Glutamate receptors are selectively targeted to postsynaptic sites in neurons

Neuron

Volumn 18, Issue 6, 1997, Pages 939-950

  Rubio, Maria E ^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; GLUTAMATE RECEPTOR; METABOTROPIC RECEPTOR; RECEPTOR SUBUNIT;

ACOUSTIC NERVE FIBER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COCHLEAR NUCLEUS; CONTROLLED STUDY; DENDRITE; EMBEDDING; IMMUNOCYTOCHEMISTRY; NERVE PROJECTION; NEWBORN; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; RAT; SPINDLE CELL; SYNAPSE VESICLE;

EID: 0030969931     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80333-5     Document Type: Article

References (99)

1. Ajima, A., Hensch, T., Kado, R.T., and Ito, M. (1991). Differential blocking action of Joro spider toxin analog on parallel fiber and climbing fiber synapses in cerebellar Purkinje cells. Neurosci. Res. 12, 281-286.
2. Bahn, S., and Wisden, W. (1997). A map of non-NMDA receptor subunit expression in the vertebrate brain derived from in situ hybridization histochemistry. In The Ionotropic Glutamate Receptors, DT. Monaghan and R.J. Wenthold, eds. (Totowa, NJ: Humana Press), pp. 149-187.
3. Baude, A., Nusser, Z., Molnar, E., McIlhinney, R.A.J., and Somogyi, P. (1995). High-resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and non-synaptic sites in rat hippocampus. Neuroscience 69, 1031-1055.
4. Bekkers, J.M., and Stevens, C.F. (1989). NMDA and non-NMDA receptors are co-localized at individual excitatory synapses in culture rat hippocampus. Nature 341, 230-233.
5. Bernard, V., Somogyi, P., and Bolam, J.P. (1997). Cellular, subcellular, and subsynaptic distribution of AMPA-type glutamate receptor subunits in the neostriatum of the rat. J. Neurosci. 17, 819-833.
6. Bilak, M.M., Bilak, S.R., and Morest, D.K. (1996). Differential expression of N-methyl-D-aspartate receptor in the cochlear nucleus of the mouse. Neuroscience 75, 1075-1097.
7. Brandstätter, J.H., Koulen, P., Kuhn, R., van der Putten, H., and Wassle, H. (1996). Compartmental localization of a metabotropic glutamate receptor (mGluR7): two different active sites at a retinal synapse. J. Neurosci. 16, 4749-4756.
8. Cant, N.B. (1992). The cochlear nucleus: neuronal types and their synaptic organization. In Springer Handbook of Auditory Research, D.B. Webster, A.N. Popper, and R.R. Fay, eds. (New York: Springer-Verlag), pp. 67-116.
9. Cant, N.B., and Morest, K.D. (1984). The structural basis for stimulus coding in the cochlear nucleus of the cat. In Hearing Science: Recent Advances, C. Berlin, ed. (San Diego: College Hill), pp. 371-421.
10. Chaudhry, F.A., Lehre, K.P., van Lookeren Campagne, M., Ottersen, O.P., Danbolt, N.C., and Storm-Mathisen, J. (1995). Glutamate transporters in glia plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15, 711-720.
11. Cho, K.-O., Hunt, C.A., and Kennedy, M.B. (1992). The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9, 929-942.
12. Cid-Arregui, A., Parton, R.G., Simons, K., and Dotti, G.G. (1995). Nocodazol-dependent transport, and brefeldin A-sensitive processing and sorting, of newly synthesized membrane proteins in culture neurons. J. Neurosci. 15, 4259-4269.
13. Derrik, B.E., Weinberg, S.B., and Martinez, J.L. (1991). Opioid receptors are involved in an NMDA receptor-independent mechanism of LTP induction at hippocampal mossy fiber-CA3 synapses. Brain Res. Bull. 27, 219-223.
14. Dong, H., O'Brien, R.J., Fung, E.T., Lanahan, A.A., Worley, P.F., and Huganir, R.L. (1997). GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature 386, 279-284.
15. Dotti, C.G., and Simons, K. (1990). Polarized sorting of viral glycoproteins to the axon and dendrites of hippocampal neurons in culture. Cell 62, 63-72.
16. Dotti, C.G., Parton, R.G., and Simons, K. (1991). Polarized sorting of glypiated proteins in hippocampal neurons. Nature 349, 158-161.
17. Eshhar, N., Petralia, R.S., Winters, C.A., Niedzielski, A.S., and Wenthold, R.J. (1993). The segregation and expression of glutamate receptor subunits in culture hippocampal neurons. Neuroscience 57, 943-964.
18. Gallo, V., Upson, L.M., Hayes, W.P., Vyklicky, L., Jr., Winters, C.A., and Buonanno, A. (1992). Molecular cloning and developmental analysis of the new glutamate receptor subunit isoform in cerebellum. J. Neurosci. 12, 1010-1023.
19. Gazzaley, A.H., Benson, D.L., Huntley, G.W., and Morrison, J.H. (1997). Differential subcellular regulation of NMDAR1 protein and mRNA in dendrites of dentate gyrus granule cells after perforant path transection. J. Neurosci. 17, 2006-2017.
20. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15, 193-204.
21. Hackney, C.M., Osen, K.K., and Kolston, J. (1990). Anatomy of the cochlear nuclear complex of guinea pig. Anat. Embryol. 182, 123-149.
22. Hackney, C.M., Osen, K.K., Ottersen, O.P., Storm-Mathisen, J., and Manjalay, G. (1996). Immunocytochemical evidence that glutamate is a neurotransmitter in the cochlear nerve: a quantitative study in the guinea-pig anteroventral cochlear nucleus. Eur. J. Neurosci. 8, 79-91.
23. Hjelle, O.P., Chaudhry, F.A., and Ottersen, O.P. (1994). Antisera to glutathione: characterization and immunocytochemical application to the rat cerebellum. Eur. J. Neurosci. 6, 794-804.
24. Hollmann, M., and Heinemann, S. (1994). Cloned glutamate receptors. Ann. Rev. Neurosci. 17, 31-108.
25. 2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252, 851-853.
26. Hoop, M.J., and Dotti, C.G. (1993). Membrane traffic in polarized neurons in culture. J. Cell Sci. Supp. 17, 85-92.
27. Huber, L.A., Hoop, M.J., deDupree, P., and Zerial, M. (1993). Protein transport to the dendritic plasma membrane of culture neurons is regulated by rab8. J. Cell Biol. 123, 47-55.
28. Hunt, C.A., Schenker, L.J., and Kennedy, M.B. (1996). PSD-95 is associated with the postsynaptic density and not with the presynaptic membrane at the forebrain synapses. J. Neurosci. 16, 1380-1388.
29. Hunter, C., Petralia, R.S., Vu, T.H., and Wenthold, R.J. (1993). Expression of AMPA-selective glutamate receptor subunits in morphologically defined neurons of the mammalian cochlear nucleus. J. Neurosci. 13, 1932-1946.
30. Isaac, J.T., Nicoll, R.A., and Malenka, R.C. (1995). Evidence for silent synapses: implications for the expression of LTP. Neuron 15, 427-434.
31. Jones, K.A., and Baughman, R.W. (1991). Both NMDA and non-NMDA subtypes of glutamate receptors are concentrated at synapses on cerebral cortical neurons in culture. Neuron 7, 593-603.
32. Juiz, J.M., Rubio, M.E., Helfert, R.H., and Altschuler, R.A. (1993). Localizing putative excitatory endings in the cochlear nucleus by quantitative immunocytochemistry. In The Mammalian Cochlear Nuclei: Organization and Function, M.A. Merchan, J.M. Juiz, D.A. Godfrey, and E. Mugnaini, eds. (New York: Plenum Press), pp. 167-177.
33. Kane, E.C. (1974). Synaptic organization in the dorsal cochlear nucleus of the cat: a light and electron microscopy study. J. Comp. Neurol. 155, 301-330.
34. Katayama, E., Funahashi, H., Michikawa, T., Shiraishi, T., Ikemoto, T., Lino, M., Hirosawa, K., and Mikoshiba, K. (1996). Native structure and arrangement of inositol-1,4,5-triphosphate receptor molecules in bovine cerebellar Purkinje cells as studied by quick-freeze deep-etch electron microscopy. EMBO J. 15, 4844-4851.
35. Kelly, R.B., and Grote, E. (1993). Protein targeting in the neuron. Annu. Rev. Neurosci. 16, 95-127.
36. Kim, E., Cho, K.-O., Rothschild, A., and Sheng, M. (1996). Heteromultimerization and NMDA receptor-clustering activity of chapsyn-110, a member of the PSD-95 family proteins. Neuron 17, 103-113.
37. Kirsch, J., Meyer, G., and Betz, H. (1996). Synaptic targeting of ionotropic neurotransmitter receptors. Mol. Cell. Neurosci. 8, 93-98.
38. Kistner, U., Wenzel, B.M., Veh, R.W., Cases-Langhoff, C., Garner, A.M., Appeltaur, U., Voss, B., Gundelfinger, E.D., and Garner, C.C. (1993). SAP90, a rat presynaptic protein related to the product of the Drosophila tumor suppressor gene dlg-A. J. Biol. Chem. 268, 4580-4583.
39. Kornau, H.-C., Schenker, L.T., Kennedy, M.B., and Seeburg, P.H. (1995). Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269, 1737-1740.
40. Krijnse-Locker, J., Parton, R.G., Fuller, S.D., Griffiths, G., and Dotti, C.G. (1995). The organization of the endoplasmic reticulum and the intermediate compartment in cultured rat hippocampal neurons. Mol. Biol. Cell 6, 1315-1332.
41. Kunimoto, M. (1995). A neuron-specific isoform of brain ankyrin, 440-kd ankyrinB is targeted to the axons of rat cerebellar neurons. J. Cell. Biol. 131, 1821-1829.
42. Landsend, A.S., Moghaddam, M.A., Matsubara, A., Bergersen, L., Usami, S.-I., Wenthold, R.J., and Ottersen, O.P. (1997). Differential localization of δ glutamate receptors in the rat cerebellum: coexpression with AMPA receptors in parallel fiber-spine synapses and absence from climbing fiber-spine synapses. J. Neurosci. 17, 834-842.
43. Lauri, D.J., and Seeburg, P.H. (1994). Regional and developmental heterogeneity in splicing of the rat brain NMDAR1 mRNA. J. Neurosci. 14, 3180-3194.
44. 2+ permeability of glutamate receptor channels in hippocampal cells. Eur. J. Neurosci. 6, 1080-1088.
45. Liao, D., Hessler, N.A., and Malinow, R. (1995). Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375, 400-404.
46. Lorente de No, R. (1981). The Primary Acoustic Nuclei (New York: Raven Press).
47. Manis, P.B. (1990). Membrane properties and discharge characteristics of guinea pig dorsal cochlear nucleus neurons studied in vitro. J. Neurosci. 10, 2338-2351.
48. Manis, P.B., and Molitor, S.C. (1996). N-methyl-D-aspartate receptors at parallel fiber synapses in the guinea pig dorsal cochlear nucleus. J. Neurophysiol. 348, 261-276.
49. Martone, M.E., Pollock, J.A., Jones, Y.Z., and Ellisman, M.H. (1996). Ultrastructural localization of dendritic messenger RNA in adult rat hippocampus. J. Neurosci. 16, 7437-7446.
50. Matsubara, A., Laake, J.H., Davanger, S., Usami, S.-I., and Ottersen, O.P. (1996). 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, 4457-4467.
51. Matter, K., Brauchbar, M., and Bucher, K. (1990). Sorting of endogenous plasma membrane proteins occurs from two sites in culture human intestinal epithelial cells (Caco-2). Cell 60, 429-437.
52. Mayat, E., Petralia, R.S., Wang, Y.-X., and Wenthold, R.J. (1995). Immunoprecipitation, immunoblotting, and immunocytochemistry studies suggest that glutamate receptor δ subunits form novel postsynaptic receptor complexes. J. Neurosci. 15, 2533-2546.
53. Merighi, A., and Polak, J.M. (1993) Postembedding immunogold staining. In Immunohistochemistry II. A.C. Cuello, ed. (New York: Wiley), pp. 229-264.
54. Miyashiro, K., Dichter, M., and Eberwine, J. (1994). On the nature and differential distribution of mRNAs in hippocampal neurites: implications for neuronal functioning. Proc. Natl. Acad. Sci. USA 91, 10800-10804.
55. Molitor, S.C., and Manis, P.B. (1997). Evidence for functional metabotropic glutamate receptors in the dorsal cochlear nucleus. J. Neurophysiol., in press.
56. Monyer, H., Seeburg, P.M., and Wisden, W. (1991). Glutamate-operated channels: developmentally early and mature forms arise by alternative splicing. Neuron 6, 799-810.
57. Mosbacher, J., Schoepfer, R., Monyer, H., Burnashev, N., Seeburg, P.H., and Ruppersberg, J.P. (1994). A molecular determinant for submillisecond desensitization in glutamate receptors. Science 266, 1059-1062.
58. Mugnaini, E., Osen, K.K., Dahl, A.-L., Friedrich, V.L., and Korte, G. (1980). Fine structure of granule cells and related interneurons (termed Golgi cells) in the cochlear nucleus complex of cat, rat and mouse. J. Neurocytol. 9, 537-570.
59. Müller, B.M., Kistner, U., Veh, R.W., Cases-Langhoff, C., Becker, B., Gundelfinger, E.D., and Garner, C.C. (1995). SAP97, a novel member of the superfamily of brain-related guanylate kinases. J. Neurosci. 15, 31-36.
60. Nusser, Z., Mulvihill, E., Streit, P., and Somogyi, P. (1994). Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localization. Neuroscience 61, 421-427.
61. Odorizzi, G., Pearse, A., Domingo, D., Trowbridge, I.S., and Hopkins, C.R. (1996). Apical and basolateral endosomes of MDCK cells are interconnected and contain a polarized sorting mechanism. J. Cell Biol. 135, 139-152.
62. Oertel, D., and Wu, S.H. (1989). Morphology and physiology of cells in slice preparations of the dorsal cochlear nucleus of mice. J. Comp. Neurol. 283, 228-247.
63. Osen, K.K., Storm-Mathisen, J., Ottersen, O.P., and Dihle, B. (1995). Glutamate is concentrated in and released from parallel fiber terminals in the dorsal cochlear nucleus: a quantitative immunocytochemical analysis in the guinea pig. J. Comp. Neurol. 357, 482-500.
64. Ottiger, H.-P., Gerfin-Moser, A., Principe, F., Dutly, F., and Streit, P. (1995). Molecular cloning and differential expression patterns of avian glutamate receptor mRNAs. J. Neurochem. 64, 2413-2426.
65. Paxinos, G., and Watson, C. (1986). The Rat Brain in Stereotaxic Coordinates (New York: Academic Press).
66. Petralia, R.S. (1997). Immunocytochemical localization of ionotropic glutamate receptors (GluRs) in neural circuits. In The Ionotropic Glutamate Receptors, DT. Monaghan and R. J. Wenthold, eds. (Totowa, NJ: Humana Press), pp. 219-263.
67. Petralia, R.S., and Wenthold, R.J. (1992). Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J. Comp. Neurol. 318, 329-354.
68. Petralia, R.S., and Wenthold, R.J. (1996). Types of excitatory amino acid receptors and their localization in the nervous system and hypothalamus. In Excitatory Amino Acids: Their Role in Neuroendocrine Function, B.W. Brann and V. B. Mahesh, eds. (New York: CRC Press), pp. 22-101.
69. Petralia, R.S., Yokotani, N., and Wenthold, R.J. (1994a). 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.
70. Petralia, R.S., Wang, Y.-X., and Wenthold, R.J. (1994b). The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J. Neurosci. 14, 6102-6120.
71. Petralia, R.S., Wang, Y.-X., Zhao, H.-M., and Wenthold, R.J. (1996). Ionotropic and metabotropic glutamate receptors show unique postsynaptic, presynaptic, and glial localizations in the dorsal cochlear nucleus. J. Comp. Neurol. 372, 356-383.
72. Racca, C., Gardol, A., and Triller, A. (1997). Dendritic and postsynaptic localizations of glycine receptor α subunit mRNAs. J. Neurosci. 17, 1691-1700.
73. Raman, I.M., Zhang, S., and Trussell, L.O. (1994). Pathway-specific variants of AMPA receptors and their contribution to neuronal signaling. J. Neurosci. 14, 4998-5010.
74. Ryugo, D.K. (1992). The auditory nerve: peripheral innervation, cell body morphology, and central projections. In Springer Handbook of Auditory Research., D.B. Webster, A.N. Popper, and R.R. Fay, eds. (New York: Springer-Verlag), pp. 23-65.
75. Ryugo, D.K., and May, S.K. (1993). The projections of intracellularly labeled auditory nerve fibers to the dorsal cochlear nucleus of cats. J. Comp. Neurol. 329, 20-35.
76. Sato, K., Kiyama, H., and Tohyama, M. (1993). The differential expression patterns of messenger RNAs encoding non-N-methyl-D-aspartate glutamate receptor subunits (GluR1-4) in the rat brain. Neuroscience 52, 515-539.
77. Shigemoto, R., Kulik, A., Roberts, J.D.B., Ohishi, H., Nusser, Z., Kaneko, T., and Somogyi, P. (1996).Targeted-cell-specific concentration of a metabotropic glutamate receptor in the presynaptic active zone. Nature 381, 523-525.
78. Siegel, S., Brosse, N., Janssen, W.G., Gasic, G.P., Jahn, R., Heinemann, S.F., and Morrison, J.H. (1994). Regional, cellular, and ultrastructural distribution of N-methyl-D-aspartate receptor subunit 1 in monkey hippocampus. Proc. Natl. Acad. Sci. USA 91, 564-568.
79. Smith, P.H., and Rhode, W.S. (1985). Electron microscopic features of physiologically characterized, HRP-labeled fusiform cells in the cat dorsal cochear nucleus. J. Comp. Neurol. 237, 127-143.
80. Spacek, J., and Harris, K.M. (1997). Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J. Neurosci. 17, 190-203.
81. Steward, O. (1997). mRNA localization in neurons: a multipurpose mechanism? Neuron 18, 9-12.
82. Sucher, N.J., Brose, N., Deitcher, D.L., Awobuluyi, M., Gasic, G.P., Bading, H., Cepko, C.L., Greenberg, M.E., Jann, R., Heinemann, S.F., and Lipton, S.A. (1993). Expression of endogenous NMDAR1 transcripts without receptor protein suggests post-transcriptional control in PC12 cells. J. Biol. Chem. 268, 22299-22304.
83. Terada, S., Nakata, T., Peterson, A.C., and Hirokawa, N. (1996). Visualization of slow axonal transport in vivo. Science 273, 784-788.
84. Terasaki, M., Slater, N.T., Fein, A., Schmidek, A., and Reese, T.S. (1994). Continuous network of endoplasmic reticulum in cerebellar Purkinje neurons. Proc. Natl. Acad. Sci. USA 91, 7510-7514.
85. Tiedge, H., and Brosius, J. (1996). Translational machinery in dendrites of hippocampal neurons in culture. J. Neurosci. 16, 7171-7181.
86. Torre, E.R., and Steward, O. (1996). Protein synthesis within dendrites: glycosylation of newly synthesized proteins in dendrites of hippocampal neurons in culture. J. Neurosci. 16, 5967-5978.
87. Trussell, L.O., Raman, I.M., and Zhang, S. (1994). AMPA receptors and the rapid synaptic transmission. Semin. Neurosci. 6, 71-79.
88. van Lookeren Campagne, M., Oestreicher, A.B., van der Krift, T.P., Gispen, W.H., and Verkleij, A.J. (1991). Freeze-substitution and Lowicryl HM20 embedding of fixed rat brain: suitability for immunogold ultrastructural localization of neural antigens. J. Histochem. Cytochem. 39, 1267-1279.
89. Verdoorn, T.A., Burnashev, N., Monyer, H., Seeburg, P.H., and Sakmann, B. (1991). Structural determinants of ion flow through recombinant glutamate receptor channels. Science 252, 1715-1718.
90. 2+ transport. Neuroscience 49, 467-477.
91. 2+ stores in cerebellum Purkinje neurons. Comp. Biochem. Physiol. 105A, 205-211.
92. Walton, P.D., Airey, J.A., Sutko, J.L., Beck, C.F., Mignery, G.A., Südhof, T.C., Deerink, T., and Ellisman, M. (1991). Ryanodine and inositol triphosphate receptors coexist in avian cerebellar Purkinje neurons. J. Cell Biol. 113, 1145-1157.
93. Wenthold, R.J., Yokotani, N., Doi, K., and Wada, K. (1992). Immunochemical characterization of the non-NMDA glutamate receptor using subunit-specific antibodies. J. Biol. Chem. 267, 501-507.
94. Wenthold, R.J., Petralia, R.S., Blahos, J.B., II, and Niedzielski, A.S. (1996). Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J. Neurosci. 16, 1982-1989.
95. Wickesburg, R.E., and Oertel, D. (1989). Auditory nerve neurotransmitter acts on a kainate receptor: evidence from intracellular recordings in brain slices from mice. Brain Res. 486, 423-460.
96. Wozniak, M., and Limbird, L.E. (1996). The three α2-adrenergic receptor subtypes achieve basolateral localization in Madin-Darby Canine Kidney II cells via different targeting mechanisms. J. Biol. Chem. 271, 5017-5024.
97. Yoshimory, T., Keller, P., Roth, M.G., and Simons, K. (1996). Differential biosynthetic transport routes to the plasma membranes in BHK and CHO cells. J. Cell Biol. 111, 987-1000.
98. Zalustky, R.A., and Nicoll, R.A. (1990). Comparison of two forms of long-term potentiation in single hippocampal neurons. Science 248, 1619-1624.
99. Zhao, H.-M., Wenthold, R.J., Wang, Y.-X., and Petralia, R.S. (1997). δ-Glutamate receptors are differentially distributed at parallel and climbing fiber synapses on Purkinje cells. J. Neurochem. 68, 1041-1052.