Organization and regulation of proteins at synapses

Current Opinion in Cell Biology

Volumn 11, Issue 2, 1999, Pages 248-254

  Kim, Jee Hae ^a   Huganir, Richard L ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN RECEPTOR; GLUTAMATE RECEPTOR; NERVE PROTEIN; NEUROTRANSMITTER RECEPTOR;

NERVE CELL PLASTICITY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS;

MAMMALIA;

EID: 0032915393     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(99)80033-7     Document Type: Article

References (64)

1. Hollmann M., Heinemann S. Cloned glutamate receptors. Annu Rev Neurosci. 17:1994;31-108.
2. Sheng M. PDZs and receptor/channel clustering: rounding up the latest suspects. Neuron. 17:1996;575-578.
3. Craven S.E., Bredt D.S. PDZ proteins organize synaptic signaling pathways. Cell. 93:1998;495-498.
4. Cho K.O., Hunt C.A., Kennedy M.B. The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron. 9:1992;929-942.
5. Kistner U., Wenzel B.M., Veh R.W., Cases-Langhoff C., Garner A.M., Appeltauer U., Voss B., Gundelfinger E.D., Garner C.C. SAP90, a rat presynaptic protein related to the product of the Drosophila tumor suppressor gene dlg-A. J Biol Chem. 268:1993;4580-4583.
6. Woods D.F., Bryant P.J. The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell. 66:1991;451-464.
7. Itoh M., Nagafuchi A., Yonemura S., Kitani-Yasuda T., Tsukita S. The 220-kD protein colocalizing with cadherins in non-epithelial cells is identical to ZO-1, a tight junction-associated protein in epithelial cells: cDNA cloning and immunoelectron microscopy. J Cell Biol. 121:1993;491-502.
8. Kennedy M.B. Origin of PDZ (DHR, GLGF) domains. Trends Biochem Sci. 20:1995;350.
9. Gomperts S.N. Clustering membrane proteins: it's all coming together with the PSD- 95/SAP90 protein family. Cell. 84:1996;659-662.
10. Saras J., Heldin C.H. PDZ domains bind carboxy-terminal sequences of target proteins. Trends Biochem Sci. 21:1996;455-458.
11. Lahey T., Gorczyca M., Jia X.X., Budnik V. The Drosophila tumor suppressor gene dlg is required for normal synaptic bouton structure. Neuron. 13:1994;823-835.
12. Guan B., Hartmann B., Kho Y.H., Gorczyca M., Budnik V. The Drosophila tumor suppressor gene, dlg, is involved in structural plasticity at a glutamatergic synapse. Curr Biol. 6:1996;695-706.
13. Budnik V., Koh Y.H., Guan B., Hartmann B., Hough C., Woods D., Gorczyca M. Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron. 17:1996;627-640.
14. Thomas U., Kim E., Kuhlendahl S., Koh Y.H., Gundelfinger E.D., Sheng M., Garner C.C., Budnik V. Synaptic clustering of the cell adhesion molecule fasciclin II by discs- large and its role in the regulation of presynaptic structure. Neuron. 19:1997;787-799.
15. Lue R.A., Marfatia S.M., Branton D., Chishti A.H. Cloning and characterization of hdlg: the human homologue of the Drosophila discs large tumor suppressor binds to protein 4.1. Proc Natl Acad Sci USA. 91:1994;9818-9822.
16. Muller B.M., Kistner U., Veh R.W., Cases-Langhoff C., Becker B., Gundelfinger E.D., Garner C.C. Molecular characterization and spatial distribution of SAP97, a novel presynaptic protein homologous to SAP90 and the Drosophila discs-large tumor suppressor protein. J Neurosci. 15:1995;2354-2366.
17. Brenman J.E., Christopherson K.S., Craven S.E., McGee A.W., Bredt D.S. Cloning and characterization of postsynaptic density 93, a nitric oxide synthase interacting protein. J Neurosci. 16:1996;7407-7415.
18. Kim E., Cho K.O., Rothschild A., Sheng M. Heteromultimerization and NMDA receptor-clustering activity of Chapsyn- 110, a member of the PSD-95 family of proteins. Neuron. 17:1996;103-113.
19. Muller B.M., Kistner U., Kindler S., Chung W.J., Kuhlendahl S., Fenster S.D., Lau L.F., Veh R.W., Huganir R.L., Gundelfinger E.D., Garner C.C. SAP102, a novel postsynaptic protein that interacts with NMDA receptor complexes in vivo. Neuron. 17:1996;255-265.
20. Ziff E.B. Enlightening the postsynaptic density. Neuron. 19:1997;1163-1174.
21. Kornau H.C., Schenker L.T., Kennedy M.B., Seeburg P.H. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science. 269:1995;1737-1740.
22. + channels by interaction with a family of membrane-associated guanylate kinases. Nature. 378:1995;85-88.
23. Kim J.H., Liao D., Lau L.F., Huganir R.L. SynGAP: a synaptic RasGAP that associates with the PSD-95/SAP90 protein family. Neuron. 20:1998;683-691. The authors found a brain specific RasGTPase activating protein, SynGAP, in association with the macromolecular NMDA receptor complex. Enriched at excitatory synapses, SynGAP may regulate synaptic Ras activity.
24. Chen H.J., Rojas-Soto M., Oguni A., Kennedy M.B. A synaptic Ras GTPase activating protein (p135 SynGAP) inhibited by CaM kinase II. Neuron. 20:1998;895-904. The paper describes the biochemical isolation of SynGAP abundant in the postsynaptic density in brain. The GTPase activating function of SynGAP was shown to be inhibited by CaM Kinase II.
25. Brenman J.E., Chao D.S., Gee S.H., McGee A.W., Craven S.E., Santillano D.R., Wu Z., Huang F., Xia H., Peters M.F.et al. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains. Cell. 84:1996;757-767.
26. Kim E., Naisbitt S., Hsueh Y.P., Rao A., Rothschild A., Craig A.M., Sheng M. 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.
27. Takeuchi M., Hata Y., Hirao K., Toyoda A., Irie M., Takai Y. SAPAPs. A family of PSD-95/SAP90-associated proteins localized at postsynaptic density. J Biol Chem. 272:1997;11943-11951.
28. Irie M., Hata Y., Takeuchi M., Ichtchenko K., Toyoda A., Hirao K., Takai Y., Rosahl T.W., Sudhof T.C. Binding of neuroligins to PSD-95. Science. 277:1997;1511-1515. The paper showed that PSD-95/SAP90 protein interacts with neuroligin, a synaptic surface protein that is highly differentially expressed via extensive alternative splicing. Previously it had been shown that neuroligin and β-neurexin interact extracellularly forming a heterotypic intercellular junction. The association between neuroligin and PSD-95/SAP90 suggests that the postsynaptic subsurface structure organized by PSD-95/SAP90 may be able to influence synapse formation.
29. Ichtchenko K., Hata Y., Nguyen T., Ullrich B., Missler M., Moomaw C., Sudhof T.C. Neuroligin 1: a splice site-specific ligand for beta-neurexins. Cell. 81:1995;435-443.
30. Nguyen T., Sudhof T.C. Binding properties of neuroligin 1 and neurexin 1beta reveal function as heterophilic cell adhesion molecules. J Biol Chem. 272:1997;26032-26039.
31. Hata Y., Butz S., Sudhof T.C. CASK: a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J Neurosci. 16:1996;2488-2494.
32. Okamoto M., Sudhof T.C. Mints, Munc18-interacting proteins in synaptic vesicle exocytosis. J Biol Chem. 272:1997;31459-31464.
33. Butz S., Okamoto M., Sudhof T.C. A tripartite protein complex with the potential to couple synaptic vesicle exocytosis to cell adhesion in brain. Cell. 94:1998;773-782. The presynaptic complex formed by three PDZ domain containing proteins, CASK, Mint1, and Velis may have a significant role in the protein sorting and localization at synapses. The LIN-2/LIN-7/LIN-10 complex in C. elegans is the invertebrate version of the complex and recently Kaech et al. [34] had shown that they are instrumental in the targeting LET-23 to the basolateral membrane. The modular domains in these proteins like PDZ, SH3, and PTB may recruit more proteins to perform the complicated task of proper targeting leading to appropriate presynaptic specialization.
34. Kaech S.M., Whitfield C.W., Kim S.K. The LIN-2/LIN-7/LIN-10 complex mediates basolateral membrane localization of the C. elegans EGF receptor LET-23 in vulval epithelial cells. Cell. 94:1998;761-771.
35. Migaud M., Charlesworth P., Dempster M., Webster L.C., Watabe A.M., Makhinson M., He Y., Ramsay M.F., Morris R.G., Morrison J.H.et al. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature. 396:1998;433-439. The role of PSD-95 was investigated using mouse transgenic technology. Previous data had suggested that the PSD-95 protein was involved in NMDA receptor clustering and serves as a scaffolding protein at synapses via interaction with other proteins like nNOS, SynGAP, neuroligin and GKA/SAPAP. Surprisingly, mutation of the PSD-95 protein in mice did not disrupt the localization of NMDA receptors at synapses but enhanced long-term potentiation and impaired spatial learning. The authors speculate that the functional role of PSD-95 may include coordinating proper signal transduction pathways downstream from the NMDA receptors and affect synaptic plasticity.
36. Dong H., O'Brien R.J., Fung E.T., Lanahan A.A., Worley P.F., Huganir R.L. GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature. 386:1997;279-284. The carboxy-terminal sequences of AMPA receptor subunits GluR2 and GluR3 were shown to interact with the PDZ domains containing GRIP protein. The critical role of the AMPA receptor carboxy-terminal tail was demonstrated in the experiment in which the overexpression of the tail in hippocampal neurons disrupted the synaptic targeting of AMPA receptors. GRIP contains seven PDZ domains which may serve to cross-link glutamate receptors or link them to other synaptic proteins involved in the targeting at synapses or the formulation of a signal transduction complex.
37. Srivastava S., Osten P., Vilim F.S., Khatri L., Inman G., States B., Daly C., DeSouza S., Abagyan R., Valtschanoff J.G.et al. Novel anchorage of GluR2/3 to the postsynaptic density by the AMPA receptor-binding protein ABP. Neuron. 21:1998;581-591.
38. Xia J., Zhang X., Staudinger J., Huganir R.L. Clustering of AMPA receptors by the synaptic PDZ domain containing protein PICK1. Neuron. 22:1999;179-187.
39. Rongo C., Whitfield C.W., Rodal A., Kim S.K., Kaplan J.M. LIN-10 is a shared component of the polarized protein localization pathways in neurons and epithelia. Cell. 94:1998;751-759. The postsynaptic localization of GLR-1 glutamate receptors investigated in C. elegans using powerful genetic analysis and LIN-10 was found to be instrumental in the proper targeting of the receptors. LIN-10 in complex with LIN-2 and LIN-7 was also implicated in the targeting of LET-23 receptor tyrosine kinase in polarized epithelial cells [34]; therefore the role of LIN-10 seems to be critical as the shared component in the targeting pathways in both neurons and epithelial cells.
40. Finkbeiner S., Greenberg M.E. Ca(2+)-dependent routes to Ras: mechanisms for neuronal survival, differentiation, and plasticity? Neuron. 16:1996;233-236.
41. Kornhauser J.M., Greenberg M.E. A kinase to remember: dual roles for MAP kinase in long-term memory. Neuron. 18:1997;839-842.
42. Brambilla R., Gnesutta N., Minichiello L., White G., Roylance A.J., Herron C.E., Ramsey M., Wolfer D.P., Cestari V., Rossi-Arnaud C.et al. A role for the Ras signalling pathway in synaptic transmission and long-term memory. Nature. 390:1997;281-286. Using mouse transgenic technology, the authors demonstrated the critical role of Ras-GRF/CDC25Mm, a neuronal Ras guanine nucleotide exchange factor, in synaptic plasticity, implicating Ras signaling in the modulation of synaptic transmission and long-term memory.
43. Rothman J.E., Wieland F.T. Protein sorting by transport vesicles. Science. 272:1996;227-234.
44. Lledo P.M., Zhang X., Sudhof T.C., Malenka R.C., Nicoll R.A. Postsynaptic membrane fusion and long-term potentiation. Science. 279:1998;399-403. The proteins in membrane fusion events were examined for their role in the postsynaptic cell in the modulation of synaptic strength resulting from long term potentiation. The results show that the postsynaptic fusion machinery may contribute to the LTP.
45. Osten P., Srivastava S., Inman G.J., Vilim F.S., Khatri L., Lee L.M., States B.A., Einheber S., Milner T.A., Hanson P.I., Ziff E.B. The AMPA receptor GluR2 C terminus can mediate a reversible, ATP- dependent interaction with NSF and alpha- and beta-SNAPs. Neuron. 21:1998;99-110. The authors describe the specific interaction between the AMPA receptor subunit GluR2 with proteins involved in membrane fusion, NSF and SNAP, and the ATP hydrolysis reversible formation of the complex. As a chaperone-like interaction of NSF is driven by ATP hydrolysis, they propose that NSF functions as a chaperone in the molecular processing of the AMPA receptor.
46. Nishimune A., Isaac J.T., Molnar E., Noel J., Nash S.R., Tagaya M., Collingridge G.L., Nakanishi S., Henley J.M. NSF binding to GluR2 regulates synaptic transmission. Neuron. 21:1998;87-97. The paper also reports the interaction between NSF and GluR2. Disrupting the interaction between the two proteins by infusing the peptide corresponding to NSF-binding domain of GluR2 decreased the AMPA receptor-mediated synaptic transmission in rat hippocampal neurons. These results demonstrate a NSF-dependent modulation of AMPA receptor function.
47. Song I., Kamboj S., Xia J., Dong H., Liao D., Huganir R.L. Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors. Neuron. 21:1998;393-400. The authors found that NSF specifically interacts with the carboxyl terminus of the GluR2 and GluR4c subunits of AMPA receptors. Also, the AMPA mediated postsynaptic response is decreased when the interaction of NSF and AMPA receptor subunits was disrupted, confirming that AMPA receptor function may be affected by NSF.
48. Bear M.F., Malenka R.C. Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol. 4:1994;389-399.
49. Linden D.J. Long-term synaptic depression in the mammalian brain. Neuron. 12:1994;457-472.
50. Nicoll R.A., Malenka R.C. Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature. 377:1995;115-118.
51. Liao D., Hessler N.A., Malinow R. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature. 375:1995;400-404.
52. Isaac J.T., Nicoll R.A., Malenka R.C. Evidence for silent synapses: implications for the expression of LTP. Neuron. 15:1995;427-434.
53. Durand G., Kovalchuk Y., Konnerth A. Long term potentiation and functional synapse induction in developing hippocampus. Nature. 381:1996;71-75.
54. 2+ of NMDA responses in spinal cord neurones. Nature. 309:1984;261-263.
55. Nowak L., Bregestovski P., Ascher P., Herbet A., Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature. 307:1984;462-465.
56. Turrigiano G.G., Leslie K.R., Desai N.S., Rutherford L.C., Nelson S.B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature. 391:1998;892-896. The visual cortical cultures experience an increase in miniature excitatory postsynaptic current (mEPSC) amplitudes, a measure of postsynaptic response, when subjected to chronic blockade of synaptic activity. And increased synaptic activity decreased mEPSC amplitudes. These results illustrate the overall synaptic activity in the neuronal network may modulate synaptic physiology via molecular modification.
57. Lissin D.V., Gomperts S.N., Carroll R.C., Christine C.W., Kalman D., Kitamura M., Hardy S., Nicoll R.A., Malenka R.C., von Zastrow M. Activity differentially regulates the surface expression of synaptic AMPA and NMDA glutamate receptors. Proc Natl Acad Sci USA. 95:1998;7097-7102. Using recombinant virus constructs with epitope-tagged glutamate receptor, the surface expression of receptors in hippocampal cultures were monitored during increased activity by blockade of inhibitory synaptic transmission in networks. The increased activity caused a decrease in the surface expression of GluR1 AMPA type glutamate receptor subunit without affecting the NMDA receptor subunit NR1 expression, indicating that neuronal activity can differentially regulate the surface expression of glutamate receptors.
58. O'Brien R.J., Kamboj S., Ehlers M.D., Rosen K.R., Fischbach G.D., Huganir R.L. Activity-dependent modulation of synaptic AMPA receptor accumulation. Neuron. 21:1998;1067-1078. The authors show the activity dependent regulation of postsynaptic response in cultured spinal neurons. Namely, increased mEPSC amplitudes was observed accompanied by the increased AMPA receptors at synapse when excitatory synaptic transmission was blocked. Interestingly it was also found that the half-life of the AMPA receptor subunit GluR1 was affected by synaptic activity blockade suggesting that postsynaptic response may be regulated by modulating the turnover of postsynaptic AMPA receptors.
59. Rao A., Craig A.M. Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons. Neuron. 19:1997;801-812. Hippocampal neurons in culture were examined for the effect of chronic blockade of NMDA receptor activity. Using immunocytochemistry, the authors showed an increase in synaptic NMDA receptor labeling without any effect of the AMPA type receptor and PSD-95 distribution, which illustrates that activity can affect the receptor expression at synapses.
60. Liao D., Zhang X., O'Brien R., Ehlers M.D., Huganir R.L. Morphological detection of postsynaptic silent synapses in developing hippocampal neurons. Nat Neurosci. 2:1999;37-43. A detailed analysis examining the effects of activity blockade in hippocampal cultured neurons revealed that the chronic AMPA receptor activity blockade increased the number, size, and density of AMPA and NMDA receptor clusters at synapses. In contrast, when the NMDA receptor activity was blocked, the number, size, and density of NMDA receptor clusters increased while the number of AMPA receptor clusters decreased. These results show that the synaptic targeting and localization of AMPA and NMDA receptors may be differentially regulated by activity.
61. Gomperts S.N., Rao A., Craig A.M., Malenka R.C., Nicoll R.A. Postsynaptically silent synapses in single neuron cultures. Neuron. 21:1998;1443-1451. Using electrophysiological and immunocytochemical methods, the authors investigated the AMPA and NMDA receptor responses and their synaptic localization in isolated hippocampal cells in culture. These cells form synapses on themselves (autapses) providing a condition where the postsynaptic responses can be carefully analyzed. The authors provide additional cytochemical and physiological data that a significant proportion of excitatory synapses contain NMDA receptors with few AMPA receptors providing further evidence for the existence of postsynaptically 'silent synapses'.
62. Nusser Z., Lujan R., Laube G., Roberts J.D., Molnar E., Somogyi P. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron. 21:1998;545-559. Synaptic AMPA receptors are quantitatively characterized in different classes of rat hippocampal synapses during development using immunogold electron microscopy. The paper reports that in young neurons at postnatal day (P) 17 there exist synapses that contain very few AMPA receptors and that these synapses may represent postsynaptic 'silent synapses'. During development these synapses appear to acquire AMPA receptors.
63. 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. Using immunogold electron microscopy, the authors examined NMDA and AMPA receptors at CA1 hippocampal synapses at different times in postnatal development. They found that early in development, synapses contained NMDA receptors with few or no AMPA receptors. The comparison between the two types of glutamate receptors strengthened the hypothesis that the 'silent synapses' lack AMPA responses due to the physical absense of AMPA receptors and acquire AMPA receptors during development and activity dependent synaptic changes.
64. Roche K.W., Tingley W.G., Huganir R.L. Glutamate receptor phosphorylation and synaptic plasticity. Curr Opin Neurobiol. 4:1994;383-388.