Development of neuron-neuron synapses

Current Opinion in Neurobiology

Volumn 10, Issue 1, 2000, Pages 125-131

  Lee, Sang Hyoung ^a   Sheng, Morgan ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GEPHYRIN; GLYCINE RECEPTOR; POSTSYNAPTIC RECEPTOR; PROTEOHEPARAN SULFATE;

DENDRITE; HIPPOCAMPUS; NERVE CELL DIFFERENTIATION; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNAPTOGENESIS;

ANIMALS; DENDRITES; HUMANS; MOTOR ENDPLATE; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NERVOUS SYSTEM; NEURONS; RECEPTORS, GLUTAMATE; SYNAPSES;

EID: 0033964412     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(99)00046-X     Document Type: Review

References (57)

1. Sanes J.R., Lichtman J.W. Development of the vertebrate neuromuscular junction. Annu Rev Neurosci. 22:1999;389-442.
2. •].
3. •].
4. •] report an interesting correlation between the diameter of the postsynaptic density and the presence of AMPA receptors in the excitatory synapses.
5. Malenka R.C., Nicoll R.A. Silent synapses speak up. Neuron. 19:1997;473-476.
6. Liao D., Zhang X., O'Brien R., Ehlers M.D., Huganir R.L. Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons. Nat Neurosci. 2:1999;37-43.
7. 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.
8. Rao A., Kim E., Sheng M., Craig A.M. Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture. J Neurosci. 18:1998;1217-1229. This paper was the first to detail the developmental sequence in which ionotropic glutamate receptors and a set of NMDA receptor-associated proteins (PSD-95, GKAP, and α-actinin) cluster in synapses. In low-density hippocampal culture (in which dissociated neurons are plated in culture at a low density, so that each neuron is well-separated from its neighbours), NMDA receptors, AMPA receptors and PSD-95/GKAP accumulate in synapses with distinct time courses, implying that they are targeted to synapses by different mechanisms.
9. O'Brien R.J., Mammen A.L., Blackshaw S., Ehlers M.D., Rothstein J.D., Huganir R.L. The development of excitatory synapses in cultured spinal neurons. J Neurosci. 17:1997;7339-7350.
10. Mammen A.L., Huganir R.L., O'Brien R.J. Redistribution and stabilization of cell surface glutamate receptors during synapse formation. J Neurosci. 17:1997;7351-7358.
11. Sheng M., Pak D.T.S. Ligand-gated ion channel interactions with cytoskeletal and signaling proteins. Annu Rev Physiol. 62:2000;755-778.
12. Kim J.H., Huganir R.L. Organization and regulation of proteins at synapses. Curr Opin Cell Biol. 11:1999;248-254.
13. Kirsch J. Assembly of signaling machinery at the postsynaptic membranes. Curr Opin Neurobiol. 9:1999;329-335.
14. ••].
15. 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., O'Dell T.J., Grant S.G. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature. 396:1998;433-439. The authors studied the first mouse knockout of a PSD-95 family gene. Their results suggest that PSD-95 is not required for synaptic targeting of NMDA receptors (although it is possible that other members of the PSD-95 family complement this function). Rather, the enhanced LTP and impaired learning ability of the mutant mice suggest that PSD-95 plays an important role in NMDA receptor function, perhaps by assembling a signaling complex linked to the NMDA receptor.
16. Passafaro M., Sala C., Niethammer M., Sheng M. Direct microtubule binding by the PSD-95 interacting protein CRIPT and its potential role in the synaptic clustering of PSD-95. Nat Neurosci. 2:1999;1063-1069.
17. Gramates S.L., Budnik V. Assembly and maturation of the Drosophila larval neuromuscular junction. Int Rev Neurobiol. 43:1999;93-117.
18. + channels and fasciclin II (FasII), at the larval NMJ. Using genetic and biochemical approaches, the authors found that DLG localization is regulated by phosphorylation by CaMKII. This is the first study to show a potential link between synaptic activity and the synaptic distribution of a MAGUK protein.
19. Wu G-Y., Cline H.T. Stabilization of dendritic arbor structure in vivo by CaMKII. Science. 279:1998;222-226.
20. 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.
21. Naisbitt S., Kim E., Tu J.C., Xiao B., Sala C., Valtschanoff J., Weinberg R.J., Worley P.F., Sheng M. 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.
22. Tu J.C., Xiao B., Naisbitt S., Yuan J.P., Petralia R.S., Brakeman P., Doan A., Aakalu V.K., Lanahan A.A., Sheng M., Worley P.F. Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron. 23:1999;583-592.
23. Irie M., Hata Y., Takeuchi M., Ichtchenko K., Toyoda A., Hirao K., Takai Y., Rosahl T.W., Südhof T.C. Binding of neuroligins to PSD-95. Science. 277:1997;1511-1515.
24. Nguyen T., Südhof T.C. Binding properties of neuroligin 1 and neurexin 1β reveal function as heterophilic cell adhesion molecules. J Biol Chem. 272:1997;26031-26039.
25. Missler M., Fernandez-Chacon R., Südhof T.C. The making of neurexins. J Neurochem. 71:1998;1339-1347.
26. Shapiro L., Colman D.R. The diversity of cadherins and implications for a synaptic adhesive code in the CNS. Neuron. 23:1999;427-430.
27. Serafini T. Finding a partner in a crowd: neuronal diversity and synaptogenesis. Cell. 98:1999;133-136.
28. Wu Q., Maniatis T. A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell. 97:1999;779-790.
29. Craig A.M. Activity and synaptic receptor targeting: the long view. Neuron. 21:1998;459-462.
30. Rao A., Craig A.M. Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons. Neuron. 19:1997;801-812.
31. Lissin D.V., Gomperts S.N., Carroll R.C., Christine C.W., Kalman D., Kitamura M., Hardy S., Nicoll R.A., Malenka R.C., Zastrow M.V. Activity differentially regulates the surface expression of synaptic AMPA and NMDA glutamate receptors. Proc Natl Acad Sci USA. 95:1998;7097-7102.
32. 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.
33. Lissin D.V., Carroll R.C., Nicoll R.A., Malenka R.C., Zastrow M.V. Rapid, activation-induced redistribution of ionotropic glutamate receptors in cultured hippocampal neurons. J Neurosci. 19:1999;1263-1272.
34. Shi S-H., Hayashi Y., Petralia R.S., Zaman S.H., Wenthold R.J., Svoboda K., Malinow R. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science. 284:1999;1811-1816. Using GFP-tagged GluR1 subunits virally transfected into hippocampal slice cultures, the authors show that local tetanic stimulation induces in spines a rapid delivery and clustering of AMPA receptors that otherwise are mostly intracellular. This activity-dependent synaptic recruitment of AMPA receptors takes place not only in synapses already containing AMPA receptors, but also in spines lacking AMPA receptors. This is the first direct visualization of AMPA receptor redistribution in real-time.
35. Carroll R.C., Lissin D.V., von Zastrow M., Nicoll R.A., Malenka R.C. Rapid redistribution of glutamate receptors contributes to long-term depression in hippocampal cultures. Nat Neurosci. 2:1999;454-460.
36. ••].
37. ••], it is shown that LTP-inducing stimuli cause a rapid outgrowth of dendritic filopodia and formation of new spines, in an NMDA-receptor-dependent manner. Thus, synaptic activity triggers morphological changes that may correlate with new connections between neurons. It remains to be determined whether the newly formed spines are functional, and what molecular mechanisms underlie such structural changes.
38. Kirov S.A., Sorra K.E., Harris K.M. Slices have more synapses than perfusion-fixed hippocampus from both young and mature rats. J Neurosci. 19:1999;2876-2886. Hippocampal slices are routinely used for electrophysiological studies (e.g. for assessing LTP or LTD). The authors found a surprising ˜ twofold increase in the density of spines in hippocampal slices, occuring within 2 h of sectioning. This increase in spine density was attributed to the temporary loss of electrical activity and release of spinogenic factors resulting from tissue trauma.
39. McKinney R.A., Capogna M., Durr R., Gahwiler B.H., Thompson S.M. Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat Neurosci. 2:1999;44-49.
40. Verderio C., Coco S., Fumagalli G., Matteoli M. Spatial changes in calcium signaling during the establishment of neuronal polarity and synaptogenesis. J Cell Biol. 126:1994;1527-1536.
41. Augustin I., Rosenmud C., Südhof T.C., Brose N. Munc 13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature. 400:1999;457-461. The authors generated knockout mice of Munc 13-1, a presynaptic phorbor ester receptor. Surprisingly, the mutant mice develop ultrastructually normal synapses, despite the fact that the synaptic vesicle cycle is arrested and most excitatory synapses are functionally silenced. Therefore, in addition to confirming the importance of Munc 13-1 in neurotransmitter release, this paper implies that synaptic activity is dispensable for morphological development of synapses.
42. ••].
43. ••], found that gephyrin localization at synapses also depends on GlyR activation.
44. Ziv N.E., Smith S.J. Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron. 17:1996;91-102.
45. Harris K.M. Structure, development, and plasticity of dendritic spines. Curr Opin Neurobiol. 9:1999;343-348.
46. Fischer M., Kaech S., Knutti D., Matus A. Rapid actin-based plasticity in dendritic spines. Neuron. 20:1998;847-854.
47. Bradke F., Dotti C.G. The role of local actin instability in axon formation. Science. 283:1999;1931-1934.
48. Carey D. Syndecans: multifunctional cell-surface co-receptors. Biochem J. 327:1997;1-16.
49. Hsueh Y-P., Yang F-C., Kharazia V., Naisbitt S., Cohen A.R., Weinberg R.J., Sheng M. Direct interaction of CASK/LIN-2 and syndecan heparan sulfate proteoglycan and their overlapping distribution in neuronal synapses. J Cell Biol. 142:1998;139-151.
50. Ethell I.M., Yamaguchi Y. Cell surface proteoglycan syndecan-2 induces the maturation of dendritic spines in rat hippocampal neurons. J Cell Biol. 144:1999;575-586. Syndecan-2 is a cell surface heparan sulfate proteoglycan that is enriched in neuronal synapses. The authors show that premature expression of syndecan-2 in immature hippocampal neurons accelerates the maturation of dendritic spines from dendritic filopodia. The carboxy terminal-EFYA motif (single letter amino acid code) of syndecan-2 (which binds to the PDZ-domain-containing proteins CASK and syntenin) is required for this spinogenic effect, suggesting that a syndecan-2-associated protein complex may play a role in spine development.
51. Hsueh Y-P., Sheng M. Regulated expression and subcellular localization of syndecan heparan sulfate proteoglycans and the syndecan-binding protein CASK/LIN-2 during rat brain development. J Neurosci. 19:1999;7415-7425.
52. Serpinskaya A.S., Feng G., Sanes J.R., Craig A.M. Synapse formation by hippocampal neurons from agrin-deficient mice. Dev Biol. 205:1999;65-78.
53. O'Brien R.J., Xu D., Petralia R.S., Steward O., Huganir R.L., Worley P. Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product Narp. Neuron. 23:1999;309-323. Narp is a neuronal pentraxin secreted from both pre- and postsynaptic cells, and it is localized to synapses. The authors show that Narp displays AMPA-receptor-clustering activity by binding directly to the ectodomain of AMPA receptor subunits. A model is proposed in which Narp acts as an extracellular aggregating factor for AMPA receptors.
54. McAllister A.K., Katz L.C., Lo D.C. Neurotrophins and synaptic plasticity. Annu Rev Neurosci. 22:1999;295-318.
55. Causing C.G., Gloster A., Aloyz R., Bamji S.X., Chang E., Fawcett J., Kuchei G., Miller F.D. Synaptic innervation density is regulated by neuron-derived BDNF. Neuron. 18:1997;257-267.
56. •].
57. •], reduced density of synaptic vesicles were noted, along with reduced expression of synaptic vesicle-associated proteins such as synaptophysin. These abnormalities correlate with presynaptic functional deficits in the BDNF knockout mice, including impaired responses to high-frequency stimulation. Additional morphological defects, such as reduced axonal elaboration, larger presynaptic boutons, and reduced synapse density, were found in TrkB- and, to a lesser extent, in TrkC-deficient mice. Thus, neurotrophins may be important for the structural and functional maturation of synapses.