289 303
59. T.V. Perneger What's wrong with Bonferroni adjustments Br. Med. J. 316 1998 1236 1238
60. T.V. Perneger Adjusting for multiple testing in studies is less important than other concerns Br. Med. J. 318 1999 1288
61. R.S. Petralia, and R.J. Wenthold Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain J. Comp. Neurol. 318 1992 329 354
62. R.S. Petralia, and R.J. Wenthold Immunocytochemistry of NMDA receptors M. Li Methods in Molecular Biology: NMDA Receptor Protocols 1999 Humana Press Totowa, NJ 73 92
63. R.S. Petralia, N. Yokotani, and R.J. Wenthold 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
64. 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
65. R.S. Petralia, H.-M. Zhao, Y.-X. Wang, and R.J. Wenthold Variations in the tangential distribution of postsynaptic glutamate receptors in Purkinje cell parallel and climbing fiber synapses during development Neuropharmacology 37 1998 1321 1334
66. R.S. Petralia, J.A. Esteban, Y.-X. Wang, J.G. Partridge, H.M. Zhao, R.J. Wenthold, and R. Malinow Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses Nat. Neurosci. 2 1999 31 36
67. R.S. Petralia, Y.-X. Wang, N. Sans, P.F. Worley, J.A. Hammer III, and R.J. Wenthold Glutamate receptor targeting in the postsynaptic spine involves mechanisms that are independent of myosin Va Eur. J. Neurosci. 13 2001 1722 1732
68. R.S. Petralia, Y.-X. Wang, and R.J. Wenthold NMDA receptors and PSD-95 are found in attachment plaques in cerebellar granular layer glomeruli Eur. J. Neurosci. 15 2002 583 587
69. R.S. Petralia, Y.-X. Wang, and R.S. Wenthold Internalization at glutamatergic synapses during development Eur. J. Neurosci. 18 2003 3207 3217
70. R.S. Petralia, N. Sans, Y.-X. Wang, B. Vissel, K. Chang, K. Noben-Trauth, S.F. Heinemann, and R.J. Wenthold Loss of GluR2 α-amino-3-hydroxy-5- methyl-4-isoxazoleproprionic acid receptor subunit differentially affects remaining synaptic glutamate receptors in cerebellum and cochlear nuclei Eur. J. Neurosci. 19 2004 2017 2029
71. L. Polo-Parada, C.M. Bose, F. Plattner, and L.T. Landmesser Distinct roles of different neural cell adhesion molecule (NCAM) isoforms in synaptic maturation revealed by analysis of NCAM 180 kDa isoform-deficient mice J. Neurosci. 24 2004 1852 1864
72. A. Rao, E. Kim, M. Sheng, and A.M. Craig Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture J. Neurosci. 18 1998 1217 1229
73. J.J. Renger, C. Egles, and G. Liu A developmental switch in neurotransmitter flux enhances synaptic efficacy by affecting AMPA receptor activation Neuron 29 2001 469 484
74. C. Romano, J.K. Miller, K. Hyrc, S. Dikranian, S. Mennerick, Y. Takeuchi, M.P. Goldberg, and K.L. O'Malley Covalent and noncovalent interactions mediate metabotropic glutamate receptor mGlu5 dimerization Mol. Pharmacol. 59 2001 46 53
75. C. Romano, S. Smout, J.K. Miller, and K.L. O'Malley Developmental regulation of metabotropic glutamate receptor 5b protein in rodent brain Neuroscience 111 2002 693 698
76. K.J. Rothman No adjustments are needed for multiple comparisons Epidemiology 1 1990 43 46
77. N. Sans, R.S. Petralia, Y.-X. Wang, J. Blahos II, J.W. Hell, and R.J. Wenthold A developmental change in NMDA receptor-associated proteins at hippocampal synapses J. Neurosci. 20 2000 1260 1271
78. N. Sans, C. Racca, R.S. Petralia, Y.-X. Wang, J. McCallum, and R.J. Wenthold SAP97 selectively associates with a subset of AMPA receptors early in their biosynthetic pathway J. Neurosci. 21 2001 7506 7516
79. N. Sans, K. Prybylowski, R.S. Petralia, K. Chang, Y.-X. Wang, C. Racca, S. Vicini, and R.J. Wenthold NMDA receptor trafficking through an interaction between PDZ proteins and the exocyst complex Nat. Cell Biol. 5 2003 520 530
80. M. Sheng, and M.J. Kim Postsynaptic signaling and plasticity Science 298 2002 776 780
81. R. Shigemoto, S. Nakanishi, and N. Mizuno Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: an in situ hybridization study in adult and developing rat J. Comp. Neurol. 322 1992 121 135
82. Y. Shiraishi, A. Mizutani, S. Yuasa, K. Mikoshiba, and T. Furuichi Differential expression of Homer family proteins in the developing mouse brain J. Comp. Neurol. 473 2004 582 599
83. J.-Y. Song, K. Ichtchenko, T.C. Südhof, and N. Brose Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses Proc. Natl. Acad. Sci. U. S. A. 96 1999 1100 1105
84. L.H. Suh, S.F. Oster, S.S. Soehrman, G. Grenningloh, and D.W. Sretavan L1/laminin modulation of growth cone response to EphB triggers growth pauses and regulates the microtubule destabilizing protein SCG10 J. Neurosci. 24 2004 1976 1986
85. D.M. Suter, G.E. Pollerberg, A. Buchstaller, R.J. Giger, W.J. Dreyer, and P. Sonderegger Binding between the neural cell adhesion molecules axonin-1 and Nr-CAM/Bravo is involved in neuron-glia interaction J. Cell Biol. 131 1995 1067 1081
86. V. Sytnyk, I. Leshchyns'ka, M. Delling, G. Dityatev, A. Dityatev, and M. Schachner Neural cell adhesion molecule promotes accumulation of TGN organelles at sites of neuron-to-neuron contacts J. Cell Biol. 159 2002 649 661
87. V. Sytnyk, I. Leshchyns'ka, A. Dityatev, and M. Schachne Trans-Golgi network delivery of synaptic proteins in synaptogenesis J. Cell Sci. 117 2004 381 388
88. J.C. Tu, B. Xiao, S. Naisbitt, J.P. Yuan, R.S. Petralia, P. Brakeman, A. Doan, V.K. Aakalu, A.A. Lanahan, M. Sheng, and P.F. Worley Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins Neuron 23 1999 583 592
89. R. Tyzio, A. Represa, I. Jorquera, Y. Ben-Ari, H. Gozlan, and L. Aniksztejn The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite J. Neurosci. 19 1999 10372 10382
90. N. Uchida, Y. Honjo, K.R. Johnson, M.J. Wheelock, and M. Takeichi The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones J. Cell Biol. 135 1996 767 779
91. T. Uemura, H. Mori, and M. Mishina Direct interaction of GluRδ2 with Shank scaffold proteins in cerebellar Purkinje cells Mol. Cell. Neurosci. 26 2004 330 341
92. J.G. Valtschanoff, and R.J. Weinberg Laminar organization of the NMDA receptor complex within the postsynaptic density J. Neurosci. 21 2001 1211 1217
93. B. van Zundert, A. Yoshii, and M. Constantine-Paton Receptor compartmentalization and trafficking at glutamate synapses: a developmental proposal Trends Neurosci. 27 2004 428 437
94. J.E. Vaughn Review: fine structure of synaptogenesis in the vertebrate central nervous system Synapse 3 1989 255 285
95. Y.-X. Wang, R.J. Wenthold, O.P. Ottersen, and R.S. Petralia Endbulb synapses in the anteroventral cochlear nucleus express a specific subset of AMPA-type glutamate receptor subunits J. Neurosci. 18 1998 1148 1160
96. 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
97. R.J. Wenthold, K. Prybylowski, S. Standley, N. Sans, and R.S. Petralia Trafficking of NMDA receptors Annu. Rev. Pharmacol. Toxicol. 43 2003 335 358
98. K. Wu, J.-L. Xu, P.-C. Suen, E. Levine, Y.-Y. Huang, H.T.J. Mount, S.-Y. Lin, and I.B. Black Functional trkB neurotrophin receptors are intrinsic components of the adult brain postsynaptic density Mol. Brain Res. 43 1996 286 290
99. B. Xiao, J.C. Tu, R.S. Petralia, J.P. Yuan, A. Doan, C.D. Breder, A. Ruggiero, A.A. Lanahan, R.J. Wenthold, and P.F. Worley Homer regulates the association of group 1 metabotropic glutamate receptors with multivalent complexes of Homer-related, synaptic proteins Neuron 21 1998 707 716
100. B. Xiao, J.C. Tu, and P.F. Worley Homer: a link between neural activity and glutamate receptor function Curr. Opin. Neurosci. 10 2000 370 374
101. K. Yamada, and T. Nabeshima Brain-derived neurotrophic factor/TrkB signaling in memory processes J. Pharmacol. 91 2003 267 270
102. K. Yamada, M. Fukaya, H. Shimizu, K. Sakimura, and M. Watanabe NMDA receptor subunits GluRε1, GluRε3 and GluRζ1 are enriched at the mossy fibre-granule cell synapse in the adult mouse cerebellum Eur. J. Neurosci. 13 2001 2025 2036
103. A. Yoshii, M.H. Sheng, and M. Constantine-Paton Eye opening induces a rapid dendritic localization of PSD-95 in central visual neurons Proc. Nat. Acad. Sci. 100 2003 1334 1339
104. R.G. Zhai, H. Vardinon-Friedman, C. Cases-Langhoff, B. Becker, E.D. Gundelfinger, N.E. Ziv, and C.C. Garner Assembling the presynaptic active zone: a characterization of an active zone precursor vesicle Neuron 29 2001 131 143
105. H.-M. Zhao, R.J. Wenthold, and R.S. Petralia Glutamate receptor targeting to synaptic populations on Purkinje cells is developmentally regulated J. Neurosci. 18 1998 5517 5528
106. N.E. Ziv, and C.C. Garner Cellular and molecular mechanisms of presynaptic assembly Nat. Rev. 5 2004 385 399